Adenosquamous Carcinoma of the Pancreas

PAPER Adenosquamous Carcinoma of the Pancreas

James A. Madura, MD; Benjamin T. Jarman; Michael G. Doherty; Moo-Nahm Yum, MD; Thomas J. Howard, MD

Hypothesis: Adenosquamous carcinoma of the pan- and or tail lesions had distal pancreatectomy and sple- creas is a rare but particularly virulent variant of inva- nectomy. Pathologically, all the tumors were poorly dif- sive ductal carcinoma. This review will demonstrate the ferentiated and aneuploid, and 5 of the 6 were locally aggressive biologic activity, histopathologic features, and metastatic. All but 1 patient had postoperative compli- DNA flow cytometric characteristics of this aggressive le- cations, but there were no operative deaths. One half of sion. In addition, the outcome is less favorable than in the patients received postoperative adjuvant chemo- other pancreatic neoplasms, in spite of aggressive surgi- therapy and radiation therapy. Only 1 patient is still alive cal and postoperative adjuvant therapy. at 9 months after surgery, but has known residual cancer around his portal vein noted during palliative distal Design: A retrospective review of 6 patients treated dur- pancreatectomy. ing an 8-year period. Conclusions: Adenosquamous carcinoma of the pan- Setting: A major urban university tertiary referral creas is an uncommon variant of exocrine pancreatic neo- hospital. plasm. It is characterized by an admixture of adenomatous and squamous cell elements and demonstrates Patients: There were 6 patients with this unusual tu- aggressive biologic behavior. This series of 6 patients is simi- mor seen between 1990 and 1998. There were 4 men and lar to the 134 cases reported since 1907, in that survival is 2 women, all white, with a mean ± SD age of 63.5 ± 14.7 short despite aggressive surgical therapy. Few patients with years. Symptoms were similar to those in patients with this disease live more than 1 year. Aggressive therapy should more common pancreatic malignant neoplasms. be tempered by the realization of the uniform poor prognosis associated with this malignant neoplasm. Results: Four patients with tumors in the head of the pancreas had pancreatoduodenectomy, and 2 with body Arch Surg. 1999;134:599-603

NVASIVE DUCTAL carcinoma ac- ture. Most of the reports have been small counts for the majority of pan- series or single case reports, and, of the creatic malignant neoplasms and large autopsy or surgical tissue reviews, has a poor prognosis with the ex- only a few reports detail clinical, his- ception of a series of highly se- topathologic, and patient outcome data. Ilected patients undergoing radical surgi- Survival times have been short in those pa- cal therapy for cure. Adenosquamous tients found to have unresectable tu- carcinoma of the pancreas is an unusual mors, as well as in those who have under- variant of pancreatic neoplasm. It has been gone aggressive resection for attempted variously referred to as adenoacan- cure. The prognosis of this uncommon le- thoma, mixed squamous and adenocarci- sion appears to be even less favorable than noma, and mucoepidermoid carcinoma. the invasive ductal tumor, with only a few These tumors are histologically charac- patients surviving more than 1 year. Be- terized by adenomatous cell populations cause of its rarity, only anecdotal studies mixed with varying amounts of keratin- of adjunctive radiation or chemotherapy From the Departments of ized squamous cell elements. Major insti- are available. Surgery (Drs Madura and tutional reviews of autopsy and/or surgi- This series of 6 cases over an 8-year Howard and Messrs Jarman cal specimens suggest an incidence of period demonstrates the aggressiveness of and Doherty) and Pathology (Dr Yum), Indiana University approximately 4% of all pancreatic neo- this tumor, and its rapid course from dis- School of Medicine, plasms; however, only 134 cases have been covery to death, despite aggressive surgi- Indianapolis. reported in the accessible world’s litera- cal treatment.

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Between 1990 and 1998, six patients were diagnosed as having adenosquamous carcinoma of the pancreas and treated at the Indiana University Medi- cal Center Hospitals, Indianapolis. There were 4 men and 2 women, all white, whose mean ± SD age was 63.5 ± 14.7 years. The duration of symptoms prior to presentation was 4.3 ± 3.9 months, and symptoms included abdominal pain and weight loss in 5 of the 6 patients, nausea and vomiting in 3 patients, and anorexia and jaundice in 2 patients. A single patient with a large tumor invading the duodenum presented with upper gastrointestinal tract bleeding and Figure 1. Computed tomographic scan of a patient with large anemia. Physical findings included upper abdomi- adenosquamous carcinoma of the mid-body of the pancreas. nal tenderness in 4 patients, jaundice in 2 patients with tumors in the head of the pancreas, and a pal- pable abdominal mass in 1 patient. Laboratory studies were unremarkable with the exception of el- evated bilirubin and alkaline phosphatase levels in the 2 patients with jaundice and moderately el- evated serum carbohydrate antigen 19-9 (Ca 19-9) of 200 U/mL (reference value, Յ70 U/mL) in 1 patient. Computed tomography and endoscopic ultra- sound both accurately demonstrated and localized a pancreatic mass in all 6 patients (Figure 1). Endo- scopic retrograde cholangiopancreatography was per- formed in 5 patients and demonstrated pancreatic ductal obstruction by tumor in the head or body, which corresponded with the tumor location on the imaging studies (Figure 2). Three patients had preoperative fine-needle aspiration biopsy of the tumor mass but none of the specimens were diagnostic of adenosquamous carcinoma. All 3 of the patients with tumors in the head of the pancreas underwent pancreatoduodenectomy, and those with tumors in the body and/or tail of the pancreas were treated by distal pancreatectomy and splenectomy. Figure 2. The endoscopic retrograde cholangiopancreatogram of the patient in Figure 1, demonstrating pancreatic ductal cutoff in the mid-body of the pancreas.

RESULTS atic parenchyma. Histologically, the tumors all displayed a mixture of ductal adenocarcinoma and squamous cell There were no postoperative deaths, but 5 of the 6 pa- carcinoma, with the latter comprising more than 30% of tients had postoperative complications, including 3 with the lesion. In a single case, the squamous cell component ventilator dependence and 2 with pancreatic fistulas that exceeded the glandular component by a 9:1 ratio. The ad- responded to nonoperative management. Postopera- enocarcinoma consisted of ductlike structures lined by co- tively, survival was short, with a mean ± SD survival of lumnar cells having large vesicular nuclei and prominent 5.04 ± 3.58 months. Three of the patients received ad- nucleoli. Most of these cells had pale to clear cytoplasm juvant chemoradiation therapy, but this did not result with occasional mucin vacuoles. The malignant squa- in significant prolongation of survival. One of the pa- mous cells were large and polygonal, having large hyper- tients who had previously undergone pulmonary resec- chromatic nuclei and eosinophilic cytoplasm with inter- tion for lung carcinoma committed suicide at 4 months cellular bridges and occasional squamous pearls. They were postoperatively. Four patients died of their malignancy arranged in diffuse sheets and lobules. These squamous at 1, 3, 5, and 12 months postoperatively. One patient and glandular components were for the most part inti- with known residual tumor surrounding the portal vein mately admixed (Figure 3). The tumors elicited a des- is alive at 8 months and has undergone radiation therapy moplastic response, which accounted for the firmness ap- along with gemcitabine therapy. preciated on gross examination. Four tumors were located in the head of the pan- Peripancreatic fat and neural invasion was present creas and 2 were in the body and tail. Tumor size ranged in all 6 cases. Lymphatic invasion was noted in 4 cases from 1.2 to 6.5 cm, with a mean size of 4.2 cm. Grossly, and the duodenal wall was invaded by tumor in 3 of the the lesions were firm with a light tan to yellowish color 4 tumors located in the head of the pancreas. Lymph node and merged imperceptibly with the surrounding pancre- metastases were found in 5 of the 6 patients. DNA flow

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©1999 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 cytometry demonstrated aneuploidy in 5 patients with S-phase determination between 5.2% and 30.0% (Table 1).

COMMENT

Exocrine tumors of the pancreas have been classified histologically in several large institutional reviews.1-4 The majority of cases are recognized as invasive ductal carcinomas. Other recognized variants include the mucinous tumors; pleomorphic, anaplastic, and large cell types; acinar cell carcinoma; spindle cell tumors; microadeno- carcinomas; and oncocytic cancers.5 Adenosquamous and squamous cell carcinomas are recognized much less fre- quently and probably account for 1% to 4% of all re- Figure 3. Histopathologic specimen in a patient with adenosquamous ported tumors. carcinoma of the pancreas. There is desmoplastic stroma with spindly The first known report of adenosquamous carci- fibroblasts and nests of squamous cell carcinoma and a malignant glandular noma in the literature is credited to Herxheimer6 in adenocarcinoma focus in the center (hematoxylin-eosin, original 1907 in which he referred to this lesion as “cancroide.” magnification ϫ250). Subsequently, other authors have referred to this tumor of mixed columnar adenocarcinoma and keratin- containing squamous cell elements as mixed squamous Table 1. Histopathological Characteristics and Flow and adenocarcinoma, mucoepidermoid carcinoma, and Cytometric Data in 6 Patients With Adenosquamous adenoacanthoma. This admixed tumor has been seen Carcinoma of the Pancreas* more commonly in other organ systems, such as the lungs, esophagus, colon, stomach, salivary glands, and Nodes, Patient Tumor No. Positive/ DNA S-Phase, DNA the female reproductive organs. Several reports describe No. Size, cm Total Cytometry % Index pancreatic tumors with a more unicellular squamous 7-9 1 1.2 ϫ 0.8 ϫ 0.3 0/15 Aneuploid 30 1.45 appearance without the glandular component. Most 2 4.6 1/1 Diploid 15 1.00 pure squamous lesions of the pancreas are thought to 3 5.0 ϫ 2.5 ϫ 1.7 1/3 Aneuploid 15 1.74 represent metastatic disease, and it is suggested that in 4 6.0 3/5 Aneuploid 20 1.52 the absence of another primary lesion the squamous 5 6.5 ϫ 5.0 ϫ 3.0 2/2 Aneuploid 13 1.86 pancreatic lesion will usually be found to have a glan- 6 2.0 6/9 Aneuploid 6 1.00 dular component with more careful histological inspec- tion.10 Since the pancreas does not normally contain *All tumors were poorly differentiated. any squamous cell elements, it has been proposed that squamous metaplasia occurs as a result of ductal inflammation due to chronic pancreatitis or obstruction metaplasia.14 In addition, there is a single report of an by an adenomatous tumor. Currently, there are several adenosquamous tumor focus in an equally unusual theories, none well proven, of the origin of the adeno- mucinous cystic neoplasm.15 squamous tumor. The most favored theory is that of The incidence of this unusual lesion is really not squamous metaplasia occurring as a result of obstruc- known, but estimates from review and classification of tion and inflammation and differentiating into a malig- pancreatic tumors from autopsy and/or surgically re- nant form.11 The “collision theory” suggests that 2 his- sected specimens have been demonstrated to be approxi- tologically different tumors arise independently and mately 4% (Table 2). Of the reported series, the inci- join or coalesce. No reports have proven this transition dence ranges from 0.9% to 11.1%, but this latter estimate phenomenon, but rather have demonstrated squamous was from a series of 27 surgical specimens.17 A number cell components intermingled in the body of the pre- of reports suggest that many of these lesions are large and dominantly adenocarcinoma. Electron microscopy has inoperable; therefore, analysis limited to surgical cases demonstrated 2 clearly different cell types. The adeno- may not be totally indicative of the true incidence since carcinoma cell demonstrates abundant endoplasmic many of these patients have not undergone subsequent reticulum and well-developed Golgi apparatus and surgery or autopsy. secretory vesicles. The other cell has scant amounts of A comprehensive review of 31 available reports be- endoplasmic reticulum but prominent bundles of tono- tween 1907 and 1997 identified 134 patients with ad- filaments, similar to cells seen in other squamous cell enosquamous tumors1-36 (Table 3). From those re- tumors.10 A final theory is that of malignant differentia- ports with detailed clinical data, there were 69 men and tion by a pluripotential duct cell into the 2 histological 45 women, a ratio of 1.53:1. The mean age of these pa- types.12 This theory has received support by an immu- tients was 62.4 ± 11.7 years, with a range of 33 to 86 years. nocytochemical study demonstrating positive stains for The major symptoms were no different than those of the Ca 19-9, ST 439, and keratin in varying degrees in both usual invasive ductal lesions of the pancreas, and in- the squamous and adenomatous cells.13 There is a cluded abdominal and back pain, weight loss, anorexia, report demonstrating carcinoma in situ in squamous and jaundice in patients with lesions in the head of the

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©1999 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 vival appears to be uniformly poor, should aggressive re- Table 2. Incidence of Adenosquamous Carcinoma section be undertaken, even if it appears potentially cura- in Major Retrospective Autopsy and Surgical Studies tive at the time of operation? From the review of the literature, there are only 5 known patients who have sur- No. of Specimens No. (%) of Adenosquamous vived 1 year or longer, in contrast to reported series of Source, y Autopsy Surgical Carcinomas highly selected patients with invasive ductal carcinomas Halpert et al,16 1965 120 0 5 (4.2) in whom 5-year survival rates of 20% to 30% have been Cihak et al,11 1972 90 0 4 (4.4) reported. In addition, mean survival with or without re- Baylor and Berg,1 1973 5075 0 46 (0.9) section is less than 6 months in the present series, as well Kissane,3 1975 205 0 6 (2.9) as those accumulated cases in the literature. One has to Cubilla and Fitzgerald,2 1980 525 120 20 (3.1) consider the risk and complications of major resective sur- Ishikawa et al,17 1980 0 27 3 (11.1) 4 gery in light of this rather short postoperative survival. If Morohoshi et al, 1983 167 97 10 (3.8) these lesions are small and there is no intraoperative evi- Chen and Baithun,5 1985 275 116 13 (3.4) Motojima et al,13 1992 145 57 6 (3.0) dence of nodal or distant metastasis, should these patients be denied an attempt at curative resection? Since pancreatoduodenectomy and distal pancreatectomy can currently be done with acceptably low morbidity and mor- Table 3. Details of Reported Patients With Adenosquamous tality, these procedures are probably the best palliative pro- Carcinoma of the Pancreas* cedures available. In the near future, more effective chemotherapy combined with radiation may allow better Literature Present survival with an acceptable quality of life. Review Series Total No. of reported patients, 1907-19971-36 134 6 Presented at the 106th Scientific Session of the Western Sur- M/F ratio 69:45 4:2 gical Association, Indianapolis, Ind, November 18, 1998. Age, mean Ϯ SD, y 62.4 ± 11.7 63.5 ± 14.7 Location in pancreas, No. Reprints: James A. Madura, MD, Department of Sur- Head 31 4 gery, Indiana University School of Medicine, 545 Barnhill Head and body 4 0 Dr, EM 244, Indianapolis, IN 46202-5125. Body 7 0 Body and tail 8 2 Tail 5 0 REFERENCES Diffuse 4 0 Survival, mo 1. Baylor SM, Berg JW. Cross-classification and survival characteristics of 5,000 Mean ± SD 5.7 ± 4.1 5.0 ± 3.6 cases of cancer of the pancreas. J Surg Oncol. 1973;5:335-358. Range 0.06-18 1.03-12.03 2. Cubilla A, Fitzgerald P. Surgical pathology of tumors of the exocrine pancreas. In: Moosa AR, ed. Tumors of the Pancreas. Baltimore, Md: Williams & Wilkins; *Not all reports contained complete data about each patient. 1980:159-193. 3. Kissane JM. 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Cell surface properties of normal, dif- differentiate it from the more common exocrine neo- ferentiating, and neoplastic pancreatic acinar cells. Cancer. 1981;47:1516-1525. plasms of the pancreas. A recent report by Kuji et al21 sug- 13. Motojima K, Tomioka T, Kohara N, et al. Immunohistochemical characteristics gests that these lesions may selectively take up gallium of adenosquamous carcinoma of the pancreas. J Surg Oncol. 1992;49:58-62. 14. Hartsock RJ, Fisher EJ. Cancer-in-situ in pancreatic squamous metaplasia. Arch 67 and be visualized by nuclear scanning. In several re- Surg. 1961;82:674-677. cent case reports, preoperative percutaneous and intra- 15. Campman SC, Fajardo MA, Rippon MB, et al. Adenosquamous carcinoma aris- operative cytologic studies have been diagnostically cor- ing in a mucinous cystadenoma of the pancreas. J Surg Oncol. 1997;64: rect, but this did not alter treatment decisions or 159-162. survival.22-25 16. Halpert B, Makk L, Jordan GLJ. A retrospective study of 120 patients with carcinoma of the pancreas. Surg Gynecol Obstetr. 1965;121:91-96. Once these lesions are identified, with or without ac- 17. Ishikawa O, Matsui Y, Aoki I, Iwanga T, Terasawa T, Wada A. Adenosquamous curate preoperative or intraoperative cytologic diagnosis, carcinoma of the pancreas: a clinicopathologic study and report of three cases. the question arises as to the extent of treatment. Since sur- Cancer. 1980;46:1192-1196.

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©1999 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 18. Sommers SC, Meissner WA. Unusual carcinomas of the pancreas. Arch Pathol. mous metaplasia in an adenocarcinoma that leads to 2 patho- 1954;58:101-111. logic entities in one tumor. 19. Cubilla AJ, Fitzgerald PJ. Morphological patterns of primary nonendocrine hu- In your lymph node metastasis, which of the elements me- man pancreas carcinoma. Cancer Res. 1975;35:2234-2248. tastasized, was it the glandular type or the squamous type? Can 20. Onoda N, Kang S-M, Sugano S, Yamashita Y, Chung Y-S, Sowa M. Mucoepider- moid carcinoma of the pancreas: report of a case. Surg Today. 1995;25:843-847. you conjecture why the prognosis was so bad in these patients? 21. Kuji I, Sumiya H, Taki J, et al. Intense Ga-67 uptake in adenosquamous carci- Is it possible that squamous metaplasia occurs more often in ad- noma of the pancreas. Ann Nucl Med. 1997;11:41-43. enocarcinoma and that we do not find it because we do not search 22. Smit W, Mathy J-P, Donaldson E. Pancreatic cytology and adenosquamous car- enough for it? The incidence of this tumor you said was 4%, but cinoma of the pancreas: a case report. Pathology. 1993;25:420-422. in a Japanese study, it was 11%. If this variant occurs more, should 23. Wilczynski SP, Valente PT, Atkinson BF. Cytodiagnosis of adenosquamous car- we be reconsidering our adjunctive therapy? Our therapy now cinoma of the pancreas: use of intraoperative fine needle aspiration. Acta Cytol. is geared toward adenocarcinoma. Should we be changing the 1984;28:733-736. chemotherapy or combining it with something geared toward 24. Leiman G, Markowitz S, Svensson LG. Intraoperative cytodiagnosis of pancreatic squamous, let’s say, platinum-based therapy? adenosquamous carcinoma: a case report. Diagn Cytopathol. 1986;2: 72-75. You talked about ERCP (endoscopic retrograde cholan- 25. Gupta RK, Wakefield SJ, Fauck R, Stewart RJ. Immunocytochemical ultrastruc- giopancreatography). If you had these patients first and you tural findings in a case of rare carcinoma of pancreas with predominance of ma- saw a CT scan clearly showing you a mass, would you put them lignant squamous cells in an intraoperative needle aspirate. Acta Cytol. 1989; through an ERCP? 33:153-156. Finally, one other question about biopsy. Because you saw 26. Case records of the Massachusetts General Hospital (case #31222). N Engl J 6 cases of this variant with bad prognosis, are you going to change Med. 1945;232:657-659. your philosophy? I suspect you are like me and do not do a 27. Frantz VK. Atlas of Tumor Pathology: Tumors of the Pancreas. Washington, DC: biopsy preoperatively or intraoperatively. Would you change Armed Forces Institute of Pathology; 1959. Section VII, fascicles 27 and 28. Ameri- your philosophy based on these 6 patients? can Registry of Pathology. 28. Elias E. Carcinoma of the pancreas. Arch Surg. 1969;98:138-140. Dr Madura: Dr Aranha, your first question was about the 29. Sasaki J, Ito S, Kashiwagi T, Imamura T, Iwashita A. Adenosquamous carci- cellular pattern of the lymph node metastases. We reviewed all noma of the pancreas. Naika Intern Med. 1977;39:337-341. of the lymph nodes in the 5 patients with metastases. Three of 30. Weitzner S. Adenoacanthoma of the pancreas: report of 4 cases and literature these patients had mixed adenocarcinoma and squamous cell car- review. Am Surg. 1978;44:206-209. cinoma in the nodes, while 2 patients, interestingly, had only squa- 31. Sears HF, Kim Y, Strawitz J. Squamous cell carcinoma of the pancreas. J Surg mous cell elements. We also evaluated the pancreatic lesions for Oncol. 1980;14:261-265. total content of each of the 2 specific cell types and found that 5 32. Yamaguchi K. Adenosquamous carcinoma of the pancreas: a clinicopathologic of the patients had 30% squamous cell cancer in their tumor, while study. J Surg Oncol. 1991;47:109-116. 1 patient had more than 90% squamous cells in his tumor. You 33. Yamaguchi K. Carcinoma of the uncinate process of the pancreas with a pecu- liar clinical manifestation. Am J Gastroenterol. 1992;87:1046-1050. asked whether these patients should be treated with a chemo- 34. Beyer KL, Marshall JB, Metzler MH, Poulter JS, Seger RM, Diaz-Arias AA. Squa- therapeutic regimen more suited for the squamous cell element. mous cell carcinoma of the pancreas: report of an unusual case and review of Unfortunately, these lesions are very unusual, and there are no the literature. Digest Dis Sci. 1992;37:312-318. series of patients treated with such an approach. Our sole survi- 35. O’Connor DS, Ruchman R. Adenosquamous carcinoma of the pancreas. N J Med. vor at this point has known residual disease but has survived nearly 1993;90:527-529. 9 months and he has been treated with gemcitabine and irradia- 36. Makiyama K, Takuma K, Zea-Iriarte W, et al. Adenosquamous carcinoma of the tion. I am not sure of this agent’s efficacy with squamous cell tu- pancreas. J Gastroent. 1995;30:798-802. mors, but it does have some advantage in adenocarcinomas. I think your concept may be correct and in the future, we might change DISCUSSION our adjuvant therapeutic approach. You asked if we had diagnosed any of these lesions ahead Gerard V. Aranha, MD, Maywood, Ill: Dr Madura has pre- of time, and, with the exception of those patients arriving with sented us with 6 cases of adenosquamous carcinoma of the pan- previous biopsy, we do not attempt a preoperative aspiration creas, a very rare variant of the usual adenocarcinoma. There nor do we do any tissue sampling in the operating room. If the were 4 patients with head lesions and 2 with lesions in the body; lesion looks amenable to removal on preoperative assessment all were resected, but none survived more than 12 months, sug- and in the operating room, we go ahead with the resection. One gesting also a poorer prognosis than patients with adenocar- of these patients gave us no choice since her tumor had eroded cinoma. The pathology evaluation revealed that 5 of the 6 pa- into the duodenum and was bleeding. I do not think that a di- tients had peripancreatic or perineural invasion as well as lymph agnosis of adenosquamous carcinoma preoperatively would node metastasis and that 5 of the 6 had aneuploid tumors, all change our approach. It would give us an opportunity to in- harbingers of poor prognosis. As far as theories go, there are form the patient and their family about the prognosis, and per- many, but the one that makes the most sense is the one that haps allow us to stimulate our oncologic colleagues to con- you first alluded to—the one that says that there may be squa- sider a different postoperative regimen.

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