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10.1245/ASO.2004.03.011
Annals of Surgical Oncology 11:310-315 (2004)
© 2004 Society of Surgical Oncology
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ORIGINAL ARTICLES

Jaundice Predicts Advanced Disease and Early Mortality in Patients With Gallbladder Cancer

William G. Hawkins, MD, Ronald P. DeMatteo, MD, William R. Jarnagin, MD, Leah Ben-Porat, MS, Leslie H. Blumgart, MD and Yuman Fong, MD

From the Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Yuman Fong, MD, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021; Fax: 212-639-4031; E-mail: fongy{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: In patients with gallbladder cancer, jaundice suggests tumor involvement of the porta hepatis. This study reports on the prevalence, etiology, and clinical significance of jaundice in patients with gallbladder cancer.

Methods: Patients who presented with gallbladder cancer from 1995 to 2002 were entered into a prospective database. Disease-specific survival and clinicopathologic correlates were analyzed.

Results: Eighty-two (34%) of 240 patients with gallbladder cancer presented with jaundice. Jaundiced patients (96%) were more likely (P < .001) to have advanced-stage disease than nonjaundiced patients (60%). Only six (7%) jaundiced patients were resected with curative intent, and only four (5%) had negative surgical margins. This was significantly different from the nonjaundiced group, in which 62 patients (39%) had negative margins (P < .001). The median disease-specific survival in patients presenting with jaundice was 6 months and was significantly lower compared with 16 months in patients without jaundice (P < .0001). In the group presenting with jaundice, there were no disease-free survivors at 2 years, compared with 21% in the group without jaundice.

Conclusions: Jaundice is common (34%) in patients who present with gallbladder cancer and is an indicator of advanced malignancy. These data do not support routine operative exploration of patients with jaundice secondary to gallbladder cancer.

Key Words: Gallbladder • Cancer • Jaundice • Operative exploration


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Gallbladder cancer is an aggressive malignancy that has a propensity to disseminate early. Historically, the 5-year survival of gallbladder cancer is <5%.1 Until recently, cure was achieved only when an early tumor was found incidentally after cholecystectomy for presumed benign disease. Beginning in 1955 with George Pack and associates’2 description of right hepatectomy and portal lymph node dissection in three patients with gallbladder cancer, a trend toward more radical resection has evolved. Nevertheless, gallbladder cancer has remained a formidable problem. In the absence of effective adjuvant therapy, the only curative treatment remains a complete resection. In several series, 5-year survival among completely resected patients with T2 tumors was as high as 60% to 80%.3–5 Unfortunately, the survival benefit of wide surgical resection is available to only a small population of patients with localized disease. In several recent reviews, survival for the population of patients with gallbladder cancer remains low. Cubertafond et al.6 reported on the French Surgical Association Survey of 724 carcinomas of the gallbladder and described a median survival of 3 months, a 1-year survival of 14%, and a 5-year survival of 5%. A review of gallbladder cancer from Australia reported a 12% 5-year survival rate.7 Notably, all survivors in this study had stage I or II disease.

The major obstacle to cure in patients with gallbladder cancer is that most present with advanced and therefore unresectable disease. Experience has shown that gallbladder cancer is a rapidly growing tumor that disseminates early to multiple sites, including the regional lymph nodes, distant hepatic parenchyma, and peritoneal surfaces. In addition, the tumor arises close to the porta hepatis, mandating extensive liver resection in many patients for complete tumor clearance. The morbidity and mortality of such resections are significant, even in experienced centers. Reported complication rates after extensive hepatectomy for gallbladder cancer are as high as 54%,8 and mortality ranges from 0% to 21%.3,9,10

Identification of patients who will potentially benefit from aggressive surgical resection is important. Conversely, identification of subgroups that will not benefit from surgical resection is equally significant. Understanding the limits of current surgical options may save patients with aggressive tumors from significant morbidity related to a procedure that is unlikely to offer benefit. It allows for identification of a group of patients for experimental therapies and will save on unnecessary tests and hospitalization, thereby reducing costs. It allows patients and physicians the opportunity to focus on palliation and quality of life.

Jaundice is a common sign in patients with advanced gallbladder cancer and implies tumor involvement of the porta hepatis. Understanding the clinical significance of jaundice in patients with gallbladder cancer will help select patients more appropriately for potentially curative (surgical) and palliative (medical) treatments.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All patients with hepatobiliary malignancies seen at Memorial Sloan-Kettering Cancer Center (MSKCC) are entered into a prospective hepatobiliary database. The database was initiated in 1986. All clinical records—including inpatient and outpatients charts, radiological studies, and laboratory results—have been computerized since 1995. The 240 patients for this study were identified as having gallbladder cancer within the hepatobiliary database from January 1995 to March 2002. Data for analysis were extracted from the hepatobiliary database and the computerized patient records and were analyzed retrospectively. This project was performed under institutional review board approval. The data examined included patient demographics, clinical history, pathology, laboratory values, and outcome. The {chi}2 test was used where appropriate. Survival analyses were performed with SPSS statistical software (SPSS, Inc., Chicago, IL). Univariate analyses were performed by log-rank comparisons of Kaplan-Meier survival curves, and Cox regression was performed for multivariate analyses. Differences were considered significant at the P < .05 level. Ninety-five percent confidence intervals (CI) are reported.

Patients were considered jaundiced if clinical jaundice was present on initial examination at MSKCC. If a prior intervention was performed at the referring institution, patients were considered jaundiced if both history and a bilirubin level >8 had been documented. At MSKCC, care for patients with gallbladder cancer is planned at a multidisciplinary hepatobiliary disease management conference where pathology, radiology, and relevant laboratory results are discussed. Decisions regarding operability and treatment reflect the opinions of the members of this team.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Demographics
During the 6-year study period, 240 patients with gallbladder cancer were seen at MSKCC. The median age for the entire group was 65 years, with an SD of 10 years. There were 77 male patients (32%) and 163 female patients (64%). Two hundred thirty-seven (99%) of 240 patients presented with primary disease. One hundred sixty patients (67%) were explored, and 70 (29%) patients were resected. Thirty-four percent of patients (n = 82) with gallbladder cancer presented with jaundice. In 80 (98%) of 82 patients, the jaundice was due to the malignancy, and in 2 patients the jaundice was the result of concomitant stones. Most patients (n = 141; 59%) presented with advanced-stage disease (Table 1).


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  		TABLE 1. Patient demographics (n = 240)
 
Survival
The median disease-specific survival for the entire population was 11 months (95% CI, 8–14 months; Fig. 1A). One hundred fifty (63%) of the 240 patients have died of disease, with a median survival of 7 months (range, 0–72 months). Disease-specific survival stratified by stage is shown in Fig. 1B. As graphed, stage reflects the changes as outlined in the recently revised American Joint Committee on Cancer staging manual (6th edition) and includes all patients. Stage I has been expanded to include all of the favorable T2NO patients previously classified as stage II. Most patients with stage I gallbladder cancer in this study do well, as shown by median disease-specific survival not yet achieved and a 5-year disease-free survival of 72%. Stage II now contains a much more diverse group of patients, including those with the larger T3 tumors with and without regional lymph node involvement and small T1/T2 tumors with lymph node involvement. The comparatively shorter survival (median disease-specific survival, 22 months; 95% CI, 12–31 months) is explained by the definition of patients with regional lymph node metastases as stage IIB. Long-term survival in stage III and IV patients was limited to a single patient with an adenosquamous variant and a T4N0M0 (stage III) tumor with extensive resection after a complete response to chemotherapy. The median disease-specific survival in stage III and IV disease was 10 months (95% CI, 6–14 months) and 5 months (95% CI, 4–7 months), respectively.



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  		FIG. 1. Kaplan-Meier disease-specific survival curves for (A) all 240 patients, (B) patients stratified by stage, (C) patients by ability to achieve an R0 resection versus all other patients, and (D) patients who presented with jaundice versus without jaundice. P values represent log-rank comparisons between curves.

 
At MSKCC, patients who are otherwise in reasonable health and have a T2 or greater tumor and no evidence of distant disease are offered operative exploration with possible resection. Of the 240 patients who presented for treatment, 160 patients (67%) were offered and consented to a surgical exploration. Seventy (29%) of the 160 underwent resection, and 66 patients were found on final pathologic review to have negative microscopic margins. The median disease-specific survival (34 months; 95% CI, 29–40 months) was statistically longer in patients able to undergo complete resection with negative margins compared with those not able to achieve a complete resection (median, 8 months; 95% CI, 7–10 months; P < .0001) or compared with all other patients (those with R1 or R2 resections and those who did not have a resection) with gallbladder cancer (median, 8 months; 95% CI, 6–9 months; P < .0001; Fig. 1C).

Jaundice occurred in 34% of patients and was an independent predictor of poor outcome on univariate analysis. Median disease-specific survival was significantly worse for patients presenting with jaundice (6 months; 95% CI, 4–8 months) compared with those without jaundice (16 months; 95% CI, 9–23 months; Fig. 1D; P < .0001). On multivariate analysis, jaundice was not an independent predictor of disease-specific survival but was closely associated with advanced-stage disease (Table 2). There were only three patients in the jaundiced group who did not have advanced disease. This included one of the two patients with concomitant stones T1N0M0 (stage IA) and two patients with T3N0M0 (stage IIA) disease with invasion of the common bile duct. A similar percentage of jaundiced (67%; n = 55) and nonjaundiced (66%; n = 105) patients were explored, but there were fewer attempted resections in the jaundiced group (n = 6; 7%) compared with the nonjaundiced group (n = 64; 41%; P < .001). In addition, there were fewer R0 resections in the jaundiced group (n = 4; 5%) compared with the nonjaundiced group (n = 62; 39%; P < .001). In the small group of jaundiced patients able to undergo resection, there were no 2-year survivors, compared with 21% in patients without jaundice as a presenting symptom (Table 3; P < .0001).


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  		TABLE 2. Survival analyses
 

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  		TABLE 3. Comparison between jaundiced and nonjaundiced patients with gallbladder cancer (n = 240)
 
Jaundice in Gallbladder Cancer
There was documentation of common bile duct involvement in 73 (89%) of the 82 patients with jaundice and the more proximal biliary tree in 7 patients (9%). Because gallstones are a common cause of jaundice, they were initially suspected in most patients but were the cause of jaundice in only two patients (2%) in this series.

Sixty-seven percent of jaundiced patients (n = 55) underwent operative exploration. Of the 27 patients who did not undergo operative exploration, 14 had radiographically documented liver metastasis, 6 had radiographically unresectable invasion of the portal vein, 12 had intra-abdominal spread of disease (6 were documented pathologically at the referring institution on biopsy samples taken at the time of cholecystectomy), and 6 had radiographically apparent peritoneal or omental metastasis, including 1 with malignant ascites. Two patients were not offered surgical exploration solely on the basis of the presence of significant medical comorbidities. Surgery was not necessary in the single patient with jaundice secondary to a common bile duct stone, who was adequately treated with cholecystectomy for a T1 tumor.

In the 55 jaundiced patients who were explored, diagnostic abdominal laparoscopy was performed in 25 patients (45.5%), and diagnostic thoracoscopy was performed in 1. In 17 patients, peritoneal metastases were diagnosed on laparoscopy, and further exploration was not performed. A lung nodule biopsied thoracoscopically proved to be of biliary origin, thus obviating abdominal exploration. A total of 37 patients underwent laparotomy for exploration, including 29 patients primarily explored and 8 patients who passed laparoscopic examination. Peritoneal metastases were identified in five patients and liver metastases in three patients. Resections were aborted because tumors were found to be invading vascular structures: portal vein in six patients, celiac artery in three patients, and hepatic artery in one. Clinically unresectable retroperitoneal disease was identified by lymph node biopsy in eight patients. Occasionally, gallbladder cancer involved other organs by direct extension, including the pancreas (n = 3), stomach (n = 2), and bowel (n = 3).

Six patients underwent attempts at curative resection for advanced-stage disease. Four patients underwent a right trisegmentectomy with common bile duct excision and lymphadenectomy. All four were reconstructed with a hepaticojejunostomy. One patient ultimately proved to have a single metastatic peritoneal implant despite a negative intraoperative frozen section. Another had a microscopically positive caudate resection margin noted on the final pathology. Two right trisegmentectomy patients achieved pathologically confirmed R0 resections, but both developed recurrence within 6 months. The two remaining patients underwent segment IV/V liver resections with excision of the common bile duct, lymphadenectomy, and hepaticojejunostomy. One patient underwent a partial gastrectomy and partial colectomy as part of an en-bloc resection with clear surgical margins, and one had a microscopically positive liver margin. Both developed clinical recurrence within 6 months. Morbidity and mortality were particularly high in this highly selected group of six patients. Five of the six patients had at least one complication, including three wound infections, two postoperative pneumonias, one case of renal failure, and one subphrenic abscess. Two patients died of these complications during their surgical hospitalization—one on postoperative day 18 from renal failure and one on postoperative day 37 from acute respiratory distress syndrome as a direct consequence of pneumonia and sepsis. In summary, of the six highly selected patients with jaundice who underwent a resection, only four had negative microscopic margins, and subsequently all had disease recurrence or died within 6 months.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In 1924, Alfred Blalock penned "in malignancy of the gallbladder when a diagnosis can be made without exploration, no operation should be performed, inasmuch as it only shortens the patient’s life."11 Although great strides have been made in the operative management of gallbladder cancer, with improvements in postoperative morbidity and mortality, the pessimism relayed in this quote is still relevant. Disseminated gallbladder cancer has a poor outcome. In this series of patients, we identified at presentation a group of patients by the clinical sign of jaundice with advanced unresectable malignancy. Rarely is a single clinical sign such a powerful predictor of outcome.

We describe our experience with 240 patients who presented with gallbladder cancer. As shown by our rate of surgical exploration and resection, we have taken a very aggressive approach to this disease. Disease-specific survival, as shown in Fig. 1 for both stage and ability to achieve an R0 resection status, demonstrates the utility of surgery in improving survival. The 5-year survival rate for patients with completely resected disease in this study was 35%. This correlates favorably with published results from other institutions.12,13 In our experience, patients with any degree of tumor dissemination do poorly. In contrast to reports from other centers,14–16 this includes patients with metastasis limited to the regional lymph nodes. In Western literature, patients with a single positive cystic duct node and complete resection will rarely have a limited survival advantage.17–19 This contrasts sharply with the 5-year survival rate of 60% in patients with metastatic disease to the N1 nodes, as reported by Onoyama et al.16

Stage IA gallbladder cancer is sufficiently treated with cholecystectomy. Stage IB or T2N0M0 tumors are best treated by extended resections that include a rim of liver parenchyma and portal lymphadenectomy. Depending on the location, these tumors may require trisegmentectomy to adequately clear the porta hepatis. Aggressive surgical treatment of this subset of patients improves survival to 80% from the historical 20% to 40% reported in the literature for cholecystectomy alone.12–14,18 Treatment of T3 stage IIB and greater tumors remains controversial. Certainly, there are reports of long-term survivors, particularly with large node-negative T3N0M0 tumors. Unfortunately, most of these patients have short survivals secondary to early recurrence, even with aggressive resection. In our experience, the presence of even minimal nodal disease seems to predict subsequent tumor dissemination in most patients.3,18,20 Stage III and IV cancers in the current staging system are not amenable to surgery. T4 tumors by definition invade the portal vasculature, and there is no indication to resect (M1) metastatic gallbladder cancer.

Selection of patients who will benefit from surgery is based on patient history, radiological studies, and review of outside pathology. Because ours is a tertiary cancer referral center, many of our patients present with the diagnosis already established. Most commonly, the diagnosis of gallbladder cancer was documented at a prior exploration for cholecystectomy or, in the case of the jaundiced patient, at the time of the intervention for jaundice. Advanced gallbladder cancer is often obvious on abdominal exploration, and prior operative reports and pathology can be extremely helpful in deciding which patients should be reexplored. Radiological studies are helpful in identifying liver or lung metastasis and portal vascular involvement. Radiological tests were not helpful in the identification of low-volume peritoneal disease or lymph node metastasis because many enlarged nodes were reactive, possibly as a consequence of the recent prior surgery.21,22

In this study, jaundice was identified in 34% of patients who presented with gallbladder cancer. This number is consistent with other series in which this physical sign has been reported.3 In this series, patients who presented with jaundice as a result of gallbladder malignancy invariably had disseminated disease even if it not detectable on preoperative evaluation or operative exploration. In very few jaundiced patients was an attempt at resection possible. Despite the advances in operative technique and tools, rates of resectability for jaundiced patients have not changed. In one study, jaundice represented unresectability in 18 of 18 patients.17,23 In our series, resection was of limited value even in those with apparently R0 resections. Jaundice was not an independent predictor of survival on multivariate analysis but was highly correlated with advanced-stage (III and IV) disease (Table 2). Gallbladder cancer that invades the biliary tree with subsequent jaundice defines a subset of patients with aggressive disease. In gallbladder cancer, the biology that allows a tumor to invade the biliary tract and cause jaundice correlates well with the gross and microscopic spread of gallbladder tumors. Patients with jaundice did not benefit from surgery. At this time, for the subset of patients with jaundice, focus should be on experimental therapies or quality-of-life issues. These results do not support the routine surgical exploration of patients with gallbladder cancer who present with jaundice.


   FOOTNOTES
 
Presented at the Society of Surgical Oncology’s 56th Annual Cancer Symposium, Los Angeles, California, March 5–9, 2003.

Jaundice is an indicator of advanced malignancy in patients with gallbladder cancer. Jaundice predicts unresectability on surgical exploration and a short disease-specific survival.

Received for publication March 6, 2003. Accepted for publication November 4, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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