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10.1245/ASO.2006.03.064
Annals of Surgical Oncology 13:75-85 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Solitary and Multiple Isolated Metastases of Clear Cell Renal Carcinoma to the Pancreas: An Indication for Pancreatic Surgery

Franz Sellner, MD1, Natascha Tykalsky, MD1, Maria De Santis, MD2, Jörg Pont, MD2 and M. Klimpfinger, MD3

1 Surgical Department, Kaiser Franz Josef Hospital, Vienna, Austria
2 Department of Medical Oncology, Kaiser Franz Josef Hospital, Vienna, Austria
3 Institute of Pathology, Kaiser Franz Josef Hospital, Vienna, Austria

Correspondence: Address correspondence and reprint requests to: Franz Sellner, MD, Kundratstrasse 3, A-1100 Vienna, Austria; E-mail: sellner.franz{at}aon.at


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Isolated pancreatic metastases (isPMs) of clear cell renal carcinoma are rare. Most of them are solitary; some are multiple. The reported rates and the clinical implications of multiple isPMs from clear cell renal cancer vary. Therefore, the available literature was analyzed to shed light on the clinical significance of these extremely rare metastatic lesions.

Methods: A literature search brought to light 236 cases of isPMs (both solitary and multiple) from renal cell carcinoma. These were analyzed.

Results: A total of 12%of the metastases were synchronous with the primary tumor, and 88%were metachronous, occurring 10.0 ± 6.5 years (mean ± SD) after nephrectomy. A predilection for a specific part of the pancreas was not identifiable. The localization of the renal cell cancer (left or right kidney) did not have any effect on the site of the metastases. Seventy-four (39%) of the metastases to the pancreas were multiple (3.2 ± 1.5). Their epidemiology did not differ from that of solitary metastatic lesions. Actuarial 3- and 5-year survival rates after radical resection were 78%and 78%, respectively, for multiple versus 75%and 64%for solitary metastases.

Conclusions: The epidemiological data do not support a direct local lymphogenous or venous spread from the primary tumor to the pancreas. They rather suggest a systemic spread. Because of the positive outcome, radical removal of both solitary and multiple metastases should be attempted in eligible patients.

Key Words: Solitary/multiple pancreatic metastases • Renal carcinoma • Epidemiology • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Isolated pancreatic metastases (isPMs), i.e., metastases confined to the pancreas at the time of diagnosis, are rare. Most of them are referable to clear cell renal carcinoma.1–3 The epidemiology, clinical presentation, and treatment of isPMs from renal cell carcinoma, most of them solitary, are known from single-institution case reports and literature reviews.1–109 However, as more and more cases have been reported, it has become obvious that isPMs may be multiple in some cases. The clinical implications and the treatment of multiple isPMs are still controversial. Although major institutional series also contain some isPMs, individual authors keep emphasizing that multiple isPMs are extremely rare. 25 Treatment recommendations for multiple isPMs vary. Whereas some advise total pancreatectomy, others1,10,12 critically reject surgery on the assumption that multiple isPMs signal incipient fatal disseminated metastatic disease. In view of the rare occurrence of the condition, the experience accumulated by single institutions can hardly be expected to yield conclusive data in the near future. This prompted an extensive literature search. On the basis of this search and three cases from the authors’ patient population, an attempt was made to establish the epidemiology, clinical presentation, and treatment of isPMs; the rate of multiple isPMs among the reported cases; and, given an adequate rate, the differences, if any, between solitary and multiple isPMs.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The literature search was based on the MEDLINE (PUBMED) registry and covered 51 years: i.e., from 1952 (the first description of an isPM by Jenssen109) to the end of 2003. Only reports of synchronous or metachronous isPMs from clear cell renal carcinoma in patients without metastases to other organs at the time of diagnosis were considered, provided that these were confirmed by tissue diagnosis. Cases reported more than once under different aspects (e.g., treatment or diagnosis) were listed only once.10,19,22,23,26,45,110–112 Data on the epidemiology and pathology, as well as clinical variables—i.e., age; sex; site of primary renal cell cancer; time to manifest metastatic disease; number, size, and site of metastases; symptoms; surgical procedure; and survival time—were collected and analyzed. The term radical resection was applied to all reports in which R0 resection of the metastatic lesions could be achieved.113

For rating metastases as solitary or multiple, only those reports were considered that specified the number of lesions or that used wording clearly indicative of singularity (e.g. a, one, or singular) or multiplicity (e.g., some). Diffuse involvement of the pancreas was not included in the count of solitary/ multiple isPMs because the source of diffuse involvement, i.e., diffuse growth of one solitary lesion or coalescence of multiple lesions, cannot be established with certainty in retrospect.

For defining the site of the metastatic lesions, only solitary isPMs that were unequivocally assignable to a specific part of the pancreas (head, body, or tail) by preoperative imaging, the surgeon’s report, or the resected specimen were considered. Reports of extensive lesions affecting more than one part of the gland were not included, because their origin also cannot be established with certainty retrospectively.

It goes without saying that, in a retrospective literature review, not all of the articles contained data on all variables evaluated. This reduced the number of articles considered for subset analyses. The actual number of articles that provided information on a given variable was specified.

All continuous data are presented as means and standard deviations. Differences were evaluated with the {chi}2 test, Fisher’s exact test, and Student’s t-test. Survival was calculated according to the Kaplan-Meier method. Differences in survival among subgroups were compared by using the log-rank test. P < .05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Epidemiology and Pathology
From 1952 to the end of 2003, at least 233 adequately documented isPMs from clear cell renal carcinoma were reported.1–109 Together with 3 cases contributed from the authors’ patient population (Table 1Go), a total of 236 observations was gathered and analyzed. Of these reports, 157 provided information on survival.


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  		TABLE 1. Summary description of three patients with isolated pancreatic metastases from clear cell renal carcinoma
 
The results are shown in Table 2Go (mean age, 63.1 years; SD, 9.7 years; 43%female; 57%male). Most of the metastases (88%) were metachronous.10,13,25–29,32 On the basis of 167 observations, the mean interval from nephrectomy to manifest pancreatic metastases was 10.0 years (SD, 6.5 years). The longest interval was 32.7 years.29 The synchronous occurrence of renal cell cancer and isPMs14,35 was uncommon, with only 23 (12%) recorded cases. Symptomatic metastases before manifest renal cell carcinoma were still more uncommon.29 Of the solitary metastases, 49 were localized in the head, 23 in the body, and 18 in the tail of the pancreas. However, because the head accounts for 46%of the total size and the body and the tail account for the remaining 54%,114 there is no significant evidence of a preference of one or the other half of the gland29 (P = .123). Similarly, the site of the primary renal cell cancer, i.e., the left or right kidney, did not influence the distribution pattern of solitary metastases to the pancreas (Table 3Go).


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  		TABLE 2. Results of literature review—236 reported cases1–109
 

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  		TABLE 3. Kidney affected by renal cell carcinoma versus site of solitary metastases (P = .402)
 
Clinical Presentation
A total of 35%of the metastases did not cause any symptoms and were detected during follow-up programs after renal cell cancer surgery.11,29,38 In patients with symptoms (n = 66), pain (20%), gastrointestinal bleeding (20%), weight loss (9%), jaundice (9%), pancreatitis (3%), and diabetes (3%)3,13,28,29,53,90 were the most common.

Outcome of Surgery
Standardized pancreatic resection adapted to the location of the tumor19,53 in terms of partial pancreaticoduodenectomy,19 distal pancreatectomy, and total pancreatectomy19,105 was generally recommended for the management of isPMs (Fig. 1Go). Because of the high recurrence rate,115 atypical local resection7,38 was confined to some exceptional cases. The three patients from the authors’ patient population are alive 3, 4 (with recurrent disease), and 5 years after surgery. By no means unique, this outcome is confirmed by the literature review. Three-year survivals were documented in at least 41 articles, and 5-year survivals were documented in 23 articles.6,15,17,19,23,26–29,54,58,63,71,83,98 The literature review showed actuarial 3- and 5-year survival rates of 78%and 72%, respectively.


Figure 1
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  		FIG. 1. Kaplan-Meier survival curves; outcome after radical resection of isolated pancreatic metastases versus omission of radical resection (P = .0383).

 
Outcome Without Radical Resection
Omission of radical resection was reserved for a few exceptional cases (Fig. 1Go).10–12,26,37–39,90,98 Ten of the 13 pertinent reports of nonresected isPMs specified the survival times. Two of the patients documented underwent what is now known to be an ineffective chemotherapeutic regimen, and another eight went without treatment. The survival data of these 10 patients with nonresected disease were compared with the data of 139 patients who underwent radical resection. The actuarial 3- and 5-year survival rates of 21%and 0%for nonresected metastases were significantly (P = .0383) poorer than those for resected lesions (78%and 72%).

Prognostic Factors of isPM
In 11 articles2,6,15,17,19,23,27,40,41,49,90 presenting a total of 58 isPMs, lymph node involvement was reported in only a single case.6 Together with multiple metastases, which are presented later, synchronous and symptomatic metastases are listed as potential risk factors.23,29 Figures 2Go and 3Go show the survival curves of synchronous/metachronous and asymptomatic/symptomatic isPMs. Although there was no difference in the effect of synchronicity or metachronicity on the prognosis, asymptomatic metastases tended to have a better prognosis than symptomatic lesions. However, the difference missed significance because of the small number of cases (P = .0832).


Figure 2
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  		FIG. 2. Kaplan-Meier survival curves; outcome after radical resection of metachronous versus synchronous isolated pancreatic metastases (P = .7372).

 

Figure 3
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  		FIG. 3. Kaplan-Meier survival curves; outcome after radical resection of symptomatic versus asymptomatic isolated pancreatic metastases (P = .0832).

 
Recurrence of Metastases
Of the 90 properly documented cases, 31 (34%) patients developed recurrent lesions after a mean disease-free interval of 24 months (SD, 23 months). The occurrence of metastatic lesions after earlier metastases to the pancreas were removed usually heralds disseminated lethal disease. This is reflected by a significant decrease in actuarial 3- and 5-year survival rates to 67%and 56%(P = .0067).

There are some reports of late metastases in only a single organ, with long-term remissions when these are removed19,27,28,36: 12 months after the resection of a periprostatic metastasis by Yavascaoglu et al.,35 47 months after the resection of a liver metastasis by Le Borgne et al.,28 and no less than 60 months after the removal of a skeletal metastasis by Faure et al.19 Our patient 3 is another case in point.

Solitary/Multiple Pancreatic Metastases
Of the total of 236 isPMs, 187 were described as solitary or multiple. Of these, no fewer than 74 were multiple.3,6,10,15–20,24–29,33,34,36,38,40,42,44,45,50,53,57,64,65,70,77,79,81–83,85–87,97,98 This is equivalent to 39%and means that at least every third patient has multiple isPMs. Discounting articles with an unspecified number of metastases (e.g., multiple), the mean number of metastases was 3.2 (SD, 1.5; lowest number, 2; highest number, 7). The number (i.e., 74) of articles that documented multiplicity permitted a comparison of solitary and multiple metastases (Table 4Go). There was no significant difference between solitary and multiple metastases in terms of age, synchronicity, and time to onset.


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  		TABLE 4. Solitary/multiple metastases to the pancreas—187 reported cases
 
Of the 187 articles, 120 provided information on survival and were analyzed (Table 4Go). Surprisingly, the outcome of radical resection for multiple metastases did not differ from that for solitary metastases. The actuarial 3-year survival rates were 78%for patients with multiple metastases and 75%for those with solitary metastases. The 5-year survival rates were 78%and 64%, respectively (Fig. 4Go). At least four patients with multiple metastases to the pancreas17,19,27 and our patient 2 survived after radical surgery for 5 years: one survived for at least 10 years.17


Figure 4
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  		FIG. 4. Kaplan-Meier survival curves; radical resection of solitary versus multiple isolated pancreatic metastases (P = .8591).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Metastases to the pancreas are rare. Most of them do not present before the end stage of various primary neoplasms,28,41,44,88 and isPMs, i.e., metastases confined to the pancreas at the time of diagnosis, are rarer still. Most of them take their origin from clear cell renal carcinoma3,27,46,51 and are an uncommon indication for pancreatic surgery. Our database of 301 pancreatic resections (34 distal pancreatectomies and 267 partial and total pancreaticoduodenectomies) from the past 30 years contained no more than the 3 cases (1%) presented. Thompson and Heffess29 found pancreatic metastases to account for 3%of all pancreatic neoplasms in clinical material. Faure et al.19 and Yachida et al.17 reported 2%of all pancreatic masses subjected to operation to be metastatic. According to Nakamura et al.,116 only 1%of all pancreatic metastases in a postmortem series were caused by renal cell carcinoma.

The symptoms of isPMs are unspecific diagnostically, and imaging also rarely shows abnormalities seen only in renal cell carcinoma. Together with the generally rare occurrence of isPMs, this explains why solitary isPMs are sometimes mistaken for primary tumors,17,25,39,47,117 particularly if the interval from the resection of the underlying renal cell cancer is long. In eight of the articles reviewed, the true nature of the lesion was not suspected before the tissue diagnosis of the resected material was available.2,25,30,32,40,43,45,48

In the differential diagnosis, isPMs from renal cell carcinoma should be distinguished from primary neoplasms of the pancreas,29 i.e., adenocarcinoma, cystadenocarcinoma,2 and apudoma,25,28,30,40 as in our patient 2. The typical features of metastases from renal cell cancer detected by imaging studies (ultrasonography, computed tomography, magnetic resonance imaging, and endoscopic ultrasonography) were repeatedly described.33,42,50,52,112,118–120 However, because these features are not confined to metastases from renal cell carcinoma, the differentiation from other neoplasms of the pancreas is problematic in the individual case.1 In the past, angiography played an important role in the differential diagnosis.2,11,20,40,47 Nowadays, tissue diagnosis can be established before surgery with fine-needle aspiration biopsy2—ultrasonography guided,11,38,117 computed tomography guided,2,39,50,51 or endoscopic ultrasonography guided.10,12,111,121 These techniques allow definitive tissue diagnosis, as well as an assessment of resectability.

Surgical treatment of isPMs from neoplasms other than renal cell cancer carry a poor prognosis,88 because they often signal the onset of disseminated metastatic disease.26 However, a recent retrospective study demonstrated that in a highly selected group of patients with distant pancreatic melanoma metastases, complete resection of the metastases may improve survival. By contrast, the outcome of surgery for isPMs from clear cell renal carcinoma is clearly superior,15,28 with a mean survival time of 4 years110,113 and actuarial 5-year survival rates of 43%to 75%,6,15,23,29 and is even better than the outcome of surgery for primary adenocarcinoma of the pancreas.2,10,14,18,23,25–27,40,41,123,124 This positive outcome suggests (1) that isPMs must not be regarded as accidental initial manifestations of impending diffuse metastatic disease and (2) that a point must be made to correctly diagnose isPMs from renal cell cancer and subject them to radical resection.2,14,27 The unusually positive outcome of treatment prompted a research group13 to question, rightfully, whether the positive outcome was really attributable to the successful removal of the metastases or whether it reflected an extremely protracted natural history of isPMs. Our analysis showed (1) a 3-year cumulative survival rate of 21%for nonresected isPMs and (2) a significantly longer survival time of patients with resected versus nonresected metastatic lesions. Point 1 is indeed indicative of a more favorable spontaneous history of isPMs,13 but point 2 reveals that the more favorable spontaneous history is substantially improved by operation.25 In view of the benefits of surgical treatment, denying radical resection because of what may be an incipient disseminated metastatic disease is contraindicated.6,13,25

The absence of lymph node involvement125 is a special feature of isPMs and may be one of the factors that explains the favorable outcome of surgery. It justifies both an omission of extended lymphadenectomy19,41 and a generous use of pylorus-preserving partial pancreaticoduodenectomy.20,23,27,28,35,40,41 Of the other prognostic factors of isPMs discussed in the literature (solitary, metachronous, and asymptomatic), only the last one tended to have a positive effect on the outcome; this underscores the usefulness of follow-up programs. However, anecdotal reports of 5-year survivors with synchronous23,64 and symptomatic17,19,27,63 metastases suggest that neither synchronous nor symptomatic metastases should be interpreted as signaling doom and that radical resection should, therefore, be invariably considered for eligible patients.

Recurrent metastatic lesions should be expected in 34%of cases after a mean disease-free interval of 2 years. This reflects generalized end-stage disease that defies surgical management.19,29,63 A less relentless course was reported only for recurrent metastatic lesions that were, again, confined to a single organ with long-term remissions, once these were removed.6,19,27,28,36 At least in these patients, the tumor apparently keeps its growth pattern, i.e., causing solitary metastases with years of disease-free intervals, during the disease course. This justifies another attempt at surgery in cases like those described previously.6

Solitary/Multiple Pancreatic Metastases
In the early reports, multiple isPMs from renal cell carcinoma were described as extremely rare events. In 2000, Fricke et al.25 still counted no more than eight cases. However, the assumption that multiple metastases to the pancreas are extremely rare is unsupported, because 74 of all metastases recorded to date were multiple.

A comparison of solitary and multiple isPMs brought to light three interesting aspects: (1) more than one third of all isPMs were multiple; (2) no significant differences were found between solitary and multiple isPMs in terms of age, synchronicity, and time to onset; and (3) solitary and multiple isPMs did not differ significantly in terms of the treatment outcome. These findings may have a dual explanation: (1) multiple metastases are not attributable to a late diagnosis (e.g., a protracted interval between nephrectomy and the detection of isPMs), and (2) most multiple metastases presumably develop during a single short metastasizing episode. If neither of these applied, then the time to manifest metastases would be longer and the age at onset would be higher in patients with multiple metastases.

Because multiple metastases do not have a significantly poorer outcome, omitting or decidedly rejecting radical surgery,1,10,12 if possible, is unfounded. Radical resection for multiple metastases is just as beneficial as it is for solitary metastases. The only difference found was in the type of operation: as would be expected, total pancreatectomy was more often performed in patients with multiple metastases (Table 4Go).

Mechanism of Disease
As the analysis shows, any concept of tumor spread leading to isPMs must account for four epidemiological facts: (1) diffuse distribution of solitary isPMs throughout the pancreas; (2) localization anywhere in the pancreas irrespective of the site of renal cell cancer, i.e., left or right kidney; (3) frequency of multiple metastases; and (4) absence of metastases to the lungs or other organs. Local lymphogenous or local venous spread through abnormal lymphatic or venous communications between the renal cell carcinoma and the pancreas19,27,90 cannot play an important role, because it would fail to explain the lack of relationship between the site of isPMs and the side affected by the primary tumor: i.e., the left or right kidney. The localization anywhere in the pancreas irrespective of the site of the renal cell carcinoma rather argues in favor of a hematogenous systemic spread. However, a systemic spread would not explain the discrepancy between the relative frequency of multiple isPMs and the absence of metastases to other organs. The most likely explanation for this unique behavior of isPMs would seem to lie in the special biology of the tumor. Apparently, the tumor cells have a high affinity for the parenchyma of the pancreas and only there find the conditions they need to mature to manifest metastases. The high affinity of some renal cancer cells for the parenchyma of the pancreas is supported by reports of metachronous late metastases, as in our patients 1 and 2, which again occurred solely in the residual pancreas.6,27 The results of basic research, which is slowly unraveling the local biochemical mechanisms that underlie the development of metastases, are promising, so it is hoped that the biochemical causes of the unique spreading pattern of some renal cell carcinomas will perhaps be understood one day.127,128


   ACKNOWLEDGMENTS
 
The authors thank Dr. J. Karner, head of the Department of Surgery of Kaiser Franz Josef Hospital, for providing cases 2 and 3 from the surgery database.

Received for publication March 8, 2005. Accepted for publication August 4, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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