Abstract
Background
Observational studies suggest an association between fruit and vegetables intake and risk of bladder cancer, but the results are controversial.
Methods
We therefore summarized the evidence from observational studies in categorical, linear, and nonlinear, dose–response meta-analysis. Pertinent studies were identified by searching EMBASE and PubMed from their inception to August 2013.
Results
Thirty-one observational studies involving 12,610 cases and 1,121,649 participants were included. The combined rate ratio (RR, 95 % CI) of bladder cancer for the highest versus lowest intake was 0.83 (0.69–0.99) for total fruit and vegetables, 0.81 (0.70–0.93) for total vegetables, 0.77 (0.69–0.87) for total fruit, 0.84 (0.77–0.91) for cruciferous vegetables, 0.79 (0.68–0.91) for citrus fruits, and 0.74 (0.66–0.84) for yellow–orange vegetables. Subgroup analysis showed study design and gender as possible sources of heterogeneity. A nonlinear relationship was found of citrus fruits intake with risk of bladder cancer (P for nonlinearity = 0.018), and the RRs (95 % CI) of bladder cancer were 0.87 (0.78–0.96), 0.80 (0.67–0.94), 0.79 (0.66–0.94), 0.79 (0.65–0.96), and 0.79 (0.64–0.99) for 30, 60, 90, 120, and 150 g/day. A nonlinear relationship was also found of yellow–orange vegetable intake with risk of bladder cancer risk (P for nonlinearity = 0.033). Some evidence of publication bias was observed for fruit, citrus fruits, and yellow–orange vegetables.
Conclusion
This meta-analysis supports the hypothesis that intakes of fruit and vegetables may reduce the risk of bladder cancer. Future well-designed studies are required to confirm this finding.
Similar content being viewed by others
References
World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington
Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63:11–30
Freedman ND, Silverman DT, Hollenbeck AR, Schatzkin A, Abnet CC (2011) Association between smoking and risk of bladder cancer among men and women. JAMA 306:737–745
Report of an IARC Working Group, Althouse R, Huff J, Tomatis L, Wllbourn J (1980) An evaluation of chemicals and industrial processes associated with cancer in humans based on human and animal data: IARC monographs volumes 1 to 20. Cancer Res 40:1–12
Badawi AF, Mostafa MH, Probert A, O’Connor PJ (1995) Role of schistosomiasis in human bladder cancer: evidence of association, aetiological factors, and basic mechanisms of carcinogenesis. Eur J Cancer Prev 4:45–59
Steinmetz KA, Potter JD (1991) Vegetables, fruit, and cancer. I. Epidemiology. Cancer Causes Control 2:325–357
Balbi JC, Larrinaga MT, De Stefani E, Mendilaharsu M, Ronco AL, Boffetta P, Brennan P (2001) Foods and risk of bladder cancer: a case–control study in Uruguay. Eur J Cancer Prev 10:453–458
Castelao JE, Yuan JM, Gago-Dominguez M, Skipper PL, Tannenbaum SR, Chan KK, Watson MA, Bell DA, Coetzee GA, Ross RK, Yu MC (2004) Carotenoids/vitamin C and smoking-related bladder cancer. Int J Cancer 110:417–423
Nagano J, Kono S, Preston DL, Moriwaki H, Sharp GB, Koyama K, Mabuchi K (2000) Bladder-cancer incidence in relation to vegetable and fruit consumption: a prospective study of atomic-bomb survivors. Int J Cancer 86:132–138
Wu JW, Cross AJ, Baris D, Ward MH, Karagas MR, Johnson A, Schwenn M, Cherala S, Colt JS, Cantor KP, Rothman N, Silverman DT, Sinha R (2012) Dietary intake of meat, fruits, vegetables, and selective micronutrients and risk of bladder cancer in the New England region of the United States. Br J Cancer 106:1891–1898
Isa F, Xie LP, Hu Z, Zhong Z, Hemelt M, Reulen RC, Wong YC, Tam PC, Yang K, Chai C, Zeng X, Deng Y, Zhong WD, Zeegers MP (2013) Dietary consumption and diet diversity and risk of developing bladder cancer: results from the South and East China case–control study. Cancer Causes Control 24:885–895
Ros MM, Bueno-de-Mesquita HB, Kampman E, Büchner FL, Aben KK, Egevad L, Overvad K, Tjønneland A, Roswall N, Clavel-Chapelon F, Boutron-Ruault MC, Morois S, Kaaks R, Teucher B, Weikert S, von Ruesten A, Trichopoulou A, Naska A, Benetou V, Saieva C, Pala V, Ricceri F, Tumino R, Mattiello A, Peeters PH, van Gils CH, Gram IT, Engeset D, Chirlaque MD, Ardanazx E, Rodríguez L, Amanio P, Gonzalez CA, Sánchez MJ, Ulmert D, Ernström R, Ljungberg B, Allen NE, Key TJ, Khaw KT, Wareham N, Slimani N, Romieu I, Kiemeney LA, Riboli E (2012) Fruit and vegetable consumption and risk of aggressive and non-aggressive urothelial cell carcinomas in the European Prospective Investigation into Cancer and Nutrition. Eur J Cancer 48:3267–3277
Park SY, Ollberding NJ, Woolcott CG, Wilkens LR, Henderson BE, Kolonel LN (2013) Fruit and vegetable intakes are associated with lower risk of bladder cancer among women in the Multiethnic Cohort Study. J Nutr 143:1283–1292
Brinkman M, Zeegers MP (2008) Nutrition, total fluid and bladder cancer. Scand J Urol Nephrol Suppl 218:25–36
Aune D, Lau R, Chan DS, Vieira R, Greenwood DC, Kampman E, Norat T (2011) Nonlinear reduction in risk for colorectal cancer by fruit and vegetable intake based on meta-analysis of prospective studies. Gastroenterology 141:106–118
Liu J, Wang J, Leng Y, Lv C (2013) Intake of fruit and vegetables and risk of esophageal squamous cell carcinoma: a meta-analysis of observational studies. Int J Cancer 133:473–485
Dauchet L, Amouyel P, Hercberg S, Dallongeville J (2006) Fruit and vegetable consumption and risk of coronary heart disease: a meta-analysis of cohort studies. J Nutr 136:2588–2593
Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560
Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634
Tobias A (1999) Assessing the influence of a single study in the meta-analysis estimate. Stata Tech Bull 47:15–17
Orsini N, Li R, Wolk A, Khudyakov P, Spiegelman D (2012) Meta-analysis for linear and nonlinear dose–response relations: examples, an evaluation of approximations, and software. Am J Epidemiol 175:66–73
Durrleman S, Simon R (1989) Flexible regression models with cubic splines. Stat Med 8:551–561
Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose-response data. Stat J 6:40–57
Jackson D, White IR, Thompson SG (2010) Extending DerSimonian and Laird’s methodology to perform multivariate random effects meta-analyses. Stat Med 29:1282–1297
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
Riboli E, González CA, López-Abente G, Errezola M, Izarzugaza I, Escolar A, Nebot M, Hémon B, Agudo A (1991) Diet and bladder cancer in Spain: a multi-centre case–control study. Int J Cancer 49:214–219
Negri E, La Vecchia C, Franceschi S, D’Avanzo B, Parazzini F (1991) Vegetable and fruit consumption and cancer risk. Int J Cancer 48:350–354
Bruemmer B, White E, Vaughan TL, Cheney CL (1996) Nutrient intake in relation to bladder cancer among middle-aged men and women. Am J Epidemiol 144:485–495
Yu Y, Hu J, Wang PP, Zou Y, Qi Y, Zhao P, Xe R (1997) Risk factors for bladder cancer: a case–control study in northeast China. Eur J Cancer Prev 6:363–369
Pohlabeln H, Jöckel KH, Bolm-Audorff U (1999) Non-occupational risk factors for cancer of the lower urinary tract in Germany. Eur J Epidemiol 15:411–419
Wakai K, Takashi M, Okamura K, Yuba H, Suzuki K, Murase T, Obata K, Itoh H, Kato T, Kobayashi M, Sakata T, Otani T, Ohshima S, Ohno Y (2000) Foods and nutrients in relation to bladder cancer risk: a case–control study in Aichi Prefecture, Central Japan. Nutr Cancer 38:13–22
Peluso M, Airoldi L, Magagnotti C, Fiorini L, Munnia A, Hautefeuille A, Malaveille C, Vineis P (2000) White blood cell DNA adducts and fruit and vegetable consumption in bladder cancer. Carcinogenesis 21:183–187
Pelucchi C, La Vecchia C, Negri E, Dal Maso L, Franceschi S (2002) Smoking and other risk factors for bladder cancer in women. Prev Med 35:114–120
Wakai K, Hirose K, Takezaki T, Hamajima N, Ogura Y, Nakamura S, Hayashi N, Tajima K (2004) Foods and beverages in relation to urothelial cancer: case–control study in Japan. Int J Urol 11:11–19
Schabath MB, Spitz MR, Lerner SP, Pillow PC, Hernandez LM, Delclos GL, Grossman HB, Wu X (2005) Case–control analysis of dietary folate and risk of bladder cancer. Nutr Cancer 53:144–151
Kellen E, Zeegers M, Paulussen A, Van Dongen M, Buntinx F (2006) Fruit consumption reduces the effect of smoking on bladder cancer risk. The Belgian case control study on bladder cancer. Int J Cancer 118:2572–2578
García-Closas R, García-Closas M, Kogevinas M, Malats N, Silverman D, Serra C, Tardón A, Carrato A, Castaño-Vinyals G, Dosemeci M, Moore L, Rothman N, Sinha R (2007) Food, nutrient and heterocyclic amine intake and the risk of bladder cancer. Eur J Cancer 43:1731–1740
Sacerdote C, Matullo G, Polidoro S, Gamberini S, Piazza A, Karagas MR, Rolle L, De Stefanis P, Casetta G, Morabito F, Vineis P, Guarrera S (2007) Intake of fruits and vegetables and polymorphisms in DNA repair genes in bladder cancer. Mutagenesis 22:281–285
Tang L, Zirpoli GR, Guru K, Moysich KB, Zhang Y, Ambrosone CB, McCann SE (2008) Consumption of raw cruciferous vegetables is inversely associated with bladder cancer risk. Cancer Epidemiol Biomarkers Prev 17:938–944
Lin J, Kamat A, Gu J, Chen M, Dinney CP, Forman MR, Wu X (2009) Dietary intake of vegetables and fruits and the modification effects of GSTM1 and NAT2 genotypes on bladder cancer risk. Cancer Epidemiol Biomarkers Prev 18:2090–2097
Pavanello S, Mastrangelo G, Placidi D, Campagna M, Pulliero A, Carta A, Arici C, Porru S (2010) CYP1A2 polymorphisms, occupational and environmental exposures and risk of bladder cancer. Eur J Epidemiol 25:491–500
Kellen E, Zeegers M, Buntinx F (2006) Selenium is inversely associated with bladder cancer risk: a report from the Belgian case–control study on bladder cancer. Int J Urol 13:1180–1184
Steineck G, Norell SE, Feychting M (1988) Diet, tobacco and urothelial cancer. A 14-year follow-up of 16,477 subjects. Acta Oncol 27:323–327
Shibata A, Paganini-Hill A, Ross RK, Henderson BE (1992) Intake of vegetables, fruits, beta-carotene, vitamin C and vitamin supplements and cancer incidence among the elderly: a prospective study. Br J Cancer 66:673–679
Chyou PH, Nomura AM, Stemmermann GN (1993) A prospective study of diet, smoking, and lower urinary tract cancer. Ann Epidemiol 3:211–216
Michaud DS, Spiegelman D, Clinton SK, Rimm EB, Willett WC, Giovannucci EL (1999) Fruit and vegetable intake and incidence of bladder cancer in a male prospective cohort. J Natl Cancer Inst 91:605–613
Zeegers MP, Goldbohm RA, van den Brandt PA (2001) Consumption of vegetables and fruits and urothelial cancer incidence: a prospective study. Cancer Epidemiol Biomarkers Prev 10:1121–1128
Michaud DS, Pietinen P, Taylor PR, Virtanen M, Virtamo J, Albanes D (2002) Intakes of fruits and vegetables, carotenoids and vitamins A, E, C in relation to the risk of bladder cancer in the ATBC cohort study. Br J Cancer 87:960–965
Larsson SC, Andersson SO, Johansson JE, Wolk A (2008) Fruit and vegetable consumption and risk of bladder cancer: a prospective cohort study. Cancer Epidemiol Biomarkers Prev 17:2519–2522
Holick CN, De Vivo I, Feskanich D, Giovannucci E, Stampfer M, Michaud DS (2005) Intake of fruits and vegetables, carotenoids, folate, and vitamins A, C, E and risk of bladder cancer among women (United States). Cancer Causes Control 16:1135–1145
Büchner FL, Bueno-de-Mesquita HB, Ros MM, Kampman E, Egevad L, Overvad K, Raaschou-Nielsen O, Tjønneland A, Roswall N, Clavel-Chapelon F, Boutron-Ruault MC, Touillaud M, Chang-Claude J, Kaaks R, Boeing H, Weikert S, Trichopoulou A, Lagiou P, Trichopoulos D, Palli D, Sieri S, Vineis P, Tumino R, Panico S, Vrieling A, Peeters PH, van Gils CH, Lund E, Gram IT, Engeset D, Martinez C, Gonzalez CA, Larrañaga N, Ardanaz E, Navarro C, Rodríguez L, Manjer J, Ehrnström RA, Hallmans G, Ljungberg B, Allen NE, Roddam AW, Bingham S, Khaw KT, Slimani N, Boffetta P, Jenab M, Mouw T, Michaud DS, Kiemeney LA, Riboli E (2009) Consumption of vegetables and fruit and the risk of bladder cancer in the European Prospective Investigation into Cancer and Nutrition. Int J Cancer 125:2643–2651
Conflict of interest
No conflict of interest existed for any of the authors.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yao, B., Yan, Y., Ye, X. et al. Intake of fruit and vegetables and risk of bladder cancer: a dose–response meta-analysis of observational studies. Cancer Causes Control 25, 1645–1658 (2014). https://doi.org/10.1007/s10552-014-0469-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-014-0469-0