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High risk factors of pancreatic carcinoma

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Summary

Over the past decades, cancer has become one of the toughest challenges for health professionals. The epidemiologists are increasingly directing their research efforts on various malignant tumor worldwide. Of note, incidence of cancers is on the rise more quickly in developed countries. Indeed, great endeavors have to be made in the control of the life-threatening disease. As we know it, pancreatic cancer (PC) is a malignant disease with the worst prognosis. While little is known about the etiology of the PC and measures to prevent the condition, so far, a number of risk factors have been identified. Genetic factors, pre-malignant lesions, predisposing diseases and exogenous factors have been found to be linked to PC. Genetic susceptibility was observed in 10% of PC cases, including inherited PC syndromes and familial PC. However, in the remaining 90%, their PC might be caused by genetic factors in combination with environmental factors. Nonetheless, the exact mechanism of the two kinds of factors, endogenous and exogenous, working together to cause PC remains poorly understood. The fact that most pancreatic neoplasms are diagnosed at an incurable stage of the disease highlights the need to identify risk factors and to understand their contribution to carcinogenesis. This article reviews the high risk factors contributing to the development of PC, to provide information for clinicians and epidemiologists.

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References

  1. American Cancer Society. Cancer facts & figures. The Society, 2014(www.cancer.org)

  2. Anderson KE, Mack TM, Silverman DT. Cancer of the pancreas. Cancer epidemiology and prevention, 3rd edd. New York Oxford: University Press, 2006: 721–763.

    Chapter  Google Scholar 

  3. Seicean A, Seicean T. Risk factors in pancreatic cancer. INTECH Open Access Publisher, 2012.

    Book  Google Scholar 

  4. Mayerle J, Simon P, Lerch MM. Pancreatitis and exogenous risk factors for pancreatic cancer. Exocrine pancreas, cancer. 30. Online, website: (http://www.cancer.org/cancer/pancreaticcancer/detailedg uide/pancreatic-cancer-risk-factors)

  5. Ghadirian P, Boyle P, Simard A, et al. Reported family aggregation of pancreatic cancer within a population-based case-control study in the Francophone community in Montreal, Canada. Int J Pancreatol, 1991, 10(3-4): 183–196

    CAS  PubMed  Google Scholar 

  6. Falk RT, Pickle LW, Fontham ET, et al. Life-style risk factors for pancreatic cancer in Louisiana: a case-control study. Am J Epidemiol, 1988, 128(2): 324–336

    CAS  PubMed  Google Scholar 

  7. Fernandez E, La Vecchia C, D'Avanzo B, et al. Family history and the risk of liver, gallbladder, and pancreatic cancer. Cancer Epidemiol Biomarkers Prev, 1994, 3(3): 209–212

    CAS  PubMed  Google Scholar 

  8. Silverman DT, Schiffman M, Everhart J, et al. Diabetes mellitus, other medical conditions and familial history of cancer as risk factors for pancreatic cancer. Brit J Cancer, 1999, 80(11): 1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Goldstein AM, Fraser MC, Struewing JP, et al. Increased risk of pancreatic cancer in melanoma-prone kindreds with p16 INK4 mutations. N England J Med, 1995, 333(15): 970–975

    Article  CAS  Google Scholar 

  10. Whelan AJ, Bartsch D, Goodfellow PJ. A familial syndrome of pancreatic cancer and melanoma with a mutation in the CDKN2 tumor-suppressor gene. N England J Med, 1995, 333(15): 975–977

    Article  CAS  Google Scholar 

  11. Borg Å, Sandberg T, Nilsson K, et al. High frequency of multiple melanomas and breast and pancreas carcinomas in CDKN2A mutation-positive melanoma families. J Natl Cancer Inst, 2000, 92(15): 1260–1266

    Article  CAS  PubMed  Google Scholar 

  12. Goldstein AM, Struewing JP, Chidambaram A, et al. Genotype-phenotype relationships in US melanoma-prone families with CDKN2A and CDK4 mutations. J Natl Cancer Inst, 2000, 92(12): 1006–1010

    Article  CAS  PubMed  Google Scholar 

  13. Vasen HF, Gruis NA, Frants RR, et al. Risk of developing pancreatic cancer in families with familial atypical multiple mole melanoma associated with a specific 19 deletion of p16 (p16-Leiden). Int J Cancer, 2000, 87(6): 809–811

    Article  CAS  PubMed  Google Scholar 

  14. de Snoo FA, Bishop DT, Bergman W, et al. Increased risk of cancer other than melanoma in CDKN2A founder mutation (p16-Leiden)-positive melanoma families. Clin Cancer Res, 2008, 14(21): 7151–7157

    Article  PubMed  Google Scholar 

  15. Bhutani MS, Thosani N, Suzuki R, et al. Pancreatic cancer screening: what we do and do not know. Clin Gastroenterol Hepatol, 2013, 6(11): 731–733

    Article  Google Scholar 

  16. McWilliams RR, Bamlet WR, de Andrade M, et al. Polymorphic variants in hereditary pancreatic cancer genes are not associated with pancreatic cancer risk. Cancer Epidemiol Biomarkers Prev, 2009, 18(9): 2549–2552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ghiorzo P, Ciotti P, Mantelli M, et al Characterization of ligurian melanoma families and risk of occurrence of other neoplasia. Int J Cancer, 1999, 83(4): 441–448

    Article  CAS  PubMed  Google Scholar 

  18. Ciotti P, Strigini P, Bianchi-Scarrà G, et al. Familial melanoma and pancreatic cancer. N Engl J Med, 1996, 334: 469–470

    Article  CAS  PubMed  Google Scholar 

  19. Bartsch DK, Sina-Frey M, Lang S, et al. CDKN2A germline mutations in familial pancreatic cancer. Ann Surg, 2002, 236(6): 730

    Article  PubMed  PubMed Central  Google Scholar 

  20. Moskaluk CA, Hruban RH, Lietman A, et al. Novel germline p16 [sup] INK4 allele (Asp145Cys) in a family with multiple pancreatic carcinomas. Hum Mutat, 1998, 12(1): 70

    Article  CAS  PubMed  Google Scholar 

  21. Moore PS, Zamboni G, Falconi M, et al. A novel germline mutation, P48T, in the CDKN2A/p16 gene in a patient with pancreatic carcinoma. Human Mutation, 2000, 16(5): 447

    Article  CAS  PubMed  Google Scholar 

  22. Vasen HF, Wasser M, van Mil A, et al. Magnetic resonance imaging surveillance detects early-stage pancreatic cancer in carriers of a p16-Leiden mutation. Gastroenterology, 2011, 140(3): 850–856

    Article  CAS  PubMed  Google Scholar 

  23. Beggs AD, Latchford AR, Vasen HF, et al. Peutz–Jeghers syndrome: a systematic review and recommendations for management. Gut, 2010, 59(7): 975–986

    Article  CAS  PubMed  Google Scholar 

  24. Van Lier MG, Westerman AM, Wagner AY, et al. High cancer risk and increased mortality in patients with Peutz–Jeghers syndrome. Gut, 2011, 60(2): 141–147

    Article  PubMed  Google Scholar 

  25. Giardiello FM, Welsh SB, Hamilton SR, et al. Increased risk of cancer in the Peutz–Jeghers syndrome. N Engl J Med, 1987, 316(24): 1511–1514

    Article  CAS  PubMed  Google Scholar 

  26. Giardiello FM, Brensinger JD, Tersmette AC, et al. Very high risk of cancer in familial Peutz–Jeghers syndrome. Gastroenterology, 2000, 119(6): 1447–1453

    Article  CAS  PubMed  Google Scholar 

  27. Hearle N, Schumacher V, Menko FH, et al. Frequency and spectrum of cancers in the Peutz-Jeghers syndrome. Clin Cancer Res, 2006, 12(10): 3209–3215

    Article  CAS  PubMed  Google Scholar 

  28. Mehenni H, Resta N, Park JG, et al. Cancer risks in LKB1 germline mutation carriers. Gut, 2006, 55(7): 984–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. You YN, Wolff BG, Boardman LA, et al. Peutz-Jeghers syndrome: a study of long-term surgical morbidity and causes of mortality. Fam Cancer, 2010, 9(4): 609–616

    Article  PubMed  Google Scholar 

  30. Korsse SE, Harinck F, van Lier MG, et al. Pancreatic cancer risk in Peutz-Jeghers syndrome patients: a large cohort study and implications for surveillance. J Med Genet, 2013, 50(1): 59–64

    Article  CAS  PubMed  Google Scholar 

  31. Lowenfels AB, Maisonneuve P, Di Magno EPY, et al. Hereditary pancreatitis and the risk of pancreatic cancer. J Natl Cancer Inst, 1997, 89(6): 442–446

    Article  CAS  PubMed  Google Scholar 

  32. Gorry MC, Gabbaizedeh D, Furey W, et al. Mutations in the cationic trypsinogen gene are associated with recurrent acute and chronic pancreatitis. Gastroenterology, 1997, 113(4): 1063–1068

    Article  CAS  PubMed  Google Scholar 

  33. Whitcomb DC. Hereditary pancreatitis: new insights into acute and chronic pancreatitis. Gut, 1999, 45(3): 317–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lowenfels AB, Maisonneuve P, Cavallini G, et al. Pancreatitis and the risk of pancreatic cancer. N Engl J Med, 1993, 328(20): 1433–1437

    Article  CAS  PubMed  Google Scholar 

  35. Whitcomb DC, Applebaum S, Martin SP. Hereditary pancreatitis and pancreatic carcinoma. Ann N Y Academy Sci, 1999, 880(1): 201–209

    Article  CAS  Google Scholar 

  36. Rebours V, Boutron-Ruault MC, Schnee M, et al. Risk of pancreatic adenocarcinoma in patients with hereditary pancreatitis: a national exhaustive series. AJG, 2008, 103(1): 111–119

    Article  PubMed  Google Scholar 

  37. Lowenfels AB, Maisonneuve P, Whitcomb DC, et al. Cigarette smoking as a risk factor for pancreatic cancer in patients with hereditary pancreatitis. JAMA, 2001, 286(2): 169–170

    Article  CAS  PubMed  Google Scholar 

  38. Greer JB, Zarnescu NO, Whitcomb DC. Hereditary Pancreatitis and Pancreatic Cancer. Springer US, 2008: 81–96.

    Book  Google Scholar 

  39. Lowenfels AB, Maisonneuve P, Lankisch PG, et al. Chronic pancreatitis and other risk factors for pancreatic cancer. Gastroenterol Clin North Am, 1999, 28(3): 673–685

    Article  CAS  PubMed  Google Scholar 

  40. Hahn SA, Greenhalf B, Ellis I, et al. BRCA2 germline mutations in familial pancreatic carcinoma. J Natl Cancer Inst, 2003, 95(3): 214–221

    Article  CAS  PubMed  Google Scholar 

  41. Howes N, Neoptolemos JP. Risk of pancreatic ductal adenocarcinoma in chronic pancreatitis. Gut, 2002, 1(6): 765–766

    Article  Google Scholar 

  42. Howes N, Wong T, Greenhalf W, et al. Pancreatic cancer risk in hereditary pancreatitis in Europe. Digestion, 2000, 61(61): 70

    Google Scholar 

  43. Witt H, Luck W, Hennies HC, et al. Mutations in the gene encoding the serine protease inhibitor, Kazal type 1 are associated with chronic pancreatitis. Nat Genet, 2000, 25(2): 213–216

    Article  CAS  PubMed  Google Scholar 

  44. Greer JB, Whitcomb DC, Brand RE. Genetic predisposition to pancreatic cancer: a brief review. AJG, 2007, 102(11): 2564–2569

    Article  CAS  PubMed  Google Scholar 

  45. Tulinius H, Olafsdottir GH, Sigvaldason H, et al. Neoplastic diseases in families of breast cancer patients. J Med Genet, 1994, 31(8): 618–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Phelan CM, Lancaster JM, Tonin P, et al. Mutation analysis of the BRCA2 gene in 49 site–specific breast cancer families. Nat Genet, 1996, 13(1): 120–122

    Article  CAS  PubMed  Google Scholar 

  47. Simard J, Tonin P, Durocher F, et al. Common origins of BRCA1 mutations in Canadian breast and ovarian cancer families. Nat Genet, 1994, 8(4): 392–398

    Article  CAS  PubMed  Google Scholar 

  48. Ford D, Easton DF, Stratton M, et al. Genetic heterogeneity and penetrance analysis of the BRCA1 and BRCA2 genes in breast cancer families. Am J Hum Genet, 1998, 62(3): 676–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Breast Cancer Linkage Consortium. Cancer risks in BRCA2 mutation carriers. J Nat Cancer Inst, 1999, 91(15): 1310-1316

  50. Hahn SA, Greenhalf B, Ellis I, et al. BRCA2 germline mutations in familial pancreatic carcinoma. J Nat Cancer Inst, 2003, 95(3): 214–221

    Article  CAS  PubMed  Google Scholar 

  51. Thompson D, Easton DF. Breast Cancer Linkage Consortium. Cancer incidence in BRCA1 mutation carriers. J Nat Cancer Inst, 2002, 94(18): 1358–1365

    Article  CAS  PubMed  Google Scholar 

  52. Risch HA, McLaughlin JR, Cole DE, et al. Prevalence and penetrance of germline BRCA1 and BRCA2 mutations in a population series of 649 women with ovarian cancer. Am J Hum Genet, 2001, 68(3): 700–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Boder E. Ataxia-telangiectasia: an overview. Kroc Foundation, 1985, 19: 1–63

    CAS  Google Scholar 

  54. Reiman A, Srinivasan V, Barone G, et al. Lymphoid tumours and breast cancer in ataxia telangiectasia; substantial protective effect of residual ATM kinase activity against childhood tumours. Brit J Cancer, 2011, 105(4): 586–591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Roberts NJ, Jiao Y, Yu J, et al. ATM mutations in patients with hereditary pancreatic cancer. Cancer Discov, 2012, 2(1): 41–46

    Article  CAS  PubMed  Google Scholar 

  56. Li A, Swift M. Mutations at the ataxia-telangiectasia locus and clinical phenotypes of A–T patients. Am J Med Genet, 2000, 92(3): 170–177

    Article  CAS  PubMed  Google Scholar 

  57. Renwick A, Thompson D, Seal S, et al. ATM mutations that cause ataxia-telangiectasia are breast cancer susceptibility alleles. Nat Genet, 2006, 38(8): 873–875

    Article  CAS  PubMed  Google Scholar 

  58. Lynch HT, de la Chapelle A. Hereditary colorectal cancer. N Engl J Med, 2003, 348(10): 919–932

    Article  CAS  PubMed  Google Scholar 

  59. Watson P, Vasen HF, Mecklin JP, et al. The risk of extra-colonic, extra-endometrial cancer in the Lynch syndrome. Int Cancer, 2008, 123(2): 444–449

    Article  CAS  Google Scholar 

  60. Win AK, Young JP, Lindor NM, et al. Colorectal and other cancer risks for carriers and noncarriers from families with a DNA mismatch repair gene mutation: a prospective cohort study. J Clin Oncol, 2012, 30(9): 958–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Giardiello FM, Offerhaus GJ, Lee DH, et al. Increased risk of thyroid and pancreatic carcinoma in familial adenomatous polyposis. Gut, 1993, 34(10): 1394–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Bartsch DK. Familial pancreatic cancer. Brit J Surg, 2003, 90(4): 386–397

    Article  CAS  PubMed  Google Scholar 

  63. Hruban RH, Petersen GM, Goggins M, et al. Familial pancreatic cancer. Ann Oncol, 1999, 10(suppl 4): S69–573

    Article  Google Scholar 

  64. Klein AP, Brune KA, Petersen GM, et al. Prospective risk of pancreatic cancer in familial pancreatic cancer kindreds. Cancer Res, 2004, 64(7): 2634–2638

    Article  CAS  PubMed  Google Scholar 

  65. Klein AP, Borges M, Griffith M, et al. Absence of deleterious palladin mutations in patients with familial pancreatic cancer. Cancer Epidemiol Biomarkers Prev, 2009, 18(4): 1328–1330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Tersmette AC, Petersen GM, Offerhaus K et al. Increased risk of incident pancreatic cancer among first-degree relatives of patients with familial pancreatic cancer. Clin Cancer Res, 2001, 7(3): 738–744

    CAS  PubMed  Google Scholar 

  67. Silverman DT, Dunn JA, Hoover RN, et al. Cigarette smoking and pancreas cancer: A case control study based on direct interviews. J Nat Cancer Inst, 1994, 86(20): 1510–1516

    Article  CAS  PubMed  Google Scholar 

  68. Gold EB, Goldin SB. Epidemiology of and risk factors for pancreatic cancer. Surg Oncol Clin North Am, 1998 1: 67–91

    Google Scholar 

  69. Rulyak SJ, Lowenfels AB, Maisonneuve P, et al. Risk factors for the development of pancreatic cancer in familial pancreatic cancer kindreds. Gastroenterology, 2003, 124(5): 1292–1299

    Article  PubMed  Google Scholar 

  70. Murphy KM, Brune KA, Griffin C, et al. Evaluation of candidate genes MAP2K4, MADH4, ACVR1B, and BRCA2 in familial pancreatic cancer: deleterious BRCA2 mutations in 17%. Cancer Res, 2002, 62(13): 3789–3793

    CAS  PubMed  Google Scholar 

  71. White K, Held KR, Weber BH. A BRCA2 germline mutation in familial pancreatic carcinoma. Int J Cancer, 2001, 91(5): 742–744

    Article  CAS  PubMed  Google Scholar 

  72. Wolpin BM, Chan AT, Hartge P, et al. ABO blood group and the risk of pancreatic cancer. J Natl Cancer Inst, 2009, 101(6): 424–431

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Wolpin BM, Kraft P, Gross M, et al. Pancreatic cancer risk and ABO blood group alleles: results from the pancreatic cancer cohort consortium. Cancer Res, 2010, 70(3): 1015–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Greer JB, Yazer MH, Raval JS, et al. Significant association between ABO blood group and pancreatic cancer. WJG, 2010, 16(44): 5588–5591

    Article  PubMed  PubMed Central  Google Scholar 

  75. Annese V, Minervini M, Gabbrielli A, et al. ABO blood groups and cancer of the pancreas. Int J Pancreatol, 1990, 6(2): 81–88

    CAS  PubMed  Google Scholar 

  76. Lüttges J, Klöppel G. Precancerous conditions of pancreatic carcinoma. J Hepatol Bil Pan Surg, 2000, 7(6): 568–574

    Article  Google Scholar 

  77. Apple SK, Hecht JR, Lewin DN, et al. Immunohistochemical evaluation of K-ras, p53, and HER-2/neu expression in hyperplastic, dysplastic, and carcinomatous lesions of the pancreas: evidence for multistep carcinogenesis. Human Pathol, 1999, 30(2): 123–129

    Article  CAS  Google Scholar 

  78. Gold EB, Cameron JL. Chronic pancreatitis and pancreatic cancer. N Engl J Med, 328(20): 1485-486

  79. Fernandez E, La Vecchia C, Porta M, et al. Pancreatitis and the risk of pancreatic cancer. Pancreas, 1995, 11(2): 185–189

    Article  CAS  PubMed  Google Scholar 

  80. Raimondi S, Lowenfels AB, Morselli-Labate AM, et al. Pancreatic cancer in chronic pancreatitis, aetiology, incidence, and early detection. Best Pract Res Clin Gastroenterol, 2010, 24(3): 349–358

    Article  PubMed  Google Scholar 

  81. Camara SN, Ramdany S, Wang CY, et al. Etiology, pathology, diagnosis, management and prognosis of chronic pancreatitis in Chinese population. A retrospective study. J Huazhong Univ Sci Technol Med Sci, 2015, 35(3): 384–389

    Article  PubMed  Google Scholar 

  82. Maisonneuve P, Lowenfels AB. Chronic pancreatitis and pancreatic cancer. Digest Dis, 2002, 20(1): 32–37

    Article  Google Scholar 

  83. Malka D, Hammel P, Maire F, et al. Risk of pancreatic adenocarcinoma in chronic pancreatitis. Gut, 2002, 51(6): 849–852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Lowenfels AB, Maisonneuve P, Cavallini G, Pancreatitis and the risk of pancreatic cancer. International Pancreatitis Study Group. N Engl J Med, 1993, 328(20): 1433–1437

    Article  CAS  PubMed  Google Scholar 

  85. Howes N, Lerch MM, Greenhalf W, et al. Clinical and genetic characteristics of hereditary pancreatitis in Europe. Clin Gastroenterol Hepatol, 2004, 2(3): 252–261

    Article  CAS  PubMed  Google Scholar 

  86. Barman KK, Premalatha G, Mohan V. Tropical chronic pancreatitis. Postgrad Med J, 2003, 79(937): 606–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Whitcomb DC. Genetics and alcohol: a lethal combination in pancreatic disease? Alcohol Clin Exp Res, 2011, 35(5): 838–842

    Article  PubMed  Google Scholar 

  88. Lowenfels AB, Maisonneuve P. Epidemiologic and etiologic factors of pancreatic cancer. Hematol Oncol Clin North Am, 2002, 16(1): 1–16

    Article  PubMed  Google Scholar 

  89. Evans JD, Morton DG, Neoptolemos JP. Chronic pancreatitis and pancreatic carcinoma. Postgrad Med J, 1997, 73(863): 543–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Batabyal P, Vander Hoorn S, Christophi C, et al. Association of diabetes mellitus and pancreatic adenocarcinoma: a meta-analysis of 88 studies. Ann Surg Oncol, 2014, 21(7): 2453–2462

    Article  PubMed  Google Scholar 

  91. Liao KF, Lai SW, Li CI, et al. Diabetes mellitus correlates with increased risk of pancreatic cancer: A population-based cohort study in Taiwan. J Gastroenterol Hepatol, 2012, 27(4): 709–713

    Article  PubMed  Google Scholar 

  92. Everhart J, Wright D. Diabetes mellitus as a risk factor for pancreatic cancer: a meta-analysis. JAMA, 1995, 273(20): 1605–1609

    Article  CAS  PubMed  Google Scholar 

  93. Huxley R, Ansary-Moghaddam A, De González AB, et al. Type-II diabetes and pancreatic cancer: a meta-analysis of 36 studies. Brit J Cancer, 2005, 92(11): 2076–2083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Pannala R, Leirness JB, Bamlet WR, et al. Prevalence and clinical profile of pancreatic cancer–associated diabetes mellitus. Gastroenterology, 2008, 134(4): 981–987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Bosetti C, Rosato V, Li D, et al. Diabetes, antidiabetic medications, and pancreatic cancer risk: an analysis from the International Pancreatic Cancer Case-Control Consortium. Ann Oncol, 2014, 25(10): 2065–2072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Pezzilli R, Fabbri D, Imbrogno A. Pancreatic ductal adenocarcinoma screening: New perspectives. WJG, 2012, 18(36): 4973

    Article  PubMed  PubMed Central  Google Scholar 

  97. De Mesquita HB, Maisonneuve P, Moerman CJ, et al. Aspects of medical history and exocrine carcinoma of the pancreas: A population-based case-control study in The Netherlands. Int J Cancer, 1992, 52(1): 17–23

    Article  Google Scholar 

  98. Gullo L, Pezzilli R, Morselli-Labate AM. Diabetes and the risk of pancreatic cancer. N Engl J Med, 1994, 331(2): 81–84

    Article  CAS  PubMed  Google Scholar 

  99. Frye JN, Inder WJ, Dobbs BR, et al. Pancreatic cancer and diabetes: Is there a relationship? A case controlled study. Aust N Z J Surg, 2000, 70(10): 722–724

    Article  CAS  PubMed  Google Scholar 

  100. Talamini G, Falconi M, Bassi C, et al. Previous cholecystectomy, gastrectomy, and diabetes mellitus are not crucial risk factors for pancreatic cancer in patients with chronic pancreatitis. Pancreas, 2001, 23(4): 364–367

    Article  CAS  PubMed  Google Scholar 

  101. Egawa N, Tu Y, Sanaka M, et al. Family history of diabetes and pancreatic cancer. Pancreas, 2005, 30(1): 15–19

    PubMed  Google Scholar 

  102. Wang F, Gupta S, Holly EA. Diabetes mellitus and pancreatic cancer in a population-based case-control study in the San Francisco Bay Area, California. Cancer Epidemiol Biomarkers Prev, 2006, 15(8): 14581–14584

    Article  Google Scholar 

  103. Gupta S, Vittinghoff E, Bertenthal D, et al, New-onset diabetes and pancreatic cancer. Clin Gastroenterol Hepatol, 2006, 4(11): 1366–1372

    Article  PubMed  Google Scholar 

  104. Chari ST, Leibson CL, Rabe KG, et al. Pancreatic cancer–associated diabetes mellitus: prevalence and temporal association with diagnosis of cancer. Gastroenterology, 2008, 134(1): 95–101

    Article  CAS  PubMed  Google Scholar 

  105. Kuang TT, Jin DY, Wang DS, et al. Clinical epidemiological analysis of the relationship between pancreatic cancer and diabetes mellitus: data from a single institution in China. J Digest Dis, 2009, 10(1): 26–29

    Article  Google Scholar 

  106. Maisonneuve P, Lowenfels AB, Bueno-de-Mesquita HB, et al. Past medical history and pancreatic cancer risk: results from a multicenter case-control study. Ann Epidemiol, 2010, 20(2): 92–98

    Article  PubMed  Google Scholar 

  107. Olson SH, Chou JF, Ludwig E, et al. Allergies, obesity, other risk factors and survival from pancreatic cancer. Int J Cancer, 2010, 127(10): 2412–1419

    Article  CAS  PubMed  Google Scholar 

  108. Elena JW, Steplowski E, Yu K, et al. Diabetes and risk of pancreatic cancer: a pooled analysis from the pancreatic cancer cohort consortium. Cancer Causes Control, 2013, 24(1): 13–25

    Article  PubMed  Google Scholar 

  109. Pierce BL, Austin MA, Ahsan H, et al. Association study of type 2 diabetes genetic susceptibility variants and risk of pancreatic cancer: an analysis of PanScan-I data. Cancer Causes Control, 2011, 22(6): 877–883

    Article  PubMed  Google Scholar 

  110. Blot WJ, Fraumeni JF, Stone BJ. Geographic correlates of pancreas cancer in the United States. Cancer, 1978, 42(1): 373–380

    Article  CAS  PubMed  Google Scholar 

  111. Mizuno S, Watanabe S, Nakamura K, et al. A multi-institute case-control study on the risk factors of developing pancreatic cancer. Jap J Clin Oncol, 1992, 22(4): 286–291

    CAS  Google Scholar 

  112. Shibata A, Mack TM, Paganini Hill A, et al. A prospective study of pancreatic cancer in the elderly. Int J Cancer, 1994, 58(1): 46–49

    Article  CAS  PubMed  Google Scholar 

  113. Silverman DT. Risk factors for pancreatic cancer: A case-control study based on direct interviews. Teratogen Carc Mut, 2001, 21(1): 7–25

    Article  CAS  Google Scholar 

  114. Luo J, Iwasaki M, Inoue M, et al. Body mass index, physical activity and the risk of pancreatic cancer in relation to smoking status and history of diabetes: a large-scale population-based cohort study in Japan–the JPHC study. Cancer Causes Control, 2007, 18(6): 603–612

    Article  PubMed  Google Scholar 

  115. Lipworth L, Zucchetto A, Bosetti C, et al. Diabetes mellitus, other medical conditions and pancreatic cancer: a case-control study. Diab Met Res Rev, 2011, 27(3): 255–261

    Article  Google Scholar 

  116. Chang CH, Toh S, Lin JW, et al. Cancer risk associated with insulin glargine among adult type 2 diabetes patients–a nationwide cohort study. PLoS One, 2011, 6(6): e21368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Stolzenberg-Solomon RZ, Graubard BI, Chari S, et al. Insulin, glucose, insulin resistance, and pancreatic cancer in male smokers. JAMA, 2005, 294(22): 2872–2878

    Article  CAS  PubMed  Google Scholar 

  118. Gapstur SM, Gann PH, Lowe W, Liu K, et al. Abnormal glucose metabolism and pancreatic cancer mortality. JAMA, 2000, 283(19): 2552–2558

    Article  CAS  PubMed  Google Scholar 

  119. Li D, Jiao L, Li Y, et al. Polymorphisms of cytochrome P4501A2 and N-acetyltransferase genes, smoking, and risk of pancreatic cancer. Carcinogenesis, 2005, 27(1): 103–111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  120. Aune D, Greenwood DC, Chan DS, et al. Body mass index, abdominal fatness and pancreatic cancer risk: a systematic review and non-linear dose–response meta-analysis of prospective studies. Ann Oncol, 2011, 23(4); 843–852

    Article  PubMed  Google Scholar 

  121. O'Rorke MA, Cantwell MM, Cardwell CR, et al. Can physical activity modulate pancreatic cancer risk? a systematic review and meta-analysis. Inter J Cancer, 2010, 126(12): 2957–2968

    Google Scholar 

  122. Michaud DS, Giovannucci E, Willett WC, et al. Physical activity, obesity, height, and the risk of pancreatic cancer. JAMA, 2001, 286(8): 921–929

    Article  CAS  PubMed  Google Scholar 

  123. Parkin DM, Boyd L. Cancers attributable to overweight and obesity in the UK in 2010. Brit J Cancer, 2011, 105: S34–S37

    Article  PubMed  PubMed Central  Google Scholar 

  124. Bosetti C, Lucenteforte E, Silverman DT, et al. Cigarette smoking and pancreatic cancer: an analysis from the International Pancreatic Cancer Case-Control Consortium (Panc4). Ann Oncol, 2012, 23(7): 1880–1888

    Article  CAS  PubMed  Google Scholar 

  125. Fuchs CS, Colditz GA, Stampfer MJ, et al. A prospective study of cigarette smoking and the risk of pancreatic cancer. Arch Intern Med, 1996, 156(19): 2255–2260

    Article  CAS  PubMed  Google Scholar 

  126. Michaud DS. Epidemiology of pancreatic cancer. Minerva Chir, 2004, 59(2): 99–111

    CAS  PubMed  Google Scholar 

  127. Lynch SM, Vrieling A, Lubin JH, et al. Cigarette smoking and pancreatic cancer: a pooled analysis from the pancreatic cancer cohort consortium. Am J Epidemiol, 2009, 170(4): 403–413

    Article  PubMed  PubMed Central  Google Scholar 

  128. Lin Y, Tamakoshi A, Kawamura T, et al. A prospective cohort study of cigarette smoking and pancreatic cancer in Japan. Cancer Causes Control, 2002, 13(3): 249–254

    Article  PubMed  Google Scholar 

  129. Akiba S, Hirayama T. Cigarette smoking and cancer mortality risk in Japanese men and women—results from reanalysis of the six-prefecture cohort study data. Environ Health Perspect, 1990, 87: 19

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Iodice S, Gandini S, Maisonneuve P, et al. Tobacco and the risk of pancreatic cancer: a review and meta-analysis. Langenbeck's Arch Surg, 2008, 393(4): 535–545

    Article  Google Scholar 

  131. Zheng W, McLaughlin JK, Gridley G, et al. A cohort study of smoking, alcohol consumption, and dietary factors for pancreatic cancer (United States). Cancer Causes Control, 1993, 4(5): 477–482

    Article  CAS  PubMed  Google Scholar 

  132. Villeneuve PJ, Johnson KC, Mao Y, et al. Environmental tobacco smoke and the risk of pancreatic cancer: findings from a Canadian population-based case-control study. Can J Public Health, 2004, 95(1): 32–37

    PubMed  Google Scholar 

  133. Arslan AA, Helzlsouer KJ, Kooperberg C, et al. Anthropometric measures, body mass index, and pancreatic cancer: a pooled analysis from the Pancreatic Cancer Cohort Consortium (PanScan). Arch Internal Med, 2010, 170(9): 791–802

    Article  Google Scholar 

  134. Weiderpass E, Partanen T, Kaaks R, et al. Occurrence, trends and environmental etiology of pancreatic cancer. Scand J Work Env Health, 1998, 24(3): 165–174

    Article  CAS  Google Scholar 

  135. de Gonzalez AB, Sweetland S, Spencer E. A meta-analysis of obesity and the risk of pancreatic cancer. Brit J Cancer, 2003, 89(3): 519–523

    Article  PubMed Central  Google Scholar 

  136. Larsson SC, Permert J, Håkansson N, et al. Overall obesity, abdominal adiposity, diabetes and cigarette smoking in relation to the risk of pancreatic cancer in two Swedish population-based cohorts. Brit J Cancer, 2005, 93(11): 1310–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Li D, Morris JS, Liu J, et al. Body mass index and risk, age of onset, and survival in patients with pancreatic cancer. JAMA, 2009, 301(24): 2553–2562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Larsson SC, Orsini N, Wolk A. Body mass index and pancreatic cancer risk: A meta-analysis of prospective studies. Int J Cancer, 2007, 120(9): 1993–1998

    Article  CAS  PubMed  Google Scholar 

  139. Genkinger JM, Spiegelman D, Anderson KE, et al. A pooled analysis of 14 cohort studies of anthropometric factors and pancreatic cancer risk. Int J Cancer, 2011, 129(7): 1708–1717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Coughlin SS, Calle EE, Patel AV, et al. Predictors of pancreatic cancer mortality among a large cohort of United States adults. Cancer Causes Control, 2000, 11(10): 915–923

    Article  CAS  PubMed  Google Scholar 

  141. Burney PG, Comstock GW, Morris JS. Serologic precursors of cancer: serum micronutrients and the subsequent risk of pancreatic cancer. Am J Clin Nutrit, 1989, 49(5): 895–900

    CAS  PubMed  Google Scholar 

  142. Nkondjock A, Ghadirian P, Johnson KC, et al. Dietary intake of lycopene is associated with reduced pancreatic cancer risk. J Nutr, 2005, 135(3): 592–597

    CAS  PubMed  Google Scholar 

  143. Risch HA. Etiology of pancreatic cancer, with a hypothesis concerning the role of N-nitroso compounds and excess gastric acidity. J Nat Cancer Inst, 2003, 95(13): 948–960

    Article  CAS  PubMed  Google Scholar 

  144. Nöthlings U, Wilkens LR, Murphy SP, et al. Meat and fat intake as risk factors for pancreatic cancer: the multiethnic cohort study. J Nat Cancer Inst, 2005, 97(19): 1458–1465

    Article  PubMed  Google Scholar 

  145. Thiébaut AC, Jiao L, Silverman DT, et al. Dietary fatty acids and pancreatic cancer in the NIH-AARP diet and health study. J Natl Cancer Inst, 2009, 101(4): 1001–1011

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  146. Ekbom A, David H. Pancreatic cancer. Textbook of cancer epidemiology. N Y, Oxford University Press, 2002: 233–247.

    Google Scholar 

  147. Michaud DS, Giovannucci E, Willett WC, et al. Dietary meat, dairy products, fat, and cholesterol and pancreatic cancer risk in a prospective study. A J Epidemiol, 2003, 157(12): 1115–1125

    Article  Google Scholar 

  148. Michaud DS, Skinner HG, Wu K, et al. Dietary patterns and pancreatic cancer risk in men and women. J Nat Cancer Inst, 2005, 97(7): 518–524

    Article  PubMed  Google Scholar 

  149. Jiao L, Flood A, Subar AF, et al. Glycemic index, carbohydrates, glycemic load, and the risk of pancreatic cancer in a prospective cohort study. Cancer Epidemiol Biomarkers Prev, 2009, 18(4): 1144–1151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Howe G, Ghadirian RP, de Mesquita HB, et al. A collaborative case-control study of nutrient intake and pancreatic cancer within the search programme. Int J Cancer, 1992, 51: 365–372

    Article  CAS  PubMed  Google Scholar 

  151. Stolzenberg-Solomon RZ, Pietinen P, Taylor PR, et al. Prospective study of diet and pancreatic cancer in male smokers. Am J Epidemiol, 2002, 155(9): 783–792

    Article  PubMed  Google Scholar 

  152. Skinner HG, Michaud DS, Giovannucci E, et al. Vitamin D intake and the risk for pancreatic cancer in two cohort studies. Cancer Epidemiol Biomarkers Prev, 2006, 15(9): 1688–1695

    Article  CAS  PubMed  Google Scholar 

  153. Grant WB. An estimate of premature cancer mortality in the US due to inadequate doses of solar ultraviolet-B radiation. Cancer, 2002, 94(6): 1867–1875

    Article  PubMed  Google Scholar 

  154. Guyton KZ, Kensler TW, Posner GH. Vitamin D and vitamin D analogs as cancer chemopreventive agents. Nutrit Rev, 2003, 61(7): 227–238

    Article  PubMed  Google Scholar 

  155. Stolzenberg-Solomon RZ, Jacobs EJ, Arslan AA, et al. Circulating 25-hydroxyvitamin D and risk of pancreatic cancer: Cohort Consortium Vitamin D Pooling Project of Rarer Cancers. Am J Epidemiol, 2010, 172(1): 81–93

    Article  PubMed  PubMed Central  Google Scholar 

  156. Stolzenberg-Solomon RZ, Hayes RB, Horst RL, et al. Serum vitamin D and risk of pancreatic cancer in the prostate, lung, colorectal, and ovarian screening trial. Cancer Res, 2009, 69(4): 1439–1447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Hassan MM, Bondy ML, Wolff RA, et al. Risk factors for pancreatic cancer: case-control study. AJG, 2007, 102(12): 2696–2707

    Article  PubMed  PubMed Central  Google Scholar 

  158. Farrow DC, Davis S. Risk of pancreatic cancer in relation to medical history and the use of tobacco, alcohol and coffee. Int J Cancer, 1990, 45(5): 816–820

    Article  CAS  PubMed  Google Scholar 

  159. Talamini G, Bassi C, Falconi M, et al. Alcohol and smoking as risk factors in chronic pancreatitis and pancreatic cancer. Digest Dis Sci, 1999, 44(7): 1303–1311

    Article  CAS  PubMed  Google Scholar 

  160. Lin Y, Tamakoshi A, Kawamura T, et al. Risk of pancreatic cancer in relation to alcohol drinking, coffee consumption and medical history: findings from the Japan collaborative cohort study for evaluation of cancer risk. Int J Cancer, 2002, 99(5): 742–746

    Article  CAS  PubMed  Google Scholar 

  161. Michaud DS, Giovannucci E, Willett WC, et al. Coffee and alcohol consumption and the risk of pancreatic cancer in two prospective United States cohorts. Cancer Epidemiol Biomarkers Prev, 2001, 10(5): 429–437

    CAS  PubMed  Google Scholar 

  162. Weisburger JH. Comments on the history and importance of aromatic and heterocyclic amines in public health. Mutation Res Fund Mol Mech Mut, 2002, 506-507: 9–20

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of General Surgery, Pancreatic Disease Institute, Huazhong University of Science and Technology, Wuhan, 430022, China

    Soriba Naby Camara, Tao Yin  (殷 涛), Ming Yang  (杨 明), Xiang Li  (李 响), Qiong Gong  (龚 琼), Gang Zhao  (赵 刚), Zhi-yong Yang  (杨智勇), Tajoo Aroun, Jiong-xin Xiong  (熊炯新), Jing Tao  (陶 京), Qi Qin  (钦 琪), Wei Zhou  (周 伟), Jing Cui  (崔 静), Min Huang  (黄 敏), Yao Guo  (郭 尧), Shan-miao Gou  (勾善淼), Bo Wang  (王 博), Tao Liu  (刘 涛), Ohoya Etsaka Terence Olivier, He-shui Wu  (吴河水) & Chun-you Wang  (王春友)

  2. Department of Breast and Thyroid Surgery, Huazhong University of Science and Technology, Wuhan, 430022, China

    Jing Zhou  (周 静)

  3. Department of Planning Family and Reproductive Institute, Huazhong University of Science and Technology, Wuhan, 430030, China

    Martin Kuete

  4. Department of General Medicine, Sir Seewoosagur Ramgoolam National Hospital of Pamplemousses, Mauritius, 21017, Mauritius

    Sonam Ramdany

  5. Department of Thoracic Surgery, National Hospital of Donka, Conakry, Guinea

    Alpha Kabinet Camara, Tenin Conde & Aboubacar Sidiki Magassouba

  6. Department of General Surgery, National Hospital of Ignace Deen, Conakry, 1147, Guinea

    Aissatou Taran Diallo, Aboubacar Toure & Naby Daouda Camara

  7. Department of Gastroenterology and Hepatology, Huazhong University of Science and Technology, Wuhan, 430022, China

    Zhen Feng  (冯 珍)

  8. Department of Nephrology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China

    Xin Ning  (宁 辛)

  9. Department of Dermatology, National Hospital of Donka, Conakry, Guinea

    Mohamed Cisse

  10. Department of Internal Medicine, Huazhong University of Science and Technology, Wuhan, 430030, China

    Sneha Ballah

  11. Department of Biochemistry, University Gamal Abdel Nasser of Conakry, Conakry, 1147, Guinea

    Naby Laye Moussa Keita

  12. Department of Neurosurgery, Friendship Hospital Sino-Guinea of Kipe, Conakry, Guinea

    Ibrahima Sory Souare

  13. Department of Medical Imaging, Good Shepherd Medical Center, The University of Texas, Longview, 75601, USA

    Sadamoudou Traore

  14. Department of Visceral Surgery, National Hospital of Donka, Conakry, Guinea

    Abdoulaye Korse Balde

  15. Department of Gynecology and Obstetrics, National Hospital of Donka, Conakry, Guinea

    Namory Keita

  16. Department of Stomatology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, China

    Dusabe Emmanuel

Authors
  1. Soriba Naby Camara
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  2. Tao Yin  (殷 涛)
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  3. Ming Yang  (杨 明)
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  4. Xiang Li  (李 响)
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  7. Gang Zhao  (赵 刚)
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  8. Zhi-yong Yang  (杨智勇)
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  9. Tajoo Aroun
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  14. Zhen Feng  (冯 珍)
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  15. Xin Ning  (宁 辛)
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  16. Jiong-xin Xiong  (熊炯新)
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  17. Jing Tao  (陶 京)
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  18. Qi Qin  (钦 琪)
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  19. Wei Zhou  (周 伟)
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  20. Jing Cui  (崔 静)
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  21. Min Huang  (黄 敏)
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  22. Yao Guo  (郭 尧)
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  23. Shan-miao Gou  (勾善淼)
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  24. Bo Wang  (王 博)
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  25. Tao Liu  (刘 涛)
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  26. Ohoya Etsaka Terence Olivier
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  27. Tenin Conde
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  28. Mohamed Cisse
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  29. Aboubacar Sidiki Magassouba
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  30. Sneha Ballah
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  31. Naby Laye Moussa Keita
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  32. Ibrahima Sory Souare
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  33. Aboubacar Toure
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  34. Sadamoudou Traore
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  35. Abdoulaye Korse Balde
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  36. Namory Keita
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  37. Naby Daouda Camara
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  38. Dusabe Emmanuel
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  39. He-shui Wu  (吴河水)
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  40. Chun-you Wang  (王春友)
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Corresponding author

Correspondence to Chun-you Wang  (王春友).

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Camara, S.N., Yin, T., Yang, M. et al. High risk factors of pancreatic carcinoma. J. Huazhong Univ. Sci. Technol. [Med. Sci.] 36, 295–304 (2016). https://doi.org/10.1007/s11596-016-1583-x

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  • DOI: https://doi.org/10.1007/s11596-016-1583-x

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