UEU-co logo

AccessSurgery – Print

  Print  |  Close Window

Note: Large images and tables on this page may necessitate printing in landscape mode.

Skandalakis’ Surgical Anatomy > Chapter 19. Liver >

History

The anatomic and surgical history of the liver is presented in Table 19-1.

Table 19-1. Anatomic and Surgical History of the Liver

Mesopotamians ca. 2000-3000 B.C. Performed hepatic divination using clay models of sheep livers for instruction
Herophilus of Chalcedon (334-280 B.C.) First anatomic description of liver. Stated: “In some [animals] the liver does not have lobes at all but is round and undifferentiated. In some however it has two, in some more, and in many four and in some more lobes.” Discovered mesenteric lacteals.
Erasistratus of Chios (310-250 B.C.) Described basic intrahepatic capillary bed while studying liver anatomy
Celsus ca. 30 B.C. Emphasized four-lobed liver in De Re Medicina 
Rufus of Ephesus 50 A.D. Described five-lobed liver
Galen (130-210 A.D.)   Documented Herophilus’ and Erasistratus’ anatomic findings. Claimed liver spreads like the five fingers of a hand. Defined liver as primary organ of sanguinification that converts chyle to blood.
Berengario da Carpi 1522 In Isagogae Breves, cautiously challenged Galen, claiming liver can have two, three, four, or five lobes  
Andreas de Laguna 1535 Observed two, three, four, and five-lobed livers
Vesalius 1538 Published Tabulae Sex, depicting a five-lobed liver 
1546 Published Fabrica, showing a symmetric two-lobed liver 
Fabricus Hildanus (1560-1634) Early 17th century Excised small piece of liver protruding from abdomen after knife wound
Gasparo Aselli 1622 Rediscovered mesenteric lacteals and claimed they drain into liver
Jan de Wale (Walaeus) 1640 Described capsule, later renamed Glisson’s capsule
Johann Vesling 1647 First to report bifurcation of human portal vein
Jean Pecquet 1647 Described the thoracic duct while correctly claiming it terminates in subclavian vein. Conclusively proved that chyle is not transported to the liver, thus challenging notion that blood is made in liver. Published findings in 1651.
Olof Rudbeck 1652 Described course of lymphatics from liver to thoracic duct and venous systems during a royal gathering in Uppsala Castle of Sweden
Thomas Bartholin 1652 Further confirmed course of lymphatic drainage. Incorrectly noted that mesenteric lacteals carry lymph to the liver. Rudbeck corrected this error in 1653.
Francis Glisson 1654 Published Anatomia Hepatis describing capsule named for him. Provided detailed account of intrahepatic vasculature. 
Marcello Malpighi 1661 Published De Pulmonibus Epistolae, describing hexagonal lobules in liver 
Johan Jacob Wepfer 1664 Discovered that “acini,” or lobules, exist in a pig’s liver
Fredrick Ruysch 1665 Hypothesized that Malpighian lobules represent interconnections between portal and vascular system
Malpighi 1666 Published De Viscerum Structura Exercitatio Anatomica further describing hexagonal lobules. Confirmed belief that hepatic and portal veins are interconnected by capillary beds. 
Gottfried Bidloo 1685 Published Anatomia Humani Corporis, writing of interconnected small units of liver 
Albrecht von Haller 1764 Provided modern account of human liver. Divided it into right, left, anterior, and caudate lobes.
Francis Kiernan 1833 Established concept of “classic” liver lobule with a hepatic vein in the center and six hepatic triads at periphery
E. Brissuad & C. Sabourin 1834 Advocated concept of portal lobule with bile ducts in center
René-Joachin-Henri Dutrochet 1838 Described cytology of hepatocytes
J. McPherson 1846 Excised a small piece of liver from a spear wound
Joseph von Gerlach 1849 Postulated liver cord theory using terms “cords” and “trabeculae” to describe arrangement of hepatocytes in relation to bile capillaries (bile canaliculi) and vascular sinusoids
1854 Noted presence of “bile caniculi” in liver
T.H. MacGillavry 1865 Reported finding space between surface of hepatocytes and sinusoidal endothelium; these later named spaces of Disse
Ewald Hering 1866 Considered liver parenchyma to be continuous mass of hepatocytes lined in a series of plates of one-celled thickness
Chrzonszczewsky 1866 Described relationship of hepatic arteries to central sinuses
Victor von Bruns 1870 Successfully excised a “nut-sized” section of liver from a fellow surgeon suffering from gunshot wounds
H. Tillmanns 1879 Removed wedge-shaped pieces of liver from 12 rabbits. Determined that degree of injury to liver depends on wound size and amount of hemorrhage.
Lawson Tait 1880 Reportedly first to use laparotomy for liver trauma
Themistokles Gluck 1883 Reported physiological data helping to establish concept that liver regenerates after surgery
P. Postemski 1885 Recommended suturing liver to control bleeding
A. Luis 1886 Removed an adenoma of liver the size of a “one-year-old child’s head”
Carl von Langebuch 1887 Performed first successful subtotal left hepatectomy
Hugo Rex 1888 Described right and left lobes as being equal in size. Showed the plane of division is through bed of gallbladder and notch of inferior vena cava and not through falciform ligament.
L. McLane Tiffany 1890 Reported performing first American subtotal left hepatectomy
Emil Ponflick 1890 Using animal pathology experiments, found liver resections of up to 80% are non-fatal due to rapid and extensive regeneration
J. Disse 1890 Described perisinusoidal spaces bearing his name in an attempt to describe relations of lymph with liver
William Williams Keen 1892 Performed first successful liver resection in America (typical left hepatectomy). Reported his findings through the 1890s while documenting 76 cases of hepatectomies in world literature. Used his thumb to strip liver capsule.
M. Kousnetzoff & 1896 Devised suture method to stem liver hemorrhage using blunt needles, mattress sutures,
J. Pensky   and “guards” such as magnesium plates to overcome liver’s friability
J. Cantlie 1897 Confirmed Rex’s findings. Rex’s lobular plane of division later named Cantlie’s line.
W. Anschutz 1903 Advocated division of liver parenchyma with blunt objects to control bleeding
R. Kretz 1905 Reported work supporting Hering’s one-cell thick parenchyma over Gerlach’s two-cell thick model
Franklin Paine Mall 1906 Advocated Brissaud and Sabourin’s “portal” lobule, and described the spaces surrounding the portal triads; these later named spaces of Mall
Hogarth Pringle 1908 Occluded portal triad with his finger and thumb (“Pringle Pinch”) to temporarily control bleeding during liver surgery
W. Wendel 1911 Performed first subtotal right hepatectomy. Deliberately tied off right hepatic artery before resection.
Sir Archibald Hector McIndoe & V. Counsellor 1927 Studied intrahepatic ducts in 42 human livers. Confirmed bilateral symmetry established by Rex and Cantlie.
G. Caprio 1931 Performed first sub-total left hepatectomy under hilar ligation
L.B. Arey 1932 Further developed “portal” lobule concept by describing the coexistence of hepatic and portal lobules in seals
Ton That Tung 1939 Published paper describing primary parenchymatous transection during liver surgery
E.J. Donovan & T.V. Santulli 1944 Performed sub-total left hepatectomy for sarcoma while tying off left hepatic artery, left hepatic duct, and left portal vein of liver
C. Hjortsjö 1948 Using corrosion specimens and cholangiograms, originated concept that branching of the bilary ducts has a segmental pattern
Ronald William Raven 1948 Applied anatomic principles during a left segmentectomy by resecting through the falciform ligament
H. Elias 1949 Restated Hering’s concept and further explained it in more than 30 papers during the ensuing 25 years
Owen Harding Wangensteen 1949 Performed first typical right hepatectomy to treat metastatic cancer
Julian Quattlebaum 1952 Performed typical right hepatectomy for primary adenoma. Used back of his scalpel as a parenchymal fracture technique.
A.M. Rappaport 1952 Proposed concept of “liver acinus” in which a cylindrical mass of hepatic tissue surrounds a portal triad. Indicated boundaries between sinuses are not visible. Doctoral thesis accepted in 1952, papers published in 1954 and 1958.
George T. Pack & Harvey W. Baker 1952 Performed total right hepatectomy; reported in 1953
J.L. Lorat-Jacob & 1953 Performed extended right hepatectomy (right trisegmentectomy) by thoracoabdominal
H.G. Robert   approach using preliminary vascular control
John E. Healey & 1953 Described segmental anatomy of liver based on patterns of bilary intrahepatic architecture.
Paul C. Schroy   Reported liver is divided into five segments (medial, lateral, posterior, anterior, and caudate).
Claude Couinaud 1954 Affirmed segmental anatomy using internal vasculature and bilary architecture as a guide. Reported liver is divided into eight sections (I-VIII).
Charles Welch 1955 Performed first liver homotransplantation in dogs, confirming liver transplantation is possible
N.A. Goldsmith & R.T. Woodburne 1957 Described segmental anatomy after examining 33 human livers in vivo. Used “subsegment” nomenclature.
Tien-Yu Lin, Kuang-Yung Hsu, Chen-Min Hsieh, & Chi-Sen Chen 1958 Published paper describing modern “finger fracture” techniques used in resection
Thomas Starzl 1963 Attempted first orthotopic liver transplant in humans
R.N. McClelland & T. Shires 1965 Published paper describing the first “nonanatomical” resections
J.P. Heaney, W.R. Stanton, D.S. Halbert, J. Seidel, & T. Vice 1966 Advanced Pringle’s occlusion principle by cross clamping aorta and inferior vena cava
Thomas Starzl 1968 Performed first successful human orthotopic liver transplant
T. Schrock, T. Baisdell, & C. Matthewson 1968 Isolated liver’s vasculature with atriocaval shunting
Thomas Starzl 1975 Performed first reduced-size liver transplant
Henri Bismuth 1980 Performed first heterotopic liver transplant in humans
Thomas Starzl 1980 Performed first extended left hepatectomy (left trisegmentectomy)
R. Pichlmayr & J. Broelsh 1984 Performed first split-liver transplant
S. Raia, J.R. Nery, & S. Mies 1989 Performed first living related-donor liver transplant
Richter et al. 1990 Introduced transjugular intrahepatic protosystemic stent-shunt (TIPS) into clinical practice; revolutionized management of difficult cases of esophagogastric variceal bleeding and other complications of portal hypertension

History table compiled by David A. McClusky III and John E. Skandalakis.

References

McClusky DA III, Skandalakis LJ, Colborn GL, Skandalakis JE. Hepatic surgery and hepatic surgical anatomy: historical partners in progress. World J Surg 1997;21:330-342.

Popper H. Vienna and the liver. In Brunner H, Thaler H (eds). Hepatology: A Festschrift for Hans Popper. New York: Raven Press, 1985, pp. 1-14.

Richter GM, Noeldge G, Palmz JC. The transjugular intrahepatic protosystemic stent-shunt (TIPS): experience results of a pilot study. Cardiovasc Intervent Radiol 1990;13:200.

Embryogenesis

Normal Development

The earliest appearance of the liver primordium occurs on Day 22 after conception. It appears at the superior intestinal portal, caudal and ventral to the heart. By Day 24, the hepatic diverticulum is growing into the transverse septum that, at this stage, contains the vitelline and umbilical veins. Differentiation of the components of the liver begins before the primordium becomes recognizable.

Using chick embryos, Croisille and LeDouarin2 postulated three separate inductive processes acting on the endoderm (Fig. 19-1). First, lateral splanchnic mesoderm migrates anteriorly and fuses across the midline beneath the embryonic pharynx. This tissue, called hepatocardiac mesoderm, induces differentiation of the overlying endoderm cells at the anterior intestinal portal.

Fig. 19-1.

Differentiation (vertical arrows) and induction (horizontal arrows) in the development of liver cords and sinuses in the embryo. (From Skandalakis JE, Gray SW (Eds). Embryology for Surgeons, 2nd Ed. Baltimore: Williams & Wilkins, 1994; with permission.)

As the hepatic bud appears, the hepatic and cardiac mesenchyme become segregated. The second and third inductions occur when the hepatic mesenchyme stimulates the cells of the endodermal cords to differentiate into hepatocytes, and simultaneously the endodermal hepatocytes stimulate the mesenchyme to form the endothelial cells of the liver sinusoids.

The vitelline and umbilical veins divide into a plexus of vessels, and the invading endoderm cells move into the spaces around and between them.3 This endodermal invasion in humans is not by cords of cells but by migration of individual endoderm cells. These endoderm cells do not maintain contact with each other, but mingle freely with mesenchyme cells of the transverse septum.

Elias4,5 and Wilson and colleagues6 suggested another source of liver parenchyma. They postulated that mesodermal celomic lining cells invading the transverse septum become indistinguishable from endodermal cells.

Bennett7 presented three sets of events:

 

Cell multiplication

New and differentiated cells from the undifferentiated zygote

New and differentiated cells with specific histology, function, and physiological destiny.

Bennett wrote that some gene activities, different proteins, and different functions of the cell are responsible for this embryonic differentiation. By differentiation, endodermal cells produce the liver diverticulum which produces liver cells.

Sherer8 speculated that the development of the hepatic parenchyma depends on interaction of its epithelial and mesenchymal tissues.

By Day 32, most of the blood flow from the umbilical veins has been tapped by the parenchyma that surrounds the venous channels. These channels become the liver sinusoids. The right umbilical vein regresses in the sixth week. The left vein carries placental blood to the fetus until birth. Its remnant is the round ligament in the free edge of the falciform ligament. By Day 51, the intrahepatic veins have nearly attained the normal adult distribution and segmentation. The hepatic arteries and the bile duct do not advance as quickly toward their adult pattern. The investing cores of parenchyma, at first three to five cells thick, become reduced to a single cell layer near term.

Growth of the liver makes it bulge out of the transverse septum so that the liver becomes a truly abdominal organ lying in the ventral mesentery. The bare area of the liver and diaphragm remains as an indication of the origin of the liver from the transverse septum. The asymmetry of the organ increases.

The intrahepatic bile ducts were long assumed to develop by extension of the extrahepatic ducts. It is now believed that the ducts differentiate from hepatic cells and join the extrahepatic duct system secondarily. The ducts appear first at the hilum and spread peripherally.4,9 Bile may appear as early as the third month and is often in the intestine by the fifth month. By the ninth week, the liver embraces as much as 10% of body volume. Its relative size decreases to 5% by term.

The earliest source of blood in the embryo is the mesoderm of the yolk sac. Groups of stem cells, the blood islands, produce cells (primitive erythrocytes) that synthesize hemoglobin and retain their nuclei. Stem cells from the blood islands seed the liver and proliferate. Adult types of erythrocytes (RBCs), granulocytes, and platelets are produced in the liver between the ninth and 24th weeks of fetal life.

With the progress of ossification and the appearance of bone marrow, which will be seeded by stem cells from the liver, the liver structure shuts down its hemopoietic activity well before birth. The potential for blood production continues into adult life, expressing itself if the bone marrow fails to function. Galen was not entirely wrong in assigning a blood-forming function to the liver!

Initially the right lobe is smaller than the left lobe. Between birth and adulthood, the right lobe increases in size at the expense of the left lobe, which undergoes some peripheral degeneration10 (Fig. 19-2).

Fig. 19-2.

The relative sizes of the left and right lobes of the liver in the fetus at 32 weeks; in the infant at 3 days and at 17 months; and in the adult. The dotted line represents the location of the main lobar fissure. (Modified from Healey JE Jr, Sterling JA. Segmental anatomy of the newborn liver. Ann NY Acad Sci 111:25-36, 1963; with permission.)

The alterations in relative size of the left and right parts of the liver are accompanied by changes in the orientation and size of the upper abdominal arteries. In this regard, note that the hepatic artery is the largest branch of the celiac trunk in newborns. In adults the splenic artery is larger than the hepatic. In later development, the mass of the liver reduces and shifts to the right side. This results in decreased size of the hepatic artery and in the left-to-right orientation of the hepatic artery and the celiac trunk.11

Remember

 

Around the middle of the 3rd week or at the beginning of the 4th week, the liver primordium (liver bud), gallbladder, and biliary duct (gallbladder bud) arise as a ventral outgrowth from the distal end of the foregut.

Early in the 5th week, the liver bud stalk is formed by proliferating cells. These cells start to infiltrate the transverse septum through the rays of its endodermal cells. This is an embryologic mesodermal (mesenchymal) entity between the pericardial cavity and the stalk of the yolk sac. The future hepatic stroma, the hemopoietic Kupffer cells, and the vessels are all of mesenchymal origin.

At this same time, the connecting elements between the hepatic diverticulum and the already-formed duodenum form the bile duct. Later this produces the cystic duct and the gallbladder.

Later the hepatic sinusoids (endothelium-lined spaces) are formed from the epithelial cells. These spaces now communicate by anastomosis with small vessels from the vitelline and umbilical veins.

Around the 9th week, rapid hepatic growth causes the liver to account for 10% of the total fetal weight. The hemopoietic function and the multiple sinusoids are, most likely, responsible for this hepatomegaly. At birth, the liver weighs approximately 5% of the total body weight.

Occlusion and canalization take place at the extrahepatic biliary system. These processes, however, are not responsible for extrahepatic biliary atresia.

The ventral mesentery (mesogastrium) produces the:

 

– Lesser omentum, formed by the gastrohepatic ligament and the hepatoduodenal ligament

– Falciform ligament from the ventral abdominal wall to the liver

 

The hepatoduodenal ligament envelops the hepatic triad, and the falciform ligament hosts the left umbilical vein at its free border. The right umbilical vein disappears very early.

According to Sergi et al.,12 “the surface and the perimeter of the portal tracts, the longest axis of the migrating peripheral tubular structures, and the maturation of bile ducts follow a process continuous and active up to term, but they slow between the 20th and the 32nd week of gestation, when intraportal granulopoiesis of the liver is active.”

A higher proportion of umbilical blood is directed to the liver and less is shunted through the ductus venosus in the human fetus than in other animals.13

Congenital Anomalies

Fig. 19-3 illustrates sites of the major congenital anomalies of the liver. Complete absence of the liver is rare and is not compatible with postnatal life. Absence of the left lobe of the liver has been detected in adults by radiography,14 ultrasonogram, and CT scan;15 this defect in itself produces no symptoms.

Fig. 19-3.

Sites of the major anomalies of the liver. (Modified from Skandalakis JE, Gray SW (Eds). Embryology for Surgeons, 2nd Ed. Baltimore: Williams & Wilkins, 1994; with permission.)

Kakitsubata et al.16 reported segmental anomalies. They observed absence of the anterior segment of the right lobe in one patient and anomalies of the left lobe in three others. Ozgun and Warshauer17 reported agenesis of the medial segment of the left lobe. Agenesis of the right lobe was reported by Morphett and Adam.18 Klin et al.19 reported a case of agenesis of the left lobe.

Transposition

Transposition of the liver is a manifestation of total or partial situs inversus viscerum. Diagnosis is suggested by a right-sided gastric air bubble on x-ray. Hepatic transposition is associated with transposition of the great vessels, tetralogy of Fallot, pulmonary stenosis, asplenia, duodenal stenosis or atresia, preduodenal portal vein, and biliary atresia. Mortality from associated malformations is as high as 50%.20

In three cases of situs inversus in adults without associated malformations, the arterial distribution was neither normal nor a true mirror image. Large intrahepatic anastomoses between right and left hepatic arteries were present.21

Anomalous Lobes of the Liver

Riedel’s Lobe

An anomalous tongue of liver extending downward from the right lobe in ten female patients was described by Riedel22 in 1888 (Figs. 19-3, 19-4, 19-5). Reitemeir and colleagues at the Mayo Clinic23 reported 31 cases, all but one in women between 31 years and 77 years of age. Using radionuclide imaging, Baum and colleagues24 found Riedel’s lobe in 19.4% of females and 6.1% of males. The hepatic tissue of the lobe was normal and often fixed to the colon at the hepatic flexure. In one patient, it produced partial colonic obstruction.25 In a more recent case, El Haddad and colleagues26 found total pyloric obstruction from a cystogastrocolic band that contained ectopic liver tissue. McGregor27 considered such bands to represent persistent portions of the embryonic ventral mesentery. Similar tongues of hepatic tissue have been reported on the left.28 The chief significance of Riedel’s lobe is that it presents as an unexplained abdominal mass. If such a lobe is present, a liver scan or ultrasound will identify it.

Fig. 19-4.

An anomalous lobe on the left side of the liver resembling Riedel’s lobe on the right side. (Modified from Dick J. Riedel’s lobe and related partial hepatic enlargements. Guy Hosp Rep 100:270-277, 1951; with permission.)

Fig. 19-5.

Examples of Riedel’s lobe of the liver. (Modified from Skandalakis JE, Gray SW (Eds). Embryology for Surgeons, 2nd Ed. Baltimore: Williams & Wilkins, 1994; with permission. Redrawn from Dick J. Riedel’s lobe and related partial hepatic enlargements. Guy Hosp Rep 100:270-277, 1951.)

Gillard et al.29 stated, “Although the identification of Riedel’s lobe has been valuable on both clinical and anatomical grounds, the usefulness of the term is now perhaps limited because of its relative prevalence as shown by modern cross-sectional imaging.”

Supradiaphragmatic Liver

Four cases of liver tissue sequestered above the diaphragm in the right thorax have been reported in living patients. In each case, the ectopic mass was attached to the liver by a pedicle passing through a small aperture in the diaphragm without a hernial sac (Fig. 19-6). The pedicle contained branches of the hepatic artery, portal vein, and bile duct, and, in one patient, the gallbladder. All cases were asymptomatic except one.30

Fig. 19-6.

Anomalous supradiaphragmatic lobe of the liver with a pedicle passing through the diaphragm, carrying an artery, a vein and a bile duct. (Modified from Skandalakis JE, Gray SW (Eds). Embryology for Surgeons, 2nd Ed. Baltimore: Williams & Wilkins, 1994; with permission.)

Because the liver forms within the transverse septum, it is surprising that portions of the liver above the diaphragm are not more common. Mendoza et al.31 reported hepatic tissue in the lung.

Accessory and Ectopic Lobes of the Liver

Heterotopic nodules of liver tissue have been described on the surface of the gallbladder,32 in the gallbladder wall,33 associated with the pancreas,34 and in an adrenal gland,25 splenic capsule,35 and omphalocele.36

Mesenchymal Hamartoma

First described in 1903 by Maresch,37 mesenchymal hamartoma is a rare, usually asymptomatic tumor of the liver. It appears shortly after birth or later in adult life38-40 as a rapidly enlarging mass in the right upper quadrant. Such a tumor can weigh as much as 3 kg and can cause respiratory embarrassment by its sheer size. Shuto and colleagues41 mentioned the appearance of 30 cases of such tumors in the Japanese literature and about 100 cases in English-language reports. These authors reported a case of bilateral lobectomy excluding the caudate lobe for giant mesenchymal hepatic hamartoma.

The tumor consists of loose fibrous connective tissue with multiple cysts ranging in size from microscopic to several centimeters in diameter. Some tumors are largely cystic; others are predominantly fibrous. If the tumor is pedicled, a simple resection will be effective. A broader attachment may require lobectomy. We have found no reports of recurrence after operation.

Intrahepatic Biliary Atresia

In this defect, there is absence of interlobular bile ducts, with or without patent extrahepatic bile ducts. Bile canaliculi are present. Whether the defect is congenital and an extension of extrahepatic biliary atresia, or acquired following hepatitis is unresolved. At the present time the most acceptable etiology is progressive fibrosis and destruction of the epithelial elements by viral, toxic, or immunologic mechanism.

Intrahepatic biliary atresia was first described in 195142 and is less common than extrahepatic biliary atresia. Most affected individuals die before the age of four years; however, some have lived as long as 13 years.43 Longmire44 believed that there may be varying degrees of hypoplasia. It is difficult to explain the long survival time if atresia is complete. At present, liver transplantation offers the greatest hope for effective treatment of intrahepatic biliary atresia.

Cysts

Congenital solitary nonparasitic cysts of the liver were reported by Quillin and McAlister45 and Karia et al.46 These are very rare cysts presenting as abdominal masses.

Koperna et al.47 concluded that laparoscopic fenestration of nonparasitic hepatic cysts should replace the conventional surgical technique.

Congenital Hepatic Fibrosis

Congenital hepatic fibrosis is an anomaly that has not been well established. Desmet48 postulates that congenital fibrosis is secondary to faulty development of interlobular bile ducts due to destructive cholangiopathy. Sung et al.49 and Lipschitz et al.50 each reported a case.

Bands of fibrous tissue with linear and circular degeneration, lined with bile duct epithelium as a simple entity but usually associated with pancreatic or renal anomalies, were reported by Murray-Lyon et al.51 as congenital hepatic fibrosis. Annand et al.52 presented this anomaly associated with polycystic renal disease.

Vascular Malformations

Congenital vascular malformation of the liver ranging from solitary hemangiomas to multiple hemangioendotheliomas are now being discovered with increased frequency. The increase is due to the widespread use of prenatal and neonatal ultrasound.

Gedaly et al.53 stated that cavernous hemangiomas of the liver can be removed safely by either hepatic resection or enucleation. Enucleation is associated with fewer intraabdominal complications and should be the technique of choice when tumor location and technical factors favor enucleation.

Surgical Anatomy

Physical Characteristics and Topography

Weight

The human liver is the largest solid organ of the body, weighing about 150 g at birth. The weight of the liver of the adult male ranges from 1.4 kg to 1.8 kg, and the adult female from 1.2 kg to 1.4 kg.54 The actual weight varies with the individual’s age, sex, somatotype, and state of health.

Because of the role of the liver in blood formation during fetal life, the organ at birth contributes 4% to 5% to body weight. In the newborn infant, the liver bulges both the left and right hypochondrium. The effect of the weight of the liver on the location of the infant’s center of gravity may be an important factor in the development of the ability to attain upright posture and locomotion.

Shape

The liver is wedge-shaped. Its average transverse diameter is 20 cm to 23 cm and its anteroposterior diameter is 10 cm to 12.5 cm at the area of the upper pole of the right kidney.55 The craniocaudal span at the right midclavicular line has been measured by scintigram,56 percussion,57 extremely soft percussion, and ultrasound.58 The ultrasound technique provides consistently higher values than do other methods of measurement. The effect of the liver on the percussion note evoked extends above the actual upper limit of the organ. Thus the upper border lies slightly below the line along which the percussion note changes.59

Extension of the inferior border of the liver below the costal margin can occur incidental to disorders other than liver enlargement. If a liver possesses a long, thin anterior inferior edge or a so-called “Riedel’s lobe,” the organ may be considered enlarged. The liver may also descend after weight loss.

Location and Extent

In the adult, the liver fills the right hypochondrium and the epigastric regions. It extends inferiorly into the right lumbar region and occupies part of the left hypochondrium, reaching to the left lateral line. The liver is covered by ribs and costal cartilages, except in the epigastric region where it reaches the anterior abdominal wall just below the infrasternal notch.

The right side of the liver is closely applied to the costal muscle fibers and the central tendon of the right leaf of the diaphragm. The left lobe (the apex of the “wedge”) reaches for a variable distance into the left upper part of the abdominal cavity, abutting the left leaf of the diaphragm.

The right lobe of the liver apposes the bony thoracic wall. Convenient sites for transthoracic puncture for liver biopsy are present in the anterior axillary line at the seventh to ninth interspaces, always one interspace below the upper limit of liver dullness. Ultrasound guidance is increasingly used to obtain an appropriate window for percutaneous biopsy.

Flament et al.60 reported the following anatomic and nonanatomic factors responsible for the fixation of the liver at the right upper quadrant of the abdomen.

Anatomic

 

Inferior vena cava

Suprahepatic veins

Several ligaments such as the round ligament and coronary ligament

Peritoneal folds

Nonanatomic

 

Positive intraabdominal pressure

Outlines of the Liver on the Anterior Body Wall

See Figure 19-7 to trace the outline of the liver on the anterior body wall:

 

Point A is 1 cm (about one-half fingerwidth) below the right nipple at the level of the fifth rib

Point B is located approximately 2 cm (about one fingerwidth) inferior to and medial to the left nipple, at the level of the left fifth intercostal space

Point C is in the right costal margin at the anterior axillary line

Fig. 19-7.

Projection of the liver on the anterior body wall. Points A-C are the usual landmarks by which the position can be established. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Lockhart et al.61 charted the approximate rib levels of the liver, lungs, and pleurae (Fig. 19-8).

Fig. 19-8.

Surface projections of the liver on the thoracic wall from A) anterior, B) posterior, and C) lateral views. The inferior limits of the lung parenchyma and the parietal pleura are noted beneath each figure and illustrated for comparison with the liver projections. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 2. Contemp Surg 30:26-38, 1987; with permission.)

The gallbladder attaches to the visceral surface of the liver and moves with it. The fundus usually projects below the liver margin and lies in contact with the anterior abdominal wall near the intersection of the ninth costal cartilage and the lateral border of the rectus sheath.

Individual Location

In broad-chested individuals, the left side of the liver is more prominent than in slender individuals. In the latter, the organ is disposed principally to the right of the midsagittal plane and can extend considerably below the right costal margin.

Motion and Activity

The position of the liver in the body is not static.59 The liver moves up and down with the diaphragm and rotates during respiration. It rotates backward when an individual lies down in the supine position. The upper surface of the liver can move upward from 1 cm to 10 cm when full expiration follows deep inspiration. The most cranial level attained by the upper border of the liver during quiet respiration shows great individual variation and reflects the type of diaphragm —high, intermediate, or low. These facts should be kept in mind when interpreting radiographic images. Fig. 19-8 summarizes the typical bony relationships of the superior extent of the liver and the inferior extent of the lungs and parietal pleura.

Remember

 

The healthy adult liver weighs between 1.0 kg and 2.0 kg.

Dimensions of the liver are as follows:

Anteroposteriorly, the distance extends 10.0 cm to 12.5 cm from the area related to the anterior abdominal wall to its rounded posterior surface

 

– The transverse diameter is 20.0 cm to 25.5 cm from the right paracolic gutter to the midpoint of the left diaphragmatic leaflet

– The anteroinferior edge stretches vertically 15.0 cm to 17.5 cm to the top of the dome of the right hepatic lobe

According to Gelfand,62 the obscurity of the hepatic borders on x-ray is due to the specific gravity of the liver (1.05). This is almost the same as all other “water density” tissues such as the diaphragm and gastrointestinal wall. The presence of fat helps prevent the blending of the liver margins with other organs. The same author stated that the anatomic relations between hepatic substance and fat are extremely important for radiographic determination of the hepatic borders.

The shadow of the inferior border expressed on x-rays is due to the combined effects of the amount of retroperitoneal fat, habitus of the patient, and “hepatic angle” (junction between lateral and inferior hepatic borders).

Surgical Considerations

 

The procedure to be performed and body habitus of the patient dictate the selection of the incision. Most surgeons use a long bilateral subcostal incision with perixiphoid extension for major hepatic resections. Combined with newer retraction systems, this incision provides wide and deep exposure. Recent reports show renewed interest in right thoracoabdominal approaches to large right lobe lesions. However, the surgeon should use the incision with which he or she is most familiar and comfortable.

Preparation of the GI tract is essential for surgery with hepatomegaly of known or unknown etiology or in cases of prior abdominal surgery (especially in cirrhotic patients).

Perihepatic adhesions should be cut carefully to avoid injury of Glisson’s capsule. Occasionally these adhesions are vascular or contain minute bile ducts. Electric cautery is advised.

Remember the relation of the liver to the diaphragm above and the several anatomic entities below.

Topographic Relations of the Liver

Although wedge-shaped and, hence, having three surfaces, the liver is “a cast of the cavity in which it grows.”63 Thus, it is convenient to think of this cast of the upper abdomen as having two surfaces, diaphragmatic and visceral (Figs. 19-9, 19-10, 19-11, and 19-12). The radiologist uses this concept.59 The diaphragmatic surface is molded by the diaphragm. The visceral surface bears impressions from the stomach, duodenum, transverse colon, and, a beautiful radiologic landmark, the right kidney.

Fig. 19-9.

Diaphragmatic aspect of the liver illustrating features of the anterior and superior surfaces. This specimen from a broadchested, muscular (mesomorphic habitus) individual is seen also in Figures 19-11 and 19-12. The liver measured 21 cm transversely, 20.3 cm vertically, and 14.6 cm in thickness. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 2. Contemp Surg 30:26-38, 1987; with permission.)

Fig. 19-10.

Diagram of the posterior aspect of the liver to show the arrangement of the peritoneal attachments. Note the horizontal course of the left branch of the portal vein and the comparatively short course of the right branch.

Fig. 19-11.

Posterior aspect of the liver. The distinction between the left and right layers of the falciform ligament is slightly exaggerated to emphasize the contributions of these to the left triangular ligament and coronary ligament, respectively. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 2. Contemp Surg 30:26-38, 1987; with permission.)

Fig. 19-12.

Visceral aspect of the liver. The inferior margin of the anterior surface is uppermost in the figure. The major impressions on the liver made by the stomach, colon, and right kidney are seen clearly. A bridge of hepatic parenchyma bridges the groove for the ligamentum venosum in this specimen. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 2. Contemp Surg 30:26-38, 1987; with permission.)

Diaphragmatic Surface

The diaphragmatic surface may be divided into superior, posterior, anterior, and right portions.

 

Superior: The superior portion is related to the diaphragm and the following organs from right to left: right pleura and lung, pericardium and heart (cardiac impression), left pleura and lung. The superior surface is covered with peritoneum except where, more dorsally, the superior reflection of the coronary ligament bounds the bare area of the liver.

Posterior: The posterior portion is related to the diaphragm and lower ribs. It contains the greater part of the bare area and the sulcus of the inferior vena cava (IVC).

Anterior: The anterior part is related to the diaphragm and costal margin, xiphoid process, the abdominal wall, and the sixth to tenth ribs on the right.

Right: The right portion is related to the diaphragm and the seventh to eleventh ribs. It is a lateral continuation of the posterior portion.

The diaphragmatic surface separates from the visceral surface at the inferior border. This surface is blunt, rounded, and unmarked posteriorly but sharp anteriorly. The clinician palpates this sharp anterior portion. However, the liver “edge” seen in a plain x-ray is the rounded posterior border. This is not a true border but represents the interface of the posterior aspect of the right lobe of the liver with retroperitoneal fat.

Anteriorly, the inferior border of the liver is marked by two notches to the right of the median plane. These are:

 

Deep notch accommodating the ligamentum teres (Fig. 19-9, Fig. 19-10)

Shallow notch allowing space for the gallbladder (Fig. 19-9)

More details of the radiology of the liver can be found in the excellent works of Whalen,59 Gamsu and associates,64 and Meyers.65

Falciform Ligament

The anterior surface of the liver is covered entirely by peritoneum except at the sagittal line of attachment of the falciform ligament (Fig. 19-11). The falciform ligament extends from the anterior surface of the liver to the diaphragm and the anterior abdominal wall and is disposed at a variable distance to the right of the midline. It contains the ligamentum teres (Figs. 19-9 and 19-10), the obliterated left umbilical vein. The ligamentum is typically accompanied by one or more paraumbilical veins in the adult. Remember that the right umbilical vein is “lost in space” very early. But in a study of 340 liver cirrhosis patients, Ibukuro et al.64 reported the hepatic falciform ligament artery (HFLA) as follows:

The HFLA was demonstrated in 26 (7.6%) of the 340 patients on angiography. Two HFLAs were observed in one patient. The origin was the middle hepatic artery (A4) in 16 cases, the superior branch of the middle hepatic artery in three, the inferior branch of the middle hepatic artery in two, the inferior branch of the left hepatic artery (A3) in three, and the confluence of A3 and A4 in three cases.

Baba et al.67 stated that the pathway of the hepatic falciform artery should be recognized before chemoembolization of the middle or left hepatic artery.

The left leaf of the falciform ligament continues laterally where, superiorly, it becomes the left triangular ligament (Figs. 19-9, 19-10). This ligament consists of the two fused layers of peritoneum from the anterior and posterior surfaces of the left lobe. It suspends the left lateral segment from the diaphragm. If the left triangular ligament is divided, the lateral segment of the left lobe becomes freely mobile. The medial inferior aspect of the left triangular ligament is continuous with the anterior layer of the lesser omentum (Fig. 19-10).

The presence of blood vessels, aberrant bile ducts, cords of hepatocytes, and nerves in the free edge of the left triangular ligament has long been known.68 More recently, Gao and Roberts69 showed that biliary ducts may be found in 80% to 90% of individuals examined, liver cords in 60%, nerve bundles in 80%, and blood vessels are always present. When sectioning the ligament, the surgeon must watch for bleeding and bile leakage.70

The right leaf of the falciform ligament diverges at the superior aspect of the liver, successively forming the superior layer of the coronary ligament (Fig. 19-9, Fig. 19-11), right triangular ligament (Fig. 19-10), and inferior layer of the coronary ligament. To the left of the midline, it forms the posterior layer of the lesser omentum.

Visceral Surface

In contrast to the smooth, rounded, generally convex shape of its parietal surface, the visceral surface of the liver (Fig. 19-12) is distinctly concave in form with variably distinct impressions from adjacent organs, intervening fat, and connective tissues, both posteriorly and inferiorly.

In addition to the contours attributable to other organs, the visceral surface is characterized by indentations that outline the porta hepatis, gateway to the liver (Fig. 19-13). These landmarks form a capital “H” (Hepar) configuration in many individuals, although they can also resemble a capital “K.”

Fig. 19-13.

Porta hepatis and features of the visceral surface of the liver. A. Typical orientation of the “H” configuration of the portal structures. B. Common but incorrect depiction of relationship of “H”-parallel with the mid-sagittal plane of the body. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 2. Contemp Surg 30:26-38, 1987; with permission.)

The right limb of the “H” bordering the porta is formed anteriorly by the fossa for the gallbladder and posteriorly by the fossa for the inferior vena cava. The left limb is formed anteriorly by the fissure for the round ligament and posteriorly by the fissure for the ligamentum venosum. The porta hepatis forms the crossbar of the “H.” Posterior to the crossbar is the caudate lobe; anterior to the crossbar is the quadrate lobe.

The visceral surface relates to several organs; we will describe them from right to left. The hepatic flexure of the colon and part of the transverse colon are related to the anterior one-third of the visceral surface of the right lobe, passing behind the sharp, anterior inferior margin of the liver. The colic impression (Fig. 19-12) begins at the right lobe and ends at the quadrate lobe.

Behind the colic impression is the renal impression (Fig. 19-12, Fig. 19-13), produced by the right kidney and right adrenal gland. Fat, connective tissue, and peritoneum intervene between these organs and the liver. The right adrenal gland is in contact with the bare area of the liver.

The gallbladder lies in a fossa (Fig. 19-13) just beneath the anterior inferior border of the liver. To the left of the gallbladder is a depression for the first and second portions of the duodenum. Posterior to the gallbladder fossa is the fossa for the inferior vena cava.

Posteriorly and to the left of the ligamentum venosum (the posterior limb of the “H”), one can see a small impression for the abdominal esophagus. Almost the entire visceral surface of the left lobe is in contact with the stomach, forming the gastric impression (Fig. 19-12, Fig. 19-13).

Surgical Considerations

 

The right lobe of the liver has a convex surface and right lateral surface. The convex surface is subdivided into superior and anterior. The superior convex surface relates to the right hemidiaphragm covered by peritoneum below and pleura above, the right pleural cavity, and the lower lobe of the right lung. The anterior convex surface relates to the right costal margin and right upper abdominal wall. The right lateral surface relates to the right costodiaphragmatic recess and to the right thoracic wall from the 7th to 11th ribs.

The left lobe of the liver relates to the diaphragm. Under normal conditions and for all practical purposes, the left lobe is not related to the left upper abdominal wall.

We have seen a few patients with echinococcal cysts of the right lobe of the liver penetrate through the right hemidiaphragm and into the lower lobe of the right lung. These cysts evacuated into the bronchial tree and the patient coughed out the material. The pathway for evacuation of the cyst created by adhesions of the anatomic entities involved is a magnificent phenomenon of nature.

Percutaneous needle biopsy of a solid or cystic mass at the superior convex of the right lobe will penetrate pleura, diaphragm, and peritoneum. For further details, see the section that follows considering supra- and infrahepatic collection.

Pathology of the anterior convex surface may be reached by a needle penetrating only the peritoneum.

Peritoneal Relations

An imaginary cross-sectional plane passing through the transverse mesocolon defines a supracolic and an infracolic compartment of the peritoneal cavity. Within the supracolic compartment lie the liver and its attachments. These define the right and left suprahepatic (subdiaphragmatic or subphrenic) and right and left subhepatic spaces.

Ventral Mesogastrium

The supracolic compartment is the most difficult area of the abdomen to conceptualize. Our description is based on the work of Livingstone,71 Ochsner and Graves,72 Mitchell,73 Autio,74 Boyd,75 Meyers,76 and Whalen.59

Early in embryonic development, both a dorsal and a ventral mesentery are present. All the ventral mesentery except the foregut disappears. The persisting ventral mesentery extends from the abdominal esophagus to the umbilicus. It contains liver, stomach, and the first 2 cm of the duodenum. The liver divides this mesentery in two, forming the falciform ligament anteriorly and the lesser omentum posteriorly.

As noted earlier, the falciform ligament passes obliquely from the umbilicus to the superior surface of the left lobe of the liver. Here it marks the fissure between the medial and lateral segments of the left lobe (Fig. 19-14). In its free edge, the falciform ligament contains the remnant of the proximal part of the left umbilical vein, the round ligament of the liver or ligamentum teres. The right umbilical vein disappears early in development. The left vein returns placental blood to the fetus and closes soon after birth. In adults, the left umbilical vein may remain patent for much of its length.77 The terminal portion of this vein is retained as the ligamentum venosum, a structure connecting the left branch of the portal vein with the left hepatic vein.

Fig. 19-14.

Anterior view of the liver. The esophagus is pulled upwards from its normal position behind the left lobe to show the peritoneal attachments. All peritoneal edges seen here are attached to the diaphragm. (Modified from Last RJ. Anatomy: Regional and Applied, 5th Ed. Baltimore: Williams & Wilkins, 1972; with permission.)

We have seen two cases in which the falciform ligament was only partially attached to the anterior abdominal wall. This created a hiatus through which a loop of intestine might have passed, causing a partial or complete small bowel incarceration.

The leaves of the falciform ligament separate as they reach the liver to form the superior layer of the coronary ligament (Fig. 19-15). Laterally, the layers reflect back medially to form the right and left triangular ligaments. They are not symmetrical. The right is more posterior and lateral. The left is more superior and medial. On the left, the anterior and posterior layers are almost in apposition until they reach the abdominal esophagus. On the right, the layers diverge as they approach the inferior vena cava. This wide separation is often surgically termed the “right coronary ligament” (Fig. 19-16). There are not distinctly separate right and left coronary ligaments, but the terms are convenient for the surgeon who is exploring the gastroesophageal junction.

Fig. 19-15.

Posterior view of the liver. The under surface of the organ, sloping down to the anterior border, is visible from this aspect. The peritoneal attachments are shown. The cut edges around the porta hepatis and in the lower part of the lesser omentum are attached to the lesser curvature of the stomach; all other peritoneal edges seen here are attached to the diaphragm. (Modified from Last RJ. Anatomy: Regional and Applied, 5th Ed. Baltimore: Williams & Wilkins, 1972; with permission.)

Fig. 19-16.

Peritoneal reflections of the stomach, gastroesophageal junction, and bare area of the diaphragm.

In spite of the convenience of the terminology, however, the concept of a “right” and a “left” coronary ligament has to be corrected. Only a left triangular ligament and the complex of coronary and right triangular ligaments exist. To be accurate we should name the layers of the coronary ligament “superior” rather than “anterior” and “inferior” rather than “posterior.” Furthermore the liberal use of the term “ligament” to describe mesothelium-covered conduits to and from the respective organs has to be revised; actually these are peritoneal attachments or reflections. We suggest use of “left triangular peritoneal attachment” of the liver instead of “left triangular ligament” and “coronary peritoneal attachment” of the liver instead of “coronary ligament.”

Nevertheless, the old terminology is so ingrained in our thinking and writing that we continue to use it and it will be found within this text. We do hope, though, that our recommended terminology will be adopted and will come into everyday usage.

The posterior component of the ventral mesentery forms the lesser omentum (Fig. 19-16). This may be divided into the proximal hepatogastric and distal hepatoduodenal ligaments. The hepatogastric ligament extends from the porta hepatis to the lesser curvature of the stomach and the abdominal esophagus. The ligament encloses the gastroesophageal junction on the right and the two leaves rejoin on the left as the gastrosplenic ligament, a portion of the embryonic dorsal mesentery. The posterior leaf does not reach the gastroesophageal junction. Therefore, the small bare area on the posterior wall of the stomach lies on the left crus of the diaphragm and is related to the left adrenal gland and the left gastric artery and vein.78 The abdominal esophagus is covered partially by peritoneum in front and on its left lateral wall.

The hepatogastric ligament contains the left gastric artery and vein and the hepatic division of the left vagal trunk. Occasionally, it may contain the right gastric artery and vein and both vagal trunks. In about one-fourth of subjects, it contains an aberrant left hepatic artery that arises from the left gastric artery.79

The hepatoduodenal ligament extends between the liver and the first portion of the duodenum and is continuous with the right border of the hepatogastric ligament. It contains the common bile duct, hepatic artery, and portal vein as well as the hepatic plexus and lymph nodes. Consider this ligament as the mesentery of the portal triad. It also forms the anterior boundary of the epiploic foramen of Winslow.

Dorsal Mesogastrium

Unlike the ventral mesentery, the primitive dorsal mesentery persists in the adult. In the supracolic compartment, it forms the greater omentum (Fig. 19-16). Initially, the fetal dorsal mesentery extended from the dorsal border of the stomach to the midline of the posterior abdominal wall. This simple relationship changes as a result of the 90° counterclockwise rotation of the stomach and the development of the spleen.

The embryonic dorsal mesentery of the supracolic compartment may be divided into the following three parts.

 

Upper, the gastrophrenic ligament

Middle, the gastrosplenic ligament

Lower, the gastrocolic ligament

In addition, the middle portion is interrupted by the spleen to form posteriorly the splenorenal ligament (Fig. 19-16).

Surgical Considerations

 

The falciform ligament may be cut with impunity if necessary. The cut should be made between proximal and distal ligations to avoid bleeding from a patent round ligament (left umbilical vein).

The left coronary ligament, including its lateral end or triangular ligament, may be also sacrificed without negative consequences using electrocautery. However, the surgeon should remember not to be overenthusiastic when cutting this ligament medially, as one may encounter the left hepatic vein in this area.

The right triangular, superior, and inferior coronary ligaments may be cut successfully using electrocautery. The superior right coronary ligament is cut with ease. Then, by anterior and caudal elevation of the right lobe, the inferior right coronary ligament is incised carefully to the foramen of Winslow. At that point the right lobe is mobilized.

The hepatogastric ligament is routinely divided during mobilization of the liver or stomach. The surgeon must take care to preserve a dominant left hepatic artery that travels through the ligament if a right hepatic lobectomy is planned, if the patient has cirrhosis, or if the patient has had prior interruption of the right hepatic artery. Division of the artery in these circumstances may lead to ischemia and insufficiency of the left lobe.

Perihepatic Spaces

Among the several spaces that the peritoneum forms in the supracolic compartment are those above and below the liver. These are extremely important to the radiologist and the surgeon. We follow the nomenclature of Whalen59 and of Ochsner and DeBakey80 in part, realizing that it is arbitrary.

Suprahepatic Spaces

A portion of the superior surface of the liver and a corresponding portion of the inferior surface of the diaphragm are in direct contact with one another without being covered by peritoneum. This area of contact is the “bare area.” Its margins are the falciform, coronary, and left and right triangular ligaments of the liver (Fig. 19-15, Fig. 19-16, Fig. 19-17).

Fig. 19-17.

The inferior surface of the diaphragm showing the peritoneal attachments of the liver (dashed lines). Within the boundaries of these attachments is the “bare area” of the liver and the diaphragm. The arrow represents the pathway behind the abdominal esophagus where surgeons may pass a finger through the inferior layer of the coronary ligament. (Modified from Gray SW, Rowe JS Jr, Skandalakis JE. Surgical anatomy of the gastroesophageal junction. Am Surg 45(9):575-587, 1979; with permission.)

Except over its bare area, the serous surfaces of the liver and diaphragm are side by side and separated by a potential space. This potential space may become the site of intraperitoneal fluid collection and of suprahepatic (subphrenic) abscess.

The suprahepatic potential space is divided into right and left spaces by the falciform ligament. The right suprahepatic space (Fig. 19-18) lies between the diaphragm and the anterosuperior surface of the right lobe and the medial segment of the left lobe of the liver. The boundaries are:

 

Left — falciform ligament

Posterior — right superior coronary and right triangular ligaments

Inferior — right lobe and medial segment of the left lobe of the liver

Fig. 19-18.

Diagrammatic parasagittal section through the upper abdomen showing the potential right suprahepatic and subhepatic spaces. The thick black line represents the diaphragm. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

The space opens into the general peritoneal cavity anteriorly and inferiorly.

The corresponding suprahepatic space on the left (Fig. 19-19) is between the diaphragm and the superior surface of the lateral segment of the left lobe of the liver and the fundus of the stomach. To the right, the left suprahepatic space is bounded by the falciform ligament and, posteriorly, by the left coronary and triangular ligaments. Anteriorly and laterally, the space communicates with the infrahepatic space and the general peritoneal cavity. On the left, the anterior and posterior leaves of the coronary ligament are side by side. The left triangular ligament separates the anterior and superior suprahepatic spaces.

Fig. 19-19.

Diagrammatic parasagittal section through the trunk showing the potential left suprahepatic and subhepatic spaces. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Min et al.81 report that the posterior left suprahepatic space is located anterior and superior to the lesser sac, with inferior continuation to the gastrohepatic space. These authors emphasize that the left posterior suprahepatic space and the lesser sac are separated by the lesser omentum and the stomach.

Each suprahepatic space may be divided into anterior and posterior portions. The distinction is unimportant in the absence of disease. On the right, fluid may collect or an abscess may form between the liver and diaphragm anteriorly just beneath the sternum (right anterior suprahepatic abscess) (Fig. 19-20). Or an abscess may form at the reflection of the superior leaf of the coronary ligament (right posterior suprahepatic abscess) (Fig. 19-21). The single space of the anatomist may be divided by pseudomembranes into two spaces.

Fig. 19-20.

Relations of an abscess in the anterior portion of the right suprahepatic space. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Fig. 19-21.

Relations of an abscess in the posterior portion of the right suprahepatic space. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

The left suprahepatic space may be similarly compartmentalized by pseudomembranes between the liver and diaphragm or the abdominal wall (Fig. 19-22, Fig. 19-23). The left suprahepatic and left anterior infrahepatic spaces are not separated anatomically, but they may become separate pathologically by pseudomembranes. Large accumulations of fluid may extend into the subhepatic space where the stomach, spleen, and liver participate in walling off the infection. The diaphragm is usually elevated over the abscess or fluid collection.

Fig. 19-22.

Relations of an abscess in the anterior portion of the left suprahepatic space. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Fig. 19-23.

Relations of an abscess in the posterior portion of the left suprahepatic space. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Anteriorly, a surgical approach from beneath the costal margin presents no anatomic complications. Posteriorly, the approach must be by an incision at the level of the spinous process of the first lumbar vertebra. This method avoids the pleura. The pleura and the twelfth rib are related at the vertebral spine. Thus the surgeon must avoid traversing the bed of the twelfth rib.

Infrahepatic Spaces

The right infrahepatic space (Fig. 19-24) (subhepatic space, hepatorenal space, pouch of Morison) is bounded superiorly and anteriorly by the right lobe and medial segment of the left lobe of the liver and the gallbladder. It is limited superiorly and posteriorly by the inferior layer of the coronary ligament and the posterior layer of the right triangular ligament. Inferiorly, the space opens into the general peritoneal cavity and is partly bounded by the hepatic flexure of the colon and the transverse mesocolon and, medially, by the hepatoduodenal ligament. The right suprahepatic space communicates with the right infrahepatic space in three places: the margin of the right lobe of the liver; the right triangular ligament; and a small space, the quadrangular space of Mitchell. The quadrangular space is bounded above by the quadrate lobe of the liver, below by the transverse colon, on the left by the falciform ligament, and on the right by the gallbladder. The coronary ligament suspends the liver not from above but from the dorsum. The left triangular ligament suspends the left lobe not from the apex of the diaphragm but from the dorsal aspect of the diaphragm.75

Fig. 19-24.

Relations of an abscess in the right infrahepatic space. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

The left infrahepatic space (Fig. 19-25) may be divided into the smaller antegastric space and the larger lesser sac of the peritoneum.

Fig. 19-25.

Relations of an abscess in the left infrahepatic space. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Antegastric Space

The anterior space lies between the left lobe of the liver above and the stomach below and behind (Fig. 19-25). The boundaries are:

 

Superior and anterior, the left lobe of the liver and the anterior abdominal wall

Posterior, the stomach and lesser omentum

Inferiorly, the middle third of the transverse colon.

This space has been termed “perigastric,” but this is misleading; “paragastric” might be better. This space is entirely anterior to the stomach. Hollinshead82 believes it is merely part of the left suprahepatic (subphrenic) space in general.

Lesser Sac

The lesser sac of the peritoneum becomes, by the terminology used here, the left posterior infrahepatic space. This is a valid concept. For practical purposes, our two preferred terms are the “lesser sac” or the “omental bursa.”

Extraperitoneal Spaces

There are two potential extraperitoneal spaces in which abscesses can occur. On the right, abscesses may form over the bare area of the liver that is outlined by the falciform, coronary, and triangular ligaments (Fig. 19-17). On the left, they may occur in a poorly defined space that is bounded by the distal pancreas, the descending (left) colon, the upper pole of the left kidney, the left adrenal gland, Gerota’s perirenal fascia, and fat. Altemeier and Alexander83 discuss these and other sites of retroperitoneal abscesses.

Surgical Considerations

 

Ultrasonography, CT scan, or MRI will help the surgeon decide whether to use the closed or open method in the treatment of a perihepatic abscess.

Percutaneous needle-guided drainage (closed method) may be achieved by guiding the needle into the abscess cavity, advancing a wire into the cavity, dilating the tract around the wire with successively larger dilators, and placing a self-retaining catheter into the cavity or cavities.

Open method

 

– Drain a right anterior subphrenic (suprahepatic) abscess using a small right subcostal incision to establish an extraperitoneal route (Fig. 19-26).

– Reach a right posterior subphrenic abscess (suprahepatic or infrahepatic) using a posterior route through the bed of the already excised 12th rib. Push the right kidney and the right adrenal gland downward (Fig. 19-27).

– Approach a left anterior suprahepatic or infrahepatic abscess (Fig. 19-28) anteriorly using a small LUQ incision and proceeding intra- or extraperitoneally.

– A left posterior suprahepatic or infrahepatic abscess can be approached as on the right posterior, pushing the peritoneum down over the spleen and the gastric fundus. This forms a space between these two organs and the diaphragm.

Fig. 19-26.

Extraperitoneal drainage of anterior subphrenic and subhepatic abscesses. Schematic position of drains. Note the position of the drain for subphrenic abscesses between parietal peritoenum and diaphragm. The drain tract to the subhepatic abscess is walled off from the rest of the peritoneal cavity by adhesions between the loops of small intestine. (Modified from Hau T. Drainage of hepatic, subphrenic, and subhepatic abscesses. In: Nyhus LM, Baker RJ, eds. Mastery of Surgery, 2nd Ed. Boston: Little, Brown, 1992; with permission.)

Fig. 19-27.

Extraperitoneal drainage of posterior subphrenic and subhepatic abscesses. Schematic position of the drains passing through the bed of the twelfth rib. Neither drain violates the peritoneal cavity. (Modified from Hau T. Drainage of hepatic, subphrenic, and subhepatic abscesses. In: Nyhus LM, Baker RJ, eds. Mastery of Surgery, 2nd Ed. Boston: Little, Brown, 1992; with permission.)

Fig. 19-28.

Transperitoneal drainage of subphrenic and subhepatic abscesses. Schematic position of drains. (Modified from Hau T. Drainage of hepatic, subphrenic, and subhepatic abscesses. In: Nyhus LM, Baker RJ, eds. Mastery of Surgery, 2nd Ed. Boston: Little, Brown, 1992; with permission.)

Lobes and Segments of the Liver

Bases of Hepatic Segmentation

On first inspection, the liver appears to be divided into a large right portion and a much smaller left portion. The apparent plane of division (left fissure) passes through the falciform ligament, the round ligament, and the ligamentum venosum. Unfortunately, this apparent division does not correspond to the internal distribution of bile ducts and blood vessels (Figs. 19-29, 19-30, 19-31, 19-32).

Fig. 19-29.

Hepatic “true” lobar and segmental divisions according to Ger. (Modified from Skandalakis JE. Liver anatomy [letter to the editor]. South Med J 73:1096, 1980.)

Fig. 19-30.

A. Three concepts of the liver lobule. The “classic” lobule, with central veins and peripheral hepatic triads; the “portal” lobule, centered on the hepatic triads; and the hepatic acinus. Both the central vein and the hepatic traids are peripheral. It is the concept of the acinus that has proved to be the most useful for understanding liver functions. B. Modern concept of the lobes and segments of the human liver. C to F. Projection of liver lobes and segments based on the distribution of intrahepatic ducts and blood vessels. C and D. Terminology of Couinaud (1954). E and F. Terminology of Healey and Schroy (1953). (CP, caudate process; RP and LP, right and left portions of the caudate lobe). G. Highly diagrammatic presentation of the segmental functional anatomy of the liver emphasizing portal distribution and hepatic veins. H. Exploded segmental view of the liver emphasizing the intrahepatic anatomy and hepatic veins. (A, Modified from Gray SW, Skandalakis JE, Colborn GL, Skandalakis LJ. Surgical anatomy of the liver and associated extrahepatic structures. Part 1. Contemp Surg 1987;30(4):37-47. B, Modified from Skandalakis JE. Liver anatomy [letter to the editor]. South Med J 1980;73:1096. C-F, Modified from Skandalakis JE, Gray SW, Skandalakis LJ, Colborn GL. Surgical anatomy of the liver and associated extrahepatic structures. Part 2. Contemp Surg 1987;30(5):26-38. G, H, Modified from Skandalakis JE, Gray SW (eds). Embryology for Surgeons, 2nd Ed. Baltimore: Williams & Wilkins, 1994. With permission.)

Fig. 19-31.

Exploded diagrammatic sketch of the liver. The umbilical fissure separates the anatomic left lobe (segments 2 and 3) from the right lobe (segments 4-8). The middle hepatic vein runs within the main portal fissure (Cantlie’s line), which separates the left liver (segments 2 to 4) from the right liver (segments 5 to 8). The hepatic veins are distributed on an intersegmental basis. VC, vena cava; R, right; M, middle; L, left hepatic veins, and 1, caudate lobe. (From Czerniak A, Lotan G, Hiss Y, Shemesh E, Avigad I, Wolfstein I. The feasibility of in vivo resection of the left lobe of the liver and its use for transplantation. Transplantation 1989;48:26; with permission.)

Fig. 19-32.

Differences in anatomic and surgical nomenclature of the liver. The division into lobes is based on external features. The division into segments is based on the intrahepatic ramifications of the hepatic veins and the portal elements. (Fr = French, US = American, NA = Nomina Anatomica). Editor’s note: The main portal fissure is also called the median fissure or the line of Rex. The umbilical fissure is also called the left fissure. (Modified from Van Damme JPJ. Behavioral anatomy of the abdominal arteries. Surg Clin North Am 73(4):699-725, 1993; with permission.)

Actual Structure

Injection and corrosion preparations, first made by Hjortsjo in 195184 and independently by Healey and Schroy in 1953,68 clearly show that the true right and left lobes of the liver are about the same size. Further, the lobes are separated by a plane called the median fissure that passes through the bed of the gallbladder below and the fossa of the inferior vena cava above (Fig. 19-29).

True Left Lobe and True Right Lobe

The true left lobe consists of a left medial segment and a left lateral segment (Fig. 19-29). The latter is the “left lobe” of older anatomic descriptions. Each of these two segments can be further divided into superior and inferior subsegments on the basis of the distribution of the bile ducts, hepatic arteries, and portal veins.

The true right lobe is divided by the right fissure into anterior and posterior segments. The plane of this fissure corresponds to the line of the eighth intercostal space. Each segment of the right lobe can be subdivided into superior and inferior subsegments.

Quadrate Lobe

The quadrate “lobe” is a portion of the inferior half or so of the medial segment of the left lobe (Figs. 19-12, 19-13, 19-15, 19-33A & B). According to Sales et al.,85 it lies to the right of the falciform ligament, anterior to the hilum, and to the left of the gallbladder. It is related to the pylorus and the first portion of the duodenum.

Fig. 19-33.

Morphology of the liver. A. Anterior view: 1. inferior vena cava, 2. right lobe, 3. left lobe, 4. fissura portalis sagittalis, 5. right liver, 6. left liver; B. Inferior view: 1. inferior vena cava. Editor’s note: The “left lobe” is, in modern terminology, the lateral segment of the left lobe. Segment IV is the medial segment of the left lobe. (Modified from Sales JP, Hannoun L, Sichez JP, Honiger J, Levy E. Surgical anatomy of liver segment IV. Anat Clin 1984;6:295; with permission.)

Caudate Lobe

The caudate lobe is a separate region divided by the interlobar plane into right and left subsegments. Its bile ducts, arteries, and portal veins arise from both right and left main branches. Hence, the plane between the true right and left lobes passes through the middle of the caudate lobe. The right portion of the caudate lobe is continuous with the true right lobe by the caudate process, or tuber. This process forms the superior boundary of the epiploic foramen. The caudate lobe is drained by two small, fairly constant hepatic veins that enter the left side of the vena cava. Names such as caudate and quadrate “lobes” are mentioned for convenience. They are not true lobes.

Padbury and Azoulay86 report the segmental anatomy of the liver as two hemilivers and a dorsal or caudate lobe (or Couinaud’s segment I). Segments II-IV form the left hemiliver. Segments V-VIII form the right hemiliver. (If we were to follow our own terminology, we would refer to them as “subsegments” II-IV and V-VIII rather than “segments,” but we follow Couinaud’s usage.)

Dodds et al.87 studied the caudate lobe from an embryologic, anatomic and pathologic standpoint. They report the following.

 

The caudate lobe may be hypertrophic (enlarged) secondary to liver cirrhosis, occlusion of the hepatic veins due to greater blood flow, and other focal lesions.

The caudal margin of the caudate lobe often attaches by a narrow connection to a papillary process. On CT, this may be identified as a large lymph node.

NOTE: The caudate (spigelian) lobe is the “third liver” of Bismuth.88 This terminology is used because the lobe has independent vascularization that receives branches from the right and left sides of the portal vein and hepatic artery, and its veins drain directly into the IVC.

Brown et al.89 emphasized the anatomic distinction of the caudate lobe from the left and right hepatic lobes. It is located between the IVC posteriorly, the left and right hepatic lobes anteriorly and superiorly, and the main portal vein inferiorly (Fig. 19-34, Fig. 19-35).

Fig. 19-34.

Diagrammatic illustration of the undersurface of the liver. The caudate lobe is distinct from the left and right hepatic lobes and is interposed between the inferior vena cava posteriorly and the left hepatic lobe anteriorly and superiorly. (Modified from Brown BM, Filly RA, Callen PW. Ultrasonographic anatomy of the caudate lobe. J Ultrasound Med 1982; 1:189; with permission.)

Fig. 19-35.

Diagrammatic illustration demonstrating the caudate lobe and its portal venous blood supply and hepatic venous drainage. (Modified from Brown BM, Filly RA, Callen PW. Ultrasonographic anatomy of the caudate lobe. J Ultrasound Med 1982;1:189; with permission.)

To be more specific, we quote Heloury et al.90 They define the caudate lobe as “. . .bounded . . .by the IVC on the right, by the fissure of the ligamentum venosum on the left, and by the hilum of the liver below and in front.” These authors report that the lobe is characterized by great morphologic variation. We strongly advise the study of their article.

Schwartz91 made the following points about the anatomy of the caudate lobe.

 

The caudate lobe is not a true lobe.

The caudate lobe is generally regarded as that portion of the liver between the line of Cantlie and the line corresponding to the falciform ligament.

It is posterior to an imaginary horizontal line in the porta hepatis.

It is divided arbitrarily and without good landmarks into the caudate lobe proper and a caudate process extending to the right lobe of the liver.

Its biliary drainage is usually into both right and left duct systems.

In most instances its arterial supply is from both right and left hepatic arterial branches. It originates totally from the right hepatic artery in 35% of cases and from the left hepatic artery in 12%.

In the Couinaud92 nomenclature, the caudate lobe makes up segment I.

According to Couinaud,92 its position varies with respect to the portal bifurcation and therefore may belong to only the left or right lobe, or it may belong to both.

We quote from Kogure et al.93 on their dissection studies of the human liver:

The caudate lobe exhibited distinct portal segmentation with a portal fissure that was indicated internally by the proper hepatic vein and externally by the notch at the caudal edge of the caudate lobe.

Hepatic segmental anatomy was also described in detail by Healey and Schroy,68 Healey,94 and Couinaud92 (Fig. 19-30B-E).

Using computed tomography scans to evaluate patients for resection of focal lesions, Rieker et al.95 found that the segmental anatomy of the liver using the planes of hepatic veins and portal trunks according to Couinaud was not an accurate tool for the presurgical localization of all liver lesions.

In 1957, Goldsmith and Woodburne96 presented another segmental terminology and nomenclature. For all practical purposes and “anatomically” at least, the paper of Goldsmith and Woodburne agreed with those of Healey and Schroy,68 Healey94 and Couinaud92 regarding hepatic segmentation. Therefore, all are correct, but because of different nomenclature, the surgical descriptions of liver resections are confusing.

Onishi et al.97 studied the surgical anatomy of the medial segment (segment 4) of the liver. They categorized two main types and several subtypes of bile duct branches, and the morphology of the portal vein, middle hepatic vein, and middle hepatic artery. They stated that knowledge of the topographic anatomy of the ducts and vessels will facilitate resection of the medial segment.

We quote from Cho et al.98 on the surgical anatomy of the right anterosuperior area (segment 8) of the liver:

In most of the patients, the dorsal branches of segment 8 supplied the dorsocranial area of the right lobe posterior to the right hepatic vein. The paracaval portion of the caudate lobe was limited to below the interval between the middle and right hepatic veins in the majority of patients who showed medial branches of segment 8 arising near the porta hepatis. Recognition of this vascular anatomy is clinically important for preoperative evaluation of hepatic tumors in segment 8 because it may contribute to a safer surgical approach.

Bismuth System and the Fissures

Soyer99 urged that the Bismuth system be accepted worldwide to put an end to ongoing confusion. Soyer’s table (Table 19-2) is self-explanatory.

Table 19-2. Anatomic Segments of the Liver and Corresponding Nomenclature

  Nomenclature
Anatomic Subsegment Couinaud Bismuth Goldsmith and Woodburne
Caudate lobe I I Caudate lobe
Left lateral superior subsegment II II Left lateral segment
Left lateral inferior subsegment III III
Left medial subsegment IV IVa, IVb Left medial segment
Right anterior inferior subsegment V V Right anterior segment
Right anterior superior subsegment VIII VIII
Right posterior inferior subsegment VI VI Right posterior segment
Right posterior superior subsegment VII VII

Source: Soyer P. Segmental anatomy of the liver: utility of a nomenclature accepted worldwide. AJR 1993;161:572; with permission.

What is the Bismuth system (Figs. 19-36, 19-37, 19-38)? In 1982, Bismuth88 combined Couinaud’s92 cadaveric and Goldsmith and Woodburne’s96 in vivo systems. Bismuth used the three vertical fissures (the homes of the three hepatic veins) and a single transverse fissure to divide the liver into seven subsegments. He counted the caudate lobe separately. Adding the caudate lobe to the seven subsegments produces eight hepatic subsegments in toto – two functional lobes (right and left) separated by the middle hepatic vein. The right has an anterior and a posterior segment separated by the right hepatic vein. The left has a medial and a lateral segment separated by the left hepatic vein.

Fig. 19-36.

Bismuth’s schematic representation of the functional anatomy of the liver: 3 main hepatic veins divide the liver into 4 sectors, each receiving a portal pedicle. Hepatic veins and portal pedicles are intertwined as the fingers of the 2 hands. (Modified from Bismuth H. Surgical anatomy of the liver. Recent Results Cancer Res 100:179-184, 1986; with permission.)

Fig. 19-37.

The functional division of the liver and the hepatic segmentation (in vivo position of the liver). (Modified from Bismuth H. Surgical anatomy of the liver. Recent Results Cancer Res 100:179-184, 1986; with permission.)

Fig. 19-38.

The obliquity of the middle and right portal fissures. Relationship to the horizontal plane (in degrees) shown in circles. (Modified from Blumgart LH, Baer HU, Czerniak A, Zimmermann A, Dennison AR. Extended left hepatectomy: technical aspects of an evolving procedure. Br J Surg 1993;80: 903; with permission.)

The transverse fissure is an imaginary line through the right and left portal branches. Note: Although readers will see horizontal lines dividing the right lobe and lateral segment of the left lobe into superior and inferior subsegments (Fig. 19-30C), illustrations in this book and other books tend not to label the “transverse fissure.” This is because there are no definite landmarks by which to place it, and because it is a morphologic rather than functional division.

The transverse fissure subdivides the segments into the following seven subsegments (Fig. 19-31):

 

Left

 

– Left lateral superior subsegment (segment II)

– Left lateral inferior subsegment (segment III)

– Left medial subsegment (segment IV)

Right

 

– Right anterior inferior subsegment (segment V)

– Right anterior superior subsegment (segment VIII)

– Right posterior inferior subsegment (segment VI)

– Right posterior superior subsegment (segment VII)

Adding the caudate lobe (segment 1), to the seven subsegments embraces all eight subsegments.

The lobes and segments are hepatic masses supplied by specific branches of bile ducts, hepatic arteries, and portal veins. In the fissures or intervals between adjacent lobes and segments lie tributaries of the hepatic veins (Fig. 19-39). These are intersegmental, and each drains portions of two adjacent segments. The hepatic veins do not follow branches of the biliary tree.

Fig. 19-39.

Diagram of the intrahepatic distribution of the hepatic veins. These veins lie between lobes and segments rather than within them. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 2. Contemp Surg 30:26-38, 1987; with permission.)

The intrahepatic arrangement of hepatic veins with respect to biliary, portal venous, and arterial branches is reminiscent of the intrapulmonic distribution of vessels. In the lungs, the pulmonary veins run between lobes; whereas the bronchi, bronchial arteries, and pulmonary arterial branches run within distinct bronchopulmonary segments.

By definition, the vertical fissures are planes that divide the liver along the pathways of the three hepatic veins. We use the term “fissure,” although Bismuth used the word “scissura.”

Right Fissure

The right fissure (Fig. 19-38) is an oblique 40° imaginary line at the anterior surface of the right functional lobe of the liver. According to Couinaud,92 it starts in the middle of the anterior border between the right angle and the right side of the gallbladder and extends to the confluence between the right hepatic vein and the inferior vena cava posteriorly.

Ton That Tung100 stated that anatomically this fissure corresponds to a line parallel to the right lateral edge of the liver, but located three finger breadths more anteriorly.

The right hepatic vein is located within the vicinity of this imaginary fissure. We have frequently observed a variably distinct notch in the inferior margin of the right lobe, a notch that coincided with the inferior extent of the right fissure.

Middle Fissure

The middle fissure (Fig. 19-38) is an oblique, 75° imaginary line at the anterior surface of the liver which connects the left side of the fossa for the gallbladder and the IVC. The middle hepatic vein is located in the vicinity of this line and, therefore, between the right and left functional hepatic lobes.

Oran and Memis101 demonstrated that in 11.1% (2 of 18) of patients, part of hepatic segment IV had a blood supply from the right hepatic artery. They concluded that there is no coincidence between the arterial watershed line between the right and left hepatic artery areas and the middle fissure of Couinaud’s segmental anatomy.

Left Fissure

The left fissure is located within the left functional lobe of the liver, in the superior aspect of the umbilical fissure, just to the left of the line of attachment of the falciform ligament (Fig. 19-29). It separates the lobe into lateral and medial segments. The left hepatic vein is located along this line. In most cases, the middle hepatic vein drains into the left hepatic vein. Occasionally it is very close to the upper part of the vein near the inferior vena cava (IVC).

Ger’s Description of the Fissures

Ger102 includes a fourth fissure in his description of the lobes and segments of the liver. Even though Ger’s concept is similar to Bismuth’s, it is so useful to the surgeon that we include it here in its entirety (Fig. 19-29).

Right Fissure

This fissure commences at the right margin of the inferior vena cava and follows the attachment of the right superior coronary ligament to about 3 to 4 cm from the junction of the latter with the right inferior layer. The fissure then curves anteriorly to a point on the inferior margin about midway between the gallbladder fossa and the right margin of the liver. Passing posteriorly, the fissure follows a line that runs parallel to the gallbladder fossa and crosses the caudate process to reach the right side of the inferior vena cava. Lying almost in the coronal plane, the fissure contains the right hepatic vein, with branches passing anteriorly to segments V and VIII and posteriorly to segments VI and VII.

Median Fissure

This fissure passes from the gallbladder fossa to the left margin of the inferior vena cava.

Posteroinferiorly, the fissure is represented by a line from the gallbladder fossa to the main bifurcation of the hepatic pedicle (portal triad) and, thence, to the retrohepatic inferior vena cava.

Left Fissure

This fissure runs from the left side of the inferior vena cava to a point between the dorsal one third and ventral two thirds of the left margin of the liver. Inferiorly, the fissure passes to the commencement of the ligamentum venosum.

Portoumbilical Fissure

This fissure is marked superficially by the attachment of the falciform ligament, which contains the ligamentum teres hepatis in its inferior border. Angled less generously than the right fissure, it meets the inferior margin of the liver at an angle of about 50°.

In a small number of instances, the relationship between the left fissure and the portoumbilical fissure may vary. In most cases the left fissure is to the right of the portoumbilical fissure. However, occasionally the left fissure is just inside the ligamentum teres and falciform ligament or just to the left of the duo.

Ger102 presented a table (Table 19-3) of resections related to the vascular and ductal structures of the liver. Blumgart et al.103 also presented a table (Table 19-4) showing anatomic classification of the five types of major resection.

Table 19-3. Relations of Resections to Vascular and Ductal Structures

Resection Line of Incision Vascular and Ductal Structures Divided Vascular and Ductal Structures Preserved
Right hepatic lobectomy (segments V, VI, VII, VIII) Gallbladder fossa to IVC Right hepatic vein; right branch of hepatic pedicle Middle and left hepatic veins; left branch hepatic pedicle
Branches entering middle hepatic vein from right; accessory veins from segments VIand VII
Extended right hepatic lobectomy (segments IV, V, VI, VII, VIII) 1 cm to right of portoumbilical fissure Right and middle hepatic veins; right branch of hepatic pedicle and branches of left hepatic pedicle to segment IV Left hepatic vein; left branch hepatic pedicle, including branches to segments II and III
Right lateral lobectomy (segments VI and VII) Right fissure Right hepatic vein, posterior division; right hepatic pedicle Middle and left hepatic veins, anterior division; right hepatic pedicle
Left hepatic lobectomy (segments II, III, IV) 1 cm to left of median fissure Left hepatic vein and tributaries entering middle hepatic vein from left; left branch hepatic pedicle Middle hepatic vein
Left lateral lobectomy (segments II and III) 1 cm to left of portoumbilical fissure Left hepatic vein before junction with the middle hepatic vein; branches of hepatic pedicle to segments II and III Middle hepatic vein; left branch of hepatic pedicle, including branches to segment IV
Mesohepatectomy/median hepatectomy (segments IV, V, VIII) 1 cm to right of portoumbilical fissure, 1 cm to left of right fissure; inferiorly obliquely to hilum, leftward to 1 cm from portoumbilical fissure, to anterior margin of liver Middle hepatic vein, branches joining left side of right hepatic vein, anterior division; right branch hepatic pedicle, left branch hepatic pedicle to segment IV, cystic duct, and artery Right and left hepatic veins, posterior division; right branch hepatic pedicle, left branch hepatic pedicle

Source: Ger R. Surgical anatomy of the liver. Surg Clin North Am 1989;69:179; with permission.

Table 19-4. Anatomical Classification of Major Hepatic Resections

Couinaud1 
 
Goldsmith and Woodburn2 
 
Right hepatectomy (segments V, VI, VII and VIII) Right hepatic lobectomy
Left hepatectomy (segments II, III and IV) Left hepatic lobectomy
Right lobectomy (segments IV, V, VI, VII and VIII; sometimes also segment I) Extended right hepatic lobectomy
Left lobectomy (segments II and III) Left lateral segmentectomy
Extended left hepatectomy (segments II, III, IV, V and VIII; sometimes also segment I) Extended left lobectomy

Right lobectomy (extended right hepatic lobectomy) has also been referred to as right trisegmentectomy and this term in commonly found in the literature. Similarly, extended left hepatectomy is referred to as left hepatic trisegmentectomy.3

References

 

1. Couinaud C. Le Foie. Etudes Anatomiques et Chirurgicales. Paris: Masson, 1957.

2. Goldsmith NA, Woodburn RT. The surgical anatomy pertaining to liver resection. Surg Gynecol Obstet 105:310-318, 1957.

3. Starzl TE, Iwatsuki S, Shaw BW, et al. Left hepatic trisegmentectomy. Surg Gynecol Obstet 55:21-27, 1982.

Source: Blumgart LH, Baer HU, Czerniak A, Zimmermann A, Dennison AR. Extended left hepatectomy: technical aspects of an evolving procedure. Br J Surg 1993;80:903; with permission.

Of the planes dividing these lobes and segments, only the one between the medial and lateral segments of the left lobe commonly marks the surface of the liver.

In retrospect, the fact that the portal vein and the hepatic ducts and arteries bifurcate and send branches of nearly equal size to the right and left might have provided a clue to the lobar structure. By overlooking the clue, we are reminded that appearances can be deceiving, and that careful analysis is always important.

Rise and Demise of Segment IX

For several years Couinaud and his colleagues, as well as several other investigators, referred to an area of the dorsal sector of the liver close to the inferior vena cava as “segment IX.” But the existence of this segment was short-lived when, in 2002, Couinaud and his associates104 published the following conclusion:

Because no separate veins, arteries, or ducts can be defined for the right paracaval portion of the posterior liver and because pedicles cross the proposed division between the right and left caudate, the concept of segment IX is abandoned.

We advise the interested reader to study the “genesis” and “death” of segment IX in articles published by none other than the “father of hepatic segmentation” – Couinaud – and several other investigators.105-108

Interlobar Anastomoses

With the true lobar anatomy of the liver established, the question of interlobar anastomoses presents itself. The accepted view was that except in the caudate lobe,109 connections between bile ducts or blood vessels of the right and left lobes are few, inconstant, and insignificant.68,96,110-112

In 1977, Mays113 challenged these views, using radiographic techniques in living human subjects. Mays was able to show that an occluded left hepatic artery fills with blood from the right side and vice versa. He also noted that, “. . .when the common hepatic artery was interrupted, inferior phrenic and pancreaticoduodenal collaterals reconstituted intrahepatic arterial blood flow. These anastomoses could not be observed in the cadaver.”

Orientation of Hepatic Lobes in Sectional Imaging

The visceral surface of the liver faces inferiorly, posteriorly, and to the left. This orientation is a composite of the two oblique planes impressed upon the liver by the midline position of the vertebral column and the deep paravertebral gutters disposed on either side of the column.

As expressed by Schneck,114 the vertebral column forms a longitudinal ridge-line within the abdominal cavity. The column’s forward portion of the lordotic lumbar curve of the column causes this ridge-line to arch anteriorly behind the liver. The posterior portions of the lower ribs cause the right and left paravertebral gutters to deepen considerably.

The right paravertebral gutter principally houses the large, rounded dextral aspect of the liver. The right kidney and right adrenal gland lie behind the right lobe on the sloping lateral aspect of the lumbar vertebrae. The left paravertebral gutter is relatively crowded with various organs, including the esophagus, body of the stomach, tail of the pancreas, spleen, left kidney, and left adrenal gland. This anteriorly displaces the left side of the liver. The pylorus, duodenum, and head and body of the pancreas are displaced forward as they approach or cross in front of the vertebral column.

The importance of the in situ obliquity of the liver’s visceral surface is best appreciated when viewing tomographic sections of the liver and attempting to identify hepatic lobes and segments in the sections. The majority of textbook and atlas illustrations of the liver’s external features and their relationships to internal hepatic segmentation are often misleading or inaccurate. The liver is not shown in its true anatomic orientation.

The falciform ligament is often shown as a midline structure passing in the midsagittal plane from the abdominal wall to the anterior surface of the liver. Likewise, the long axis of the H-shaped features of the porta hepatis is shown as parallel with the midsagittal plane of the body (Fig. 19-13). In fact, the left side of the liver is displaced both anteriorly and to the right by the vertebral column and viscera. This causes the falciform ligament, ligamentum teres, and portal indentation to shift markedly toward the right in most individuals. In cross-sectional imaging, the fissure for the ligamentum teres lies at the right midclavicular line in many cases. The fissure for the ligamentum venosum and the lesser omentum lies roughly parallel with a coronal plane of the abdomen.

In cadaveric sections or computer-generated images, intrahepatic fissures can be used to approximate the margins of the intrahepatic lobes and their primary segments.115 This process can be facilitated by observing other features, such as the hepatic veins (disposed roughly intersegmentally), ligaments, inferior vena cava, and gallbladder (Figs. 19-40, 19-41).

Fig. 19-40.

Semischematic drawings of transverse sections of a liver and adjacent structures as often seen in cross-sectional imaging showing in situ relations of liver segments. Sections A-B proceed from superior to inferior, as indicated by vertebral levels. The dotted line in D approximates the line of separation between the anterior and posterior segments of the right lobe. Ao, aorta; C, caudate lobe; CP, caudate process; GB, gallbladder; IVC, inferior vena cava; LL, left lateral segment; LM, left medial segment; Q, quadrate lobe; RA, right anterior segment; RK, right kidney; RP, right posterior segment. (From Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 2. Contemp Surg 30:26-38, 1987; with permission.)

Fig. 19-41.

Semischematic drawings of sagittal sections of a liver depicting relations of liver segments. A, Midsagittal section passing through liver and aorta. B, C, Sagittal sections through inferior vena cava. D, Sagittal section through the right side of the liver and the gallbladder. Abbreviations as in Fig. 19-40; M, medial. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 2. Contemp Surg 30:26-38, 1987; with permission.)

In upper abdominal transverse sections, the fissure for the ligamentum venosum departs obliquely from the left intersegmental fissure (left fissure) toward a coronal plane with the lesser omentum in front of the caudate lobe (Fig. 19-40A-C). The caudate lobe separates the left lobe anteriorly and the left lobe from the right lobe posteriorly and to the right.

To approximate the interlobar (median) fissure between the right and left lobes draw a line between the left margin of the bed of the gallbladder and the sulcus for the IVC. The superior recess of the bed of the gallbladder can often be seen above the gallbladder as a space containing fat, the portal vein, and small vessels (Fig. 19-40C). The right lobe is situated posterior to and to the right of the line. The medial lobe lies anteriorly and to the left. In the intermediate level sections, the porta hepatis and caudate process separate the left and right lobes.

The intersegmental fissure (right fissure) between the right anterior and right posterior segments can be roughly defined by one of two methods. Either place a line over the right hepatic vein running between the two segments or construct a line midway between the anterior and posterior branches of the right portal vein (Fig. 19-40D, E). The surface marking of this plane may correspond to the line of the 7th or 8th rib.

The left intersegmental fissure (left fissure) between the medial and lateral segments of the left lobe is usually readily visible in lower transverse sections through the liver (Fig. 19-40D). This fissure contains the ligamentum teres and some fat. It may vary in orientation from parallel with the midsagittal abdominal plane to 45° or greater to the right of that plane.

In sagittal sections through the middle of the liver, such as images computer-reconstructed from transverse sections, observe the lateral segment of the left lobe anterior and to the left of the quadrate lobe (Fig. 19-41). The lateral segment is also anterior to the caudate lobe in such sections. From a study of sagittal images, one readily understands how intermediate level transverse sections can pass through the quadrate and caudate lobes at the same level. Sagittal sections through the bed of the gallbladder often reveal the quadrate lobe’s location anterior to the right lobe. See the transverse section shown in Fig. 19-40C.

Sagittal sections through the right side of the liver reveal the roughly coronal plane assumed by the right hepatic vein as it passes inferiorly between the anterior and posterior segments of the right lobe (Fig. 19-41D).

Bismuth and Garden116 state that Anglo-Saxon terminology such as lobectomy, segmentectomy, etc., is anatomically wrong. Perhaps so, but we have used this terminology anyway, because of its general acceptance and usage in the medical literature.

Intrahepatic Architecture

The hepatic arteries branch repeatedly to form interlobular arteries in the hepatic triads, with branches to the structures of the triad and to the sinusoids at varying distances between the periphery and the central vein. The portal vein similarly branches to form interlobular veins that open into the sinusoids.

The sinusoids receive both venous (75 percent) and arterial (25 percent) blood. In the center of the lobule, the radially arranged sinusoids open into a central vein. The central vein emerges at the end of the lobule to become a sublobular tributary of a hepatic vein. The hepatic veins empty into the inferior vena cava.

Hepatocytes

Hepatocytes (Fig. 19-42) range in diameter from 20 to 30 micrometers and have a life span of about five months. Liver cells are seen to lie in plates such that between adjacent cells are the bile canaliculi into which project some microvilli. Paralleling the plates of liver cells are the hepatic sinusoids, the walls of which are composed of endothelial cells and stellate sinusoidal macrophages (Kuppfer cells). The endothelial cells are generously fenestrated, and there are numerous, large gaps between adjacent cells of the sinusoidal walls. Between the sinusoids and the basal sides of the plates of hepatic cells is the perisinusoidal space (of Disse). Microvilli of the hepatocytes project into this space.

Fig. 19-42.

Diagram of a liver cell (hepatocyte) and its relation to an adjacent cell (right) and to liver sinusoids. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

Due to the large gaps between adjacent sinusoidal cells and the absence of a continuous basal lamina, no significant barrier exists between the blood plasma in the sinusoids and the hepatocyte membrane. Proteins and lipoproteins synthesized by the hepatocytes are transferred into the blood in the perisinusoidal space. This is the pathway for the endocrine secretions of the liver. In the perisinusoidal space is a cell type called the lipocyte or adipose cell (also known as Ito cell) which serves as a storage site for vitamin A. When depleted of lipid, these cells resemble fibroblasts and secrete collagen type III (reticular fibers) which forms a stroma. An increase in the latter fibers may be an early sign of hepatic response to toxins and can lead to fibrosis. Two to four other surfaces of the hepatocytes are in contact with adjacent liver cells of the plates.

Bile Secretion

Between the adjacent hepatocytes is a tubular space, the bile canaliculus or bile capillary (Fig. 19-42). The space contains a few short microvilli from the bordering hepatocytes. On either side of the canaliculus, the hepatocytes are held together by gap junctions and desmosomes.

Bile is secreted into the canaliculi and carried from the center of the lobule to the periphery; thus it flows in a direction counter to that of the incoming blood of the liver. At the periphery of the lobule, the canaliculi continue as the ductules of Hering, small channels bordered in part proximally by hepatocytes and much smaller cuboidal cells. From there on, the hepatocytes of the ductules are replaced entirely by cuboidal cells in the terminal biliary vessels. These slender channels drain into the bile ducts of the portal triad, which form the tributaries of the intrahepatic biliary tract.

Vascular Distribution

Two blood vessels, the hepatic artery and the portal vein, supply the liver. About one-fourth of the blood and one-half the oxygen come by way of the hepatic artery. The remainder is carried by the portal vein.117 Blood from these two sources mingles in the blood sinusoids of the liver parenchyma and is drained by tributaries of the hepatic veins. These veins open into the inferior vena cava.

The hepatic artery, portal vein, and intrahepatic bile ducts are arranged in a lobar pattern with dichotomous branching into segment vessels that, in turn, divide into area vessels. Because of their similar distribution, the terminology of the three systems is much the same. The general pattern applicable to all three is shown in Fig. 19-43. The branching of the left portal vein differs somewhat from this pattern. The hepatic veins, which drain the liver, in contrast, follow an interlobar pattern of distribution (Fig. 19-39).

Fig. 19-43.

Terminology of the branches of the hepatic artery, portal vein, and tributaries of the bile ducts, which all branch similarly (in most cases). (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

Ohkubo118 described dissection findings of an absent right gastric vein with an aberrant left gastric vein which directly drained into the liver. He considered the aberrant left gastric vein an important portal collateral pathway, corresponding to the phylogenetic and ontogenetic “left portal vein.”

Hepatic Vasculature

(Fig. 19-44) The fundamental studies of the intrahepatic pattern of the hepatic artery are those of Healey and colleagues,110 Couinaud,92 Michels,111 and Suzuki and colleagues.119

Fig. 19-44.

Diagram to show the intrahepatic distribution of the hepatic artery. Note the “returning loop” of the left branch at the junction of medial and lateral segments. It is liable to injury here during left lateral segmentectomy. (Modified from Dawson JL. Anatomy. In: Wright R, Alberti AGMM, Karran S, Millward-Sadler GH (eds). Liver and Biliary Diseases. Philadelphia: Saunders, 1979; with permission.)

Proper Hepatic Artery

In the usual pattern, the common hepatic artery arises from the celiac trunk. After giving origin to the gastroduodenal artery, the hepatic artery continues as the proper hepatic artery in the hepatoduodenal ligament. In this ligament, the proper hepatic artery lies to the left of the common bile and hepatic ducts and anterior to the portal vein. It divides into right and left hepatic (lobar) arteries before it enters the porta.

Right Hepatic Artery

The right hepatic (lobar) artery passes to the right, usually posterior to the hepatic duct but occasionally anterior to it. The cystic artery generally arises from the right hepatic in the hepatocystic triangle located between the cystic duct and the common hepatic duct.

The right hepatic artery bifurcates to form the anterior and posterior segment arteries. This division may take place within the liver or extrahepatically in the porta. The segment arteries divide, in turn, into superior and inferior area arteries that run with and are, generally, inferior to the bile ducts serving the same area.120

The anterior segmental branch of the right hepatic artery is more tortuous than the posterior segmental branch. After passing downward toward the neck of the gallbladder, it turns abruptly upward to accompany the bile duct of the anterior segment. In the downward part of its course near the gallbladder fossa, the anterior segment branch can be vulnerable to injury during operative procedures on the gallbladder.120

Left Hepatic Artery

The left hepatic artery is shorter than the right because the right and left hepatic arteries arise to the left of the interlobar (median) fissure. In about 40 percent of Healey’s subjects,121 the left hepatic artery ended at its bifurcation into medial and lateral segmental arteries (Fig. 19-45, Fig. 19-46A). In 35 percent, however, the lateral segmental artery divided into laterosuperior and lateroinferior branches to the right of the intersegmental fissure (right fissure). In these the medial segmental artery arose from the lateroinferior branch (Fig. 19-46B). In addition, in 25 percent of subjects, the medial and lateral segmental arteries arose separately from the proper hepatic artery so that there was no true left hepatic artery. In such cases, the left medial segmental artery arose from the right hepatic artery, crossing the midline to reach the left medial lobe (Fig. 19-46C). A similar configuration on the right was less common.

Fig. 19-45.

Hepatic arteries. A. Usual pattern of segmental hepatic arteries. B. Anomalous origin of the left medial segmental artery from the right hepatic artery, crossing the midline to reach the medial segment of the left lobe. This may be encountered in 25 percent of individuals. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Fig. 19-46.

A, B, C. Variations in the branching of the left hepatic artery. In C, the left medial branch arises from the right hepatic artery, crossing the interlobar (median) fissure to do so. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

The medial segmental artery passes into the substance of the quadrate lobe. In 70 percent of specimens, it divided into two superior and two inferior area arteries. In 30 percent, various combinations occurred in which two or more area arteries arose from a common trunk. The other area arteries arose separately from the medial segmental artery.

Lateral Segmental Artery

The lateral segmental artery usually divides into its superior and inferior branches along the line of the left intersegmental fissure or, variably, to the right of the fissure. The arterial branches run with the bile ducts serving these areas and may course either just above or below them.

Caudate Lobe Arteries

The configuration of arteries to the caudate lobe of the liver varies. Typically, one artery arises from the right hepatic artery and supplies the caudate process and right side of the caudate lobe. A similar vessel from the left hepatic artery supplies the left side of the lobe. The arteries may number one (23 percent), two (45 percent), three (30 percent), or four (two percent), as reported by Healey et al.110 The caudate lobe is supplied entirely by the right hepatic artery in 35 percent of cases and by the left hepatic artery in 12 percent.120

Arterial Supply

Branches of the hepatic arteries have long been considered to be end arteries. Small and inconstant anastomoses between arterial branches outside the liver parenchyma have been reported.110 The most important anastomoses are in the connective tissue of the capsule and its intrahepatic reflections.

More than ninety years ago, von Haberer122 showed that ligation of the common hepatic artery proximal to the gastroduodenal artery produced no liver changes. Ligation distal to the gastroduodenal artery usually, but not always, resulted in liver necrosis.123

Distal ligation of a lobar artery beyond the branches to the subcapsular plexus always results in lobar ischemia and necrosis. Graham and Cannell124 concluded that the more distal the ligation of the artery, the greater the probability of liver necrosis. Bengmark and Rosengren125 and Mays and colleagues113,126,127 disputed the concept that hepatic arteries are end arteries in humans. They agreed that anastomoses cannot be seen in arteriograms of normal living individuals or in injection preparations of cadavers, but that such anastomoses arise de novo in the presence of hepatic artery ligation. Such collaterals between segmental arteries within the liver may appear 10 hours to 15 hours after ligation.

Survival of a liver segment following arterial ligation is the result of all the following:

 

Increased extraction of oxygen from portal venous blood128

Extrahepatic collateral circulation

Intrahepatic collateral circulation formed in response to the ligation

Mays113 reported that the hepatic necrosis seen in experimental animals after arterial ligation is due to species differences and that animal models do not behave in the same manner as human beings.

Intrahepatic Portal Venous Network

The portal vein divides into left and right lobar branches at the porta before entering the liver. The portal lobar veins lie posterior to the hepatic arteries and the bile ducts. This relationship to the arteries and ducts is preserved in the intrahepatic distribution of the vessels.

Right Portal Vein

The branches of the right portal vein (Fig. 19-47) follow the pattern of distribution of the right hepatic duct and right hepatic artery. The right portal vein is short and typically divides into anterior and posterior segmental vessels. Each of these subdivides into superior and inferior subsegmental branches. The right portal vein sends a small branch to the caudate process and the right side of the caudate lobe. The right portal system is more variable than the left.

Fig. 19-47.

Intrahepatic distribution of the hepatic portal vein. The pars umbilicus (U) is the site of the embryonic ductus venosus. T, pars transversus; P, posterior segment; A, anterior segment. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

Left Portal Vein

The left portal vein (Fig. 19-47) is longer than the right. It begins in the hepatic portal as the pars transversa and courses to the left. It turns inferiorly in the liver’s left lateral fissure at the umbilical fossa and is the markedly dilated pars umbilicus. As the vein enters the left lobe it is joined by the paraumbilical veins (of Sappey) and the ligamentum teres hepati, the nearly obliterated and functionless remnants of the left umbilical vein. The left hepatic vein goes on to be connected to the inferior vena cava by the ligamentum venosum, a vestige of the ductus venosus. The small extrahepatic section of the left branch, from which veins to the quadrate and left lobes arise, is a persistent part of the left umbilical vein.

The distribution of the left portal vein differs from the typical branching pattern of the left hepatic artery and bile duct in the following ways.68

 

The superior and inferior subsegmental veins of the lateral segment arise from the left side of the pars umbilicus of the left portal vein.

The medial segmental veins arise from the right side of the pars umbilicus of the left portal vein. Usually, one common mediosuperior and medioinferior trunk arises from the umbilical portion.

In the majority of cases, the left portal vein provides one branch to the left side of the caudate (segment I) lobe. This branch arises from the pars transversus.

Remember

 

The right portal vein divides into two parts: anterior and posterior. The anterior branch of the right portal vein further subdivides into ascending (for segment VIII) and descending (for segment V). The posterior branch also divides into ascending (for segment VII) and descending (for segment VI).

The left portal vein also displays a unique subdivision. Two branches from its lateral side supply segments II and III. The vein, however, continues to supply segment IV.

Hepatic Veins

The hepatic veins lie in the planes that divide the lobes and segments of the liver. Thus, they are intersegmental (Fig. 19-39) and drain parts of adjacent segments. This is in contrast to the hepatic arteries, portal veins, and tributaries of the bile ducts (Fig. 19-43) which define these areas of the liver.

Surgical implications of this arrangement are that in a right lobectomy the line of resection should be placed just to the right of the interlobar plane; in a left lobectomy, it should be just to the left.

The hepatic veins arise as central veins of the liver lobules. They coalesce to form interlobular veins, several orders of collecting veins, and right, middle, and left hepatic veins that emerge from the liver to enter the inferior vena cava.

Right Hepatic Vein

The right hepatic vein lies in the right fissure and drains the:

 

Superior and inferior areas of the right posterior segment

Superior area of the anterior segment

Middle Hepatic Vein

The middle hepatic vein lies in the median fissure and drains the:

 

Anteroinferior area of the right lobe

Medial inferior area of the left lobe

Left Hepatic Vein

The left hepatic vein lies in the upper part of the left fissure and drains the:

 

Left lateral segment

Superior area of the medial segment

A variable number of small veins entering the vena cava directly drain the:

 

Caudate lobe

Posterior segment of the right lobe (inconstant)

Remember

 

The right hepatic vein drains segments V, VI, VII, and partially drains segment VIII.

The middle hepatic vein drains segments IV, V, and VIII.

The left hepatic vein drains segments II and III and partially drains segment IV.

The multiple accessory hepatic veins drain mostly into the right hepatic vein. These are short and variable, and must be carefully ligated.

Nakamura and Tsuzuki129 reported the anatomy of the common trunk of the middle and left hepatic veins. Figure 19-48 represents their findings.

Fig. 19-48.

Various patterns of ramifications of the middle and left hepatic vein. A, Type I, 9 (10.8 percent), has no ramification within less than 1 cm from the inferior vena cava. B, Type II, 35 (42.2 percent), has two ramifications within 1 cm from the inferior vena cava. a, Type IIa, 22 (26.5 percent), has the middle and left hepatic vein. b, Type IIb, 6 (7.2 percent), has a right anterosuperior vein. c, Type IIc, 5 (6 percent), has a left superior vein. d, Type IId, 1 (1.2 percent), has an independent left superior vein and the common trunk. e, Type IIe, 1 (1.2 percent), has an independent right anterosuperior vein and the common trunk. C, Type III, 22 (26.5 percent), has a trifurcation within 1 cm from the inferior vena cava. a, Type IIIa, 5 (6 percent), has a trifurcation consisting of the right anterosuperior, middle, and left hepatic veins. b, Type IIIb, 8 (9.6 percent), has a trifurcation consisting of the middle, left, and left superior veins. c, Type IIIc, 4 (4.8 percent), has a trifurcation consisting of the middle, left medial, and left hepatic veins. d, Type IIId, 3 (3.6 percent), has an independent left superior vein and the common trunk of the middle and left hepatic veins. e, Type IIIe, 2 (2.4 percent), has a trifurcation consisting of the right anterosuperior, common trunk of the middle and left hepatic veins, and the left superior vein. D, Type IV, 4 (4.8 percent), has a quadrifurcation within 1 cm from the inferior vena cava. a, Type IVa, 2 (2.4 percent), has a quadrifurcation consisting of the right anterosuperior, middle, left medial, and left hepatic veins. b, Type IVb, 1 (1.2 percent), has an independent right anterosuperior vein and a trifurcation consisting of the middle, left, and left superior veins. c, Type IVc, 1 (1.2 percent), has a quadrifurcation consisting of the right anterosuperior, middle, and left superior veins. E, Type V, 13 (15.7 percent), has the independent middle and left hepatic veins. a, Type Va, 6 (7.2 percent), has the independent middle and left hepatic vein without ramification. b, Type Vb, 3 (3.6 percent), has the middle and left hepatic veins with left superior vein. c, Type Vc, 2 (2.4 percent), has the middle hepatic vein with right anterosuperior vein and the left hepatic vein with left medial vein. d, Type Vd, 1 (1.2 percent), has the middle hepatic vein with right anterosuperior and left medial veins and the left hepatic vein. e, Type Ve, 1 (1.2 percent), has the middle hepatic vein with right anterosuperior and the left hepatic veins. (Modified from Nakamura S, Tsuzuki T. Surgical anatomy of the hepatic veins and the inferior vena cava. Surg Gynecol Obstet 152:43-50, 1981; with permission.)

In more than half of subjects, the left and middle hepatic veins join and enter the vena cava as a single vein less than 1 cm below the diaphragm. Nakamura and Tsuzuki129 found, in addition to the three major veins, up to 50 small dorsal hepatic veins entering the vena cava. Only about 14 of the veins were of significant size. For evaluation, these authors assumed that 1 cm of vein, free from tributaries, would be adequate for successful ligation. By their standard, the right hepatic vein could be ligated in 51 of 83 cadavers examined (61.4 percent). The left vein could be ligated in only nine specimens (10.8 percent). The hepatic veins could be exposed by dividing the triangular and coronary ligaments and retracting the right lobe downward and to the left and the left lobe downward and to the right.

The intrahepatic venous network, formed by the incoming portal blood and outgoing hepatic blood, is intimately related to the liver cell. Ger102 stated that a perivascular fibrous sheath envelops the portal network within the liver, a network consisting of branches of the portal vein, hepatic artery, and bile duct. No such fibrous sheath surrounds the hepatic veins and their tributaries; indeed, one can differentiate the hepatic vein tributaries from the other vessels in the liver by magnetic resonance imaging, due to the difference in contrast attributable to the presence or absence of the fibrous sheath. The hepatic veins receive blood directly from the liver sinusoids by way of central veins of the liver lobules, carrying both portal venous blood and hepatic arterial flow. The sinusoids lie immediately adjacent to the hepatic cells. The absence of a protective fibrous investment leaves the hepatic veins unprotected and prone to bleeding in hepatic trauma.

Intrahepatic Biliary System

The bile canaliculi join to form ductules (canals of Hering) which are lined with cuboidal epithelial cells. These are not hepatocytes and have a complete basal lamina. The ductules open into interlobular bile ducts which form part of the portal triads. The interlobular ducts join to form right and left lobar ducts which join at the hilum to form the extrahepatic common hepatic duct (Fig. 19-49).

Fig. 19-49.

Intrahepatic distribution of the bile ducts. (From Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

Right Biliary Tree

The right biliary tree (Fig. 19-50) originates in the four areas of the right lobe. The branches take their names from their locations: anterosuperior, anteroinferior, posterosuperior, and posteroinferior. These area ducts join to form anterior and posterior segment ducts that, in turn, form the right hepatic duct. Some variations occur in the biliary vessels of the right lobe.

Fig. 19-50.

Variations of the tributaries of the right hepatic duct. A, Usual pattern in which the right hepatic duct receives the anterior and posterior segment ducts. B, Alternate pattern in which the posteroinferior area duct enters the common hepatic duct. C, Anterior and posterior segment ducts enter the left hepatic duct; the right hepatic duct is absent. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

Left Biliary Tree

(Fig. 19-51) The left hepatic duct usually forms by the confluence of the ducts of the medial and lateral segments. Healey and Schroy68 describe 14 possible arrangements of the left medial segment ducts of which nine were actually present among their 100 specimens.

Fig. 19-51.

Variations of the left hepatic duct. A, Usual pattern in which the left hepatic duct is formed by the confluence of the medial and lateral segment ducts. B, The medial segment duct may enter the lateroinferior duct. The medial segment duct is usually doubled. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

The laterosuperior biliary duct may extend upward into the left triangular ligament, as Healey and Schroy68 noted. The frequency of occurrence of aberrant biliary and blood vessels in the proximal one-third of the ligament may exceed 80 percent in human livers, according to data of Gao and Roberts.69 They further observed that 60 percent of the specimens they studied contained rudimentary liver cords, perhaps retained after developmental regression of the left lobe. Biliary leakage and bleeding may occur subsequent to surgical division of the left triangular ligament if adequate preventive precautions are not taken.

Caudate Lobe

The tributaries of the right and left hepatic ducts drain the caudate lobe. A separate duct serves the caudate process, draining into the right hepatic duct.

Variations of hepatic duct confluence and of the intrahepatic ductal system are shown in Figs. 19-52, 19-53.

Fig. 19-52.

Main variations of the hepatic duct confluence (Couinaud 1957185). A, Typical anatomy of the confluence. B, Triple confluence. C, Ectopic drainage of a right sectoral duct into the common hepatic duct: C1, right anterior duct draining into the common hepatic duct; C2, right posterior ducts draining into the common hepatic duct. D, Ectopic drainage of a right sectoral duct into the left hepatic ductal system: D1, right posterior sectoral duct draining into the left hepatic ductal system; D2, right anterior sectoral duct draining into the left hepatic ductal system. E, Absence of the hepatic duct confluence. F, Absence of right hepatic duct and ectropic drainage of the right posterior duct into the cystic duct. ra, right anterior; rp, right posterior; lh, left hepatic. (Modified from Smadja C, Blumgart LH. The biliary tract and the anatomy of biliary exposure. In: Blumgart LH (ed). Surgery of the Liver and Biliary Tract. New York, Churchill Livingstone, 1988, pp. 11-22; with permission.)

Fig. 19-53.

A sketch to show the main variations of the intrahepatic ductal system (Healey and Schroy 195368). A, Variations of segment V. B, Variations of segment VI. C, Variations of segment VIII. D, Variations of segment IV. Note that there is no variation of drainage of segments II, III and VII. (Modified from Smadja C, Blumgart LH. The biliary tract and the anatomy of biliary exposure. In: Blumgart LH (ed). Surgery of the Liver and Biliary Tract. New York, Churchill Livingstone, 1988, pp. 11-22; with permission.)

Remember

 

The right hepatic duct drains segments V, VI, VII and VIII.

The left hepatic duct drains segments II, III, IV.

The caudate lobe (segment I) drains to both right and left hepatic ducts.

Meyers et al.130 reported that low insertion of hepatic segmental duct VII-VIII is an important cause of major biliary injury or misdiagnosis. They emphasized that knowledge of the topographic anatomy is paramount in avoiding such injury or misdiagnosis.

IVC and Liver

The anatomic entities related to the IVC, from cranial to caudal, are:

 

1. Epiploic foramen: IVC forms its posterior boundary

2. Groove between right and caudate lobes: This occasionally becomes intrahepatic tunnel

3. Right diaphragmatic crus posterior to the IVC

4. Right adrenal gland and right adrenal vein posterior to the IVC

5. Central tendon

6. Right atrium of the heart

The IVC may be exposed after mobilizing the right lobe of the liver, careful suture ligation of the right adrenal vein, and several other small named and unnamed veins.

According to Sing and colleagues,131 measurement of vena caval diameter and anatomy may be performed bedside in critically ill patients using carbon dioxide as a contrast agent.

Ger102 enriched the surgical profession with a classic presentation of the relations of resections to vascular and ductal structures (see Table 19-3). This table illustrates our surgical considerations.

Surgical Considerations

 

Hepatic arteries are not end arteries. In humans, intrahepatic, translobar, and subcapsular collateral circulation develops within 24 hours after ligation of the right or left hepatic artery.

The subcostal, right inferior phrenic, and pancreaticoduodenal arteries provide collateral intrahepatic circulation after ligation of the common hepatic artery in humans. In rare cases, ligation of the right or left artery may be necessary for control of arterial hemorrhage. More often, the Pringle maneuver or total vascular isolation of the porta hepatis and suprahepatic and infrahepatic vena cavae allows for direct repair of vascular injuries or resection, if necessary.

The portal vein may be ligated in human beings, but repair is preferred because the mortality rate with ligation is much higher.

When it is necessary for the portal vein to be excised in extended liver surgery, Lorf et al.132 have used the excised hepatic vein to reconstruct the portal vein.

Temporary occlusion of the total afferent blood supply (hepatic artery and portal vein) may be tolerated in humans for 30 to 45 minutes routinely and for periods up to 60 minutes if the body is cooled and no concurrent liver disease is present. Wang et al.133 reported that the safest method of hepatic vascular clamping is 60 minutes of intermittent ischemia consisting of 6 cycles of 10 minutes interrupted by 5 minutes of reperfusion. Vascular occlusion in a cirrhotic liver is fraught with danger. Man et al.134 concluded that the safe and effective upper limit of tolerance of the liver to intermittent Pringle maneuver is 120 minutes.

Nakamura et al.135 removed the right and middle hepatic veins during total resection of segments VII and VIII, and partial resection of segments V and VI including the caudate lobe, and reported successful direct hepatic vein anastomosis (Fig. 19-54).

Grazi et al.136 reported that total vascular exclusion to control blood inflow to the liver during hepatic surgery must have a limited role, but it can be useful in cases of liver trauma.

Malassagne et al.137 recommended selective vascular clamping for major hepatectomies in selected patients with peripheral hepatic tumors.

Evans et al.138 stated that total vascular exclusion is a safe hemodynamic procedure for liver resection, even in patients older than 70 years, as long as clamp times do not exceed 45 minutes.

Segmental hepatic vein ligation may be done without hepatic resection.

Ligation of both branches of the hepatic artery and portal vein may be performed in liver trauma in extremely rare cases. Ligate the artery first. If good results are not obtained, then ligate the branch of the portal vein to that lobe. A significant percentage of hepatic necrosis will ensue, but the patient is likely to survive.

Ligation of an extrahepatic duct produces atrophy of the corresponding lobe and will likely be complicated by cholangitis until the atrophy is complete. Repair is preferred.

Remember that approximately 10 percent of human beings have some type of anomaly of the biliary tract.

Due to unknown factors, the liver regenerates within four to six months.

Ten to twenty percent of normal liver tissue is sufficient to maintain life.

To prevent stricture formation, do not devascularize the anterior surface of the CBD.

Fig. 19-54.

Diagrams showing the procedure from isolation of the hepatic veins to completion of direct anastomosis. A, Skeletonization of the right hepatic vein. B, Sites for cutting the right hepatic vein are shown by arrows. C, Completion of direct anastomosis. (Modified from Nakamura S, Suzuki S, Hachiya T, Ochiai H, Konno H, Baba S. Direct hepatic vein anastomosis during hepatectomy for colorectal liver metastases. Am J Surg 174(3):331-333, 1997; with permission.)

Lymphatics of the Liver

The liver sinusoids (Fig. 19-42) have an endothelial lining composed of flattened squamous cells and stellate macrophages (Kupffer cells). This endothelial layer is separated from the surrounding hepatocytes by a narrow perivascular space (of Disse) partially filled by microvilli of the hepatocytes.

The openings in this endothelial lining of sinusoids in humans allow the passage of blood plasma and chylomicrons. Cellular elements cannot pass. These openings are usually considered discontinuities of the endothelium. Others139 believe they are fenestrae in the endothelial cells. There are no closing membranes in the fenestrae and no basal lamina in human sinusoids.

The perivascular space of Disse (Fig. 19-42) is the source of lymph produced by the liver. The flow is toward the portal triads at the periphery of the lobule. Here the lymph is collected in the slightly larger space of Mall around the vessels of the triad.

The spaces of Disse and Mall are tissue spaces, not lymphatic vessels. The true endothelium-lined lymphatic vessels originate in the connective tissue around the portal triad. They presumably end blindly in the space of Mall because retrograde injections of lymphatic vessels do not pass from the lymphatics to the spaces.

The lymphatics of the liver are usually divided into superficial or subcapsular and deep or portal systems. Hardy and associates140 wrote that the hepatic lymphatics form a single functional unit.

Superficial Lymphatics

The superficial lymphatics (Fig. 19-55) lie near the surface of the liver beneath the serosa and within Glisson’s capsule. Five pathways were described by Rouviere,141 with later modifications.

Fig. 19-55.

Superficial lymphatic drainage of the liver. About one-half of the drainage is to the thoracic duct. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

These five pathways extend from the:

 

Anterior and right superior surfaces of the liver through the sternocostal foramen (of Morgagni) to anterior phrenic nodes

Posterior and superior surfaces through the caval hiatus to middle (lateral) phrenic nodes

Posterior surface of the left lateral segment to the paracardial group of left gastric nodes

Posterior surface of the right lobe to celiac nodes by way of nodes of the inferior phrenic artery

Entire anterior margin of the liver and the entire visceral surface to hepatic nodes

A summary of connections of the phrenic nodes is provided in Table 19-5.

Table 19-5. The Phrenic Lymph Nodes

  Anterior Group Middle Group Posterior Group
Number 2-3 2-3 2-3
Location Behind, on either side of the xiphoid With the right phrenic nerve Crura of the diaphragm
Drainage from (afferent) Convex surface of liver, diaphragm and anterior abdominal wall Middle of diaphragm, right portion of convex surface of liver, deep lymphatics of the region of the hepatic vein Posterior part of diaphragm, lymphatic from middle phrenic group
Drainage to (efferent) Sternal nodes Posterior phrenic nodes Lumbar nodes, posterior mediastinal nodes, celiac nodes

Source: Colborn GL, Skandalakis LJ, Gray SW, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.

Deep Lymphatics

The deep lymphatics (Fig. 19-56) carry the greater part of the lymphatic outflow and drain to:

 

Middle (lateral) phrenic nodes of the diaphragm, following tributaries of the hepatic veins to the vena cava and ascending through the caval hiatus

Nodes of the porta hepatis following portal vein branches.

Fig. 19-56.

Deep lymphatic drainage of the liver. The superficial and deep lymphatics anastomose freely. (Modified from Skandalakis LJ, Gray SW, Colborn GL, Skandalakis JE. Surgical anatomy of the liver and associated extrahepatic structures: Part 3. Contemp Surg 30:15-23, 1987; with permission.)

There is free communication between the superficial and deep lymphatic systems.

Fahim and associates142 state that the lymphatic drainage of the right lobe, gallbladder, and extrahepatic biliary system pass through pericholedochal nodes. These include the hiatal (epiploic) and superior pancreatoduodenal nodes. The lymph from the left lobe flows to nodes along the hepatic artery.

Therefore, the transdiaphragmatic hepatic drainage reaches the internal mammary and diaphragmatic lymph nodes. Lymph reaches the right lymphatic duct, partly via the tracheobronchial lymph nodes.54

Nerve Supply to the Liver

The liver and biliary ducts receive sympathetic and parasympathetic fibers from the anterior hepatic plexus around the hepatic artery and the posterior hepatic plexus around the portal vein (Fig. 19-57).

Fig. 19-57.

The distribution of vagus nerve fibers in the thorax and upper abdomen. The hepatic division of the anterior vagus trunk contains parasympathetic and sensory fibers to the liver. The intrahepatic course of these is not well known. (Modified from Skandalakis LJ, Colborn GL, Gray SW, Skandalakis JE. Surgical anatomy of the liver and extrahepatic biliary tract. In: Nyhus LM, Baker RJ, eds. Mastery of Surgery, 2nd Ed. Boston: Little, Brown, 1992; with permission.)

The sympathetic fibers arise from thoracic spinal cord segments 7 to 10. The parasympathetic efferent fibers arise from the hepatic division of the anterior and posterior vagal trunks. Some fibers appear to arise from the right phrenic nerve143 and others may enter the liver by following the hepatic veins.144 The phrenic nerve supply via its C3, 4, 5 roots is probably the basis of shoulder pain in biliary colic.145

The most obvious of the hepatic nerves is the hepatic division of the anterior vagal trunk (Fig. 19-58). The nerve structure may be single or multiple as it passes through the lesser omentum.146 After passing through the hepatogastric ligament near the fissure for the ligamentum venosum, this division branches extensively with the biliary vessels.

Fig. 19-58.

Transition from bile canaliculi of the liver cords to bile ducts of the hepatic triads. (Modified from Junqueira LC, Carneiro J, Kelley RO. Basic Histology, 9th Ed. Stamford, Conn: Appleton & Lange, 1998; with permission.)

Galen saw the hepatic division of the anterior vagal trunk and speculated about the need for a nerve to the liver, an organ that has neither movement nor sensation.147 We are only a little better informed today. Section of this nerve produces ill-defined and often contradictory effects.

The hepatic branch of the posterior vagal trunk passes, in part, through the celiac plexus. Its branches then accompany the hepatic artery to the liver. Hess and Tamm145 report that the right vagus nerve (posterior trunk) provides the principal source of parasympathetic fibers to the biliary passages, including the sphincter of Oddi.

According to Jungermann148 and Friedman,149 the intrahepatic autonomic nerves regulate blood flow and liver metabolism. Afferent nerves connect chemoreceptors, osmoreceptors, and baroreceptors. These nerves have vasomotor regulation and play a role in controlling metabolic hepatic function.150,151

Sutherland152 studied the intrinsic innervation of the liver. He reported that peritoneal folds associated with the liver are the pathways that myelinated and non-myelinated fibers use to reach the liver.

Meguid et al.153 state that a liver that had not been denervated might inhibit the release of dopamine in the lateral hypothalmus, and this might play an inhibitory role in the regulation of food intake.

Within the liver, perivascular nerve fibers terminate on smooth muscle fibers in the media of arterioles and venules. There is little doubt that adrenergic fibers produce vasomotor responses, but there is some question whether hepatic parenchymal cells receive nerve fibers. Nobin, Moghimzedeh, and their colleagues154,155 found innervated hepatic cells in humans and other primates but not in mice or rats. Kyosola and associates156 could not confirm the presence of nerve fibers distributed to hepatocytes in human livers.

Sawchenko and Friedman157 reviewed the evidence for the direct innervation of intralobular hepatic cells. They concluded that “. . .modern light microscopic studies do provide ample evidence of fibers circumscribing, and probably terminating upon, hepatocytes.”

Amenta et al.158 found cholinergic fibers associated with extrahepatic and intrahepatic hepatic arteries, portal veins, and hepatic veins. They found a few cholinergic fibers innervating the parenchyma and sinusoids of the liver in humans. Fibers have been reported travelling through the perivascular spaces of Disse, ending on hepatocytes and even on Kupffer cells,159 and fat storage cells.160 The existence of an intrinsic nerve plexus corresponding to that of the gastrointestinal wall was suggested by Burnett and colleagues;143 however, ganglion cells have not been found.

Contrary to Galen’s view that the liver has no sensation,147 it now appears that 75 to 90 percent of vagal fibers in the abdomen are afferent and almost all of them unmyelinated. Specific receptors have not been recognized, but osmoreceptors, ionic receptors, baroreceptors, and metabolic receptors are considered to exist in the liver.157

Glissonian Sheaths

While lecturing in Egypt, the senior author of this chapter, Dr. John Skandalakis, had the opportunity to hear a very interesting paper, Surgical Anatomy of the Glissonian Sheaths: A Prerequisite for Hepatic Resection and Liver Transplantation. He proposed that the authors, Ramadan M. El-Gharbawy, Moustafa M. El-Hennawi, Farouk A. Mekky, Ossama A. El-Deeb, and Mohamed K. El-Saiedy of the Departments of Anatomy and General Surgery of the Faculty of Medicine, Alexandria University, publish their work in this book, and we are grateful that they agreed.

ABSTRACT. A complete knowledge of the anatomic variations in arterial supply, bile duct, portal, and hepatic venous anatomy, as well as the segmental anatomy of the liver, is an essential prerequisite for hepatic resection and liver transplantation. Twenty normal fresh human livers were injected with colored latex and dissected to study the glissonian sheaths of the eight hepatic segments. Segment I had three sheaths that entered the anterior surface of the lower end of the segment. The glissonian sheaths of segments II, III, and the lower part of segment IV arose constantly in the fissure for ligamentum teres from the left main sheath. The upper part of segment IV had its sheath in the porta hepatis in ten specimens from the left main sheath and from the right anterior sector sheath in the other ten specimens. The right main sheath bifurcated into the right anterior and the right posterior sector sheaths. The right anterior sector sheath gave the sheaths of segments V and VIII. The right posterior sector sheath gave the sheaths of segments VI and VII exhibiting two patterns of distribution.

INTRODUCTION. Hepatic resection for primary tumors and metastases has gained increasing support as it represents the only chance to improve long-term survival of selected patients.161-164 In the last three decades, extensive hepatic resection has become a safe operative procedure.165 In patients with impaired hepatic function, preservation of hepatic parenchyma is an important consideration during resection.166 These resections, whether extensive or segmental, could be performed on the anatomic basis of the liver.165

Liver transplantation has developed into a major effort to support patients with advanced liver disease. Although the techniques have been standardized, it remains a difficult and complex procedure. A complete knowledge of the anatomic variations in arterial supply, bile duct, portal and hepatic venous anatomy, as well as the segmental anatomy of the liver, is an essential prerequisite to developing the surgical skills for this form of surgery.54

The capsule of the liver (Glisson’s capsule) condenses around the hepatic trinity structures and surrounds them as they enter the liver substance. Thus each bile duct, hepatic artery, and portal vein unit is surrounded by a fibrous sheath which is called the “glissonian sheath.” When approached from within the liver substance, the sheaths simplify ligation of the hepatic trinity and if the sheath to a particular segment is ligated it will contain contain structures passing to or from that segment only. Ligation of the individual sheaths is therefore not only simpler but safer.167

The present study aimed at studying the glissonian sheaths of the eight hepatic segments.

MATERIAL AND METHODS. Twenty normal fresh human livers were used in the present study. Ten of them were harvested from adult cadavers brought to the Anatomy Department, Alexandria Faculty of Medicine prior to injection with the fixative. The other ten were livers of stillborns obtained from the Department of Obstetrics, Alexandria Faculty of Medicine. The portal vein and the common bile duct were ligated and divided behind the neck of the pancreas. The hepatic artery was ligated and divided at its origin from the celiac trunk, and also the accessory or replacing hepatic arteries were ligated and divided at suitable lengths from the liver if they were present. The inferior vena cava was ligated and divided above the renal veins and at the level of the right atrium, and the segment in between was removed with the liver. The liver was then taken out of the cadaver.

The portal vein, the bile duct, the hepatic artery(ies), and the inferior vena cava were cannulated and perfused with normal saline to wash out their contents. The liver was then perfused with 500 mL of three percent formol saline and left for four hours taking care not to squeeze it. After that the bile duct, the hepatic artery(ies), the portal vein, and the inferior vena cava were injected with colored latex in that order.

After the injection was completed, the liver was wrapped with a towel soaked with a wetting fluid168 and refrigerated for 24-48 hours. The livers were dissected starting at the porta hepatis. The right and left main glissonian sheaths were identified. Their segmental branches were followed, then the sheaths were opened and their contents were studied, photographed, and documented.

RESULTS. Glissonian sheaths of the right and left lobes. The glissonian sheaths of the right lobe (right main sheath) and of the left lobe (left main sheath) arose from the structures of portal trinity in the right end of the porta hepatis (Figs. 19-59, 19-60).

Fig. 19-59.

A photograph showing the posterior surface of the hilar plate (HP) after encircling the right main (R) and left main (L) sheaths with silk threads. PV, portal vein; d, bile duct; a, hepatic artery proper; IVC, inferior vena cava. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

Fig. 19-60.

A photograph of the inferior surface of the liver showing the contents of the right main and left main sheaths. The right main sheath passes immediately into the parenchyma. The course of the left main sheath is wholly extrahepatic. PV, portal vein; LP, left branch of portal vein; LH, left branch of hepatic artery; R, right hepatic duct; III, contents of segment III’s sheath; IV, contents of lower part of segment IV’s sheath; RH, right branch of hepatic artery; RP, right branch of portal vein; CHD, common hepatic duct; II, contents of segment II’s sheath; g, ligamentum teres. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

THE RIGHT MAIN SHEATH. The right main sheath contained the right branches of the portal vein, the hepatic artery proper and the right hepatic duct. It arose from the structures of portal trinity in the right end of the porta hepatis and passed to the right into the parenchyma of the right lobe to bifurcate into the right anterior and right posterior sector sheaths (Figs. 19-60, 19-61).

Fig. 19-61.

A photograph showing the contents of the right main and left main sheaths. The contents of the right main sheath divide into the contents of the right anterior and right posterior sector sheaths. RH, right branch of hepatic artery proper; RP, right branch of portal vein; D2 & D3, bile ducts in the left main sheath; rp, contents of the right posterior sector sheath; r, m, L, contents of the right, middle and the left sheaths of segment I (S1); LH, left branch of the hepatic artery proper; LP, left branch of the portal vein; ra, contents of the right anterior sector sheath. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

THE LEFT MAIN SHEATH. This fascial sheath contained the branches of the portal vein, the hepatic artery, and the bile ducts of the left lobe of the liver. The sheath passed to the left end of the porta hepatis then anteroinferiorly in the fissure for ligamentum teres. In all specimens, the whole course of the left main sheath was extrahepatic (Figs. 19-60, 19-61).

Glissonian sheaths of segment I. Segment I had three sheaths in all specimens (Figs. 19-61, 19-62). One, to the left, entered the anteroinferior aspect of the papillary process. Its vein arose from the adjacent side of the left branch of the portal vein. Its artery arose from the branch of the left branch of the hepatic artery going to the lower part of segment IV in 16 specimens (80%) and from a replacing hepatic artery arising from the left gastric artery in the remaining four (20%). The artery crossed posterior to the left portal branch. Its duct joined the posterosuperior aspect of the duct to segment II.

Fig. 19-62.

A photograph of the inferior surface of a stillborn’s liver showing the three glissonian sheaths (right [r]. middle [m] and left [L] of segment I [S1]). PV, portal vein; d, ductus venosus; IVC, inferior vena cava; G, gallbladder. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

The middle sheath entered the middle of the antero-inferior aspect of the lower end of the segment. Its vein arose from the posterior surface of the bifurcation of the portal vein. Its artery arose from the branch of the right branch of the hepatic artery running medial to the portal branch of the sheath of the right anterior sector. Its duct joined the posterosuperior aspect of the duct to segment II.

One, to the right, entered the anteroinferior aspect of the caudate process. Its vein arose from the adjacent side of the right branch of the portal vein. Its artery arose from the artery going to segment VII. Its duct joined the beginning of the stem of the duct to both segment VI and VII.

Glissonian sheath of segment II. Segment II had one sheath in all specimens (Figs. 19-63, 19-64, 19-65, 19-66). The sheath arose from the left main sheath at the left end of the porta hepatis, where the inferior end of the fissure for ligamentum venosum met the posterosuperior end of the fissure for ligamentum teres. On reaching the left end of the porta hepatis, the left branch of the portal vein gave several branches (avg. 3 ± 0.75) where it changed its direction to run in the bottom of the fissure for ligamentum teres. These formed the portal component of segment II sheath.

Fig. 19-63.

A photograph of a stillborn’s liver showing the contents of the glissonian sheaths of segments II, III, and lower part of IV. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

Fig. 19-64.

A photograph of the inferior surface of the liver showing the course and contents of the left main sheath, the contents of the sheaths of segments II, III and lower part of IV and round ligament (g). (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

Fig. 19-65.

A photograph showing the arteries and ducts of the sheaths of segments II, III, and lower part of IV. The ducts of the right (r), the middle (m), and the left (L) sheaths of segment I (SI) are also shown. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

Fig. 19-66.

A photograph showing the arteries of the sheaths of segments II, III, and lower part of IV. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

The duct draining segment II received the ducts of the left and middle sheaths of segment I and joined the right hepatic duct in 16 specimens. In the remaining 4 specimens it received, in addition to the ducts of the left and middle sheaths of segment I, a duct from segment III. The artery of segment II sheath arose from the left branch of the hepatic artery proper in 16 specimens (80%) and from a replacing hepatic artery in 4 specimens (20%). This replacing hepatic artery, when present, arose from the left gastric artery near the cardia and ran in the lesser omentum to reach the fissure for ligamentum venosum skirting its left bank. In these four specimens the replacing hepatic artery provided the artery of the left sheath of segment I.

Glissonian sheath of segment III. Segment III had one sheath in all specimens (Figs. 19-63, 19-64, 19-65, 19-66). The sheath was found in the bottom of the fissure for ligamentum teres on the left side of the attachment of the round ligament with the left branch of the portal vein. The number of the portal branches in the sheath was 3 ± 0.17. The artery of the sheath arose from the left branch of the hepatic artery proper in 16 specimens (80%) and from a replacing hepatic artery in 4 specimens (20%). The latter arose from the left gastric artery and passed in the gastrohepatic ligament (lesser omentum) to the fissure for ligamentum venosum. It skirted the left banks of the fissures for ligament venosum and teres passing posterior to the portal branches to segment II providing the artery to that segment and continued to reach the sheath of segment III and became its artery.

The duct of segment III was present posterosuperior to the portal branches of the segment. In eight specimens it followed the left side of the portal branch superiorly to pass anterior to the portal branches of segment II, then it curved to the right traversing the porta hepatis posterosuperior to the left portal branch. This configuration was called by the author “curved duct pattern.” In another eight specimens (40%) the duct passed directly to the right anterior to the left portal branch to reach the porta hepatis. This configuration was called by the author “straight duct pattern.” In the remaining four specimens (20%), the segment was drained by two ducts that passed to the porta hepatis anterior to the left portal branch and one superior to the other. This configuration was called by the author “double duct pattern.”

Glissonian sheaths of segment IV. The lower part of segment IV received its sheath in the fissure for ligamentum teres, nearly opposite to the sheath of segment III in all specimens. This sheath contained 3 to 7 portal branches (mean 5 ± 0.92) that arose from the left portal branch just before it became continuous with the round ligament. The artery in the sheath arose from the left branch of the hepatic artery proper in all specimens. Its duct jolned the duct of segment III in 16 specimens (80%). In four specimens (20%), where segment III was drained by two ducts, the duct of the lower part of segment IV joined the inferior one (Figs. 19-63, 19-64, 19-65, 19-66).

The sheath of the upper part of segment IV in ten specimens (50%) originated in the porta hepatis. The portal branches arose from the left portal branch. The artery arose from the left branch of the hepatic artery. The duct joined that draining segment III. In the other ten specimens the sheath originated from the sheath of the right anterior sector “segments V and VIII.” In these ten specimens (50%), the branches of the right branch of the portal vein and the right branch of the hepatic artery to the right anterior sector were the source of the blood supply to the upper part of segment IV. The duct joined that of the anterior sector (Figs. 19-67 and 19-68).

Fig. 19-67.

A photograph showing the anterior surface of an adult’s liver. The parenchyma was removed to show the glissonian sheaths of segments V, VIII, and the upper part of IV. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

Fig. 19-68.

A photograph showing the components of the glissonian sheaths of segment VIII and the upper part of segment IV. RHV, right hepatic vein; rp, components of right posterior sector. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

Glissonian sheath of the right anterior sector. The sheath passed from the end of the right main sheath anteriorly (Figs. 19-61 and 19-69) to provide 1 to 3 sheaths (2.05 ± 0.99) to segment V and one sheath for segment VIII in all specimens. In addition it provided 1 to 2 sheaths (1.3 ± 0.23) to the upper part of segment IV in ten specimens (50%) (Figs. 19-67 and 19-68).

Fig. 19-69.

A photograph showing the portal branches of segments V and VIII arising from the portal branch of the right anterior sector. The portal branch of the right posterior sector has been retracted to the left and its branches to segments VI and VII are shown. The ducts and arteries of segments VI & VII are also shown. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

Glissonian sheaths of segments V and VIII. The right anterior sector sheath was the origin of the sheaths of segment V. In all specimens (Figs. 19-67, 19-68, 19-69) the segment had 1 to 3 sheaths (2.05 ± 0.99). In all livers, segment VIII received single sheath (Figs. 19-67, 19-68, and 19-69).

Glissonian sheath of the right posterior sector. The right posterior sector sheath passed to the right and posteriorly from the point of bifurcation of the right main sheath (Fig. 19-61).

Glissonian sheaths of segments VI and VII. The right posterior sector sheath was the origin of the sheaths of segments VI and VII in all specimens. In the present study, the manner in which the right posterior sector was distributed to both segments could be classified into two patterns.

In the first, the right posterior sector sheath bifurcated into the sheaths of segments VI and VII. This pattern was encountered in three adult livers and in all the stillborns’ livers (65%) (Figs. 19-69, 19-70, and 19-71).

Fig. 19-70.

A photograph of a stillborn’s liver showing the first pattern of the right posterior (PL) sector sheath. It bifurcated into the sheaths of segments VI and VII. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

Fig. 19-71.

A photograph of an adult’s liver showing the first pattern of the right posterior (rp) sector sheath. It bifurcated into the sheaths of segments VI and VII. The inferior right hepatic vein (lRHV) was severed from the inferior vena cava (lVC) and retracted to expose the point of bifurcation. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

The second pattern was encountered in seven adults’ livers (35%). The right posterior sector sheath ran first towards the inferior border, then to the right, and, lastly, superiorly; i.e., it ran a curved course in segments VI and VII respectively. It gave several branches to either segment from its convex border. Segment VI received 3 to 5 branches (4 ± 0.66) and segment VII received 4 to 7 (5.28 ± 1.24) (Fig. 19-72).

Fig. 19-72.

A photograph of an adult’s liver showing the second pattern of the right posterior (rp) sector sheath. An accessory hepatic vein (ahv) is cut and retracted. Two tributaries (t) of the right hepatic vein (RV) are shown. (Courtesy of El-Gharbawy, El-Hennawi, Mekky, El-Deeb, El-Saiedy.)

DISCUSSION. The sheaths of segment I arose from the posterior aspects of the right main and left main sheaths and entered the anteroinferior aspect of the lower end of the segment. This critical anatomical location of the sheaths, in addition to the presence of the segment on the posterior surface of the liver behind the upper part of segment IV and its direct venous drainage into the inferior vena cava, made Launois and Jamieson167 regard segment I difficult to excise. Ton That Tung169 and Bismuth and Houssin170 had proposed excising segments II and III to gain access to segment I. Launois and Jamieson167 had proposed excision of segments I and IV together.

Segment II had single sheath in all specimens. It arose from the left main sheath when the latter left the left end of the porta hepatis to run in the fissure for ligamentum teres. The banks of the fissure can be easily and safely forced apart to expose the origin of segment II sheath.171 Segment II can be excised alone. On doing segmentectomy II, the operator has to dissect the sheath of segment II in the liver substance 1 cm to the left of its origin. In this way the duct and the artery of segment III are safeguarded if they are coursing along the left side of the left portal branch.

In the present study segment III received single sheath that arose from the left side of the left main sheath where it became continuous with the round ligament in the fissure for ligamentum teres. The origin of the sheath was extrahepatic and constant in all specimens, and the round ligament served as a guide to its site. Launois and Jamieson167 mentioned that there might be one, two, or even three glissonian sheaths to segment III.

The extrahepatic origin and the constant location of the sheaths of segments II and III, the peripheral position of the segments, and their easily identifiable borders on the anterosuperior surface (falciform ligament) and postero-inferior surface (fissures venosum and teres) could explain why segmentectomy II and III is a straightforward operation.167

Segment IV is formed of two parts. Its lower part, i.e., the quadrate lobe, is well circumscribed. The sheath of this lower part arose constantly in the fissure for ligamentum teres from the right side of the left main sheath just proximal to the attachment of the latter with the round ligament so resection of the quadrate lobe is a straightforward segmentectomy. The sheaths of the upper part arose from the left main sheath in the porta hepatis in ten specimens and from the right anterior sector sheath in the other ten. This upper part is bounded above by two major structures, i.e., the middle and left hepatic veins, and lies in front of segment I separated from it by the dorsal fissure whose plane has to be guessed during resection of this upper part. This might explain why the resection of this part is difficult.167

The right main sheath bifurcated into the sheaths of the right anterior and the right posterior sectors inside the liver substance. The right main sheath could be dissected in the porta hepatis and controlled with a tape in right hepatectomy.167

The right main sheath branched into the sheaths of the right anterior and the right posterior sectors inside the liver parenchyma. This fact is the basis of the “posterior approach” adopted by the French surgeons in segmentectomies of the right lobe of the liver. They dissect the right anterior sector sheath through the inferior surface of the liver prior to parenchymatous transection and clamp it with the hepatic pedicle unclamped. The right anterior sector became cyanosed and its right and left borders delineate the right and main hepatic fissures respectively.167,172

The sheath of the right anterior sector ran anteroposterior. It gave 1 to 3 sheaths to segment V that ran anteroinferiorly and single sheath to segment VIII. Launois and Jamieson167 stated that the glissonian sheaths of segment V are usually 1 to 3 in number, anteroposterior in direction, straight, and never recurrent. They also reported two sheaths for segment VIII. To the best of the investigators’ knowledge, the branches of the right anterior sector sheath to the upper part of segment IV were not mentioned before and need further confirmation.

The right posterior sector sheath had two patterns of distribution. In the first pattern (65%) it bifurcated into the sheaths of segments VI and VII. This means that either segment can be resected alone safely. In the second pattern (35%) the sector’s sheath ran a curved course first through segment VI, then through segment VII. It had several segmental branches that arose from its convex border. In this case resection of segment VI jeopardizes the blood supply of segment VII.

In the present study, segment VI had single sheath in 65% of specimens and received 3 to 5 sheaths in 35% of specimens. According to Launois and Jamieson,167 the number of cases in which a single glissonian sheath supplies segment VII is probably less than half and there are often two or even three sheaths, with the first arising from the right main sheath. On excising segment VII, they expressed the importance of leaving all the sheaths that are recurrent or posterior, as they supply segment VI. This could be clearly explained by the second pattern of distribution described in the present study.

Segment VII received single sheath in 65% of specimens and had 4 to 7 sheaths in the remaining 35%. Launois and Jamieson167 stated that segment VII is usually supplied by a single sheath.

Histology and Physiology

The liver is the main metabolic organ of the body. It is composed of parenchyma (hepatocytes) and its supporting connective tissue stroma. The exocrine secretion of the hepatocytes is bile. The bile passes into intercellular bile canaliculi; these open into bile ducts. Endocrine secretions into the bloodstream include glucose, plasma proteins, and lipoproteins. Important metabolic activities of the hepatocytes are:

 

converting glucose to glycogen and vice versa

degrading steroid hormones

detoxifying toxic substances and drugs

utilizing lipids in lipoprotein synthesis

Each hepatocyte borders on a bile canaliculus and on one or more blood sinusoids. Overall, the liver is composed of parenchymal units arranged in six-sided prisms about 0.7 mm x 2.0 mm in size (Fig. 19-30A). These units are the “classic” liver lobules but not the functional lobules. In the center of the prisms are the tributaries of the hepatic veins. On the edges of the prisms are the three elements of the hepatic triad. They are the:

 

Branches of the bile ducts

Hepatic arteries

Hepatic portal vein

The hepatic portal vein is surrounded by connective tissue that continues at the porta with the connective tissue of the fibrous (Glisson’s) capsule of the liver. Three to six triads are associated with each unit.

The liver cells (hepatocytes) of the unit are arranged in fenestrated plates disposed radially from the central vein to the periphery. The spaces between the plates are occupied by the liver sinusoids, the walls of which are formed by a discontinuous endothelium. This endothelium lies on the microvilli of the hepatocyte forming a perivascular space (of Disse) (Fig. 19-42). Because the discontinuities of the endothelium are smaller than erythrocytes, the space of Disse contains macromolecules but not blood cells. Fixed macrophages (Kupffer cells) are associated with the endothelial cells of the sinusoid. Stellate “fat storing” cells are also present in the perivascular spaces.

According to Sasse et al.,173 each hepatocyte has a vascular pole responsible for an ingestive sense and a biliary pole responsible for secretory function.

The biliary tract begins with the bile canaliculi (Fig. 19-42). These canaliculi are bounded by two or three hepatocytes and range from about 0.5 Ìm to 1.0 Ìm in diameter. They form a polyhedral network between hepatocytes. The network is continuous from lobule to lobule and is without blind ends. With the light microscope, the canaliculi appear to be lined by a membrane. This appearance is due to adenosine triphosphate activity in the hepatocyte at the surface of the canaliculus.

The canaliculus is bounded by the plasma membrane of two or more hepatocytes from which short, stubby microvilli project into the lumen. On either side of the canaliculus, adjacent hepatocytes are attached to one another by a zonula occludens. Thus, the bile is confined to the bile canaliculus and can move only toward the periphery of the lobule.

As the canaliculi approach the periphery, small ducts lined with cuboidal epithelium appear; these are the bile ductules (Hering’s canals) (Fig. 19-58). As these enter the connective tissue of the portal triad, they become true bile ducts of the triads. The lining of the duct is a regular cuboidal or columnar epithelium and the duct is covered by a sheath of connective tissue.

The classic liver lobule (Fig. 19-30A) exhibits a hexagonal shape. The portal tract area (or radicle) at each “corner” contains portal vein branches, the hepatic artery, bile ducts, lymphatics, and connective tissue. The central vein lies within the center of the lobule. Within the lobule are portal vein and hepatic artery branches entering and anastomosing with thin-walled sinusoids. These extend from the radicle to the central vein of the lobule. This vein opens into the sublobular veins that drain into hepatic veins, and these open into the inferior vena cava. Trabeculae are plates of hepatocytes radiating from central vein to edge of the lobule.

“True” ducts of Luschka are in the hepatic surface. These are ductlike structures which may connect with bile ducts but never open into gallbladder lumen.

The surgical physiology of the liver may be summarized in Merrell’s174 beautiful table (Table 19-6).

Table 19-6. Hepatic Functions

Filtration (i.e. reticuloendothelial system) 
Process incoming substrate & vitamins 
Metabolic homeostasis 
  Fundamental mechanisms 
    Capture
    Maintenance of intracellular metabolism
    Storage
    Release
  Metabolic substrates 
    Carbohydrates—modulate glucose 
    Lipids—modulate free fatty acids
    Amino acids—modulate amino acid pools
Specific protein synthesis 
Coagulation Fibrinogen
Prothrombin
VII, IX, X
Carrier proteins Albumin 
Transferrin
Lipoprotein
Lipid phase metabolism 
  Drug metabolism
  Bile formation
  Lysosomal and nonlysosomal transport

Source: Clark JH III, Wood RP. Hepatic physiology. In: Miller TA (ed). Physiologic Basis of Modern Surgical Care (2nd ed). St. Louis: CV Mosby, 1998, pp. 491-511; with permission.

The capacity of the liver to regenerate is well-known. This enigmatic act has been appreciated for many centuries. Even after a 75 to 90 percent hepatectomy, a liver possessing a normal remnant may fully regenerate within weeks or months.175 The mechanism of regeneration is highly hypothetical; however, it is known that hepatocytes proliferate first, and nonparenchymal cells appear later. Insulin, glucagon, epidermal growth factor, and other elements may possibly be involved.

Holley176 reported that growth factors and hormones may act by invoking the same intracellular growth-control mechanisms affected by nutrients. Barker and colleagues177 and Lambotte and Tagliaferri,178 all of the University of Louvain in Belgium, are engaged in ongoing studies of in vivo “priming” and “progression” factors as well as the synthesis of DNA in liver regeneration following partial hepatectomy.

After experimenting in rats, Hashimoto and Sanjo179 stated that functional liver capacity was minimal during parenchymal cell mitosis in the regenerating liver. The same authors observed that functional restoration after two-thirds hepatectomy was delayed in comparison with morphologic restoration in rats.

Surgery

The liver, because of its unforgiving and extraordinarily difficult surgical anatomy and complex physiology, will remain the Mount Everest of organs for surgeons. It is no place for the fainthearted, perhaps, but it will continue to challenge the bright and the bold.—James H. Foster180

Exploration of the Abdomen

Upon entering the abdomen, if a pathologic diagnosis is needed prior to proceeding, perform a needle biopsy or wedge biopsy of the liver as soon as possible. This avoids any changes in the liver due to injury by instruments or the effects of the anesthetic drugs. As a rule, the biopsy should be taken far away from the area of the gallbladder, especially if there are pathologic processes involving the gallbladder that might affect the adjacent liver tissue. Ultrasonographic examination may be performed to identify the area of pathology if necessary.

Exploration should begin with the omentum, transverse colon, and mesocolon, which should be withdrawn from the abdomen and positioned between a warm pack outside and the upper part of the incision. The hand should pass down to the pelvis to palpate the left colon, male or female pelvic organs, urinary bladder, great vessels, and the anatomic entities within the retroperitoneal space.

The surgeon may choose to palpate the right colon at this time or after examining the small intestine and its mesentery from the ligament of Treitz to the ileocecal valve. We do not object to retrograde examination from the valve to the ligament. Examine part of the second, third, and fourth parts of the duodenum. Observe the relation of the superior mesenteric artery to the third part of the duodenum. Harvest any abnormal lymph nodes and send them for examination while mobilization of the liver begins.

The pancreas must now be palpated. The inspection of the infracolic compartment concludes with examination of the abdominal wall for hernias, omphalomesenteric anomalies, and urachal cysts.

Replace the omentum and transverse colon and its mesentery in the abdomen. Inspect the supracolic compartment from the right, starting by palpating the right kidney, duodenum, head of the pancreas, and pylorus. The stomach, up to and including the gastroesophageal junction, should be felt. Palpate the spleen with great care; the peritoneal attachments are short and the splenic capsule is easily torn.

Exploration of the Liver

The entire liver and biliary tract must be methodically evaluated. Examine the inferior surface of the diaphragm prior to the actual hepatic exploration. The area of suspected pathology should be the last to be examined. Intraoperative ultrasonography is the most accurate method for examination of the liver and should be performed routinely.

Palpate the lateral segment of the liver by passing the hand to the left of the falciform ligament and move backward until the fingertips reach the coronary and left triangular ligaments. Similarly, the hand may be passed to the right of the falciform ligament, moving backward to palpate the coronary and right triangular ligaments. Palpate the falciform and splenorenal ligaments. Occasionally the base of the falciform ligament is not fused with the abdominal wall, leaving a hiatus through which a loop of intestine may herniate.

We quote from Takao and Kawarada181 on the hepatic hilar area:

It is important to understand the main variations of the biliary and vascular elements inside the plate system for hilar bile duct carcinoma because all variations of these elements occur in this plate system. The plate system consists of the hilar plate, cystic plate, and umbilical plate which cover the extrahepatic vascular system and are fused with the hepatoduodenal ligament. The bile duct and vascular system that penetrate the plate system form Glisson’s capsule in the liver, but the caudate branch and the medial segmental branch are exceptions. The bile duct and hepatic artery accompanying the plate system can be exfoliated from the portal vein with numerous lymph ducts and nerves. The bile ducts in the right hepatic lobe are classified into 4 types, and the standard type is present in 53-72% of cases. In the left bile duct, the medial segmental bile duct is connected in the vicinity of the hilar area in 35.5% of cases, and these cases should be treated the same as the caudate lobe in hilar bile duct carcinoma. Generally, there is little main variation of the portal vein (16-26%), but more variation in the hepatic artery (31-33%). During surgery for hilar bile duct carcinoma, it is important to observe the plate system and the many variations of the bile duct vascular system.

The Surgeon and the Liver in the Operating Room

It is not within the scope of this chapter to discuss details of liver pathology. We will, however, describe the gross appearance of some hepatic pathology collectively, but not specifically. We hope this will help the surgeon make the right decision in the operating room.

The dilemma of the surgeon is whether to perform a partial hepatectomy and thus cure the patient if the lesion is benign, to palliate the patient for a longer or shorter period if the lesion is malignant, or whether to leave the patient alone. The patient’s history and laboratory reports will help the surgeon decide.

Another dilemma is the choice of an open or needle biopsy. Nearly all common pathologic entities can currently be distinguished by their appearance on imaging studies (CT, spiral CT, MRI, arteriograms, etc.). Biopsies may be done for confirmation but are not always necessary. Remember that a small hemangioma will bleed copiously, and the aspiration of an Echinococcus cyst of the liver may produce a fatal anaphylactic reaction.

Tables 19-7 and 19-8 list anatomic differential diagnosis of the liver and gallbladder and ducts in the operating room. We present these tables with mixed feelings, since the gross appearance of a hepatocellular carcinoma, for example, overlaps the gross appearance of a cholangiocarcinoma. Liver cell adenoma, focal nodular hyperplasia, and hemangioma may have the same or different appearance. If the anatomist, with the aid of the pathologist, can help the surgeon differentiate between benign and malignant lesions, the patient is the beneficiary.

Table 19-7. Anatomic Differential Diagnosis of the Liver in the Operating Room

PATHOLOGY 
I. Abscesses
  A. Pyogenic
    Abscesses usually small and multiple; may be solitary and multilocular. According to Schwartz (1984) a solitary abscess is usually in the right lobe.
  B. Amebic
    Single large abscesses usually in the right lobe on either hepatic surface. Aspiration will give the characteristic chocolate-like or “anchovy paste” fluid. Variable; may be multiple.
II. Cirrhosis
  A. Cirrhosis (micronodular)
    Hepatomegaly with minute nodules and panhepatic fibrosis. The liver is a dark brown color if hemosiderosis is present; tan or yellow if fatty metamorphosis has occurred.
  B. Cirrhosis (macronodular)
    Liver, large or small, with large nodules
III. Cysts
  A. Nonparasitic
    Solitary, usually at the anterior inferior surface of the right lobe, containing crystal clear fluid or brown-yellow semiliquid material. Traumatic cysts are single without epithelium and filled with bile (Schwartz, 1964). Polycystic cysts are usually throughout the liver but they may be limited to the right lobe. They have a honeycomb appearance. About one half of patients will have polycystic kidneys also.
  B. Parasitic Hydatid (Echinococcus) 
    1. E. granulosus 
       85% are superficial in the right lobe. The cystic wall consists of an outer (adventitia) and an inner (germinative) membrane. The cysts contain clear fluid at high pressure.
    2. E. multilocularis (alveolar) 
       There is no capsule or cystic wall. Multiple minute cysts with gelatinous rather than fluid contents. They infiltrate the surrounding tissue.
IV. Tumors
  A. Benign
    May or may not be encapsulated. May be large or small, discrete or nodular, well defined or ill defined, single or multiple, often subscapular.
  B. Malignant
    1. Primary
       Single or multiple masses or nodules in one or both lobes of the liver. Hepatomegaly may be present. Cirrhotic appearance is usual. The tumor may be nodular, massive or diffuse. If firm and whitish and in the periphery of the liver, consider cholangiocarcioma. Portal vein thrombosis in malignant hepatoma has been reported (Albacete et al. 1967).
    2. Metastatic—superficial
       Discrete yellow or grayish nodules, or centrally necrosed, under the hepatic capsule, but very visible. Hepatomegaly. Lesions mimic fibrous scars, tubercular nodules, nodular hyperplasia, bile duct adenoma, syphylitic nodules, etc.
    3. Metastatic—deep
       Lesions deep in the liver parenchyma without visible nodules. The absence of visible nodules on the surface does not rule out metastatic disease (Goligher, 1941).

References

Schwartz SI. Liver. In: Schwartz SI, Shires GT, Spencer FC, Storer EH (eds). Principles of Surgery. New York: McGraw-Hill, 1984.

Schwartz SI. Surgical Diseases of the Liver. New York: McGraw-Hill, 1964.

Albacete RA, Matthews MJ, Saini N. Portal vein thromboses in malignant hepatoma. Ann Intern Med 67:337, 1967.

Goligher JC. Surgery of the Anus, Rectum and Colon, 5th Ed. London: Balliere Tindall, 1984, p. 450.

Table 19-8. Anatomic Differential Diagnosis of the Gallbladder and Ducts in the Operating Room

PATHOLOGY 
I. Cholecystitis
  A. Acute calculus
    The gallbladder is red and edematous and is distended due to cystic duct obstruction secondary to an impacted stone. The color is black if gangrene is present. Perforation may have occurred with evidence of local bile peritonitis. After aspiration the gallstones are palpable under the thick, hypertrophic, edematous wall. Large lymph nodes are present. Pus is present with pyogenic membranes. The ducts, particularly the common bile duct, are covered by the edematous gastrohepatic omentum and the duct may be inflammed sympathetically. If the epiploic foramen is obliterated secondary to edema, stones may be palpated in the common bile duct. Remember: gallstone ileus. Jaundice may be present. A large solitary calculus in Hartmann’s pouch may distend the gallbladder with mucocele, hydrops or empyema.
  B. Acute acalculus—10%
    As above but without stones. Perforation is frequent.
  C. Chronic calculus
    The wall may be thickened, but stones are palpable. Jaundice, adhesions and enlarged lymph nodes may be present. The common bile duct may be dilated due to distal obstruction. The gallbladder may be normal or shrunken.
  D. Chronic acalculus
    As above but without stones.
  E. Choledocholithiasis
    Impaction at the lower end. Jaundice may be present; the common bile duct may be dilated. Remember two synchronous impactions: cystic duct and ampulla of Vater. The results are jaundice and mucocele or empyema. The presence of stones does not proclude malignancy. Check the head of the pancreas and the porta hepatis. Remember: a stone may produce acute pancreatitis.
  F. Cancer of gallbladder
    Metastases to choledochal lymph nodes. Rarely a cause of obstruction by compression.
  G. Other pathology of the common bile duct
    With cancer of the head of the pancreas the common duct is dilated, thin walled and bluish. With distal cancer the gallbladder is usually distended, the common duct is not affected with chronic pancreatitis; jaundice may be present. The common bile duct and the gallbladder are distended, edematous and pale.

The surgeon goes to the operating room with a definite strategy. His or her armamentarium includes a variety of diagnostic procedures, which, along with their complications, are described below.

The surgery of the liver consists of biopsies; suture of lacerations; right hepatectomy (lobectomy), typical or extended; left hepatectomy (lobectomy), typical or extended; segmentectomy; removal or drainage of cysts; and total or partial transplantation.

Czerniak et al.182 reported the following. [Authors’ note: For clarity, we would replace all occurrences of the term “left lobe” with “segments II and III.”]

The anatomical possibility of resecting the left lobe of the liver (segments II and III) in living subjects and using it for transplantation was evaluated. A group of 60 cadaveric livers were dissected at autopsy. The vascular and biliary elements of the left lobe were isolated and the lobe was resected and evaluated for possible grafting.

The left lobe was 12% to 28% (mean 19.4%) of the liver mass. An extrahepatic segment of the left hepatic vein was isolated in 95% of specimens. Arterial blood supply to the left lobe consisted of a single artery (92%) or two arteries (8%).

A single portal vein segment to the left lobe (type I) was found in 35% livers. Portal vein branches originated from a common orifice (type II, 35%) or separately (type III, 30%) from the left portal vein, and in these instances, preparation of a portal segment necessitated partial section of the left portal vein wall.

Biliary drainage was extrahepatic in 56 livers and consisted of a single duct (type I, 78%), or two ducts (type II, 15%).

The resected left lobe was evaluated as satisfactory (single hepatic vein and artery, types I or II portal vein, type I bile duct) in 48% of cases, while a less-satisfactory lobe (type III portal vein or type II bile duct) was obtained in 33%.

It was found anatomically difficult or impossible to resect the left lobe for possible transplantation in 11 (19%) liver specimens.

However, Kazemier et al.183 disagreed “strikingly” with Czerniak and colleagues. Table 19-9 is Kazemier’s summary of the differences between the results of his team’s study of 39 corrosion casts and Czerniak’s dissection of 60 human cadaveric livers along the umbilical fissure.

Table 19-9. Anatomy of Supplying and Draining Structures of Couinaud Segments II and III (Resection at Plane in Umbilical Fissure)

  Czerniak et al.178 (n = 60) 
 
Kazemier et al.179 (n = 39) 
 
Arterial blood supply to segments II and III:    
  1 Artery 92% 59%
  >1 Artery 8% 41%
Portal blood supply to segments II and III:    
  Type I (single portal vein to segments II and III) 35% 0%
  Type II (common orifice of portal vein branches to segments II and III) 35% 0%
  Type III (separate orifices of portal vein branches to segments II and III) 30% 100%
Biliary drainage of segments II and III:    
  Type I (single duct) 78% 56%
  Type II (two ducts) 15% 44%

Source: Kazemier G, Hesselink EJ, Terpstra OT. Hepatic anatomy. Transplantation 1990;49:1029; with permission.

The reply of Czerniak et al.184 to Kazemier et al. follows verbatim.

. . .We suggest that the difference in the technique used (dissection vs. the cast method) may explain the discrepancy between the results of our study and the study of Kazemier et al. Michels78 in his detailed dissection study of 200 livers, has found a single artery to the left lobe in 88.5% of cases. Couinaud185 reports the portal blood supply to segments II and III to consist of a single portal vein branch in 96% and 31%, respectively. A type I portal vein (though not named as such) is also described (Couinaud). In the same study, and based on dissection of 100 livers, a single bile duct draining the left lobe was found in 77% of livers.185 These results are comparable with ours.

There are often ducts and vessels coming from the liver substance underlying the umbilical fissure and the fossa for the ligamentum venosum,78 and it may be difficult to ascertain the relationship between these structures and the various structures of the left lobe by the cast method.

Moreover, using the cast method, judgement about the various planes of resection of the liver parenchyma as being within or adjacent to the umbilical fissure, is only approximate.186 Kazemier et al.183 have found a single artery to the left lobe in 59% and a type I bile duct in 56% of the 39 livers examined. However, when they examined a plane that is presumed to be to the right of the umbilical fissure, a single artery supplying the graft was obtained in 77%, and a single biliary branch in 95% of cases. When one considers the possible discrepancies in the planes of resection between the two studies, these results approximate ours (92% and 78%, respectively).

Based on our dissection studies, we suggest that the plane of resection of the liver should be within the umbilical fissure. Using this plane, both an accurate extrahepatic dissection and preparation of the portal structures to the left lobe, and an avoidance of damage to segment IV structures can be achieved.

However, the scientific battle for the anatomy of the noble organ continues.

Kazemier et al.,187 analyzing 60 corrosion casts of human cadaveric livers for dissection planes for transplantation, reported the following (Table 19-10).

. . .Our anatomical study suggests that cutting plane A (in the umbilical fissure, just left of Rex’ sinus) necessitates the highest average total number of arterial, portal, and biliary anastomoses (6.4) for a viable (left) graft in liver transplantation using SG [split grafting] or LRG [living related grafting] techniques. Cutting plane B [in the umbilical fissure, through Rex’ sinus, by a longitudinal section of the left portal vein wall] reduces this number significantly (4.2). Both planes have the advantage of creating a small wound surface in the liver at the place of resection. Both cutting planes leave segment IV attached to the right liver half (SG) or to the donor (LRG), including a volume reduction of only two small segments (segments II and III), but transection of arterial and/or biliary branches to segment IV in 17% and 20%, respectively, limited the number of viable segments IV. Plane B requires the additional reconstruction of the left portal vein (Rex’ sinus) to ensure sufficient portal blood flow to segment IV. Cutting plane C (in the liver hilum, just left of the arterial, portal, and biliary bifurcations) has the clear advantage of the lowest average total number of arterial, portal, and biliary anastomoses for a viable (left) graft (3.1), but it also creates the largest wound surface in the liver and in the case of LRG it will reduce the amount of liver tissue left with the donor by three segments (II, III, and IV). However, using plane C, vasculobiliary branches to segment II and III can be denuded, by dissecting and removing the parenchyma of segment IV.188 Thereby one achieves sufficient length of these branches, thus facilitating the anastomosing procedure of the (left) graft in the recipient. In this way only one arterial, one portal, and one biliary anastomosis of branches with acceptable length and diameter remain. In conclusion, cutting plane C, in the liver hilum seems to be the best option to split a liver into two parts for transplantation purposes using SG or LRG techniques. When using this plane, a relatively large wound surface is created and the functional liver mass in the living donor is reduced by segments II, III, and IV. In the clinical setting this plane has proven to be a usable one, regarding several reports.188-190

Table 19-10. Average Number of Arterial, Portal, Biliary, and Total (= A + P + B) Anastomoses (±SD; Range) to Be Made at Three Different Cutting Planes in the Left Liver to Create a Viable (Left) Graft for SG and LRG Purposes

  Average Number of Anastomoses (±SD; Range)
Cutting Plane Arterial Portal Biliary Total
A 2.0 (±0.66; 1-4) 2.3 (±0.51; 2-4) 2.1 (±0.58; 1-3) 6.4 (±1.32; 4-12)
B 1.6 (±0.62; 1-4) 1.0 (±0.0) 1.6 (±0.52; 1-3) 4.2 (±0.90; 3-7)*
C 1.1 (±0.34; 1-2) 1.0 (±0.0) 1.0 (±0.0) 3.1 (±0.34; 3-4),‡ 
 

Note. (A) In the umbilical fissure, just left of Rex’ sinus; (B) in the umbilical fissure, through Rex’ sinus; (C) in the liver hilum, just left of the arterial, portal, and biliary bifurcations.

*vs A: P <.001.

 vs A: P <.001.

‡vs B: P <.001.

SG, Split graft; LRG, Living related graft.

Source: Kazemier G, Hesselink EJ, Lange JF, Terpstra OT. Dividing the liver for the purpose of split grafting or living related grafting: a search for the best cutting plane. Transplant Proc 1991;23:1545; with permission.

Blumgart et al.103 (whose colleagues included Czerniak) presented the anatomic entities involved in left extended hepatectomy. It is not within the scope of this book to describe the technique. The interested reader should refer to the book of Blumgart, Surgery of the Liver and Biliary Tract.191

Czerniak et al.192 proposed a direct approach to the hepatic veins in left hepatectomy. Their work is based upon Elias and Petty,193 Goldsmith and Woodburne,96 Banner and Brasfield,194 Baird and Britton,195 Depinto et al.,196 Nakamura and Tsuzuki,129 Castaing et al.,197 and Ou and Herman.198

Czerniak and colleagues advised that the anatomy of the veins in most instances is extrahepatic, but fixed to the left lobe of the liver and IVC by an avascular fibroareolar tissue. The authors advised, “once a plane is made between them and the liver, their true extrahepatic nature is disclosed.”192

The authors have seen this avascular tissue in the laboratory covered occasionally by a very thin stroma of hepatic tissue. This is confusing for the surgeon. Of course, Czerniak et al.182 emphasized this dissection in vivo.

Nery et al.199 studied the surgical anatomy and blood supply of the left biliary tree and the use of the lateral segment of the left lobe for transplantation, which is quite adequate for living donation. Their study demonstrated the following.

 

The hepatic arteries had the usual origin (Table 19-11).

The left bile duct and its tributaries did not receive any contributions from the portal system.

The left biliary tree had 13 variations. In 85.9%, the left hepatic duct was long; in 14.1%, it was very short (Fig. 19-73).

The left hepatic artery was the main and only artery of the lateral segment of the left lobe.

The surgeon must avoid entering the hilar plate too close to the bile duct wall.

Angiographic studies are essential to verify the arterial anatomy.

Table 19-11. Extra-Hepatic Segmental Arteries to the Left Hepatic Lobe According to Origin. Multiple Branches to a Single Segment Are Underlined

n  Origin Segmental Branches
36 LHA II, III, IV
16 LHA II, III
RHA IV
07 LHA II, III, IV, IV
06 LHA II, III, III, IV
05 LHA II, III, III
RHA IV
01 LHA II, II, III, IV
01 LHA II, II, II, III, IV
01 LHA II, II, II, III, III, IV
01 LHA II, III, III, IV, IV
01 LHA II, III, IV
RHA IV
01 LHA II, III
RHA IV, IV
01 LHA III
RHA II, IV
01 LHA II, II, III, III
RHA IV
Total: 78    

LHA, Left hepatic artery; RHA, Right hepatic artery.

Source: Nery JR, Frasson E, Rilo HLR, Purceli E, Barros MFA, Neto JB, Mies S, Raia S, Belzer FO. Surgical anatomy and blood supply of the left biliary tree pertaining to partial liver grafts from living donors. Transplantation Proc 1990;22: 1492; with permission.

Fig. 19-73.

Morphologic patterns of the extra-hepatic left biliary tree. Patterns A to H show a long left hepatic duct (85.9%), while I to M have a very short or absent left hepatic duct (14.1%). Morphologic identification previous to dissection will help to avoid injury to segmental ducts during graft resection. Numbers represent the number of specimens that contained the depicted pattern in a study of 78 livers. (Modified from Nery JR, Frasson E, Rilo HLR, Purceli E, Barros MFA, Neto JB, Mies S, Raia S, Belzer FO. Surgical anatomy and blood supply of the left biliary tree pertaining to partial liver grafts from living donors. Transplantation Proc 1990;22:1492; with permission.)

Couinaud and Houssin200 reported that blind partition of the right and left lobes to obtain two transplants is problematic because of left arterial and right ductal variations. These authors advised the following procedures.

 

Arteriography and cholangiography prior to surgery for mapping and protecting arterial and biliary networks

The following three surgical maneuvers

 

– Resection of segment IV when arterio-biliary duplications are present

– Attribution of the common hepatic artery at its duplication

– Partial attribution of the common hepatic duct at the side of the biliary duplication

Couinaud,201 in a calculation spreading to six digits, showed the “vanity” of attempting to classify the multiple variations of the right ductal system, and advised cholangiography. In a discussion appended to that article, Hureau reminds the hepatic surgeon to search beyond the “ideal” and “average” subject of the textbook to best operate on a given patient’s own “personal anatomy.” Houssin and colleagues (including Couinaud)202 reported similar findings.

Portography or ultrasonography to detect absence of portal vein bifurcation has been used by Couinaud.199 He reported five occurrences of this anomaly (1.9 percent frequency). Three figures (Figs. 19-74, 19-75, 19-76) demonstrate this rare anomaly.

Fig. 19-74.

Diagram of liver without portal bifurcation as observed by Couinaud. (Modified from Couinaud C. Absence de la bifurcation porte. J Chir (Paris) 130(3):111-115, 1993; with permission.)

Fig. 19-75.

Views of liver without portal bifurcation as observed by Agossou-Voyème. HG, left hepatic segment; HM, middle hepatic segment; HD, right hepatic segment. (Modified from Couinaud C. Absence de la bifurcation porte. J Chir (Paris) 130(3):111-115, 1993; with permission.)

Fig. 19-76.

Liver without portal bifurcation as observed by Hardy. UV, umbilical vein; IVC, inferior vena cava; GB, gallbladder; PV, portal vein; PP, principal plane. (Modified from Couinaud C. Absence de la bifurcation porte. J Chir (Paris) 130(3):111-115, 1993; with permission.)

Characteristically, portal vein bifurcation absence manifests with a “huge portal ring.”203 The large vein turns toward the right. After reaching the umbilical fissure, it sends the usual branches, ending at the caudate lobe. Thus, there is no left portal vein. The author advises total vascular bypass, skeletonization of the portal vein, and resection. Another technique consists of deep interruption of the portal stem in the hilum, division of the main portal fissure at the right margin of the middle hepatic vein, and transection of the transverse portion of the portal ring.

In a further publication, Couinaud204 stated that partition of the right and left lobes maintains segment IV’s association with the right lobe. However, this interrupts its portal vessels springing from the left portal pedicle. In a large series, he reported a 12.15 percent rate of preservation of the bile ducts. The segment had a good blood supply from the segmental artery (originating from the right hepatic stem) in 10.75 percent. The author also stated that disruption of both arterial and portal branches produces a potentially fatal necrosis of segment IV (a “sword of Damocles”). According to Couinaud, the segment should be resected, since its survival is rarely possible. He terms maltreatment of segment IV in liver transplantation “un scandale”204 in the ancient Hebrew sense of “stumbling block.” Couinaud’s philosophy of transplantation is illustrated in Figures 19-77, 19-78, 19-79, and 19-80.

Fig. 19-77.

Modalities of bipartition. A, Right liver-left liver bipartition. The inferior vena cava is conserved on the right transplant; the left hepatic vein (with a cuff of inferior vena cava, if necessary, occluding the orifice with a venous patch graft) drains the left transplant. The caudate lobe is usually sacrificed. The division is performed along the main portal fissure. B, Right liver-left lobe bipartition. Segment IV is amputated. The division is performed along the umbilical fissure. C, Right lobe-left lobe bipartition is prohibited. The portal elements of segment IV (shown with dotted shading) are derived from the left paramedian pedicle situated in the inferior part of the umbilical fissure and are interrupted when segment IV remained attached to the right liver, resulting in necrosis of this segment. (From Couinaud C. (A “scandal”: segment IV and liver transplantation). (French) J Chir (Paris) 1993;130:443; with permission.)

Fig. 19-78.

Portal veins of segment IV. a, Inferior view, anterior margin of the liver upward. b, Superior view. c, Sagittal section, anterior margin of the liver to the left. d, Inferior view. A deep posterior vein arises from the left portal vein. The separation of segment IV from the left portal pedicle interrupts all portal branches. (Modified from Couinaud C. (A “scandal”: segment IV and liver transplantation). (French) J Chir (Paris) 1993;130:443; with permission.)

Fig. 19-79.

Biliary canals of segment IV. a, The canal enters near the upper biliary confluent. b, The canal terminates in the upper confluent. c, The canal becomes the primary pathway. Sectioning the left hepatic canal to the left of the segment IV canal preserves the biliary tree of the right lobe. (Modified from Couinaud C. (A “scandal”: segment IV and liver transplantation). (French) J Chir (Paris) 1993;130:443; with permission.)

Fig. 19-80.

The segment IV artery arises from the right hepatic artery. a, The main artery vascularizes the right lobe after right-left partition (10.75 percent incidence). b, Preservation of both arterial and biliary duct function after right-left partition occurs in only 2.15 percent of livers. (Modified from Couinaud C. (A “scandal”: segment IV and liver transplantation). (French) J Chir (Paris) 1993;130:443; with permission.)

Couinaud’s paper “Surgical approach to the dorsal section of the liver,”205 painstakingly explains why the triangular ligaments, the coronary ligament, and the inferior vena cava present “formidable but illusory barriers,” and is a classic. We advise all hepatobiliary surgeons to familiarize themselves with its contents.

Couinaud,206 the patriarch of intrahepatic anatomy, reported variations in liver morphology and vasculobiliary elements (Figs. 19-81, 19-82, 19-83, 19-84, and 19-85). We quote Couinaud’s summary in toto.

Fig. 19-81.

Upper: Type (II+III) and IV left arterial or biliary distribution is shown in a through c. a, The elements of segments II and III have a common trunk into which drain the elements of segment IV. When the latter are close to the bifurcation, the bile duct or left hepatic artery is short. Such a left-sided distribution was observed in 36 out of 93 cases for the artery and in 69 out of 93 cases for the bile duct. b, The element of segment IV drains into the right-left bifurcation or lower down, in the main duct, resulting in duplication of the left elements. This distribution was observed in 44 out of 93 cases for the artery and 8 out of 93 cases for the bile duct. In 5 out of 93 cases, the artery of segment IV was derived from the right artery and/or bile duct for a left transplant which, in this case, is the left lobe. c, A left hepatic artery, arising from the left gastric artery and supplying the left lobe, constitutes this type of duplication: a left liver transplant is obtained by collecting the celiac trunk (which is excluded in vivo), or a left lobe transplant is obtained by amputating segment IV: 16 out of 93 cases. Lower: Type (III+IV) and II left arterial or biliary distribution is shown in a through c. a, The elements of segments III and IV have a common trunk into which drain the elements of segment II. When left cut is short: this distribution was observed in 5 out of 93 cases for the artery and in 14 out of 93 cases for the bile duct. b, The element of segment II drains into the bifurcation or lower down, in the main duct, resulting in duplication of the left elements: observed in 2 out of 93 cases for the bile duct. Amputation of segment IV does not allow a single artery or bile duct to be obtained for a left lobe transplant and this type of distribution excludes in vivo transplant collection. c, A left hepatic artery, arising from the left gastric artery and only supplying segment II, constitutes this type of duplication: 5 out of 93 cases. (From Couinaud C. Anatomie intra-hépatique: application â la transplantation du foie. Ann Radiol 37(5):323-333, 1994; with permission.)

Fig. 19-82.

Left hepatic artery derived from the left gastric artery. a, Supplying the whole left liver = solitary artery (5 out of 93 cases). b, Supplying the left lobe = type (II+III) and IV duplication (16 out of 93 cases). c, Supplying the left lobe and part of segment IV (1 out of 93 cases). d, e, Only supplying segment II = type (III+IV) and II duplication (7 out of 93 cases). f, Anastomosed with the normal middle hepatic artery (2 out of 93 cases). (From Couinaud C. Anatomie intra-hépatique: application â la transplantation du foie. Ann Radiol 37(5): 323-333, 1994; with permission.)

Fig. 19-83.

Right hepatic artery arising from the superior mesenteric artery or celiac trunk. a, Right hepatic artery according to the classical definition. b, A right hepatic artery arising from the superior mesenteric artery may ascend anterior to the portal trunk. c, A right hepatic artery arising from the celiac trunk may cross over behind the portal trunk (according to Michels, this is always the case when the celiac trunk gives two branches to the liver). (Modified from Couinaud C. Anatomie intra-hépatique application â la transplantation du foie. Ann Radiol 37(5):323-333, 1994; with permission.)

Fig. 19-84.

The surgeon’s 3 assets. A) The surgeon’s first asset: resection of segment IV. In the case of a type (II+III) and IV duplication of a left element (a), resection of segment IV results in a left lobe with a single pedicle (b). This resection may also be performed exclusively to reduce the volume of an excessively large left liver for a child (c). In a type (III+IV) and II duplication, resection of segment IV does not allow a single pedicle to be obtained for the left lobe, but IV is possible (d). B) The second asset: the common hepatic duct. (a and a’) A segment of common hepatic duct is retained on the side of the duplication. On the right side, a double anastomosis onto a jejunal loop or, when possible, a side-to-side biliary anastomosis may be preferred (b and b’). C) The third asset: common hepatic artery. The common hepatic artery is retained on the side of an arterial duplication (b) or triplication (c). (Modified from Couinaud C. Anatomie intra-hépatique: application â la transplantation du foie. Ann Radiol 37(5):323-333, 1994; with permission.)

Fig. 19-85.

Tripartition of the liver. a, Right lateral sector with lateral pedicle in its sheath and the inferior vena cava. The right hepatic vein is in the right portal fissure. Below diagram “a”: right lateral pedicle. b, Right paramedian sector with the right portal pedicle in its sheath and the middle hepatic vein. The middle hepatic vein is in the principal portal fissure. Below diagram “b”: diagram showing procurement of the right portal pedicle. c, Left lobe with left portal pedicle and left hepatic vein. (Modified from Couinaud C. Anatomie intra-hépatique: application â la transplantation du foie. Ann Radiol 37(5):323-333, 1994; with permission.)

In transplantation of the whole liver, the variable shape of the organ can exceptionally be the source of difficulties, as in the rare cases of situs inversus. Arterial variants may be the source of great difficulties. Among the biliary variants, the low junction of the right and left hepatic ducts in the main portal pedicle, and especially the cysto-hepatic ducts (entrance of a right duct into the gallbladder or the cystic duct) are particularly important, with a frequency ranging from 2% to 15% of the cases. Right liver-left liver, or right liver-left lobe bipartition is now a well controlled technique. Right lobe, left lobe bipartition should never be per-formed. The left hepatic vein is attributed to the left transplant (left liver or left lobe). In case of duplication of the left vein, the terminal portion of the middle vein is attributed to the left transplant, and the continuity of the middle vein with the inferior vena cava must be reconstructed. The middle vein is always attributed to the right transplant. When the portal bifurcation is missing, usually bipartition is impossible. When the right portal vein is duplicated, the portal stem is attributed to the right liver. Duplications of right and left arteries and ducts make difficulties. A thorough preoperative investigation is necessary in case of a living donor. Cholangiography and arteriography on the back table are essential to achieve an ex vivo bipartition. The surgeon then disposes of three mano-euvres: resection of segment IV, attribution of a short segment of the main duct on the side of a biliary duplication, attribution of the main hepatic artery (or the celiac axis) on the side of an arterial duplication. In vivo harvesting of a left transplant (left liver or left lobe) is possible in 86% of cases, ex vivo is possible in 95.70% of cases. Tripartition of the liver is not yet a controlled technique.

Hepatic Resections

For our discussion of hepatic resections, Figures 19-86, 19-87, and 19-88 will serve as orientation. The triumph of hepatic surgery and anatomic resection of hepatic lobes and segments prompts us to quote Meyers,207 who employs a logical approach to remembering the segmental sections (Figure 19-88):

The following logic can be employed to remember the segmental sections: The caudate lobe is its own segment (segment I) and is located posteriorly. In a clockwise order beginning from the top, segments II and III determine the tissue left of the falciform ligament (i.e., the left lateral segment in the American system). Segment IV corresponds to the tissue between the falciform ligament and Cantlie’s line or the middle hepatic vein (and corresponds to the left medial segment). Segment IV is sometimes divided into part A, a superior part, and part B, an inferior part. Segments V, VI, VII, and VIII continue according to this clockwise labeling. The gallbladder fossa lies between segments IV and V. The figure depicts the internal vascular skeleton, which is confirmed with intraoperative ultrasonography.

Fig. 19-86.

Planes of transection of the liver for lobectomy and segmentectomy. Trisegmentectomy includes anterior and posterior segments of the right lobe and the medial segment of the left lobe. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Fig. 19-87.

The true lobulation and segmentation of the liver: diaphragmatic surface. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

Fig. 19-88

. Subsegmentation of the liver. Segment I is not shown. (Modified from Meyers WC. Segmental hepatic resection. In: Sabiston DC Jr. Atlas of General Surgery. Philadelphia: WB Saunders, 1994, p. 535; with permission.)

Except for the sulcus, which divides the lateral segments (II, III) and medial segment (IV) of the left lobe, the diaphragmatic surface of the liver gives little indication of its internal lobulation.

In resection, the following segments are removed:

 

Right hepatic lobectomy: V, VI, VII, and VIII (Fig. 19-89)

Left hepatic lobectomy: II, III, and IV (Fig. 19-90).

Left lateral segmentectomy: II and III (Fig. 19-91)

Right trisegmentectomy: IV, V, VI, VII, VIII and I (Fig. 19-92)

Several other combinations

Fig. 19-89.

Right hepatic lobectomy: shaded segments are removed. (Modified from Meyers WC. Segmental hepatic resection. In: Sabiston DC Jr. Atlas of General Surgery. Philadelphia: WB Saunders, 1994, p. 536; with permission.)

Fig. 19-90.

Left hepatectomy (left lobectomy): shaded segments are removed. A. Anterior view. B. Inferior view. (Modified from Bismuth H, Garden OJ. Regular and extended right and left hepatectomy for cancer. In: Nyhus LM, Baker RJ, eds. Mastery of Surgery, 2nd Ed. Boston: Little, Brown, 1992; with permission.)

Fig. 19-91.

Left lateral segmentectomy: shaded segments are removed. (Modified from Meyers WC. Segmental hepatic resection. In: Sabiston DC Jr. Atlas of General Surgery. Philadelphia: WB Saunders, 1994, p. 536; with permission.)

Fig. 19-92.

Extended right hepatectomy: shaded segments are removed. A. Anterior view. B. Inferior view. (Modified from Bismuth H, Garden OJ. Regular and extended right and left hepatectomy for cancer. In: Nyhus LM, Baker RJ, eds. Mastery of Surgery, 2nd Ed. Boston: Little, Brown, 1992; with permission.)

The basic plan of blood vessels within the liver is subject to many variations. Thus, preoperative aortic, celiac, or selective hepatic arteriography must be performed and the films studied carefully before attempting any surgical procedure. The main arterial trunk to the medial segment arises from the right hepatic artery and passes to the left across the midline in about 25 percent of individuals. Precede ligation of any arterial branch with manual occlusion and observation of the limits of color change in the tissue.

Because interlobar and intersegmental spaces are occupied by the hepatic veins (Fig. 19-93), it is necessary to transect the liver in a paralobular or parasegmental plane. Liver transection patterns are as follows.

 

Right of the middle vein for a right lobectomy

Right of the left vein for trisegmentectomy

Left of the right vein for a left lobectomy

Left of the middle vein for a lateral segmentectomy

Fig. 19-93.

Diagram of the intrahepatic distribution of the hepatic veins. Note that they are interlobular rather than lobular. C = caudate, L = left, M = medial, R = right. (Modified from Skandalakis JE, Gray SW, Rowe JS Jr. Anatomical Complications in General Surgery. New York: McGraw-Hill, 1983; with permission.)

This is especially important in the true interlobar (umbilical) fissure, where vessels and bile ducts may lie in the fissure and return to the medial lobe more distally.

Right Lobectomy

For a right lobectomy or for a trisegmental lobectomy208,209 (“extended” right lobectomy210,211), use a right subcostal incision. It may be continued upward into the thorax or paraxiphoid or to the left, if necessary.

Incise the right triangular and coronary ligaments so that the right lobe may be retracted. Divide all ligamentous attachments of the liver to allow complete mobilization and visualization of all hepatic structures. In a “true” right or left lobectomy, the gallbladder must be sacrificed.

Dissection begins at the hilum. Ligate branches of the hepatic artery, portal vein, and bile duct of the lobe to be removed, and preserve the interlobar hepatic veins. Use blunt dissection throughout.

The line of the interlobar fissure (line of Rex, median fissure) extends from the gallbladder fossa below to the inferior vena cava above. The dissection must pass to the right of the middle hepatic vein to preserve drainage of segment IV (Fig. 19-89). Ligate the right hepatic vein extrahepatically before transection of the liver.129

Left Lobectomy

If the left lobe is to be resected, ligate the left hepatic artery, portal vein, and bile duct. Sectioning of the triangular ligament permits mobilization of the left lobe. Transection should follow a line from the left side of the fossa of the gallbladder to the left side of the fossa of the inferior vena cava (Fig. 19-94). Expose and ligate the left and middle hepatic veins within the liver or extrahepatically at the vena cava after ultrasonic confirmation of the precise anatomy.

Fig. 19-94.

Right trisegmentectomy: shaded segments are removed. (From Meyers WC. Segmental hepatic resection. In: Sabiston DC Jr. Atlas of General Surgery. Philadelphia: WB Saunders, 1994, p. 536; with permission.)

In most cases, the left and middle hepatic veins form a common trunk before emerging from the liver.194,212 It may be best to ligate the hepatic veins at the end of the dissection to be sure of ligating only the veins from the resected segments.213 A left resection may be lobar, segmental, or even wedge-shaped for a superficially located tumor. Povoski et al.214 found extended left hepatectomy “a viable resectional technique for large, strategically placed left-sided and central hepatic lesions that extend rightward to involve the right anterior sectorial portal pedicular structures.”

Left Lateral Segmentectomy

A left lateral segmentectomy (Fig. 19-91) consists of the removal of segments II and III. These segments are lateral to the falciform ligament. Segment IV remains in situ.

Trisegmentectomy

A right “extended” lobectomy (trisegmentectomy) (Fig. 19-92) is similar, but the liver is transected just to the right of the falciform ligament. The middle hepatic vein must be ligated, since the medial segment is to be removed. Take extreme care to preserve the left hepatic vein, as the middle vein typically joins it prior to its junction with the vena cava.

Mesohepatectomy

Wu et al.215 reported that even though mesohepatectomy (removal of segments IV, V, and VIII) is time-consuming, its advantages justify its use for selected patients with centrally located large hepatocellular carcinoma.

Liver Resection and Trauma

The treatment of traumatic liver injury has seen rapid evolution since the early 1980s. In 1989 the American Association for the Surgery of Trauma (AAST) developed the liver injuries scale now in use216 (Table 19-12). Seventy to ninety percent of liver injuries are grade I or II and may be managed nonoperatively. The utility of CT scanning in liver trauma cannot be overstated. Patients with subcapsular or intrahepatic hematomas who previously might have undergone exploration can now be safely managed with close observation and serial CT scans.

Table 19-12. Liver Injury Scale (1994 Revision)

  Gradea 
 
Injury Description
I Hematoma Subcapsular, <10% surface area
Laceration Capsular tear, <1 cm parenchymal depth
II Hematoma Subcapsular, 10-50% surface area; intraparenchymal, <10 cm in diameter
Laceration 1-3 cm parenchymal depth, <10 cm in length
III Hematoma Subcapsular, >50% surface area or expanding; ruptured subcapsular or parenchymal hematoma
Intraparenchymal hematoma > 10 cm or expanding
Laceration >3 cm parenchymal depth
IV Laceration Parenchymal disruption involving 25-75% of hepatic lobe or 1-3 Couinaud’s segments within a single lobe
V Laceration Parenchymal disruption involving >75% of hepatic lobe or >3 Couinaud’s segments within a single lobe
Vascular Juxtahepatic venous injuries; i.e., retrohepatic vena cava/central major hepatic veins
VI Vascular Hepatic avulsion

aAdvance one grade for multiple injuries, up to grade III.

Source: Moore EE, Cogbill TH, Jurkovich GJ, Shackford SR, Malangoni MA, Champion HR. Organ injury scaling: spleen and liver (1994 revision). J Trauma 1995;38:323-324; with permission.

Fang et al.217 reported that the presence of pooling contrast material within the hepatic parenchyma on computed tomography indicates active bleeding. Angiography should help in the decision whether to perform emergency exploratory laparotomy.

Pursuant to progress in prehospital care, patients often arrive in extremis but alive with enormous hepatic injuries. This has led to a resurgence in the use of perihepatic packing for the early management of complex liver injuries.218-220 Packing and reexploration work best when:

 

Used early in an operation

The patient is cold, coagulopathic, and needs further resuscitation prior to undertaking a complex hepatic repair, or

A specific injury has been identified that will require complex repair but the patient is coagulopathic

Hepatic resection is safe when performed electively. Formal hepatic resection for trauma, however, carries a high mortality rate. Cogbill and associates reported a rate of formal hepatic resection of 0.89 percent with a mortality rate of 58 percent,221 though other authors have reported lower mortality rates.222,223 In the Hollins and Littell series of 281 patients, 42 (14 percent) underwent hepatic resection and 83 percent of those underwent resectional debridement.224 The mortality for the entire group was 21 percent.

Extensive experience by American trauma surgeons indicates that formal hepatic resection for trauma is rare. Resectional debridement is more common and is often required to approach the site of a specific injury. The finger fracture technique is useful in this approach. Portal occlusion is safe in otherwise healthy trauma patients for up to an hour. Madding and Kennedy112 proposed only the following two reasons for formal lobectomy in trauma. The reasons are:

 

Blunt or penetrating injuries resulting in extensive devitalization of a major portion of the right lobe

Damage to the hepatic veins or vena cava requiring right lobectomy for visualization and repair

Pachter et al.225 would modify these to the following cases:

 

Total destruction of normal hepatic parenchyma

Injury extensive enough to preclude perihepatic packing

Resection was performed by the injury itself and can be quickly completed using several additional clamps

Hepatic resection is the only method of controlling exsanguinating hemorrhage.

During the past decade numerous specialized techniques in the management of hepatic trauma have been developed. These are beautifully reviewed by Pachter and colleagues.225

Liver Resection for Cancer

Liver resection is the best therapy available for primary or metastatic lesions in the liver, and the only therapy with a chance for cure. The five-year survival rates for resection of liver-colorectal metastases are 25 to 39 percent with a current mortality rate from the operation of less than 5 percent.226-228 Five-year survival rates in resection for hepatoma range from 12 percent to 39 percent. The operative mortality rate is slightly higher because of the incidence of cirrhosis in patients with hepatoma.229 Mortality risk rises when factors such as progressive cholangitis, elevated serum creatine, elevated serum bilirubin, high operative blood loss and vena cava resection are found in combination.230 Palliative resection offers no benefit if curative resection cannot be performed.

The size ratio of future liver remnant to preoperative liver volume may relate to biochemical and clinical outcome parameters. In an excellent paper, Vauthey and colleagues231 found the correlation to be a useful method to evaluate response to portal vein embolization and a predictor of outcomes prior to extended liver resection.

Newer techniques, most significantly intraoperative ultrasonography, are critical for the safe performance of hepatic resection. Moreover, nonresectional techniques such as cryoablative therapy and microwave coagulation are under study and may offer significant advances in tumor ablation.

Bakalakos et al.232 reported that patients with unilobar metastatic disease and certain patients with bilobar hepatic metastasis can achieve longterm survival after undergoing surgical resection with tumor-free margins.

Another study by Bakalakos et al.233 found that patients with liver metastasis from colorectal cancer whose preoperative carcino-embryonic antigen level was 30 ng/mL are more likely to be resectable and have the longest survival. Wigmore et al.234 found no evidence to support a differential pattern of hepatic metastasis related to the location of the primary colorectal cancer.

D’Angelica et al.235 stated that patients with metastatic colorectal cancer who are disease-free 5 years after hepatic resection are likely to have been cured. These authors encouraged aggressive followup, including further surgery if recurrence takes place, because chances for longterm survival are good. The perspective of Bismuth and Majno236 must be added: “Today the limitation to survival in primary and metastatic liver cancer lies not in the surgical technique but in the difficulty of dealing with microscopic and extrahepatic disease.”

Weimann et al.237 reported that nuclear medicine helps differentiate hepatic hemangioma and focal nodular hyperplasia from adenoma, which assists the surgeon in determining the appropriateness of surgery.

Based on studies of adult rats, Smail et al.238 concluded that the organs responsible for increasing the levels of nitric oxide after trauma and hemorrhagic shock might be the liver and small intestine. They advised use of specific inhibitors for reduction of nitric acid.

To avoid the occurrence of postoperative liver failure, Miyazaki et al.239 advised limited resection of segments I and IV for hepatic hilar cholangiocarcinoma.

Roayaie et al.240 advised aggressive surgical approach with tumorfree margins in patients with intrahepatic cholangiocarcinoma.

Iwatsuki et al.241 stated that both hepatic resection and liver transplantation offer satisfactory longterm survival for hilar cholangiocarcinoma.

Scientific techniques are helping us in the operating room. Delbeke et al.242 reported the possibility of differentiation and evaluation of benign and malignant tumors of the liver by doing positron emission tomography using [18F] fluorodeoxyglucose. However, limitations of this evaluation include false-positive results in a minority of hepatic abscesses and false-negative results in a minority of hepatocellular carcinoma.

Hepatocellular carcinoma (HCC) is the most common solid organ tumor worldwide, responsible for more than 1 million deaths annually.243

We quote Bilimoria et al.244:

Death caused by HCC is rare beyond 5 years after resection of HCC in the absence of fibrosis or cirrhosis. The data suggest that chronic liver disease acts as a field of cancerization contributing to new HCC. These patients may benefit from therapies directed at the underlying liver disease.

However, Nakajima et al.245 state that repeat resection for recurrent HCC has a low disease-free survival rate.

Billingsley et al.246 recommended segmental hepatic resection for patients with metastatic neoplasms and hepatocellular carcinoma. A commentary by Meyers and Chari247 in the same issue about this description of the progress in hepatic resection by Billingsley et al. stated that they make it sound so clear and simple that it may encourage inexperienced surgeons to attempt it. Meyers and Chari remind surgeons that hepatic resection must be done by experienced hands.

Yamamoto et al.248 isolate and remove the caudate lobe of the liver by an anterior transhepatic approach by separating the hepatic parenchyma along the interlobar plane and anatomic identification of the right margin of the caudate lobe.

We quote from Azoulay et al.249:

The anterior approach is useful for massive liver resection. It minimizes the risk of tumor rupture with spillage into the peritoneal cavity and hemorrhage from freeing vascularized adhesions or damaging the right hepatic vein or the retrohepatic vena cava. It also avoids the need for rotation of the huge right liver toward the remnant liver, preventing warm ischemia of the latter use of congestion or pedicle torsion.

Yamamoto et al.250 treated a huge liver tumor involving all of the hepatic venous confluence and the inferior vena cava by in situ pedicle resection in a left trisegmentectomy of the liver with right hepatic vein reconstruction.

Midorikawa et al.251 stated that hepatectomy for the impaired liver is now as safe a procedure as for the normal liver, provided their overall guidelines are followed.

Twelfth rib resection as a posterior direct approach was used by Bosscha et al.252 to treat subphrenic abscesses in cases of failure of percutaneous drainage, abandonment of percutaneous drainage in view of a too high risk of perforation of adjacent organs, or contamination of the pleural space, or an inaccessible abdomen.

Guidelines for minimally invasive hepatic surgery for malignant processes were proposed by Katkhouda and Mavor253:

Open surgery is the treatment of choice when primary tumors are malignant, located posteriorly, or in proximity to major hepatic vasculature. Laparoscopic resection of liver metastases with a safety margin of 1 cm, when the total number is less than four, is not unreasonable and can be offered to patients without evidence of extrahepatic disease.

Minimally invasive adjuvant therapies for the treatment of primary and secondary malignant hepatic tumors may have clinical results which exceed conventional chemotherapy or radiation therapy. Radio-frequency ablation, microwave ablation, laser ablation, cryoablation, ethanol ablation, and chemoembolization are acceptable for nonsurgical patients and may one day challenge surgical resection as the treatment of choice for patients with limited hepatic tumors.254

Operative Management of Portal Hypertension

Numerous options are available for managing acute or refractory bleeding from esophageal varices. Factors including underlying liver disease, comorbid conditions, and the experience and expertise of the local physicians and surgeons determine the most appropriate therapies. Medical therapies include -blockers for prophylaxis and vasopressin or somatostatin infusion for acute bleeding. Endoscopic sclerotherapy or variceal banding can be used for either acute bleeding or to prevent rebleeding. Liver transplantation is the most radical and definitive therapy in appropriate candidates.

Distal Splenorenal Shunt

Surgical treatment of patients with bleeding varices or varices at risk to rebleed has changed in the past three decades. The side-to-side or end-to-side portacaval shunt was the primary option for portal decompression until the 1970s. Dean Warren and his colleagues255-257 then developed the distal splenorenal shunt (DSRS). This procedure selectively decompresses the esophageal and gastric varices while maintaining antegrade portal perfusion. This procedure has undergone numerous refinements and long term evaluation. The re-bleeding rate at three years to five years following DSRS is approximately six percent. The operative mortality in series from the past five years ranges from zero percent to 15 percent. Encephalopathy, extremely common after portacaval shunt, occurs in only 15 percent of patients and is typically easily controlled with restriction of protein intake and lactulose administration.

Small-Bore Portacaval H-Graft

The small-bore portacaval H-graft is formed using a reinforced 8-mm polytetrafluoroethylene (PTFE) graft between the portal vein and vena cava.258 It decompresses the portal vein less completely, but it decreases portal pressure and maintains antegrade flow to the liver. This procedure is technically easier than DSRS, although the rate of flow reversal in the portal vein is higher and perioperative complications are similar.

Transjugular Intrahepatic Portasystemic Shunt

Transjugular intrahepatic portasystemic shunt (TIPS)259 is the newest method of treating portal hypertension by shunting portal blood to the systemic circulation. Using the jugular vein, a wire passes from the hepatic vein into a portal vein branch that is then dilated and stented with an expandable metal stent. This procedure forms a functional side-to-side portacaval shunt that decompresses the portal vein and, therefore, the esophageal and gastric varices. TIPS shows a success rate of at least 90 percent in reducing the portal vein-to-hepatic vein gradient to less than 12 mm Hg. The early re-bleeding rate is roughly equivalent to that of DSRS and significantly lower than sclerotherapy. Follow-up periods of 18 months to 24 months, however, show high rates (40 percent to 70 percent) of shunt stenosis or thrombosis.260

A randomized clinical trial is needed to determine the exact role of TIPS in the armamentarium of portal decompression techniques. At present the procedure is not recommended for definitive portal decompression in patients with Child A cirrhosis and good hepatic function256 (Table 19-13). The technique is currently best suited for patients with Child C cirrhosis who are waiting for liver transplantation or who bleed from the varices but are at high risk for a surgical procedure. Patients with Child B cirrhosis occupy an intermediate category and the best longterm treatment for these patients remains unknown.

Table 19-13. Child’s Classification of Hepatic Reserve

Criteria Good A Moderate B Poor C
Serum bilirubin (mg%) <2.0 2.0-3.0 >3.0
Serum albumin (g%)  >3.5 3.0-3.5 <3.0
Ascites None Easily controlled Poorly controlled
Encephalopathy None Minimal Advanced, “coma”
Nutrition Excellent Good Poor, muscle wasting

Source: Richardson JD, Gardner B. Gastrointestinal bleeding. In: Polk HC Jr, Gardner B, Stone HH. Basic Surgery, 4th Ed. St. Louis: Quality Medical Publishing, 1993; with permission.

Hepatic Injuries

Demetriades et al.261 stated that selected patients with isolated grades I and II gunshot injuries to the liver can be managed nonoperatively.

Moore262 wrote that the previously cited study by Demetriades et al. adds useful data to support selective nonoperative management of gunshot wounds to the liver. He contends, however, that candidates for observation are infrequent and that surgeons using this approach must be aware of the risks and have the resources to address potential complications.

Anatomic Complications

Complications of Some Diagnostic Procedures

Open (Wedge) Biopsy

A wedge biopsy can be obtained through a mini-laparotomy or during another surgical procedure. Bleeding is the only complication, and it is easily controlled.

Percutaneous (Needle) Biopsy

The colon is the organ most frequently perforated during percutaneous biopsy. In such a procedure, pancreatic and renal tissue occasionally appear. Pneumothorax is said to occur once in about 800 biopsies.263 A summary of the possible complications is presented in Table 19-14.

Table 19-14. Complications of Percutaneous (Needle) Biopsy

Organ Injury  Result 
Colon Peritonitis1 
 
Right kindey Peritonitis1 
 
Pancreas Pancreatitis
Diaphragm Pain
Lung or pleura Pneumothorax,6 hemothorax 
 
Gallbladder or bile ducts Bile peritonitis,3 hemobilia 
 
Hematoma between chest wall and liver Hemorrhage
Intercostal artery or veins Hemorrhage4 
 
Intrahepatic Injury   
Hepatic artery, vein or portal vein Hemorrhage, hematoma2 
 
Bile ducts Bile peritonitis
General Complications   
  Infections of needle track
  Needle fracture
  Pain5 
 
  Shock
 

1. Injury to abdominal viscera is rare (Terry, 1952).

2. Three cases of intrahepatic hematoma have been described by Rainer (1974).

3. Six cases have been reported by Madden (1961).

4. Hemorrhage is the most frequent complication and the major cause of death following needle biopsy.

5. Pain is more frequently associated with the use of the Vim-Silverman needle (20 percent) than with the Menghini needle (3.2 percent), though the specimen is smaller with the latter instrument (Schwartz, 1964).

6. One case in 2000 biopsies (Brown, 1961).

References

Brown CH. Needle biopsy of the liver. Am J Diag Dis 6:269, 1961.

Madden RE. Complications of needle biopsy of the liver. Arch Surg 83:778, 1961.

Rainer DR, van Heertum RL, Johnson LF. Intrahepatic hematoma: A complication of percutaneous liver biopsy. Gastroenterology 67:284, 1974.

Schwartz SI. Surgical Diseases of the Liver. New York: McGraw-Hill, 1964.

Terry RB. Risks of needle biopsy of the liver. Br Med J 1:1102, 1952.

Hemorrhage and peritonitis are the most frequent complications of needle biopsy, with intrahepatic hematoma and perforation of organs in addition to the colon also possible.

Millward-Sadler and Whorwell264 have reported mortality rates in several large series beginning in the 1950s. In 1992, they estimated rates to be approximately 0.01 percent (one death per 10,000 biopsies), whereas some years earlier they had found the rate to be 0.1 percent (one death per 1,000 biopsies). In 1994, Schwartz265 concluded that the overall mortality rate was 0.8 percent, with pain, pneumothorax, hemorrhage, and bile peritonitis the most common complications. Among uncommon complications is needle fracture during biopsy.266,267

Anatomic Complications of Liver Surgery

Vascular Injury

Hepatic Vein

When a hepatic vein occludes, it might be anticipated that the tissue drained by it would demand resection. Mays113 stated that this is unnecessary in humans because of the anastomoses between the left and right hepatic veins. He cited two reports of hepatic vein ligation when most of the affected liver survived. In one patient, the left hepatic vein was ligated;268 in the other, the middle and left hepatic veins were ligated.196 Segmental hepatic vein ligation without hepatic resection avoids the tedious construction of a vena caval shunt, a procedure usually requiring the facilities of a large medical center and a skilled surgeon. In experienced hands, intraoperative ultrasonography and detailed anatomic knowledge can prevent the vast majority of hepatic venous occlusions.

Portal Vein

The umbilical portion of the portal vein lies within the umbilical fissure. In a left lateral segmental resection, incise the liver 1 cm to the left of the fissure.

Ligation of the left or right portal vein following injury to the liver has been successful in some patients,269-272 but the mortality rate from portal vein injuries is still about 50 percent.273 Stone274 reported 15 survivors among 20 patients undergoing emergency portal vein ligations.

Pachter and associates275 feel that portal vein ligation, even with its risk of portal hypertension and intestinal infarction, may be safer than immediate shunting procedures, which risk encephalopathy. “Severe hepatic trauma limited to one lobe of the liver is the main indication for ligating both the portal vein and hepatic artery supplying the injured lobe. The artery should be ligated first. If this fails to stop hemorrhage, then the branch of the portal vein to that lobe should be ligated.”113 Resectional debridement may then be necessary to remove devitalized tissue.

Hepatic Artery

If possible, repair inadvertent ligation of a lobar hepatic artery. With good supportive care, the patient usually survives even if blood flow cannot be restored. Kim and colleagues276 found 50 deaths among 322 hepatic artery occlusions. Twenty-seven deaths were from accidental ligation during major operations. Ligation was the direct cause of death in only 12 cases. Using these figures, the mortality could be said to be less than 4 percent.

The degree of hepatic ischemia depends on the location of the hepatic artery ligation. Ligation proximal to the gastroduodenal artery or even proximal to the origin of the right gastric artery will probably not result in liver ischemia. In some individuals, if the ligation is distal to the right gastric artery, an aberrant hepatic artery may provide the sole supply of oxygenated blood to the liver. Ligation of the left hepatic artery seems to carry a higher mortality rate than does ligation of the right artery. No valid reason is known.

The surgeon performing a formal lobectomy must remember that in as many as 25 percent of individuals, the left medial segmental artery (segment IV) arises from the right hepatic artery.110 Sectioning of the right hepatic artery for a right lobectomy could result in arterial ischemia of the left medial segment.

Summary of Ligation of Hepatic Vessels

Hepatic Veins

 

Lobar or segmental hepatic vein ligation is feasible.

Hepatic resection following ligation of a hepatic vein is not always necessary.

Portal Vein

 

Portal veins may be ligated without fatality. The hepatic sinusoids of the adjacent lobules provide intersegmental communication. There are few true anastomoses between venous branches.

Reduction in portal blood flow increases hepatic artery blood flow. The reverse is not true.

Atrophy follows portal vein ligation.

Ligation of both lobar hepatic artery and portal vein results in atrophy without necrosis.

Following a radical pancreaticoduodenal resection, the portal vein should not be ligated. Portal blood flow must be restored by a shunt or a replacement graft.

Hepatic Artery

 

Hepatic arteries are not end arteries in vivo. Ligation of a right or left hepatic artery results in translobar and subcapsular collateral circulation within 24 hours.

After proximal ligation of the common hepatic artery, the right gastric and gastroduodenal arteries will maintain hepatic blood flow.

Hepatic artery ligation is well-tolerated. Death following such ligation is not usually the result of the artery ligation.

Cholecystectomy must always accompany hepatic artery ligation.

Organ Injury

Bile Ducts

Accidental section of a segmental bile duct requires immediate repair, proximal and distal ligation of the severed duct, or resection of the segment. Ligation of a segmental bile duct produces jaundice, hypocholic stools and urine, and enlargement of the lobe of the liver on the side of the obstruction.277 Braasch and colleagues278 reported atrophy of the obstructed segment. Possibly initial hypertrophy is followed later by atrophy. It is curious that unilateral lobar obstruction produces jaundice, while unilateral lobectomy does not. One would expect the unaffected lobe to prevent the occurrence of jaundice.

Lo et al.279 recommended the following for avoiding biliary complications after hepatic resection: 1) Preresection cholangiography for left-sided hepatectomy, and 2) early surgical intervention for leakage of the common bile duct. Tables 19-15 and 19-16 demonstrate the incidence and sites of complications.

Table 19-15. Types of Hepatic Resection and Incidence of Biliary Complications

Operation No. of Patients (No. of Concomitant Caudate Resections) Biliary Complication, No. of Patients (%)
Major*    
  Right hemihepatectomy 118 (9) 11 (9.3)
  Right extended hepatectomy 32 (2) 1 (3.1)
  Right trisegmentectomy 30 (7) 2 (6.7)
  Left hemihepatectomy 32 (4) 6 (18.8)
  Left extended hepatectomy 14 (2) 3 (21.4)
  Left trisegmentectomy 3 (0) 2 (66.7)
Minor 
 
   
  Left lateral segmentectomy 61 (0) 2 (3)
  Segmentectomy 25 (0) 0 (0)
  Subsegmentectomy 32 (0) 1 (3.1)

*Includes 229 patients.

Includes 118 patients

Source: Lo C-M, Fan S-T, Liu C-L, Lai ECS, Wong J. Biliary complications after hepatic resection: risk factors, management, and outcome. Arch Surg 133:156-161, 1998; with permission.

Table 19-16. Site of Biliary Leakage According to Different Types of Hepatic Resection

  Type of Resection, No. of Patients
Site Right-sided* Left-sided* Minor
Hepatic duct stump 4 2 0
Biloenteric anastomosis 1 3 0
Common hepatic duct 1 2 0
Raw surface of liver 1 1 0
T-tube insertion 1 0 0
Unknown 6 3 3
Total  14  11  3 

*Includes hemihepatectomy, extended hepatectomy, and trisegmentectomy.

Source: Lo C-M, Fan S-T, Liu C-L, Lai ECS, Wong J. Biliary complications after hepatic resection: risk factors, management, and outcome. Arch Surg 133:156-161, 1998; with permission.

Other Organs

Most of the organs of the upper abdomen are close enough to the liver that resection of that organ provides many opportunities for inadvertent injury.

Complications of DSRS, Portacaval H-Graft, and TIPS

Vascular Injury

 

The splenic vein has many branches draining the pancreas. Failure to carefully ligate these leads to significant bleeding. The splenic vein may be torn during this dissection, preventing its use.

Angulation, distortion, and tension are the chief dangers in forming the splenorenal or H-graft anastomoses.

Multiple vascular complications may occur during or following TIPS procedures. These include perforation or tearing of the portal vein or vena cava, formation of a portobiliary fistula with resultant hemobilia, or stent migration into the superior mesenteric vein with eventual thrombosis.

During exposure of the portal vein for portacaval H-graft, anomalous or variant hepatic arteries or collateral veins may be ligated. This can lead to segmental ischemia that might be well-tolerated in noncirrhotic patients, but dangerous or fatal in a patient with marginal hepatic reserve.

During DSRS, failure to adequately ligate retroperitoneal lymphatics when exposing the renal vein may cause chylous ascites. This may require drainage and may become infected.

Organ Injury

Segmental liver ischemia may follow accidental injury to an aberrant hepatic artery.

Surgical Anatomy of Liver Transplantation

The following description of preparation of the donor liver is anatomic rather than technical, and does not include the physiologic basis of the procedure. The description of donor total hepatectomy is based on the papers of Starzl and colleagues,280 Shaw and colleagues,281 Gordon and colleagues,282 Quinones-Baldrich and colleagues,283 and Ekberg and associates.284

Freeing and Preparing the Donor Liver

The following steps free the donor liver and prepare it for placement in the recipient (Fig. 19-95).

 

1. Make a long midline incision from the suprasternal notch to the symphysis pubis to provide maximum exposure.

2. Inspect the liver for good color and texture.

3. Look for anomalies of the extrahepatic blood vessels. Specifically, look for aberrant accessory or replacing hepatic arteries arising from the left gastric or the superior mesenteric artery. (See below for procedure in the presence of an aberrant right hepatic artery).

4. Dissect the celiac axis very close to the aorta if possible, with ligation and division of the left gastric and splenic arteries.

5. Ligate and divide the gastroduodenal and right gastric arteries.

6. Open the gallbladder and wash out the extrahepatic biliary tree. Remove the gallbladder, then mobilize and transect the common bile duct.

7. Locate the portal vein under the gastroduodenal artery. Isolate and clean the vein as far as the junction of the splenic and superior mesenteric veins.

8. Cannulate and ligate the splenic vein close to the spleen.

9. Locate and encircle the superior mesenteric vein. Divide the neck of the pancreas if necessary.

10. Ligate the inferior mesenteric artery.

11. Divide, cannulate, and ligate the aorta above the bifurcation.

12. Divide, cannulate, and ligate the inferior vena cava above the junction of the iliac veins.

13. Wash out the organs with cold preservation solution.

14. Ligate the lumbar vessels.

15. Ligate the superior mesenteric artery and vein.

16. Clamp the aorta as for a graft nephrectomy.

17. Detach the celiac axis from the aorta with an aortic patch or full aortic circumference (Fig. 19-96).

18. Dissect the suprahepatic vena cava free with a cuff of the caval hiatus of the diaphragm.

19. Cut the posterior attachments of the liver.

20. Ligate the right adrenal veins.

21. Remove the liver and ligate tributaries of the inferior vena cava.

Fig. 19-95.

Transplantation of the liver. In situ perfusion method of Starzl and associates. This is suitable for removal of liver and kidneys from the same donor. Rga = right gastric artery; Gda = gastroduodenal artery; Sa, Sv = splenic artery and vein; PV = portal vein; Smv = superior mesenteric vein. (Modified from Starzl TE, Hakala TR, Shaw BW Jr, Hardesty RL, Rosenthal TJ, Griffith BP, Iwatsuki S, Bahnson HT. A flexible procedure for multiple cadaveric organ procurement. Surg Gynecol Obstet 158:223, 1984; with permission.)

Fig. 19-96.

Liver transplantation in the presence of an aberrant blood supply to the donor liver. Shown is a right “accessory” artery arising from the superior mesenteric artery, a left “accessory” artery arising from the left gastric artery, and a “normal” common hepatic artery arising from the celiac trunk. A patch of donor aorta containing the origin of the celiac trunk and the superior mesenteric artery is placed in the wall of the recipient aorta. The donor superior mesenteric artery distal to the aberrant hepatic artery is anastomosed to the recipient hepatic artery. LHA, RHA = left and right “accessory” hepatic arteries; cd = common bile duct; ha = common hepatic artery; LGA = left gastric artery; sma, smv = superior mesenteric artery and vein; pv = portal vein; LRA, RRA = left and right renal arteries; ca = celiac axis; sa = splenic artery. (Modified from Gordon RD, Shaw BW, Iwatsuki S, Todo S, Starzl TE. A simplified technique for revascularization of homographs of the liver with a variant right hepatic artery from the superior mesenteric artery. Surg Gynecol Obstet 160:474, 1985; with permission.)

The operator must remember that the arterial supply is “abnormal” in almost half of patients encountered. The dictum must be accepted, whether right or wrong, that all hepatic arteries are end arteries and that accessory as well as replacing arteries must be preserved.

We can do no better than to use the words of Gordon and associates282 who describe their method for forming a common channel when the hepatic arterial supply arises from the celiac axis and the superior mesenteric artery:

If a left gastric branch to the left lobe can be seen and palpated in the gastrohepatic ligament lying beneath the left lobe of the liver, it can be preserved by dissecting the vessel back to its origin from the main left gastric artery which in turn is preserved to its origin from the celiac axis.

If a right hepatic artery arises from the superior mesenteric artery, it can be located by its pulsation posterior to the portal vein and common duct. Its origin from the superior mesenteric artery is usually found just beneath the splenic vein near its junction with the portal vein. Division of the splenic vein for insertion of a portal perfusion cannula also facilitates exposure for the superior mesenteric artery and the origin of a right hepatic branch. The superior mesenteric artery is dissected from its beginning at the aorta to at least one cm beyond the origin of the anomalous right hepatic artery. The origin of the celiac axis also is dissected clean at the aorta.

The technique of cold perfusion and preservation has been described. A patch of anterior aortic wall containing the origin of both the celiac axis and the superior mesenteric artery is removed. This preserves the entire hepatic arterial supply and is first in reconstruction of a common channel. As the patch is cut, the aortic origins of the renal arteries are noted and avoided. These are in close proximity to the origin of the superior mesenteric artery.

Components of Hepatic Transplantation

From a surgicoanatomic standpoint, Dodson285 divides the surgical components of hepatic transplantation into the following three areas.

 

Donor hepatectomy

Recipient hepatectomy

Implantation of donor liver

We advise very strongly that the student of hepatic transplantation study carefully the above-referenced excellent paper of Dodson.

Bismuth et al.189 reported that the liver can be divided into two hemilivers for transplantation. The line of division is the main fissure. The hemilivers are the right with segments V, VI, VII, and VIII, and the left with segments II, III, and IV. Bismuth and coworkers also advised resection of the caudate lobe (segment I).

Srinivasan et al.286 transplanted only segment III of the liver (monosegment liver transplantation) to six babies with liver failure, with an 83.3% success rate.

Couinaud’s Approach

Couinaud287 presented a simplified method for controlled left hepatectomy. In 1994,206 he discussed the intrahepatic anatomy in relation to transplantation. He emphasized variations in shape, arterial, and biliary variants, and the cystohepatic ducts. Couinard stated that right lobe/left lobe bipartition should never be performed. A left transplant (left liver or left lobe) should include the left hepatic vein. A right transplant should include the middle hepatic vein. Preoperative investigation should cover absence of portal bifurcation, duplication of the right portal vein, and duplication of both right and left hepatic arteries and ducts. The authors of this chapter strongly advise the study of these articles written by the father of segmental hepatic anatomy.

In 1995, Thompson et al.288 criticized the Couinaud technique of hepatic resection as presented in his 1985 article on controlled left hepatectomy.287 They considered this technique unsafe unless biliary anatomic variants are stringently excluded prior to right or left hepatic lobectomy.

Our comment is that embryology and anatomy must always be fellow travelers. Evaluation prior to surgery and in the operating room of every case must proceed without ANY acceptance of ANY assumption. This is essential! We owe as much to our patients and to Couinaud.

Hardy and Jones289 found hepatic artery anomalies in 38.5 percent of prospective donor livers in their sample. However, arterial anastomosis may be carried out successfully in transplantations from these livers.

Living-Related Donor Procedure

When reconstructing the hepatic vein on living-related donor liver transplantation patients, Egawa et al.290 advised wide end-to-side anastomosis between the donor hepatic vein and cuffs consisting of the recipient middle and left hepatic veins and an incision to the inferior vena cava.

Marcos et al.291 studied the anatomic variations of the right lobe in living donor transplantation:

Anatomical variations of the right lobe can be accommodated without donor complications or complex reconstruction. Previous transplantation and transjugular intrahepatic portosystemic shunt do not significantly complicate right lobe transplantation. Microvascular arterial anastomosis is not necessary, and vascular complications should be infrequent. Biliary complications can be minimized with stenting.

Pomfret et al.292 stress the need for careful evaluation of potential living donors, since significant donor morbidity is encountered even with careful selection.

Treatment of Postoperative Ascites

We quote from Cirera et al.293:

[M]assive ascites after liver transplantation is relatively uncommon but associated with increased morbidity and mortality and is primarily related to difficulties of hepatic venous drainage. Measurement of hepatic vein and atrial pressures to detect a significant gradient and correct possible alterations in hepatic vein outflow should be the first approach in the management of these patients.

Neuberger294 summed up the current status of liver transplantation:

One of the major challenges facing the transplant community is the shortage of donor organs: imaginative approaches to overcome this problem include more effective use of marginal donor livers, splitting livers and development of living related transplants. While advances have been made in the field of xenotransplantation, there remain many hurdles to be overcome before this approach can be introduced into human transplantation.

Treatment of Postoperative Stenosis

Azoulay et al.295 reported that postoperative stenosis of the portal vein after hepatic transplantation may be treated by balloon dilatation through an iliac vein.

 Read an Editorial Comment

References

1. Hippocrates. Tradition in Medicine. In: Lloyd GER (ed). Chadwick J, Mann WN (trans). Hippocratic Writings. New York: Viking Penguin, 1983, pp. 85-6.

2. Croisille Y, Le Douarin NM. Development and regeneration of the liver. In: De Haan RL, Urspung H, eds. Organogenesis. New York: Holt, Rinehart & Winston, 1965.

3. Lipp W. Die Entwicklung der Parenchymarchitektur der Leber. Verh Anat Ges 50:241-249, 1952.

4. Elias H. Origin and early development of the liver in various vertebrates. Acta Hepat 3:1-56, 1955.

5. Elias H. Appositional growth of the embyronic liver. Rev Int Hepat 14:317-322, 1964. [PubMed: 14194080]

6. Wilson JW, Groat CS, Leduc EH. Histogenesis of the liver. Ann NY Acad Sci 111:8-24, 1963. [PubMed: 14085884]

7. Bennett D. Modern views of embryonic development and differentiation. In: Javitt NB, ed. Neonatal Hepatitis and Biliary Atresia: An International Workshop. Bethesda: National Institutes of Health, March 21-23, 1977.

8. Sherer GK. Vasculogenic mechanisms and epithelio-mesenchymal specificity in endodermal organs. In: Feinberg RN, Sherer GK, Auerbach R. eds. The Development of the Vascular System. Basel: Karger, 1991.

9. Horstmann E. Entwicklung und entwicklungsbedingungen des intrahepatischen Gallengangsystems. Arch Entwicklungsmech Organ 139:363-392, 1939.

10. Healey JE Jr, Sterling JA. Segmental anatomy of the newborn liver. Ann NY Acad Sci 111:25-36, 1963. [PubMed: 14085851]

11. Van Damme JPJ, Bonte J. The branches of the celiac trunk. Acta Anat 122:110, 1985.

12. Sergi C, Adam S, Kahl P, Otto HF. The remodeling of the primitive human biliary system. Early Hum Dev 2000;58:167-178. [PubMed: 10936437]

13. Kiserud T, Rasmussen S, Skulstad S. Blood flow and the degree of shunting through the ductus venosus in the human fetus. Am J Obstet Gynecol 2000;182:147-153. [PubMed: 10649170]

14. Merrill GG. Complete absence of left lobe of liver. Arch Pathol 42:232, 1946.

15. Belton RL, VanZandt TF. Congenital absence of the left lobe of the liver: a radiologic diagnosis. Radiology 147:184, 1983. [PubMed: 6828725]

16. Kakitsubata Y, Kakitsubata S, Asada K, Ochiai R, Watanabe K. MR imaging of anomalous lobes of the liver. Acta Radiol 34(4):417-419, 1993.

17. Ozgun B, Warshauer DM. Absent medial segment of the left hepatic lobe: CT appearance. J Comput Assist Tomogr 16(4):666-668, 1992.

18. Morphett A, Adam A. Agenesis of the right lobe of the liver: diagnosis by computed tomography. Australas Radiol 36(1):68-69, 1992.

19. Klin B, Efrati Y, Vinograd I. Case report: selective occipital lobe hydrocephalus and agenesis of the left lobe of the liver in congenital myotonic dystrophy. Clin Radiol 46(4):284-285, 1992.

20. Fonkalsrud EW, Tompkins R, Clatworthy HW. Abdominal manifestations of situs inversus in infants and children. Arch Surg 92:791, 1966. [PubMed: 5934225]

21. Ion A, Tiberiu CG. Anatomical features of the liver in situs inversus. Acta Anat 112:353, 1982. [PubMed: 7113639]

22. Riedel BMKL. Uber den zungenformigen Fortsatz des rechten Leberlappens und seine pathognostische Bedeutung fur die Erkrankung der Gallenblase nebst Bemerkungen uber Gallensteinoperationen. Berlin Klin Wschr 25:577, 1888.

23. Reitemeier RJ, Butt HR, Bagenstoss AH. Riedel’s lobe of the liver. Gastroenterology 34:1090, 1958. [PubMed: 13548342]

24. Baum S, Locko RC, d’Avignon MB. Functional anatomy and radionuclide imaging: Riedel’s lobe of the liver. Anat Clin 4:121, 1982.

25. Cullen TS. Accessory lobes of the liver. Arch Surg 11:718, 1925.

26. El Haddad MJY, Currie ABM, Honeyman M. Pyloric obstruction by ectopic liver tissue. Br J Surg 72:917, 1985.

27. McGregor AL, Du Plessis DJ. A Synopsis of Surgical Anatomy, 10th Ed. Baltimore: Williams and Wilkins, 1969.

28. van der Reis L, Clark AG, McPhee VG. Congenital hepatomegaly. Calif Med 85:41, 1956.

29. Gillard JH, Patel MC, Abrahams PH, Dixon AK. Riedel’s lobe of the liver: fact or fiction? Clin Anat 11:47-49, 1998. [PubMed: 9445097]

30. Organ CH, Hayes DF. Supradiaphragmatic right liver lobe and gallbladder. Arch Surg 115:989, 1980. [PubMed: 7396709]

31. Mendoza A, Voland J, Wolf P, Benirschke K. Supradiaphragmatic liver in the lung. Arch Pathol Lab Med 110(11):1085-1086, 1986.

32. Bassis ML, Izenstark JL. Ectopic liver: its occurrence in the gallbladder. Arch Surg 73:204, 1956. [PubMed: 13354110]

33. Horanyi J, Fusy F. Nebenpankreas in der Gallenblasenwand. Zbl Chir 88:1414, 1963.

34. Davies JNP. Accessory liver in Africans. Br Med J 2:736, 1946.

35. Heid GJ, von Haam E. Hepatic heterology in the splenic capsule. Arch Pathol 46:377, 1948.

36. Fock G. Ectopic liver in omphalocele. Acta Paediat 52:288, 1963. [PubMed: 13945673]

37. Maresch R. A lymphangioma of the liver. Z Heilk 24:39, 1903.

38. Drachenberg CB, Papadimitriou JC, Rivero MA, Wood C. Distinctive case. Adult mesenchymal hamartoma of the liver: report of a case with light microscopic, FNA cytology, immunohistochemistry, and ultrastructural studies and review of the literature. [Review]. Mod Pathol 4(3):392-395, 1991.

39. Chau KY, Ho JW, Wu PC, Yuen WK. Mesenchymal hamartoma of liver in a man: comparison with cases in infants. J Clin Pathol 47 (9):864-866, 1994.

40. Wada M, Ohashi E, Jin H, Nishikawa M, Shintani S, Yamashita M, Kano M, Yamanaka N, Nishigami T, Shimoyama T. Mesenchymal hamartoma of the liver: report of an adult case and review of the literature. [Review]. Intern Med 31(12):1370-1375, 1992.

41. Shuto T, Kinoshita H. Yamada C, Hirohashi K, Shiokawa C, Kubo S, Fujio N, Kobayashi Y. Bilateral lobectomy excluding the caudate lobe for giant mesenchymal hamartoma of the liver. Surgery 113(2):215-222, 1993.

42. Ahrens EH Jr, Harris RC, MacMahon HE. Atresia of the intrahepatic bile ducts. Pediatrics 8:628, 1951. [PubMed: 14891320]

43. Krovetz LJ. Intrahepatic biliary atresia. J Lancet 79:228, 1959. [PubMed: 13665170]

44. Longmire WP. Congenital biliary hypoplasia. Ann Surg 159:335, 1964. [PubMed: 14129377]

45. Quillin SP, McAlister WH. Congenital solitary nonparasitic cyst of the liver in a newborn. Pediatr Radiol 22(7):543-544, 1992.

46. Karia M, Dasgupta TK, Sharma V, Chaudhuri MM, Mazumder DN. Symptomatic solitary giant congenital cysts of liver. Indian J Gastroenterol 11(3):136-138, 1992.

47. Koperna T, Vogl S, Satzinger U, Schulz F. Nonparasitic cysts of the liver: results and options of surgical treatment. World J Surg 21:850-855, 1997. [PubMed: 9327677]

48. Desmet VJ. What is congenital hepatic fibrosis? [Review]. Histopathology 20(6):465-477, 1992.

49. Sung JM, Huang JJ, Lin XZ, Ruaan MK, Lin CY, Chang TT, Shu HF, Chow NH. Caroli’s disease and congenital hepatic fibrosis associated with polycystic kidney disease. A case presenting with acute focal bacterial nephritis. Clin Nephrol 38(6):324-328, 1992.

50. Lipschitz B, Berdon WE, Defelice AR, Levy J. Association of congenital hepatic fibrosis with autosomal dominant polycystic kidney disease. Report of a family with review of literature. [Review]. Pediatr Radiol 23(2):131-133, 1993.

51. Murray-Lyon IM, Ochendan BG, Williams R. Congenital hepatic fibrosis: is it a single clinical entity? Gastroenterology 64:653-656, 1973. [PubMed: 4573445]

52. Annand SK, Chan JG, Liberman E. Polycystic disease and hepatic fibrosis in children. Am J Dis Child 129:810-825, 1975.

53. Gedaly R, Pomposelli JJ, Pomfret EA, Lewis WD, Jenkins RL. Cavernous hemangioma of the liver. Arch Surg 134:407-411, 1999. [PubMed: 10199314]

54. Williams PL. Gray’s Anatomy, 38th ed. New York: Churchill Livingstone, 1995.

55. Kennedy PA, Madding GF. Surgical anatomy of the liver. Surg Clin North Am 1977;57:233. [PubMed: 322332]

56. Naftalis J, Leevy CM. Clinical estimation of liver size. Am J Dig Dis 1963;8:236. [PubMed: 13937084]

57. Castell DO, O’Brien KD, Muench H, Chalmers TC. Estimation of liver size by percussion in normal individuals. Ann Intern Med 1969;70:1183. [PubMed: 5795743]

58. Sapira JD, Williamson DL. How big is the normal liver? Arch Intern Med 1979;139:971. [PubMed: 475535]

59. Whalen JP. Radiology of the Abdomen: Anatomic Basis. Philadelphia: Lea and Febiger, 1976.

60. Flament JB, Delattre JF, Hidden G. The mechanisms responsible for stabilising the liver. Anat Clin 4:125-135, 1982.

61. Lockhart RD, Hamilton GF, Fyfe FW. Anatomy of the Human Body. Philadelphia: JB Lippincott, 1959.

62. Gelfand DW. Anatomy of the liver. Radiol Clin North Am 1980; 18:187. [PubMed: 7208858]

63. Last RJ. Anatomy: Regional and Applied. 7th ed. Edinburgh: Churchill Livingstone, 1984.

64. Gamsu G, Webb WR, Sheldon P, Kaufman L, Crooks LE. Nuclear magnetic resonance imaging of the thorax. Radiology 147:473, 1983. [PubMed: 6836125]

65. Meyers MA. Dynamic Radiology of the Abdomen. 4th ed. New York: Springer-Verlag, 1994.

66. Ibukuro K, Tsukiyama T, Mori K, Inoue Y. Hepatic falciform ligament artery: angiographic anatomy and clinical importance. Surg Radiol Anat 20:367-371, 1998. [PubMed: 9894319]

67. Baba Y, Miyazono N, Ueno K, Kanetsuki I, Nishi H, Inoue H, Nakajo M. Hepatic falciform artery. Angiographic findings in 25 patients. Acta Radiol 2000;41:329-333. [PubMed: 10937752]

68. Healey JE Jr, Schroy PC. Anatomy of the biliary ducts within the human liver: analysis of the prevailing pattern of branchings and the major variations of the biliary ducts. Arch Surg 1953;66:599. [PubMed: 13039731]

69. Gao XH, Roberts A. The left triangular ligament of the liver and the structures in its free edge (appendix fibrosa hepatis) in Chinese and Canadian cadavers. Am Surg 1986;52:246. [PubMed: 3706914]

70. Rapant V, Hromada JA. A contribution to the surgical significance of aberrant hepatic ducts. Ann Surg 1950;132:253. [PubMed: 15433193]

71. Livingstone EM. A Clinical Study of the Abdominal Cavity and Peritoneum. New York: Hoeber, 1933.

72. Ochsner A, Graves AM. Subphrenic abscesses: analysis of 3372 collected and personal cases. Ann Surg 1933;98:961.

73. Mitchell GAG. Spread of acute intraperitoneal effusions. Br J Surg 1940;28:291.

74. Autio G. The spread of intraperitoneal infections: studies with roentgen contrast medium. Acta Chir Scand (suppl) 1964;321:1.

75. Boyd DP. The subphrenic spaces and the emperor’s new robes, New Engl J Med 1966;275:913.

76. Meyers MA. The spread and localization of acute intraperitoneal effusions. Radiology 1970;95:547. [PubMed: 5442658]

77. Silva YJ. In vivo use of human umbilical vessels and the ductus venosus arantii. Surg Gynecol Obstet 1979;148:595. [PubMed: 432777]

78. Michels NA. Blood Supply and Anatomy of the Upper Abdominal Organs, Philadelphia: Lippincott, 1955.

79. Gray SW, Rowe JS Jr, Skandalakis JE. Surgical anatomy of the gastroesophageal junction. Am Surg 1979;45:575. [PubMed: 507565]

80. Ochsner A, DeBakey M. Subphrenic abscesses: collective review and an analysis of 3608 collected and personal cases. Surg Gynecol Obstet (Int Abstr Surg Suppl) 1938;66:426.

81. Min PQ, Yang ZG, Lei QF, Gao XH, Long WS, Jiang SM, Zhou DM. Peritoneal reflections of left perihepatic region: radiologic-anatomic study. Radiology 1992;182:553. [PubMed: 1732980]

82. Hollinshead WH. Anatomy for Surgeons. New York: Paul B. Hoeber, 1956

83. Altemeier WA, Alexander JW. Retroperitoneal abscess. Arch Surg 1961;83:512. [PubMed: 13860719]

84. Hjortsjo CH. The topography of the intrahepatic duct system. Acta Anat 1951;11:599. [PubMed: 14829155]

85. Sales JP, Hannoun L, Sichez JP, Honiger J, Levy E. Surgical anatomy of liver segment IV. Anat Clin 1984;6:295. [PubMed: 6525304]

86. Padbury R, Azoulay D. Anatomy. In: Toouli J (ed) Surgery of the Biliary Tract. New York: Churchill Livingstone, 1993, pp. 3-19.

87. Dodds WJ, Erickson SJ, Taylor AJ, Lawson TL, Stewart ET. Caudate lobe of the liver: anatomy, embryology, and pathology. AJR 1990;154:87. [PubMed: 2104732]

88. Bismuth H. Surgical anatomy and anatomical surgery of the liver. World J Surg 1982;6:3. [PubMed: 7090393]

89. Brown BM, Filly RA, Callen PW. Ultrasonographic anatomy of the caudate lobe. J Ultrasound Med 1982;1:189. [PubMed: 7169640]

90. Heloury Y, Leborgne J, Rogez JM, Robert R, Barbin JY, Hureau J. The caudate lobe of the liver. Surg Radiol Anat 1988;10:83. [PubMed: 3131903]

91. Schwartz SI. Resection of the caudate lobe of the liver. (Editorial). J Am Coll Surg 184:75-76, 1997. [PubMed: 8989304]

92. Couinaud C. Lobes et segments hepatiques: note sur l’architecture anatomique et chirurgicale du foie. Presse Med 1953;62:709.

93. Kogure K, Kuwano H, Fujimaki N, Makuuchi M. Relation among portal segmentation, proper hepatic vein, and external notch of the caudate lobe in the human liver. Ann Surg 2000;231:223-228. [PubMed: 10674614]

94. Healey JE. Clinical anatomic aspects of radical hepatic surgery. J Int Coll Surg 1954;22:542. [PubMed: 13212155]

95. Rieker O, Mildenberger P, Hintze C, Schunk K, Otto G, Thelen M. [Segmental anatomy of the liver in computed tomography: do we localize the lesion accurately?]. Rofo 2000;172:147-152. [PubMed: 10723488]

96. Goldsmith NA, Woodburne RT. Surgical anatomy pertaining to liver resection. Surg Gynecol Obstet 1957;105:310. [PubMed: 13467662]

97. Onishi H, Kawarada Y, Das BC, Nakano, Gadzijev EM, Ravnik D, Isaji S. Surgical anatomy of the medial segment (S4) of the liver with special reference to bile ducts and vessels. Hepatogastroenterology 2000;47:143-150. [PubMed: 10690598]

98. Cho A, Okazumi S, Takayama W, Takeda A, Iwasaki K, Sasagawa S, Natsume T, Kono T, Kondo S, Ochiai T, Ryu M. Anatomy of the right anterosuperior area (segment 8) of the liver: evaluation with helical CT during arterial portography. Radiology 2000;214:491-495. [PubMed: 10671598]

99. Soyer P. Segmental anatomy of the liver: utility of a nomenclature accepted worldwide. AJR 1993;161:572. [PubMed: 8352107]

100. Ton That Tung. La vascularisation veineuse du foie et ses applications aux résections hépatiques. (Thesis). Hanoi, 1939.

101. Oran I, Memis A. The watershed between right and left hepatic artery territories: findings on CT scans after transcatheter oily chemoembolization of hepatic tumors. A preliminary report. Surg Radiol Anat 20:355-360, 1998. [PubMed: 9894317]

102. Ger R. Surgical anatomy of the liver. Surg Clin North Am 1989; 69:179. [PubMed: 2928899]

103. Blumgart LH, Baer HU, Czerniak A, Zimmermann A, Dennison AR. Extended left hepatectomy: technical aspects of an evolving procedure. Br J Surg 1993;80:903. [PubMed: 8369932]

104. Abdalla EK, Vauthey JN, Couinaud C. The caudate lobe of the liver: implications of embryology and anatomy for surgery. Surg Oncol Clin North Am 2002 Oct; 11(4):835-848.

105. Couinaud C. (Surgical approach to the dorsal section of the liver). (French) Chirurgie 1993-1994;119(9):485-488.

106. Couinaud C. (Dorsal sector of the liver). (French) Chirurgie 1998 Feb; 123(1):8-15.

107. Filipponi F, Romagnoli P, Mosca F, Couinaud C. The dorsal sector of human liver: embryological, anatomical and clinical relevance. Hepatogastroenterology 2000 Nov-Dec; 47(36):1726-1731.

108. Gadžijev EM, Ravnik D, Stanisavljevič D, Trotovek B. Venous drainage of the dorsal sector of the liver: differences between segments I and IX. Surg Radiol Anat 1997; 19:79-83.

109. Michels NA. The hepatic, cystic and retroduodenal arteries and their relations to the biliary ducts. Ann Surg 1951;133:503. [PubMed: 14819988]

110. Healey JE Jr, Schroy PC, Sorensen RJ. The intrahepatic distribution of the hepatic artery in man. J Int Coll Surg 1953;20:133. [PubMed: 13084954]

111. Michels NA. Newer anatomy of the liver and variant blood supply and collateral circulation. Am J Surg 1966;112:337. [PubMed: 5917302]

112. Madding GF, Kennedy PA. Trauma to the Liver. Philadelphia: WB Saunders, 1965.

113. Mays ET. Vascular occlusion. Surg Clin North Am 1977;57:291. [PubMed: 403622]

114. Schneck CD. The anatomical basis of abdominopelvic sectional imaging. In: Ultrasound in Inflammatory Disease (Clinics in Diagnostic Ultrasound, Vol II). New York: Churchill Livingstone, 1983.

115. Baron RL, Freeny PC, Moss AA. The liver. In: Moss AA, Gamsu G, Gerant K. Computed Tomography of the Body. Philadelphia: WB Saunders, 1983.

116. Bismuth H, Garden OJ. Regular and extended right and left hepatectomy for cancer. In: Nyhus LM, Baker RJ. Mastery of Surgery. 2nd ed. Boston: Little, Brown; 1992, pp. 864-72.

117. Dawson JL. Anatomy. In: Wright R, Alberti AGMM, Karran S, Millward-Sadler GH (eds). Liver and Biliary Diseases. Philadelphia: Saunders, 1979.

118. Ohkubo M. Aberrant left gastric vein directly draining into the liver. Clin Anat 2000;13:134-137. [PubMed: 10679857]

119. Suzuki T, Nakayasu A, Kauabe K, Takeda H, Honjo I. Surgical significance of anatomic variations of the hepatic artery. Am J Surg 1971;122:505. [PubMed: 5098656]

120. Healey JE Jr, Schwartz SI. Surgical anatomy. In: Schwartz SI. Surgical Diseases of the Liver. New York: McGraw-Hill, 1964.

121. Healey JE Jr. Vascular anatomy of the liver. Ann NY Acad Sci 1970;170:8.

122. von Haberer H. Experimentelle Unterbindung der Leberarterie. Arch Klin Chir 1905;78:557.

123. Edgecombe P, Garner C. Accidental ligation of the hepatic artery and its treatment. Can Med Assoc J 1951;64:518. [PubMed: 14839587]

124. Graham RR, Cannell D. Accidental ligation of hepatic artery. Br J Surg 1933;20:566.

125. Bengmark S, Rosengren K. Angiographic study of the collateral circulation to the liver after ligation of the hepatic arteries in man. Am J Surg 1970;119:620. [PubMed: 5445983]

126. Mays ET, Wheeler CS. Demonstration of collateral arterial flow after interruption of hepatic arteries in man. New Engl J Med 1974;290:993. [PubMed: 4594527]

127. Mays ET, Conti S, Fallahzadeh H, Rosenblatt M. Hepatic artery ligation. Surgery 1979;86:536. [PubMed: 483163]

128. Tygstrup N, Winkler K, Meelemgaard K. Determination of the hepatic arterial blood flow and oxygen supply in man by clamping the hepatic artery during surgery. J Clin Invest 1962;41:447. [PubMed: 13923352]

129. Nakamura S, Tsuzuki T. Surgical anatomy of the hepatic veins and the inferior vena cava. Surg Gynecol Obstet 152:43-50, 1981. [PubMed: 7455890]

130. Meyers WC, Peterseim DS, Pappas TN, Schauer PR, Eubanks S, Murray E, Suhocki P. Low insertion of hepatic segmental duct VII-VIII is an important cause of major biliary injury or misdiagnosis. Am J Surg 171:187-191, 1996. [PubMed: 8554138]

131. Sing RF, Stackhouse DJ, Jacobs DG, Heniford BT. Safety and accuracy of bedside carbon dioxide cavography for insertion of inferior vena cava filters in the intensive care unit. J Am Coll Surg 2001;192:168-171. [PubMed: 11220716]

132. Lorf T, Hanack U, Ringe B. Portal vein replacement by hepatic vein transposition. Am J Surg 174:353-354, 1997. [PubMed: 9324154]

133. Wang M, Sakon M, Umeshita K, Miyoshi H, Taniguchi K, Kishimoto S, Imajoh-Ohmi S, Monden M. Determination of a safe vascular clamping method for liver surgery. Arch Surg 133: 983-987, 1998. [PubMed: 9749852]

134. Man K, Fan ST, Ng IOL, Lo CM, Liu CL, Yu WC, Wong J. Tolerance of the liver to intermittent Pringle Maneuver in hepatectomy for liver tumors. Arch Surg 134:533-539, 1999. [PubMed: 10323426]

135. Nakamura S, Suzuki S, Hachiya T, Ochiai H, Konno H, Baba S. Direct hepatic vein anastomosis during hepatectomy for colorectal liver metastases. Am J Surg 174(3):331-333, 1997.

136. Grazi GL, Mazziotti A, Jovine E, Pierangeli F, Ercolani G, Gallucci A, Cavallari A. Total vascular exclusion of the liver during hepatic surgery. Arch Surg 132:1104-1109, 1997. [PubMed: 9336509]

137. Malassagne B, Cherqui D, Alon R, Brunetti F, Humeres R, Fagniez PL. Safety of selective vascular clamping for major hepatectomies. J Am Coll Surg 187:482-486, 1998. [PubMed: 9809563]

138. Evans PM, Vogt DP, Mayes JT III, Henderson JM, Walsh RM. Liver resection using total vascular exclusion. Surgery 124:807-815, 1998. [PubMed: 9781005]

139. Wisse E. An electron microscope study of the fenestrated endothelial lining of rat liver sinusoids. J Ultrastruct Res 1970:31:125.

140. Hardy KJ, Wheatley IC, Anderson AIE, Bond RJ. The lymph nodes of the porta hepatis. Surg Gynecol Obstet 1976;143:225. [PubMed: 941077]

141. Rouviere H. Anatomy of the Human Lymphatic System. Tobias MJ (trans). Ann Arbor MI: Edwards Brothers, 1938.

142. Fahim RB, McDonald JR, Richards JC, Ferns DO. Carcinoma of the gallbladder: a study of its modes of spread. Ann Surg 1962; 156:114. [PubMed: 13891308]

143. Burnett W, Cairns FW, Bacsich P. Innervation of the extrahepatic biliary system. Ann Surg 1964;159:8. [PubMed: 14103280]

144. Honjo I, Hasebe S. Studies on the intrahepatic nerves in the cirrhotic liver. Rev Int Hepat 1965;15:595. [PubMed: 5890695]

145. Hess W, Tamm H. Surgery of the Biliary Passages and the Pancreas. Princeton NJ: D. Van Nostrand, 1965.

146. Skandalakis LJ, Gray SW, Skandalakis JE. The history of surgical anatomy of the vagus nerve. Surg Gynecol Obstet 1986;162:75. [PubMed: 3940410]

147. Galen C. On the Usefulness of the Parts of the Body. May MT (trans) New York: Cornell University Press, 1968.

148. Jungermann K. Regulation von Stoffwechsel und Hämodynamik der Leber durch die hepatischen Nerven. Z Gastroenterol 1987; 25(suppl 1):44.

149. Friedman MI. Hepatic nerve function. In: Hue L, Schachter D, Shafritz DA (eds). The Liver: Biology and Pathobiology. New York: Raven Press, 1988, pp.949-59.

150. De Wulf H, Carton H. Neural control of glycogen metabolism. In: Hue L, van de Werve G (eds). Short Term Regulation of Liver Metabolism. Amsterdam: Elsevier North Holland, 1981.

151. Shimazu T. Central nervous system regulation of liver and adipose tissue metabolism. Diabetologia 1981;20:343. [PubMed: 7014330]

152. Sutherland SD. The intrinsic innervation of the liver. Rev Int Hepat 1965;15:569. [PubMed: 5832087]

153. Meguid MM, Yang ZJ, Bellinger LL, Gleason JR, Koseki M, Laviano A, Oler A. Innervated liver plays an inhibitory role in regulation of food intake. Surgery 1996;119:202. [PubMed: 8571207]

154. Nobin A, Baumgarten HG, Falck B, Ingemansson S, Moghimzadeh E, Rosengren E. Organization of the sympathetic innervation in liver tissue from monkey and man. Cell Tissue Res 1978; 195:371. [PubMed: 103622]

155. Moghimzadeh E, Nobin A, Rosengren E. Fluorescence microscopical and chemical characterization of the adrenergic innervation in mammalian liver tissue. Cell Tissue Res 1983;230:605. [PubMed: 6406068]

156. Kyosola K, Penttila O, Ihamaki T, Varis K, Salaspuro M. Adrenergic innervation of the human liver: a fluorescence histochemical analysis of clinical liver biopsy specimens. Scand J Gastroenterol 1985;20:254. [PubMed: 3992183]

157. Sawchenko PE, Friedman MI: Sensory functions of the liver: a review. Am J Physiol 1979;236:R5.

158. Amenta F, Cavallotti C, Ferrante F, Tonelli F. Cholinergic nerves in the human liver. Histochem J 1981;13:419. [PubMed: 7251394]

159. Forssman WG, Ito S. Hepatocyte innervation in primates. J Cell Biol 1977;73:299.

160. Ito T, Shibasaki S. Electron microscopy study on the hepatic sinusoidal wall and the fat-storing cells in the normal human liver. Arch Histol Jpn Niigata Jpn 1968;29:137. [PubMed: 5691853]

161. Tan KC, Rela M, Ryder SD, Rizzi PM, Karani J, Portmann B, Heaton ND, Howard ER, Williams R. Experience of orthotopic liver transplantation and hepatic resection for hepatocellular carcinoma of less than 8 cm in patients with cirrhosis. Br J Surg 1995; 82:253-6.

162. Cherqui D, Alon R, Piedbois P, Duvoux C, Dhumeaux D, Julien M, Fagniez PL. Combined liver transplantation and pancreato-duodenectomy for irresectable hilar bile duct carcinoma. Br J Surg 1995, 82: 397-8. [PubMed: 7796023]

163. Karajia ND, Rees M, Schache D, Heald RJ. Hepatic resection for colorectal secondaries. Br J Surg 1990; 77:27-9.

164. Doci R, Gennari L, Bignami P, Montalto F, Morabito A, Bozzetti F, Bonalumi MG. Morbidity and mortality after hepatic resection of metastases from colorectal cancer. Br J Surg 1995; 82:377-81.

165. Makuuchi M, Hasegawa H, Yamazaki S. Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet 1985; 161:346-50.

166. Makuuchi M, Hasegawa H, Yamazaki S, Takayasu K. Four new hepatectomy procedures for resection of the right hepatic vein and preservation of the inferior right hepatic vein. Surg Gynecol Obstet 1987; 164:69-72.

167. Launois B, Jamieson GG. Modern operative techniques in liver surgery. Churchill Livingstone: Edinburgh; 1993; 9-89.

168. Tompsett DH. Anatomical Techniques, 2nd ed. Edinburgh: E & S Livingstone 1970; 180-1.

169. Ton That Tung. Les resections et mineures du foie. Masson: Paris 1979. Quoted from Launois B, Jamieson GG. Modern operative techniques in liver surgery. Churchill Livingstone: Edinburgh; 1993; 9-110.

170. Bismuth H, Houssin D. Major and minor segmentectomies “Réglées” in liver surgery. World J Surg. 1982; 6:10. [PubMed: 7090385]

171. Blumgart LH. Hilar and intrahepatic biliary enteric anastomosis. Surg Clin North Am 1994;74(4):845-63.

172. Schwartz SI. Hepatic resection. In: Maingot’s Abdominal Operations, 9th ed. USA: Prentice-Hall International Inc. Vol. 111, 1990; 1273-4.

173. Sasse D, Spornitz UM, Maly IP. Liver architecture. Enzyme 1992;46:8. [PubMed: 1289084]

174. Merrell RC. Hepatic physiology. In: Miller TA (ed). Physiologic Basis of Modern Surgical Care. St. Louis: CV Mosby, 1988, pp. 404-416.

175. Meyers WC. Anatomy and physiology. In: Sabiston DC Jr. Textbook of Surgery 15th ed. Philadelphia: WB Saunders, 1996, pp. 1046-1061.

176. Holley RW. Control of growth mammalian cells in cell culture. Nature 1975;258:487. [PubMed: 1105198]

177. Barker A, Baranski A, Lambotte L. Study of the control of liver regeneration: partial hepatectomy followed by auxilliary liver transplantation. Hepatology 1993;18(Pt.2):163A.

178. Lambotte L, Tagliaferri E. Liver regeneration after temporary partial hepatectomy. Gastroenterology 1993;104(Pt. 2):A934.

179. Hashimoto M, Sanjo K. Functional capacity of the liver after two-thirds partial hepatectomy in the rat. Surgery 121:690-697, 1997. [PubMed: 9186470]

180. Foster JH. History of liver surgery. Arch Surg 126:381-387, 1991. [PubMed: 1998481]

181. Takao H, Kawarada Y. [Surgical anatomy of the hepatic hilar area]. J Jpn Surg Soc 2000;101:386-392. [PubMed: 10884985]

182. Czerniak A, Lotan G, Hiss Y, Shemesh E, Avigad I, Wolfstein I. The feasibility of in vivo resection of the left lobe of the liver and its use for transplantation. Transplantation 1989;48:26. [PubMed: 2665231]

183. Kazemier G, Hesselink EJ, Terpstra OT. Hepatic anatomy. Transplantation 1990;49:1029. [PubMed: 2336699]

184. Czerniak A, Lotan G, Hiss Y, Shemesh E, Avigad I, Wolfstein I. Reply to Kazemier et al. Transplantation 1990;49:1030.

185. Couinaud C. Le Foie: Etudes Anatomiques et Chirurgicales. Paris: Masson, 1957.

186. Hobsley M. Intrahepatic anatomy: a surgical evaluation. Br J Surg 1958;45:635. [PubMed: 13560770]

187. Kazemier G, Hesselink EJ, Lange JF, Terpstra OT. Dividing the liver for the purpose of split grafting or living related grafting: a search for the best cutting plane. Transplant Proc 1991;23:1545. [PubMed: 1989283]

188. Strong RW, Lynch SV, Ong TH, Matsunami H, Koido Y, Balderson GA. Successful liver transplantation from a living donor to her son. New Engl J Med 1990;322:1505. [PubMed: 2336076]

189. Bismuth H, Morino M, Castaing D, Gillon MC, Descorps Declere A, Saliba F, Samuel D. Emergency orthotopic liver transplantation in two patients using one donor liver. Br J Surg 76(7): 722-724, 1989.

190. Merz B. Two new approaches to liver transplantation: one organ, two patients . . .two organs, one patient (news). JAMA 1989;262: 14, Jul 7.

191. Blumgart LH (ed). Surgery of the Liver and Biliary Tract. New York, Churchill Livingstone, 1988.

192. Czerniak A, Shabtai M, Avigad I, Ayalon A. A direct approach to the left and middle hepatic veins during left-sided hepatectomy. Surg Gynecol Obstet 1993;177:303. [PubMed: 8356502]

193. Elias H, Petty D. Gross anatomy of the blood vessels and ducts within the human liver. Am J Anat 1952;90:59. [PubMed: 14902689]

194. Banner RL, Brasfield RD. Surgical anatomy of the hepatic veins. Cancer 1958;11:22. [PubMed: 13500290]

195. Baird RA, Britton RC. The surgical anatomy of the hepatic veins. J Surg Res 1973;15:345. [PubMed: 4586302]

196. Depinto DJ, Nucha SJ, Powers PC. Major hepatic vein ligation necessitated by blunt abdominal trauma. Ann Surg 1976;183:243. [PubMed: 1259479]

197. Castaing D, Kunstlinger F, Habib N, Bismuth H. Intraoperative sonography study of the liver. Am J Surg 1985;149:576.

198. Ou QJ, Herman RE. Hepatic vein ligation and preservation of liver segments in major resections. Arch Surg 1987;122:1198. [PubMed: 2821957]

199. Nery JR, Frasson E, Rilo HLR, Purceli E, Barros MFA, Neto JB, Mies S, Raia S, Belzer FO. Surgical anatomy and blood supply of the left biliary tree pertaining to partial liver grafts from living donors. Transplantation Proc 1990;22:1492. [PubMed: 2389377]

200. Couinaud C, Houssin D. (Bisection of the liver for transplantation. Simplification of the method). (French) Chirurgie 1992; 118:217. [PubMed: 1339732]

201. Couinaud C. (Variations of the right bile ducts. The futility of complete anatomical classifications). (French) Chirurgie 1993-1994;119:354.

202. Houssin D, Boillot O, Soubrane O, Couinaud C, Pitre J, Ozier Y, Devictor D, Bernard O, Chapuis Y. Controlled liver splitting for transplantation in two recipients: technique, results and perspectives. Br J Surg 1993;80:75. [PubMed: 8428301]

203. Couinaud C. (Absence of portal bifurcation). (French) J Chir (Paris) 1993;130:111. [PubMed: 8320295]

204. Couinaud C. (A “scandal”: segment IV and liver transplantation). (French) J Chir (Paris) 1993;130:443. [PubMed: 8163597]

205. Couinaud C. (Surgical approach to the dorsal section of the liver). (French) Chirurgie 1993-1994;119:485.

206. Couinaud C. (Intrahepatic anatomy: application to liver transplantation). (French) Ann Radiol (Paris) 1994;37:323. [PubMed: 7993018]

207. Meyers WC. Segmental hepatic resection. In: Sabiston DC Jr. Atlas of General Surgery. Philadelphia: WB Saunders, 1994, p. 535.

208. Starzl TE, Bell RH, Beart RW, Putnam CW. Hepatic trisegmentectomy and other liver resections. Surg Gynecol Obstet 1975;141:429-437. [PubMed: 1162576]

209. Starzl TE, Koep LJ, Weil R III, Lilly JR, Putnam CW, Aldrete JA. Right trisegmentectomy for hepatic neoplasms. Surg Gynecol Obstet 1980;150:208-214. [PubMed: 7352313]

210. Pack GT, Miller TR, Brasfield RD. Total right hepatic lobectomy for cancer of the gallbladder. Ann Surg 142:6, 1955. [PubMed: 14388606]

211. Erath HG Jr, Sawyers JL, O’Neill JA Jr, Adkins RB Jr. Major hepatic resection. South Med J 74:653, 1981. [PubMed: 7244739]

212. Mays ET. Bursting injuries to the liver. Arch Surg 93:92, 1966. [PubMed: 5936558]

213. Raffucci FL, Ramirez-Schon G. Management of tumors of the liver. Surg Gynecol Obstet 130:371, 1970. [PubMed: 4189075]

214. Povoski SP, Fong Y, Blumgart LH. Extended left hepatectomy. World J Surg 1999;23:1289-1293. [PubMed: 10552123]

215. Wu CC, Ho WL, Chen JT, Tang CS, Yeh DC, Liu TJ, P’eng FK. Mesohepatectomy for centrally located hepatocellular carcinoma: an appraisal of a rare procedure. J Am Coll Surg 188:508-515, 1999. [PubMed: 10235579]

216. Moore EE, Shackford SR, Pachter HL, et al. Organ injury scaling: spleen, liver and kidney. J Trauma 29:1664, 1989. [PubMed: 2593197]

217. Fang JF, Chen RJ, Wong YC, Lin BC, Hsu YB, Kao JL, Kao YC. Pooling of contrast material on computed tomography mandates aggressive management of blunt hepatic injury. Am J Surg 176: 315-319, 1998. [PubMed: 9817246]

218. Feliciano DV, Mattox KL, Birch JM. Packing for control of hepatic hemorrhage: 58 consecutive patients. J Trauma 26:738, 1986. [PubMed: 3488413]

219. Svoboda JA, Peter ET, Dan CU, et al. Severe liver trauma in the face of coagulopathy —a case for temporary packing and early re-exploration. Am J Surg 144:717, 1982. [PubMed: 6756183]

220. Beal SL. Fatal hepatic hemorrhage: an unresolved problem in the management of complex liver injuries. J Trauma 30:163, 1990. [PubMed: 2304109]

221. Cogbill TH, Moore EE, Jurkovich GJ, et al. Severe hepatic trauma: a multi-center experience with 1,335 liver injuries. J Trauma 28: 1433, 1988. [PubMed: 3172301]

222. Balasegaram M, Joishy SK. Hepatic resection: the logical approach to surgical management of major trauma to the liver. Am J Surg 142:580, 1981. [PubMed: 7304814]

223. Blumgart LH, Drury JK, Wood CB. Hepatic resection for trauma, tumour, and biliary obstruction. Br J Surg 66:762, 1979. [PubMed: 519158]

224. Hollands MJ, Little JM. The role of hepatic resection in the management of blunt liver trauma. World J Surg 14:478, 1990. [PubMed: 2382452]

225. Pachter HL, Spencer FC, Hofstetter SR, et al. Significant trends in the treatment of hepatic trauma: experience with 411 injuries. Ann Surg 215:492, 1992. [PubMed: 1616386]

226. Gayowski TJ, Iwatsuki S, Madariaga JR, et al. Experience in hepatic resection for metastatic colorectal cancer: analysis of clinical and pathologic risk factors. Surgery 116:703-711, 1994. [PubMed: 7940169]

227. Rosen CB, Nagorney DM, Taswell HF. Perioperative blood transfusion and determinants of survival after liver resection for metastatic colorectal carcinoma. Ann Surg 216:493-505, 1992. [PubMed: 1417198]

228. Scheele J, Stangl R, Altendorf-Hofmann A, et al. Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery 110:13-29, 1991. [PubMed: 1866690]

229. Farmer DG, Rososve MH, Shaked A. Current treatment for hepatocellular carcinoma. Ann Surg 219:236-247, 1994. [PubMed: 8147605]

230. Melendez J, Ferri E, Zwillman M, Fischer M, DeMatteo R, Leung D, Jarnagin W, Fong Y, Blumgart LH. Extended hepatic resection: a 6-year retrospective study of risk factors for perioperative mortality. J Am Coll Surg 2001;192:47-53. [PubMed: 11192922]

231. Vauthey JN, Chaoui A, Do KA, Bilimoria MM, Fenstermacher MJ, Charnsangavej C, Hicks M, Alsfasser G, Lauwers G, Hawkins IF, Caridi J. Standardized measurement of future liver remnant prior to extended liver resection: methodology and clinical associations. Surgery 2000;127:512-519. [PubMed: 10819059]

232. Bakalakos EA, Kim JA, Young DC, Martin EW Jr. Determinants of survival following hepatic resection for metastatic colorectal cancer. World J Surg 22:399-405, 1998. [PubMed: 9523523]

233. Bakalakos EA, Burak WE, Young DC, Martin EW Jr. Is carcino-embyronic antigen useful in the follow-up management of patients with colorectal liver metastases? Am J Surg 177:2-6, 1999. [PubMed: 10037299]

234. Wigmore SJ, Madhavan K, Redhead DN, Currie EJ, Garden OJ. Distribution of colorectal liver metastases in patients referred for hepatic resection. Cancer 2000;89:285-287. [PubMed: 10918157]

235. D’Angelica M, Brennan MF, Fortner JG, Cohen AM, Blumgart LH, Fong Y. Ninety-six five-year survivors after liver resection for metastatic colorectal cancer. J Am Coll Surg 185:554-559, 1997. [PubMed: 16456920]

236. Bismuth H, Majno PE. Hepatobiliary surgery. J Hepatol 2000; 32:208-224.

237. Weimann A, Ringe B, Klempnauer J, Lamesch P, Gratz KF, Prokop M, Maschek H, Tusch G, Pichlmayr R. Benign liver tumors: differential diagnosis and indications for surgery. World J Surg 21:983-991, 1997. [PubMed: 9361515]

238. Smail N, Catania RA, Wang P, Cioffi WG, Bland KI, Chaudry IH. Gut and liver: the organs responsible for increased nitric oxide production after trauma-hemorrhage and resuscitation. Arch Surg 133:399-405, 1998. [PubMed: 9565120]

239. Miyazaki M, Ito H, Nakagawa K, Ambiru S, Shimizu H, Shimizu Y, Okuno A, Nozawa S, Nukui Y, Yoshitomi H, Nakajima N. Segments I and IV resection as a new approach for hepatic hilar cholangiocarcinoma. Am J Surg 175:229-231, 1998. [PubMed: 9560126]

240. Roayaie S, Guarrera JV, Ye MQ, Thung SN, Emre S, Fishbein TM, Guy SR, Sheiner PA, Miller CM, Schwartz ME. Aggressive surgical treatment of intrahepatic cholangiocarcinoma: predictors of outcomes. J Am Coll Surg 187:365-372, 1998. [PubMed: 9783782]

241. Iwatsuki S, Todo S, Marsh JW, Madariaga JR, Lee RG, Dvorchik I, Fung JJ, Starzl TE. Treatment of hilar cholangiocarcinoma (Klatskin tumors) with hepatic resection or transplantation. J Am Coll Surg 187:358-364, 1998. [PubMed: 9783781]

242. Delbeke D, Martin WH, Sandler MP, Chapman WC, Wright JK Jr, Pinson CW. Evaluation of benign vs malignant hepatic lesions with positron emission tomography. Arch Surg 133:510-516, 1998. [PubMed: 9605913]

243. Fong Y, Kemeny N, Lawrence TS. Cancer of the liver and biliary tree. In: DeVita VT Jr, Hellman S, Rosenberg SA (eds). Cancer: Principles & Practice of Oncology (6th ed). Philadelphia: Lippincott Williams & Wilkins, 2001, pp. 1162-1203.

244. Bilimoria MM, Lauwers GY, Doherty DA, Nagorney DM, Belghiti J, Do KA, Regimbeau JM, Ellis LM, Curley SA, Ikai I, Yamaoka Y, Vauthey JN. Underlying liver disease, not tumor factors, predicts long-term survival after resection of hepatocellular carcinoma. Arch Surg 2001;136:528-535. [PubMed: 11343543]

245. Nakajima Y, Ko S, Kanamura T, Nagao M, Kanehiro H, Hisanaga M, Aomatsu Y, Ikeda N, Nakano H. Repeat liver resection for hepatocellular carcinoma. J Am Coll Surg 2001;192: 339-344. [PubMed: 11245376]

246. Billingsley KG, Jarnagin WR, Fong Y, Blumgart LH. Segment-oriented hepatic resection in the management of malignant neoplasms of the liver. J Am Coll Surg 187:471-481, 1998. [PubMed: 9809562]

247. Meyers WC, Chari RS. We’ve come a long way, baby! [Editorial] J Am Coll Surg 187:534-535, 1998. [PubMed: 9809572]

248. Yamamoto J, Kosuge T, Shimada K, Yamasaki S, Takayama T, Makuuchi M. Anterior transhepatic approach for isolated resection of the caudate lobe of the liver. World J Surg 23:97-101, 1999. [PubMed: 9841771]

249. Azoulay D, Marin-Hargreaves G, Castaing D, Adam R, Savier E, Bismuth H. The anterior approach: the right way for right massive hepatectomy. J Am Coll Surg 2001;192:412-417. [PubMed: 11245386]

250. Yamamoto Y, Terajima H, Ishikawa Y, Uchinami H, Taura K, Nakajima A, Yonezawa K, Yamamoto N, Ikai I, Yamaoka Y. In situ pedicle resection in left trisegmentectomy of the liver combined with reconstruction of the right hepatic vein to an inferior vena caval segment transpositioned from the infrahepatic portion. J Am Coll Surg 2001;192:137-141. [PubMed: 11192916]

251. Midorikawa Y, Kubota K, Takayama T, Toyoda H, Ijichi M, Torzilli G, Mori M, Makuuchi M. A comparative study of postoperative complications after hepatectomy in patients with and without chronic liver disease. Surg 1999;126:484-91. [PubMed: 10486600]

252. Bosscha K, Roukema AJ, van Vroonhoven TJ, van der Werken C. Twelfth rib resection: a direct posterior surgical approach for subphrenic abscesses. Eur J Surg 2000;166:119-122. [PubMed: 10724488]

253. Katkhouda N, Mavor E. Laparoscopic management of benign liver disease. Surg Clin North Am 2000;80:1203-1211. [PubMed: 10987031]

254. Dodd GD III, Soulen MC, Kane RA, Livraghi T, Lees WR, Yamashita Y, Gillams AR, Karahan OI, Rhim H. Minimally invasive treatment of malignant hepatic tumors: at the threshold of a major breakthrough. Radiogr 2000;20:9-27. [PubMed: 10682768]

255. Warren WD, Zeppa R, Fomon JJ: Selective transplenic decompression of gastroesophageal varices by distal splenorenal shunt. Ann Surg 166:437, 1967. [PubMed: 6068492]

256. Warren WD, Salam AA, Hutson D, et al.: Selective distal splenorenal shunt: Technique and results of operation. Arch Surg 108: 307, 1974.

257. Warren WD, Millikan WJ Jr, Henderson JM, et al.: Ten years’ portal hypertensive surgery at Emory: Results and new perspective. Ann Surg 195:530, 1982. [PubMed: 7073351]

258. Sarfeh IJ, Rypins EB, Mason GR.: A systemic appraisal of portcaval H-graft diameters. Ann Surg 204:356, 1986. [PubMed: 3490229]

259. LaBerge JM, Ring EJ, Gordon RL, et al.: Creation of transjugular intrahepatic portosystemic shunts with the wallstent endoprosthesis: results in 100 patients. Radiology 187:413, 1993. [PubMed: 8475283]

260. Shiffman ML, Jeffers L, Hoofnagle JH, et al.: The role of transjugular intrahepatic portosystemic shunt for treatment of portal hypertension and its complications: a conference sponsored by the National Digestive Diseases Advisory Board. Hepatology 22:1591, 1995. [PubMed: 7590680]

261. Demetriades D, Gomez H, Chahwan S, Charalambides K, Velmahos G, Murray J, Asensio J, Berne TV. Gunshot injuries to the liver: the role of selective nonoperative management. J Am Coll surg 1999;188:343. [PubMed: 10195716]

262. Moore EE. When is nonoperative management of a gunshot wound to the liver appropriate? J Am Coll Surg 188:427-428, 1999. [PubMed: 10195728]

263. Brown CH. Needle biopsy of the liver. Am J Dig Dis 6:269, 1961.

264. Millward-Sadler GH, Whorwell PJ. Liver biopsy: methods, diagnostic value and interpretation. In: Wright’s Liver and Biliary Disease. 3rd ed. Millward-Sadler GH, Wright R, Arthur MJP (eds). Philadelphia: WB Saunders, 1992, pp. 476-97.

265. Schwartz SI. The liver. In: Principles of Surgery. 6th ed. Schwartz SI (ed). New York: McGraw-Hill, 1994, pp. 1319-66.

266. Purow E, Grosberg SJ, Wapnick S. Menghini needle fracture after attempted liver biopsy. Gastroenterology 1977;73:1404. [PubMed: 913981]

267. Piccinino F, Sagnelli E, Pasquale G. Complications following percutaneous liver biopsy. J Hepatol 1986;2:165. [PubMed: 3958472]

268. Feldman EA. Injury to the hepatic vein. Am J Surg 111:244, 1966. [PubMed: 5903696]

269. Brewer GE. Hydatid cyst of the liver with ligature of the portal vein. Ann Surg 47:619, 1908.

270. Colp R. The treatment of pylephlebitis of appendicular origin. Surg Gynecol Obstet 43:627, 1926.

271. Child C, Holswade G, McClure R, Gore A, O’Neil EA. Pancreaticoduodenectomy with resection of the portal vein in the macaca mulatta monkey and in man. Surg Gynecol Obstet 94:31, 1952. [PubMed: 14893090]

272. Honjo I, Suzuki T, Ozawa K, Takasan H, Kitamura O, Ishikawa T. Ligation of a branch of the portal vein for carcinoma of the liver. Am J Surg 130:296, 1975. [PubMed: 170837]

273. Busuttil RW, Kitahama A, Cerise E, McFadden M, Lo R, Longmire WP. Management of blunt and penetrating injuries to the porta hepatis. Ann Surg 191:641, 1980. [PubMed: 7369824]

274. Stone HH. Discussion, in Busuttil RW et al. Management of blunt and penetrating injuries to the porta hepatis. Ann Surg 191:641, 1980.

275. Pachter HL, Drager S, Godfrey N, LeFleur R. Traumatic injuries of the portal vein: the role of acute ligation. Ann Surg 189:383, 1979. [PubMed: 443892]

276. Kim DK, Kinne DW, and Fortner JG. Occlusion of the hepatic artery in man. Surg Gynecol Obstet 136:966, 1973. [PubMed: 4703477]

277. Braasch JW, Preble HE. Unilateral hepatic duct obstruction. Ann Surg 158:17, 1963. [PubMed: 14042628]

278. Braasch JW, Whitcomb FF Jr, Watkins E Jr, Maguire RR, Khazei AM. Segmental obstruction of the bile duct. Surg Gynecol Obstet 134:915, 1972. [PubMed: 5032387]

279. Lo C-M, Fan S-T, Liu C-L, Lai ECS, Wong J. Biliary complications after hepatic resection: risk factors, management, and outcome. Arch Surg 133:156-161, 1998. [PubMed: 9484727]

280. Starzl TE, Hakala TR, Shaw BW Jr, Hardesty RL, Rosenthal TJ, Griffith BP, Iwatsuki S, Bahnson HT. A flexible procedure for multiple cadaveric organ procurement. Surg Gynecol Obstet 1984;158:223-230. [PubMed: 6367113]

281. Shaw BW, Iwatsuki S, Starzl TE. Alternative methods of arterialization of the hepatic graft. Surg Gynecol Obest 1984;159: 491.

282. Gordon RD, Shaw BW, Iwatsuki S, Todo S, Starzl TE. A simplified technique for revascularization of homographs of the liver with a variant right hepatic artery from the superior mesenteric artery. Surg Gynecol Obest 1985;160:475.

283. Quinones-Baldrich WJ, Memsic L, Ramming K, Hiatt J, Busuttil R. Branch patch arterialization of hepatic grafts. Surg Gynecol Obstet 1986;162: 489.

284. Ekberg H, Tranberg KG, Anderson R, Jeppsson B, Bengmark S. Major liver resection: perioperative course and management. Surgery 1986;100:1. [PubMed: 3014674]

285. Dodson TF. Surgical anatomy of hepatic transplantation. Surg Clin North Am 1993;73:645. [PubMed: 8378815]

286. Srinivasan P, Vilca-Melendez H, Muiesan P, Prachalias A, Heaton ND, Rela M. Liver transplantation with monosegments. Surg 1999;126:10-12. [PubMed: 10418586]

287. Couinaud C. A simplified method for controlled left hepatectomy. Surgery 1985;97:358. [PubMed: 3975857]

288. Thompson EC, Grier JF, Gholson CF, McDonald JC. A critical review of the Couinaud technique of hepatic resection. Arch Surg 1995;130:553. [PubMed: 7748097]

289. Hardy KJ, Jones RM. Hepatic artery anatomy in relation to reconstruction in liver transplantation: some unusual variations. Aust NZ J Surg 1994;64:437. [PubMed: 8010909]

290. Egawa H, Inomata Y, Uemoto S, Asonuma K, Kiuchi T, Okajima H, Yamaoka Y, Tanaka K. Hepatic vein reconstruction in 152 living-related donor liver transplantation patients. Surgery 121: 250-257, 1997. [PubMed: 9068666]

291. Marcos A, Ham JM, Fisher RA, Olzinski AT, Posner MP. Surgical management of anatomical variations of the right lobe in living donor liver transplantation. Ann Surg 2000;231:824-831. [PubMed: 10816625]

292. Pomfret EA, Pompselli JJ, Lewis D, Gordon FD, Burns DL, Lally A, Raptopoulos V, Jenkins RL. Live donor adult liver transplantation using right lobe grafts. Arch Surg 2001;136:425-433. [PubMed: 11296114]

293. Cirera I, Navasa M, Rimola A, Garcia-Pagan JC, Grande L, Garcia-Valdecasas JC, Fuster J, Bosch J, Rodes J. Ascites after liver transplantation. Liver Transplant 2000;6:157-162. [PubMed: 10719013]

294. Neuberger J. Liver transplantation. J Hepatol 2000;32:198-207. [PubMed: 10728805]

295. Azoulay D, Castaing D, Ahchong K, Adam R, Bismuth H. A minimally invasive approach to the treatment of stenosis of the portal vein after hepatic transplantation. Surg Gynecol Obstet 1993; 176: 599.

Copyright ©2006 The McGraw-Hill Companies. All rights reserved.
Privacy Notice. Any use is subject to the Terms of Use and Notice. Additional Credits and Copyright Information.

Leave a Reply


Time limit is exhausted. Please reload the CAPTCHA.

Categories

apply_now Pepperstone Group Limited