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Hepatic lobectomy
Hepatic Lobectomy JOHN
Major hepatic resections have been performed for more than a century, yet the risk of such resections was almost prohibitive until recently. Progress in hepatic surgery has been slow, but this is understandable considering the technical difficulties encountered in massive liver resection in addition to disturbances occurring after removal of a viscus which performs so many indispensable physiologic functions. It was not until 1954 that anatomic dissections demonstrated the true lobar and segmental pattern of the liver [1,2], and subsequent physiologic experiments have demonstrated its tremendous regenerative capacity [3-51. These two advancements enable the surgeon to perform major hepatic resections safely and with confidence. Indications for and the results of hepatic lobectomy have shown such differences that enthusiasm for the operation has varied from omission to panacea. In general, the operation is rarely indicated or performed. Consequently, an individual surgeon has little opportunity for a large personal experience. It seems desirable, therefore, to analyze the experience at the Ochsner Clinic over a twenty-two year period. Clinical Material
During a twenty-two year period ending in 1968, twenty patients underwent hepatic lobectomy at the Ochsner Clinic. In this paper the term “lobectomy” conforms to both the topographic anatomy and the lobar pattern as defined by the distribution of the Glissonian structures, that is, the hepatic artery, portal vein, and bile ducts. The anatomic boundaries of the latter were not delineated until fairly recently and most authors today refer to this anatomic division, although some still prefer the topographic anatomy. In regard to the topographic anatomy, there were twelve right lobectomies and eight left lobectomies. In regard to the distribution of the Glissonian structures there were ten right lobectomies, two extended right lobectomies (right From the Department dation Hospital, New Reprint requests Clinic, 1514 Jefferson * Present address:
of Surgery, Ochsner Clinic and Ochsner FounOrleans, Louisiana. may be addressed to John Ochsner. Ochsner Highway, New Orleans, Louisiana 70121. 320 Tuttle Road, San Antonio, Texas 78209.
Volume 121,
1971
March
L. OCHSNER,
BARRY
E. MEYERS,
ALTON
OCHSNER,
MD,
New
MD,* MD,
New
Orleans, Louisiana Orleans,
New Orleans,
Louisiana
Louisiana
lobe and medial segment of left lobe), four left lobectomies, and four left lateral segmentectomies. (Table I.) The ages of the patients ranged from five months to eighty-eight years. Of the patients, all Caucasians, nine were male ; and eleven, female. All patients have been followed. Historical Background
Berta [6] is credited with performing the first hepatic resection in 1760 when he amputated an exteriorized portion of the right lobe of the liver. The first planned right hepatic lobectomy was performed by Wendel [7] in 1911, when he individually ligated the right hepatic artery and the right bile duct. He did not ligate the right portal vein for fear of a thrombus propagating from the stump into the contralateral portal system. The first anatomic total hepatic lobectomy (left hepatic lobectomy) performed according to the units of vascular and ductal distribution preceded by hilar ligation was carried out by Pettinari [8] in 1940. In 1952 Lortat-Jacob and Robert [9] demonstrated that bleeding could be controlled during hepatic lobectomy by preliminary isolation and ligation of the vascular structures in the porta hepatis and careful parenchymal dissection based on knowledge of the anatomic segments of the liver. Extensive experience in hepatic lobectomy, using various technical maneuvers, has been described by Balasegaram [ IO], Brunschwig [ .ZI], Lawrence et al [12], Longmire et al [13], Lin [IS], Pack [15], Pettinari and Dagradi [16], Quattlebaum [ 171, and Smith et al [18]. The operative mortality has progressively declined, and although early reports gave a pessimistic outlook toward long-term results, recent reports have been encouraging. Surgical Indications Liver Cell Carcinoma.
Until relatively recently malignant disease was the most common indication for hepatic lobectomy. As in other areas of the body, wide excision along anatomically defined boundaries offers the best chance of cure. Threefourths of all primary malignant tumors of the liv273
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Meyers,
I
TABLE
and
Ochsner
Hepatic Lobectomy at Ochsner Clinic (1946-1968) Type of Operation
Number
Right lobectomy Extended right lobectomy Left lobectomy Left lateral segmentectomy Total
10 2 4 4 20
-
er arise from the liver cell. Primary liver cell carcinoma appears with greater frequency in certain geographic areas and seems to be produced by various environmental factors [ 19,20]. This neoplasm occurs relatively frequently in Southeast Asia and in Southern Africa, but it is uncommon in the United States and Europe. The majority of patients with primary liver cell carcinoma have extrahepatic metastasis at the time of diagnosis. Intrahepatic metastases often lie within the same portal tract as the initial lesion, since metastases result from invasion of portal vein trunks, which makes the lesion resectable. Six patients. in this series had hepatic lobectomy for primary liver cell carcinoma, which was the most common indication for hepatic lobectomy. (Table II.) The operations employed were a left lateral segmentectomy in one, left lobectomy in two, right lobectomy in two, and extended right lobectomy in one. Bile Duct Carcinoma. Bile duct carcinoma is the second most common primary malignant tumor of the liver. These tumors are invariably multicentric, widespread, and rarely are amenable to curative resections. Only one patient in our group had a bile duct carcinoma for which right lobectomy was performed. Embryonal Carcinoma. Carcinomas of the liver in infants and children differ greatly, both clinically and histologically, from those seen in adults and show evidence of congenital origin [21]. Therefore, the term “embryonal carcinoma” apTABLE
II
Indications
for Hepatic
Indications Neoplasm Malignant Primary Liver cell carcinoma Bile duct carcinoma Embryonal carcinoma Metastatic Colon carcinoma Leiomyosarcoma Stomach carcinoma Benign Hemangioma Trauma Inflammatory Bile duct stricture Total
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Lobectomy Number
6 1 3 2 1 1 1 4 1 20
pears appropriate. These interesting neoplasms are among the most common malignant tumors seen in infants. They are generally solitary, confined to the liver, and are therefore resectable, but the prognosis is poor. There are reports of successful single short and long-term survivals after hepatic lobectomy [22-271. Three children with this tumor had either a right or extended right hepatic lobectomy in our series. Two had elective resections, whereas in one an emergency lobectomy was performed because of rupture of the neoplasm after minor trauma. Other Primary Malignant Tumors. Hepatic lobectomy has been used successfully f’or other solitary primary malignant tumors, such as angiosarcoma [I I I and malignant mesenchymoma [ 281. Metastatic Lesions. Subtotal hepatic resection, including lobectomy, under favorable circumstances has been advocated for metastatic lesions of the liver, whether these are direct extensions from a contiguous structure or embolic from a distant primary tumor. Adenocarcinoma of the gallbladder has a uniformly poor prognosis, largely because of the late diagnosis and proximity to the liver with the possibility of direct spread. The infrequent cure depends primarily on the fortuitous excision of small lesions at the time of cholecystectomy for cholelithiasis. Prophylactic wedge resection of the hepatic bed is considered the least measure which offers a chance of cure [29]. Pack et al [30], however, had little success with wedge resection and advocate right hepatic lobectomy when liver extension from gallbladder carcinoma is discovered. Direct extension to the liver from carcinoma of the stomach and colon has also been treated by excision of the primary lesion with en bloc concomitant hepatic lobectomy, usually left lobectomy. Results have generally been disappointing, but involvement by direct spread offers a more favorable outlook than involvement by hematogenous route. Four patients underwent hepatic lobectomy for metastatic disease. In each instance the metastasis was of such size or so positioned as to require lobectomy for removal of the lesion. Blood-borne metastasis from carcinoma of the colon, previously resected, was the indication for Iobectomy in two patients. In the oldest patient in this series, an eighty-eight year old woman, right hepatic lobectomy was performed to control bleeding from rupture of a metastatic leiomyosarcoma. A left hepatic lobectomy was combined with total gastrectomy in excision of a carcinoma of the stomach with direct extension into the liver. Benign Lesions. Results of resection of benign hepatic lesions have been excellent. Peripheral The American
Journal
of Surgery
Hepatic Lobectomy
lesions can be excised with minimal risk and afford an accurate diagnosis of questionable lesions. Hepatic lobectomy for benign lesions should be reserved for those which cause disabling symptoms. Hepatic and bile duct adenomas are rare. Although usually exceedingly small, they may become large and produce pressure symptoms, such as fullness and nausea, and can cause biliary obstruction. Because of the difficulty in differentiating them from primary malignant neoplasms, and because of the possibility of malignant transformation, these lesions should be widely resected. Patients with such lesions have been followed up for as long as seventeen years after resection with no apparent recurrence [31]. Hemangiomas are the most commonly resectable hepatic tumors and, although generally small, may attain massive size, necessitating lobectomy for extirpation. Large hemangiomas may produce symptoms as the result of pressure and are SWceptible ,to traumatic or spontaneous rupture. Of the fourteen cases of ruptured hemangiomas reviewed by Longmire and Marable [32], twelve were fatal. Large arteriovenous communications within the hemangioma can cause congestive heart failure. Vascular lesions must be resected through a rim of normal tissue to prevent uncontrollable hemorrhage. Irradiation may be advisable preoperatively to reduce the size of the tumor and has even been used as the sole method of therapy. Although irradiation may reduce the size of hemangiomas of the liver, it probably should never be used in young patients because of the carcinogenic effect of radiation. The most common vascular malformation, cavernous hemangiomas of the liver, may in reality be vascular hamartomas [33]. They appear to have no growth potential, but grossly may be indistinguishable from true neoplasms. Areas of focal nodular hyperplasia of the liver have been considered tumor-like lesions. Opinions differ as to whether these lesions are the result of regenerative phenomena, hamartoma, or neoplasm. Edmondson [21] believes that some type of local injury to the liver and interference or diminution of blood supply are causative factors. These areas may become quite large and require resection if symptomatic [31]. Compensatory hypertrophy of the liver should not be confused with focal nodular hyperplasia or any condition of the liver which might require resection. Compensatory hyperplasia may grossly resemble a neoplasm, especially, liver cell carcinoma. The hypertrophied liver, however, must not be excised, for it may represent the only functioning liver tissue, the hypertrophy being stimulated by liver destruction. Volume 121, March
1971
Only one benign neoplasm of the liver at this institution attained such size as to require a lobectomy. A huge hemangioma necessitated left lateral segmentectomy for removal, Trauma. Hepatic injuries have increased in number and severity, because of the increasing number of automobile accidents. Blunt injuries have mortality rates ranging from 20 to 81 per cent [ 18,31,33-371, whereas penetrating injuries have a much better prognosis. The prognostic difference is due to the severity of the injury, late diagnosis, and frequent procrastination associated with blunt trauma, as well as inadequate surgical treatment. The immediate consideration is control of hemorrhage. Superficial lacerations can be adequately treated by simple suture, but deep lacerations may require excisional therapy. Surgeons often are satisfied with surface closure of a deep laceration and rely on drainage to protect the patient from the dire consequences of the injury. After such inadequate treatment a cavity containing blood, bile, and necrotic tissue typically results. Postoperative infection, hemorrhage, and bile peritonitis may subsequently develop. An aggressive approach to massive hepatic injuries is necessary, including control of hemorrhage and extensive debridement of devitalized hepatic tissue, which may require resection of an entire lobe. According to McClelland et al [35], lobectomy in the treatment of severe hepatic injuries has reduced the mortality to 20 per cent. There is no doubt that today with the frequency of automobile accidents, the most common indication for hepatic lobectomy is injury. Liver destruction as the result of blunt trauma required hepatic lobectomies in four of our patients. In three patients the lobectomy was performed as the initial treatment, whereas in one, lobectomy was performed to excise hemorrhagic necrotic liver which had been inadequately treated one week previously. A right lobectomy was necessary in each instance. Congenital Malformations. Congenital malformations such as hamartomas and cysts occasionally attain such size as to cause symptoms. Any congenital anomaly that becomes large enough to cause symptoms, or whose histology is uncertain, should be excised. Occasionally massive resections, such as lobectomies, are necessary [13,38-421. Infection. Major resections for infectious processes, including granulomatous lesions and abscesses, are seldom necessary ; however, such operations have occasionally been performed with gratifying results [43,44]. Hepatic duct obstruction due to infection and fibrosis may also require hepatic lobectomy for relief [SS]. This was the in275
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dication for a left lobectomy in one patient early in this study. Intrahepatic biliary stenosis had been treated previously with a vitallium tube followed by fibrotic obstruction of the left hepatic duct with retrograde infection. Diagnostic Studies
Special diagnostic procedures aid in the selection of patients for hepatic lobectomy. In trauma, however, no time is allowed for ancillary studies, and decision for lobectomy can be made only by assessment at the time of exploration. On the other hand, when time permits, most unruptured spaceoccupying lesions of the liver can be better defined as to their nature and extent by various diagnostic technics. The usual liver function tests are of little value. Percutaneous Biopsy. By percutaneous liver biopsy the histologic diagnosis can be recognized in ‘75 per cent of cases. A positive diagnosis of malignant tumor should not be interpreted as a contraindication to operation, but should be a stimulus for exploration ; however, if malignant tumor is suspected on clinical grounds, percutaneous biopsy should not be carried out because spillage of tumor, hemorrhage, and bile peritonitis are formidable possibilities. Instead, exploratory celiotomy is performed. Should biopsy become necessary, then needle aspiration can be performed as an open procedure. Although we prefer not to perform a biopsy on what appears to be a malignant lesion, occasionally such biopsy may not only be warranted, but also life-saving. Compensatory hypertrophy of a liver in response to destruction of the liver by pre-existing disease may grossly resemble a malignant neoplasm. Excision of this hypertrophied tissue, which may be the only functioning liver tissue, would be catastrophic ; therefore, where doubt exists as to the true nature of any lesion, biopsy by confirmatory histologic examination is necessary. Angiography and Scintography. Hepatic arteriography and hepatic scintography can be used to outline masses and determine function of diseased segments. Selective hepatic arteriography will delineate the mass and help differentiate between neoplasm and other space-occupying lesions. Radioisotope scanning can be performed with either rose-bengal 1131which has an affinity for normal parenchymal cells, or with radioactive colloidal goldl”s and technetium colloidal sulfur190M which are picked up by the Kupffer’s cells. These diagnostic procedures outline a hepatic mass by a negative shadow. Splenoportography shows a mass by distortion of the intrahepatic portal venous system, but contrast media will not opacify the lesion. 276
Cholangiography. In our estimation operative cholangiography has been the most valuable method of demonstrating disease deep within the hepatic substance and determining the extent of the lesion. This simple procedure, by disclosing displacement or obstruction of biliary radicles, will determine the extent of resection necessary to eliminate the tumor. Preoperative Preparation
In the four patients who underwent hepatic lobectomy for traumatic lacerations and in two in whom there was rupture of a malignant neoplasm, time did not allow preparation except for resuscitation and control of equally severe concomitant injuries. Most patients with long-standing severe hepatic disease are critically ill and cachectic, with major metabolic disturbances. Before a major hepatic resection is performed on such a patient, existing abnormalities should be corrected when possible. In addition to general measures, we use a 3,000 calorie, 200 gram protein, and 350 gram carbohydrate diet. It is imperative to correct any defect in blood volume by transfusions and to reverse any clotting abnormalities which may exist. Serum potassium concentration has also been found to be decreased in some of these patients and may need replacement. Glucose with insulin may be given to insure adequate glycogen stores. Antibiotic intestinal sterilization to prevent local or systemic infections postoperatively is also advocated. Ancillary Precautions at Operation
At the time of surgery a large bore intravenous catheter should be inserted into both arms for the administration of blood and fluids. The hazards of hemorrhage in hepatic lobectomy are real, particularly from the hepatic veins and inferior vena cava. Therefore, blood should be administered into the superior vena cava and not into the inferior vena cava because replacement through the inferior vena cava may not only prove worthless, but also may further obscure the operative field. Since large volumes of blood may be necessary, and since cardiac venous return may be obstructed at various times during manipulation of a large hepatic mass, both central venous pressure and direct arterial pressures should be monitored continuously. By observing these parameters, preferably on an oscilloscope, both surgeon and anesthesiologist can better maintain homeostasis. Precautions to prevent the detrimental effects of massive transfusions should be instituted. Transfused blood should be warmed and the patient’s The
American
Journal
of Surgery
Hepatic Lobectomy temperature monitored. The patient should be on a circulating water blanket to control temperature to the desired level. A continuous electrocardiogram is also monitored on the oscilloscope in order to observe myocardial disturbances. Most anesthetics with various relaxing agents have been used without harmful effect in hepatic surgery. However, because of adverse publicity given to halothane in regard to hepatic injury, it is probably wise for legal reasons, if no other, to avoid this agent. It is important to maintain a high oxygen concentration at all times since liver cells withstand anoxia poorly. With an arterial needle in place for direct pressure measurements, blood gases can also be analyzed. Operative Technic
The technics for hepatic lobectomy have changed with time and indication. In the early experience resection was by the “guillotine” method and the tissue excised during a lobectomy was in reference to the topographic anatomy of the liver. In recent years the “controlled” method of resection with hilar dissection and individual ligation of the lobar structures has been used and the tissue excised has corresponded to this lobar distribution. Occasionally, when persistent and continuous bleeding exists, as in trauma, time cannot be taken to dissect individually the structures in the porta hepatis, and here a combination of technics, such as intermittent clamping of the portal triad structures, combined with a guillotine resection are employed. The surgeon should have a thorough knowledge of the anatomy of the liver and should be well versed in the many methods of controlling hemorrhage. Resection by the guillotine technic consists of insertion of large interlocking mattress sutures on each side of resection with progressive incision and ligation of necessary structures. This technic often results in profuse hemorrhage and necrosis of large amounts of hepatic substance. Consequently, it has been superseded by the control method when possible. The type of incision is most important. For right lobectomy a right thoracoabdominal incision is essential for adequate exposure, especially of the juncture of the hepatic veins with the vena cava. An initial vertical abdominal incision for exploration to determine resectability may be extended into the chest through the eighth or ninth intercostal space. The liver is fully mobilized by division of all peritoneal attachments. The use of this incision lessens obstruction of venous return and danger of rupturing a large tumor during manipulation. Also, by entering the chest there is neutralization of the intrapleural negative pressure, thereby deVolume
121,
March
1971
creasing the chance of air emboli from an open hepatic vein or vena cava. In hepatic trauma, adequate exposure to inspect the extent of injury must be obtained, especially for laceration in the dome of the liver, and a thoracoabdominal incision is usually necessary. On the other hand, most lesions of the left lobe can be treated through an abdominal incision. In the performance of hepatic lobectomy, attention is first directed toward dissection of the structures in the porta hepatis. When doubt exists, the appropriate hepatic duct may be identified by opening the common duct and inserting a probe which can remain in place until the duct is ligated and divided. After ligation of the corresponding hepatic artery, the lobe to be excised will change to a darker hue. Similarly, the appropriate branch of the portal vein and bile ducts are divided. All three structures should be divided as near to the liver as possible. Individual dissection of the portal triad structures may not be possible when a tumor is in a location or attains such size as to obscure the porta hepatis. In such a situation, or when confronted with hemorrhage, it is possible to control afferent bleeding by temporary occlusion of these structures. This maneuver may insure adequate visualization for dissection of the appropriate structures or resection with tolerable blood loss. Temporary control can be accomplished by occluding the structures between the thumb and index finger as the index finger lies in the foramen of Winslow, or by the application of an atraumatic vascular clamp. The danger of uncontrollable bleeding remains, however, until the corresponding branch of the hepatic vein is identified and controlled. This procedure must be done carefully since interruption of venous drainage from another area will result in infarction of that area. Because identification of the correct hepatic vein is often difficult at its junction with the vena cava, it may be preferable to divide the vein within the hepatic substance. If there is any question, division of the veins should be delayed until completion of the dissection. The middle hepatic vein must be preserved in lobectomies. A major problem arises when tumors encroach on the interlobar plane, displacing the middle hepatic vein, which can be a source of major hemorrhage. In such instances, amounts of tissue greater than a single lobe can be resected, a so-called extended hepatic lobectomy. Control of hepatic vein bleeding can also be accomplished by total exclusion of the liver from the inferior vena cava [46,47]. The insertion of an internal shunt into the vena cava with tentative control tourniquets above and below the liver can accomplish this. 277
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The hepatic substance is divided by sharp, blunt, or cautery dissection. For this purpose we prefer to use a semiblunt instrument, such as a knife handle. This allows identification of larger vessels and ducts which can be individually ligated to secure further hemostasis and prevent leakage of bile. Injection of normal saline solution into a T tube in the common duct will help demonstrate any remaining,patent bile ducts. Many methods have been used to insure hemostasis and aid in preventing leakhge of bile from the cut surface of the remaining liver. Muscle, the falciform ligament, omentum, and synthetic substances have been used to cover this cut surface. Experimentally an inflammatory reaction to most of these substances has been noted, with discharge of the material and production of foreign body granulomas [44]. However, clinically we have been impressed by the control of leakage after covering the cut surface with a viable pedicle of omentum. Both internal decompression by a T tube in the common duct and external drainage by multiple Penrose and catheter drains are necessary to prevent postoperative accumulation of blood, bile, or serum. Hypothermia has been a valuable technical adjunct to hepatic surgery. It is especially useful when total stasis of hepatic inflow is anticipated. Generalized or local intraperitoneal hypothermia to less than 30”~ will decrease hepatic metabolism and the amount of anesthesia required, prevent accumulation of toxic metabolites, and increase the tolerance of hepatic cells to anoxia. Both the afferent and efferent vascular structures can be occluded for periods up to one hour, and the operation can be performed in a relatively bloodless field [48]. Induced controlled systemic hypotension with or without portal hypotension may further reduce the hazards of hemorrhage [49,50]. Blood loss varied with the size of patient, indication for resection, technical difficulties, and method of resection. The least amount of blood (320 cc) was given to a five month old infant in whom easy control of the vasculature was obtained; and the TABLE
III
Complications Lobectomy
Occurring
Type of Complication Major Subphrenic abscess Pulmonary embolus Wound dehiscence Serum hepatitis Minor Transient jaundice Temporary biliary fistula
278
after Hepatic
Number
3 2 1 1 8 2
largest amount (14,000 cc) was given to an adult with traumatic laceration to the right lobe in whom only temporary control of the afferent and no control of the efferent vessels could be accomplished. The average amount of blood given to adult patients was 4,000 cc. Generalized hypothermia was used in three patients, but it is difficult to assess its value. No patient had controlled hypotension. Postoperative Management
The incidence of postoperative disturbances, such as fluid and electrolyte imbalance, pulmonary infection, and cardiac failure is no greater than that for any other major operation. Because of the large amount of blood replacement usually necessary, complications of massive blood transfusion exist. Prevention of a bleeding diathesis by appropriate replacement of necessary elements for proper coagulation is important. Fresh blood should be used whenever possible. Aminocaproic acid (Amica@, Lederle) is given to combat the fibrinolytic activity associated with liver destruction and vitamin K is given to insure adequate prothrombin time. Should congestive atelectasis occur as the result of multiple transfusions, prolonged ventilatory assistance and limitation of fluids is necessary [51,52]. Serum hepatitis resulting from large numbers of transfusions is a potentially serious problem particularly in patients with a small amount of residual functioning liver tissue. In one patient in our series serum hepatitis developed, but the patient quickly responded to the usual medical management without sequelae. (Table III.) Infection resulting from localized accumulation of blood, bile, or avascular necrosis of hepatic tissue is the most common complication, but the incidence can be lessened by attention to technical details and effective drainage. Awareness of the possibility of infected subphrenic fluid is important, for early drainage is mandatory in order to prevent sequelae. Subphrenic abscess developed in three patients which required drainage, and in each a septic course was reversed. Prolonged biliary drainage occurs, but fistulas usually close spontaneously or with mild negative pressure on drainage catheters and the T tube. Generalized bile peritonitis is a serious but infrequent complication. In two patients prolonged biliary fistulas developed which pers.isted four and six weeks before spontaneous closure. Two patients exhibited signs and symptoms of pulmonary embolism. In one the inferior vena cava was ligated and the other underwent bilateral suThe American
Journal of Surgery
Hepatic
perficial femoral vein ligation. Both patients survived this complication. In another patient, a wound dehiscence occurred on the sixth postoperative day with recovery after resuture. The most serious and immediate postoperative sequelae are associated with functional inadequacy of the hepatic remnant and can be avoided with proper care. The period after major hepatic resection is one of severe generalized stress as the remaining liver attempts to maintain homeostasis. Metabolic processes normally performed by the liver are greatly altered, as evidenced by abnormal results seen on hepatic function studies, and demands are placed on the body by the residual liver as it attempts to regenerate. Most important clinically is the immediate demand for protein by the regenerating liver, manifested by rapid decrease in total serum protein, mainly the albumin fraction. However, most patients will have normal serum protein levels by the third postoperative week. Serum albumin-globulin ratio may be reversed for as long as three months after hepatic lobectomy. There is frequently a transient increase in bilirubin, alkaline phosphatase, and bromsulfalein retention as the result of extrinsic pressure on the intrahepatic bile ducts, with partial occlusion by the intense portal venous congestion. Jaundice was recorded in eight of our patients but, in all of them, disappeared within three weeks. Serum transaminase values were slightly increased in the majority of patients, due to parenchymal anoxia or necrosis, but rapidly returned to normal. There is immediate decrease in blood sugar levels, but a return to normal usually within forty-eight hours. Mild decreases have been noted in prothrombin activity, fibrinogen, and factor VII. An increase in euglobulin fibrinolytic activity has also been noted. Ammonium toxicity was not noticed in any of our patients. In addition to the usual postoperative care, specific therapy is necessary to supply needed nutrients unt.il satisfactory liver function returns. Up TABLE
IV
Long-Term
Indications Liver carcinoma Hemangioma Trauma Embryonal carcinoma Trauma Embryonal carcinoma Liver carcinoma Liver carcinoma Trauma Trauma
Survivors
Operation Left lateral segmentectomy Left lobectomy Left lobectomy Right lobectomy Right lobectomy Right lobectomy Right Right Right Right
Volume 121, March 1971
lobectomy lobectomy lobectomy lobectomy
Years after Operation 21 13 8 8 8 6
Lobectomy
to 150 gm of glucose is administered intravenously daily for seventy-two hours since 10 per cent glucose is necessary to compensate for the immediate decrease in blood sugar. To combat profound hypoproteinemia, 25 to 50 gm of protein (parenteral albumin or plasma) are given daily for seven to ten days. Oral alimentation, with a high protein, high carbohydrate diet, should begin as soon as possible. Wide spectrum antibiotics are prophylactically given for five to seven days. We have not used steroids postoperatively, although steroids will accelerate the rapidity of regenerative hyperplasia of the liver. Results
Results of hepatic lobectomies have varied with the time, technic, and indication. Obviously, results today should be better than they were previously because of improvement in ancillary technics, such as the advances in anesthesia, the continuous monitoring of specific physiologic functions, and the improved procurement, processing, and administration of blood. In general, technical advances are simultaneous but a certain era is often considered the particular moment in time when technical advancements in a specific operation were made. The period covered in this study has definitely shown the greatest technical improvement in hepatic surgery. The accurate description of the true anatomy of the liver has enabled the surgeon to perform hepatic lobectomy by dissection of the lobar structures. Modern vascular surgery has taught technics that facilitate control of hemorrhage. Operative results depend upon the condition of the patient at the time of operation and the acuteness of the situation. The elderly hypotensive patient in need of a rapid lobectomy as’ the result of massive injury is undoubtedly a higher risk than a young patient with a space-occupying lesion which has yet to manifest symptoms. On the other hand, late results will undoubtedly be worse in patients undergoing lobectomy for malignant lesions, and particularly worse for those with metastatic lesions in contract to primary lesions. There was one operative death in this series, which occurred in 1950 from exsanguination resulting from laceration of the left hepatic vein during a left lobectomy for intrahepatic biliary obstruction. Ten of the twenty patients (50 per cent) can be considered long-term survivors. (Table IV.) Of the six patients with liver cell carcinoma, three died at six months, eight months, and eleven months respectively. Three are long-term survivors. One patient who survived twenty-one years recently died from myocardial insufficiency. At 279
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autopsy no recurrent tumor was found. Two other patients with primary liver cell carcinoma are now alive and well more than four years postoperatively. One of them recently underwent abdominal exploration for intestinal obstruction secondary to adhesions. At operation no residual or recurrent tumor was noted. This patient is particularly interesting, for it is believed that this represents a case of irradiation-induced liver cell carcinoma. During childhood this patient received 2,550 r to a large hemangioma located in the hilum of the liver because it was considered unresectable by the surgeon. Twenty years later a huge mass developed in the right lobe of the liver. At operation the hemangioma was completely obliterated by the previous x-ray therapy, but a massive multicentric liver cell carcinoma involved the right lobe of the liver. An extended right hepatic lobectomy was performed. The one patient with bile duct carcinoma survived thirty-two months, although recurrent disease was suspected fourteen months after operation. Two of the three children with embryonal carcinoma are alive and well six and eight years, respectively, after right hepatic lobectomy. The third child underwent an emergency right hepatic lobectomy after rupture of the tumor and survived only three months. The results of surgical treatment of primary carcinoma of the liver are not as dismal as previously thought. Of ten such patients with these neoplasms in this study, five (50 per cent) are considered to be long-term survivors or cures. This cure rate ranks high when compared to that of patients with malignant tumors of other major organs. Results of hepatic resection for metastatic lesions have varied, as has the extent of resection, from a small wedge resection for a solitary small peripheral metastasis to a lobectomy for extensive deep-seated metastasis. Many beneficial limited resections have been reported for metastatic disease, performed either at the time of resection of the primary tumor or many years later. No matter how infrequent the cure, limited hepatic resection and possibly left lateral segmentectomy for metastatic disease appear warranted in view of their relative safety. In contrast, when size and location of metastasis necessitate a hepatic lobectomy for eradication, the cure rate has been negligible and operative mortality high. Review of the literature reveals only two five year survivors of total hepatic lobectomy for embolic metastatic lesions [ 53,541. Our experience and that of others [55] with lobectomy in the treatment of metastatic disease support the inefficiency of such therapy. There were four patients in whom lobectomies were performed 280
for metastatic carcinoma. In an eighty-eight year old woman, an emergency right hepatic lobectomy was performed for rupture of a metastatic leiomyosarcoma with survival for only six months. Two patients underwent hepatic lobectomy for a solitary metastatic lesion from a carcinoma of the colon. Although one died in the early postoperative period, another survived for twenty months. One patient had a left lobectomy for a direct extension from a carcinoma of the stomach and this patient survived only one year. The combination of low curability and increased operative mortality suggests to us that if embolic metastasis is so extensive or in a location requiring hepatic lobectomy, the procedure is unwarranted. An exception to the natural response of embolic liver metastasis is that of functioning tumors. Immediate relief of the debilitating symptoms of a carcinoid syndrome has been reported by resection of massive hepatic metastasis of carcinoid tumors. Even when excision is incomplete, the levels of 5-hydroxyindole-acetic acid in the urine become negative in the immediate postoperative period and remain so for periods up to three years [56,57].
There was only one patient who underwent hepatic lobectomy for a benign tumor. This was a huge symptomatic hemangioma of the left lobe. The patient is alive and well thirteen years after operation. All four patients survived in whom hepatic lobectomy was necessary to control hemorrhage and/or to remove devitalized tissue as the result of trauma. Two of these operations were performed eight years ago, and although two had surgery relatively recently, they are apparently well and will probably be long-term survivors. Summary
Hepatic lobectomy was performed on twenty patients at the Ochsner Clinic over a twenty-two year period. The most common indication for operation in this series was primary malignant neoplasm. However, in recent years, due to the increase in automobile accidents, blunt trauma has become the most common indication for hepatic lobectomy. The operations performed in accordance to the segmental anatomy were ten right lobectomies, two extended right lobectomies, four left lobectomies, four left lateral segmentectomies. The surgeon should have a thorough knowledge of the anatomy of the liver and should be wellversed in the many methods to control hemorrhage. Proper preparation, precautions, and technical maneuvers establish hepatic lobectomy as a safe and effective operation. The
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Hepatic
There was one operative death (5 per cent). Five of the ten patients (50 per cent) who had lobectomy for primary malignant neoplasms are long-term survivors. In contrast, none of the four patients who had a hepatic lobectomy for metastatic disease were long-term survivors. All patients who had hepatic lobectomies for benign conditions are living. Of the total twenty patients in this series, ten (50 per cent) are considered to be long-term survivors.
24. 25.
26.
27.
28.
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22.
23.
29. Healey JE Jr: Clinical anatomic aspects of radical hepatic surgery. J lnternat Coil Surg 22: 542, 1954. Goldsmith NA, Woodburne RT: The surgical anatomy pertaining to liver resection. Surg Gynec Obstet 105: 310, 1957. Brearley R: Modern developments in liver surgery. Lancet 1: 935, 1961. lslami AH, Pack GT, Hubbard JC: The humoral factor in regeneration of the liver in parabiotic rats. Surg Gynec Obstet 108: 549, 1959. McDermott WV Jr, Greenberger NJ, lsselbacher KJ, Weber AL: Major hepatic resection: diagnostic techniques and metabolic problems. Surgery 54: 56, 1963. Berta: Cited by Brearley R 131. Wendel W: Beitrlge zur Chirurgie der Leber. Arch Klin Chir 95: 887, 1911. Pettinari V: La resezione epatica second0 la mia esperienza. Seizieme Congres Sot Int Chir. p 1169, 1955. Lortat-Jacob JL, Robert HG: Hepatectomie droite reglee. Presse Med 60: 549, 1952. Balasegaram M: Hepatic resection. Brit J Surg 55: 168, 1968. Brunschwig A: Hepatic lobectomies. Amer J Gastroent 44: 245, 1965. Lawrence GH, Grauman D, Lasersohn J, Baker JW: Primary carcinoma of the liver. Amer J Surg 112: 200, 1966. Longmire WP, Passaro EP, Joseph WL: The surgical treatment of hepatic lesions. Brit J Surg 53: 852, 1966. Lin TY: The results of hepatic lobectomy for primary carcinoma of the liver. Surg Gynec Obstet 123: 289, 1966. Pack GT: Surgical management of primary and metastatic cancers of the liver. Northwest Med 57: 881. 1958. Pettinari V, Dagradi A: Hepatic resection. Panminerva Med 5: 123,1963. Quattlebaum JK, Quattlebaum JK Jr: Technic of hepatic lobectomy. Ann Surg 149: 648, 1959. Smith R, Hobsley M, Stephen JL: Hepatectomy (abridged). Proc Roy Sot Med 57: 547, 1%4. Burdette WJ: Primary Hepatoma. Salt Lake City, University of Utah Press, 1965. Chan KT: The management of primary liver carcinoma. Ann Roy Coil Surg Eng 41: 253,1967. Edmondson HA: Tumors of the Liver and lntrahepatic Bile Ducts, section VII. fascicle 25. D 216. Atlas of Tumor Pathology. Washington, DC, Armed Forces Institute of Pathology, 1958. Bradham RR, Paul JR, Thrower WB, Mclver FA: Malig nant hepatoma in a child, survival following right hepatectomy, right pneumonectomy and resection of diaphragmatic and parietal recurrence. Surgery 57: 767, 1965. Clatworthy HW Jr, Boles ET Jr, Kottmeier PK: Liver
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30.
31. 32. 33. 34.
35. 36.
37.
38.
39. 40.
41.
42.
43. 44.
45.
46.
47. 48. 49.
50.
Lobectomy
tumors in infancy and childhood. Ann Surg 154: 475, 1961. Haller JA Jr, Stowens D: Right hepatic lobectomy in infancy. Surgery 53: 368, 1963. Peterson RD, Varco RL, Good RA: Five-year survival of an infant after surgical excision of an embryonal hepatoma. Pediatrics 27: 474, 1961. Steiner MM: Primary carcinoma of liver in childhood: report of 2 cases with critical review of literature. Amer J Dis Child 55: 807, 1938. Watkins GL: Primary carcinoma of the liver in an infant, right lobectomy with 6-year survival. Ann Surg 162: 264,1965. Lorimer WS Jr: Right hepatolobectomy for primary mesenchymoma of the liver. Ann Surg 141: 246, 1955. Woodington GF, Waugh JM: Results of resection of metastatic tumors of the liver. Amer J Surg 105: 24, 1963. Pack GT, Miller TR, Brasfield RD: Total right hepatic lobectomy for cancer of the gallbladder: report of three cases. Ann Surg 142: 6, 1955. Longmire WP Jr: Hepatic surgery: trauma, tumors and cysts. Ann Surg 161: 1, 1965. Longmire WP Jr, Marable SA: Clinical experiences with major hepatic resections. Ann Surg 154: 460, 1961. Ochsner JL, Halpert B: Cavernous hemangioma of the liver. Surgery 43: 577, 1958. Crosthwait RW, Allen JE, Murga F, Beall AC Jr, Debakey ME: The surgical management of 640 consecutive liver injuries in civilian practice. Surg Gynec Obstet 114: 650, 1962. McClelland R, Shires T, Poulos E: Hepatic resection for massive trauma. J Trauma 4: 282, 1964. Atik M, Grossman R, Dekernian J: Hepatectomy for severe liver injury. Arch Surg (Chicago) 92: 636, 1966. Ackroyd FW, Pollard J, McDermott WV Jr: Massive hepatic resection in the treatment of severe liver trauma. Amer J Surg 117: 442, 1969. Henson SW, Gray HK, Dockerty MB: Benign tumors of the liver. IV. Polycystic disease of surgical significance. Surg Gynec Obstet 104: 63, 1957. Clay RC, Finney GG: Lobectomy of the liver for benign conditions. Ann Surg 147: 827, 1958. Minton JP, Kinsey DL: Surgical management of a recurrent solitary multilocular nonparasitic cyst of the liver. Amer J Surg 102: 710, 1961. Monaco AP, Hallgrimsson J, McDermott WV Jr: Multiple adenoma (hamartoma) of the liver treated by subtotal (90%) resection: morphological and functional studies of regeneration. Ann Sure 159: 513. 1964. Taylor PH, Filler RM, Nebesar RA, Tefft M: ‘Experience with hepatic resection in childhood. Amer J Surg 117: 435, 1969. Pack GT, Baker HW: Total right hepatic lobectomy: report of a case. Ann Surg 138: 253, 1953. Hicken NF, McAllister AJ, Nilsson J: Resection of the entire left lobe of the liver: intrahepatic abscesses, stones and foreign bodies. Amer J Surg 105: 278, 1963. Mistilis S, Schiff L: A case of jaundice due to unilateral hepatic duct obstruction with relief after hepatic lobectomy. Gut 4: 13, 1963. Timmis HH, Rosanova AR Jr, Larkin WB: Bloodless hepatic resection with an internal caval shunt. Surgery 65: 109, 1969. Blaisdell W: Discussion of Timmis paper. Surgery 65: 117, 1969. Tung TT, Quang ND: A new technique for operating on the liver. Lancet 1: 192, 1963. Martin DS, Galliano R: Bloodless liver resection under hypotensive hypothermia. Amer J Surg 109: 625, 1965. Kaplan A, Davies JI, Heilbrunn A: The experimental use 281
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and Ochsner
of controlled portal and systemic hypotension for liver resection. Surgery 62: 325, 1967. 51. Jenkins MT, Jones RF, Wilson 6, Moyer CA: Congestive atelectasis: complication of intravenous infusion of fluid. Ann Surg 132: 327, 1950. 52. Hatch HB Jr, Carrera GM: Congestive atelectasis: a fatal postoperative complication. J Thorac Cardiovasc Surg 37: 257, 1959. 53. Peden JC Jr, Blalock WN: Right hepatic lobectomy for metastatic carcinoma of the large bowel, five year survival. Cancer 16: 1133, 1963. 54. Wedemeyer PP, White JG, Nesbit ME, Aust JB, Leonard
282
AS, D’Angio GJ, Krivit W: Resection of metastases in Wilms’ tumor: a report of three cases cured of pulmonary and hepatic metastases. Pediatrics 41: 446,
1968. 55. Gaston EA: Liver resections cancer
of the colon
for embolic metastases from and rectum. Dis Colon Rectum 9:
189, 1966. 56. Mosenthal WT: Resection
57.
the malignant port of a case. Adson MA: Major Mayo Clin Proc
of massive liver metastases in carcinoid syndrome: review and reSurg Clin N Amer 43: 1253, 1963. hepatic resections: elective operations.
42: 791, 1967.
The American
Journal
of Surgery
Major hepatic resections have been performed for more than a century, yet the risk of such resections was almost prohibitive until recently. Progress in hepatic surgery has been slow, but this is understandable considering the technical difficulties encountered in massive liver resection in addition to disturbances occurring after removal of a viscus which performs so many indispensable physiologic functions. It was not until 1954 that anatomic dissections demonstrated the true lobar and segmental pattern of the liver [1,2], and subsequent physiologic experiments have demonstrated its tremendous regenerative capacity [3-51. These two advancements enable the surgeon to perform major hepatic resections safely and with confidence. Indications for and the results of hepatic lobectomy have shown such differences that enthusiasm for the operation has varied from omission to panacea. In general, the operation is rarely indicated or performed. Consequently, an individual surgeon has little opportunity for a large personal experience. It seems desirable, therefore, to analyze the experience at the Ochsner Clinic over a twenty-two year period. Clinical Material
During a twenty-two year period ending in 1968, twenty patients underwent hepatic lobectomy at the Ochsner Clinic. In this paper the term “lobectomy” conforms to both the topographic anatomy and the lobar pattern as defined by the distribution of the Glissonian structures, that is, the hepatic artery, portal vein, and bile ducts. The anatomic boundaries of the latter were not delineated until fairly recently and most authors today refer to this anatomic division, although some still prefer the topographic anatomy. In regard to the topographic anatomy, there were twelve right lobectomies and eight left lobectomies. In regard to the distribution of the Glissonian structures there were ten right lobectomies, two extended right lobectomies (right From the Department dation Hospital, New Reprint requests Clinic, 1514 Jefferson * Present address:
of Surgery, Ochsner Clinic and Ochsner FounOrleans, Louisiana. may be addressed to John Ochsner. Ochsner Highway, New Orleans, Louisiana 70121. 320 Tuttle Road, San Antonio, Texas 78209.
Volume 121,
1971
March
L. OCHSNER,
BARRY
E. MEYERS,
ALTON
OCHSNER,
MD,
New
MD,* MD,
New
Orleans, Louisiana Orleans,
New Orleans,
Louisiana
Louisiana
lobe and medial segment of left lobe), four left lobectomies, and four left lateral segmentectomies. (Table I.) The ages of the patients ranged from five months to eighty-eight years. Of the patients, all Caucasians, nine were male ; and eleven, female. All patients have been followed. Historical Background
Berta [6] is credited with performing the first hepatic resection in 1760 when he amputated an exteriorized portion of the right lobe of the liver. The first planned right hepatic lobectomy was performed by Wendel [7] in 1911, when he individually ligated the right hepatic artery and the right bile duct. He did not ligate the right portal vein for fear of a thrombus propagating from the stump into the contralateral portal system. The first anatomic total hepatic lobectomy (left hepatic lobectomy) performed according to the units of vascular and ductal distribution preceded by hilar ligation was carried out by Pettinari [8] in 1940. In 1952 Lortat-Jacob and Robert [9] demonstrated that bleeding could be controlled during hepatic lobectomy by preliminary isolation and ligation of the vascular structures in the porta hepatis and careful parenchymal dissection based on knowledge of the anatomic segments of the liver. Extensive experience in hepatic lobectomy, using various technical maneuvers, has been described by Balasegaram [ IO], Brunschwig [ .ZI], Lawrence et al [12], Longmire et al [13], Lin [IS], Pack [15], Pettinari and Dagradi [16], Quattlebaum [ 171, and Smith et al [18]. The operative mortality has progressively declined, and although early reports gave a pessimistic outlook toward long-term results, recent reports have been encouraging. Surgical Indications Liver Cell Carcinoma.
Until relatively recently malignant disease was the most common indication for hepatic lobectomy. As in other areas of the body, wide excision along anatomically defined boundaries offers the best chance of cure. Threefourths of all primary malignant tumors of the liv273
Ochsner,
Meyers,
I
TABLE
and
Ochsner
Hepatic Lobectomy at Ochsner Clinic (1946-1968) Type of Operation
Number
Right lobectomy Extended right lobectomy Left lobectomy Left lateral segmentectomy Total
10 2 4 4 20
-
er arise from the liver cell. Primary liver cell carcinoma appears with greater frequency in certain geographic areas and seems to be produced by various environmental factors [ 19,20]. This neoplasm occurs relatively frequently in Southeast Asia and in Southern Africa, but it is uncommon in the United States and Europe. The majority of patients with primary liver cell carcinoma have extrahepatic metastasis at the time of diagnosis. Intrahepatic metastases often lie within the same portal tract as the initial lesion, since metastases result from invasion of portal vein trunks, which makes the lesion resectable. Six patients. in this series had hepatic lobectomy for primary liver cell carcinoma, which was the most common indication for hepatic lobectomy. (Table II.) The operations employed were a left lateral segmentectomy in one, left lobectomy in two, right lobectomy in two, and extended right lobectomy in one. Bile Duct Carcinoma. Bile duct carcinoma is the second most common primary malignant tumor of the liver. These tumors are invariably multicentric, widespread, and rarely are amenable to curative resections. Only one patient in our group had a bile duct carcinoma for which right lobectomy was performed. Embryonal Carcinoma. Carcinomas of the liver in infants and children differ greatly, both clinically and histologically, from those seen in adults and show evidence of congenital origin [21]. Therefore, the term “embryonal carcinoma” apTABLE
II
Indications
for Hepatic
Indications Neoplasm Malignant Primary Liver cell carcinoma Bile duct carcinoma Embryonal carcinoma Metastatic Colon carcinoma Leiomyosarcoma Stomach carcinoma Benign Hemangioma Trauma Inflammatory Bile duct stricture Total
274
Lobectomy Number
6 1 3 2 1 1 1 4 1 20
pears appropriate. These interesting neoplasms are among the most common malignant tumors seen in infants. They are generally solitary, confined to the liver, and are therefore resectable, but the prognosis is poor. There are reports of successful single short and long-term survivals after hepatic lobectomy [22-271. Three children with this tumor had either a right or extended right hepatic lobectomy in our series. Two had elective resections, whereas in one an emergency lobectomy was performed because of rupture of the neoplasm after minor trauma. Other Primary Malignant Tumors. Hepatic lobectomy has been used successfully f’or other solitary primary malignant tumors, such as angiosarcoma [I I I and malignant mesenchymoma [ 281. Metastatic Lesions. Subtotal hepatic resection, including lobectomy, under favorable circumstances has been advocated for metastatic lesions of the liver, whether these are direct extensions from a contiguous structure or embolic from a distant primary tumor. Adenocarcinoma of the gallbladder has a uniformly poor prognosis, largely because of the late diagnosis and proximity to the liver with the possibility of direct spread. The infrequent cure depends primarily on the fortuitous excision of small lesions at the time of cholecystectomy for cholelithiasis. Prophylactic wedge resection of the hepatic bed is considered the least measure which offers a chance of cure [29]. Pack et al [30], however, had little success with wedge resection and advocate right hepatic lobectomy when liver extension from gallbladder carcinoma is discovered. Direct extension to the liver from carcinoma of the stomach and colon has also been treated by excision of the primary lesion with en bloc concomitant hepatic lobectomy, usually left lobectomy. Results have generally been disappointing, but involvement by direct spread offers a more favorable outlook than involvement by hematogenous route. Four patients underwent hepatic lobectomy for metastatic disease. In each instance the metastasis was of such size or so positioned as to require lobectomy for removal of the lesion. Blood-borne metastasis from carcinoma of the colon, previously resected, was the indication for Iobectomy in two patients. In the oldest patient in this series, an eighty-eight year old woman, right hepatic lobectomy was performed to control bleeding from rupture of a metastatic leiomyosarcoma. A left hepatic lobectomy was combined with total gastrectomy in excision of a carcinoma of the stomach with direct extension into the liver. Benign Lesions. Results of resection of benign hepatic lesions have been excellent. Peripheral The American
Journal
of Surgery
Hepatic Lobectomy
lesions can be excised with minimal risk and afford an accurate diagnosis of questionable lesions. Hepatic lobectomy for benign lesions should be reserved for those which cause disabling symptoms. Hepatic and bile duct adenomas are rare. Although usually exceedingly small, they may become large and produce pressure symptoms, such as fullness and nausea, and can cause biliary obstruction. Because of the difficulty in differentiating them from primary malignant neoplasms, and because of the possibility of malignant transformation, these lesions should be widely resected. Patients with such lesions have been followed up for as long as seventeen years after resection with no apparent recurrence [31]. Hemangiomas are the most commonly resectable hepatic tumors and, although generally small, may attain massive size, necessitating lobectomy for extirpation. Large hemangiomas may produce symptoms as the result of pressure and are SWceptible ,to traumatic or spontaneous rupture. Of the fourteen cases of ruptured hemangiomas reviewed by Longmire and Marable [32], twelve were fatal. Large arteriovenous communications within the hemangioma can cause congestive heart failure. Vascular lesions must be resected through a rim of normal tissue to prevent uncontrollable hemorrhage. Irradiation may be advisable preoperatively to reduce the size of the tumor and has even been used as the sole method of therapy. Although irradiation may reduce the size of hemangiomas of the liver, it probably should never be used in young patients because of the carcinogenic effect of radiation. The most common vascular malformation, cavernous hemangiomas of the liver, may in reality be vascular hamartomas [33]. They appear to have no growth potential, but grossly may be indistinguishable from true neoplasms. Areas of focal nodular hyperplasia of the liver have been considered tumor-like lesions. Opinions differ as to whether these lesions are the result of regenerative phenomena, hamartoma, or neoplasm. Edmondson [21] believes that some type of local injury to the liver and interference or diminution of blood supply are causative factors. These areas may become quite large and require resection if symptomatic [31]. Compensatory hypertrophy of the liver should not be confused with focal nodular hyperplasia or any condition of the liver which might require resection. Compensatory hyperplasia may grossly resemble a neoplasm, especially, liver cell carcinoma. The hypertrophied liver, however, must not be excised, for it may represent the only functioning liver tissue, the hypertrophy being stimulated by liver destruction. Volume 121, March
1971
Only one benign neoplasm of the liver at this institution attained such size as to require a lobectomy. A huge hemangioma necessitated left lateral segmentectomy for removal, Trauma. Hepatic injuries have increased in number and severity, because of the increasing number of automobile accidents. Blunt injuries have mortality rates ranging from 20 to 81 per cent [ 18,31,33-371, whereas penetrating injuries have a much better prognosis. The prognostic difference is due to the severity of the injury, late diagnosis, and frequent procrastination associated with blunt trauma, as well as inadequate surgical treatment. The immediate consideration is control of hemorrhage. Superficial lacerations can be adequately treated by simple suture, but deep lacerations may require excisional therapy. Surgeons often are satisfied with surface closure of a deep laceration and rely on drainage to protect the patient from the dire consequences of the injury. After such inadequate treatment a cavity containing blood, bile, and necrotic tissue typically results. Postoperative infection, hemorrhage, and bile peritonitis may subsequently develop. An aggressive approach to massive hepatic injuries is necessary, including control of hemorrhage and extensive debridement of devitalized hepatic tissue, which may require resection of an entire lobe. According to McClelland et al [35], lobectomy in the treatment of severe hepatic injuries has reduced the mortality to 20 per cent. There is no doubt that today with the frequency of automobile accidents, the most common indication for hepatic lobectomy is injury. Liver destruction as the result of blunt trauma required hepatic lobectomies in four of our patients. In three patients the lobectomy was performed as the initial treatment, whereas in one, lobectomy was performed to excise hemorrhagic necrotic liver which had been inadequately treated one week previously. A right lobectomy was necessary in each instance. Congenital Malformations. Congenital malformations such as hamartomas and cysts occasionally attain such size as to cause symptoms. Any congenital anomaly that becomes large enough to cause symptoms, or whose histology is uncertain, should be excised. Occasionally massive resections, such as lobectomies, are necessary [13,38-421. Infection. Major resections for infectious processes, including granulomatous lesions and abscesses, are seldom necessary ; however, such operations have occasionally been performed with gratifying results [43,44]. Hepatic duct obstruction due to infection and fibrosis may also require hepatic lobectomy for relief [SS]. This was the in275
Ochsner,
Meyers,
and
Ochsner
dication for a left lobectomy in one patient early in this study. Intrahepatic biliary stenosis had been treated previously with a vitallium tube followed by fibrotic obstruction of the left hepatic duct with retrograde infection. Diagnostic Studies
Special diagnostic procedures aid in the selection of patients for hepatic lobectomy. In trauma, however, no time is allowed for ancillary studies, and decision for lobectomy can be made only by assessment at the time of exploration. On the other hand, when time permits, most unruptured spaceoccupying lesions of the liver can be better defined as to their nature and extent by various diagnostic technics. The usual liver function tests are of little value. Percutaneous Biopsy. By percutaneous liver biopsy the histologic diagnosis can be recognized in ‘75 per cent of cases. A positive diagnosis of malignant tumor should not be interpreted as a contraindication to operation, but should be a stimulus for exploration ; however, if malignant tumor is suspected on clinical grounds, percutaneous biopsy should not be carried out because spillage of tumor, hemorrhage, and bile peritonitis are formidable possibilities. Instead, exploratory celiotomy is performed. Should biopsy become necessary, then needle aspiration can be performed as an open procedure. Although we prefer not to perform a biopsy on what appears to be a malignant lesion, occasionally such biopsy may not only be warranted, but also life-saving. Compensatory hypertrophy of a liver in response to destruction of the liver by pre-existing disease may grossly resemble a malignant neoplasm. Excision of this hypertrophied tissue, which may be the only functioning liver tissue, would be catastrophic ; therefore, where doubt exists as to the true nature of any lesion, biopsy by confirmatory histologic examination is necessary. Angiography and Scintography. Hepatic arteriography and hepatic scintography can be used to outline masses and determine function of diseased segments. Selective hepatic arteriography will delineate the mass and help differentiate between neoplasm and other space-occupying lesions. Radioisotope scanning can be performed with either rose-bengal 1131which has an affinity for normal parenchymal cells, or with radioactive colloidal goldl”s and technetium colloidal sulfur190M which are picked up by the Kupffer’s cells. These diagnostic procedures outline a hepatic mass by a negative shadow. Splenoportography shows a mass by distortion of the intrahepatic portal venous system, but contrast media will not opacify the lesion. 276
Cholangiography. In our estimation operative cholangiography has been the most valuable method of demonstrating disease deep within the hepatic substance and determining the extent of the lesion. This simple procedure, by disclosing displacement or obstruction of biliary radicles, will determine the extent of resection necessary to eliminate the tumor. Preoperative Preparation
In the four patients who underwent hepatic lobectomy for traumatic lacerations and in two in whom there was rupture of a malignant neoplasm, time did not allow preparation except for resuscitation and control of equally severe concomitant injuries. Most patients with long-standing severe hepatic disease are critically ill and cachectic, with major metabolic disturbances. Before a major hepatic resection is performed on such a patient, existing abnormalities should be corrected when possible. In addition to general measures, we use a 3,000 calorie, 200 gram protein, and 350 gram carbohydrate diet. It is imperative to correct any defect in blood volume by transfusions and to reverse any clotting abnormalities which may exist. Serum potassium concentration has also been found to be decreased in some of these patients and may need replacement. Glucose with insulin may be given to insure adequate glycogen stores. Antibiotic intestinal sterilization to prevent local or systemic infections postoperatively is also advocated. Ancillary Precautions at Operation
At the time of surgery a large bore intravenous catheter should be inserted into both arms for the administration of blood and fluids. The hazards of hemorrhage in hepatic lobectomy are real, particularly from the hepatic veins and inferior vena cava. Therefore, blood should be administered into the superior vena cava and not into the inferior vena cava because replacement through the inferior vena cava may not only prove worthless, but also may further obscure the operative field. Since large volumes of blood may be necessary, and since cardiac venous return may be obstructed at various times during manipulation of a large hepatic mass, both central venous pressure and direct arterial pressures should be monitored continuously. By observing these parameters, preferably on an oscilloscope, both surgeon and anesthesiologist can better maintain homeostasis. Precautions to prevent the detrimental effects of massive transfusions should be instituted. Transfused blood should be warmed and the patient’s The
American
Journal
of Surgery
Hepatic Lobectomy temperature monitored. The patient should be on a circulating water blanket to control temperature to the desired level. A continuous electrocardiogram is also monitored on the oscilloscope in order to observe myocardial disturbances. Most anesthetics with various relaxing agents have been used without harmful effect in hepatic surgery. However, because of adverse publicity given to halothane in regard to hepatic injury, it is probably wise for legal reasons, if no other, to avoid this agent. It is important to maintain a high oxygen concentration at all times since liver cells withstand anoxia poorly. With an arterial needle in place for direct pressure measurements, blood gases can also be analyzed. Operative Technic
The technics for hepatic lobectomy have changed with time and indication. In the early experience resection was by the “guillotine” method and the tissue excised during a lobectomy was in reference to the topographic anatomy of the liver. In recent years the “controlled” method of resection with hilar dissection and individual ligation of the lobar structures has been used and the tissue excised has corresponded to this lobar distribution. Occasionally, when persistent and continuous bleeding exists, as in trauma, time cannot be taken to dissect individually the structures in the porta hepatis, and here a combination of technics, such as intermittent clamping of the portal triad structures, combined with a guillotine resection are employed. The surgeon should have a thorough knowledge of the anatomy of the liver and should be well versed in the many methods of controlling hemorrhage. Resection by the guillotine technic consists of insertion of large interlocking mattress sutures on each side of resection with progressive incision and ligation of necessary structures. This technic often results in profuse hemorrhage and necrosis of large amounts of hepatic substance. Consequently, it has been superseded by the control method when possible. The type of incision is most important. For right lobectomy a right thoracoabdominal incision is essential for adequate exposure, especially of the juncture of the hepatic veins with the vena cava. An initial vertical abdominal incision for exploration to determine resectability may be extended into the chest through the eighth or ninth intercostal space. The liver is fully mobilized by division of all peritoneal attachments. The use of this incision lessens obstruction of venous return and danger of rupturing a large tumor during manipulation. Also, by entering the chest there is neutralization of the intrapleural negative pressure, thereby deVolume
121,
March
1971
creasing the chance of air emboli from an open hepatic vein or vena cava. In hepatic trauma, adequate exposure to inspect the extent of injury must be obtained, especially for laceration in the dome of the liver, and a thoracoabdominal incision is usually necessary. On the other hand, most lesions of the left lobe can be treated through an abdominal incision. In the performance of hepatic lobectomy, attention is first directed toward dissection of the structures in the porta hepatis. When doubt exists, the appropriate hepatic duct may be identified by opening the common duct and inserting a probe which can remain in place until the duct is ligated and divided. After ligation of the corresponding hepatic artery, the lobe to be excised will change to a darker hue. Similarly, the appropriate branch of the portal vein and bile ducts are divided. All three structures should be divided as near to the liver as possible. Individual dissection of the portal triad structures may not be possible when a tumor is in a location or attains such size as to obscure the porta hepatis. In such a situation, or when confronted with hemorrhage, it is possible to control afferent bleeding by temporary occlusion of these structures. This maneuver may insure adequate visualization for dissection of the appropriate structures or resection with tolerable blood loss. Temporary control can be accomplished by occluding the structures between the thumb and index finger as the index finger lies in the foramen of Winslow, or by the application of an atraumatic vascular clamp. The danger of uncontrollable bleeding remains, however, until the corresponding branch of the hepatic vein is identified and controlled. This procedure must be done carefully since interruption of venous drainage from another area will result in infarction of that area. Because identification of the correct hepatic vein is often difficult at its junction with the vena cava, it may be preferable to divide the vein within the hepatic substance. If there is any question, division of the veins should be delayed until completion of the dissection. The middle hepatic vein must be preserved in lobectomies. A major problem arises when tumors encroach on the interlobar plane, displacing the middle hepatic vein, which can be a source of major hemorrhage. In such instances, amounts of tissue greater than a single lobe can be resected, a so-called extended hepatic lobectomy. Control of hepatic vein bleeding can also be accomplished by total exclusion of the liver from the inferior vena cava [46,47]. The insertion of an internal shunt into the vena cava with tentative control tourniquets above and below the liver can accomplish this. 277
Ochsner,
Meyers, and
Ochsner
The hepatic substance is divided by sharp, blunt, or cautery dissection. For this purpose we prefer to use a semiblunt instrument, such as a knife handle. This allows identification of larger vessels and ducts which can be individually ligated to secure further hemostasis and prevent leakage of bile. Injection of normal saline solution into a T tube in the common duct will help demonstrate any remaining,patent bile ducts. Many methods have been used to insure hemostasis and aid in preventing leakhge of bile from the cut surface of the remaining liver. Muscle, the falciform ligament, omentum, and synthetic substances have been used to cover this cut surface. Experimentally an inflammatory reaction to most of these substances has been noted, with discharge of the material and production of foreign body granulomas [44]. However, clinically we have been impressed by the control of leakage after covering the cut surface with a viable pedicle of omentum. Both internal decompression by a T tube in the common duct and external drainage by multiple Penrose and catheter drains are necessary to prevent postoperative accumulation of blood, bile, or serum. Hypothermia has been a valuable technical adjunct to hepatic surgery. It is especially useful when total stasis of hepatic inflow is anticipated. Generalized or local intraperitoneal hypothermia to less than 30”~ will decrease hepatic metabolism and the amount of anesthesia required, prevent accumulation of toxic metabolites, and increase the tolerance of hepatic cells to anoxia. Both the afferent and efferent vascular structures can be occluded for periods up to one hour, and the operation can be performed in a relatively bloodless field [48]. Induced controlled systemic hypotension with or without portal hypotension may further reduce the hazards of hemorrhage [49,50]. Blood loss varied with the size of patient, indication for resection, technical difficulties, and method of resection. The least amount of blood (320 cc) was given to a five month old infant in whom easy control of the vasculature was obtained; and the TABLE
III
Complications Lobectomy
Occurring
Type of Complication Major Subphrenic abscess Pulmonary embolus Wound dehiscence Serum hepatitis Minor Transient jaundice Temporary biliary fistula
278
after Hepatic
Number
3 2 1 1 8 2
largest amount (14,000 cc) was given to an adult with traumatic laceration to the right lobe in whom only temporary control of the afferent and no control of the efferent vessels could be accomplished. The average amount of blood given to adult patients was 4,000 cc. Generalized hypothermia was used in three patients, but it is difficult to assess its value. No patient had controlled hypotension. Postoperative Management
The incidence of postoperative disturbances, such as fluid and electrolyte imbalance, pulmonary infection, and cardiac failure is no greater than that for any other major operation. Because of the large amount of blood replacement usually necessary, complications of massive blood transfusion exist. Prevention of a bleeding diathesis by appropriate replacement of necessary elements for proper coagulation is important. Fresh blood should be used whenever possible. Aminocaproic acid (Amica@, Lederle) is given to combat the fibrinolytic activity associated with liver destruction and vitamin K is given to insure adequate prothrombin time. Should congestive atelectasis occur as the result of multiple transfusions, prolonged ventilatory assistance and limitation of fluids is necessary [51,52]. Serum hepatitis resulting from large numbers of transfusions is a potentially serious problem particularly in patients with a small amount of residual functioning liver tissue. In one patient in our series serum hepatitis developed, but the patient quickly responded to the usual medical management without sequelae. (Table III.) Infection resulting from localized accumulation of blood, bile, or avascular necrosis of hepatic tissue is the most common complication, but the incidence can be lessened by attention to technical details and effective drainage. Awareness of the possibility of infected subphrenic fluid is important, for early drainage is mandatory in order to prevent sequelae. Subphrenic abscess developed in three patients which required drainage, and in each a septic course was reversed. Prolonged biliary drainage occurs, but fistulas usually close spontaneously or with mild negative pressure on drainage catheters and the T tube. Generalized bile peritonitis is a serious but infrequent complication. In two patients prolonged biliary fistulas developed which pers.isted four and six weeks before spontaneous closure. Two patients exhibited signs and symptoms of pulmonary embolism. In one the inferior vena cava was ligated and the other underwent bilateral suThe American
Journal of Surgery
Hepatic
perficial femoral vein ligation. Both patients survived this complication. In another patient, a wound dehiscence occurred on the sixth postoperative day with recovery after resuture. The most serious and immediate postoperative sequelae are associated with functional inadequacy of the hepatic remnant and can be avoided with proper care. The period after major hepatic resection is one of severe generalized stress as the remaining liver attempts to maintain homeostasis. Metabolic processes normally performed by the liver are greatly altered, as evidenced by abnormal results seen on hepatic function studies, and demands are placed on the body by the residual liver as it attempts to regenerate. Most important clinically is the immediate demand for protein by the regenerating liver, manifested by rapid decrease in total serum protein, mainly the albumin fraction. However, most patients will have normal serum protein levels by the third postoperative week. Serum albumin-globulin ratio may be reversed for as long as three months after hepatic lobectomy. There is frequently a transient increase in bilirubin, alkaline phosphatase, and bromsulfalein retention as the result of extrinsic pressure on the intrahepatic bile ducts, with partial occlusion by the intense portal venous congestion. Jaundice was recorded in eight of our patients but, in all of them, disappeared within three weeks. Serum transaminase values were slightly increased in the majority of patients, due to parenchymal anoxia or necrosis, but rapidly returned to normal. There is immediate decrease in blood sugar levels, but a return to normal usually within forty-eight hours. Mild decreases have been noted in prothrombin activity, fibrinogen, and factor VII. An increase in euglobulin fibrinolytic activity has also been noted. Ammonium toxicity was not noticed in any of our patients. In addition to the usual postoperative care, specific therapy is necessary to supply needed nutrients unt.il satisfactory liver function returns. Up TABLE
IV
Long-Term
Indications Liver carcinoma Hemangioma Trauma Embryonal carcinoma Trauma Embryonal carcinoma Liver carcinoma Liver carcinoma Trauma Trauma
Survivors
Operation Left lateral segmentectomy Left lobectomy Left lobectomy Right lobectomy Right lobectomy Right lobectomy Right Right Right Right
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lobectomy lobectomy lobectomy lobectomy
Years after Operation 21 13 8 8 8 6
Lobectomy
to 150 gm of glucose is administered intravenously daily for seventy-two hours since 10 per cent glucose is necessary to compensate for the immediate decrease in blood sugar. To combat profound hypoproteinemia, 25 to 50 gm of protein (parenteral albumin or plasma) are given daily for seven to ten days. Oral alimentation, with a high protein, high carbohydrate diet, should begin as soon as possible. Wide spectrum antibiotics are prophylactically given for five to seven days. We have not used steroids postoperatively, although steroids will accelerate the rapidity of regenerative hyperplasia of the liver. Results
Results of hepatic lobectomies have varied with the time, technic, and indication. Obviously, results today should be better than they were previously because of improvement in ancillary technics, such as the advances in anesthesia, the continuous monitoring of specific physiologic functions, and the improved procurement, processing, and administration of blood. In general, technical advances are simultaneous but a certain era is often considered the particular moment in time when technical advancements in a specific operation were made. The period covered in this study has definitely shown the greatest technical improvement in hepatic surgery. The accurate description of the true anatomy of the liver has enabled the surgeon to perform hepatic lobectomy by dissection of the lobar structures. Modern vascular surgery has taught technics that facilitate control of hemorrhage. Operative results depend upon the condition of the patient at the time of operation and the acuteness of the situation. The elderly hypotensive patient in need of a rapid lobectomy as’ the result of massive injury is undoubtedly a higher risk than a young patient with a space-occupying lesion which has yet to manifest symptoms. On the other hand, late results will undoubtedly be worse in patients undergoing lobectomy for malignant lesions, and particularly worse for those with metastatic lesions in contract to primary lesions. There was one operative death in this series, which occurred in 1950 from exsanguination resulting from laceration of the left hepatic vein during a left lobectomy for intrahepatic biliary obstruction. Ten of the twenty patients (50 per cent) can be considered long-term survivors. (Table IV.) Of the six patients with liver cell carcinoma, three died at six months, eight months, and eleven months respectively. Three are long-term survivors. One patient who survived twenty-one years recently died from myocardial insufficiency. At 279
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autopsy no recurrent tumor was found. Two other patients with primary liver cell carcinoma are now alive and well more than four years postoperatively. One of them recently underwent abdominal exploration for intestinal obstruction secondary to adhesions. At operation no residual or recurrent tumor was noted. This patient is particularly interesting, for it is believed that this represents a case of irradiation-induced liver cell carcinoma. During childhood this patient received 2,550 r to a large hemangioma located in the hilum of the liver because it was considered unresectable by the surgeon. Twenty years later a huge mass developed in the right lobe of the liver. At operation the hemangioma was completely obliterated by the previous x-ray therapy, but a massive multicentric liver cell carcinoma involved the right lobe of the liver. An extended right hepatic lobectomy was performed. The one patient with bile duct carcinoma survived thirty-two months, although recurrent disease was suspected fourteen months after operation. Two of the three children with embryonal carcinoma are alive and well six and eight years, respectively, after right hepatic lobectomy. The third child underwent an emergency right hepatic lobectomy after rupture of the tumor and survived only three months. The results of surgical treatment of primary carcinoma of the liver are not as dismal as previously thought. Of ten such patients with these neoplasms in this study, five (50 per cent) are considered to be long-term survivors or cures. This cure rate ranks high when compared to that of patients with malignant tumors of other major organs. Results of hepatic resection for metastatic lesions have varied, as has the extent of resection, from a small wedge resection for a solitary small peripheral metastasis to a lobectomy for extensive deep-seated metastasis. Many beneficial limited resections have been reported for metastatic disease, performed either at the time of resection of the primary tumor or many years later. No matter how infrequent the cure, limited hepatic resection and possibly left lateral segmentectomy for metastatic disease appear warranted in view of their relative safety. In contrast, when size and location of metastasis necessitate a hepatic lobectomy for eradication, the cure rate has been negligible and operative mortality high. Review of the literature reveals only two five year survivors of total hepatic lobectomy for embolic metastatic lesions [ 53,541. Our experience and that of others [55] with lobectomy in the treatment of metastatic disease support the inefficiency of such therapy. There were four patients in whom lobectomies were performed 280
for metastatic carcinoma. In an eighty-eight year old woman, an emergency right hepatic lobectomy was performed for rupture of a metastatic leiomyosarcoma with survival for only six months. Two patients underwent hepatic lobectomy for a solitary metastatic lesion from a carcinoma of the colon. Although one died in the early postoperative period, another survived for twenty months. One patient had a left lobectomy for a direct extension from a carcinoma of the stomach and this patient survived only one year. The combination of low curability and increased operative mortality suggests to us that if embolic metastasis is so extensive or in a location requiring hepatic lobectomy, the procedure is unwarranted. An exception to the natural response of embolic liver metastasis is that of functioning tumors. Immediate relief of the debilitating symptoms of a carcinoid syndrome has been reported by resection of massive hepatic metastasis of carcinoid tumors. Even when excision is incomplete, the levels of 5-hydroxyindole-acetic acid in the urine become negative in the immediate postoperative period and remain so for periods up to three years [56,57].
There was only one patient who underwent hepatic lobectomy for a benign tumor. This was a huge symptomatic hemangioma of the left lobe. The patient is alive and well thirteen years after operation. All four patients survived in whom hepatic lobectomy was necessary to control hemorrhage and/or to remove devitalized tissue as the result of trauma. Two of these operations were performed eight years ago, and although two had surgery relatively recently, they are apparently well and will probably be long-term survivors. Summary
Hepatic lobectomy was performed on twenty patients at the Ochsner Clinic over a twenty-two year period. The most common indication for operation in this series was primary malignant neoplasm. However, in recent years, due to the increase in automobile accidents, blunt trauma has become the most common indication for hepatic lobectomy. The operations performed in accordance to the segmental anatomy were ten right lobectomies, two extended right lobectomies, four left lobectomies, four left lateral segmentectomies. The surgeon should have a thorough knowledge of the anatomy of the liver and should be wellversed in the many methods to control hemorrhage. Proper preparation, precautions, and technical maneuvers establish hepatic lobectomy as a safe and effective operation. The
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There was one operative death (5 per cent). Five of the ten patients (50 per cent) who had lobectomy for primary malignant neoplasms are long-term survivors. In contrast, none of the four patients who had a hepatic lobectomy for metastatic disease were long-term survivors. All patients who had hepatic lobectomies for benign conditions are living. Of the total twenty patients in this series, ten (50 per cent) are considered to be long-term survivors.
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