Aust. N . Z . J . Surg. 1990, 60,

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SURGICAL HISTORY LIVER SURGERY: THE PAST 2000 YEARS K. J. HARDY Univei-sity o j Melbourne Department of Surgery, Austin Hospital, Heidelberg, Victoria Liver surgery has grown over 2000 years from the mystic hepatoscopy of the Babylonians to the ultimate of orthotopic transplantation by Starzl in 1968. The first successful liver resection was for trauma by Hildanus in the 17th century. The first successful planned resection was by Langenbuch in 1888 and the first heniihepatectomy by Wendel in 191 I . The principles of liver regeneration and liver haeinostasis were determined in the period 1880- 1900: Ponfick, Mayer, Kousnetzoff, Pensky and Pringle made significant contributions. Couinaud and Healey and Schroy popularized segmental anatomy; Lortat-Jacob and Robert performed the first inflow ligation resection and started the modern era. Starzl brought liver transplantation to its current status and Bismuth introduced hepatobiliary units as a means of optimizing treatment of liver disease.

Key words: haemorrhage control, liver anatomy, liver surgery. Introduction

Liver surgery has been relatively late in developing. A revolution in this surgery has occurred in the past two decades.’ The liver was regarded as a mystical organ, full of blood and fearsome to operate upon. The history of liver surgery consists of a number of phases: the times of myths and speculation, the recording of isolated extraordinary events and then, at the turn of the century, a sudden appreciation of the natural history of liver pathology and of liver regeneration. Finally, methods of haemorrhage control and adequate exposure were developed. Without these last two developments, surgical procedures on the liver could not be contemplated, even though anaesthesia and Listerian principles of antisepsis had been introduced some 50 years earlier. The next phase was of planned liver resection with inflow occlusion. This method spread and evolved with the application of precise anatomical studies and scientific technology. Liver transplantation came of age and can be regarded as the ultimate step. The histories of biliary reconstruction and portal hypertension are considered separate topics of their own. The reader will be taken through aspects of the noteworthy steps the bold, the inventive and the experimental - made by surgeons. Myths and speculation

It is fascinating that two special aspects of liver surgery, massive venous bleeding and the remarkable powers of the liver to regenerate, feature in Correspondence: K . J . Hardy, University Department of Surgery, Austin Hospital. Heidelhcrg. Vic. 3084. Australia. Acccpted for publication X Dcccmhcr 1YXY

Greek mythology. For the first, one of the greatest of bards, Homer, sang that ‘Achilles stabbed with his sword at the liver, the liver was torn from its place, and from it the dark blood drenched the fold of his tunic and Troy’s eyes were shrouded in darkness and the light went out.’’ In relation to liver regeneration, there is the tale of the supreme trickster, the fire-god Prometheus, who made Man from clay, gave Man fire and, when Zeus, king of the gods, deprived them of it, stole fire back from the forge of Hephaestus. Prometheus then tricked Zeus into choosing the bones instead of the meat in apportioning sacrifices at feasts. To avenge himself, Zeus sent Pandora and her evil box to Man and had Prometheus chained to a rock in the Caucasus by Hephaestus. Here an eagle fed by day on his liver, which regenerated each night.’ The event is made famous in the painting by Titian. The Babylonians (around 3000 BC) regarded the liver as the seat of the soul: their word for liver meant ‘life’. Superstitions were stoked by an art called hepatoscopy - a soothsayer divining the future by reading the liver.4 Early writings on liver surgery concern recommendations of abscess drainage only. For instance, Hippocrates, and then Celsus, recommended incision of liver abscesses which were probably amoebic.’ The literature is then quiet until the 17th century. Isolated extraordinary events

One of the earliest recorded successful liver operations was by Hildanus in the early 17th century (Fig. 1 ) . A young man fell and accidentally stabbed himself in the upper abdomen with a knife he was carrying. A large piece of liver protruded from the wound and there was a massive haemorrhage. Fabricus Hildanus excised the piece of liver and the

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patient survived. Three years later the patient died and a post niortcm showed scar tissue on the livciand an absence o f part of thc livcr, while the remainder was healthy." A similar episode is recorded for Bena in 17 16. The segmental anatomy of the liver was described by Francis Glisson from Cambridge in 1654 (Fig. 2).' This wiis to be the basis of modern liver surgery but was foi-gotten for 300 years. There is then ii gap in progress until thc 19th century. In 1870. during the Franco-Priissian war. Brtins successfiilly excised a section of the liver of a fellow surgeon who had suffered a gunshot wound." Until this time liver wounds WCI-cconsidered fatal and even thotigh the indic:itions (or operation were plain, because of severe hncniorrhagc, no attempts were made to control it stirgically. Toward the end of the 19th century the situation began to change as surgeons took on the challenge of liver surgery. 111 I887 Burckhardt pachcd a stab wound o f the liver to stem hacmorrhage; the patient survived. "I One year later ~ i I I c t tperformed thc first successful laparotoniy lor liver trauma. The standard method of treatment was observation. Rcports werc beginning to appear of planned surgical operations. i n America by Keen in 1887 (Fig. 3 ) and Dalton i n 1888, in Italy by Postcmski in 1885. and in Germany by Burckhardt in I887 arid Vollbrecht i n 1888."'.1'~i'A classic paper i n 1887 by Edlcr reviewed reports of 543 patients with liver injuries. If' All were managed without operation. Hc grouped the liver trauma into subcutiineotis (now described a s blunt) and open. His findings are interesting: the causes were falls from a height. gunshot wounds and stabs; the right lobe was damaged six times more lrequcntly than thc left and the convex surface twice ;is frequently a s the concave; the overall mortality was 06'%,.being 78'% for subcutiineous injuries (blunt) and 38% lor open injuries.

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Fig. I . Fahricua Hildanus (1560-1634). English surgeon, physician and nobleman, Courtesy Royal College oT Suryeons of Enyland.

Basic science considerations As sur-geons explored the livcr, the concept of

regeneration and haemorrhage control based on anatomical considerations began to be utilized. General anaesthesia, introduccrl in 1846. and antisepsis. introduced in 1865. had allowed a rapid advance in surgery but pi-ogress with the livci- was slow. This wiis because little was known :thotit how much liver tissue the body could lose without fatal consequences and any hacmorrhage that occurred was considered uncontrollable; an infection was considered universally fatal. In the last two decades of the 19th ccntury this changed Ponfick realized

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also observed that bile secretion was maintained after resection. This opened the door for the concept of elective liver resection. With respect to haemorrhage control, Maycr analysed liver wounds and found a mortality of59‘%, instead of the expected 100%”. This was confirmed by Tillmanns, who removed wedge-shaped pieces of liver from 12 rabbits under Lister’s antiseptic spray. “I All recovered and he was surprised at the small amount of bleeding; he concluded that liver wounds were only dangerous when large vessels were involved. So it was realized that the natural history of liver injury was that most stopped bleeding spontaneously and only when major vessels were damaged was therc protracted bleeding. ’() However, two reports in particular alarmed surgeons and retarded progress because of the severe blccding they described. An adenoma of the liver ‘about the size of a man’s head’ was excised by Escher in 1886. Therrnocautery was used to cut the blood base of the turnour but produced profuse bleeding; the divided surface was then stitched to the abdominal incision but the sutures pulled out and the patient died of bleeding 6 hours later.” The second was the excision by Langenbuch in I888 of a ‘constricted’ lobe weighing 370g (Fig. 4).” He blamed the wearing of corsets for the constriction. A massive secondary haeniorrhage occurred and, at re-exploration, a vcssel of the hilum was found to be bleeding and was ligated. and the patient recovered.



Fig. 3. William W. Keen (1837-1932), Contract Surgeon Army Medical Department, Philadelphia, USA. Courtesy Royal College of Surgeons of England.

Haernorrhage control and adequate exposure

Fig. 4. Carl Langenbuch (1846-1901), Chief. Lazaruskrankenhaus. Berlin. Courtesy Royal College of Surgeons of England.

The great name surgeons of the late 19th century and early 20th century had the same problems of controlling bleeding and obtaining adequate exposure as today. Steps were tentative but extraordinarily inventive. Positive pressure anaesthesia was still more than 50 years away. Methods of haemorrhage control were of the pedicle, of the surface and of inflow. Thoughts that seem peculiar now had a strong folklore and impeded progress; for example, it was thought that the contents of the abdomen should be sutured to the abdominal wound after surgery and that the blood vessels of the liver were too friable to tie. Suture of the liver to control bleeding was recommcnded by Postemski in 1885 and the Italian experience during this period was considerable. “ In 1897 De Gaetano had collected 40 reports of operations by Italians for wounds of the liver, and in 1901 Giordano collected 257 cases, of which I15 had been dealt with by ltalian surgeons.’”.’‘ Discussion began on the most suitable method by which to suture the liver. In 1896 Kousnetzoff and Pensky introduced a method considered to be a major advance at the time.’s A blunt-ended needle was

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used with a double thread and passed through the whole liver in a continuous manner above the resection line; the loops were then cut and tied. As sutures pulled into the soft liver tissue a series of ‘guards’, such as fascia1 wrapping of the whole liver and magnesium plates, were devised to prevent this.’6 Von Eiselberg, Keen, and Kousnetzoff and Pensky favoured individual ligation of bleeding vessels on the cut surface, but massive bleeding made this difficult. Iz2’ A series of inventive methods was developed: steam, hot air, liquid air, decalcified bone to the surface, specially designed sutures and compression forceps on for 24 hours.” Mikulicz suggested pressure and adrenalin. The pedicle of the resection was first handled by thermocautery and then by elastic ligature compression of the stump which was attached to the abdominal wall with the tourniquet secured by fixation pins. This was followed by recommendations that the stump be ligated with silk or catgut and later be transfixed. Tampons and packs were used, held by sutures across the capsule whenever possible. Then followed the stimulating paper by Hogarth Pringle (Fig. 5 ) in 1908.’’ This paper is remarkable because the eponym of ‘Pringle Pinch’ survives when all the patients described in this paper died.

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Fig. 5. J . Hogarth Pringle, FRCS (1863-1941). Surgeon, Royal Infirmary, Glasgow. Courtesy Hospital Administration, Royal Infirmary, Glasgow, Scotland.

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Pringle had independently thought of occlusion of the portal triad by finger and thumb: the ‘Pringle pinch’. This was to stop bleeding temporarily so that the liver surface could be viewed and the appropriate haemostasis made. Langenbuch had considered this approach but rejected it after rabbits failed to survive in the experimental situation.” He recommended occlusion of the superior and inferior mesenteric arteries during portal vein occlusion, to prevent venous intestinal stasis. Pringle rejected the arterial occlusion. He travelled from Glasgow to the Institute of Pathology in Vienna to test his hypothesis and repeated the portal triad occlusion of up to an hour in 4 rabbits, all of which survived. Pringle then concluded that this temporary occlusion was a safe procedure. In 1887 Loretta resected a hydatid cyst and sutured the capsule across the liver to close the raw area2’ Clamps were first used solely during an operation by Clementi in 1891 when he resected an abdominal fibrosarcoina attached to the liver; 9 X 5 cm of liver was excised.’9 The second significant concept at this time was that of adequate exposure, especially for trauma to the posterior superior segment of the liver. It is interesting to recall some of the exposure procedures used 90 years ago. It was recommended that the laparotomy incision be parallel with the costal arch and in a transverse direction to obtain access to the right lobe of the liver. A midline incision was recommended for left lobe lesions. In addition, a costal flap was recommended with division of the 1 Ith and 12th ribs to raise this flap. It was also recommended that, if the convex surface of the liver was damaged, strong traction be made on the round ligament and the suspensory and lateral ligaments divided, especially the triangular ligament, taking care not to divide the vena cava. Both Langenbuch and Pringle suggested division of the coronary and triangular ligaments for posterior lacerations of the liver. As their scissors were too short, the ligament was divided mainly by tearing. This proved difficult and both carried their incision through the costal margin in two places and pulled a flap of diaphragm upward. Once the chest could be opened and the transverse incision with a vertical extension became popularized the big advance was the use of self-retaining retractors fixed to the operating table. Of these the DeBergeret is perhaps the simplest, the most useful and the cheapest. So, by 1900 many fundamentals of hepatic injury had been established: smaller wounds tended to stop bleeding spontaneously, the liver regenerated rapidly, massive haemorrhage could be controlled by a variety of suture techniques, temporary occlusion of the portal triad gained control of haemorrhage while packs gained haemostasis. By 1912 Thole was able to obtain the records of 680 patients

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who had had operations for liver injury .30 The mortality for liver wounds in World War I was about 66Y0." There was then little advance in this area until the past two decades. The mid-20th century saw hepatic artery ligation and portal vein occlusion of more than 15 minutes regarded as a guarantee for liver necrosis and packing as close to malpractice."'

Resections In 1898 Cantlie denionstrated that the liver was divided into a right and left half by a principal plane between the fossa of the gall bladder and thc left of the inferior vena cava, and not at the falciform ligament ." The history of the descriptive anatomy of the liver has been outlined previously in this journal .33 The next step in liver surgery following the resections of Langenbuch was the planned resections of Keen and Wendel.'2.'2.34 In 1899 Keen excised the left lobe and packed the Liver for 24 hours; a biliary fistula followed but the patient survived. I' Wendel performed the first successful 'hemihepatectomy' in 191 I.34 He used the concept of right and left halves and ligated the right hepatic artery and right hepatic duct proximally before dissection. The right portal vein was not ligated, for fear of thrombosis. The patient had a hepatoma and died 9 years later. In 1948 Raven started to apply anatomical principles when he resected electively the left lobe of the liver through the plane of the falciform ligament for

metastatic carcinoma of the colon. However, it was not until 1952 that the concept of resecting through liver according to its anatomical planes was reintroduced. This was by Seneque, who performed a left hemi-hepatectomy for hydatid cysts, and LortatJacob and Robert who resected the right half of the liver and the quadrate lobe for neoplasm, initially ligating the right hepatic artery, duct and portal vein.'"37 Shortly afterwards a number of workers described the intrahepatic anatomy: Couinaud (Fig. 6); Healey, Schroy and Sorenson.3x.3' Only after the foundation of such anatomical principles could resection for trauma with survival proceed. The 'finger-fracture' technique was recorded first by Keen, who stripped the liver capsule with his thumb.12 But the principle of this technique is gentleness, emphasized first by Anschutz in 1905 and subsequently by Couinaud in 1952.'1.3x They realized that liver tissue is very soft and so gentle squeezing will display only the firm structures such as the bile ducts and vessels. This technique was popularized by using the handle of the scalpel by Quattlebaum in 1953.") Lin in Taiwan, Ton That Tung in Hanoi and also Pack used this method.4'-43

Inflow occlusion Hepatic artery ligation occurred early in the treatment of liver injuries. In 1903 Von Haberer studied this experimentally and various reports followed, such as the report by Sudek for an intrahepatic aneurysm following a gunshot wound, and by Calmerf for laceration of the liver - both patients survived.44 Other early reports of survival after ligation of a large hepatic vessel close to the liver were by Meyer, Kehr, Korte and Haberer. Few patients survive ligation of the portal vein and, although Brewer reported that he had tied it when removing a hydatid cyst, surgeons were quick to realize that it was not wise. Between 1897 and 1920 Haberer and Giorgi had success using direct suture of the damaged portal vein. The temporary occlusion principle of Pringle was advanced in 1966 by Heaney with cross clamping of the aorta below the diaphragm and the inferior vena cava below the liver, and in 1968 by atriocaval shunting by Schrock to isolate the l i ~ e r . ' ~ .It~ " has been shown that the human liver can tolerate ischaemia for up to I hour if n o r m o t e n ~ i v e . ~ ~

The modern era

Fig. 6. Claude Couinaud, MD, Surgeon, St Louis Hospital, Paris, France.

The modern era arrived with the stimulus of the Korean and Vietnam wars, liver transplantation and the application of practical anatomy and technology. This followed discussions on the merits of packing, suture, free grafts, abdominal drains and T-tube drainage of the common bile duct.'' Madding reported that in World War 11, when use of

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drains rose from 40% to 90% and use of packing dropped from 35% to 10%. the inoi-tality rate of patients with liver injuries fell from 30% to 17"h."~ The Korean and Vietnam wars produced a trend towards early operation, blood transfusion, antibiotics and direct intrahepatic haeniostasis. The anatomy o f the liver in 8 segments capable of resection was displayed by the casts of Healey, Schroy and Sorenson and the dissections of CouinaUd,3X,3'lUntil the mid- 1960s the mortality of electivc liver resection was 15% or higher. Based upon segmental anatomy knowledge, a school of liver surgeons developed in Paris: Heppe. Mercadier. Bismuth and Hotissin. Their contribution has been t h e development of specialized hcpatobiliary units and the fall of mortality rates to less than 5 % .'(I Now, technology involving ultrasonography, CT scanning and intraoperativc imaging has allowed grouping of patients into subsets of major resections and segmental resections and avoiding stirgery. In 1975, Starzl described a safe technique for ive liver resection, now with a reported operative mortality o f O'X,. ' .5' Orthotopic liver transplantation was first performed in 1963 and first successfully performed in 1968 in the USA, both by Starzl (Fig. 7)." This is the nujor advance in liver surgery in the 20th century a s the treatment of endstage liver disease. Although the culmination of all these developments has been liver transplantation, of more widespread significance is an acceptance that the liver

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Liver surgery: the past 2000 years.

Liver surgery has grown over 2000 years from the mystic hepatoscopy of the Babylonians to the ultimate of orthotopic transplantation by Starzl in 1968...
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