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Annals of Surgical Oncology 9:675-679 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Results After Pancreatic Resection for Metastatic Lesions

Spiros P. Hiotis, MD, PhD, David S. Klimstra, MD, Kevin C. Conlon, MD, MBA and Murray F. Brennan, MD

From the Departments of Surgery (SPH, KCC, MFB) and Pathology (DSK), Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Spiros P. Hiotis, MD, PhD, NYU Department of Surgery, 550 1st Ave., NB 15 S 6, New York, NY 10016; Fax: 212-263-8640; E-mail: hiotis01{at}med.nyu.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Unlike primary pancreatic carcinoma, isolated metastatic lesions to the pancreas are uncommon. Although the value of surgical resection is poorly documented, resection may be deemed appropriate in selected cases. The aim of this study was to review our experience with the operative management of pancreatic metastases.

Methods: Sixteen patients who underwent pancreatic resection for the treatment of metastatic disease were identified from a prospective pancreatic database. The clinical features of and results after resection were examined.

Results: Renal cell carcinoma was the most frequent primary histopathology (10 of 16; 62%). In the remaining patients, the primary histopathology was non-small-cell lung cancer (n = 3), sarcoma (n = 1), melanoma (n = 1), or transitional cell carcinoma of the bladder (n = 1). A prolonged disease-free interval (median, 7.5 years) was characteristic of most patients. Operative procedures performed included eight pancreaticoduodenectomies, seven distal pancreatectomies, and one total pancreatectomy. The operative mortality was 6%, and the morbidity was 25%. The overall 2- and 5-year actuarial survival rates were 62% and 25%, respectively. A trend toward improved survival was observed in the renal cell carcinoma patients, but this finding was not statistically significant.

Conclusions: Long-term survival after pancreatic resection for metastatic disease is achievable, and patients with primary renal cell carcinoma seem to have a more favorable prognosis. Surgical resection should thus be offered to selected patients with isolated metastatic disease to the pancreas.

Key Words: Pancreas neoplasm • Metastasis • Renal cell carcinoma • Pancreatectomy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The potential benefit of metastasectomy for a variety of metastatic tumors is well documented in the literature. Colorectal carcinoma, sarcoma, and renal cell carcinoma are examples of common diseases that are clearly amenable to metastasectomy.1–4 As a result of an increasing body of literature to justify metastasectomy, major resections for metastatic lesions in sites such as the liver, lungs, and brain are often performed. The most common setting in which metastasectomy is undertaken for curative intent is isolated metastatic disease that is amenable to complete resection.

Although isolated metastatic disease to the pancreas is relatively uncommon, there are select cases in which this process does occur. Unfortunately, experience with pancreatic resection for the treatment of isolated metastatic lesions is very limited.5–14 As a result, few guidelines exist regarding the appropriate management of such lesions. There are several inherent biases with which clinicians sometimes approach the treatment of pancreatic malignancies. Thus, the potential benefit of a major pancreatic resection for metastatic disease is not obvious. Specifically, the poor prognosis associated with primary pancreatic adenocarcinoma and the historically high rates of perioperative morbidity and mortality after pancreatectomy may lead to a reluctance to treat pancreatic metastases with a major surgical resection. However, more recent data have clearly shown that pancreatectomy performed in high-volume clinical centers is increasingly safe. In fact, mortality rates after pancreatectomy have decreased to <5% when performed by experienced surgeons in high-volume institutions.15–19

The purpose of this article is to describe the Memorial Sloan-Kettering Cancer Center experience with pancreatic resection for metastatic disease. Results included in this article come from a retrospective analysis of prospectively collected data.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients were identified from a prospective pancreatic database maintained by our department of surgery since 1983. All patients admitted and treated with pancreatectomy for any diagnosis at Memorial Sloan-Kettering Cancer Center between the years of 1983 and 2000 were included. For the purposes of this study, only patients who had undergone pancreatic resection for distant metastatic disease were selected. Patients who underwent pancreatectomy for direct involvement of the pancreas by other locally advanced intra-abdominal malignancies (e.g., colon, gastric, sarcoma, and so on) were excluded.

The demographics of the patient population and clinical variables—including the type of pancreatic resection, primary histopathology, presenting symptoms, perioperative morbidity and mortality, disease-free interval (dfi; the interval between presentation with the primary tumor and development of pancreatic metastases), and overall survival—were examined. This was assessed by a retrospective review of each individual patient’s chart and by review of information from the prospective pancreas database. Statistical analyses, including Student’s t-test, Kaplan-Meier analysis, and univariate regression analysis, were performed with the SPSS statistical software package (SPSS, Inc., Chicago, IL). The median follow-up of the survivors in the study was 3.1 years.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient Demographics
Sixteen patients who underwent pancreatic resection for metastatic disease were identified. Of these 16 patients, 7 (44%) were women, and 9 (56%) were men. The median age was 63 years, with a range of 39 to 81 years.

Symptoms
Eleven (69%) patients were asymptomatic at the time of presentation (Table 1). In these patients, the pancreatic metastases were identified incidentally as part of an extent of disease work-up. Two (13%) patients presented with jaundice, and three (19%) presented with hemorrhage. The intent of resection was cure or prolonged survival in 13 (81%) patients. Palliation was the intent of resection in three (19%) patients.


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  		TABLE 1. Resection of metastatic disease to the pancreas
 
Histopathology
Renal cell carcinoma was the most frequent primary histopathology (10 of 16; 62%). In the remaining patients, the primary histopathology was non-small-cell lung cancer (n = 3), sarcoma (n = 1), melanoma (n = 1), or transitional cell carcinoma of the bladder (n = 1).

Disease-Free Interval
A prolonged dfi was characteristic of this patient population. The median dfi for the entire group of patients was 7.5 years (range, 1–24 years). When patients were separated according to histopathology, a trend toward increased dfi was observed among the renal cell carcinoma patients as compared with all other patients (median dfi, 9.1 vs. 4.3 years; Fig. 1). However, this difference in dfi was not statistically significant (Student’s t-test).



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  		FIG. 1. Disease-free interval before presentation with pancreatic metastases for patients with renal cell carcinoma, as compared with all other patients.

 
Perioperative Morbidity and Mortality
Eight of the 16 patients underwent pancreaticoduodenectomy for lesions in the head of the pancreas. Seven patients underwent distal pancreatectomy. One patient underwent total pancreatectomy for simultaneous lesions in the head and tail of the pancreas. The observed 30-day perioperative morbidity rate was 25%. Postoperative complications included pneumonia, myocardial infarction, gastric perforation, and sepsis. There was a single postoperative death that occurred after pancreaticoduodenectomy for metastatic renal cell carcinoma to the head of the pancreas. This occurred secondary to complications of myocardial infarction, accounting for a mortality rate of 6%.

Survival After Pancreatectomy
When patients were analyzed as a single group, the median postoperative survival was 3.3 years (Fig. 2). The 1- and 2-year actuarial survival rates for the group as a whole were 79% and 62%, respectively (Table 2). When survival analyses were performed according to primary histopathology, a trend toward improved survival was observed in the renal cell carcinoma patients (Fig. 3; the median survival was 4.8 years in the renal cell carcinoma patients vs. 1.4 years in all others). A trend toward increased actuarial survival rates was also observed in the renal cell carcinoma patients. However, this trend did not achieve statistical significance.



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  		FIG. 2. Kaplan-Meier analysis: overall survival.

 

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  		TABLE 2. Overall actuarial survival according to primary histopathology
 


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  		FIG. 3. Kaplan-Meier analysis: overall survival according to histopathology.

 
Univariate analysis was performed to determine a possible association between improved survival and the following clinical variables: sex, age <60 years, prolonged dfi, and renal cell histopathology. No statistically significant relationship between survival and any of these factors was observed, because of the small number of patients.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Isolated metastatic disease to the pancreas is uncommon relative to metastases to sites such as the liver, lungs, and brain. As a consequence of limited experience, few guidelines exist for the management of these lesions. Three large series with long-term follow-up of isolated pancreatic metastases that were managed with surgical resection currently exist in the literature. Long-term survival after pancreatectomy was achievable in each of these series (Table 3).5–7 The purpose of our study was to determine the experience with pancreatic metastasectomy at our institution.


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  		TABLE 3. Recent series reported in the English literature describing experience with pancreatectomy for isolated metastatic lesions to the pancreas
 
The majority (62%) of patients with isolated pancreatic metastases who received resection at our institution had a primary diagnosis of renal cell carcinoma. Prior data from our institution and others have shown that patients with metastatic renal cell carcinoma to a variety of sites clearly exhibit prolonged survival when curative resection is undertaken.4 All of the patients in our study were treated with complete surgical resection, and long-term survival after resection was achievable. Kaplan-Meier analysis according to primary histopathology suggested superior long-term survival in the renal cell carcinoma patients, but because of our small patient population, this observation was not statistically significant. Whether resection itself played a significant role in the survival of these patients is somewhat debatable. The possibility exists that resection, particularly in the absence of symptoms or life-threatening complications, did not actually alter the natural history of this disease.

A prolonged dfi was a characteristic feature seen in our study population. This was particularly the case for patients in the renal cell carcinoma group. In fact, two thirds of the renal cell carcinoma patients developed pancreatic metastases 6 years or longer after the appearance of the primary tumor. Thus, metastatic disease to the pancreas must always be considered in patients with an isolated pancreatic lesion and any history of a preceding malignancy, regardless of the dfi. In cases in which the preceding malignancy was a renal cell carcinoma, the diagnosis for isolated metastatic disease to the pancreas is especially likely.

Because of the small size of our study population, we are unable to demonstrate a significant association between long-term survival after pancreatic metastasectomy and any clinical or pathologic factor. Thus, all patients who are acceptable-risk candidates for surgery should be offered pancreatic resection for isolated metastatic disease. As additional data are obtained, it is likely that we will be able to select the most appropriate candidates for pancreatic metastasectomy in the future.


   Footnotes
 
This study reviews a single institution's experience with pancreatic resection for metastatic disease. Long-term survival after pancreatic resection for metastatic disease is achievable, and patients with primary renal cell carcinoma seem to have a more favorable prognosis.

Received for publication June 11, 2001. Accepted for publication April 25, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Weber SM, Jarnagin WR, DeMatteo RP, Blumgart LH, Fong Y. Survival after resection of multiple hepatic colorectal metastases. Ann Surg Oncol 2000; 7: 643–50.[Abstract]
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  3. Bindal RK, Sawaya R, Leavens ME, Lee JJ. Surgical treatment of multiple brain metastases. J Neurosurg 1993; 79: 210–6.[Medline]
  4. Kavolius JP, Mastorakos DP, Pavlovich C, Russo P, Burt ME, Brady MS. Resection of metastatic renal cell carcinoma. J Clin Oncol 1998; 16: 2261–6.[Abstract]
  5. Z’graggen K, Fernandez-del Castillo C, Rattner DW, Sigala H, Warshaw AL. Metastases to the pancreas and their surgical extirpation. Arch Surg 1998; 133: 413–7.[Abstract/Free Full Text]
  6. Ghavamian R, Klein KA, Stephens DH, et al. Renal cell carcinoma metastatic to the pancreas: clinical and radiological features. Mayo Clin Proc 2000; 75: 581–5.[Medline]
  7. Faure JP, Tuech JJ, Richer JP, Pessaux P, Arnaud JP, Carretier M. Pancreatic metastasis of renal cell carcinoma: presentation, treatment and survival. J Urol 2001; 165: 20–2.[CrossRef][Medline]
  8. Roland CF, van Heerden JA. Nonpancreatic primary tumors with metastasis to the pancreas. Surg Gynecol Obstet 1989; 168: 345–7.[Medline]
  9. Kassabian A, Stein J, Jabbour N, et al. Renal cell carcinoma metastatic to the pancreas: a single-institution series and review of the literature. Urology 2000; 56: 211–5.[CrossRef][Medline]
  10. Barras JP, Baer H, Stenzl A, Czerniak A. Isolated late metastasis of a renal cell cancer treated by radical distal pancreatectomy. HPB Surg 1996; 10: 51–3.[Medline]
  11. Hirota T, Tomida T, Iwasa M, Takahashi K, Kaneda M, Tamaki H. Solitary pancreatic metastasis occurring eight years after nephrectomy for renal cell carcinoma. A case report and surgical review. Int J Pancreatol 1996; 19: 145–53.[Medline]
  12. Paz A, Koren R, Gal R, Wolloch Y. Late solitary pancreatic metastasis from renal cell carcinoma. Isr J Med Sci 1996; 32: 1319–21.[Medline]
  13. Stankard CE, Karl RC. The treatment of isolated pancreatic metastases from renal cell carcinoma: a surgical review. Am J Gastroenterol 1992; 87: 1658–60.[Medline]
  14. Hashimoto M, Watanabe G, Matsuda M, Dohi T, Tsurumaru M. Management of the pancreatic metastases from renal cell carcinoma: report of four resected cases. Hepatogastroenterology 1998; 45: 1150–4.[Medline]
  15. Balcom JHIV, Rattner DW, Warshaw AL, Chang Y, Fernandez-del Castillo C. Ten-year experience with 733 pancreatic resections: changing indications, older patients, and decreasing length of hospitalization. Arch Surg 2001; 136: 391–8.[Abstract/Free Full Text]
  16. Sohn TA, Yeo CJ, Cameron JL, et al. Resected adenocarcinoma of the pancreas—616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg 2000; 4: 567–79.[CrossRef][Medline]
  17. Porter GA, Pisters PW, Mansyur C, et al. Cost and utilization impact of a clinical pathway for patients undergoing pancreaticoduodenectomy. Ann Surg Oncol 2000; 7: 484–9.[Abstract]
  18. Tsiotos GG, Farnell MB, Sarr MG. Are the results of pancreatectomy for pancreatic cancer improving? World J Surg 1999; 23: 913–9.[CrossRef][Medline]
  19. Conlon KC, Klimstra DS, Brennan MF. Long-term survival after curative resection for pancreatic ductal adenocarcinoma. Clinicopathologic analysis of 5-year survivors. Ann Surg 1996; 223: 273–9.[CrossRef][Medline]



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