Abstract
Background/Aim
Smoking is a recognized risk factor for pancreatic cancer. The aim of this study was to perform a meta-analysis to provide a robust estimate of the strength of the association between smoking and pancreatic cancer, to determine the risk of pipe and cigar smoking, and to estimate the duration of an elevated risk after smoking cessation.
Methods
We performed a meta-analysis of 82 published studies containing epidemiologic information about smoking and pancreatic cancer. Information on studies published between 1950 and 2007 was abstracted and prepared for analysis using standard meta-analytic procedures.
Results
The overall risk of pancreatic cancer estimated from the combined results for current and former smokers was, respectively, 1.74 (95% CI 1.61–1.87) and 1.2 (95% CI 1.11–1.29). The risk of pancreatic cancer for current and former pipe and/or cigar smokers was respectively 1.47 (95% CI 1.17–1.83) and 1.29 (95% CI 0.68–2.45). For former cigarette smokers, the risk remains elevated for a minimum of 10 years after cessation.
Conclusions
Based on estimates from four continents, smoking cigarettes causes a 75% increase in the risk of pancreatic cancer compared to non-smokers, and the risk persists for a minimum of 10 years after smoking cessation. This implies that in a population where the prevalence of smoking is 30%, the population’s attributable risk (the proportion of pancreatic cancer explained by smoking) is estimated to be 20%.
Similar content being viewed by others
References
Danaei G, Vander HS, Lopez AD, Murray CJ, Ezzati M (2005) Causes of cancer in the world: comparative risk assessment of nine behavioural and environmental risk factors. Lancet 366:1784–1793
Rulyak SJ, Lowenfels AB, Maisonneuve P, Brentnall TA (2003) Risk factors for the development of pancreatic cancer in familial pancreatic cancer kindreds. Gastroenterology 124:1292–1299
Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30
Van Houwelingen HC, Arends LR, Stijnen T (2002) Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med JID-8215016 21:589–624
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560
SAS Institute Inc (1999) SAS Windows version. (8.02). Cary, NC. (GENERIC) Ref Type: Computer Program
Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose–response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309
Copas JB, Shi JQ (2001) A sensitivity analysis for publication bias in systematic reviews. Stat Methods Med Res 10:251–265
Macaskill P, Walter SD, Irwig L (2001) A comparison of methods to detect publication bias in meta-analysis. Stat Med JID-8215016 20:641–654
Liaw KM, Chen CJ (1998) Mortality attributable to cigarette smoking in Taiwan: a 12-year follow-up study. Tob Control 7:141–148
Nishi M, Ohba S, Hirata K, Miyake H (1996) Dose–response relationship between coffee and the risk of pancreas cancer. Jpn J Clin Oncol 26:42–48
Jee SH, Samet JM, Ohrr H, Kim JH, Kim IS (2004) Smoking and cancer risk in Korean men and women. Cancer Causes Control 15:341–348
Mori M, Hariharan M, Anandakumar M et al (1999) A case-control study on risk factors for pancreatic diseases in Kerala, India. Hepatogastroenterology 46:25–30
Inoue M, Tajima K, Takezaki T et al (2003) Epidemiology of pancreatic cancer in Japan: a nested case-control study from the Hospital-based Epidemiologic Research Program at Aichi Cancer Center (HERPACC). Int J Epidemiol 32:257–262
Khurana V, Sheth A, Caldito G, Barkin JS (2007) Statins reduce the risk of pancreatic cancer in humans: a case-control study of half a million veterans. Pancreas 34:260–265
Prizment AE, Anderson KE, Hong CP, Folsom AR (2007) Pancreatic cancer incidence in relation to female reproductive factors: Iowa Women’s Health Study. JOP 8:16–27
Harnack LJ, Anderson KE, Zheng W, Folsom AR, Sellers TA, Kushi LH (1997) Smoking, alcohol, coffee, and tea intake and incidence of cancer of the exocrine pancreas: the Iowa Women’s Health Study. Cancer Epidemiol Biomarkers Prev 6:1081–1086
Durbec JP, Chevillotte G, Bidart JM, Berthezene P, Sarles H (1983) Diet, alcohol, tobacco and risk of cancer of the pancreas: a case-control study. Br J Cancer 47:463–470
Mulder I, Hoogenveen RT, van Genugten ML et al (2002) Smoking cessation would substantially reduce the future incidence of pancreatic cancer in the European Union. Eur J Gastroenterol Hepatol 14:1343–1353
Heuch I, Kvale G, Jacobsen BK, Bjelke E (1983) Use of alcohol, tobacco and coffee, and risk of pancreatic cancer. Br J Cancer 48:637–643
Mills P, Beeson W, Abbey D, Fraser G, Phillips RL (1988) Dietary habits and past medical history as related to fatal pancreas cancer risk among adventists. Cancer 61:2578–2585
Hirayama T (1989) Epidemiology of pancreatic cancer in Japan. Jpn J Clin Oncol 19:208–215
Akiba S, Hirayama T (1990) Cigarette smoking and cancer mortality risk in Japanese men and women—results from reanalysis of the six-prefecture cohort study data. Environ Health Perspect 87:19–26
Kuller LH, Ockene JK, Meilahn E, Wentworth DN, Svendsen KH, Neaton JD (1991) Cigarette smoking and mortality. MRFIT Research Group. Prev Med 20:638–654
Zheng W, McLaughlin JK, Gridley G et al (1993) A cohort study of smoking, alcohol consumption, and dietary factors for pancreatic cancer (United States). Cancer Causes Control 4:477–482
Tverdal A, Thelle D, Stensvold I, Leren P, Bjartveit K (1993) Mortality in relation to smoking history: 13 years’ follow-up of 68,000 Norwegian men and women 35–49 years. J Clin Epidemiol 46:475–487
Shibata A, Mack TM, Paganini-Hill A, Ross RK, Henderson BE (1994) A prospective study of pancreatic cancer in the elderly. Int J Cancer 58:46–49
McLaughlin JK, Hrubec Z, Blot WJ, Fraumeni JF (1995) Smoking and cancer mortality among U.S. veterans: a 26-years follow-up. Int J Cancer 60:190–193
Engeland A, Andersen A, Haldorsen T, Tretli S (1996) Smoking habits and risk of cancers other than lung cancer: 28 year’s follow-up of 26,000 Norwegian men and women. Cancer Causes Control 7:497–506
Fuchs CS, Colditz GA, Stampfer MJ et al (1996) A prospective study of cigarette smoking and the risk of pancreatic cancer. Arch Intern Med 156:2255–2260
Yuan JM, Ross RK, Wang XL, Gao YT, Henderson BE, Yu MC (1996) Morbidity and mortality in relation to cigarette smoking in Shanghai, China. A prospective male cohort study. JAMA 275:1646–1650
Tulinius H, Sigfusson N, Sigvaldason H, Bjarnadottir K, Tryggvadottir L (1997) Risk factors for malignant diseases: a cohort study on a population of 22,946 Icelanders. Cancer Epidemiol Biomarkers Prev 6:863–873
Nordlund LA, Carstensen JM, Pershagen G (1997) Cancer incidence in female smokers: a 26-year follow-up. Int J Cancer 73:625–628
Iribarren C, Tekawa IS, Sidney S, Friedman GD (1999) Effect of cigar smoking on the risk of cardiovascular disease, chronic obstructive pulmonary disease, and cancer in men. N Engl J Med 340:1773–1780
Coughlin SS, Calle EE, Patel AV, Thun MJ (2000) Predictors of pancreatic cancer mortality among a large cohort of United States adults. Cancer Causes Control 11:915–923
Nilsen TI, Vatten LJ (2000) A prospective study of lifestyle factors and the risk of pancreatic cancer in Nord-Trondelag, Norway. Cancer Causes Control 11:645–652
Shapiro JA, Jacobs EJ, Thun MJ (2000) Cigar smoking in men and risk of death from tobacco-related cancers. J Natl Cancer Inst 92:333–337
Stolzenberg-Solomon RZ, Albanes D, Nieto FJ et al (1999) Pancreatic cancer risk and nutrition-related methyl–group availability indicators in male smokers. J Natl Cancer Inst 91:535–541
Nilsson S, Carstensen JM, Pershagen G (2001) Mortality among male and female smokers in Sweden: a 33 year follow up. J Epidemiol Community Health 55:825–830
Lin Y, Tamakoshi A, Kawamura T et al (2002) A prospective cohort study of cigarette smoking and pancreatic cancer in Japan. Cancer Causes Control 13:249–254
Isaksson B, Jonsson F, Pedersen NL, Larsson J, Feychting M, Permert J (2002) Lifestyle factors and pancreatic cancer risk: a cohort study from the Swedish Twin Registry. Int J Cancer 98:480–482
Henley SJ, Thun MJ, Chao A, Calle EE (2004) Association between exclusive pipe smoking and mortality from cancer and other diseases. J Natl Cancer Inst 96:853–861
Larsson SC, Permert J, Hakansson N, Naslund I, Bergkvist L, Wolk A (2005) Overall obesity, abdominal adiposity, diabetes and cigarette smoking in relation to the risk of pancreatic cancer in two Swedish population-based cohorts. Br J Cancer 93:1310–1315
Sinner PJ, Schmitz KH, Anderson KE, Folsom AR (2005) Lack of association of physical activity and obesity with incident pancreatic cancer in elderly women. Cancer Epidemiol Biomarkers Prev 14:1571–1573
Gallicchio L, Kouzis A, Genkinger JM et al (2006) Active cigarette smoking, household passive smoke exposure, and the risk of developing pancreatic cancer. Prev Med 42:200–205
Ansary-Moghaddam A, Huxley R, Barzi F et al (2006) The effect of modifiable risk factors on pancreatic cancer mortality in populations of the Asia-Pacific region. Cancer Epidemiol Biomarkers Prev 15:2435–2440
Yun JE, Jo I, Park J et al (2006) Cigarette smoking, elevated fasting serum glucose, and risk of pancreatic cancer in Korean men. Int J Cancer 119:208–212
Nothlings U, Wilkens LR, Murphy SP, Hankin JH, Henderson BE, Kolonel LN (2007) Vegetable intake and pancreatic cancer risk: the multiethnic cohort study. Am J Epidemiol 165:138–147
Gapstur SM, Gann PH, Lowe W, Liu K, Colangelo L, Dyer A (2000) Abnormal glucose metabolism and pancreatic cancer mortality. JAMA 283:2552–2558
Michaud DS, Joshipura K, Giovannucci E, Fuchs CS (2007) A prospective study of periodontal disease and pancreatic cancer in US male health professionals. J Natl Cancer Inst 99:171–175
Wynder EL, Mabuchi K, Maruchi N, Fortner J (1973) A case-control study of cancer of the pancreas. Cancer 31:641–648
MacMahon B, Yen S, Trichopoulos D, Warren K, Nardi G (1981) Coffee and Cancer of the Pancreas. N Engl J Med 304:630–633 (Abstract)
Whittemore AS, Paffenberger RS, Anderson K, Halpern J (1983) Early precursors of pancreatic cancer in college men. J Chronic Dis 36:251–256
Kinlen L, McPherson K (1984) Pancreas cancer and coffee and tea consumption: a case-control study. Br J Cancer 49:93–96
Gold EB, Gordis L, Diener MD et al (1985) Diet and other risk factors for cancer of the pancreas. Cancer 55:460–467
Hsieh CC, MacMahon B, Yen S, Trichopoulos D, Warren K, Nardi G (1986) Coffee and pancreatic cancer (Chapter 2). N Engl J Med 319:587–589
Mack TM, Yu MC, Hanisch R, Henderson BE (1986) Pancreas cancer and smoking, beverage consumption, and past medical history. J Natl Cancer Inst 76:49–60 (Abstract)
Wynder EL, Dieck G, Hall NEL (1986) Case-control study of decaffeinated coffee consumption and pancreatic cancer. Cancer Res 46:53600–55363
Hiatt RA, Klatsky AL, Armstrong MA (1988) Pancreatic cancer, blood glucose and beverage consumption. Int J Cancer 41:794–797
Clavel F, Benhamou E, Auquier A, Tarayre M, Flamant R (1989) Coffee, alcohol, smoking and cancer of the pancreas: a case-control study. Int J Cancer 43:17–21
Cuzick J, Babiker AG (1989) Pancreatic cancer, alcohol, diabetes mellitus and gallbladder disease. Int J Cancer 43:415–421
Farrow DC, Davis S (1990) Risk of pancreatic cancer in relation to medical history and use of tobacco, alcohol and coffee. Int J Cancer 45:816–820
Falk R, Pickle LW, Fontham E (1990) Occupation and pancreatic cancer in Louisiana. Am J Ind Med 18:565–576
Baghurst PA, McMichael AJ, Slavotinek A, Baghurst K, Boyle P, Walker AM (1991) A case-control study of diet and cancer of the pancreas. Am J Epidemiol 134:167–179
Bueno de Mesquita HB, Maisonneuve P, Moerman CJ, Runia S, Boyle P (1991) Life-time history of smoking and exocrine carcinoma of the pancreas: a population-based case-control study in the Netherlands. Int J Cancer 49:816–822
Howe GR, Jain M, Burch JD, Miller AB (1991) Cigarette smoking and cancer of the pancreas: evidence from a population-based case-control study in Toronto, Canada. Int J Cancer 47:323–328
Vioque J, Walker AM (1991) [Pancreatic cancer and ABO blood types: a study of cases and controls]. Med Clin (Barc) 96:761–764
Ghadirian P, Simard A, Baillargeon J (1991) Tobacco, alcohol, and coffee and cancer of the pancreas: a population-based, case-control study in Quebec, Canada. Cancer 67:2664–2670
Lyon JL, Egger MJ, Robison LM, French TK, Gao R (1992) Misclassification of exposure in a case-control study: the effects of different types of exposure and different proxy respondents in a study of pancreatic cancer. Epidemiology 3:223–231
Mizuno S, Watanabe S, Nakamura K (1992) A multi-institute case-control study on the risk factors of developing pancreatic cancer. Jpn J Clin Oncol 22:286–291
Zatonski W, Boyle P, Przewozniak K, Maisonneuve P, Drosik K, Walker AM (1993) Cigarette smoking, alcohol, tea and coffee consumption and pancreas cancer risk: a case-control study from Opole, Poland. Int J Cancer 53:601–607
Kalapothaki V, Tzonou A, Hsieh CC, Toupadaki N, Karakatsani A, Trichopoulos D (1993) Tobacco, ethanol, coffee, pancreatitis, diabetes mellitus, and cholelithiasis as risk factors for pancreatic carcinoma. Cancer Causes Control 4:375–382
Silverman DT, Dunn J, Hoover RN et al (1994) Cigarette smoking and pancreas cancer: a case-control study based on direct interviews. J Natl Cancer Inst 86:1510–1516
Ji BT, Chow WH, Dai Q et al (1995) Cigarette smoking and alcohol consumption and the risk of pancreatic cancer: a case-control study in Shanghai, China. Cancer Causes Control 6:369–376
Gullo L, Pezzilli R, Morselli-Labate AM, The Italian Pancreatic Study Group (1995) Coffee and cancer of the pancreas: an Italian multicenter study. Pancreas 3:223–229
Siemiatycki J, Krewski D, Franco E, Kaiserman M (1995) Associations between cigarette smoking and each of 21 types of cancer: a multi-site case-control study. Int J Epidemiol 24:504–514
Fernandez E, La Vecchia C, Decarli A (1996) Attributable risks for pancreatic cancer in Northern Italy. Cancer Epidemiol Biomarkers Prev 5:23–27
Lee CT, Chang FY, Lee SD (1996) Risk factors for pancreatic cancer in Orientals. J Gastroenterol Hepatol 11:491–495
Murata M, Takayama K, Choi BC, Pak AW (1996) A nested case-control study on alcohol drinking, tobacco smoking, and cancer. Cancer Detect Prev 20:557–565
Kokic NZ, Adanja JB, Vlajinac DH, Marinkovic PJ, Colovic BR, Jarebinski SM (1996) Case-control study of pancreatic cancer in Serbia, Yugoslavia. Neoplasma 43:353–356
Muscat JE, Stellman SD, Hoffmann D, Wynder EL (1997) Smoking and pancreatic cancer in men and women. Cancer Epidemiol Biomarkers Prev 6:15–19
Fryzek JP, Garabrant DH, Harlow SD et al (1997) A case-control study of self-reported exposures to pesticides and pancreas cancer in southeastern Michigan. Int J Cancer 72:62–67
Partanen TJ, Vainio HU, Ojajarvi IA, Kauppinen TP (1997) Pancreas cancer, tobacco smoking and consumption of alcoholic beverages: a case-control study. Cancer Lett 116:27–32
Alguacil J, Porta M, Benavides FG et al (2000) Occupation and pancreatic cancer in Spain: a case-control study based on job titles. PANKRAS II Study Group. Int J Epidemiol 29:1004–1013
Maruchi N, Brian D, Ludwig J, Elveback L, Kurland L (1979) Cancer of the pancreas in Olmsted county, Minnesota, 1935–1974. Mayo Clin Proc 54:245–249
Villeneuve PJ, Johnson KC, Hanley AJ, Mao Y (2000) Alcohol, tobacco and coffee consumption and the risk of pancreatic cancer: results from the Canadian Enhanced Surveillance System case-control project. Canadian Cancer Registries Epidemiology Research Group.. Eur J Cancer Prev 9:49–58
Bonelli L, Aste H, Bovo P et al (2003) Exocrine pancreatic cancer, cigarette smoking, and diabetes mellitus: a case-control study in northern Italy. Pancreas 27:143–149
Alguacil J, Silverman DT (2004) Smokeless and other noncigarette tobacco use and pancreatic cancer: a case-control study based on direct interviews. Cancer Epidemiol Biomarkers Prev 13:55–58
Carta P, Aru G, Cadeddu C et al (2004) Mortality for pancreatic cancer among aluminium smelter workers in Sardinia, Italy. G Ital Med Lav Ergon 26:83–89
Duell EJ, Holly EA (2005) Reproductive and menstrual risk factors for pancreatic cancer: a population-based study of San Francisco Bay Area women. Am J Epidemiol 161:741–747
Lu XH, Wang L, Li H, Qian JM, Deng RX, Zhou L (2006) Establishment of risk model for pancreatic cancer in Chinese Han population. World J Gastroenterol 12:2229–2234
Li W, Ray RM, Gao DL et al (2006) Occupational risk factors for pancreatic cancer among female textile workers in Shanghai, China. Occup Environ Med 63:788–793
Boyle P, Maisonneuve P, Bueno DM et al (1996) Cigarette smoking and pancreas cancer: a case control study of the search programme of the IARC. Int J Cancer 67:63–71
Author information
Authors and Affiliations
Corresponding author
Additional information
Supported by grants from the Italian Association for Cancer Research (AIRC), Solvay Pharmaceuticals, and the C.D. Smithers Foundation.
Rights and permissions
About this article
Cite this article
Iodice, S., Gandini, S., Maisonneuve, P. et al. Tobacco and the risk of pancreatic cancer: a review and meta-analysis. Langenbecks Arch Surg 393, 535–545 (2008). https://doi.org/10.1007/s00423-007-0266-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00423-007-0266-2