Skip to main content

Coffee consumption and risk of bladder cancer: a pooled analysis of 501,604 participants from 12 cohort studies in the BLadder Cancer Epidemiology and Nutritional Determinants (BLEND) international study

Abstract

Recent epidemiological studies have shown varying associations between coffee consumption and bladder cancer (BC). This research aims to elucidate the association between coffee consumption and BC risk by bringing together worldwide cohort studies on this topic. Coffee consumption in relation to BC risk was examined by pooling individual data from 12 cohort studies, comprising of 2601 cases out of 501,604 participants. Pooled multivariate hazard ratios (HRs), with corresponding 95% confidence intervals (CIs), were obtained using multilevel Weibull regression models. Furthermore, dose–response relationships were examined using generalized least squares regression models. The association between coffee consumption and BC risk showed interaction with sex (P-interaction < 0.001) and smoking (P-interaction = 0.001). Therefore, analyses were stratified by sex and smoking. After adjustment for potential confounders, an increased BC risk was shown for high (> 500 ml/day, equivalent to > 4 cups/day) coffee consumption compared to never consumers among male smokers (current smokers: HR = 1.75, 95% CI 1.27–2.42, P-trend = 0.002; former smokers: HR = 1.44, 95% CI 1.12–1.85, P-trend = 0.001). In addition, dose–response analyses, in male smokers also showed an increased BC risk for coffee consumption of more than 500 ml/day (4 cups/day), with the risk of one cup (125 ml) increment as 1.07 (95% CI 1.06–1.08). This research suggests that positive associations between coffee consumption and BC among male smokers but not never smokers and females. The inconsistent results between sexes and the absence of an association in never smokers indicate that the associations found among male smokers is unlikely to be causal and is possibly caused by residual confounding of smoking.

This is a preview of subscription content, access via your institution.

Fig. 1

Abbreviations

BLEND:

BLadder Cancer Epidemiology and Nutritional Determinants

BC:

Bladder cancer

GLS:

Generalized least squares

IARC:

International Agency for Research on Cancer

EPIC:

European Prospective Investigation into Cancer and Nutrition Cohort Studies

NLCS:

NetherLands Cohort Study

VITAL:

VITamins And Lifestyle cohort study

RERF-LSS:

Radiation Effects Research Foundation-Life Span Study

FFQ:

Food frequency questionnaires

ICD-O:

International classification of diseases for oncology

NMIBC:

Non-muscle invasive bladder cancer

MIBC:

Muscle invasive bladder cancer

HR:

Hazard ratio

CI:

Confidence interval

CYP1A2:

Cytochrome P450 1A2

PAHs:

Polycyclic aromatic hydrocarbons

ATM:

Ataxia-telangiectasia mutated

BMI:

Body Mass Index

SES:

Socioeconomic status

ml:

Millilitre

kcal:

Kilocalorie

g:

Gram

mg:

Microgram

References

  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30. https://doi.org/10.3322/caac.21387.

    Article  PubMed  Google Scholar 

  2. Antoni S, Ferlay J, Soerjomataram I, Znaor A, Jemal A, Bray F. Bladder cancer incidence and mortality: a global overview and recent trends. Eur Urol. 2017;71(1):96–108. https://doi.org/10.1016/j.eururo.2016.06.010.

    Article  PubMed  Google Scholar 

  3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69–90. https://doi.org/10.3322/caac.20107.

    Article  PubMed  Google Scholar 

  4. Ploeg M, Aben KK, Kiemeney LA. The present and future burden of urinary bladder cancer in the world. World J Urol. 2009;27(3):289–93. https://doi.org/10.1007/s00345-009-0383-3.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Marugame T, Mizuno S. Comparison of prostate cancer mortality in five countries: France, Italy, Japan, UK and USA from the WHO mortality database (1960–2000). Jpn J Clin Oncol. 2005;35(11):690–1. https://doi.org/10.1093/jjco/hyi185.

    Article  PubMed  Google Scholar 

  6. Stewart B, Wild CP. World cancer report 2014. New York: International Agency for Research on Cancer, World Health Organization: WHO Press; 2017.

    Google Scholar 

  7. Letašiová S, Medveďová A, Šovčíková A, et al. Bladder cancer, a review of the environmental risk factors. Environ Health. 2012;11(Suppl 1):S11. https://doi.org/10.1186/1476-069X-11-S1-S11.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Botteman MF, Pashos CL, Redaelli A, Laskin B, Hauser R. The health economics of bladder cancer. Pharmacoeconomics. 2003;21(18):1315–30. https://doi.org/10.1007/BF03262330.

    Article  PubMed  Google Scholar 

  9. Johansson SL, Cohen SM. Epidemiology and etiology of bladder cancer. Semin Surg Oncol. 1997;13(5):291–8. https://doi.org/10.1002/(sici)1098-2388(199709/10)13:5%3c291:aid-ssu2%3e3.0.co;2-8.

    CAS  Article  PubMed  Google Scholar 

  10. Thun M, Linet MS, Cerhan JR, Haiman CA, Schottenfeld D. Cancer epidemiology and prevention. 3rd ed. Oxford: Oxford University Press; 2017. https://doi.org/10.1093/ije/dyy166.

    Book  Google Scholar 

  11. Cole P. Coffee-drinking and cancer of the lower urinary tract. Lancet. 1971;1(7713):1335–7. https://doi.org/10.1016/S0140-6736(71)91890-3.

    CAS  Article  PubMed  Google Scholar 

  12. Nagano J, Kono S, Preston DL, Moriwaki H, Sharp GB, Koyama K, et al. Bladder-cancer incidence in relation to vegetable and fruit consumption: a prospective study of atomic-bomb survivors. Int J Cancer. 2000;86(1):132–8. https://doi.org/10.1002/(sici)1097-0215(20000401)86:1%3c132:aid-ijc21%3e3.0.co;2-m.

    CAS  Article  PubMed  Google Scholar 

  13. Pujolar AE, Gonzalez CA, Lopez-Abente G, Errezola M, Izarzugaza I, Nebot M, et al. Bladder cancer and coffee consumption in smokers and non-smokers in Spain. Int J Epidemiol. 1993;22(1):38–44. https://doi.org/10.1093/ije/22.1.38.

    Article  Google Scholar 

  14. Bruemmer B, White E, Vaughan TL, Cheney CL. Fluid intake and the incidence of bladder cancer among middle-aged men and women in a three-county area of western Washington. Nutr Cancer. 1997;29(2):163–8. https://doi.org/10.1080/01635589709514619.

    CAS  Article  PubMed  Google Scholar 

  15. Demirel F, Cakan M, Yalçınkaya F, Topcuoglu M, Altug U. The association between personal habits and bladder cancer in Turkey. Int Urol Nephrol. 2008;40(3):643–7. https://doi.org/10.1007/s11255-008-9331-1.

    Article  PubMed  Google Scholar 

  16. Kobeissi LH, Yassine IA, Jabbour ME, Moussa MA, Dhaini HR. Urinary bladder cancer risk factors: a Lebanese case–control study. Asian Pac J Cancer Prev APJCP. 2013;14(5):3205–11. https://doi.org/10.7314/apjcp.2013.14.5.3205.

    Article  PubMed  Google Scholar 

  17. Sugiyama K, Sugawara Y, Tomata Y, Nishino Y, Fukao A, Tsuji I. The association between coffee consumption and bladder cancer incidence in a pooled analysis of the Miyagi Cohort Study and Ohsaki Cohort Study. Eur J Cancer Prev. 2017;26(2):125–30. https://doi.org/10.1097/cej.0000000000000226.

    Article  PubMed  Google Scholar 

  18. Kurahashi N, Inoue M, Iwasaki M, Sasazuki S, Tsugane S. Coffee, green tea, and caffeine consumption and subsequent risk of bladder cancer in relation to smoking status: a prospective study in Japan. Cancer Sci. 2009;100(2):284–91. https://doi.org/10.1111/j.1349-7006.2008.01027.x.

    CAS  Article  Google Scholar 

  19. Vena JE, Freudenheim J, Graham S, Marshall J, Zielezny M, Swanson M, et al. Coffee, cigarette smoking, and bladder cancer in western New York. Ann Epidemiol. 1993;3(6):586–91. https://doi.org/10.1016/1047-2797(93)90079-J.

    CAS  Article  PubMed  Google Scholar 

  20. Geoffroy-Perez B, Cordier S. Fluid consumption and the risk of bladder cancer: results of a multicenter case–control study. Int J Cancer. 2001;93(6):880–7. https://doi.org/10.1002/ijc.1411.

    CAS  Article  PubMed  Google Scholar 

  21. De Stefani E, Boffetta P, Deneo-Pellegrini H, Correa P, Ronco AL, Brennan P, et al. Non-alcoholic beverages and risk of bladder cancer in Uruguay. BMC Cancer. 2007;7:57. https://doi.org/10.1186/1471-2407-7-57.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Mills PK, Beeson WL, Phillips RL, Fraser GE. Bladder cancer in a low risk population: results from the Adventist Health Study. Am J Epidemiol. 1991;133(3):230–9. https://doi.org/10.1093/oxfordjournals.aje.a115867.

    CAS  Article  PubMed  Google Scholar 

  23. Chyou P-H, Nomura AM, Stemmermann GN. A prospective study of diet, smoking, and lower urinary tract cancer. Ann Epidemiol. 1993;3(3):211–6. https://doi.org/10.1016/1047-2797(93)90021-U.

    CAS  Article  PubMed  Google Scholar 

  24. Tripathi A, Folsom AR, Anderson KE. Risk factors for urinary bladder carcinoma in postmenopausal women. Cancer. 2002;95(11):2316–23. https://doi.org/10.1002/cncr.10975.

    Article  PubMed  Google Scholar 

  25. Loftfield E, Freedman ND, Inoue-Choi M, Graubard BI, Sinha R. A prospective investigation of coffee drinking and bladder cancer incidence in the United States. Epidemiology. 2017;28(5):685–93. https://doi.org/10.1097/ede.0000000000000676.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Loomis D, Guyton KZ, Grosse Y, et al. Carcinogenicity of drinking coffee, mate, and very hot beverages. Lancet Oncol. 2016;17(7):877–8. https://doi.org/10.1016/S1470-2045(16)30239-X.

    Article  PubMed  Google Scholar 

  27. Swanson JA, Lee JW, Hopp JW. Caffeine and nicotine: a review of their joint use and possible interactive effects in tobacco withdrawal. Addict Behav. 1994;19(3):229–56. https://doi.org/10.1016/0306-4603(94)90027-2.

    CAS  Article  PubMed  Google Scholar 

  28. Zhou Y, Tian C, Jia C. A dose–response meta-analysis of coffee consumption and bladder cancer. Prev Med. 2012;55(1):14–22. https://doi.org/10.1016/j.ypmed.2012.04.020.

    Article  PubMed  Google Scholar 

  29. Benowitz NL, Peng M, Jacob P. Effects of cigarette smoking and carbon monoxide on chlorzoxazone and caffeine metabolism. Clin Pharmacol Ther. 2003;74(5):468–74. https://doi.org/10.1016/j.clpt.2003.07.001.

    CAS  Article  PubMed  Google Scholar 

  30. Zevin S, Benowitz NL. Drug interactions with tobacco smoking. Clin Pharmacokinet. 1999;36(6):425–38. https://doi.org/10.2165/00003088-199936060-00004.

    CAS  Article  PubMed  Google Scholar 

  31. De Leon J, Diaz FJ, Rogers T, et al. A pilot study of plasma caffeine concentrations in a US sample of smoker and nonsmoker volunteers. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27(1):165–71. https://doi.org/10.1016/S0278-5846(02)00348-2.

    Article  PubMed  Google Scholar 

  32. Plowchalk DR, Yeo KR. Prediction of drug clearance in a smoking population: modeling the impact of variable cigarette consumption on the induction of CYP1A2. Eur J Clin Pharmacol. 2012;68(6):951–60. https://doi.org/10.1007/s00228-011-1189-y.

    CAS  Article  PubMed  Google Scholar 

  33. Yu EY, Wesselius A, van Osch F, Stern MC, Jiang X, Kellen E, et al. The association between coffee consumption and bladder cancer in the Bladder Cancer Epidemiology and Nutritional Determinants (BLEND) international pooled study. Cancer Causes Control CCC. 2019. https://doi.org/10.1007/s10552-019-01191-1.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Riboli E, Kaaks R. The EPIC project: rationale and study design. European Prospective Investigation into Cancer and Nutrition. Int J Epidemiol. 1997;26(Suppl 1):S6–14. https://doi.org/10.1093/ije/26.suppl_1.s6.

    Article  PubMed  Google Scholar 

  35. Clavel-Chapelon F, van Liere MJ, Giubout C, Niravong MY, Goulard H, Le Corre C, et al. E3N, a French cohort study on cancer risk factors. E3N Group Etude Epidemiologique aupres de femmes de l’Education Nationale Eur J Cancer Prev. 1997;6(5):473–8. https://doi.org/10.1097/00008469-199710000-00007.

    CAS  Article  PubMed  Google Scholar 

  36. Boeing H, Korfmann A, Bergmann MM. Recruitment procedures of EPIC-Germany. European Investigation into Cancer and Nutrition. Ann Nutr Metab. 1999;43(4):205–15. https://doi.org/10.1159/000012787.

    CAS  Article  PubMed  Google Scholar 

  37. Riboli E, Hunt KJ, Slimani N, Ferrari P, Norat T, Fahey M, et al. European Prospective Investigation into Cancer and Nutrition (EPIC): study populations and data collection. Public Health Nutr. 2002;5(6b):1113–24. https://doi.org/10.1079/phn2002394.

    CAS  Article  PubMed  Google Scholar 

  38. Panico S, Dello Iacovo R, Celentano E, Galasso R, Muti P, Salvatore M, et al. Progetto ATENA, a study on the etiology of major chronic diseases in women: design, rationale and objectives. Eur J Epidemiol. 1992;8(4):601–8.

    CAS  Article  PubMed  Google Scholar 

  39. Beulens JW, Monninkhof EM, Verschuren WM, van der Schouw YT, Smit J, Ocke MC, et al. Cohort profile: the EPIC-NL study. Int J Epidemiol. 2010;39(5):1170–8. https://doi.org/10.1093/ije/dyp217.

    Article  PubMed  Google Scholar 

  40. Lund E, Dumeaux V, Braaten T, Hjartaker A, Engeset D, Skeie G, et al. Cohort profile: The Norwegian Women and Cancer Study–NOWAC–Kvinner og kreft. Int J Epidemiol. 2008;37(1):36–41. https://doi.org/10.1093/ije/dym137.

    Article  PubMed  Google Scholar 

  41. Manjer J, Carlsson S, Elmstahl S, Gullberg B, Janzon L, Lindstrom M, et al. The Malmo Diet and Cancer Study: representativity, cancer incidence and mortality in participants and non-participants. Eur J Cancer Prev. 2001;10(6):489–99. https://doi.org/10.1097/00008469-200112000-00003.

    CAS  Article  PubMed  Google Scholar 

  42. Hallmans G, Agren A, Johansson G, Johansson A, Stegmayr B, Jansson JH, et al. Cardiovascular disease and diabetes in the Northern Sweden Health and Disease Study Cohort—evaluation of risk factors and their interactions. Scand J Public Health Suppl. 2003;61:18–24. https://doi.org/10.1080/14034950310001432.

    Article  PubMed  Google Scholar 

  43. Davey GK, Spencer EA, Appleby PN, Allen NE, Knox KH, Key TJ. EPIC-Oxford: lifestyle characteristics and nutrient intakes in a cohort of 33 883 meat-eaters and 31 546 non meat-eaters in the UK. Public Health Nutr. 2003;6(3):259–69. https://doi.org/10.1079/phn2002430.

    Article  PubMed  Google Scholar 

  44. Day N, Oakes S, Luben R, Khaw KT, Bingham S, Welch A, et al. EPIC-Norfolk: study design and characteristics of the cohort. European Prospective Investigation of Cancer. Br J Cancer. 1999;80(Suppl 1):95–103.

    PubMed  Google Scholar 

  45. van den Brandt PA, Goldbohm RA, van’t Veer P, Volovics A, Hermus RJ, Sturmans F. A large-scale prospective cohort study on diet and cancer in The Netherlands. J Clin Epidemiol. 1990;43(3):285–95. https://doi.org/10.1016/0895-4356(90)90009-e.

    Article  PubMed  Google Scholar 

  46. White E, Patterson RE, Kristal AR, Thornquist M, King I, Shattuck AL, et al. VITamins and lifestyle cohort study: study design and characteristics of supplement users. Am J Epidemiol. 2004;159(1):83–93. https://doi.org/10.1093/aje/kwh010.

    Article  PubMed  Google Scholar 

  47. Ozasa K, Shimizu Y, Sakata R, Sugiyama H, Grant EJ, Soda M, et al. Risk of cancer and non-cancer diseases in the atomic bomb survivors. Radiat Prot Dosimetry. 2011;146(1–3):272–5. https://doi.org/10.1093/rpd/ncr168.

    CAS  Article  PubMed  Google Scholar 

  48. Radiation Effects Research Foundation Ethics Committee. https://www.rerforjp/en/programs/general_research_e/committee/. Accessed 15 July, 2019.

  49. Goossens ME, Isa F, Brinkman M, et al. International pooled study on diet and bladder cancer: the bladder cancer, epidemiology and nutritional determinants (BLEND) study: design and baseline characteristics. Arch Public Health. 2016;74(1):30–9. https://doi.org/10.1186/s13690-016-0140-1.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Satia-Abouta J, Patterson RE, King IB, Stratton KL, Shattuck AL, Kristal AR, et al. Reliability and validity of self-report of vitamin and mineral supplement use in the vitamins and lifestyle study. Am J Epidemiol. 2003;157(10):944–54. https://doi.org/10.1093/aje/kwg039.

    Article  PubMed  Google Scholar 

  51. Zeegers MP, Goldbohm RA, van den Brandt PA. Are retinol, vitamin C, vitamin E, folate and carotenoids intake associated with bladder cancer risk? Results from the NetherLands Cohort Study. Br J Cancer. 2001;85(7):977–83. https://doi.org/10.1054/bjoc.2001.1968.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. Sauvaget C, Allen N, Hayashi M, Spencer E, Nagano J. Validation of a food frequency questionnaire in the Hiroshima/Nagasaki Life Span Study. J Epidemiol. 2002;12(5):394–401. https://doi.org/10.2188/jea.12.394.

    Article  PubMed  Google Scholar 

  53. Ferrari P, Slimani N, Ciampi A, Trichopoulou A, Naska A, Lauria C, et al. Evaluation of under- and overreporting of energy intake in the 24-hour diet recalls in the European Prospective Investigation into Cancer and Nutrition (EPIC). Public Health Nutr. 2002;5(6b):1329–45. https://doi.org/10.1079/phn2002409.

    CAS  Article  PubMed  Google Scholar 

  54. Poortvliet E, Klensin J, Kohlmeier L. Rationale document for the Eurocode 2 food coding system (version 91/2). Eur J Clin Nutr. 1992;46(Suppl 5):S9–24.

    PubMed  Google Scholar 

  55. Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D. Meta-analysis for linear and nonlinear dose–response relations: examples, an evaluation of approximations, and software. Am J Epidemiol. 2012;175(1):66–73. https://doi.org/10.1093/aje/kwr265.

    Article  PubMed  Google Scholar 

  56. Desquilbet L, Mariotti F. Dose–response analyses using restricted cubic spline functions in public health research. Stat Med. 2010;29(9):1037–57. https://doi.org/10.1002/sim.3841.

    Article  PubMed  Google Scholar 

  57. Istvan J, Matarazzo JD. Tobacco, alcohol, and caffeine use: a review of their interrelationships. Psychol Bull. 1984;95(2):301–26. https://doi.org/10.1037/0033-2909.95.2.301.

    CAS  Article  PubMed  Google Scholar 

  58. Emurian HH, Nellis MJ, Brady JV, Ray RL. Event time-series relationship between cigarette smoking and coffee drinking. Addict Behav. 1982;7(4):441–4. https://doi.org/10.1016/0306-4603(82)90016-8.

    CAS  Article  PubMed  Google Scholar 

  59. Lane JD. Association of coffee drinking with cigarette smoking in the natural environment. Exp Clin Psychopharmacol. 1996;4(4):409. https://doi.org/10.1037/1064-1297.4.4.409.

    Article  Google Scholar 

  60. Brown CR, Jacob P 3rd, Wilson M, Benowitz NL. Changes in rate and pattern of caffeine metabolism after cigarette abstinence. Clin Pharmacol Ther. 1988;43(5):488–91. https://doi.org/10.1038/clpt.1988.63.

    CAS  Article  PubMed  Google Scholar 

  61. Swanson JA, Lee JW, Hopp JW, Berk LS. The impact of caffeine use on tobacco cessation and withdrawal. Addict Behav. 1997;22(1):55–68. https://doi.org/10.1016/S0306-4603(96)00023-8.

    CAS  Article  PubMed  Google Scholar 

  62. Langmann P, Bienert A, Zilly M, Väth T, Richter E, Klinker H. Influence of smoking on cotinine and caffeine plasma levels in patients with alcoholic liver cirrhosis. Eur J Med Res. 2000;5(5):217–21.

    CAS  PubMed  Google Scholar 

  63. Ossip DJ, Epstein LH. Relative effects of nicotine and coffee on cigarette smoking. Addict Behav. 1981;6(1):35–9. https://doi.org/10.1016/S0306-4603(81)80006-8.

    CAS  Article  PubMed  Google Scholar 

  64. Landi M, Sinha R, Lang N, Kadlubar F. Human cytochrome P4501A2. IARC Sci Publ. 1999;148:173–95.

    CAS  Google Scholar 

  65. Kalow W, Tang BK. Use of caffeine metabolite ratios to explore CYP1A2 and xanthine oxidase activities. Clin Pharmacol Ther. 1991;50(5–1):508–19.

    CAS  Article  PubMed  Google Scholar 

  66. Gunes A, Dahl M-L. Variation in CYP1A2 activity and its clinical implications: influence of environmental factors and genetic polymorphisms. Pharmacogenomics. 2008;9(5):625–37. https://doi.org/10.2217/14622416.9.5.625.

    CAS  Article  PubMed  Google Scholar 

  67. Yu EY, Wesselius A, van Osch F, Stern MC, Jiang X, Kellen E, et al. The association between coffee consumption and bladder cancer in the Bladder Cancer Epidemiology and Nutritional Determinants (BLEND) international pooled study. Cancer Causes Control CCC. 2019;30(8):859–70. https://doi.org/10.1007/s10552-019-01191-1.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Hashemian M, Sinha R, Murphy G, Weinstein SJ, Liao LM, Freedman ND, et al. Coffee and tea drinking and risk of cancer of the urinary tract in male smokers. Ann Epidemiol. 2019. https://doi.org/10.1016/j.annepidem.2019.03.014.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Wu W, Tong Y, Zhao Q, Yu G, Wei X, Lu Q. Coffee consumption and bladder cancer: a meta-analysis of observational studies. Sci Rep. 2015;5:1–9. https://doi.org/10.1038/srep09051.

    CAS  Article  Google Scholar 

  70. Dobruch J, Daneshmand S, Fisch M, Lotan Y, Noon AP, Resnick MJ, et al. Gender and bladder cancer: a collaborative review of etiology, biology, and outcomes. Eur Urol. 2016;69(2):300–10. https://doi.org/10.1016/j.eururo.2015.08.037.

    Article  PubMed  Google Scholar 

  71. Rothwell JA, Loftfield E, Wedekind R, Freedman N, Kambanis C, Scalbert A, et al. A metabolomic study of the variability of the chemical composition of commonly consumed coffee brews. Metabolites. 2019. https://doi.org/10.3390/metabo9010017.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Zhang Z-W, Xiao J, Luo W, Wang B-H, Chen J-M. Caffeine suppresses apoptosis of bladder cancer RT4 cells in response to ionizing radiation by inhibiting ataxia telangiectasia mutated-Chk2-p53 axis. Chin Med J. 2015;128(21):2938–45. https://doi.org/10.4103/0366-6999.168065.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  73. Sarkaria JN, Busby EC, Tibbetts RS, et al. Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 1999;59(17):4375–82.

    CAS  PubMed  Google Scholar 

  74. Tej G, Nayak PK. Mechanistic considerations in chemotherapeutic activity of caffeine. Biomed Pharmacother. 2018;105:312–9. https://doi.org/10.1016/j.biopha.2018.05.144.

    CAS  Article  PubMed  Google Scholar 

  75. Azam S, Hadi N, Khan NU, Hadi SM. Antioxidant and prooxidant properties of caffeine, theobromine and xanthine. Med Sci Monit Int Med J Exp Clin Res. 2003;9(9):Br325–30.

    CAS  Google Scholar 

  76. Venkata Charan Tej GN, Neogi K, Verma SS, Chandra Gupta S, Nayak PK. Caffeine-enhanced anti-tumor immune response through decreased expression of PD1 on infiltrated cytotoxic T lymphocytes. Eur J Pharmacol. 2019;859:172538. https://doi.org/10.1016/j.ejphar.2019.172538.

    CAS  Article  PubMed  Google Scholar 

  77. Maughan RJ, Griffin J. Caffeine ingestion and fluid balance: a review. J Hum Nutr Diet. 2003;16(6):411–20. https://doi.org/10.1046/j.1365-277x.2003.00477.x.

    CAS  Article  PubMed  Google Scholar 

  78. Renouf M, Marmet C, Guy P, Fraering AL, Longet K, Moulin J, et al. Nondairy creamer, but not milk, delays the appearance of coffee phenolic acid equivalents in human plasma. J Nutr. 2010;140(2):259–63. https://doi.org/10.3945/jn.109.113027.

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge all principal investigators for their willingness to participate in this jointed project. The author E Y.W. Yu gives thanks to the financial support from China Scholarship Council (No. 201706310135).

Funding

This work was partly funded by the World Cancer Research Fund International (WCRF 2012/590) and European Commission (FP7-PEOPLE-618308). The NetherLands Cohort Study on diet and cancer was supported by the Dutch Cancer Society. The RERF atomic bomb survivors Study was supported by The Radiation Effects Research Foundation (RERF), Hiroshima and Nagasaki, Japan, a public interest foundation funded by the Japanese Ministry of Health, Labour and Welfare (MHLW) and the US Department of Energy (DOE). The research was also funded in part through DOE award DE-HS0000031 to the National Academy of Sciences. This publication was supported by RERF Research Protocol RP-A5-12. The VITamins and Lifestyle Study (VITAL) was supported by a Grant (R01CA74846) from the National Cancer Institute. The European Prospective Investigation into Cancer and Nutrition (EPIC) was carried out with financial support of the ‘Europe Against Cancer’ Programme of the European Commission (SANCO); Ligue contre le Cancer (France); Société 3 M (France); Mutuelle Générale de l’Éducation Nationale; Institut National de la Santé et de la Recherche Médicale (INSERM); Institute Gustave Roussy; German Cancer Aid; German Cancer Research Centre; German Federal Ministry of Education and Research; Health Research Fund (FIS) of the Spanish Ministry of Health; the Spanish Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra; Cancer Research UK; Medical Research Council, UK; Stroke Association, UK; British Heart Foundation; Department of Health, UK; Food Standards Agency, UK; Wellcome Trust, UK; Greek Ministry of Health; Greek Ministry of Education; Italian Association for Research on Cancer; Italian National Research Council; Dutch Ministry of Public Health, Welfare and Sports; Dutch Prevention Funds; LK Research Funds; Dutch ZON (Zorg Onderzoek Nederland); World Cancer Research Fund; Swedish Cancer Society; Swedish Scientific Council; Regional Government of Skane, Sweden; Norwegian Cancer Society; Norwegian Research Council. Partial support for the publication of this supplement was provided by the Centre de Recherche et d’Information Nutritionnelles (CERIN).

Author information

Authors and Affiliations

Authors

Contributions

Study conception and design: AW and MPZ; Analyses and interpretation of data: EYY and YD; Drafting of the manuscript: EYY and YD; Revised the manuscript: AW, FVO, MB and MPZ; Provided the data: PvdB, EG, EW, EW, MG, BH; Approved the manuscript: all authors.

Corresponding author

Correspondence to Anke Wesselius.

Ethics declarations

Conflict of interest

All the authors declare no conflict of interest.

Ethics approval and consent to participate

Each participating study has been approved by the local ethic committee. Informed consent was obtained from all individual participants included in each study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Disclaimer: Where authors are identified as personnel of the International Agency for Research on Cancer/World Health Organization, the authors alone are responsible for the views expressed in this article and they do not necessarily represent the decisions, policy or views of the International Agency for Research on Cancer/World Health Organization.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 375 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yu, E.Y.W., Dai, Y., Wesselius, A. et al. Coffee consumption and risk of bladder cancer: a pooled analysis of 501,604 participants from 12 cohort studies in the BLadder Cancer Epidemiology and Nutritional Determinants (BLEND) international study. Eur J Epidemiol 35, 523–535 (2020). https://doi.org/10.1007/s10654-019-00597-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10654-019-00597-0

Keywords

  • Bladder cancer
  • Coffee consumption
  • Smoking
  • Dose–response analyses
  • Cohort study