Biliary Tract

The early part of the eighteenth century saw rapid development in the understanding of biliary disease. The ideas of Morgagni rapidly spread and were a firm basis for the changes to come. Studies regarding the structure, origin, and functions of bile were initiated in the latter half of the eighteenth century and culminated in Wieland’s clarification of the structure of the various bile acids and Windaus’s demonstration of the relationship of bile acids to steroids, which earned him a Nobel prize in 1927 and 1928. Boerhaave (1668-1738) established a wide surgical reputation at the University of Leiden in Holland and worked extensively on diseases of the liver and biliary tract. In 1743, Jean Louis Petit presented to the Paris Academy of Surgery a paper entitled “Considerations Concerning Tumors Produced by Retained Bile in the Gallbladder of the Liver, Sometimes Taken for Liver Abscesses.” He introduced the term “biliary colic” and established the clinical treatment of it and of obstructive cholecystitis. In cases in which the gallbladder adhered firmly to the abdominal wall, Petit advised that it be punctured and opened to remove calculi, and he applied this procedure successfully in the case of one patient; this preceded Morgagni’s publication of 1769 referred to earlier. Petit also coined the term “biliary colic” (“colique hepatique”).

Biliary surgery began in Indiana on July 15, 1867, when John Bobbs operated on a woman who had a large tumor that he believed to be an ovarian cyst. To his amazement, when the abdomen was opened, he found an enormous gallbladder filled with stones. He opened it and extracted the calculi, sutured it carefully, and replaced it back in the abdomen (Bobbs, 1868). It was nearly a decade before a similar cholecystostomy was performed almost simultaneously by a Swiss, Theodore Kocher (Fig. 4), a North American, Sims, and an Englishman, Lawson Tait. All three surgeons planned operations in which the gallbladder was affixed to the abdominal wall to allow extraction of stones and pus and to leave it open to the exterior, so that peritonitis as a result of maneuvers within the abdomen could be avoided.

FIGURE 4 Theodore Kocher (1841–1917), surgeon.

Sims worked on both sides of the Atlantic, and in Paris he operated on a patient with long-standing jaundice and a tumor in the right hypochondrium. With antiseptic technique, he opened the gallbladder and extracted 60 calculi then sutured the gallbladder to the abdominal wall; this was perhaps the first elective surgical procedure for obstructive jaundice (Sims, 1878). In the same year, in Bern, Switzerland, Kocher performed a cholecystostomy in two stages (Glenn, 1971). In the first stage, he packed the wound with gauze to the bottom of the gallbladder, and 8 days later, he emptied the residual stones from the gallbladder. Incidentally, Kocher, who won the Nobel prize in medicine in 1909 for his work on the physiology and surgery of the thyroid gland, also described sphincterotomy, or internal choledochoduodenostomy. His name is remembered by every biliary surgeon who performs mobilization of the duodenum as described by the great master (Kocher, 1903). Kocher originally described the maneuver for use in gastric surgery, but similar to so many other firsts in surgery at that time, the maneuver was first described by Jourdan (1895) and was first performed in biliary surgery by Vautrin (1896). Perhaps the maneuver should be referred to as “Vautrin’s maneuver” rather than Kocher’s. Tait, the great British surgeon, is given credit for performing the first cholecystostomy for gallbladder lithiasis in one stage. The patient, a 40-year-old woman, survived, and by 1884, he had performed the procedure in 14 cases with only 1 death (Tait, 1885).

The first elective cholecystectomy was done by Langenbuch (Fig. 5). While others were pursuing the construction of biliary fistulae and direct removal of gallstones, Langenbuch observed that because stones were known to recur, others had “busied themselves with the product of the disease, not the disease itself” (Langenbuch, 1882). As he was later to recount, two thoughts kept occurring to him: first, that in animal experiments, Zambeccari in 1630 and Teckoff in 1667 had performed cholecystostomy and cholecystectomy in dogs and had shown that the gallbladder was not essential to life (Langenbuch, 1896); second, that his medical colleagues believed that the gallbladder itself gave rise to stones. He developed the technique for cholecystectomy over several years of cadaver dissection and performed the operation at the Lazarus hospital in Berlin on July 15, 1882. The patient had had biliary colic for 16 years and was addicted to morphine. He was afebrile the day after the operation, had little pain, and was smoking a cigar; the patient was walking at 12 days and left the hospital 6 weeks later, pain free and gaining weight (Traverso, 1976). Report of this case (Langenbuch, 1882) led to a controversy over cholecystostomy as championed by Tait. Langenbuch’s operation was the new cholecystectomy.

FIGURE 5 Karl Langenbuch (1846–1901), surgeon.

In 1886, Gaston had tabulated 33 cholecystostomy operations with a mortality of 27% compared with 8 cholecystectomies (5 by Langenbuch) with 1 death recorded, a mortality of 12%. By 1890, 47 cholecystectomies had been done by 27 surgeons, and in 1897, the number had increased to nearly 100 operations with a mortality of less than 20% (Gaston, 1897).

The most important recent advance in surgery of the gallbladder came 100 years after Langenbuch’s first cholecystectomy. Laparoscopic cholecystectomy was conceived and first performed in Germany by Muhe in 1985. Between 1985 and 1987, he performed 94 laparoscopic cholecystectomies (Muhe, 1986, 1991). Mouret in Lyon, France, performed the first video laparoscopic cholecystectomy. He did not publish his experience, but the news spread rapidly, and Dubois in Paris published the first series of laparoscopic cholecystectomies (Dubois et al, 1989, 1990). Perissat, working in Bordeaux, further developed the laparoscopic approach and introduced it to the United States in 1989 (Perissat et al, 1990). The procedure has since been extended, so that laparoscopic exploration of the common bile duct is now possible and is routinely carried out. Today, most cholecystectomies are done using laparoscopic techniques, such that the modern surgical trainee often has little or no experience in open cholecystectomy. More recently, cholecystectomy has been done via minimally invasive techniques using robotics (Marescaux et al, 1998; Satava, 1999) to manipulate the instruments.

Not long after the performance of the first cholecystectomy, attempts were made to remove stones from the bile ducts. In 1898, Thornton performed the first removal of a stone from the common bile duct. A year later, Courvoisier operated successfully on another case of choledocholithiasis and published his well-known monograph on the pathology and surgery of the biliary ducts. He also enunciated the law that was to bear his name, which established that in cases of jaundice, if the gallbladder is not distended, the case is more likely to be one of stones. The operative procedure for exploration of the common bile duct for choledocholithiasis was not popularized, however, because of the risk of peritoneal infiltration of bile.

In 1897, Kehr (Fig. 6) performed the procedure and placed a rubber tube in the common bile duct through the cystic duct; this was the first systematic use of biliary intubation. Kehr’s name is properly associated with the development of biliary intubation; Kehr (1912) and Quenu and Duval (1908) were able to extract stones along the tunnels created by the drainage tubes. These were the precursors for techniques later developed by Mondet (1962) and Mazzariello (1966, 1974). Kehr had developed numerous combinations of drainage in patients with biliary stones, and many other surgeons rapidly developed choledochotomy without suture and using tube drainage.

FIGURE 6 Hans Kehr (1862–1916), surgeon.

Surgery of the bile ducts rapidly disseminated across Europe, England, and the United States, and in 1912, Kehr developed what came to be known as the T-tube. Not only was choledochotomy simplified, but biliary tract repair was done over these tubes. Kehr became justly famous for his introduction of biliary intubation and was probably the most outstanding biliary surgeon of his day. In 1913, he published a treatise entitled Surgery of the Biliary Tract, which for more than 40 years was the most respected text on the subject. Kehr (1908a, 1908b) described the resection of cancerous gallbladders, including hepatic resection, and he resected hepatic tumors and aneurysms of the hepatic artery. He also performed the first hepaticoenteric anastomosis.

Before the development of Kehr’s tubes, choledochotomies often became biliary fistulae, either because of residual supraampullary stones, or because the surgeon had inadvertently opened the bile duct proximal to a cancer. German and Austrian surgeons were the first to perform supraduodenal choledochoduodenostomy (Riedel, 1892; Sprengel, 1891). Sprengel’s operation described a side-to-side choledochoduodenostomy, and it subsequently became popular in Europe and the United States (Madden et al, 1965). Cholecystenterostomy also was developed initially by von Winiwarter (1882) and was used later by many surgeons, including Oddi (1888).

Transduodenal surgery was not long in developing. In 1895, Kocher wrote an article on internal choledochoduodenostomy to remove supraampullary choledochal calculi; by 1899 he had performed the operation 20 times. MacBurney (1898) published his experience with duodenostomy and papillotomy in patients with impacted periampullary calculi. These early procedures of a choledochotomy and choledochoenteric anastomosis for the treatment of jaundice and of stones in the biliary tract are still used today, with frequent application of the same principles but with the use of the endoscope.

At about the same time, surgeons began to operate on cancer of the papilla. In Baltimore in 1900, Halsted resected a portion of the duodenum that included a tumor and reimplanted the common duct, at the same time performing a cholecystostomy. He then reoperated to remove the gallbladder. Mayo (1901) reported an operation on a 49-year-old man with papillary cancer. Mayo opened the duodenum, removed the tumor, and carried out a choledochoduodenostomy. This was the first transduodenal ampullectomy. Kausch (1912) in Germany and Harmann (1923) in France gave accounts of resections of ampullary tumors. In Lausanne, Switzerland, Roux, a disciple of Kocher, had described preparation of a “jejunal loop” for use in gastric surgery, and it soon became an adjunct in biliary surgery (Roux, 1897). This Roux-en-Y procedure was soon used by Monprofit (1904) in the performance of cholecystojejunostomy, and he proposed it for hepaticojejunostomy at the French Congress of Surgery in 1908. Dahl (1909), in what he called “a new operation on the bile ducts,” was the first to advocate the Roux anastomosis in biliary surgery.

With the advent of cholecystectomy and choledochostomy came the inevitable sequelae of residual bile duct stones and iatrogenic lesions. Initially, these were treated by various forms of intubation, similar to the techniques advocated by Kehr, but many leading surgeons, such as Moynihan and Mayo, used hepaticoduodenal anastomoses (Estefan et al, 1977). Dahl (1909) used the Roux-en-Y loop, but more recently, other authors (Madden et al, 1965; Schein & Gliedman, 1981) have preferred choledochoduodenostomy as described previously.

Operative biliary drainage in upper biliary tract cancer and in patients with severe scarring in the porta hepatis is always difficult. Kehr (1913) successfully performed three operations in which he fixed a jejunal loop to a cut section of a hepatostomy wound; similar procedures were done by others, as cited by Praderi (1982). Longmire and Sanford (1948) performed a similar operation, resecting the end of the left lobe of the liver and anastomosing it to a jejunal loop. This technique, although popular for a short time, was complicated by stenosis and has fallen out of favor.

Goetze (1951) developed a procedure of transanastomotic drainage with a catheter that went through the hepatic parenchyma, the anastomosis, and the jejunal loop. Goetze’s contribution was apparently forgotten but was reinvented and popularized by others, including Praderi in 1962 (Praderi, 1982). Praderi argued strongly that Goetze’s procedure was the answer to difficult procedures in the high biliary tract but conceded that the development of transhepatic percutaneous cholangiography (Okuda et al, 1974) allowed for the development of transhepatic percutaneous methods for intubation and dilation of the biliary tract, which are now common procedures throughout the world.

The greatest advances in techniques for repair of biliary injuries came from two sources. At the Lahey clinic in the United States, three generations of famous surgeons headed by Lahey, Cattell, and Warren perfected the reconstruction of the common bile duct as an immediate or delayed procedure and splinted their anastomoses with a variety of tubes (Estefan et al, 1977). The results of these techniques were unsatisfactory, with numerous recurrent strictures. However, following the detailed study of the anatomy by Couinaud in France (1954), Hepp and Couinaud (1956) and Soupault and Couinaud (1957) developed techniques for direct biliary–enteric anastomosis, either to the left hepatic duct or to the segment III duct of the left liver. These surgical techniques have become widely accepted and are used throughout the world (Bismuth & Corlette, 1956; Bismuth et al, 1978; Voyles & Blumgart, 1982; Warren & Jefferson, 1973).

Pancreas

Like liver surgery, pancreatic surgery developed largely as a result of responding to wounds inflicted in wars. Claessen (1842), Ancelet (1866), Da Costa (1858), and Nimier (1893) documented the early development of pancreatic surgery. In 1923, Harmann wrote an extensive review of the French, German, and English literature. Early efforts at elective pancreatic surgery largely revolved around drainage of cysts (Thiersch, 1881). In 1883, Gussenbauer marsupialized a pancreatic pseudocyst, and the patient survived. Other surgeons, including Senn (1886), soon performed similar procedures.

Direct anastomosis of the pancreas to the gastrointestinal tract followed in the early part of the twentieth century, when Coffey (1909) performed an anastomosis of the tail of the pancreas to the small bowel. Ombredanne (1911) anastomosed a pancreatic cyst to the duodenum, and Jedlicka (1923) anastomosed a cyst to the posterior wall of the stomach. Chesterman (1943) performed a cystojejunostomy, and König (1946) carried out the same operation to a Roux-en-Y loop of jejunum.

Operations for pancreatic tumors were being done at about the same time. Ruggi (1890) reported a resection of a large lesion of the tail of the pancreas, and Briggs (1890) performed a similar operation. Biondi (1897) reported resection of a tumor arising from the inferior part of the head of the pancreas, and the patient was still alive 18 months later.

Whipple (Fig. 7) and associates (1935) published a technique for cephalic duodenopancreatectomy, done in two stages, for cancer of the ampulla of Vater. In the first operation, they performed a cholecystogastrostomy and gastroenterostomy. In the second and subsequent procedure, they resected the head of the pancreas with a portion of the duodenum without anastomosis to the stump of the pancreas, which they sutured. Whipple (1941) subsequently performed this operation in one stage and reported 41 cases with a mortality of 27%. Eventually, the technique of this operation was perfected. Although English-speaking surgeons throughout the world continue to call this operation “Whipple’s operation,” the procedure had been done many years before.

FIGURE 7 Allen O. Whipple (1881–1963), surgeon.

Sauve (1908) reviewed the literature on pancreatectomy and reported that several surgeons had resected small tumors from the head of the pancreas, and larger ones from the body of the organ, without touching the duodenum. Codivilla of Italy is reported to have resected the duodenum and head of the pancreas and performed a cholecystojejunostomy in 1898, but the patient died in the postoperative period. The first surgeon to perform cephalic pancreaticoduodenectomy successfully was Kausch, a professor of surgery in Breslau and later in Berlin. On June 15, 1909, he performed a cholecystojejunostomy on a jaundiced 49-year-old man; on August 21, 1909, Kausch reoperated, performing a posterolateral gastroenterostomy and resection of the head of the pancreas with the tumor, the pylorus, and the first and second part of the duodenum. He anastomosed the third portion of the duodenum to the pancreatic stump. Kausch (1912) published a report entitled “Cancer of the Duodenal Papilla and Its Radical Treatment.” He gathered in that publication all reports that included excisions of the papilla. Tenani (1922) reproduced this operation with success, also in two stages but with one difference: Tenani performed a choledochojejunostomy, and the patient survived 3 years. Kausch and Tenani, although cited by Whipple (1941), are generally ignored in the English and American literature.

Resection later was extended to deal with cancers of the common bile duct and of the duodenum (cancers of the proximal bile duct are described subsequently in the section on liver surgery). Recognition of endocrine tumors of the pancreas later led to operations for these conditions. Wilder and colleagues (1927) reported the first case of resection of an insulinoma arising from the islet cells of the pancreas. Mayo operated on a patient in whom he found a tumor of the pancreas with metastases to the liver, and an extract from one of the metastases produced an insulin-type reaction when injected into a rabbit. Graham and Hartman (1934) reported subtotal pancreatectomy for hypoglycemia, and total pancreatectomy was performed by Priestley and colleagues (1944) for a patient in whom there was proven hyperinsulinism, but no tumor of the pancreas was to be found. The patient was cured by the operation, and the small tumor causing the syndrome was discovered during the pathologic examination.

Later, Fallis and Szilagyi (1948) performed total pancreatectomy for cancer, and this procedure was developed further in the hope that total removal of the gland would reduce morbidity and mortality and perhaps lead to better results. ReMine and colleagues (1970) and Brooks and Culebras (1976) adopted this approach, but early suggestions regarding efficacy were not fulfilled, and total pancreatectomy for pancreatic cancer has largely been abandoned. Fortner (1973) described the even more extensive procedure of regional pancreatectomy. The operation included an extensive total pancreatectomy and resection of the pancreatic segment of the portal vein—and sometimes the hepatic and superior mesenteric arteries, if these vessels were invaded by tumor—together with subtotal gastrectomy and regional lymph node dissection. Fortner’s results have not been reproduced by others.

Surgery for pancreatitis also developed over the same period, and the severity of acute pancreatitis was recognized. Ockinczyc (1933) revealed the frustration of the times when he advocated “the use of drainage of the pancreas and hope.” Because the mortality of emergency surgery reached 78%, the conservative approach to acute pancreatitis was advocated. Nevertheless, some patients with acute pancreatitis still came to operation because of the necessity to treat gallstones and pancreatitis or to deal with complications, such as abscess and pseudocyst (Cattell & Warren, 1953).

The development of intensive care, antibiotics, and better metabolic management of patients with acute pancreatitis led to improvements in outcome, although the death rates remained unacceptably high. Ranson and colleagues (1976) and Imrie (1978) made important contributions in that they defined the evaluation of the severity of an attack. The surgical treatments of abscess and peritonitis were made systematic. The role of gallstones in acute pancreatitis was defined, particularly by Acosta and Ledesma (1974), and endoscopic papillotomy to extract calculi impacted at the papilla of Vater was also described.

Surgical procedures aimed at the treatment of chronic pancreatitis had been developing since the beginning of the twentieth century. As mentioned previously, Coffey (1909) had anastomosed the tail of the pancreas to a loop of jejunum, and in 1953, Link reported external drainage of a pancreatic duct in a patient who lived for a prolonged period but expelled calculi periodically from the fistula tract. Roget (1958) described 50 cases treated this way, but only a few patients were cured by drainage. Doubilet and Mulholland (1948) attempted sphincterotomy in the treatment of pancreatitis. As a result of the success of cystojejunostomy in the treatment of pancreatic pseudocyst mentioned earlier, Cattell in 1947 used a side-to-side anastomosis between a loop of jejunum and the pancreatic duct in an attempt to relieve pain in a patient with cancer of the head of the pancreas. Subsequently, Longmire and associates (1956) carried out end-to-end pancreaticojejunostomy to a Roux-en-Y loop of jejunum; however, this procedure proved unsuccessful. Du Val (1957) performed a similar operation in an attempt to drain the pancreatic duct, but this too was unsuccessful.

Leger and Brehand (1956) and von Puestow and Gillespy (1958) performed pancreatic ductal drainage in chronic pancreatitis patients for the relief of pain. Longitudinal opening of the pancreactic duct allowed better decompression after anastomosis to a jejunal loop. Mercadier (1964) performed a similar operation without the need for splenectomy, and further technical variations were introduced more recently by Prinz and Greenlee in 1981 and by Frey and Smith in 1987. Mallet-Guy (1952) and Mercadier (1964) performed resection of the left pancreas for chronic pancreatitis. This approach subsequently was extended, so that only a small portion of the head of the pancreas remained. A more modern approach aimed at conserving pancreatic parenchyma has since been developed (Beger et al, 1985) and was further promoted by Buchler and collegues (Di Sebastiano et al, 2007).

Major Hepatic Resection

Wendell (1911) was the first to perform a successful right hepatic lobar resection using hilar ligation. Nevertheless, his achievement was lost to his colleagues for many years, and it was not until the detailed anatomic studies of Hjortsjo in 1951, Healey and Schroy in 1953, and Couinaud in 1954 that the concept of segmental anatomy as originally described by Rex and Cantlie was finally accepted. Couinaud’s (Fig. 10) seminal work in 1954 simplified the understanding of segmental liver anatomy and made it easily applicable by numbering the liver segments I through VIII. Goldsmith and Woodburne (1957) used a different nomenclature but subdivided the liver similarly. Subsequent refinements in the description of the liver were offered by Couinaud (1981) in a monograph, which contributed greatly to the understanding of practical surgical anatomy.

FIGURE 10 Claude Couinaud (1922–2008), surgical anatomist.

In 1950, Honjo published a case of anatomic right hepatectomy; the operation was performed in Kyoto, Japan, on March 7, 1949, and was later reported by Honjo and Araki (1955) in English. In 1952, Lortat-Jacob (Fig. 11) and Robert performed a true anatomic liver resection with preliminary vascular control. These reports opened the way for the development of liver surgery. Lortat-Jacob’s operation captured much attention, and many further case reports followed. As recounted by Fortner and Blumgart (2001), at the Southern Surgical Association’s meeting in the United States on December 10, 1952, Quattlebaum (1953) described a right hepatic lobectomy for hepatoma. The operation had been done about 4 months after that of Lortat-Jacob and Robert. Apparently unaware of Quattlebaum’s achievement, and thinking he would be the first to do a so-called right hepatic lobectomy in the United States, Pack at Memorial Sloan–Kettering Cancer Center in New York performed the operation on a 40-year-old woman on December 14, 1952 (Pack et al, 1955).

FIGURE 11 Jean Louis Lortat-Jacob (1908–1992), surgeon.

Pack and colleagues (1962) recognized quickly the opportunity to study liver regeneration. Their studies were the first to describe and document regeneration of the human liver after major resection and suggested that complete regeneration occurs over 3 to 6 months. Later, Lin and Chen (1965) studied metabolic function and regeneration of the cirrhotic liver and found no discernible regeneration after resection. Blumgart and colleagues (1971) described the speed of liver regeneration as recovery of liver size within 10 to 11 days after major hepatic resection for trauma.

Contrary to the trends toward anatomic precision, Lin (1958) advocated a finger-fracture technique for liver resection, removing a hepatic lobe in 10 minutes with an average of 2000 mL of blood replacement. The surgical bluntness of this approach and the absence of the customary surgical principles and techniques precluded widespread acceptance of the technique. Similarly, a prominent figure in the early development of liver surgery, Brunschwig (1953; Serrea & Brunschwig, 1955) advocated nonanatomic resection, but his results—with a very high operative mortality for so-called simple right lobectomy, mostly from uncontrolled hemorrhage—led him to accept the approach of Lortat-Jacob. Brunschwig’s report of long-term survivors after hepatic resection for advanced cancer challenged the prevailing skepticism about resecting liver tumors.

The laparothoracotomy approach of Lortat-Jacob and Robert in 1952 quickly became the standard for major hepatic resection. Opening the chest added operating time and increased morbidity but gave needed exposure to the liver. Later, the introduction of costal arch retractors made thoracotomy extension obsolete for most hepatic resections. Steps generally considered unnecessary, such as T-tube drainage of the common bile duct, were eliminated in the 1970s. Opinions were divided in the 1970s and 1980s about the superiority of either intrahepatic or extrahepatic management of the major hepatic veins. Closed drainage was substituted for multiple Penrose drains and packing, although these were still advocated by some in the 1980s. Many hepatic resections have been done without drainage, as described by Franco and associates (1989) and subsequently at Memorial Sloan–Kettering Cancer Center (Fong et al, 1996).

Methods for anatomically based segmental liver resection that conserves parenchyma were developed and have proved valuable in hepatic resection for tumor. Numerous methods to transect the liver parenchyma had been advocated, including the knife handle (Quattlebaum, 1953), nitrogen knife (Serrea & Brunschwig, 1955), electrocautery (Fortner et al, 1978), microwave tissue coagulator (Tabuse, 1979), waterjet (Papachristou & Barters, 1982), ultrasonic aspiration dissector (Hodgson & DelGuercio, 1984), and harmonic scalpel; other techniques are described on an almost daily basis, and simple crushing of the liver tissue remains in use by many.

Bleeding has remained a problem in many cases, and preliminary vascular control is difficult or impossible in some clinical settings. Inflow occlusion using the Pringle maneuver for longer than 15 to 20 minutes was considered hazardous. Local and general hypothermia was used in an effort to increase the liver’s tolerance of the presumed ischemic anoxia associated with the procedure (Longmire & Marable, 1961). More complete vascular control was obtained by Heaney and colleagues (1966), without hypothermia, by employing aortic cross clamping and temporary occlusion of the porta hepatis and vena cava for 24 minutes without ill effect. Fortner and colleagues (1971) described isolation-hypothermic perfusion of the liver, making prolonged vascular isolation for complicated resections possible. Huguet and associates (1978) challenged the long-held belief that the liver could tolerate only 15 to 20 minutes of normothermic perfusion by extending the period to 65 minutes. This observation was subsequently confirmed (Bismuth et al, 1989; Huguet et al, 1992, 1994). As described previously, however, major bleeding during liver resection usually arises from the major hepatic veins or vena cava, and development of techniques of low central venous pressure anesthesia during liver resection, as first described by Blumgart and colleagues (Cunningham et al, 1994, Melendez et al, 1998), have proved simple and efficacious and have rendered vascular isolation techniques rarely necessary (Jarnagin et al, 2002).

Apart from hepatic resection, many other techniques for the enucleation of tumors and of hydatid cysts have been developed. Garre (1907) had first noted that if he kept close to the line of the dense membrane around hydatid cysts—so as not to enter the tissues of the liver too deeply, where large vessels may be encountered—it was possible to resect such lesions with minimal blood loss. Enucleative techniques are now used by contemporary surgeons, not only for the removal of hydatid cysts but also for the enucleation of giant hemangiomata (Baer et al, 1992; Blumgart et al, 2000; Hochwald & Blumgart, 2000). As described in this book, enucleation also may be used for resection of certain neoplasms of the liver, such as fibronodular hyperplasia.

The widespread use of laparoscopic cholecystectomy led to the development of techniques for laparoscopic resection of the liver. First used by Gagner and colleagues (1992), laparoscopic partial hepatectomy has been used by many surgeons. Ferzli and colleagues (1995) and Azagra and colleagues (1996) developed the operation for anatomic resection of the left lateral segment, and most operations have involved this procedure. More recently, major hepatectomy has been performed using laparoscopic techniques. Experience is limited, however, and the indications and place of laparoscopic liver resection are under active investigation.

Liver Transplantation

Starzl (2001) has provided a fascinating overview of the origins of clinical organ transplantation. A historical consensus development conference was convened in March 1999 at the University of California, Los Angeles, to identify the principal milestones leading to the clinical use of various transplantation procedures; the conclusions were published in the July 2000 issue of the World Journal of Surgery (Groth & Longmire, 2000). The early history of the evolution of organ transplantation followed the first convincing evidence that organ rejection is a host-versus-graft immune response (Gibson & Medawar, 1943; Medawar, 1944). For further details, the reader is referred to the publications of Starzl (2001) and of Murray and Hills (2005). This portion of the review of the history of liver surgery is concerned with the history of liver transplantation.

In a magnificent leap forward, Starzl (Fig. 12) and associates (1968) in the United States did the first successful total hepatectomy with orthotopic liver transplantation. Calne and Williams (1968) in the United Kingdom reported similar studies. The contributions of both groups to the development of liver transplantation and immunosuppressive therapy have been monumental. Fortner and colleagues (1970) reported the first successful heterotopic (auxillary) liver homograft. This contribution was the forerunner of the further development of heterotopic liver transplantation and of split-liver and living related-donor transplants. Liver transplantation underwent continued evolution despite the only modestly effective immunosuppressive therapy initially available. One-year survival rates slowly reached 50% by 1979 (Calne & Williams, 1979; Starzl et al, 1979). Chronic infection, rejection, and surgical infections diminished the small group to only a few long-term survivors. The report in 1979 of immunosuppression with cyclosporine by Calne and associates (1979) transformed the field rapidly. A consensus conference held in 1983 declared that liver transplantation was now an acceptable therapy and no longer an experimental procedure. Zeevi and colleagues (1987) reported on another powerful immunosuppressive agent, tacrolimus.

FIGURE 12 Thomas Starzl (1926–), surgeon.

Serious complications of immunosuppressive therapy for liver and other organ transplants have been described, including de novo malignancy (Penn, 1988; Penn & Brunson, 1988; Penn & Starzl, 1972). In 1988, Iwatsuki and associates reported an overall 54% survival of patients at 5 years. Development was rapid, and by 1992, more than 3,000 orthotopic liver transplantations were done annually in the United States (United Network for Organ Sharing).

Total hepatectomy and liver transplantation were initially disappointing for liver cancer. Iwatsuki and colleagues (1988) reported that three of every four patients who lived at least 2 months after transplantation for cancer had recurrence, and adjuvant chemotherapy had no demonstrable benefit. Ringe and associates (1989) reported a 5-year survival of 15.2% for such patients, and Calne and colleagues (1986) had similar results. The best results and apparent cure were obtained when a cancer was an incidental finding in a liver removed for noncancerous disease (e.g., alcoholic cirrhosis). Geevarghese and associates (1998) reported an 1-year survival of 85% and a 5-year survival of 78% for such cases.

Current adjuvant chemotherapy may improve the results. Olthoff and colleagues (1995) reported a 3-year survival of 45% using fluorouracil, doxorubicin, and cisplatin, but only three survivors had cancers larger than 5 cm. Laine and associates (1999) reported five children with advanced hepatoma who were alive at a mean of 4.6 years after transplantation preceded by induction chemotherapy.

Improved immunosuppression has allowed surgical techniques to blossom. Bismuth and Houssin (1984) reported reduced-size orthotopic liver grafts in children, and Pichlmayr and colleagues (1988) reported the use of one donor liver for two recipients (split-liver transplantation). Raia and associates (1989), in a letter to the Lancet, and Strong and colleagues (1990) were the first to report living-donor liver transplantation using segments II and III of the liver; Yamaoka and colleagues (1994) reported using the right lobe of the liver. Use of split-liver grafts and living, related donors for grafts of both the right and left lobes has been driven by cultural restrictions and by a shortage of donor organs. This has been a major development, and the potential for mortality and morbidity not only of recipients but also of the live donors has remained a major ethical concern.

Liver transplantation for tumors has evolved considerably in the field of primary HCC. Although liver resection remains the treatment of choice for HCC in patients with good liver function, similar patients with compromised liver function and patients with hepatitis C and a small tumor in a portion of the liver geographically unfavorable for resection are now considered best treated by liver transplantation. Liver transplantation has come to be a recognized therapy for many patients with small HCCs (Bismuth et al, 1999), a wide range of benign disease, and in particular for patients with compromised liver function as a result of cirrhosis of the liver, Budd–Chiari syndrome, polycystic liver and kidney disease, sclerosing cholangitis, and for patients with a wide variety of other parenchymal and metabolic liver diseases. Liver transplantation for patients with hilar cholangiocarcinoma is under investigation and is occasionally indicated for patients with widespread neuroendocrine metastatic disease of the liver. Patients with metastatic disease from adenocarcinoma have had poor results, and transplantation is no longer used for this indication.

In writing this historical account, I have drawn freely on the work of the following excellent publications: Chakravorty and Wanebo (1987), Glenn (1971), Praderi (1982), and Starzl (2001). I have no doubt that there will be some inaccuracies and disputed claims as to “firsts,” but I have attempted to relate a fascinating surgical story. I apologize for any disagreement I may ignite.