Partial or total resection of the biliary tract — Surgical strategies for hilar cholangiocarcinoma

Acta Chir. Aus t r iaca - Heft 4 • 1998 211

From the Department of Surgery, the *Department of Internal Medicine, Gastroenteroiogy/Hepatology, and the **Department of Radiodiagnostics, Virchow Clinic, Humboldt University, Berlin, Germany

Partial or Total Resection of the Biliary Tract - Surgical Strategies for Hilar Cholangiocarcinoma S. Jonas, W. O. Bechstein, H. Keck, W. Veltzke*, R. Hintze*, T. Vogl**, and P. Neuhaus

Key-words: Biliary tract, partial or total resection - cholangiocarcinoma - surgical strategies.

SchliisselwOrter: Gallenwege, partielle oder totale Resektion - Gal- lengangska~inom - chirurgische Behandlungsstrategien.

Summary: Background: Surgical resection provides the only chance of cure for patients suffering from hilar cholangiocarcinoma. Although appropriate procedures are not agreed upon, an increase in radicality has been observed during the past 20 years. Methods: The literature as well as our own experience after 80 resections of hilar cholangiocarcinomas were reviewed retro- spectively. Results: Tumor-free margins represent the most important prognostic parameter. Hilar resections as least radical resective procedure will generate rates of formally curative resections of less than 50%. Curative resection and 5-year survival rates after additional hemihepatectomy generally do not exceed 65% and 25% in the more promising reports, respectively, in our series, the best 5-year survival rate was achieved after right trisegmentectomy with 59%. After conventional liver transplantation, 5-year survivors can only exceptionally be observed. Although extended bile duct resection or abdominal organ cluster transplantation may significantly increase the rate of formally curative resections, long term survival is still disappointing. Conclusions: In our hands, right trisegmentectomy will provide the most pronounced benefit, if this procedure is applicable with respect to tumor extension and functioning hepatic reserve. Extended bile duct resections cannot be evaluated definitely at this stage. However, patterns of recurrence clearly demonstrate the need for adjuvant treatment protocols.

(Acta Chir. Austriaca 1998;30:211-214

PartieUe oder totale Resektion tier Gallenwege - ch i rur - gische Behandlungss t ra tegien beim zent ra len Gallen- gangskarz inom Zusammenfassung: Grundlagen: Resektionen stellen die einzi- gen potentiell kurativen Therapieoptionen beim zentralen Gal- lengangskarzinom dar. In den vergangenen 20 Jahren konnte eine Zunahme der Radikalitfit in der chirurgischen Therapie beobachtet werden, ohne dag einheitliche Therapiekonzepte bestfinden.

Methodik: Retrospektive Untersuchung der Literatur sowie unserer eigenen Erfahmng nach 80 Resektionen zentraler Gailen- gangskarzinome.

Ergebnisse: Formal kurative Resektabilit~,t stellt den wichtig- s~en Prognosefaktor dar. Hilusresektionen als Verfahre~ mit der geringsten Radikatit~it sind in weniger als 50% der F~ille formai kurativ. Die Raten formal kurativer Resektionen sowie des 5-Jah- res-Uberlebens nach zustitzlicher Hemihepatektomie tibersteigen auch in giinstigeren Serien in der Reget 65% bzw. 25% nicht. Im eigenen Krankengut wurde mit 59% die h/3chste 5-Jahres-15ber- lebensrate nach rechtsseitiger Trisegmentektomie beobachtet. Nach konventioneller Lebertransplantation kommt es nur in Aus-

Corresponding address: S. Jonas, M.D., Department of Surgery, Virchow Clinic, Humboldt University, Augustenburger Platz 1, D-13353 Berlin, Germany. Fax: ++49/30/450- 52900 E-mail: [email protected]

nahmef~illen zu einem Langzeittiberleben. Erweiterte Gallen- gangsresektionen sowie auch abdominelle ,,Cluster-Transplanta- tionen" ktinnen zwar die Rate formal kurativer Resektionen si- gnifikant steigern, fiJhren aber nicht zu einer h6heren 5-Jahres- Uberlebensrate.

Schlul3folgerungen-- Nach unserer Erfahrung krnnen die gtin- stigsten Ergebnisse nach Trisegmentektomien beobachtet werden, wenn Tumorausmat3 oder Parenchyrnreserve diese Verfah- renswahl zulassen. Erweiterte Gallengangsresektionen krnnen derzeit nicht abschliel3end beurteilt werden. Das Rezidivmuster verdeutlicht die Notwendigkeit adjuvanter Therapieans~itze.

In t roduct ion

Surgical strategies in the therapy of hilar cholangiocarcinoma afford patients the best chance for significant survival. Radi- cal resections are currently considered as optimal treatment. but less than 20% of patients are estimated to be amenable to a formally curative approach (9, 11). Although these tumors usually have a low propensity for metastases and tend to grow slowly, curative attempts are impaired by a longitudinally and laterally advanced local infiltration, as the diagnosis is generally not made until a patient is jaundiced (7, 39). The deter- gent properties of bile facilitate its passage through tiny gaps in an obstructed lumen long before it becomes clinically apparent (31).

The type of growth provides another condition for technically difficult or even impossible resections in the vicinity of vital hilar structures. The nodular type with a well demarcated tumor is rarely found in cholangiocarcinoma and a fibrous capsule, which can frequently be detected in hepatocellular carcinoma, is almost always absent. Conversely, the periductal type, with infiltration and proliferation along thickened bile duct walls with minimal mass formation, is exclusively observed in the hilar type of cholangiocarcinoma (13, 38). The resection rate of this subset of tumors approximates only 10%. Apart from a local spread via lymphatic vessels, microscopic tumor extension can inde- pendently be observed through perineural spaces, predomi- nantly in hepatofugal direction due to the intrahepatic narro- wing of the perineurium (6, 41). Thereby, the already difficult diagnosis of hilar cholangiocarcinoma including its differentiation from benign fibrosing diseases at the hepatic confluence, especially primary sclerosing cholangitis, primary biliary cirrhosis and Caroli's disease, is further complicated by an even intraoperatively hardly definable tumor extension, which may easily reach beyond its palpable confines. Moreover, hi- stologic carcinomatous invasion of surrounding vessels may occur, but is less common and macroscopically indistinguishable from adherence and perivascv.ia- fibrosis (2).

Fig. l. Modified Bismuth-Corlette classification ofhilar cholangiocarcinoma according to the tumor extension at the bifurcation of the biliam., tree.

212 Acta Chir. Austriaca. Heft 4 . 1998

Table 1. Pattern of cholangiocarcinoma recurrence after formally curative hilar resections (according to [25]).

Site of recurrence Overall frequency of recurrence

Liver 62%

'Tumor bed 42%

Regional lymph nodes

Peritoneum

Lungs

Bone

Subcutaneous tissue

20%

16%

71%

31%

7%

Frequency of primary recurrence

76%

24%

Loca l r e s e c t i o n

The type of resection that may be indicated for hilar cholangiocarcinoma depends on the site and extent of the tumor. The loca- tion of a carcinoma within the biliary tree and its relation to the hepatic confluence is practically standardized in the modified Bismuth-Corlette classification (Fig. 1).

Local or hilar resections including the extrahepatic, suprapan- creatic biliary tract represent the least extended resective procedures and have been shown to be safe, the operative mortality rate being even less than 1% in selected series (4). Theoretically, patients suffering from Bismuth-Corlette type I or type II tumors could undergo hilar resections in a curative intent. However, the pattern of failure after formally curative extrahepatic bile duct resections demonstrated a high percentage of patients (76%) with locoregional recurrence (25). Distant metastases developed in most patients exhibiting a locoregional recurrence but were the site of first failure in only 24% (Table 1). The liver was identified as the most frequent site of recurrence, either by direct parenchy- real invasion or along the segmental duct draining the caudate lobe (segment 1) (26). A 97% rate of segment 1 ramifications at the hepatic confluence or within a distance of less than 10 mm into the main left or right hepatic duct is likely to result in an early tumor involvement and led to the postulate to generally in- clude caudate lobe resections into the surgical strategy, if cure is intended (5, 20, 27).

Patient longevity after hilar resection remains poor and single- center experiences achieving 5-year-survival rates of 30% have to be considered as favorable (12, 32). Moreover, it could not be demonstrated that an additional caudate lobe resection had a be- neficial impact on survival (26, 32). Prime targets of tumor recurrence were still locoregional within the former tumor bed, liver parenchyma and pancreatic lymph nodes.

L i v e r r e s e c t i o n

Resections are considered curative if tumor-free margins are ob- tained on pathologic examination of a resected specimen. The true extent of a periductular infltrating carcinomatous lesion cannot be recognized by the surgeon and even pathologic deter- mination of intraoperative frozen-section biopsies may be difficult, especially in the setting of concomitant cholangitis, hepato- lithiasis or biliary obstruction. Retrospective analyses of speci- mens from hilar resections showed tumor-free margins in less than 50% of the patients, concluding an increased risk of residual cancer after hilar resections when compared to additional liver resection (2). Therefore, adequate clearance and the chance of long-term survival may only be preserved after hepatic resections (5, 20, 33, 42).

Hilar cholangiocarcinomas involving either the right or left hepatic duct (Bismuth-Corlette types IIIa/IIIb) are generally propo- sed to require resection of the respective hemiliver in order to achieve cleared margins. Recent studies on prognostic parame- ters after resection identified only tumor-free margins as a common predictor of postoperative survival in multivariate analyses, while histopathologic differentiation and tumor-stage showed a clear correlation only in single studies (32, 37). The improved equipment and understanding of techniques requisite for liver surgery allow performance of extended resections without major concessions to perioperative safety. In a French multicentric survey of 278 patients suffering from hilar cholangiocarcinoma, perioperative mortality was highest after surgical exploration (58%) or palliative decompression by transtumoral intubation (27%) and biliary digestive anastomosis (26%) (35). The mortality rates after resective surgery were significantly lower with 17% after local resections and 14% after hepatectomies, which in part may have been due to the fact that many of the participating institutions treated only few patients while the majority of hepatectomies was performed in centers. In addition, these results also re- vealed a selection of patients with more favorable tumor stages for major surgery. In our experience, hepatic resections of hilar cholangiocarcinoma had a postoperative mortality of 10% which is reflected in other recently reported series of experienced centers (22, 32, 37).

Combined tumor and hepatic resections could increase not only the rate of curative resections which in our experience of 80 resected hilar cholangio¢arcinomas rose from 44% after hilar resections to 65% after additional hepatic resections but also the

Fig. 3. CT scan 1 month after decompression of the left hepatic duct and embolization of the right hepatic arte~ showing atrophy of the right and hypertrophy of the left hemiliver. The radiologic density of the right segments has decreased following arterial embolization.

Fig. 2. Endoscopic retrograde cholangiography showing dilation of the left biliar 3' system in a patient suffering from hilar cholangiocarcinoma (~,pe llla according to the modified Bismuth-Corlette classification). Prior to right trisegmentectomy, left hepatic hypertrophy and right hepatic atrophy are induced b.v decompression of the left hepatic duct via transhtmoral stenting and embolization of the right hepatic arte~, by angiographically inserted platinum coils (arrows). The long distance between obstracted confluence and ramification of the left lateral segments is obvious, allowing for a wide rumor-free resection margin.

Acta Chir. Aust r iaca • Heft 4 • 1998 213

total number of patients amenable to surgery. Over the long term, these surgical approaches could not be associated with favorable survival figures, although a number of survivors are reported in many series. 5-year survival rates range from 40% in the most optimistic reports to 10% in other accounts (22, 29, 30, 32, 37, 43).

In our series, the most favorable outcome was observed among the subset of patients undergoing right trisegmentectomy. The rate of formally curative resections in this group was 75% (9 of 12 patients) with a 5-year survival rate of 59%. Although only 1 tumor in this group presented with a poor histopathological differentiation, anatomical considerations may as well account for this superior figure. With respect to the hepatic hilum, a more distant segmental ramification of the left hepatic duct which va- ries in size from 1 to 5 cm is likely to allow more radical right- sided than left-sided resections. Conversely, the anterior and po- sterior right ducts, which are formed by the segmental ducts 5/8 and 6/7, respectively, combine at a confluence constituting the right hepatic duct which rarely exceeds a length of 1 cm (10). In addition, the common bile duct is located on the right side of the hepatoduodenal ligament with the right hepatic artery behind its proximal portion. In order to comply with the basic principle of surgical oncology to achieve wide tumor-free margins, it may be appropriate to perform right trisegmentectomies even for some hilar cholangiocarcinomas infiltrating the left hepatic duct.

The main obstacle to this approach is frequently represented by the preoperative anticipation of a limited functioning hepatic remnant due to the small size of the left lateral segments in some patients or to an insufficient postoperative compensatory enlar- gement due to cholestasis-associated liver damage. A preoperative hypertrophy of the future remnant liver, induced by unilateral portal vein embolization, has been shown to minimize the associated risk of postoperative liver failure (24). Decompression of the biliary system may also be indicated to improve hepatocellular function. Former randomized trials did not demonstrate an advantage associated with preoperative external biliary drainage (17). However, older studies mainly comprised bypass surgery and suffer from a low share of hepatectomies. We use a modified approach with internal stent decompression of the remnant left lobe and arterial platinum-coil embolization of the fight liver artery (Fig. 2). In our experience, insidious arterial embolization by coiling is comparable to portal embolization with respect to safety and extent of contralaterally induced hypertrophy (Fig. 3). Moreover, the deleterious effects of a decreased arterial supply to bile ducts are well-known from ischemic type biliary lesions (ITBL) after liver transplantation and may be more appropriate as an antitumoral concept than portal embolization.

Total hepatectomy Unresectable tumors and functional restrictions, but also the as- sumption that greater exstirpative procedures might provide an increased chance for cure, resulted in the more radical concept of resecting the entire intrahepatic biliary tree by combining hilar resection, total hepatectomy and liver transplantation. Arguments in favor of this approach included a putative rise in rates of formally curative resections, the simultaneous therapy of underlying or associated diseases, e.g. primary sclerosing cholangitis, as well as the prevention of de novo and recurrent tumors, since multifocal lesions within the biliary tract may be identified in as many as 10% of patients (16). Moreover, tumor stage and poly- centricity are likely to be assessed with higher reliability by histopathological staging after total hepatectomy when compared to radiological visualization of the hepatic remnant after partial resections.

Postoperative mortality was even expected to decrease as liver transplants in a patient population not suffering from complica- ting portal hypertension can be performed rather straighttbrward. However, postoperative and long term survival figures have been disappointing. In a review of 56 patients originating from 13 studies, 90-day mortality and 5-year survival rates after total hepatectomy and liver transplantation for hilar cholangiocarcinoma

were approximately 25% and 5%, respectively (14). Cancer recurrence predominated as cause of death in 85% of the patients surviving more than 90 days posttransplant. Many of these patients underwent operation in the 1980s, when the initial surgical endeavour was made to establish liver transplantation as a wide- spread treatment option for liver diseases in general. Therefore, postoperative mortality rates are likely to be cut at least in half some ten years later. However, the major obstacle to patient longevity remains the unpredictable risk caused by a potentially accelerated growth of residual tumor cells during chronic immuno- suppression, which has been shown after hepatectomy and liver transplantation for hepatocellular carcinoma (44).

Another lesson learned from liver transplantation for hepatocellular carcinoma in cirrhosis is that the formerly adopted attitu- de to resect when resection is feasible and perform transplantation for those tumors being unresectable represented a complete misconception. If successful outcome is observed posttransplant, it will be in patients suffering from resectable lesions, whereas total hepatectomy and liver transplantation will not confer a survival benefit to those suffering from otherwise unresectable hepatocellular carcinomas (8, 21). At least, the latter principle may hold true for hilar cholangiocarcinoma as well, while a poor pro- gnosis is not an exception but the rule in the small subset of patients in whom diagnosis of a hilar cholangiocarcinoma is made at an early stage or incidentally (15, 32). Therefore, most transplant centers have abandoned the policy to consider hilar cholangiocarcinomas as an indication for liver transplantation.

To t a l r esec t ion of the b i l i a ry t r a c t 3 mechanisms are likely to serve as an explanation for long term failure after total hepatectomy and liver transplantation for hilar cholangiocarcinoma: unrecognized distant metastases, intra- or preoperative tumor cell seeding, e.g. via biopsy needle tracts, and peripancreatic tumor extensions in lymphatic vessels or perineural sheathes along the distal residual bile duct.

Nodal infiltration may occur in as many as one-third of patients whereas blood born metastases are distinctly unusual (23, 40). Indeed, careful follow-up frequently disclosed postoperative failure of tumor control with recurrence at the pancreatic head and local peritoneal carcinosis (3). Therefore, it may be doubted that distal radicality can be achieved by partial bile duct resections, all the more considering tumor-free margins of less than 10 mm, which are not uncommon in oncological biliary surgery, as insufficient for all other gastrointestinal cancers. Similarly, intraabdo- minal tumor seeding probably confronts the surgeon with an even more important problem, as it is common practice in some centers to establish tumor diagnosis by open biopsies. Dissection of tumor or peritumor is considered obsolete for other carcinomas. In rectal cancer for example, not only perforation of the tumor but even dissection of the mesorectum, which is considered a "holy plane", has been identified as main reason for local recurrence (18, 19). The "holy plane" in oncological surgery of the extrahepatic biliary tract may be represented by the hepatoduodenal ligament which is regularly dissected during preparation of the hepatic artery and portal vein for conventional liver transplantation.

In order to comply with these roles of oncological surgery, we have described the "extended bile duct resection", i.e. en bloc eradication of the entire biliary ~ee by a no-touch technique combining total hepatectomy, partial pancreatoduodenectomy, extended lymphadenectomy and liver transplantation (28). Moreover, an attempt was made to select patients suffering from less advanced tumors, because it is known from other cancers that there is limited chance of cure at an advanced stage even if the surgical technique is excellent.

In spite of an attempted selection, only 4 of 14 patients presented with UICC I/II tumors (UICC IVa: n -- 9; UICC IVb: n = 1). After 14 extended bile duct resections, formally curative resections were achieved in all but 1 patient, in whom a metastasis at the right ovary was not apparent until the procedure had already reached an irreversible stage. During the postoperative course, 2

214 Acta Chir. Austriaca. Heft 4 -1998

patients (14%) were lost due to complications associated with the pancreatic tail. After a change in the protocol to administer oc- treotide routinely, we did not observe any more severe complications. Currently, the 4-year survival rate including the postoperative mortality is 30%. An analysis of the late failures disclosed implantation metastases in about half of the patients with tumor recurrence. The pathway is not fully apparent, though an exfolia- tion of tumor cells into the bile running freely into the operative field via gastric or jejunal succus, is likely to be operative.

Comparably disappointing results are reported after abdominal organ cluster transplantation performed by Starzl et al. in Pitts- burgh (1, 36). This procedure was designed to resect the whole complexity of visceral organs deriving during embryonal life from the portion of the foregut which later in life differentiates into duodenum, liver and pancreas. In the subset of patients suffering from cholangiocarcinoma, postoperative mortality and 5- year survival rates were 20% and 14%, respectively. Most of these patients underwent additional transplantation of the pancreas and all postoperative fatalities could be related to the pancreatic graft. Transplantation of the liver alone was advocated for some patients despite creating a hardly adjustable diabetes mellitus, in order to avoid the considerable morbidity and mortality associated with the pancreas graft.

Conc lus ions Even highly extended resective procedures do not achieve the expected survival benefit in the treatment of hilar cholangiocarcinoma, although the observed advantage after formally curative resections can be confered to a significantly increased share of patients. The pathways of recurrence are not fully investigated, but clearly demonstrate the need for adjuvant treatment protocols. So far, chemotherapy and radiation have failed to contribute to improved survival figures (34).

In our hands, right trisegmentectomy will provide the most pronounced benefit, if this procedure is applicable with respect to tumor extension and functioning hepatic reserve. Extended bile duct resections cannot be evaluated definitely at this stage and must be applied with considerable caution regarding tumor seeding. As most issues concerning an optimal treatment of hilar cholangiocarcinoma remain unsolved, it should be emphasized that the evaluation of these patients has to be concentrated in spe- cialized institutions.

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Partial or total resection of the biliary tract — Surgical strategies for hilar cholangiocarcinoma