Substaging Nodal Status in Ampullary Carcinomas has Significant Prognostic Value: Proposed Revised Staging Based on an Analysis of 313 Well-Characterized Cases

Annals of Surgical Oncology

Volumn 22, Issue 13, 2015, Pages 4392-4401

  Balci, Serdar ^a   Basturk, Olca ^b   Saka, Burcu ^c   Bagci, Pelin ^a   Postlewait, Lauren M ^a   Tajiri, Takuma ^d   Jang, Kee Taek ^e   Ohike, Nobuyuki ^f   Kim, Grace E ^g   Krasinskas, Alyssa ^a   Choi, Hyejeong ^e   Sarmiento, Juan M ^h   Kooby, David A ^a   El Rayes, Bassel F ^h   Knight, Jessica H ^h   Goodman, Michael ^h   Akkas, Gizem ^a   Reid, Michelle D ^a   Maithel, Shishir K ^a   Adsay, Volkan ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c ISTANBUL MEDIPOL UNIVERSITY   (Turkey)

^d TOKAI UNIVERSITY HACHIOJI HOSPITAL   (Japan)

^e Sungkyunkwan University School of Medicine   (South Korea)

^f SHOWA UNIVERSITY FUJIGAOKA HOSPITAL   (Japan)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 20; CYTOKERATIN 7; MUCIN 1; MUCIN 2; MUCIN 5AC; TRANSCRIPTION FACTOR CDX2;

ADULT; AGED; ARTICLE; CANCER LOCALIZATION; CANCER PROGNOSIS; CANCER SIZE; CANCER STAGING; CANCER SURVIVAL; FEMALE; FOLLOW UP; HISTOPATHOLOGY; HUMAN; INTESTINE CARCINOMA; LYMPH NODE METASTASIS; LYMPH VESSEL METASTASIS; MAJOR CLINICAL STUDY; MALE; MULTICENTER STUDY (TOPIC); OVERALL SURVIVAL; PANCREATICODUODENECTOMY; PERINEURAL INVASION; PROTEIN EXPRESSION; SURVIVAL RATE; TUMOR INVASION; VATER PAPILLA ADENOCARCINOMA; VATER PAPILLA CARCINOMA; ADENOCARCINOMA; AMPULLA OF VATER; COMMON BILE DUCT NEOPLASMS; LYMPH NODE; MIDDLE AGED; MORTALITY; PANCREATIC NEOPLASMS; PATHOLOGY; PROGNOSIS; STANDARDS; VERY ELDERLY;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; AMPULLA OF VATER; COMMON BILE DUCT NEOPLASMS; FEMALE; FOLLOW-UP STUDIES; HUMANS; LYMPH NODES; MALE; MIDDLE AGED; NEOPLASM STAGING; PANCREATIC NEOPLASMS; PROGNOSIS; SURVIVAL RATE;

EID: 84947129027     PISSN: 10689265     EISSN: 15344681     Source Type: Journal    
DOI: 10.1245/s10434-015-4499-y     Document Type: Article

References (66)

1. Klimstra DS, Albores-Saavedra J, Hruban RH, Zamboni G. Tumours of the ampullary region. In: Bosman FT, Carneiro F, Hruban RH, Theise ND, eds. WHO classification of tumours of the digestive system. Lyon: International Agency for Research on Cancer (IARC); 2010. p. 81–94.
2. Adsay NV, Basturk O. Tumors of major and minor ampulla. In: Odze R, Goldblum J, eds. Surgical pathology of the GI tract, liver, biliary tract, and pancreas. Philadelphia: Elsevier; 2014. p. 1120–39.
3. Thompson LDR, Basturk O, Adsay NV. Pancreas. In: Mills SE, ed. Sternberg’s diagnostic surgical pathology. Philadelphia: Lippincott Williams & Wilkins; 2015. p. 1577–662.
4. Shi HY, Wang SN, Lee KT. Temporal trends and volume-outcome associations in periampullary cancer patients: a propensity score-adjusted nationwide population-based study. Am J Surg. 2014;207:512–19.
5. Bronsert P, Kohler I, Werner M, et al. Intestinal-type of differentiation predicts favourable overall survival: confirmatory clinicopathological analysis of 198 periampullary adenocarcinomas of pancreatic, biliary, ampullary and duodenal origin. BMC Cancer. 2013;13:428.
6. Kumari N, Prabha K, Singh RK, Baitha DK, Krishnani N. Intestinal and pancreatobiliary differentiation in periampullary carcinoma: the role of immunohistochemistry. Hum Pathol. 2013;44:2213–9.
7. Lee SR, Kim HO, Park YL, Shin JH. Lymph node ratio predicts local recurrence for periampullary tumours. ANZ J Surg. 2014;84:353–8.
8. Bornstein-Quevedo L, Gamboa-Dominguez A. Carcinoid tumors of the duodenum and ampulla of vater: a clinicomorphologic, immunohistochemical, and cell kinetic comparison. Hum Pathol. 2001;32:1252–6.
9. Gutierrez JC, Franceschi D, Koniaris LG. How many lymph nodes properly stage a periampullary malignancy? J Gastrointest Surg. 2008;12:77–85.
10. Kim K, Chie EK, Jang JY, et al. Prognostic significance of tumour location after adjuvant chemoradiotherapy for periampullary adenocarcinoma. Clin Transl Oncol. 2012;14:391–5.
11. Maithel SK, Khalili K, Dixon E, et al. Impact of regional lymph node evaluation in staging patients with periampullary tumors. Ann Surg Oncol. 2007;14:202–10.
12. Westgaard A, Pomianowska E, Clausen OP, Gladhaug IP. Intestinal-type and pancreatobiliary-type adenocarcinomas: how does ampullary carcinoma differ from other periampullary malignancies? Ann Surg Oncol. 2013;20:430–9.
13. Riall TS, Cameron JL, Lillemoe KD, et al. Resected periampullary adenocarcinoma: 5-year survivors and their 6- to 10-year follow-up. Surgery. 2006;140:764–72.
14. Ahn DH, Bekaii-Saab T. Ampullary cancer: an overview. Am Soc Clin Oncol Educ Book. 2014; 112–115.
15. Williams JA, Cubilla A, Maclean BJ, Fortner JG. Twenty-two year experience with periampullary carcinoma at Memorial Sloan-Kettering Cancer Center. Am J Surg. 1979;138:662–5.
16. Cubilla AL, Fitzgerald PJ. Surgical pathology aspects of cancer of the ampulla-head-of-pancreas region. Monogr Pathol. 1980;21:67–81.
17. Perysinakis I, Margaris I, Kouraklis G. Ampullary cancer: a separate clinical entity? Histopathology. 2014;64:759–68.
18. Washington K, Berlin J, Branton P; for the College of American Pathologists (CAP). Protocol for the examination of specimens from patients with carcinoma of the ampulla of Vater. 2012. Available at: http://www.cap.org/apps/docs/committees/cancer/cancer_protocols/2012/Ampulla_12protocol_3101.pdf. Accessed 24 Jan 2014.
19. Adsay V, Ohike N, Tajiri T, et al. Ampullary region carcinomas: definition and site specific classification with delineation of four clinicopathologically and prognostically distinct subsets in an analysis of 249 cases. Am J Surg Pathol. 2012;36:1592–608.
20. Ohike N, Kim GE, Tajiri T, et al. Intra-ampullary papillary-tubular neoplasm (IAPN): characterization of tumoral intraepithelial neoplasia occurring within the ampulla: a clinicopathologic analysis of 82 cases. Am J Surg Pathol. 2010;34:1731–48.
21. Tajiri T, Basturk O, Krasinskas A, et al. Prognostic differences between ampullary carcinomas and pancreatic ductal adenocarcinomas: the importance of size of invasive component [abstract]. Mod Pathol. 2009;22:323A.
22. Saka B, Tajiri T, Ohike N, et al. Clinicopathologic comparison of ampullary versus pancreatic carcinoma: preinvasive component, size of invasion, stage, resectability and histologic phenotype are the factors for the significantly favorable outcome of ampullary carcinoma [abstract]. Mod Pathol. 2013;26:429A.
23. Mori K, Ikei S, Yamane T, et al. Pathological factors influencing survival of carcinoma of the ampulla of Vater. Eur J Surg Oncol. 1990;16:183–8.
24. Shyr YM, Su CH, Wu LH, Li AF, Chiu JH, Lui WY. DNA ploidy as a major prognostic factor in resectable ampulla of Vater cancers. J Surg Oncol. 1993;53:220–5.
25. Woo SM, Ryu JK, Lee SH, et al. Recurrence and prognostic factors of ampullary carcinoma after radical resection: comparison with distal extrahepatic cholangiocarcinoma. Ann Surg Oncol. 2007;14:3195–201.
26. Zhou J, Zhang Q, Li P, Shan Y, Zhao D, Cai J. Prognostic factors of carcinoma of the ampulla of Vater after surgery. Tumour Biol. 2014;35(2):1143–8.
27. Kim WS, Choi DW, Choi SH, Heo JS, You DD, Lee HG. Clinical significance of pathologic subtype in curatively resected ampulla of vater cancer. J Surg Oncol. 2012;105:266–72.
28. Inoue Y, Hayashi M, Hirokawa F, Egashira Y, Tanigawa N. Clinicopathological and operative factors for prognosis of carcinoma of the ampulla of vater. Hepatogastroenterology. 2012;59:1573–6.
29. Kohler I, Jacob D, Budzies J, et al. Phenotypic and genotypic characterization of carcinomas of the papilla of Vater has prognostic and putative therapeutic implications. Am J Clin Pathol. 2011;135:202–11.
30. Ohike N, Coban I, Kim GE, et al. Tumor budding as a strong prognostic indicator in invasive ampullary adenocarcinomas. Am J Surg Pathol. 2010;34:1417–24.
31. Hsu HP, Shan YS, Jin YT, Lai MD, Lin PW. Loss of E-cadherin and beta-catenin is correlated with poor prognosis of ampullary neoplasms. J Surg Oncol. 2010;101:356–62.
32. de Paiva Haddad LB, Patzina RA, Penteado S, et al. Lymph node involvement and not the histophatologic subtype is correlated with outcome after resection of adenocarcinoma of the ampulla of vater. J Gastrointest Surg. 2010;14:719–28.
33. Lowe MC, Coban I, Adsay NV, et al. Important prognostic factors in adenocarcinoma of the ampulla of Vater. Am Surg. 2009;75:754–60; discussion 761.
34. Yao HS, Wang Q, Wang WJ, Hu ZQ. Intraoperative allogeneic red blood cell transfusion in ampullary cancer outcome after curative pancreatoduodenectomy: a clinical study and meta-analysis. World J Surg. 2008;32:2038–46.
35. Shimizu Y, Kimura F, Shimizu H, Yoshidome H, Ohtsuka M, Miyazaki M. The morbidity, mortality, and prognostic factors for ampullary carcinoma and distal cholangiocarcinoma. Hepatogastroenterology. 2008;55:699–703.
36. Qiao QL, Zhao YG, Ye ML, et al. Carcinoma of the ampulla of Vater: factors influencing long-term survival of 127 patients with resection. World J Surg. 2007;31:137–43; discussion 144-136.
37. Chen J, Cai S, Dong J. Predictors of recurrence after pancreaticoduodenectomy for carcinoma of the ampulla of Vater [in Chinese]. Nan Fang Yi Ke Da Xue Xue Bao 2012;32:1242–4.
38. Showalter TN, Zhan T, Anne PR, et al. The influence of prognostic factors and adjuvant chemoradiation on survival after pancreaticoduodenectomy for ampullary carcinoma. J Gastrointest Surg. 2011;15:1411–6.
39. Casaretto E, Andrada DG, Granero LE. Results of cephalic pancreaticoduodenectomy for ampullary carcinoma. Analysis of 18 consecutive cases [in Spanish]. Acta Gastroenterol Latinoam. 2010;40:22–31.
40. Sudo T, Murakami Y, Uemura K, et al. Prognostic impact of perineural invasion following pancreatoduodenectomy with lymphadenectomy for ampullary carcinoma. Dig Dis Sci. 2008;53:2281–6.
41. Barauskas G, Gulbinas A, Pranys D, Dambrauskas Z, Pundzius J. Tumor-related factors and patient’s age influence survival after resection for ampullary adenocarcinoma. J Hepatobiliary Pancreat Surg. 2008;15:423–8.
42. Sessa F, Furlan D, Zampatti C, Carnevali I, Franzi F, Capella C. Prognostic factors for ampullary adenocarcinomas: tumor stage, tumor histology, tumor location, immunohistochemistry and microsatellite instability. Virchows Arch. 2007;451:649–57.
43. Dahl S, Bendixen M, Fristrup CW, Mortensen MB. Treatment outcomes for patients with papilla of Vater cancer [in Danish]. Ugeskr Laeger. 2010;172:1361–5.
44. Pomianowska E, Westgaard A, Mathisen O, Clausen OP, Gladhaug IP. Prognostic relevance of number and ratio of metastatic lymph nodes in resected pancreatic, ampullary, and distal bile duct carcinomas. Ann Surg Oncol. 2013;20:233–41.
45. Roland CL, Katz MH, Gonzalez GM, et al. A high positive lymph node ratio is associated with distant recurrence after surgical resection of ampullary carcinoma. J Gastrointest Surg. 2012;16:2056–63.
46. Hurtuk MG, Hughes C, Shoup M, Aranha GV. Does lymph node ratio impact survival in resected periampullary malignancies? Am J Surg. 2009;197:348–52.
47. Zhou J, Zhang Q, Li P, Shan Y, Zhao D, Cai J. Prognostic relevance of number and ratio of metastatic lymph nodes in resected carcinoma of the ampulla of Vater. Chin J Cancer Res. 2013;25:735–42.
48. Falconi M, Crippa S, Dominguez I, et al. Prognostic relevance of lymph node ratio and number of resected nodes after curative resection of ampulla of Vater carcinoma. Ann Surg Oncol. 2008;15:3178–86.
49. Bogoevski D, Chayeb H, Cataldegirmen G, et al. Nodal microinvolvement in patients with carcinoma of the papilla of vater receiving no adjuvant chemotherapy. J Gastrointest Surg. 2008;12:1830–7; discussion 1837-1838.
50. van der Gaag NA, ten Kate FJ, Lagarde SM, Busch OR, van Gulik TM, Gouma DJ. Prognostic significance of extracapsular lymph node involvement in patients with adenocarcinoma of the ampulla of Vater. Br J Surg. 2008;95:735–43.
51. Hornick JR, Johnston FM, Simon PO, et al. A single-institution review of 157 patients presenting with benign and malignant tumors of the ampulla of Vater: management and outcomes. Surgery. 2011;150:169–76.
52. Shroff S, Overman MJ, Rashid A, et al. The expression of PTEN is associated with improved prognosis in patients with ampullary adenocarcinoma after pancreaticoduodenectomy. Arch Pathol Lab Med. 2013;137:1619–26.
53. Sakata J, Shirai Y, Wakai T, Ajioka Y, Akazawa K, Hatakeyama K. Assessment of the nodal status in ampullary carcinoma: the number of positive lymph nodes versus the lymph node ratio. World J Surg. 2011;35:2118–24.
54. Lee JH, Lee KG, Ha TK, et al. Pattern analysis of lymph node metastasis and the prognostic importance of number of metastatic nodes in ampullary adenocarcinoma. Am Surg. 2011;77:322–9.
55. Choi SB, Kim WB, Song TJ, Suh SO, Kim YC, Choi SY. Surgical outcomes and prognostic factors for ampulla of Vater cancer. Scand J Surg. 2011;100:92–8.
56. Sommerville CA, Limongelli P, Pai M, et al. Survival analysis after pancreatic resection for ampullary and pancreatic head carcinoma: an analysis of clinicopathological factors. J Surg Oncol. 2009;100:651–6.
57. Sierzega M, Nowak K, Kulig J, Matyja A, Nowak W, Popiela T. Lymph node involvement in ampullary cancer: the importance of the number, ratio, and location of metastatic nodes. J Surg Oncol. 2009;100:19–24.
58. Sakata J, Shirai Y, Wakai T, et al. Number of positive lymph nodes independently affects long-term survival after resection in patients with ampullary carcinoma. Eur J Surg Oncol. 2007;33:346–51.
59. Edge SB, American Joint Committee on Cancer. AJCC cancer staging manual. 7th ed. New York: Springer; 2010.
60. Kang HJ, Eo SH, Kim SC, et al. Increased number of metastatic lymph nodes in adenocarcinoma of the ampulla of Vater as a prognostic factor: a proposal of new nodal classification. Surgery. 2014;155(1):74–84.
61. Saka B, Bagci P, Krasinskas A, et al. Duodenal carcinomas of non-ampullary origin are significantly more aggressive than ampullary carcinomas. Mod Pathol. 2013;26:176A–177A.
62. Balci S, Kim GE, Ohike N, et al. Applicability and prognostic relevance of ampullary carcinoma histologic typing as pancreatobiliary versus intestinal [abstract]. Mod Pathol. 2010;23:350A.
63. Adsay NV, Basturk O, Altinel D, et al. The number of lymph nodes identified in a simple pancreatoduodenectomy specimen: comparison of conventional vs orange-peeling approach in pathologic assessment. Mod Pathol. 2009;22:107–12.
64. Adsay NV, Basturk O, Saka B, et al. Whipple made simple for surgical pathologists: orientation, dissection, and sampling of pancreaticoduodenectomy specimens for a more practical and accurate evaluation of pancreatic, distal common bile duct, and ampullary tumors. Am J Surg Pathol. 2014;38(4):480–93.
65. Pai RK, Beck AH, Mitchem J, et al. Pattern of lymph node involvement and prognosis in pancreatic adenocarcinoma: direct lymph node invasion has similar survival to node-negative disease. Am J Surg Pathol. 2011;35:228–34.
66. Partelli S, Crippa S, Capelli P, et al. Adequacy of lymph node retrieval for ampullary cancer and its association with improved staging and survival. World J Surg. 2013;37:1397–404.