The British Journal of Surgery Vol. 62 : No. 6 : June 1975 Br. J. Surg. Vol. 62 (1975) 421-430
Hepatic resection* G. B . O N G A N D N . W. L E E t SUMMARY
One hundred and twenty-five hepatic resections were done in the University Surgical Unit at the Queen Mary Hospital, Hong Kong, from 1964 to I974 for conditions varying from primary hepatoma and recurrent pyogenic cholangitis to spontaneous rupture of the liver due to a bleeding haemangioma. The overall mortality was 17.6 per cent. A case was classed as an. operative death unless the patient was discharged from hospital. There has been long term survival after resection for primary carcinoma of the liver and no mortality when resection was carried out for benign conditions.
IN 1953 we performed a subtotal gastrectomy for a carcinoma of the stomach with resection of the lateral segment of the left lobe of the liver. The patient made an uneventful recovery but subsequently died of metastases 3 years after the initial operation. However, it was not until 1955 that we carried out hepatectomy for primary hepatoma with any frequency at the Kowloon Hospital, Hong Kong. All the records accumulated during the period from 1955 to 1963 were lost except for those of 1 patient who has been followed up since. Patients Over a period of 10 years, from 1964 to 1974, 125 resections of the liver were carried out; one of these, as Table I : CONDITIONS FOR WHICH LlVER RESECTION WAS CARRlED OUT, 1964-74 Sex Age (yr) Range M F Ratio Pathology Average 50 59 11 5 : 1 94 mth-85 yr Hepatocellular carcinoma 20-77 Recurrent pyogenic 15 23 1 : 2 49 cholangitis 3 : 1 17-52 35 3 1 Trauma 0 2 0 :2 63-76 70 cyst 3 1 3 :1 Liver abscess 45-59 5' 1 2 1 :2 58-75 Carcinoma of colon 47-58 Carcinoma of intra- 2 0 2 : 0 hepatic duct Leiomyosarcoma 0 1 0 : l 44 of jejunum 0 1 0 : l 43 Ruptured haemangioma
z;
31
mentioned, was done at the Kowloon Hospital, the remainder being performed at the Queen Mary Hospital, Hong Kong. There were 83 males and 42 females, giving a sex ratio of 2 : 1 . Lesions of the liver requiring resection Table I shows the conditions for which liver resection was carried out. Primary carcinoma of the liver There was a total of 70 cases of carcinoma of the liver where resection was possible; of these, 9 were cholangiohepatoma and 61 hepatocellular carcinoma. Of the 61 cases of hepatocellular carcinoma, cirrhosis was present in 35, while among the cases of cholangiohepatoma it was found in 3. The incidence of hepatocellular carcinoma with cirrhosis of the liver has been reported as 73.1 per cent (Tull, 1932) and 89 per cent (Stewart, 1931). Hou (1958) found that of the 66 per cent of his series with primary liver cancer associated with cirrhosis, 46.5 per cent also had clonorchiasis. Wang and Li (1963) studied 130 resected cases of primary carcinoma of the liver and reported an association of primary cancer with cirrhosis in all except 2 cases. This is of importance as the cirrhotic liver does not take kindly to resection, for even when the liver is mildly cirrhotic but the resection extensive the patient often succumbs to liver failure. Lin (1966) stated that when the liver is cirrhotic, right or left hepatectomy is contraindicated. While it is true that massive resection in a cirrhotic liver often ends in liver failure, at times the resected liver is found to have verv little functioning tissue. Hence., a heDatectomy in such cases is still compatible with survival. Eighteen out of the 70 cases were admitted because the hepatoma had ruptured. The mechanism of rupture has been previously biscussed (Ong et al., 1965; Ong and Taw. 1972). As a 'result of cirrhosis a number of patients developed portal hypertension, and the resulting bleeding could have been the cause of death in the postoperative period. I
* Based on a lecture delivered at the Repatriation Hospital, Concord, New South Wales, Australia. t Department of Surgery, University of Hong Kong, Hong Kong. 421
G. B. Ong and N. W. Lee Recurrent pyogenic cholangitis Some cases with recurrent pyogenic cholangitis reqi:ire resection of the liver. In the present series it was done for intrahepatic stones which most frequently formed in the lateral segment of the left lobe. The bile ducts were thickened, dilated and contained infected bile with stones (Fig. 1). The liver parenchyma showed degeneration and was often shrunken to such an extent that it was almost a fibrotic bag. There was usually a stricture at the junction between the medial and the lateral segments of the left lobe and this was possibly the cause of stone formation in the liver. As the bile was invariably infected, resection of the liver often resulted in subphrenic abscess or biliary fistula and occasionally septicaemia. Altogether 38 such cases were subjected to resection of the liver. Trauma to the liver Although the incidence of trauma to the liver is increasing owing to more road traffic accidents, the number of cases that require resection is relatively small. In the 10 years of this study there were only 4 cases in which it was necessary to remove a lobe of the liver. In 2 of them the right lobe of the liver had a stellate fracture which compromised the blood supply so that it was necessary to remove this lobe. In 1 patient the right lobe had a linear fracture which was repaired, while the lateral segment of the left lobe was removed. In the remaining patient the fracture was over the medial segment of the left lobe and it was necessary to perform a resection because of necrosis. These patients were relatively young when compared with the patients with other conditions necessitating hepatectomy . cysts There were 2 patients with a cyst in the left lobe of the liver; both patients were elderly females. The cysts were simple and did not contain any malignant tumour. Liz;er abscess During the last 5 years of the study 4 cases of liver abscess were seen. In 1 case an extended right hepatectomy was carried out because the abscess was mistaken for a carcinoma of the liver. On examination, the resected liver contained hardly any normal liver tissue (Fig. 2). In another case a right hemihepatectomy was carried out because of haemorrhage into the abscess. Both of these cases were subsequently proved to be amoebic liver abscesses. In addition to these cases there were 2 cases of liver abscess which had initially been drained and subsequently developed a discharging sinus. No amoebae were demonstrated either in the pus or in the wall of the abscess in these cases. Culture was originally sterile, but after drainage pyogenic bacteria were isolated. These were probably the cause of the discharging sinus (Fig. 3). Carcinoma of the colon with metastases to the liver There were 3 cases in this group; 2 females and 1 male. The male and 1 female patients had a carcinoma of the hepatic flexure which had invaded the right lobe of the 422
liver; t h e rest of the liver was normal (Fig. 4). The third patient had a carcinoma of the sigmoid colon with metastases to the medial segment of the left lobe. The liver was also cirrhotic. Carcinoma of the bile ducts There were 2 cases of carcinoma of the right hepatic duct. The patients were markedly jaundiced; the liver was not cirrhotic but was deeply stained. Both were males, one aged 47 and the other 58. Histologically, the tumours were shown to be adenocarcinoma arising from the right hepatic duct. Leiomyosarcoma of the jejunum In 1 case a leiomyosarcoma of the jejunum was found with secondaries in the right lobe of the liver. The rest of the liver was normal. Bleeding haemangioma A case of bleeding haemangioma was seen in this series. A huge cavernous haemangioma arising from the right lobe of the liver and extending to the medial segment of the left lobe occurred in a female patient. The rest of the liver was normal. The left lobe was rather hypertrophic and the cut section of the resected specimen showed there were some fibro-fatty tissues at the centre (Fig. 5).
Clinical features Abdominal mass This was by far the most common finding in the patients undergoing liver resection. It was present in all the patients with primary carcinoma of the liver, and in addition the 4 cases of liver abscess also had a mass palpable in the upper part of the abdomen. The patients with a cyst presented with a mass in the upper abdomen which moved with respiration and was nontender. In carcinoma of the bile duct the palpable mass in the upper quadrant could be identified as a uniformly enlarged liver. The patient with secondary leiomyosarcoma also had an enlarged liver with irregular masses studded over it. Abdominal pain Abdominal pain was a constant finding and was usually confined to the right upper quadrant, occasionally radiating to the back or referred to the shoulders. This was present in the majority of the patients with carcinoma of the liver and in the patient with a ruptured haemangioma. The pain was rather sudden and was described as ‘bursting’ in nature in all cases of ruptured hepatic tumour. Sometimes it was associated with the rapid onset of shock. Intraperitoneal haemorrhage This occurred in 18 cases of ruptured carcinoma of the liver. Traumatic rupture of the liver produced intraperitoneal haemorrhage with very severe pain and the patient rapidly went into shock. The amount of fluid varied. In primary hepatoma ascites might be present, and any bleeding, even if severe, would yield only heavily bloodstained fluid on paracentesis.
Hepatic resection
Fig. 3. Persistent sinus after drainage of a liver abscess which was treated and cured by resection.
Fig. 1. Resected specimen of the lateral segment of the left lobe of a liver. The ducts are dilated, fibrotic and contain stones.
Fig. 2. Specimen of destroyed liver due to amoebiasis. There is hardly any normal liver tissue.
Fig. 4. Carcinoma of the hepatic flexure invading the right lobe of a liver. This was treated by right hepatectomy and right hemicolectomy.
423
G. B. Ong and N. W. Lee
occasionally demonstrated displacement stomach, indicating a hepatic mass.
of
the
Splenovenography The usefulness of this investigation lies in the fact that the portal vein may be obliterated as a result of tumour invasion. Should the obstruction extend beyond the bifurcation of the portal vein, then surgical treatment is contraindicated. Portal hypertension is also demonstrated by this procedure. Hepatic arteriography Hepatic arteriography is useful in differentiating a malignant lesion with new vessels from a benign one, when the vessels are only displaced. Fig. 5. Bleeding haernangioma of the liver.
Weight loss Weight loss was found in 37 of the 70 cases of primary hepatoma. It was not found in recurrent pyogenic cholangitis, traumatic rupture, cysts or in the case of a ruptured haemangioma. A variable degree of weight loss was noticed in carcinoma of the colon with liver secondaries, while the patient with carcinoma of the bile duct had marked loss of weight. The patient with leiomyosarcoma of the jejunum had also lost weight. Anorexia Approximately half the patients with primary hepatoma complained of anorexia. It was also present in the patients with recurrent pyogenic cholangitis, liver abscess and other malignancy, but was absent in these with traumatic rupture of the liver, cyst and ruptured haemangioma.
Preoperative investigations Except for emergency operations for bleeding, all the cases were subjected to laboratory investigations. Laboratory findings Anaemia was present, although of a mild degree, in all the cases of primary hepatoma. Polycythaemia in primary hepatoma, as reported by McFadzean et al. (1958), was not present in any of these patients. Leucocytosis was also an occasional finding in primary hepatoma and was noticeably absent in the 4 cases of liver abscess, while the white cell count was moderately raised in all the cases of recurrent pyogenic cholangitis. a-Fetal protein gave positive results in 70 per cent of the cases of hepatocellular carcinoma. This test was invariably negative in the patients with cholangiohepatoma. The liver function tests were of little value except in a case of carcinoma of an intrahepatic duct when the bilirubin was markedly raised. The alkaline phosphatase was not helpful except in the case with obstructive jaundice. X-ray examinafion When X-ray examination showed a soft tissue shadow at the upper abdomen a barium meal study 424
Scanning of the liver Scanning with 99Tcdoes not differentiate a malignant tumour from a benign one. When the lesion is small, scanning usually does not demonstrate any filling defect, and then it is necessary to depend on other investigations for diagnosis as a therapeutic guide. Peritoneoscopy Peritoneoscopy is a useful means of diagnosing a liver condition requiring a resection. A primary hepatoma as well as secondary tumour can be seen on the surface. Biopsy under direct vision can then be done and a histological diagnosis made of the lesion. In addition, it is useful in demonstrating the cirrhotic state of the liver. However, peritoneoscopy has many blind spots. The posterior surface of the liver is obscured by adhesions. Any centrally situated lesion will be out of the field of vision. Inferior vena cavogvam An inferior vena cavogram may occasionally be useful, especially in carcinoma when the tumour has invaded the inferior vena cava, in which case resection is contraindicated.
Preoperative preparations In most of the cases undergoing elective operation the nutrition should be maintained, and intravenous hyperalimentation will help in getting the patient fit for a major operation. A diet rich in vitamins should be given. Supplementary vitamin A in liquid solution with 10 000 units of vitamin B should be given daily, to which 500 mg of vitamin C may be added. When the prothrombin time is prolonged vitamin K SO/lOO mg may be given by intramuscular injection. A diet rich in protein with a high carbohydrate and moderate fat content should be given. Anaemia should be corrected by blood transfusion. Contraindications to operation Operative treatment is contraindicated under the following circumstances: 1. Metastatic spread: When metastases are demonstrated in the lungs or the bones, surgical exploration should not be carried out. When there are secondaries in the supraclavicular lymph nodes, particularly in
Hepatic resection cholangiohepatoma or carcinoma of the colon, operative treatment is out of the question. 2. Jaundice: The presence of jaundice is not a contraindication to operation, but may be a contraindication to resection of the liver. Occasionally an hepatocellular carcinoma will spread into the common hepatic duct and produce obstructive jaundice. In such cases resection is not compatible with a cure. S. A. T., a male patient aged 53 years, was admitted in 1969 because of obstructive jaundice. An operation was performed on 14 July 1969 when aright extended hepatectomy was carried out. He survived 5 months before dying of multiple secondaries in the remnant of the liver (Fig. 6 ) .
3 . Ascites: The presence of ascites is a contraindication to operation, as it indicates that the liver is failing and will not tolerate any operative procedure. 4. Biochemical changes : Biochemical changes showing poor liver function indicate that the patients, particularly those with primary hepatoma, with cephalin flocculation of over 3 units, bromsulphthalein retention of over 35 per cent and serum albumin below 2-5 g per cent or prothrombin time below 60 per cent, are unlikely to survive an operation and hence surgery should not be done.
Operations currently practised Lefr medial segmental resection This is an operation that is seldom carried out. It was done only twice in this series; once for trauma to the liver in which the medial segment was completely necrotic and bleeding. It was also done for a ruptured carcinomatous nodule situated in the medial segment of the left lobe. This man subsequently died of bleeding varices. The artery, portal veins and segmental duct were dissected out; these were found half an inch deep to the insertion of the ligamentum teres. The segment was then resected from in front backwards until the medial segmental hepatic vein was exposed and ligated. The segment was removed and the edges of the liver remnant were brought together. Left lateral segmental resection In performing left lateral segmental resection the left coronary ligament*was freed from the undersurface of the diaphragm. The free end of the coronary ligament contained a few small vessels and in a cirrhotic liver bled profusely. The raw area left on the diaphragm had to be sutured with atraumatic catgut. After the left lateral segment had been freed, the forceps holding its tip were depressed to expose the lateral segmental hepatic vein. A little dissection freed it from the inferior vena cava. Often the medial segmental vein joined it before they became a single vein draining into the inferior vena cava. In order to ligate the lateral segmental vein it was occasionally necessary to dissect into the substance of the liver. After its ligature and division, the liver containing the tumour or stone was rotated forwards so that the lateral segment of the left lobe was brought out of the abdomen. The segmental hepatic artery, the segmental duct and the segmental branch of the portal vein were ligated as they ran near the posterior border
Fig. 6. Secondaries which appeared in the remnant of a hypertrophic liver. Arrow points at the hepaticojejunostomy.
of the left lobe of the liver. After ligating the artery, vein and the duct, the lateral segment of the liver was ready for division. Further haemostasis of the transhepatic segmental hepatic veins could be attained by suture ligatures. Lefi hemihepatectomy In this operation the liver was divided along the principal plane dividing the right and left lobes of the liver. A Mayo-Robson incision was made and the left coronary ligament was divided and detached. The left hepatic vein was dissected out, divided between clamps and stitched as for lateral segmental resection. After division of the left branch of the portal vein, hepatic artery and hepatic duct, the left lobe of the liver became a dusky colour or sometimes even black. The division of this lobe of the liver was now made by cutting through the capsule of the liver and, with the handle of the scalpel, the intersegmental veins were teased out and ligated or stitched. The cut edge of the liver was either sutured with a series of interrupted or continuous catgut sutures, or, in most cases, after controlling the bleeding from the raw surface a piece of Surgicel was placed over it and then pieces of Gelfoam to cover the whole raw area. The Gelfoam was stitched to the capsule of the liver. This method resulted in good healing. Right hemihepatectomy Exploration of the back of the liver was first carried out. This avoids division of the structures at the porta hepatis which makes it necessary to resect the devascularized liver. If the tumour has infiltrated the inferior vena cava, resection will result in either part of the tumour being left behind or the inferior vena cava being torn beyond repair. After exploration, attention was focused on the structures at the porta hepatis. Division and ligation of these structures were performed. Next, the hepatic vein was dealt with. If the coronary ligament had been freed when the hepatic veins were explored, the liver could be 425
G. B. Ong and N. W. Lee TABLE 11: COMPLICATIONS IN RESECTIONS Complication No. Haemorrhage Biliary fistula Infection Septicaemia Subphrenic abscess Liver abscess Pleural effusion
125 LIVER
of cases
0,
/o
4
3
11
9
6 13 1
10.4
4
3
5
0.8
delivered out into the wound. In so doing, there would be a kink of the inferior vena cava. Lin (1966) believed that the kinking of the inferior vena cava would impede the venous return and could cause cardiac arrest. Hence he devised his finger-fracture technique so that the hepatic veins could be divided within the liver substance. Division and removal of the liver were then carried out in the same manner as for left hemihepatectomy. However, kinking of the inferior vena cava can be lessened if the lower hepatic veins are dissected out first and ligatured. This can be done with the liver in the abdomen, and leaves the uppermost hepatic vein which is short and can be found at the bare area of the liver. In dividing the uppermost hepatic vein over the kink of the inferior vena cava a piece of the inferior vena caval wall might inadvertently be included. If this occurred a transfixion of the vein would inevitably cause the suture ligature to slip and severe bleeding might take place. It is therefore wise, at this stage, to have ready a vascular clamp of the Satinsky type. Should such an accident happen the inferior vena cava could be clamped and sutured. Extended right hepatectomy Occasionally, a tumour is large enough to require removal of the liver to the right of the falciform ligament. The exploration and method of dealing with the hepatic veins were similar to those for right hemihepatectomy. The ligature of structures at the porta hepatis was similarly carried out. However, the left medial segmental artery and the right segmental portal vein with the segmental duct have to be dealt with in this procedure. The lateral segmental duct, artery and portal vein were preserved and found to be half an inch deep to the ligamentum teres. At this stage of the division of the medial segmental duct it would be prudent to place a T-tube into the left hepatic duct, for it would prevent damage to the lateral segmental duct. The raw surface of the liver was again dealt with either by suturing the capsule together or by placing some haemostatic agents and stitching them to the capsule of the liver. If the falciform ligament is not involved it provides a convenient piece of material to stitch over the raw surface. Extended right hepatectomy represented a removal of between 75 and 80 per cent of the liver tissue, while a right hemihepatectomy removed between 55 and 60 per cent, and removing the left half of the liver represented 45-50 per cent of liver tissue by weight. 426
Postoperative care Patients undergoing liver resection required intensive supportive treatment until the remaining liver had regenerated sufficiently to take care of the metabolic needs of the body. Broad spectrum antibiotics were given to prevent chest infection.
Care of the drain Whenever the chest was opened an underwater seal drain was inserted and removed on the third or fourth postoperative day. An X-ray of the chest was taken on the day after the operation and repeated after the drain had been removed. Subsequent pleural effusion would require thoracocentesis. A subdiaphragmatic drain was usually placed in the space formerly occupied by the resected liver. A small amount of serosanguineous fluid was always present, but occasionally there was an excessive amount of ascitic fluid in which case the drain was removed. This would prevent excessive loss of ascitic fluid. The drain occasionally might be blocked by a blood clot and therefore too much reliance must not be placed on its efficiency to demonstrate the presence of bleeding. A large distended abdomen with the patient going into shock would indicate postoperative bleeding and steps should be taken to control it. Administration of fluids After blood replacement and administration of fluid, 25 per cent glucose should be given through the inferior vena cava via a cut-down; 200 g of glucose were given daily and adequate vitamins were also administered. Oral feeding can usually be restarted on the second or third postoperative day. A high protein diet should be avoided as it has been shown by Pack and Molander (1960) that too high a protein intake might cause intoxication in a patient with massive resection of the liver. Complications These are detailed in Table If.
Postoperative haemorrhage Haemorrhage occurred postoperatively in 4 patients undergoing hepatic resection, all for carcinoma of the liver, and in 1 instance the bleeding was into the pericardium from the upper part of the inferior vena cava. The patient was explored again and subsequently made an uneventful recovery. The other 3 cases had bleeding from the collaterals resulting from portal hypertension in a cirrhotic liver. At the conclusion of the first operation there was no bleeding as every part of the raw surface had been run over with atraumatic catgut. Subsequently, further collaterals which had been missed started bleeding and they were controlled by suturing. Biliary fistula Eleven cases (9 per cent) had a biliary fistula. Four patients had undergone resection for carcinoma of the liver and in 1 instance it had been a left hepatectomy in which the duct had been closed with interrupted silk in
Hepatic resection
good approximation. However, a fistula developed. A biopsy taken at the margin showed that carcinomatous cells were still present. In one of these cases after an extended right hepatectomy a T-tube was inserted and the medial segmental duct was carefully closed with interrupted fine silk. Nevertheless, leakage occurred but the fistula healed spontaneously. Six cases had had resection for recurrent pyogenic cholangitis. In each instance the closure had been performed with interrupted silk. Subsequently, the incidence of biliary fistula was lowered by reverting back to closure with atraumatic catgut and then suturing the liver capsule over it. In 1 case the biliary fistula developed after a right hepatectomy for traumatic rupture of the liver. The fistula healed spontaneously without any further operation. Infection
Infection accounted for the greatest number of complications in the patients undergoing hepatic resections. There were 6 patients who developed septicaemia, and Gram-negative enteric organisms were cultured from the blood. In 3 of them the hepatectomy was for hepatocellular carcinoma while in the other cases for recurrent pyogenic cholangitis. Subphrenic abscess occurred in 13 patients (10.4 per cent). The abscesses usually developed following incomplete or inefficient drainage of the space left after resection of the liver. Suction drains were used but even this could not completely prevent the development of subphrenic abscess.
Y . S. K., a female patient, was admitted in 1972 because of an enlarging mass which was found to be a hepatoma involving the right lobe of the liver. An hepatic arteriogram showed that the tumour arose from the upper division of the right lobe (Fig. 7). This was confirmed by a splenovenogram (Fig. 8). Peritoneoscopy not only revealed the presence of the tumour but also cirrhosis of the liver. A needle biopsy confirmed the diagnosis of hepatocellular carcinoma. At operation it was decided that the tumour should be removed, sparing the inferior division of the right lobe. Accordingly, the segmental duct, the branch of the hepatic artery and the branch of the portal vein to this division were preserved. The rest of the right lobe was then removed. Examination of the operated specimen showed that the tumour had a narrow rim of normal tissue (Fig. 9). The patient had a postoperative haemorrhage at the site where the superior branch of the hepatic vein drained into the inferior vena cava. This had previously been stitched, but a new tear in the upper part of the inferior vena cava extending into the atrium was found at the second operation. This was sutured and the patient made an uneventful recovery. Subsequently, a hepatic arteriogram showed that this segment was functioning and scanning showed a good-sized segment. This patient has been followed up for the past 2 years and she is quite well without any evidence of recurrence of her disease or metastases (Fig. 10).
It is possible that this patient would have died had the whole of her right lobe had been removed. The amount of liver tissue that was functioning and removed at operation was minimal. Among the 70 resections for primary hepatoma 34 patients had cirrhosis of liver and there were 9 deaths, giving a mortality rate of 26 per cent. The causes of death were liver failure in 5 cases, septicaemia in 2 and hypovolaemic shock following uncontrolled haemorrhage in 2. The remaining portion of a very cirrhotic liver did not appear to be able to regenerate sufficiently to take over the function of the removed Pleural effusion Pleural effusion occurred in 4 cases and was confined segment or lobe. Furthermore, bleeding in cirrhotics, to cases of right hepatectomy in which the chest had especially from collaterals, was always profuse. Even been opened. In 2 of them the effusion kept recurring at the very early stage of resection when the liver was and malignant cells were found in the pleural fluid. In being mobilized, much blood could be lost from these 1 case a combination of right hepatectomy and collaterals. The haemorrhage could be controlled by pulmonary lobectomy caused pleural effusion of the packing and subsequently with running stitches. In an left pleural cavity. Rupture of the spleen occurred attempt to replace blood loss with massive transfusion, a coagulation defect could develop and this was often during thoracocentesis. the cause of death. Septicaemia was also much more likely to occur in Operative mortality After undergoing hepatectomy every patient who did these patients, for they tolerated infection poorly. Two not leave the hospital was considered an operative of the cases dying of septicaemia belonged to the group mortality. Thus, a case might have undergone an of patients with recurrent pyogenic cholangitis that operation and then died of liver failure 45 or 60 days required liver resection. Traumatic rupture of the liver occurred in 2 patients after operation. This would still be considered as an with multiple injuries; both patients died of cardiac operative mortality. There were 22 deaths out of 125 resections, giving arrest following irreversible shock shortly after an overall mortality of 17.6 per cent. Of these, 15 had operation. Although the resections were extensive, the had resection for primary hepatoma; 7 of these 15 died other benign conditions in this series did not give rise in the first 5 years of the series, that is, from 1964 to to any mortality. None of the patients operated on for 1969, when 22 resections were performed, giving a carcinoma of the colon with liver metastases died mortality of 32 per cent. In the succeeding 5 years, within the postoperative period. The patient with leiomyosarcoma who died of from 1969 to 1974, there were 48 resections with 8 deaths, giving a mortality rate of 17 per cent. There is cardiac failure was known to have cardiac ischaemia. Two cases of carcinoma of the bile ducts were therefore a definite drop in operative mortality. This results not only from improved technique but also from operated on; one was an extended right hepatectomy better selection of the best operation for a particular and the other a right hepatectomy. Reconstruction of case. The following case report is an example of such the biliary tract was in each instance by hepaticojejunostomy. One patient developed a subphrenic selection. 427
G. B. Ong and N. W. Lee
Fig. 9. Resected specimen of a liver showing a large carcinoma.
Fig. 7.Hepatic arteriograrn in a primary carcinoma of the liver. Note the new vessels entering the turnour. The right inferior division is normal.
Fig. 10. Patient who had had a primary hepatoma resected; ( A ) during convalescence, and ( B ) 2 years afterwards.
Fig. 8. Splenovenogram showing infiltration of cancer in the segmental vein.
abscess but both died of liver failure. Their jaundice never subsided and their condition deteriorated until they went into coma and died 40 and 48 days after operation respectively. The survivors Of the 103 patients who survived hepatic resection, 39 subsequently died from 5 to 41 months after 428
operation, the average being 10 months. All died of their original disease. One patient with recurrent pyogenic cholangitis died 18 months after hepatectomy. She developed leakage of bile through the old drainage wound which was persistent and it was necessary to explore the bile ducts to close this biliary fistula. She died of uncontrolled haemorrhage due to a coagulation defect. Carcinoma of the colon with metastases to the liver accounted for 2 deaths. One was a female patient who survived a right hepatectomy with the right hemicolectomy carried out in continuity. This patient was operated on in 1968. She survived for 18 months but eventually died of her disease. Up to the present time 64 cases are still alive out of the original 125. Table Iff shows that 19 of the patients with carcinoma of the liver are alive and the longest survival is now 13 years. This is a patient who had a left hemihepatectomy done in 1962 for a ruptured hepatoma and who emigrated in 1971. The second longest survivor is a man with hepatoma which
Hepatic resection ruptured while being investigated. An emergency extended right hepatectomy together with partial excision of the diaphragm was carried out. This patient is still alive and well. A female who was operated on for a hepatoma of the left lobe with two secondary nodules on the medial segment is alive and well today, 5 years after the operation. Of the remaining surviving patients, 1 was operated on in 1971,3 in 1972, 4 in 1973 and 8 in 1974. Of the patients with other conditions who are still alive after hepatic resection (Table I V ) , one had a carcinoma of the sigmoid colon with metastases to the liver for which a total colectomy and left medial segmental resection was carried out I5 months ago. Thirty-five of the cases with recurrent pyogenic cholangitis are still alive 6 months to 10 years after operation. Of the patients with traumatic rupture, one who had a right hemihepatectomy done 7 years ago and another who had a left medial segmental resection performed 3 years ago are alive at the present time. The 2 patients with a cyst which was treated by left hemihepatectomy have survived without problems for 2 years and 5 years respectively. Of the patients with liver abscess who were operated on, one had an extended right hepatectomy which was carried out 4 years ago. This was a patient who was operated on because of a mistaken diagnosis of hepatoma arising from the right lobe of the liver. As the lesion was soft it was thought to be a necrotic tumour. No aspiration of the abscess was carried out. He made an uneventful recovery and was discharged from hospital after 2 weeks. He has been followed up since and the liver has regenerated to its original size and he is at the present moment quite well (Fig. 11).
Fig. 11. Patient who had undergone resection of a liver abscess; ( A ) 6 months, and (B) 4 years following operation.
The ruptured haemangioma was operated upon on 6 July 1974; the patient was discharged 10 days after the operation. Discussion Certain conclusions can be drawn from the present series. Operative mortality Primary hepatoma carried the highest operative mortality, which is understandable because hepatoma is a complication of a cirrhotic liver. Islami et al. (1958) have shown that in rats with carbon-tetrachlorideinduced cirrhosis the liver remnant after resection could regenerate and function normally. However, in humans when a cirrhotic liver is resected it does not
Table 111: DETAILS OF 19 SURVIVING PATIENTS WHO UNDERWENT RESECTION FOR PRIMARY HEPATOMA Year of operation
Type of resection
Lesion
1962 1966 1969 1971 1972 I973
Left hemihepatectomy Extended right hepatectomy Left hemihepatectomy Left hemihepatectomy Right or left hemihepatectomy Right or left hemihepatectomy or extended right hepatectomy Right or left hemipatectomy or extended right hepatectomy
Ruptured hepatoma Ruptured hepatoma Hepatoma Hepatoma with cirrhosis Hepatoma with mild cirrhosis Hepatoma, 2 with and 2 without cirrhosis
1974
No. of cases
Hepatoma with or without cirrhosis
Table IV: DETAILS OF SURVIVING PATIENTS WHO UNDERWENT RESECTION FOR CONDITIONS OTHER Length of THAN PRIMARY HEPATOMA No. of survival to Lesion
Type of resection
cases
Carcinoma of sigrnoid colon with metastasis to liver Recurrent pyogenic cholangitis Traumatic rupture Liver cyst Liver abscess
Total colectomy with left medial segmental resect ion Left lateral segmental resection Right hemihepatectomy, left medial resection Left hemihepatectomy Extended right hepatectomy Left hemihepatectomy Right hemihepatectomy Right hemihepatectomy
1
Ruptured haemangioma
35 2 2 1
date 15 mth 6 mth-10 yr 7 and 3 yr 2 and 5 yr 4-9 yr
2
1 1
10 d
429
G . B. Ong and N. W. Lee
regenerate into a normal functional unit. There may be islands of regeneration. In fact, the hepatoma most probably arises from one of these regenerated nodules. As hepatocellular carcinomas are always at an advanced stage when first seen, massive resection is often required. If cirrhosis of the liver is severe, massive resection will always end in death from liver failure. However, with proper selection of cases and correct application of operative treatment the mortality rate should be reduced to an acceptable level. From 1964 to 1969 the operative mortality from hepatic resection for primary hepatoma was 32 per cent. In 1974 there were 9 resections for primary carcinoma of the liver with only 1 death, a mortality of 11 per cent. Lin (1973) reported a mortality rate of 11.9 per cent in a series of resections for primary hepatoma of the liver. Further, he gave a figure of 19.1 per cent for 5-year survival. Hepatic resection for secondary carcinoma should carry a very low mortality. In 3 resections for metastasis from carcinoma of the colon there was not a single death. When resection is carried out for a benign non-infective condition there should be no mortality, as shown by results for the cysts and the bleeding haemangioma in the present series. However, when the operation is performed for infected bile ducts with intrahepatic stones, then the mortality is 5 per cent. Technical dificuities Exposure of the liver has always been found to be difficult. A correct incision gives a good view of the liver which is fixed to the posterior abdominal wall. The incision that we have employed is a right transrectus incision. On exploration if it is found that the right hepatic resection is necessary the upper end of the incision is extended to the right side of the chest, cutting through the costal cartilage without opening the pleura. However, there is no bar to opening the pleura if a better exposure is required. Smith (1968) preferred a right thoraco-abdominal incision as he considered it desirable to open the chest to minimize the likelihood of air being sucked into the hepatic vein during resection and believed that positive pressure could prevent this action. We have not encountered this problem of air embolism. Control of haernorrhage Lin (1966) believed that it was extremely difficult to control haemorrhage from the hepatic veins if they were divided first. We have not found any problem in dividing the hepatic veins. The left hepatic duct is found and ligated fairly easily. There are two veins
430
draining each segment of the liver; the right hepatic veins are much more difficult to expose. Bleeding also occurs from the collaterals between the surface of the liver and the diaphragm. As much as a litre of blood may be lost rapidly when the right coronary ligament is divided. This can first be controlled with packing and subsequently with a continuous running stitch of atraumatic catgut. Bleeding can also occur as a result of a coagulation defect. This should be prevented and adequate fibrinogen given if massive transfusion is needed. Fibrinolysis can take place during or after resection of the liver; hence epsilon aminocaproic acid should be available and used when the blood fails to clot. Bleeding from the intersegmental veins has led many surgeons to use hepatic clamps. We have not found this to be necessary.
References
c. (1958) Malignant tumours of the liver, extrahepatic ducts and gall bladder. In: RAVEN R. w. Cancer, Vol. 2. London, Butterworths, pp. 168-185. ISLAMI A. H., PACK G. T. and HUBBARD J. c. (1958) Regenerative hyperplasia of the cirrhotic liver following partial hepatectomy. Cancer 11, 663686. LIN T. Y. (1966) The results of hepatic lobectomy for primary carcinoma of the liver. Surg. Cynecol. Obstet. 123, 289-294. LIN T. Y. (1973) Results of 107 hepatic lobectomies with a preliminary report on the use of a clamp to reduce blood loss. Ann. Surg. 177, 413-421. MCFADZEAN A. J. S., TODD D. and TSANG K. C. (1958) Polycythemia in primary carcinoma of the liver. Blood 13,427-435. ONG G. B., CHU E. P. H., Y U F. Y. K. and LEE T. C. (1965) Spontaneous rupture of hepatocellular carcinoma. Br. J. Surg. 52, 123-129. ONG G. B. and TAW J. L. (1972) Spontaneous rupture of hepatocellular carcinoma. Br. Med. J. 4, 146-1 49. PACK G. T. and MOLANDER D. W. (1960) Metabolism before and after hepatic lobectomy for cancer; studies in 23 patients. Arch. Surg. 80, 685-692. SMITH R. (1968) Personal communication. STEWART M. .I. (1931) Precancerous lesions of the alimentary tract. Lancet 2, 617-622. TULL J. c. (1932) Primary carcinoma of the liver: a study of 134 cases. J. Pathol. Bact. 35, 557-562. WANG c. E. and LI K. T. (1963) Surgical treatment of primary carcinoma of liver. China Med. J. 82, 65-78. HOU P.
Hepatic resection* G. B . O N G A N D N . W. L E E t SUMMARY
One hundred and twenty-five hepatic resections were done in the University Surgical Unit at the Queen Mary Hospital, Hong Kong, from 1964 to I974 for conditions varying from primary hepatoma and recurrent pyogenic cholangitis to spontaneous rupture of the liver due to a bleeding haemangioma. The overall mortality was 17.6 per cent. A case was classed as an. operative death unless the patient was discharged from hospital. There has been long term survival after resection for primary carcinoma of the liver and no mortality when resection was carried out for benign conditions.
IN 1953 we performed a subtotal gastrectomy for a carcinoma of the stomach with resection of the lateral segment of the left lobe of the liver. The patient made an uneventful recovery but subsequently died of metastases 3 years after the initial operation. However, it was not until 1955 that we carried out hepatectomy for primary hepatoma with any frequency at the Kowloon Hospital, Hong Kong. All the records accumulated during the period from 1955 to 1963 were lost except for those of 1 patient who has been followed up since. Patients Over a period of 10 years, from 1964 to 1974, 125 resections of the liver were carried out; one of these, as Table I : CONDITIONS FOR WHICH LlVER RESECTION WAS CARRlED OUT, 1964-74 Sex Age (yr) Range M F Ratio Pathology Average 50 59 11 5 : 1 94 mth-85 yr Hepatocellular carcinoma 20-77 Recurrent pyogenic 15 23 1 : 2 49 cholangitis 3 : 1 17-52 35 3 1 Trauma 0 2 0 :2 63-76 70 cyst 3 1 3 :1 Liver abscess 45-59 5' 1 2 1 :2 58-75 Carcinoma of colon 47-58 Carcinoma of intra- 2 0 2 : 0 hepatic duct Leiomyosarcoma 0 1 0 : l 44 of jejunum 0 1 0 : l 43 Ruptured haemangioma
z;
31
mentioned, was done at the Kowloon Hospital, the remainder being performed at the Queen Mary Hospital, Hong Kong. There were 83 males and 42 females, giving a sex ratio of 2 : 1 . Lesions of the liver requiring resection Table I shows the conditions for which liver resection was carried out. Primary carcinoma of the liver There was a total of 70 cases of carcinoma of the liver where resection was possible; of these, 9 were cholangiohepatoma and 61 hepatocellular carcinoma. Of the 61 cases of hepatocellular carcinoma, cirrhosis was present in 35, while among the cases of cholangiohepatoma it was found in 3. The incidence of hepatocellular carcinoma with cirrhosis of the liver has been reported as 73.1 per cent (Tull, 1932) and 89 per cent (Stewart, 1931). Hou (1958) found that of the 66 per cent of his series with primary liver cancer associated with cirrhosis, 46.5 per cent also had clonorchiasis. Wang and Li (1963) studied 130 resected cases of primary carcinoma of the liver and reported an association of primary cancer with cirrhosis in all except 2 cases. This is of importance as the cirrhotic liver does not take kindly to resection, for even when the liver is mildly cirrhotic but the resection extensive the patient often succumbs to liver failure. Lin (1966) stated that when the liver is cirrhotic, right or left hepatectomy is contraindicated. While it is true that massive resection in a cirrhotic liver often ends in liver failure, at times the resected liver is found to have verv little functioning tissue. Hence., a heDatectomy in such cases is still compatible with survival. Eighteen out of the 70 cases were admitted because the hepatoma had ruptured. The mechanism of rupture has been previously biscussed (Ong et al., 1965; Ong and Taw. 1972). As a 'result of cirrhosis a number of patients developed portal hypertension, and the resulting bleeding could have been the cause of death in the postoperative period. I
* Based on a lecture delivered at the Repatriation Hospital, Concord, New South Wales, Australia. t Department of Surgery, University of Hong Kong, Hong Kong. 421
G. B. Ong and N. W. Lee Recurrent pyogenic cholangitis Some cases with recurrent pyogenic cholangitis reqi:ire resection of the liver. In the present series it was done for intrahepatic stones which most frequently formed in the lateral segment of the left lobe. The bile ducts were thickened, dilated and contained infected bile with stones (Fig. 1). The liver parenchyma showed degeneration and was often shrunken to such an extent that it was almost a fibrotic bag. There was usually a stricture at the junction between the medial and the lateral segments of the left lobe and this was possibly the cause of stone formation in the liver. As the bile was invariably infected, resection of the liver often resulted in subphrenic abscess or biliary fistula and occasionally septicaemia. Altogether 38 such cases were subjected to resection of the liver. Trauma to the liver Although the incidence of trauma to the liver is increasing owing to more road traffic accidents, the number of cases that require resection is relatively small. In the 10 years of this study there were only 4 cases in which it was necessary to remove a lobe of the liver. In 2 of them the right lobe of the liver had a stellate fracture which compromised the blood supply so that it was necessary to remove this lobe. In 1 patient the right lobe had a linear fracture which was repaired, while the lateral segment of the left lobe was removed. In the remaining patient the fracture was over the medial segment of the left lobe and it was necessary to perform a resection because of necrosis. These patients were relatively young when compared with the patients with other conditions necessitating hepatectomy . cysts There were 2 patients with a cyst in the left lobe of the liver; both patients were elderly females. The cysts were simple and did not contain any malignant tumour. Liz;er abscess During the last 5 years of the study 4 cases of liver abscess were seen. In 1 case an extended right hepatectomy was carried out because the abscess was mistaken for a carcinoma of the liver. On examination, the resected liver contained hardly any normal liver tissue (Fig. 2). In another case a right hemihepatectomy was carried out because of haemorrhage into the abscess. Both of these cases were subsequently proved to be amoebic liver abscesses. In addition to these cases there were 2 cases of liver abscess which had initially been drained and subsequently developed a discharging sinus. No amoebae were demonstrated either in the pus or in the wall of the abscess in these cases. Culture was originally sterile, but after drainage pyogenic bacteria were isolated. These were probably the cause of the discharging sinus (Fig. 3). Carcinoma of the colon with metastases to the liver There were 3 cases in this group; 2 females and 1 male. The male and 1 female patients had a carcinoma of the hepatic flexure which had invaded the right lobe of the 422
liver; t h e rest of the liver was normal (Fig. 4). The third patient had a carcinoma of the sigmoid colon with metastases to the medial segment of the left lobe. The liver was also cirrhotic. Carcinoma of the bile ducts There were 2 cases of carcinoma of the right hepatic duct. The patients were markedly jaundiced; the liver was not cirrhotic but was deeply stained. Both were males, one aged 47 and the other 58. Histologically, the tumours were shown to be adenocarcinoma arising from the right hepatic duct. Leiomyosarcoma of the jejunum In 1 case a leiomyosarcoma of the jejunum was found with secondaries in the right lobe of the liver. The rest of the liver was normal. Bleeding haemangioma A case of bleeding haemangioma was seen in this series. A huge cavernous haemangioma arising from the right lobe of the liver and extending to the medial segment of the left lobe occurred in a female patient. The rest of the liver was normal. The left lobe was rather hypertrophic and the cut section of the resected specimen showed there were some fibro-fatty tissues at the centre (Fig. 5).
Clinical features Abdominal mass This was by far the most common finding in the patients undergoing liver resection. It was present in all the patients with primary carcinoma of the liver, and in addition the 4 cases of liver abscess also had a mass palpable in the upper part of the abdomen. The patients with a cyst presented with a mass in the upper abdomen which moved with respiration and was nontender. In carcinoma of the bile duct the palpable mass in the upper quadrant could be identified as a uniformly enlarged liver. The patient with secondary leiomyosarcoma also had an enlarged liver with irregular masses studded over it. Abdominal pain Abdominal pain was a constant finding and was usually confined to the right upper quadrant, occasionally radiating to the back or referred to the shoulders. This was present in the majority of the patients with carcinoma of the liver and in the patient with a ruptured haemangioma. The pain was rather sudden and was described as ‘bursting’ in nature in all cases of ruptured hepatic tumour. Sometimes it was associated with the rapid onset of shock. Intraperitoneal haemorrhage This occurred in 18 cases of ruptured carcinoma of the liver. Traumatic rupture of the liver produced intraperitoneal haemorrhage with very severe pain and the patient rapidly went into shock. The amount of fluid varied. In primary hepatoma ascites might be present, and any bleeding, even if severe, would yield only heavily bloodstained fluid on paracentesis.
Hepatic resection
Fig. 3. Persistent sinus after drainage of a liver abscess which was treated and cured by resection.
Fig. 1. Resected specimen of the lateral segment of the left lobe of a liver. The ducts are dilated, fibrotic and contain stones.
Fig. 2. Specimen of destroyed liver due to amoebiasis. There is hardly any normal liver tissue.
Fig. 4. Carcinoma of the hepatic flexure invading the right lobe of a liver. This was treated by right hepatectomy and right hemicolectomy.
423
G. B. Ong and N. W. Lee
occasionally demonstrated displacement stomach, indicating a hepatic mass.
of
the
Splenovenography The usefulness of this investigation lies in the fact that the portal vein may be obliterated as a result of tumour invasion. Should the obstruction extend beyond the bifurcation of the portal vein, then surgical treatment is contraindicated. Portal hypertension is also demonstrated by this procedure. Hepatic arteriography Hepatic arteriography is useful in differentiating a malignant lesion with new vessels from a benign one, when the vessels are only displaced. Fig. 5. Bleeding haernangioma of the liver.
Weight loss Weight loss was found in 37 of the 70 cases of primary hepatoma. It was not found in recurrent pyogenic cholangitis, traumatic rupture, cysts or in the case of a ruptured haemangioma. A variable degree of weight loss was noticed in carcinoma of the colon with liver secondaries, while the patient with carcinoma of the bile duct had marked loss of weight. The patient with leiomyosarcoma of the jejunum had also lost weight. Anorexia Approximately half the patients with primary hepatoma complained of anorexia. It was also present in the patients with recurrent pyogenic cholangitis, liver abscess and other malignancy, but was absent in these with traumatic rupture of the liver, cyst and ruptured haemangioma.
Preoperative investigations Except for emergency operations for bleeding, all the cases were subjected to laboratory investigations. Laboratory findings Anaemia was present, although of a mild degree, in all the cases of primary hepatoma. Polycythaemia in primary hepatoma, as reported by McFadzean et al. (1958), was not present in any of these patients. Leucocytosis was also an occasional finding in primary hepatoma and was noticeably absent in the 4 cases of liver abscess, while the white cell count was moderately raised in all the cases of recurrent pyogenic cholangitis. a-Fetal protein gave positive results in 70 per cent of the cases of hepatocellular carcinoma. This test was invariably negative in the patients with cholangiohepatoma. The liver function tests were of little value except in a case of carcinoma of an intrahepatic duct when the bilirubin was markedly raised. The alkaline phosphatase was not helpful except in the case with obstructive jaundice. X-ray examinafion When X-ray examination showed a soft tissue shadow at the upper abdomen a barium meal study 424
Scanning of the liver Scanning with 99Tcdoes not differentiate a malignant tumour from a benign one. When the lesion is small, scanning usually does not demonstrate any filling defect, and then it is necessary to depend on other investigations for diagnosis as a therapeutic guide. Peritoneoscopy Peritoneoscopy is a useful means of diagnosing a liver condition requiring a resection. A primary hepatoma as well as secondary tumour can be seen on the surface. Biopsy under direct vision can then be done and a histological diagnosis made of the lesion. In addition, it is useful in demonstrating the cirrhotic state of the liver. However, peritoneoscopy has many blind spots. The posterior surface of the liver is obscured by adhesions. Any centrally situated lesion will be out of the field of vision. Inferior vena cavogvam An inferior vena cavogram may occasionally be useful, especially in carcinoma when the tumour has invaded the inferior vena cava, in which case resection is contraindicated.
Preoperative preparations In most of the cases undergoing elective operation the nutrition should be maintained, and intravenous hyperalimentation will help in getting the patient fit for a major operation. A diet rich in vitamins should be given. Supplementary vitamin A in liquid solution with 10 000 units of vitamin B should be given daily, to which 500 mg of vitamin C may be added. When the prothrombin time is prolonged vitamin K SO/lOO mg may be given by intramuscular injection. A diet rich in protein with a high carbohydrate and moderate fat content should be given. Anaemia should be corrected by blood transfusion. Contraindications to operation Operative treatment is contraindicated under the following circumstances: 1. Metastatic spread: When metastases are demonstrated in the lungs or the bones, surgical exploration should not be carried out. When there are secondaries in the supraclavicular lymph nodes, particularly in
Hepatic resection cholangiohepatoma or carcinoma of the colon, operative treatment is out of the question. 2. Jaundice: The presence of jaundice is not a contraindication to operation, but may be a contraindication to resection of the liver. Occasionally an hepatocellular carcinoma will spread into the common hepatic duct and produce obstructive jaundice. In such cases resection is not compatible with a cure. S. A. T., a male patient aged 53 years, was admitted in 1969 because of obstructive jaundice. An operation was performed on 14 July 1969 when aright extended hepatectomy was carried out. He survived 5 months before dying of multiple secondaries in the remnant of the liver (Fig. 6 ) .
3 . Ascites: The presence of ascites is a contraindication to operation, as it indicates that the liver is failing and will not tolerate any operative procedure. 4. Biochemical changes : Biochemical changes showing poor liver function indicate that the patients, particularly those with primary hepatoma, with cephalin flocculation of over 3 units, bromsulphthalein retention of over 35 per cent and serum albumin below 2-5 g per cent or prothrombin time below 60 per cent, are unlikely to survive an operation and hence surgery should not be done.
Operations currently practised Lefr medial segmental resection This is an operation that is seldom carried out. It was done only twice in this series; once for trauma to the liver in which the medial segment was completely necrotic and bleeding. It was also done for a ruptured carcinomatous nodule situated in the medial segment of the left lobe. This man subsequently died of bleeding varices. The artery, portal veins and segmental duct were dissected out; these were found half an inch deep to the insertion of the ligamentum teres. The segment was then resected from in front backwards until the medial segmental hepatic vein was exposed and ligated. The segment was removed and the edges of the liver remnant were brought together. Left lateral segmental resection In performing left lateral segmental resection the left coronary ligament*was freed from the undersurface of the diaphragm. The free end of the coronary ligament contained a few small vessels and in a cirrhotic liver bled profusely. The raw area left on the diaphragm had to be sutured with atraumatic catgut. After the left lateral segment had been freed, the forceps holding its tip were depressed to expose the lateral segmental hepatic vein. A little dissection freed it from the inferior vena cava. Often the medial segmental vein joined it before they became a single vein draining into the inferior vena cava. In order to ligate the lateral segmental vein it was occasionally necessary to dissect into the substance of the liver. After its ligature and division, the liver containing the tumour or stone was rotated forwards so that the lateral segment of the left lobe was brought out of the abdomen. The segmental hepatic artery, the segmental duct and the segmental branch of the portal vein were ligated as they ran near the posterior border
Fig. 6. Secondaries which appeared in the remnant of a hypertrophic liver. Arrow points at the hepaticojejunostomy.
of the left lobe of the liver. After ligating the artery, vein and the duct, the lateral segment of the liver was ready for division. Further haemostasis of the transhepatic segmental hepatic veins could be attained by suture ligatures. Lefi hemihepatectomy In this operation the liver was divided along the principal plane dividing the right and left lobes of the liver. A Mayo-Robson incision was made and the left coronary ligament was divided and detached. The left hepatic vein was dissected out, divided between clamps and stitched as for lateral segmental resection. After division of the left branch of the portal vein, hepatic artery and hepatic duct, the left lobe of the liver became a dusky colour or sometimes even black. The division of this lobe of the liver was now made by cutting through the capsule of the liver and, with the handle of the scalpel, the intersegmental veins were teased out and ligated or stitched. The cut edge of the liver was either sutured with a series of interrupted or continuous catgut sutures, or, in most cases, after controlling the bleeding from the raw surface a piece of Surgicel was placed over it and then pieces of Gelfoam to cover the whole raw area. The Gelfoam was stitched to the capsule of the liver. This method resulted in good healing. Right hemihepatectomy Exploration of the back of the liver was first carried out. This avoids division of the structures at the porta hepatis which makes it necessary to resect the devascularized liver. If the tumour has infiltrated the inferior vena cava, resection will result in either part of the tumour being left behind or the inferior vena cava being torn beyond repair. After exploration, attention was focused on the structures at the porta hepatis. Division and ligation of these structures were performed. Next, the hepatic vein was dealt with. If the coronary ligament had been freed when the hepatic veins were explored, the liver could be 425
G. B. Ong and N. W. Lee TABLE 11: COMPLICATIONS IN RESECTIONS Complication No. Haemorrhage Biliary fistula Infection Septicaemia Subphrenic abscess Liver abscess Pleural effusion
125 LIVER
of cases
0,
/o
4
3
11
9
6 13 1
10.4
4
3
5
0.8
delivered out into the wound. In so doing, there would be a kink of the inferior vena cava. Lin (1966) believed that the kinking of the inferior vena cava would impede the venous return and could cause cardiac arrest. Hence he devised his finger-fracture technique so that the hepatic veins could be divided within the liver substance. Division and removal of the liver were then carried out in the same manner as for left hemihepatectomy. However, kinking of the inferior vena cava can be lessened if the lower hepatic veins are dissected out first and ligatured. This can be done with the liver in the abdomen, and leaves the uppermost hepatic vein which is short and can be found at the bare area of the liver. In dividing the uppermost hepatic vein over the kink of the inferior vena cava a piece of the inferior vena caval wall might inadvertently be included. If this occurred a transfixion of the vein would inevitably cause the suture ligature to slip and severe bleeding might take place. It is therefore wise, at this stage, to have ready a vascular clamp of the Satinsky type. Should such an accident happen the inferior vena cava could be clamped and sutured. Extended right hepatectomy Occasionally, a tumour is large enough to require removal of the liver to the right of the falciform ligament. The exploration and method of dealing with the hepatic veins were similar to those for right hemihepatectomy. The ligature of structures at the porta hepatis was similarly carried out. However, the left medial segmental artery and the right segmental portal vein with the segmental duct have to be dealt with in this procedure. The lateral segmental duct, artery and portal vein were preserved and found to be half an inch deep to the ligamentum teres. At this stage of the division of the medial segmental duct it would be prudent to place a T-tube into the left hepatic duct, for it would prevent damage to the lateral segmental duct. The raw surface of the liver was again dealt with either by suturing the capsule together or by placing some haemostatic agents and stitching them to the capsule of the liver. If the falciform ligament is not involved it provides a convenient piece of material to stitch over the raw surface. Extended right hepatectomy represented a removal of between 75 and 80 per cent of the liver tissue, while a right hemihepatectomy removed between 55 and 60 per cent, and removing the left half of the liver represented 45-50 per cent of liver tissue by weight. 426
Postoperative care Patients undergoing liver resection required intensive supportive treatment until the remaining liver had regenerated sufficiently to take care of the metabolic needs of the body. Broad spectrum antibiotics were given to prevent chest infection.
Care of the drain Whenever the chest was opened an underwater seal drain was inserted and removed on the third or fourth postoperative day. An X-ray of the chest was taken on the day after the operation and repeated after the drain had been removed. Subsequent pleural effusion would require thoracocentesis. A subdiaphragmatic drain was usually placed in the space formerly occupied by the resected liver. A small amount of serosanguineous fluid was always present, but occasionally there was an excessive amount of ascitic fluid in which case the drain was removed. This would prevent excessive loss of ascitic fluid. The drain occasionally might be blocked by a blood clot and therefore too much reliance must not be placed on its efficiency to demonstrate the presence of bleeding. A large distended abdomen with the patient going into shock would indicate postoperative bleeding and steps should be taken to control it. Administration of fluids After blood replacement and administration of fluid, 25 per cent glucose should be given through the inferior vena cava via a cut-down; 200 g of glucose were given daily and adequate vitamins were also administered. Oral feeding can usually be restarted on the second or third postoperative day. A high protein diet should be avoided as it has been shown by Pack and Molander (1960) that too high a protein intake might cause intoxication in a patient with massive resection of the liver. Complications These are detailed in Table If.
Postoperative haemorrhage Haemorrhage occurred postoperatively in 4 patients undergoing hepatic resection, all for carcinoma of the liver, and in 1 instance the bleeding was into the pericardium from the upper part of the inferior vena cava. The patient was explored again and subsequently made an uneventful recovery. The other 3 cases had bleeding from the collaterals resulting from portal hypertension in a cirrhotic liver. At the conclusion of the first operation there was no bleeding as every part of the raw surface had been run over with atraumatic catgut. Subsequently, further collaterals which had been missed started bleeding and they were controlled by suturing. Biliary fistula Eleven cases (9 per cent) had a biliary fistula. Four patients had undergone resection for carcinoma of the liver and in 1 instance it had been a left hepatectomy in which the duct had been closed with interrupted silk in
Hepatic resection
good approximation. However, a fistula developed. A biopsy taken at the margin showed that carcinomatous cells were still present. In one of these cases after an extended right hepatectomy a T-tube was inserted and the medial segmental duct was carefully closed with interrupted fine silk. Nevertheless, leakage occurred but the fistula healed spontaneously. Six cases had had resection for recurrent pyogenic cholangitis. In each instance the closure had been performed with interrupted silk. Subsequently, the incidence of biliary fistula was lowered by reverting back to closure with atraumatic catgut and then suturing the liver capsule over it. In 1 case the biliary fistula developed after a right hepatectomy for traumatic rupture of the liver. The fistula healed spontaneously without any further operation. Infection
Infection accounted for the greatest number of complications in the patients undergoing hepatic resections. There were 6 patients who developed septicaemia, and Gram-negative enteric organisms were cultured from the blood. In 3 of them the hepatectomy was for hepatocellular carcinoma while in the other cases for recurrent pyogenic cholangitis. Subphrenic abscess occurred in 13 patients (10.4 per cent). The abscesses usually developed following incomplete or inefficient drainage of the space left after resection of the liver. Suction drains were used but even this could not completely prevent the development of subphrenic abscess.
Y . S. K., a female patient, was admitted in 1972 because of an enlarging mass which was found to be a hepatoma involving the right lobe of the liver. An hepatic arteriogram showed that the tumour arose from the upper division of the right lobe (Fig. 7). This was confirmed by a splenovenogram (Fig. 8). Peritoneoscopy not only revealed the presence of the tumour but also cirrhosis of the liver. A needle biopsy confirmed the diagnosis of hepatocellular carcinoma. At operation it was decided that the tumour should be removed, sparing the inferior division of the right lobe. Accordingly, the segmental duct, the branch of the hepatic artery and the branch of the portal vein to this division were preserved. The rest of the right lobe was then removed. Examination of the operated specimen showed that the tumour had a narrow rim of normal tissue (Fig. 9). The patient had a postoperative haemorrhage at the site where the superior branch of the hepatic vein drained into the inferior vena cava. This had previously been stitched, but a new tear in the upper part of the inferior vena cava extending into the atrium was found at the second operation. This was sutured and the patient made an uneventful recovery. Subsequently, a hepatic arteriogram showed that this segment was functioning and scanning showed a good-sized segment. This patient has been followed up for the past 2 years and she is quite well without any evidence of recurrence of her disease or metastases (Fig. 10).
It is possible that this patient would have died had the whole of her right lobe had been removed. The amount of liver tissue that was functioning and removed at operation was minimal. Among the 70 resections for primary hepatoma 34 patients had cirrhosis of liver and there were 9 deaths, giving a mortality rate of 26 per cent. The causes of death were liver failure in 5 cases, septicaemia in 2 and hypovolaemic shock following uncontrolled haemorrhage in 2. The remaining portion of a very cirrhotic liver did not appear to be able to regenerate sufficiently to take over the function of the removed Pleural effusion Pleural effusion occurred in 4 cases and was confined segment or lobe. Furthermore, bleeding in cirrhotics, to cases of right hepatectomy in which the chest had especially from collaterals, was always profuse. Even been opened. In 2 of them the effusion kept recurring at the very early stage of resection when the liver was and malignant cells were found in the pleural fluid. In being mobilized, much blood could be lost from these 1 case a combination of right hepatectomy and collaterals. The haemorrhage could be controlled by pulmonary lobectomy caused pleural effusion of the packing and subsequently with running stitches. In an left pleural cavity. Rupture of the spleen occurred attempt to replace blood loss with massive transfusion, a coagulation defect could develop and this was often during thoracocentesis. the cause of death. Septicaemia was also much more likely to occur in Operative mortality After undergoing hepatectomy every patient who did these patients, for they tolerated infection poorly. Two not leave the hospital was considered an operative of the cases dying of septicaemia belonged to the group mortality. Thus, a case might have undergone an of patients with recurrent pyogenic cholangitis that operation and then died of liver failure 45 or 60 days required liver resection. Traumatic rupture of the liver occurred in 2 patients after operation. This would still be considered as an with multiple injuries; both patients died of cardiac operative mortality. There were 22 deaths out of 125 resections, giving arrest following irreversible shock shortly after an overall mortality of 17.6 per cent. Of these, 15 had operation. Although the resections were extensive, the had resection for primary hepatoma; 7 of these 15 died other benign conditions in this series did not give rise in the first 5 years of the series, that is, from 1964 to to any mortality. None of the patients operated on for 1969, when 22 resections were performed, giving a carcinoma of the colon with liver metastases died mortality of 32 per cent. In the succeeding 5 years, within the postoperative period. The patient with leiomyosarcoma who died of from 1969 to 1974, there were 48 resections with 8 deaths, giving a mortality rate of 17 per cent. There is cardiac failure was known to have cardiac ischaemia. Two cases of carcinoma of the bile ducts were therefore a definite drop in operative mortality. This results not only from improved technique but also from operated on; one was an extended right hepatectomy better selection of the best operation for a particular and the other a right hepatectomy. Reconstruction of case. The following case report is an example of such the biliary tract was in each instance by hepaticojejunostomy. One patient developed a subphrenic selection. 427
G. B. Ong and N. W. Lee
Fig. 9. Resected specimen of a liver showing a large carcinoma.
Fig. 7.Hepatic arteriograrn in a primary carcinoma of the liver. Note the new vessels entering the turnour. The right inferior division is normal.
Fig. 10. Patient who had had a primary hepatoma resected; ( A ) during convalescence, and ( B ) 2 years afterwards.
Fig. 8. Splenovenogram showing infiltration of cancer in the segmental vein.
abscess but both died of liver failure. Their jaundice never subsided and their condition deteriorated until they went into coma and died 40 and 48 days after operation respectively. The survivors Of the 103 patients who survived hepatic resection, 39 subsequently died from 5 to 41 months after 428
operation, the average being 10 months. All died of their original disease. One patient with recurrent pyogenic cholangitis died 18 months after hepatectomy. She developed leakage of bile through the old drainage wound which was persistent and it was necessary to explore the bile ducts to close this biliary fistula. She died of uncontrolled haemorrhage due to a coagulation defect. Carcinoma of the colon with metastases to the liver accounted for 2 deaths. One was a female patient who survived a right hepatectomy with the right hemicolectomy carried out in continuity. This patient was operated on in 1968. She survived for 18 months but eventually died of her disease. Up to the present time 64 cases are still alive out of the original 125. Table Iff shows that 19 of the patients with carcinoma of the liver are alive and the longest survival is now 13 years. This is a patient who had a left hemihepatectomy done in 1962 for a ruptured hepatoma and who emigrated in 1971. The second longest survivor is a man with hepatoma which
Hepatic resection ruptured while being investigated. An emergency extended right hepatectomy together with partial excision of the diaphragm was carried out. This patient is still alive and well. A female who was operated on for a hepatoma of the left lobe with two secondary nodules on the medial segment is alive and well today, 5 years after the operation. Of the remaining surviving patients, 1 was operated on in 1971,3 in 1972, 4 in 1973 and 8 in 1974. Of the patients with other conditions who are still alive after hepatic resection (Table I V ) , one had a carcinoma of the sigmoid colon with metastases to the liver for which a total colectomy and left medial segmental resection was carried out I5 months ago. Thirty-five of the cases with recurrent pyogenic cholangitis are still alive 6 months to 10 years after operation. Of the patients with traumatic rupture, one who had a right hemihepatectomy done 7 years ago and another who had a left medial segmental resection performed 3 years ago are alive at the present time. The 2 patients with a cyst which was treated by left hemihepatectomy have survived without problems for 2 years and 5 years respectively. Of the patients with liver abscess who were operated on, one had an extended right hepatectomy which was carried out 4 years ago. This was a patient who was operated on because of a mistaken diagnosis of hepatoma arising from the right lobe of the liver. As the lesion was soft it was thought to be a necrotic tumour. No aspiration of the abscess was carried out. He made an uneventful recovery and was discharged from hospital after 2 weeks. He has been followed up since and the liver has regenerated to its original size and he is at the present moment quite well (Fig. 11).
Fig. 11. Patient who had undergone resection of a liver abscess; ( A ) 6 months, and (B) 4 years following operation.
The ruptured haemangioma was operated upon on 6 July 1974; the patient was discharged 10 days after the operation. Discussion Certain conclusions can be drawn from the present series. Operative mortality Primary hepatoma carried the highest operative mortality, which is understandable because hepatoma is a complication of a cirrhotic liver. Islami et al. (1958) have shown that in rats with carbon-tetrachlorideinduced cirrhosis the liver remnant after resection could regenerate and function normally. However, in humans when a cirrhotic liver is resected it does not
Table 111: DETAILS OF 19 SURVIVING PATIENTS WHO UNDERWENT RESECTION FOR PRIMARY HEPATOMA Year of operation
Type of resection
Lesion
1962 1966 1969 1971 1972 I973
Left hemihepatectomy Extended right hepatectomy Left hemihepatectomy Left hemihepatectomy Right or left hemihepatectomy Right or left hemihepatectomy or extended right hepatectomy Right or left hemipatectomy or extended right hepatectomy
Ruptured hepatoma Ruptured hepatoma Hepatoma Hepatoma with cirrhosis Hepatoma with mild cirrhosis Hepatoma, 2 with and 2 without cirrhosis
1974
No. of cases
Hepatoma with or without cirrhosis
Table IV: DETAILS OF SURVIVING PATIENTS WHO UNDERWENT RESECTION FOR CONDITIONS OTHER Length of THAN PRIMARY HEPATOMA No. of survival to Lesion
Type of resection
cases
Carcinoma of sigrnoid colon with metastasis to liver Recurrent pyogenic cholangitis Traumatic rupture Liver cyst Liver abscess
Total colectomy with left medial segmental resect ion Left lateral segmental resection Right hemihepatectomy, left medial resection Left hemihepatectomy Extended right hepatectomy Left hemihepatectomy Right hemihepatectomy Right hemihepatectomy
1
Ruptured haemangioma
35 2 2 1
date 15 mth 6 mth-10 yr 7 and 3 yr 2 and 5 yr 4-9 yr
2
1 1
10 d
429
G . B. Ong and N. W. Lee
regenerate into a normal functional unit. There may be islands of regeneration. In fact, the hepatoma most probably arises from one of these regenerated nodules. As hepatocellular carcinomas are always at an advanced stage when first seen, massive resection is often required. If cirrhosis of the liver is severe, massive resection will always end in death from liver failure. However, with proper selection of cases and correct application of operative treatment the mortality rate should be reduced to an acceptable level. From 1964 to 1969 the operative mortality from hepatic resection for primary hepatoma was 32 per cent. In 1974 there were 9 resections for primary carcinoma of the liver with only 1 death, a mortality of 11 per cent. Lin (1973) reported a mortality rate of 11.9 per cent in a series of resections for primary hepatoma of the liver. Further, he gave a figure of 19.1 per cent for 5-year survival. Hepatic resection for secondary carcinoma should carry a very low mortality. In 3 resections for metastasis from carcinoma of the colon there was not a single death. When resection is carried out for a benign non-infective condition there should be no mortality, as shown by results for the cysts and the bleeding haemangioma in the present series. However, when the operation is performed for infected bile ducts with intrahepatic stones, then the mortality is 5 per cent. Technical dificuities Exposure of the liver has always been found to be difficult. A correct incision gives a good view of the liver which is fixed to the posterior abdominal wall. The incision that we have employed is a right transrectus incision. On exploration if it is found that the right hepatic resection is necessary the upper end of the incision is extended to the right side of the chest, cutting through the costal cartilage without opening the pleura. However, there is no bar to opening the pleura if a better exposure is required. Smith (1968) preferred a right thoraco-abdominal incision as he considered it desirable to open the chest to minimize the likelihood of air being sucked into the hepatic vein during resection and believed that positive pressure could prevent this action. We have not encountered this problem of air embolism. Control of haernorrhage Lin (1966) believed that it was extremely difficult to control haemorrhage from the hepatic veins if they were divided first. We have not found any problem in dividing the hepatic veins. The left hepatic duct is found and ligated fairly easily. There are two veins
430
draining each segment of the liver; the right hepatic veins are much more difficult to expose. Bleeding also occurs from the collaterals between the surface of the liver and the diaphragm. As much as a litre of blood may be lost rapidly when the right coronary ligament is divided. This can first be controlled with packing and subsequently with a continuous running stitch of atraumatic catgut. Bleeding can also occur as a result of a coagulation defect. This should be prevented and adequate fibrinogen given if massive transfusion is needed. Fibrinolysis can take place during or after resection of the liver; hence epsilon aminocaproic acid should be available and used when the blood fails to clot. Bleeding from the intersegmental veins has led many surgeons to use hepatic clamps. We have not found this to be necessary.
References
c. (1958) Malignant tumours of the liver, extrahepatic ducts and gall bladder. In: RAVEN R. w. Cancer, Vol. 2. London, Butterworths, pp. 168-185. ISLAMI A. H., PACK G. T. and HUBBARD J. c. (1958) Regenerative hyperplasia of the cirrhotic liver following partial hepatectomy. Cancer 11, 663686. LIN T. Y. (1966) The results of hepatic lobectomy for primary carcinoma of the liver. Surg. Cynecol. Obstet. 123, 289-294. LIN T. Y. (1973) Results of 107 hepatic lobectomies with a preliminary report on the use of a clamp to reduce blood loss. Ann. Surg. 177, 413-421. MCFADZEAN A. J. S., TODD D. and TSANG K. C. (1958) Polycythemia in primary carcinoma of the liver. Blood 13,427-435. ONG G. B., CHU E. P. H., Y U F. Y. K. and LEE T. C. (1965) Spontaneous rupture of hepatocellular carcinoma. Br. J. Surg. 52, 123-129. ONG G. B. and TAW J. L. (1972) Spontaneous rupture of hepatocellular carcinoma. Br. Med. J. 4, 146-1 49. PACK G. T. and MOLANDER D. W. (1960) Metabolism before and after hepatic lobectomy for cancer; studies in 23 patients. Arch. Surg. 80, 685-692. SMITH R. (1968) Personal communication. STEWART M. .I. (1931) Precancerous lesions of the alimentary tract. Lancet 2, 617-622. TULL J. c. (1932) Primary carcinoma of the liver: a study of 134 cases. J. Pathol. Bact. 35, 557-562. WANG c. E. and LI K. T. (1963) Surgical treatment of primary carcinoma of liver. China Med. J. 82, 65-78. HOU P.
