4 C -January 1990 Volume 2 1 1, Number 1 <2; "i i. Is of i 5 S What's New Surgery In General Surgery a Hepatic Resection SEYMOUR I. SCHWARTZ.M.D.

The current performance and applicability of elective hepatic From the Department of Surgery, University of Rochester resection represents an impressive evolution. From removal of School of Medicine and Gentistry, Rochester, New York tumor-bearing, ill-defined portions of the liver, which is always threatened by the inability to control bleeding, surgery of the liver has progressed to hrnostzitically controlled dissection of anatomically defined portions of the organ. Accompanying the series of technical refinements that have markedly reducea the' mortality and morbidity rates associated with the procedure, there

has been an expansion of the indications for hepatic resection. hEPATIC RESECTION CaN be traced through three distinct periods based on perception of the anatomy of the liver. In the first period, portions of the liver were removed without regard for intrahepatic planes, and it was taught that the liver was divided solely along the line of the falciforme ligament. The second period stemmet from revised appreciation of the anatomy of the liver. In 1898 Cantlie used casts to demonstrate that the main lobar fissure extended from approximately the bed of the gallbladder anteroinferiorly to the right side of the inferior vena cava posterosuperiorly. This work was extended by Hjortsjo and by Healey and Schroy, who demonstrated that the right lobe was divided into an anterior and posterior segment and that the left lobe was divided into a medial and lateral segment by the line of the falciform ligament. The understanding of this anatomy led to development of surgical planes of the liver and to anatomic resection along these intersegmental planes. More recently Couinaud refined the anatomic concept and demonstrated that the two lobes of the liver actually were hemilivers that consisted of eight segments. each of which, theoretically, could be resected. The first elective removal of a liver lesion was reported

in 1886 by Luis ,who removed an adenoma: in this case the patient died. The first successful elective hepatic resection is credited to Langenbuch who, in 1888, excised a portion of the left lobe of the liver. That patient required re-exploration for internal hemorrhage a few hours after the operation and the patient survived.Tiffany,in 1890, was the first American surgeon to report a case of hepatic resection for tumor, and the following year Lucke reported the first successful removal of a malignancy from the left lobe of the liver. In 1892 Keen reported the excision of a cystic adenoma of the bile ducts within the liver using a technique of ligature through the base of the tumor, cautery, and stripping the liver from the tumor with a thumbnail. This article included the first collective review in which 20 cases were extracted from the liver. In 1899 the same author performed the first successful left lobectomy for cancer of the liver, a procedure we would today ten left lateral segmentectomy. In this operation five vessels were ligated individually with catgut and cautery was applied to the raw surface. Wende reported the first case of near-total right lobectomy for primary tumor in 1911. The major problem confronting the surgeon during hepatic resection, both in the past and today, has been hemorrhage control. In 1896, during the early historical period.

Kousnetzoff and pensky devised the use of blunt needles and the application of ligatures to isolated blood vessels when the parenchyma was transected. One year later Auvray described a series of mattress sutures that resembled those suggested by Kousnetzoff and Pensky, and first he applied the technique to humans. Ten years later in the United States, Hough described using a series of mattress sutures with a crossover to permit approximation of the Glisson's capsule to effect tamponade. The next approach to managing bleeding from the hepatic parenchyma was that of temporary inflow occulsion, which is still called the Pringle maneuver. In 1908 J. Hogarth Pringle, a Scottish surgeon, published an article in the Annals of surgerv on the arrest of hepatic hemorrhage due to trauma. He reported on eight patients with hepatic trauma, only four of whom had undergone operation. Two of these patients died on the operating room table, and the remaining two patients died shortly thereafter. It is interesting that, given this data, the technique was ever adopted. Unquestionably the adoption of the technique was based on Pringle's experiments on rabbits, which demonstrated that inflow occlusion could effectively reduce bleeding from the transected hepatic parenchyma. In 1940 Cattell reported the successful removal of a liver metastases from a primary lesion in the colon. In

1943 Wangensteen reported coincidental partial hepatectomy for gastric carcinoma involving the liver by direct extension. In 1948 Raven reported a left lateral segmentectomy for metastatic colon cancer in which the triangular and coronary ligaments were transected and the left hepatic artery, left portal vein, and the left bile duct were ligated within the hepatoduodenal ligament. The left hepatic vein was isolated extrahepatically, after which the parenchyma was transected. The modern era of hepatic resection dates from the 1952 report of Lortat-Jacob and Robert in which the blood vessels and bile duct to the right lobe were ligated within the hepatoduodenal ligament and the right hepatic vein was ligated extrahepatically before transection of the hepatic parenchyma. In 1953 Quattlebaum reported three cases of major hepatic resection, one of which was the first recorded right lobectomy for primary hepatocellular carcinoma. Also in 1953 Mersheimer published a similar experience. A significant technical contribution, the so-called finger fracture has inappropriate been ascribed to Oriental surgeons . In 1903 Anschutz demonstrated that when the liver parenchyma was disrupted digitally, only the intrahepatic portal pedicles and hepatic veins resisted. In his 1953 publication. Quattlebaum described performing liver dissection with the handle ofthe scalpel and indicated that this permitted exposure of the intrahepatic vessels. In 1956 Fineberg et aL,reported dividing the parenchyma

by means of his finger during a right lobectomy. The technique was popularized by Lin, who applied it successfully to a large series of patients. The procedure was finally refined by Ton That Tung,w ho combined in flow occlusion of the vessels and ducts within the hepatoduodenal ligament with "finger fracture" of the parenchyma. Couinaud emphasized that "finger fracture (digitoclasia) should be a gentle technique and must be respectful of anatomy." Indications for Elective Hepatic Resection Resection of segments or a lobe of the liver may be indicated for a nonparasitic cyst, for localized granulomatous processes, and for diffuse multiple abscesses confined to a resectable area (Fig. I). The most common benign primary lesion that may require resection for pain or a mass is a hemangioma2' (Fig. 2). Hepatic-cell adenomas should usually be resected because of their potential to bleed either intraparenchymally (Fig. 3) or intraperitoneally, and the potential for malignant transformati on . Mesenchymal hamartoma is a rare, resectable tumor. Primary hepatic malignancies that may be resected with the potential for cure are hepatocellular carcinoma, including follicular carcinoma, and hepatoblastoma. Some tumors that have metastasized to the liver are resected because of the potential for cure. Resection for metastases

from the colon or rectum is associated with a 25% -year survival rate. Resection for hepatic metastases from Wilms' tumor has a survival rate of more than 50%. Occasional long-term survivals have been reported after hepatic resection for metastases from gastric, renal, and ovarian carcinomas and from occular melanomas. Significant palliation has been effected by a debulking resection of symptomatic carcinoids. Advanced cirrhosis generally precludes a major hepatic resection. Intraoperative bleeding is increased; the incidence of postoperative liver failure is also increased because of lack of functional reserve. Hepatic regeneration is markedly impaired and reported cures for malignant tumors are rare in cirrhotic patients. Anatomic Basis for Hepatic Resection The liver is divided into two lobes, or hemilivers, by the main portal fissure or scissura (Cantlie's line). This line extends from the anteroinferior gallbladder fossa posterosuperiorly to the left side of the inferior vena cava. The organization of the right and left lobes or hemilivers is similar. On either side of the main portal fissure there is a right or left paramedian sector. Lateral to each of these is a variable fissure lateral to which is a right or left lateral sector. The left lobe consists of the hepatic tissue to the left of the falciform ligament plus the quadrate and caudate lobes, as they were called in the previous nomenclature. The right portal fissure divides the right lobe into an

anteromedial and posterolateral sector. The right hepatic vein courses along this fissure. The left portal fissure, in which the left hepatic vein courses, divides the left lobe into an anterior and posterior sector. The liver is further divided into eight segments, which are the smallest anatomic units. In the right and left lobes, each of the two sectors is divided into two segments; the anteromedial sector is divided into segment V anteriorly and segment VIII posteriorly. The posterolateral sector is divided into segment VI anteriorly and segment VII posteriorly. In the left lobe, the anterior sector is divided by the umbilical fissure into segment IV, the anterior part of the quadrate lobe, and segment 111, which is the anterior part of the left lobe. The posterior sector is comprised only of segment 11. The Spigelian lobe, or segment I, is an autonomous segment, with vascularization independent of portal division and the hepatic veins. As a consequence of these anatomic divisions, a nomenclature for hepatic resection has been established. Two classifications, that of Couinaud and the more commonly applied nomenclature of Goldsmith and Woodburne, are used for the four major resections (Table I; Fig. 4). Unisegmentectomy is not applicable for segment I because access to this segment requires preliminary removal of segments II and III. There is little advantage to removing

either segment I or III independently because they can be removed together easily as a left lateral segmentectomy. Segmentectomy IV usual refers to excision of the anterior part of that segment. Resection of segment VI alone is rarely performed. Segment VIII resection is difficult because it is connected with the intrahepatic vena cava and segment I. Plurisegmentectomy VI and VII may be called right lateralsectorectomy. Bisegmentectomy IV and V is used for patients with carcinoma of the gallbladder extending into the liver or for Klatskin tumor. Segments IV, V, and VI may be removed as a unit. TABLE I. Comparisotz of Classi/lcntion of Hepatic Resection: Goldsmith and WoodburneVersusCouinaz~d Goldsmith and Woodburne Right hepatic lobectomy Extended right lobectomy (trisegrnentectomy) Left hepatic lobectomy Left lateral segrnentectomy Couinaud Right hepatectomy (segments V, VII, VII, VIII) Right lobectomy (segments IV, V, VI, VII, VIII, & I) Left hepatectomy (segments II, III, IV)

Left lobectomy (segments II, III) Operative Techniques Resection of a major anatomic portion (Fig. 5) of the liver incorporates several basic features: mobilization, temporary or permanent occlusion of the inflow vessels, transection of the hepatic parenchyma, ligation of intrahepatic vessels and ducts, 'control of the hepatic veins, and hemostasis of the remaining raw surface. Mobilization frees the lobe to be resected so it can be delivered into the wound. The ligamentum teres is transected and the falciform ligament is divided to a point adjacent to the inferior vena cava. The triangular ligament supporting the lobe to be excised is divided and the dissection is continued by transecting the anterior and posterior coronary ligaments until the suprahepatic vena cava is exposed (Fig. 6). There are two techniques for right or left lobectomy. The first incorporates individual ligation of the structures in the hepatoduodenal ligament supplying the lobe to be removed and ligation of the hepatic vein draining the lobe before transecting the parenchyma. The advantage of this approach is reductiorl of irltraoperative bleeding and demarkation of the devascularized portion to be removed. The disadvantages are the potential for injury to the inferior vena cava during dissection of the hepatic veins.

The second technique begins with anteroinferior transection of the parenchyma in the plane of lobar division. Before this temporary inflow occlusion can be affected by anatraumatic clamp or an occluding loop incorporating all structures within the hepatoduodenal ligament. Inflow vascular occlusion can be continued for up to 60 minutes without impairing liver function permanently. The portal elements are ligated and divided as they traverse the plane of dissection within the liver. Dissection is continued posterosuperiorly toward the inferior vena cava. The hepatic vein draining the lobe to be removed is isolated, ligated, and divided, or the vein is preferentially divided between clamps and oversewn within the parenchyma. This technique reduces operative time, removes an amount of liver tissue specifically related to tumor size and location, and avoids erroneous ligation of vessels providing inflow or outflow for the portion of liver to be preserved. The disadvantage of this approach is that intraoperative bleeding may be greater than with the other technique. I usually use this technique, endorsed by Bismuth, for lobectomy (Fig. 7);31 for resection of the right lobe? plus the medial sector of the left lobe (trisegmentectomy), the left hepatic artery and portal vein should be skeletonized to allow individual ligation and division of branches to the caudate lobe and feedback vessels to

the medical sector of the left lobe. Technical Refinements A variety of technical innovations has been applied to hepatic resection. These are generally directed at reducing the extent of bleeding associated with transection of the parenchyma. There are three categories of refinements: ( I ) improved compression of parenchyma to effect tamponade during dissection; (2) methods of dissection to skeletonizeintraparenchymal vessels and; (3) control of bleeding from the raw surface. In the category of parenchymal compression, several devices have been applied. The first modern report describing a clamp specifically designed for this purpose appeared in 1971. Storm and Longmire reported that their clamp provided uniform pressure on hepatic tissue, and that it significantly reduced the time required to perform a hepatic lobectomy. In his 1973 article, Lin reported that he had designed a special hepatic clamp that made hepatic transection without preliminary inflow or outflow occlusion "almost bloodless. More recently Goldwasser et al. described a new clamp for hepatic resection. The clamp is made of two parallel arms consisting of blunt cylindrical teeth. The crushing action provided by the teeth leaves the blood vessels and bile ducts that course along the line of resection exposed. Lee and effected compression with a plastic band and locking device (Insulok

TR/5OL) that was readily applied. It is especially appropriate when the lesion is peripheral. This is a simplification of the first instrument devised to control the hepatic parenchyma by direct compression.The ultimate modification provides permanent compression by a series of interlocking through-and-through sutures placed by means of teeth in a comblike device (Fig. 8). My inclination is not to incorporate any compressive instrument during hepatic resection and, if necessary, to have the first assistant apply pressure to the hepatic parenchyma parallel to the line of dissection. A variety of approaches has been introduced as a substitute for finger fracture of the parenchyma. In 1974 Almersjo and hafstrom de scribed a suction knife to facilitate parenchymal transection. In 1984 Hodgson and DelGuercio reported their experience with the ultrasonic dissector (CUSA'" system, Cavitron, Inc., Stanford, CT) j to disrupt liver parenchyma and isolate traversing vessels and ducts. The system provides fragmentation of tissue, irrigation, and aspiration of the fragments. The instrument should be set at 80% to 90% of full power during the dissection until larger vessels are approached, at which time the power should be reduced to 70%. The ultrasonic device is a dissector and provides no hemostasis in itself. A specially designed water jet has been used to fragment and wash away parenchymal tissue, leaving ducts and vessels to be ligated.40 The system is an inexpensive variation of ultrasonic dissection. Lasers combine dissection and hemostasis. The hemostatic

property is related to formation of a thin coagulum on the surface. In the case of the C02 laser, this is only 0.05 mm thick .The Nd-Yag laser offers a theoretic advantage, but one study showed that ultrasonic dissection was superior to the noncontact Nd-Yag laser method and finger fracture when measuring tissue damage.42 In contrast another group reported that the ultrasonic dissector and contact Nd-Yag laser were not significantly better than the suction knife in performing major resections when operating time, blood loss, and postoperative liver function were assessed. My preference is the finger fracture approach because I am familiar with that technique, and because it minimizes the time of parenchymal transection. I use the ultrasonic dissector on occasion for a trisegmentomy or for excision of a large central hemangioma with multiple contributing vessels. I have no experience with laser dissection of the liver. Diffuse oozing from the remaining raw surface of the transected liver can usually be controlled by temporarily applying direct pressure or a local hemostatic agent (such as oxydized cellulose or micronized collagen). Glues and adhesive sprays have been used but have been too intlammatory. A saphir infrared device has been used to produce hemostasis on the surface. Microwave application to the raw surface to induce a 2-to-3-mm deep coagulation is

being evaluated. In addition to the three categories that have been discussed, real-time operative ultrasonography has reduced operative bleeding. Although the procedure was introduced to define the extent and multiplicity of tumors, it provides a mapping of the major intrahepatic portal and hepatic venous vessels. This aids in guiding the line of transection and thereby reduces blood loss. As a consequence of better understanding the liver anatomy and the development ofeffective operative techniques, hepatic resection is now associated with acceptably low mortality and morbidity rates when it is performed by experienced surgeons. This has led to a broadening of indications for resection. Continued concern for intraoperative bleeding during parenchymal transection has stimulated refinements of technique and instrumentation, but the advantages ofthese refinements have not yet been documented. References 1. Cantlie J. On a new arrangement of the right and left lobes of the liver. Journal of Anatomy and Physiology 1898; 32:4. 2. Hjonsja C-H. The topography of the intrahepatic duct system.Acta Anat 1951; 11:599-615. 3. Healey JE Jr, Schroy PC. Anatomy of the biliary ducts within the human liver. Arch Surg 1953; 66599-6 16.

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Bile Ducts. Paris: C. Couinaud, 1981. 27. Schwartz SI, Husser W. Cavernous hemagioma of the liver. ~ nn Surg 1987; 205:456-465. 28. Gyorffy U, Bredfeldt JE, Black WC. Transformation ofhepatic cell adenoma to hepatocellular carcinoma due to oral contraceptive use. Ann Intern Med 1989; 110:489-490. 29. Goldsmith NA, Woddburne RT. The surgical anatomy pertaining to liver resection. SurgGynecolObstet 1957; 105:310-318. 30. Delva E, Camus Y, Nordlinger B, et al. Vascular occlusions of liver resections. Ann Surg 1989; 209:2 1 1-2 18. 31. Bismuth H, Houssin D, Castaing D. Major and minor segmentectomies "reglCes" in liver surgery. World J Surg 1982; 6:lO-24. 32. Storm FK, Longmire WP. A simplified clamp for hepatic resection. SurgGynecolObstet 197 1; 133: 103-104. 33. Lin F-Y. Results in 107 hepatic lobectomies with a preliminary report on the use of a clamp to reduce blood loss. Ann Surg 1973; 177: 413-421. 34. Goldwasser B, Bowers BA, Carson CC Ill, et al. A new clamp for hepatic resection. SurgGynecolObstet 1987; 164:379-380. 35. Lee KS, k m BR. The banding method as a simplified technique for resection of the liver. SurgGynecolObstet 1988; 167:77-78. 36. Doty DB, Kugler HW, Moseley RV. Surgical techiques. Control of the hepatic parenchyma by direct compression: a new instrument. Surgery 1970; 67:720-724. 37. Nagao T, Kawano N, Morioka Y. The surgeon at work. A new

instrument for hepatic resection. SurgGynecolObstet 1988; 166: 269-27 1. 38. Almersjo 0, Hafstrom L. The "suction knife". A new devise for dividing liver parenchyma. ActaChirScand 1974; 140:58 1-583. 39. Hodgson WJB, DelGuercio RM. Surgical technique. Preliminary experience in liver surgery using the ultrasonic scalpel. Surgery 1984; 95:230-234. 40. Persson BG, Jeppsson B, Tranberg KG, et al. Transection of the liver with a water jet. SurgGynecolObstet 1989; 168:267-268. 41. Fidler JP, Hoefer RW, Polanyi TG, et al. Laser surgery in exsanguinating liver injury. Ann Surg 1975; 181:74-80. 42. Transberg K-G, Rigotti P, Brackett KA, et al. Liver resection: a comparison using the Nd: YAG laser, ultrasonic aspirator, or blunt dissection. Am J Surg 1985; 151:368-372. 43. Schriider T, Hasselgren PO, Brackett K, et al. Techniques of liver resection. Arch Surg 1987; 122: 1 166-1 17 1. 44. Bismuth H, Castaing D, Garden OJ. The use of operative ultrasound in surgery of primary liver tumors. World J Surg 1987; 11:6 10614. 45. Makuuchi M, Hasegawa H, Yamazaki S, et al. The use ofoperative ultrasound as an aid to liver resection in patients with hepatocellular carcinoma. World J Surg 1987; 1 1 :6 15-62 1.