Life course sun exposure and risk of prostate cancer: Population-based nested case-control study and meta-analysis
Corresponding Author
Rebecca Gilbert
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Fax: +44-117-3313914.
University of Bristol, Department of Social Medicine, Canynge Hall, 39 Whatley Road, Bristol BS8 2PS, United KingdomSearch for more papers by this authorChris Metcalfe
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorSteven E. Oliver
Department of Health Sciences, University of York and the Hull York Medical School, York, United Kingdom
Search for more papers by this authorDavid C. Whiteman
Division of Population Studies and Human Genetics, Queensland Institute of Medical Research, Queensland, Australia
Search for more papers by this authorChris Bain
School of Population Health, The University of Queensland, Queensland, Australia
Search for more papers by this authorAndy Ness
Department of Oral and Dental Science, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorJenny Donovan
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorFreddie Hamdy
Nuffield Department of Surgery, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorDavid E. Neal
Department of Oncology, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorJ. Athene Lane
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorRichard M. Martin
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorCorresponding Author
Rebecca Gilbert
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Fax: +44-117-3313914.
University of Bristol, Department of Social Medicine, Canynge Hall, 39 Whatley Road, Bristol BS8 2PS, United KingdomSearch for more papers by this authorChris Metcalfe
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorSteven E. Oliver
Department of Health Sciences, University of York and the Hull York Medical School, York, United Kingdom
Search for more papers by this authorDavid C. Whiteman
Division of Population Studies and Human Genetics, Queensland Institute of Medical Research, Queensland, Australia
Search for more papers by this authorChris Bain
School of Population Health, The University of Queensland, Queensland, Australia
Search for more papers by this authorAndy Ness
Department of Oral and Dental Science, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorJenny Donovan
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorFreddie Hamdy
Nuffield Department of Surgery, University of Oxford, Oxford, United Kingdom
Search for more papers by this authorDavid E. Neal
Department of Oncology, University of Cambridge, Cambridge, United Kingdom
Search for more papers by this authorJ. Athene Lane
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorRichard M. Martin
Department of Social Medicine, University of Bristol, Bristol, United Kingdom
Search for more papers by this authorAbstract
There is currently no means of primary prevention for prostate cancer. Increased exposure to ultraviolet-radiation may be protective, but the literature is inconclusive. We investigated associations of life course exposure to sunlight with prostate cancer. The study design was a UK-wide nested case-control study, based on 1,020 prostate specific antigen-detected cases and 5,044 matched population controls and a systematic review with meta-analysis. Men with olive/brown skin (OR = 1.47; 95% CI: 1.00 to 2.17), men who burnt rarely/never (OR = 1.11; 0.95 to 1.29) and men with the lowest levels of intense sun exposure in the 2 years prior to diagnosis (OR = 1.24; 1.03 to 1.50) had an increased prostate cancer risk. However, amongst men with prostate cancer, spending less time outside was associated with a reduced risk of advanced cancer (OR = 0.49; 0.27 to 0.89) and high Gleason grade (OR = 0.62; 0.43 to 0.91), and men who burnt rarely/never had a reduced risk of advanced cancer (OR = 0.71; 0.47 to 1.08). The meta-analysis provided weak evidence that men with the lowest (versus highest) sunlight exposure had an increased prostate cancer risk (4 studies, random-effects pooled relative risk = 1.13; 0.98 to 1.29) and higher advanced or fatal prostate cancer risk (6 studies, random-effects pooled relative risk = 1.14; 0.98 to 1.33). Our data and meta-analyses provide limited support for the hypothesis that increased exposure to sunlight may reduce prostate cancer risk. The findings warrant further investigation because of their implications for vitamin D chemoprevention trials. © 2009 UICC
References
- 1 Parkin DM,Bray FI,Devesa SS. Cancer burden in the year 2000. The global picture. Eur J Cancer 2001; 37( .Suppl 8): 4–66.
- 2 Cancer Research UK. Commonly diagnosed cancers worldwide. Available at http://info.cancerresearchuk.org/cancerstats/geographic/world/commoncancers/. Accessed on 2008 March 19.
- 3 Gronberg H. Prostate cancer epidemiology. Lancet 2003; 361: 859–64.
- 4 World Cancer Research Fund/American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of cancer: a global perspective. Washington DC: AICR, 2007.
- 5
Hanchette CL,Schwartz GG.
Geographic patterns of prostate cancer mortality. Evidence for a protective effect of ultraviolet radiation.
Cancer
1992;
70:
2861–9.
10.1002/1097-0142(19921215)70:12<2861::AID-CNCR2820701224>3.0.CO;2-G CAS PubMed Web of Science® Google Scholar
- 6 Schwartz GG,Hanchette CL. UV, latitude, and spatial trends in prostate cancer mortality: all sunlight is not the same (United States). Cancer Causes Control 2006; 17: 1091–101.
- 7 Giovannucci E. The epidemiology of vitamin D and cancer incidence and mortality: a review (United States). Cancer Causes Control 2005; 16: 83–95.
- 8 Schwartz GG. Vitamin D and the epidemiology of prostate cancer. Semin Dial 2005; 18: 276–89.
- 9 Polek TC,Weigel NL. Vitamin D and prostate cancer. J Androl 2002; 23: 9–17.
- 10 Garland CF,Garland FC,Gorham ED,Lipkin M,Newmark H,Mohr SB,Holick MF. The role of vitamin D in cancer prevention. Am J Public Health 2006; 96: 252–61.
- 11 Lou YR,Qiao S,Talonpoika R,Syvala H,Tuohimaa P. The role of Vitamin D3 metabolism in prostate cancer. J Steroid Biochem Mol Biol 2004; 92: 317–25.
- 12 Kricker A,Armstrong B. Does sunlight have a beneficial influence on certain cancers? Prog Biophys Mol Biol 2006; 92: 132–9.
- 13 van der Rhee HJ,de Vries E,Coebergh JWW. Does sunlight prevent cancer? A systematic review. Eur J Cancer 2006; 42: 2222–32.
- 14 Ben-Shlomo Y,Evans S,Ibrahim F,Patel B,Anson K,Chinegwundoh F,Corbishley C,Dorling D,Thomas B,Gillatt D,Kirby R,Muir G, et al. The risk of prostate cancer amongst black men in the United Kingdom: the PROCESS cohort study. Eur Urol 2008; 53: 99–105.
- 15 Luscombe CJ,French ME,Liu S,Saxby MF,Jones PW,Fryer AA,Strange RC. Outcome in prostate cancer associations with skin type and polymorphism in pigmentation-related genes. Carcinogenesis 2001; 22: 1343–7.
- 16 Grant WB. Geographic variation of prostate cancer mortality rates in the United States: implications for prostate cancer risk related to vitamin D. [Comment]. Int J Cancer 2004; 111: 470–1.
- 17 Donovan J,Hamdy F,Neal D,Peters T,Oliver S,Brindle L,Jewell D,Powell P,Gillatt D,Dedman D,Mills N,Smith M, et al. Prostate Testing for cancer and treatment (ProtecT) feasibility study. Health Technol Assess (Winchester, England) 2003; 7: 1–88.
- 18
Ohori M,Wheeler TM,Scardino PT.
The new American joint committee on cancer and international union against cancer. TNM classification of prostate cancer. Clinicopathologic correlations.
Cancer
1994;
74:
104–14.
10.1002/1097-0142(19940701)74:1<104::AID-CNCR2820740119>3.0.CO;2-5 CAS PubMed Web of Science® Google Scholar
- 19 Harvey I,Frankel S,Marks R,Shalom D,Nolan-Farrell M. Non-melanoma skin cancer and solar keratoses II analytical results of the South Wales Skin Cancer Study. Br J Cancer 1996; 74: 1308–12.
- 20 Harvey I,Frankel S,Marks R,Shalom D,Nolan-Farrell M. Non-melanoma skin cancer and solar keratoses. I. Methods and descriptive results of the. South Wales Skin Cancer Study. Br J Cancer 1996; 74: 1302–7.
- 21 Han J,Colditz GA,Hunter DJ. Risk factors for skin cancers: a nested case-control study within the Nurses' Health Study. Int J Epidemiol 2006; 35: 1514–21.
- 22 Whiteman D,Green A. Wherein lies the truth? Assessment of agreement between parent proxy and child respondents. Int J Epidemiol 1997; 26: 855–9.
- 23
Whiteman DC,Valery P,McWhirter W,Green AC.
Risk factors for childhood melanoma in Queensland, Australia.
Int J Cancer
1997;
70:
26–31.
10.1002/(SICI)1097-0215(19970106)70:1<26::AID-IJC4>3.0.CO;2-8 CAS PubMed Web of Science® Google Scholar
- 24 Green A,Siskind V,Bain C,Alexander J. Sunburn and malignant melanoma. Br J Cancer 1985; 51: 393–7.
- 25 Green A,Bain C,McLennan R,Siskind V. Risk factors for cutaneous melanoma in Queensland. Recent Results Cancer Res 1986; 102: 76–97.
- 26 Whiteman DC,Stickley M,Watt P,Hughes MC,Davis MB,Green AC. Anatomic site, sun exposure, and risk of cutaneous melanoma. J Clin Oncol 2006; 24: 3172–7.
- 27 Higgins JP,Thompson SG,Deeks JJ,Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557–60.
- 28 Luscombe CJ,Fryer AA,French ME,Liu S,Saxby MF,Jones PW,Strange RC. Exposure to ultraviolet radiation: association with susceptibility and age at presentation with prostate cancer. Lancet 2001; 358: 641–2.
- 29 Bodiwala D,Luscombe CJ,French ME,Liu S,Saxby MF,Jones PW,Fryer AA,Strange RC. Associations between prostate cancer susceptibility and parameters of exposure to ultraviolet radiation. Cancer Lett 2003; 200: 141–8.
- 30 Bodiwala D,Luscombe CJ,French ME,Liu S,Saxby MF,Jones PW,Ramachandran S,Fryer AA,Strange RC. Susceptibility to prostate cancer: studies on interactions between UVR exposure and skin type. Carcinogenesis 2003; 24: 711–7.
- 31 Bodiwala D,Luscombe CJ,Liu S,Saxby M,French M,Jones PW,Fryer AA,Strange RC. Prostate cancer risk and exposure to ultraviolet radiation: further support for the protective effect of sunlight. Cancer Lett 2003; 192: 145–9.
- 32 Rukin N,Blagojevic M,Luscombe CJ,Liu S,Saxby MF,Ramachandran S,Fryer AA,Jones PW,Strange RC. Associations between timing of exposure to ultraviolet radiation. T-stage and survival in prostate cancer. Cancer Detect Prev 2007; 31: 443–9.
- 33 John EM,Dreon DM,Koo J,Schwartz GG. Residential sunlight exposure is associated with a decreased risk of prostate cancer. J Steroid Biochem Mol Biol 2004; 89–90: 549–52.
- 34 Freedman DM,Dosemeci M,McGlynn K. Sunlight and mortality from breast, ovarian, colon, prostate, and non-melanoma skin cancer: a composite death certificate based case-control study. Occup Environ Med 2002; 59: 257–62.
- 35 Rukin NJ,Zeegers MP,Ramachandran S,Luscombe CJ,Liu S,Saxby M,Lear J,Strange RC. A comparison of sunlight exposure in men with prostate cancer and basal cell carcinoma. Br J Cancer 2007; 96: 523–8.
- 36 de Vries E,Soerjomataram I,Houterman S,Louwman MWJ,Coebergh JW. Decreased risk of prostate cancer after skin cancer diagnosis: a protective role of ultraviolet radiation? Am J Epidemiol 2007; 165: 966–72.
- 37 John EM,Koo J,Schwartz GG. Sun exposure and prostate cancer risk: evidence for a protective effect of early-life exposure. Cancer Epidemiol Biomarkers Prev 2007; 16: 1283–6.
- 38 John EM,Schwartz GG,Koo J,Van Den Berg D,Ingles SA. Sun exposure, vitamin d receptor gene polymorphisms, and risk of advanced prostate cancer. Cancer Res 2005; 65: 5470–9.
- 39 Robsahm TE,Tretli S,Dahlback A,Moan J. Vitamin D3 from sunlight may improve the prognosis of breast-, colon- and prostate cancer (Norway). Cancer Causes Control 2004; 15: 149–58.
- 40 Willis MS,Wians FH. The role of nutrition in preventing prostate cancer: a review of the proposed mechanism of action of various dietary substances. Clin Chim Acta 2003; 330: 57–83.
- 41 Lokeshwar BL,Schwartz GG,Selzer MG,Burnstein KL,Zhuang SH,Block NL,Binderup L. Inhibition of prostate cancer metastasis in vivo: a comparison of 1,25-dihydroxyvitamin d (calcitriol) and EB1089. Cancer Epidemiol Biomarkers Prev 1999; 8: 241–8.
- 42 Stewart LV,Weigel NL. Vitamin D and prostate cancer. Exp Biol Med 2004; 229: 277–84.
- 43 MacLaughlin J,Holick MF. Aging decreases the capacity of human skin to produce vitamin D3. J Clin Invest 1985; 76: 1536–8.
- 44 Platz EA,Rimm EB,Willett WC,Kantoff PW,Giovannucci E. Racial variation in prostate cancer incidence and in hormonal system markers among male health professionals. J Natl Cancer Inst 2000; 92: 2009–17.
- 45 Vieth R. Vitamin D supplementation, 25-hydroxyvitamin D concentrations, and safety. Am J Clin Nutr 1999; 69: 842–56.
- 46 Tuohimaa P,Tenkanen L,Ahonen M,Lumme S,Jellum E,Hallmans G,Stattin P,Harvei S,Hakulinen T,Luostarinen T,Dillner J,Lehtinen M, et al. Both high and low levels of blood vitamin D are associated with a higher prostate cancer risk: a longitudinal, nested case-control study in the Nordic countries. Int J Cancer 2004; 108: 104–8.
- 47 Ahn J,Peters U,Albanes D,Purdue MP,Abnet CC,Chatterjee N,Horst RL,Hollis BW,Huang WY,Shikany JM,Hayes RB. For the prostate LCaOCSTPT serum vitamin D concentration and prostate cancer risk: a nested case-control study. J Natl Cancer Inst 2008; 100: 796–804.
- 48 Mikhak B,Hunter DJ,Spiegelman D,Platz EA,Hollis BW,Giovannucci E. Vitamin D receptor (VDR) gene polymorphisms and haplotypes, interactions with plasma 25-hydroxyvitamin D and 1,25-dihydroxyvitamin D, and prostate cancer risk. Prostate 2007; 67: 911–23.
- 49 Miller GJ,Stapleton GE,Hedlund TE,Moffat KA. Vitamin D receptor expression, 24-hydroxylase activity, and inhibition of growth by 1alpha,25-dihydroxyvitamin D3 in seven human prostatic carcinoma cell lines. Clin Cancer Res 1995; 1: 997–1003.
- 50 Albertson DG,Ylstra B,Segraves R,Collins C,Dairkee SH,Kowbel D,Kuo WL,Gray JW,Pinkel D. Quantitative mapping of amplicon structure by array CGH identifies CYP24 as a candidate oncogene. Nat Genet 2000; 25: 144–6.
- 51 Peehl DM,Feldman D. The role of vitamin D and retinoids in controlling prostate cancer progression. Endocr Relat Cancer 2003; 10: 131–40.
- 52 Ma JF,Nonn L,Campbell MJ,Hewison M,Feldman D,Peehl DM. Mechanisms of decreased Vitamin D 1 alpha-hydroxylase activity in prostate cancer cells. Mol Cell Endocrinol 2004; 221: 67–74.
- 53 Holick MF. McCollum award lecture, 1994: vitamin D—new horizons for the 21st century. Am J Clin Nutr 1994; 60: 619–30.
- 54 Wolpowitz D,Gilchrest BA. The vitamin D questions: how much do you need and how should you get it? J Am Acad Dermatol 2006; 54: 301–17.
- 55 Waltz P,Chodick G. International comparisons of prostate cancer mortality rates with dietary practices and sunlight levels. Urol Oncol: Semin Orig Investig 2007; 25: 85.
- 56 English DR,Armstrong BK,Kricker A. Reproducibility of reported measurements of sun exposure in a case-control study. Cancer Epidemiol Biomarkers Prev 1998; 7: 857–63.
- 57 Thompson IM,Ankerst DP,Chi C,Lucia MS,Goodman PJ,Crowley JJ,Parnes HL,Coltman CA,Jr. Operating characteristics of prostate-specific antigen in men with an initial PSA level of 3.0 ng/mL or lower. JAMA 2005; 294: 66–70.
- 58 European Travel Commission. European Tourism Insights 2007. Europe: European Travel Commission, 2008.
- 59 Thompson IM,Goodman PJ,Tangen CM,Lucia MS,Miller GJ,Ford LG,Lieber MM,Cespedes RD,Atkins JN,Lippman SM,Carlin SM,Ryan A, et al. The influence of finasteride on the development of prostate cancer. N Engl J Med 2003; 349: 215–24.
Citing Literature
