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Published in: Journal of Gastrointestinal Surgery 4/2019

01-04-2019 | Neuroendocrine Tumor | Original Article

Natural History and Treatment Trends in Pancreatic Cancer Subtypes

Authors: Courtney J. Pokrzywa, Daniel E. Abbott, Kristina A. Matkowskyj, Sean M. Ronnekleiv-Kelly, Emily R. Winslow, Sharon M. Weber, Alexander V. Fisher

Published in: Journal of Gastrointestinal Surgery | Issue 4/2019

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Abstract

Background

While pancreatic ductal adenocarcinoma is the most common form of pancreatic cancer, many other histologic forms of pancreatic cancer are also recognized. These histologic variants portray unique characteristics in terms of patient demographics, tumor behavior, survival, and responsiveness to treatments.

Materials and Methods

Patients who underwent surgical resection of the pancreas for non-metastatic, invasive pancreatic cancer between 2004 and 2014 were selected from the National Cancer Data Base and categorized by histologic variant according to WHO classification guidelines. Patient demographics, tumor variables, treatment characteristics, and survival were compared between histologic groups and subgroups.

Results

A total of 57,804 patients met inclusion and exclusion criteria and were grouped into eight major histologic categories. Survival analysis by the histologic group showed median overall survival of 20.2 months for ductal adenocarcinoma, 20.5 months for squamous cell carcinoma, 26.8 months for mixed acinar-neuroendocrine carcinomas, 52.6 months for cystic mucinous neoplasms with an associated invasive carcinoma, 67.5 months for acinar cell carcinoma, and 69.3 months for mesenchymal tumors. Median survival was not reached for neuroendocrine tumors and solid-pseudopapillary neoplasms, with 5-year overall survival rates of 84% and 97% respectively.

Conclusions

Rare subtypes of pancreatic cancer present unique clinicopathologic characteristics and display distinct tumor biologies. This study presents data on demographic, prognostic, treatment, and survival outcomes between rare forms of pancreatic neoplasms in order to aid understanding of the natural history and behavior of these neoplasms, with the hope of serving as a reference in clinical decision-making and ability to provide accurate prognostic information to patients.
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Literature
1.
go back to reference Siegel R, Miller K, Jemal A. Cancer Statistics. Ca Cáncer J. 2017;67(1):7–30.CrossRef Siegel R, Miller K, Jemal A. Cancer Statistics. Ca Cáncer J. 2017;67(1):7–30.CrossRef
2.
go back to reference Paniccia A, Hosokawa P, Henderson W, Schulick RD, Edil BH, McCarter MD, Gajdos C. Characteristics of 10-year survivors of pancreatic ductal adenocarcinoma. JAMA Surg. 2015;150(8):701–710.CrossRefPubMed Paniccia A, Hosokawa P, Henderson W, Schulick RD, Edil BH, McCarter MD, Gajdos C. Characteristics of 10-year survivors of pancreatic ductal adenocarcinoma. JAMA Surg. 2015;150(8):701–710.CrossRefPubMed
3.
go back to reference Colbert LE, Hall WA, Nickleach D, Switchenko J, Kooby DA, Liu Y, Gillespie T, Lipscomb J, Kauh J, Landry JC. Chemoradiation therapy sequencing for resected pancreatic adenocarcinoma in the national cancer data base. Cancer. 2014;120(4):499–506.CrossRefPubMedPubMedCentral Colbert LE, Hall WA, Nickleach D, Switchenko J, Kooby DA, Liu Y, Gillespie T, Lipscomb J, Kauh J, Landry JC. Chemoradiation therapy sequencing for resected pancreatic adenocarcinoma in the national cancer data base. Cancer. 2014;120(4):499–506.CrossRefPubMedPubMedCentral
4.
go back to reference Åkerberg D, Ansari D, Andersson R. Re-evaluation of classical prognostic factors in resectable ductal adenocarcinoma of the pancreas. World J Gastroenterol. 2016;22(28):6424–6433.CrossRefPubMedPubMedCentral Åkerberg D, Ansari D, Andersson R. Re-evaluation of classical prognostic factors in resectable ductal adenocarcinoma of the pancreas. World J Gastroenterol. 2016;22(28):6424–6433.CrossRefPubMedPubMedCentral
5.
go back to reference Zhou J, Enewold L, Stojadinovic A, Clifton GT, Potter JF, Peoples GE, Zhu K. Incidence rates of exocrine and endocrine pancreatic cancers in the United States. Cancer Causes Control. 2010;21(6):853–861.CrossRefPubMed Zhou J, Enewold L, Stojadinovic A, Clifton GT, Potter JF, Peoples GE, Zhu K. Incidence rates of exocrine and endocrine pancreatic cancers in the United States. Cancer Causes Control. 2010;21(6):853–861.CrossRefPubMed
6.
go back to reference Fesinmeyer MD, Austin MA, Li CI, Roos AJ De, Bowen DJ. Differences in Survival by Histologic Type of Pancreatic Cancer Differences in Survival by Histologic Type of Pancreatic Cancer. 2005;14(July):1766–1773. Fesinmeyer MD, Austin MA, Li CI, Roos AJ De, Bowen DJ. Differences in Survival by Histologic Type of Pancreatic Cancer Differences in Survival by Histologic Type of Pancreatic Cancer. 2005;14(July):1766–1773.
7.
go back to reference Kloppel G, Solcia E, Longnecker DS, Capella C, Sobin LH. Histological Typing of Tumours of the Exocrine Pancreas. Vol 49.; 1996. Kloppel G, Solcia E, Longnecker DS, Capella C, Sobin LH. Histological Typing of Tumours of the Exocrine Pancreas. Vol 49.; 1996.
8.
go back to reference Paniccia A, Hosokawa PW, Schulick RD, Henderson W, Kaplan J, Gajdos C. A matched-cohort analysis of 192 pancreatic anaplastic carcinomas and 960 pancreatic adenocarcinomas: A 13-year North American experience using the National Cancer Data Base (NCDB). Surg (United States). 2016;160(2):281–292.PubMed Paniccia A, Hosokawa PW, Schulick RD, Henderson W, Kaplan J, Gajdos C. A matched-cohort analysis of 192 pancreatic anaplastic carcinomas and 960 pancreatic adenocarcinomas: A 13-year North American experience using the National Cancer Data Base (NCDB). Surg (United States). 2016;160(2):281–292.PubMed
9.
go back to reference Raigani S, Ammori J, Kim J, Hardacre JM. Trends in the Treatment of Resectable Pancreatic Adenocarcinoma. J Gastrointest Surg. 2014;18(1):113–123.CrossRefPubMed Raigani S, Ammori J, Kim J, Hardacre JM. Trends in the Treatment of Resectable Pancreatic Adenocarcinoma. J Gastrointest Surg. 2014;18(1):113–123.CrossRefPubMed
10.
go back to reference Youngwirth LM, Nussbaum DP, Thomas S, Adam MA, Blazer DG, Roman SA, Sosa JA. Nationwide trends and outcomes associated with neoadjuvant therapy in pancreatic cancer: An analysis of 18 243 patients. J Surg Oncol. 2017;116(2):127–132.CrossRefPubMed Youngwirth LM, Nussbaum DP, Thomas S, Adam MA, Blazer DG, Roman SA, Sosa JA. Nationwide trends and outcomes associated with neoadjuvant therapy in pancreatic cancer: An analysis of 18 243 patients. J Surg Oncol. 2017;116(2):127–132.CrossRefPubMed
11.
go back to reference Shubert CR, Bergquist JR, Groeschl RT, Habermann EB, Wilson PM, Truty MJ, Smoot RL, Kendrick ML, Nagorney DM, Farnell MB. Overall survival is increased among stage III pancreatic adenocarcinoma patients receiving neoadjuvant chemotherapy compared to surgery first and adjuvant chemotherapy: An intention to treat analysis of the National Cancer Database. Surg (United States). 2016;160(4):1080–1096.PubMed Shubert CR, Bergquist JR, Groeschl RT, Habermann EB, Wilson PM, Truty MJ, Smoot RL, Kendrick ML, Nagorney DM, Farnell MB. Overall survival is increased among stage III pancreatic adenocarcinoma patients receiving neoadjuvant chemotherapy compared to surgery first and adjuvant chemotherapy: An intention to treat analysis of the National Cancer Database. Surg (United States). 2016;160(4):1080–1096.PubMed
12.
go back to reference Bilimoria KY, Tomlinson JS, Merkow RP, Stewart AK, Ko CY, Talamonti MS, Bentrem DJ. Clinicopathologic features and treatment trends of pancreatic neuroendocrine tumors: Analysis of 9,821 patients. J Gastrointest Surg. 2007;11(11):1460–1469.CrossRefPubMed Bilimoria KY, Tomlinson JS, Merkow RP, Stewart AK, Ko CY, Talamonti MS, Bentrem DJ. Clinicopathologic features and treatment trends of pancreatic neuroendocrine tumors: Analysis of 9,821 patients. J Gastrointest Surg. 2007;11(11):1460–1469.CrossRefPubMed
13.
go back to reference Hill JS, McPhee JT, McDade TP, Zhou Z, Sullivan ME, Whalen GF, Tseng JF. Pancreatic neuroendocrine tumors. Cancer. 2009;115(4):741–751.CrossRefPubMed Hill JS, McPhee JT, McDade TP, Zhou Z, Sullivan ME, Whalen GF, Tseng JF. Pancreatic neuroendocrine tumors. Cancer. 2009;115(4):741–751.CrossRefPubMed
14.
go back to reference Roland CL, Bian A, Mansour JC, Yopp AC, Balch GC, Sharma R, Xie XJ, Schwarz RE. Survival impact of malignant pancreatic neuroendocrine and islet cell neoplasm phenotypes. J Surg Oncol. 2012;105(6):595–600.CrossRefPubMed Roland CL, Bian A, Mansour JC, Yopp AC, Balch GC, Sharma R, Xie XJ, Schwarz RE. Survival impact of malignant pancreatic neuroendocrine and islet cell neoplasm phenotypes. J Surg Oncol. 2012;105(6):595–600.CrossRefPubMed
15.
go back to reference Wisnoski NC, Townsend CM, Nealon WH, Freeman JL, Riall TS. 672 Patients With Acinar Cell Carcinoma of the Pancreas: a Population-Based Comparison To Pancreatic Adenocarcinoma. Surgery. 2008;144(2):141–148.CrossRefPubMed Wisnoski NC, Townsend CM, Nealon WH, Freeman JL, Riall TS. 672 Patients With Acinar Cell Carcinoma of the Pancreas: a Population-Based Comparison To Pancreatic Adenocarcinoma. Surgery. 2008;144(2):141–148.CrossRefPubMed
16.
go back to reference Stelow EB, Shaco-Levy R, Bao F, Garcia J, Klimstra DS. Pancreatic acinar cell carcinomas with prominent ductal differentiation: Mixed acinar ductal carcinoma and mixed acinar endocrine ductal carcinoma. Am J Surg Pathol. 2010;34(4):510–518.CrossRefPubMed Stelow EB, Shaco-Levy R, Bao F, Garcia J, Klimstra DS. Pancreatic acinar cell carcinomas with prominent ductal differentiation: Mixed acinar ductal carcinoma and mixed acinar endocrine ductal carcinoma. Am J Surg Pathol. 2010;34(4):510–518.CrossRefPubMed
17.
go back to reference Seth AK, Argani P, Campbell KA, Cameron JL, Pawlik TM, Schulick RD, Choti MA, Wolfgang CL. Acinar cell carcinoma of the pancreas: An institutional series of resected patients and review of the current literature. J Gastrointest Surg. 2008;12(6):1061–1067.CrossRefPubMed Seth AK, Argani P, Campbell KA, Cameron JL, Pawlik TM, Schulick RD, Choti MA, Wolfgang CL. Acinar cell carcinoma of the pancreas: An institutional series of resected patients and review of the current literature. J Gastrointest Surg. 2008;12(6):1061–1067.CrossRefPubMed
18.
go back to reference Schmidt CM, Matos JM, Bentrem DJ, Talamonti MS, Lillemoe KD, Bilimoria KY. Acinar cell carcinoma of the pancreas in the united states: Prognostic factors and comparison to ductal adenocarcinoma. J Gastrointest Surg. 2008;12(12):2078–2086.CrossRefPubMed Schmidt CM, Matos JM, Bentrem DJ, Talamonti MS, Lillemoe KD, Bilimoria KY. Acinar cell carcinoma of the pancreas in the united states: Prognostic factors and comparison to ductal adenocarcinoma. J Gastrointest Surg. 2008;12(12):2078–2086.CrossRefPubMed
19.
go back to reference Reddy RP, Smyrk TC, Zapiach M, Levy MJ, Pearson RK, Clain JE, Farnell MB, Sarr MG, Chari ST. Pancreatic mucinous cystic neoplasm defined by ovarian stroma: Demographics, clinical features, and prevalence of cancer. Clin Gastroenterol Hepatol. 2004;2(11):1026–1031.CrossRefPubMed Reddy RP, Smyrk TC, Zapiach M, Levy MJ, Pearson RK, Clain JE, Farnell MB, Sarr MG, Chari ST. Pancreatic mucinous cystic neoplasm defined by ovarian stroma: Demographics, clinical features, and prevalence of cancer. Clin Gastroenterol Hepatol. 2004;2(11):1026–1031.CrossRefPubMed
20.
go back to reference Crippa S, Salvia R, Warshaw AL, Domínguez I, Bassi C, Falconi M, Thayer SP, Zamboni G, Lauwers GY, Mino-Kenudson M, Capelli P, Pederzoli P, Del Castillo CF. Mucinous cystic neoplasm of the pancreas is not an aggressive entity: Lessons from 163 resected patients. Ann Surg. 2008;247(4):571–579.CrossRefPubMedPubMedCentral Crippa S, Salvia R, Warshaw AL, Domínguez I, Bassi C, Falconi M, Thayer SP, Zamboni G, Lauwers GY, Mino-Kenudson M, Capelli P, Pederzoli P, Del Castillo CF. Mucinous cystic neoplasm of the pancreas is not an aggressive entity: Lessons from 163 resected patients. Ann Surg. 2008;247(4):571–579.CrossRefPubMedPubMedCentral
21.
go back to reference D’Angelica M, Brennan MF, Suriawinata AA, Klimstra D, Conlon KC. Intraductal Papillary Mucinous Neoplasms of the Pancreas: An Analysis of Clinicopathologic Features and Outcome. Ann Surg. 2004;239(3):400–408.CrossRefPubMedPubMedCentral D’Angelica M, Brennan MF, Suriawinata AA, Klimstra D, Conlon KC. Intraductal Papillary Mucinous Neoplasms of the Pancreas: An Analysis of Clinicopathologic Features and Outcome. Ann Surg. 2004;239(3):400–408.CrossRefPubMedPubMedCentral
22.
go back to reference Gil E, Choi SH, Choi DW, Heo JS, Kim MJ. Mucinous cystic neoplasms of the pancreas with ovarian stroma. ANZ J Surg. 2013;83(12):985–990.CrossRefPubMed Gil E, Choi SH, Choi DW, Heo JS, Kim MJ. Mucinous cystic neoplasms of the pancreas with ovarian stroma. ANZ J Surg. 2013;83(12):985–990.CrossRefPubMed
23.
go back to reference Grützmann R, Niedergethmann M, Pilarsky C, Klöppel G, Saeger HD. Intraductal papillary mucinous tumors of the pancreas: biology, diagnosis, and treatment. Oncologist. 2010;15(12):1294–1309.CrossRefPubMedPubMedCentral Grützmann R, Niedergethmann M, Pilarsky C, Klöppel G, Saeger HD. Intraductal papillary mucinous tumors of the pancreas: biology, diagnosis, and treatment. Oncologist. 2010;15(12):1294–1309.CrossRefPubMedPubMedCentral
25.
go back to reference Nguyen D, Dawson D, Hines J, Reber H, Donahue TR. Mucinous Cystic Neoplasms of the Pancreas : Are We Overestimating Malignant Potential ? Am Surg. 2014;80:915–919.PubMed Nguyen D, Dawson D, Hines J, Reber H, Donahue TR. Mucinous Cystic Neoplasms of the Pancreas : Are We Overestimating Malignant Potential ? Am Surg. 2014;80:915–919.PubMed
26.
go back to reference Rodriguez JR, Salvia R, Crippa S, Warshaw AL, Bassi C, Falconi M, Thayer SP, Lauwers GY, Capelli P, Mino-Kenudson M, Razo O, McGrath D, Pederzoli P, Fernández-Del Castillo C. Branch-duct intraductal papillary mucinous neoplasms: observations in 145 patients who underwent resection. Gastroenterology. 2007;133(1):72–9; quiz 309-10.CrossRefPubMedPubMedCentral Rodriguez JR, Salvia R, Crippa S, Warshaw AL, Bassi C, Falconi M, Thayer SP, Lauwers GY, Capelli P, Mino-Kenudson M, Razo O, McGrath D, Pederzoli P, Fernández-Del Castillo C. Branch-duct intraductal papillary mucinous neoplasms: observations in 145 patients who underwent resection. Gastroenterology. 2007;133(1):72–9; quiz 309-10.CrossRefPubMedPubMedCentral
27.
go back to reference Tanaka M, Fernández-Del Castillo C, Adsay V, Chari S, Falconi M, Jang JY, Kimura W, Levy P, Pitman MB, Schmidt CM, Shimizu M, Wolfgang CL, Yamaguchi K, Yamao K. International consensus guidelines 2012 for the management of IPMN and MCN of the pancreas. Pancreatology. 2012;12(3):183–197.CrossRefPubMed Tanaka M, Fernández-Del Castillo C, Adsay V, Chari S, Falconi M, Jang JY, Kimura W, Levy P, Pitman MB, Schmidt CM, Shimizu M, Wolfgang CL, Yamaguchi K, Yamao K. International consensus guidelines 2012 for the management of IPMN and MCN of the pancreas. Pancreatology. 2012;12(3):183–197.CrossRefPubMed
28.
go back to reference Testini M, Gurrado A, Lissidini G, Venezia P, Greco L, Piccinni G. Management of mucinous cystic neoplasms of the pancreas. World J Gastroenterol. 2010;16(45):5682–5692.CrossRefPubMedPubMedCentral Testini M, Gurrado A, Lissidini G, Venezia P, Greco L, Piccinni G. Management of mucinous cystic neoplasms of the pancreas. World J Gastroenterol. 2010;16(45):5682–5692.CrossRefPubMedPubMedCentral
29.
go back to reference Wada K, Kozarek RA, Traverso LW, Cook DW. Outcomes following resection of invasive and noninvasive intraductal papillary mucinous neoplasms of the pancreas. Am J Surg. 2005;189(5 SPEC. ISS.):632–637.CrossRefPubMed Wada K, Kozarek RA, Traverso LW, Cook DW. Outcomes following resection of invasive and noninvasive intraductal papillary mucinous neoplasms of the pancreas. Am J Surg. 2005;189(5 SPEC. ISS.):632–637.CrossRefPubMed
30.
go back to reference Brown H a, Dotto J, Robert M, Salem RR. Squamous Cell Carcinoma of the Pancreas. 2005;39(10):915–919. Brown H a, Dotto J, Robert M, Salem RR. Squamous Cell Carcinoma of the Pancreas. 2005;39(10):915–919.
31.
go back to reference Baylor SM, Berg JW. Cross-classification and survival characteristics of 5,000 cases of cancer of the pancreas. J Surg Oncol. 1973;5(4):335–358.CrossRefPubMed Baylor SM, Berg JW. Cross-classification and survival characteristics of 5,000 cases of cancer of the pancreas. J Surg Oncol. 1973;5(4):335–358.CrossRefPubMed
32.
go back to reference Nakashima H, Hayakawa T, Hoshino M, Kamiya Y, Ohara H, Yamada T, Mizuno K, Inagaki T, Nakazawa T, Yamada H, et al. Squamous cell carcinoma of the pancreas with massive invasion of the retroperitoneum. Intern Med. 1995;34(1):61–64.CrossRefPubMed Nakashima H, Hayakawa T, Hoshino M, Kamiya Y, Ohara H, Yamada T, Mizuno K, Inagaki T, Nakazawa T, Yamada H, et al. Squamous cell carcinoma of the pancreas with massive invasion of the retroperitoneum. Intern Med. 1995;34(1):61–64.CrossRefPubMed
33.
go back to reference Kodavatiganti R, Campbell F, Hashmi A, Gollins SW. Primary squamous cell carcinoma of the pancreas: A case report and review of the literature. J Med Case Rep. 2012;6(1):1. Journal of Medical Case Reports.CrossRef Kodavatiganti R, Campbell F, Hashmi A, Gollins SW. Primary squamous cell carcinoma of the pancreas: A case report and review of the literature. J Med Case Rep. 2012;6(1):1. Journal of Medical Case Reports.CrossRef
34.
go back to reference Ntanasis-Stathopoulos I, Tsilimigras DI, Georgiadou D, Kanavidis P, Riccioni O, Salla C, Psaltopoulou T, Sergentanis TN. Squamous cell carcinoma of the pancreas: A systematic review and pooled survival analysis. Eur J Cancer. 2017;79(2017):193–204.CrossRefPubMed Ntanasis-Stathopoulos I, Tsilimigras DI, Georgiadou D, Kanavidis P, Riccioni O, Salla C, Psaltopoulou T, Sergentanis TN. Squamous cell carcinoma of the pancreas: A systematic review and pooled survival analysis. Eur J Cancer. 2017;79(2017):193–204.CrossRefPubMed
37.
go back to reference Kim JY, Song JS, Park H, Byun JH, Song K, Hong S. Primary Mesenchymal Tumors of the Pancreas. 2014;43(6):959–968. Kim JY, Song JS, Park H, Byun JH, Song K, Hong S. Primary Mesenchymal Tumors of the Pancreas. 2014;43(6):959–968.
38.
go back to reference Dai G, Huang L, Du Y, Yang L, Yu P. Solid pseudopapillary neoplasms of the pancreas : clinical analysis of 45 cases. 2015;8(9):11400–11406. Dai G, Huang L, Du Y, Yang L, Yu P. Solid pseudopapillary neoplasms of the pancreas : clinical analysis of 45 cases. 2015;8(9):11400–11406.
39.
go back to reference Yang F, Jin C, Long J, Yu XJ, Xu J, Di Y, Li J, Fu DL, Ni QX. Solid pseudopapillary tumor of the pancreas: a case series of 26 consecutive patients. Am J Surg. 2009;198(2):210–215.CrossRefPubMed Yang F, Jin C, Long J, Yu XJ, Xu J, Di Y, Li J, Fu DL, Ni QX. Solid pseudopapillary tumor of the pancreas: a case series of 26 consecutive patients. Am J Surg. 2009;198(2):210–215.CrossRefPubMed
40.
go back to reference Shuja A, Alkimawi K a. Solid pseudopapillary tumor: a rare neoplasm of the pancreas. Gastroenterol Rep. 2014;2(2):145–149.CrossRef Shuja A, Alkimawi K a. Solid pseudopapillary tumor: a rare neoplasm of the pancreas. Gastroenterol Rep. 2014;2(2):145–149.CrossRef
41.
go back to reference Chang MK, Kyung SK, Jin SC, Kim H, Woo JL, Byong RK. Solid pseudopapillary tumor of the pancreas suggesting malignant potential. Pancreas. 2006;32(3):276–280.CrossRef Chang MK, Kyung SK, Jin SC, Kim H, Woo JL, Byong RK. Solid pseudopapillary tumor of the pancreas suggesting malignant potential. Pancreas. 2006;32(3):276–280.CrossRef
42.
go back to reference de Castro SM, Singhal D, Aronson DC, Busch OR, van Gulik TM, Obertop H, Gouma DJ. Management of solid-pseudopapillary neoplasms of the pancreas: a comparison with standard pancreatic neoplasms. World J Surg. 2007;31(5):1130–1135.CrossRefPubMedPubMedCentral de Castro SM, Singhal D, Aronson DC, Busch OR, van Gulik TM, Obertop H, Gouma DJ. Management of solid-pseudopapillary neoplasms of the pancreas: a comparison with standard pancreatic neoplasms. World J Surg. 2007;31(5):1130–1135.CrossRefPubMedPubMedCentral
43.
go back to reference Yachida S, Vakiani E, White CM, Zhong Y, Saunders T, Morgan R, de Wilde RF, Maitra A, Hicks J, DeMarzo AM, Shi C, Sharma R, Laheru D, Edil BH, Wolfgang CL, Schulick RD, Hruban RH, Tang LH, Klimstra DS, Iacobuzio-Donahue CA. Small Cell and Large Cell Neuroendocrine Carcinomas of the Pancreas Are Genetically Similar and Distinct from Well- differentiated Pancreatic Neuroendocrine Tumors. Am J Surg Pathol. 2012;36(2):173–184.CrossRefPubMedPubMedCentral Yachida S, Vakiani E, White CM, Zhong Y, Saunders T, Morgan R, de Wilde RF, Maitra A, Hicks J, DeMarzo AM, Shi C, Sharma R, Laheru D, Edil BH, Wolfgang CL, Schulick RD, Hruban RH, Tang LH, Klimstra DS, Iacobuzio-Donahue CA. Small Cell and Large Cell Neuroendocrine Carcinomas of the Pancreas Are Genetically Similar and Distinct from Well- differentiated Pancreatic Neuroendocrine Tumors. Am J Surg Pathol. 2012;36(2):173–184.CrossRefPubMedPubMedCentral
44.
go back to reference Goh BKP, Tan YM, Cheow PC, Chung YFA, Chow PKH, Wong WK, Ooi LLPJ. Solid pseudopapillary neoplasms of the pancreas: An updated experience. Journal of Surgical Oncology. Vol 95. ; 2007:640–644.CrossRefPubMed Goh BKP, Tan YM, Cheow PC, Chung YFA, Chow PKH, Wong WK, Ooi LLPJ. Solid pseudopapillary neoplasms of the pancreas: An updated experience. Journal of Surgical Oncology. Vol 95. ; 2007:640–644.CrossRefPubMed
45.
go back to reference Ohike N, Kosmahl M, Klöppel G. Mixed acinar-endocrine carcinoma of the pancreas. A clinicopathological study and comparison with acinar-cell carcinoma. Virchows Arch. 2004;445(3):231–235.CrossRefPubMed Ohike N, Kosmahl M, Klöppel G. Mixed acinar-endocrine carcinoma of the pancreas. A clinicopathological study and comparison with acinar-cell carcinoma. Virchows Arch. 2004;445(3):231–235.CrossRefPubMed
46.
go back to reference Ogbonna OH, Garcon MC, Syrigos KN, Saif MW. Mixed acinar-neuroendocrine carcinoma of the pancreas with neuroendocrine predominance. Case Rep Med. 2013;2013(grade 3):10–13. Ogbonna OH, Garcon MC, Syrigos KN, Saif MW. Mixed acinar-neuroendocrine carcinoma of the pancreas with neuroendocrine predominance. Case Rep Med. 2013;2013(grade 3):10–13.
47.
go back to reference Klimstra DS, Rosai J, Heffess CS. Mixed acinar-endocrine carcinomas of the pancreas. Am J Surg Pathol. 1994;18(8):765–778.CrossRefPubMed Klimstra DS, Rosai J, Heffess CS. Mixed acinar-endocrine carcinomas of the pancreas. Am J Surg Pathol. 1994;18(8):765–778.CrossRefPubMed
48.
go back to reference Kyriazi MA, Arkadopoulos N, Stafyla VK, Yiallourou AI, Dafnios N, Theodosopoulos T, Kairi-Vassilatou E, Smyrniotis V. Mixed acinar-endocrine carcinoma of the pancreas: A case report and review of the literature. Cases J. 2009;2(4):1–5. Kyriazi MA, Arkadopoulos N, Stafyla VK, Yiallourou AI, Dafnios N, Theodosopoulos T, Kairi-Vassilatou E, Smyrniotis V. Mixed acinar-endocrine carcinoma of the pancreas: A case report and review of the literature. Cases J. 2009;2(4):1–5.
49.
go back to reference Boman FT, Carneiro F, Hruban RH TN. WHO Classification of Tumours of the Digestive System, 4th edn. Fr IARC. 2010. Boman FT, Carneiro F, Hruban RH TN. WHO Classification of Tumours of the Digestive System, 4th edn. Fr IARC. 2010.
50.
go back to reference Ferrone CR, Pieretti-Vanmarcke R, Bloom JP, Zheng H, Szymonifka J, Wargo JA, Thayer SP, Lauwers GY, Deshpande V, Mino-Kenudson M, Fernández-del Castillo C, Lillemoe KD, Warshaw AL. Pancreatic ductal adenocarcinoma: long-term survival does not equal cure. Surgery. 2012;152(3 Suppl 1):S43–9.CrossRefPubMedPubMedCentral Ferrone CR, Pieretti-Vanmarcke R, Bloom JP, Zheng H, Szymonifka J, Wargo JA, Thayer SP, Lauwers GY, Deshpande V, Mino-Kenudson M, Fernández-del Castillo C, Lillemoe KD, Warshaw AL. Pancreatic ductal adenocarcinoma: long-term survival does not equal cure. Surgery. 2012;152(3 Suppl 1):S43–9.CrossRefPubMedPubMedCentral
51.
go back to reference Wagner M, Redaelli C, Lietz M, Seiler CA, Friess H, Büchler MW. Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. Br J Surg. 2004;91(5):586–594.CrossRefPubMed Wagner M, Redaelli C, Lietz M, Seiler CA, Friess H, Büchler MW. Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. Br J Surg. 2004;91(5):586–594.CrossRefPubMed
52.
go back to reference Raut CP, Tseng JF, Sun CC, Wang H, Wolff RA, Crane CH, Hwang R, Vauthey JN, Abdalla EK, Lee JE, Pisters PWT, Evans DB. Impact of resection status on pattern of failure and survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Ann Surg. 2007;246(1):52–60.CrossRefPubMedPubMedCentral Raut CP, Tseng JF, Sun CC, Wang H, Wolff RA, Crane CH, Hwang R, Vauthey JN, Abdalla EK, Lee JE, Pisters PWT, Evans DB. Impact of resection status on pattern of failure and survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Ann Surg. 2007;246(1):52–60.CrossRefPubMedPubMedCentral
53.
go back to reference Ferrone CR, Brennan MF, Gonen M, Coit DG, Fong Y, Chung S, Tang L, Klimstra D, Allen PJ. Pancreatic adenocarcinoma: The actual 5-year survivors. J Gastrointest Surg. 2008;12(4):701–706.CrossRefPubMed Ferrone CR, Brennan MF, Gonen M, Coit DG, Fong Y, Chung S, Tang L, Klimstra D, Allen PJ. Pancreatic adenocarcinoma: The actual 5-year survivors. J Gastrointest Surg. 2008;12(4):701–706.CrossRefPubMed
54.
go back to reference Sho M, Murakami Y, Motoi F, Satoi S, Matsumoto I, Kawai M, Honda G, Uemura K, Yanagimoto H, Kurata M, Fukumoto T, Akahori T, Kinoshita S, Nagai M, Nishiwada S, Unno M, Yamaue H, Nakajima Y. Postoperative prognosis of pancreatic cancer with para-aortic lymph node metastasis: A multicenter study on 822 patients. J Gastroenterol. 2015;50(6):694–702.CrossRefPubMed Sho M, Murakami Y, Motoi F, Satoi S, Matsumoto I, Kawai M, Honda G, Uemura K, Yanagimoto H, Kurata M, Fukumoto T, Akahori T, Kinoshita S, Nagai M, Nishiwada S, Unno M, Yamaue H, Nakajima Y. Postoperative prognosis of pancreatic cancer with para-aortic lymph node metastasis: A multicenter study on 822 patients. J Gastroenterol. 2015;50(6):694–702.CrossRefPubMed
55.
go back to reference Ahmad N a, Lewis JD, Ginsberg GG, Haller DG, Morris JB, Williams NN, Rosato EF, Kochman ML. Long term survival after pancreatic resection for pancreatic adenocarcinoma. Am J Gastroenterol. 2001;96(9):2609–2615.CrossRef Ahmad N a, Lewis JD, Ginsberg GG, Haller DG, Morris JB, Williams NN, Rosato EF, Kochman ML. Long term survival after pancreatic resection for pancreatic adenocarcinoma. Am J Gastroenterol. 2001;96(9):2609–2615.CrossRef
56.
go back to reference Cleary SP, Gryfe R, Guindi M, Greig P, Smith L, MacKenzie R, Strasberg S, Hanna S, Taylor B, Langer B, Gallinger S. Prognostic factors in resected pancreatic adenocarcinoma: Analysis of actual 5-year survivors. J Am Coll Surg. 2004;198(5):722–731.CrossRefPubMed Cleary SP, Gryfe R, Guindi M, Greig P, Smith L, MacKenzie R, Strasberg S, Hanna S, Taylor B, Langer B, Gallinger S. Prognostic factors in resected pancreatic adenocarcinoma: Analysis of actual 5-year survivors. J Am Coll Surg. 2004;198(5):722–731.CrossRefPubMed
57.
go back to reference Rutter CE, Park HS, Corso CD, Lester-Coll NH, Mancini BR, Yeboa DN, Johung KL. Addition of radiotherapy to adjuvant chemotherapy is associated with improved overall survival in resected pancreatic adenocarcinoma: An analysis of the National Cancer Data Base. Cancer. 2015;121(23):4141–4149.CrossRefPubMed Rutter CE, Park HS, Corso CD, Lester-Coll NH, Mancini BR, Yeboa DN, Johung KL. Addition of radiotherapy to adjuvant chemotherapy is associated with improved overall survival in resected pancreatic adenocarcinoma: An analysis of the National Cancer Data Base. Cancer. 2015;121(23):4141–4149.CrossRefPubMed
58.
go back to reference Yeo CJ, Abrams RA, Grochow LB, Sohn TA, Ord SE, Hruban RH, Zahurak ML, Dooley WC, Coleman JA, Sauter PK, Pitt HA, Lilltemoe KD, Cameron JL. Pancreaticoduodenectomy for pancreatic adenocarcinoma: Postoperative adjuvant chemoradiation improves survival: A prospective, single-institution experience. Ann Surg. 1997;225(5):621–636.CrossRefPubMedPubMedCentral Yeo CJ, Abrams RA, Grochow LB, Sohn TA, Ord SE, Hruban RH, Zahurak ML, Dooley WC, Coleman JA, Sauter PK, Pitt HA, Lilltemoe KD, Cameron JL. Pancreaticoduodenectomy for pancreatic adenocarcinoma: Postoperative adjuvant chemoradiation improves survival: A prospective, single-institution experience. Ann Surg. 1997;225(5):621–636.CrossRefPubMedPubMedCentral
59.
go back to reference Nitecki SS, Sarr MG, Colby T V, van Heerden JA. Long-term survival after resection for ductal adenocarcinoma of the pancreas. Is it really improving? Ann Surg. 1995;221(1):59–66.CrossRefPubMedPubMedCentral Nitecki SS, Sarr MG, Colby T V, van Heerden JA. Long-term survival after resection for ductal adenocarcinoma of the pancreas. Is it really improving? Ann Surg. 1995;221(1):59–66.CrossRefPubMedPubMedCentral
60.
go back to reference Schnelldorfer T, Ware AL, Sarr MG, Smyrk TC, Zhang L, Qin R, Gullerud RE, Donohue JH, Nagorney DM, Farnell MB. Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma is cure possible? Ann Surg. 2008;247(3):456–462.CrossRefPubMed Schnelldorfer T, Ware AL, Sarr MG, Smyrk TC, Zhang L, Qin R, Gullerud RE, Donohue JH, Nagorney DM, Farnell MB. Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma is cure possible? Ann Surg. 2008;247(3):456–462.CrossRefPubMed
61.
go back to reference Donahue TR, Reber HA. Surgical management of pancreatic cancer - Pancreaticoduodenectomy. Semin Oncol. 2015;42(1):98–109.CrossRefPubMed Donahue TR, Reber HA. Surgical management of pancreatic cancer - Pancreaticoduodenectomy. Semin Oncol. 2015;42(1):98–109.CrossRefPubMed
62.
go back to reference Kuhlmann KFD, De Castro SMM, Wesseling JG, Ten Kate FJW, Offerhaus GJA, Busch ORC, Van Gulik TM, Obertop H, Gouma DJ. Surgical treatment of pancreatic adenocarcinoma: Actual survival and prognostic factors in 343 patients. Eur J Cancer. 2004;40(4):549–558.CrossRefPubMed Kuhlmann KFD, De Castro SMM, Wesseling JG, Ten Kate FJW, Offerhaus GJA, Busch ORC, Van Gulik TM, Obertop H, Gouma DJ. Surgical treatment of pancreatic adenocarcinoma: Actual survival and prognostic factors in 343 patients. Eur J Cancer. 2004;40(4):549–558.CrossRefPubMed
63.
go back to reference Liu Z, Dong C, Wang C, Liu Q, Sun D, Wang L. Mixed acinar-endocrine carcinoma of pancreas: A case report and brief review of the literature. Onco Targets Ther. 2015;8:1633–1642.CrossRefPubMedPubMedCentral Liu Z, Dong C, Wang C, Liu Q, Sun D, Wang L. Mixed acinar-endocrine carcinoma of pancreas: A case report and brief review of the literature. Onco Targets Ther. 2015;8:1633–1642.CrossRefPubMedPubMedCentral
64.
go back to reference Boyd CA, Benarroch-Gampel J, Sheffield KM, Cooksley CD, Riall TS. 415 patients with adenosquamous carcinoma of the pancreas: A population-based analysis of prognosis and survival. J Surg Res. 2012;174(1):12–19.CrossRefPubMed Boyd CA, Benarroch-Gampel J, Sheffield KM, Cooksley CD, Riall TS. 415 patients with adenosquamous carcinoma of the pancreas: A population-based analysis of prognosis and survival. J Surg Res. 2012;174(1):12–19.CrossRefPubMed
65.
go back to reference Imaoka H, Shimizu Y, Mizuno N, Hara K, Hijioka S, Tajika M, Kondo S, Tanaka T, Ogura T, Obayashi T, Hasegawa T, Niwa Y, Yamao K. Clinical characteristics of adenosquamous carcinoma of the pancreas: A matched case-control study. Pancreas. 2014;43(2):287–290.CrossRefPubMed Imaoka H, Shimizu Y, Mizuno N, Hara K, Hijioka S, Tajika M, Kondo S, Tanaka T, Ogura T, Obayashi T, Hasegawa T, Niwa Y, Yamao K. Clinical characteristics of adenosquamous carcinoma of the pancreas: A matched case-control study. Pancreas. 2014;43(2):287–290.CrossRefPubMed
66.
go back to reference Clancy TE. Surgical Management of Pancreatic Neuroendocrine Tumors. Hematol Oncol Clin North Am. 2016;30(1):103–118.CrossRefPubMed Clancy TE. Surgical Management of Pancreatic Neuroendocrine Tumors. Hematol Oncol Clin North Am. 2016;30(1):103–118.CrossRefPubMed
67.
go back to reference Reid MD, Balci S, Saka B, Adsay NV. Neuroendocrine tumors of the pancreas: Current concepts and controversies. Endocr Pathol. 2014;25(1):65–79.CrossRefPubMed Reid MD, Balci S, Saka B, Adsay NV. Neuroendocrine tumors of the pancreas: Current concepts and controversies. Endocr Pathol. 2014;25(1):65–79.CrossRefPubMed
68.
go back to reference Wang Y, Wang S, Zhou X, Zhou H, Cui Y, Li Q, Zhang L. Acinar cell carcinoma: A report of 19 cases with a brief review of the literature. World J Surg Oncol. 2016;14(1):1–8.CrossRef Wang Y, Wang S, Zhou X, Zhou H, Cui Y, Li Q, Zhang L. Acinar cell carcinoma: A report of 19 cases with a brief review of the literature. World J Surg Oncol. 2016;14(1):1–8.CrossRef
69.
go back to reference Matos JM, Schmidt CM, Turrini O, Agaram NP, Niedergethmann M, Saeger HD, Merchant N, Johnson CS, Lillemoe KD, Grützmann R. Pancreatic acinar cell carcinoma: A multi-institutional study. J Gastrointest Surg. 2009;13(8):1495–1502.CrossRefPubMed Matos JM, Schmidt CM, Turrini O, Agaram NP, Niedergethmann M, Saeger HD, Merchant N, Johnson CS, Lillemoe KD, Grützmann R. Pancreatic acinar cell carcinoma: A multi-institutional study. J Gastrointest Surg. 2009;13(8):1495–1502.CrossRefPubMed
70.
go back to reference Lowery MA, Klimstra DS, Shia J, Yu KH, Allen PJ, Brennan MF, O’Reilly EM. Acinar Cell Carcinoma of the Pancreas: New Genetic and Treatment Insights into a Rare Malignancy. Oncologist. 2011;16(12):1714–1720.CrossRefPubMedPubMedCentral Lowery MA, Klimstra DS, Shia J, Yu KH, Allen PJ, Brennan MF, O’Reilly EM. Acinar Cell Carcinoma of the Pancreas: New Genetic and Treatment Insights into a Rare Malignancy. Oncologist. 2011;16(12):1714–1720.CrossRefPubMedPubMedCentral
71.
go back to reference Boffa DJ, Rosen JE, Mallin K, Loomis A, Gay G, Palis B, Thoburn K, Gress D, McKellar DP, Shulman LN, Facktor MA, Winchester DP. Using the National Cancer Database for Outcomes Research. JAMA Oncol. 2017. Boffa DJ, Rosen JE, Mallin K, Loomis A, Gay G, Palis B, Thoburn K, Gress D, McKellar DP, Shulman LN, Facktor MA, Winchester DP. Using the National Cancer Database for Outcomes Research. JAMA Oncol. 2017.
72.
go back to reference Lerro CC, Robbins AS, Phillips JL, Stewart AK. Comparison of cases captured in the national cancer data base with those in population-based central cancer registries. Ann Surg Oncol. 2013. Lerro CC, Robbins AS, Phillips JL, Stewart AK. Comparison of cases captured in the national cancer data base with those in population-based central cancer registries. Ann Surg Oncol. 2013.
Metadata
Title
Natural History and Treatment Trends in Pancreatic Cancer Subtypes
Authors
Courtney J. Pokrzywa
Daniel E. Abbott
Kristina A. Matkowskyj
Sean M. Ronnekleiv-Kelly
Emily R. Winslow
Sharon M. Weber
Alexander V. Fisher
Publication date
01-04-2019
Publisher
Springer US
Published in
Journal of Gastrointestinal Surgery / Issue 4/2019
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI
https://doi.org/10.1007/s11605-019-04113-3

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