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Sunlight exposure in association with risk of lymphoid malignancy: a meta-analysis of observational studies

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Abstract

Purpose

Several observational studies have shown contradictory results regarding the association between sunlight exposure and the risk of malignant lymphoma. Thus, we aimed to systematically determine the association between sunlight exposure and lymphoid malignancy risk through a meta-analysis.

Methods

A thorough search of four electronic databases (PubMed, Embase, Web of Science, and Scopus) was performed to identify eligible studies until 13 August 2020. A random-effects model was used to calculate risk estimates of sunlight exposure. The main outcome measure was the risk of lymphoid malignancy subtypes with odds ratios (ORs) and 95% confidence intervals (CIs) according to various forms of solar ultraviolet radiation.

Results

In total, 17 case–control studies and 9 cohort studies including 216,285 non-Hodgkin lymphoma (NHL) and 23,017 Hodgkin’s lymphoma (HL) patients were included in the final analysis. Personal sunlight exposure was significantly associated with a decreased risk of HL (OR 0.77; 95% CI 0.68–0.87) and NHL (OR 0.81; 95% CI 0.71–0.92), including all subtypes except T-cell lymphoma. Ambient sunlight exposure at residence was associated with a reduced risk of HL (OR 0.88; 95% CI 0.81–0.95) and all NHL subtypes (OR 0.84; 95% CI 0.73–0.96), except for chronic lymphocytic leukemia/small lymphocytic lymphoma. As the number of sunburns and sunbaths increased, the risk of NHL tended to decrease.

Conclusion

While there was an observed protective effect both from case–control and prospective studies, substantial heterogeneity was found in the current study. Thus, more evidence is required to confirm that promoting sunlight exposure can prevent the development of lymphoid neoplasia.

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References

  1. Allemani C, Matsuda T, Di Carlo V et al (2018) Global surveillance of trends in cancer survival 2000–14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 391:1023–1075

    Article  PubMed  PubMed Central  Google Scholar 

  2. American Cancer Society (2010) Cancer facts & figures 2010. American Cancer Society, Atlanta, p 68

    Google Scholar 

  3. Morton LM, Slager SL, Cerhan JR et al (2014) Etiologic heterogeneity among non-Hodgkin lymphoma subtypes: the InterLymph Non-Hodgkin Lymphoma subtypes project. J Natl Cancer Inst Monogr 2014:130–144

    Article  PubMed  PubMed Central  Google Scholar 

  4. Hidayat K, Li HJ, Shi BM (2018) Anthropometric factors and non-Hodgkin’s lymphoma risk: systematic review and meta-analysis of prospective studies. Crit Rev Oncol Hematol 129:113–123

    Article  PubMed  Google Scholar 

  5. Cartwright RA, Watkins G (2004) Epidemiology of Hodgkin’s disease: a review. Hematol Oncol 22:11–26

    Article  CAS  PubMed  Google Scholar 

  6. International Agency for Research on Cancer (1992) IARC monographs on the evaluation of carcinogenic risks to humans. Solar and ultraviolet radiation, vol 55. International Agency for Research on Cancer, Lyon, pp 1–316

    Google Scholar 

  7. Frisch M, Hjalgrim H, Olsen JH, Melbye M (1996) Risk for subsequent cancer after diagnosis of basal-cell carcinoma. A population based, epidemiologic study. Ann Intern Med 125:815–821

    Article  CAS  PubMed  Google Scholar 

  8. Levi F, Randimbison L, Te VC, La Vecchia C (1996) Non-Hodgkin’s lymphomas, chronic lymphocytic leukaemias and skin cancers. Br J Cancer 74:1847–1850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Krilaviciute A, Vincerzevskiene I, Smailyte G (2016) Basal cell skin cancer and the risk of second primary cancers: a cancer registry-based study in Lithuania. Ann Epidemiol 26:511–514

    Article  PubMed  Google Scholar 

  10. Cooper KD, Oberhelman L, Hamilton T et al (1992) UV exposure reduces immunization rates and promotes tolerance to epicutaneous antigens in humans: relationship to dose, CD1a-DR+ epidermal macrophage induction, and Langerhans cell depletion. Proc Natl Acad Sci USA 89:8497–8501

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Opelz G, Henderson R (1993) Incidence of non-Hodgkin lymphoma in kidney and heart transplant recipients. Lancet 342:1514–1516

    Article  CAS  PubMed  Google Scholar 

  12. Kasiske BL, Snyder JJ, Gilbertson DT, Wang C (2004) Cancer after kidney transplantation in the United States. Am J Transplant 4:905–913

    Article  PubMed  Google Scholar 

  13. Kinlen LJ (1992) Immunosuppressive therapy and acquired immunological disorders. Cancer Res 52:5474s–5476s

    CAS  PubMed  Google Scholar 

  14. McMichael AJ, Giles GG (1996) Have increases in solar ultraviolet exposure contributed to the rise in incidence of non-Hodgkin’s lymphoma? Br J Cancer 73:945–950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hartge P, Devesa SS, Grauman D, Fears TR, Fraumeni JF Jr (1996) Non Hodgkin’s lymphoma and sunlight. J Natl Cancer Inst 88:298–300

    Article  CAS  PubMed  Google Scholar 

  16. Boscoe FP, Schymura MJ (2006) Solar ultraviolet-B exposure and cancer incidence and mortality in the United States, 1993–2002. BMC Cancer 6:264

    Article  PubMed  PubMed Central  Google Scholar 

  17. van Leeuwen MT, Turner JJ, Falster MO (2013) Latitude gradients for lymphoid neoplasm subtypes in Australia support an association with ultraviolet radiation exposure. Int J Cancer 133:944–951

    Article  CAS  PubMed  Google Scholar 

  18. Kricker A, Armstrong BK, Hughes AM, Interlymph Consortium et al (2008) Personal sun exposure and risk of non Hodgkin lymphoma: a pooled analysis from the Interlymph Consortium. Int J Cancer 122:144–154

    Article  CAS  PubMed  Google Scholar 

  19. Monnereau A, Glaser SL, Schupp CW et al (2013) Exposure to UV radiation and risk of Hodgkin lymphoma: a pooled analysis. Blood 122:3492–3499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Park HY, Hong YC, Lee K, Koh J (2019) Vitamin D status and risk of non-Hodgkin lymphoma: an updated meta-analysis. PLoS ONE 14:e0216284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Stroup DF, Berlin JA, Morton SC et al (2000) Meta-analysis of Observational Studies in Epidemiology (MOOSE) Group. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 283:2008–2012

    Article  CAS  PubMed  Google Scholar 

  22. Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097

    Article  PubMed  PubMed Central  Google Scholar 

  23. Musselman JR, Spector LG (2011) Childhood cancer incidence in relation to sunlight exposure. Br J Cancer 104:214–220

    Article  CAS  PubMed  Google Scholar 

  24. Wells GA, Shea B, O’Connell D (2011) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.htm. Accessed 4 Sept 2020

  25. Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560

    Article  PubMed  PubMed Central  Google Scholar 

  26. Higgins JP, Altman DG, Gøtzsche PC, Cochrane Statistical Methods Group et al (2011) The cochrane collaboration’s tool for assessing risk of bias in randomized trials. BMJ 343:d5928

    Article  PubMed  PubMed Central  Google Scholar 

  27. Borenstein M, Hedges LV, Higgins JP, Rothstein HR (2010) A basic introduction to fixed effect and random effects models for meta-analysis. Res Synth Methods 1:97–111

    Article  PubMed  Google Scholar 

  28. Davey EM, Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  Google Scholar 

  29. Hughes AM, Armstrong BK, Vajdic CM et al (2004) Sun exposure may protect against non-Hodgkin lymphoma: a case-control study. Int J Cancer 112:865–871

    Article  CAS  PubMed  Google Scholar 

  30. Smedby KE, Hjalgrim H, Melbye M et al (2005) Ultraviolet radiation exposure and risk of malignant lymphomas. J Natl Cancer Inst 97:199–209

    Article  PubMed  Google Scholar 

  31. Tavani A, Bosetti C, Franceschi S, Talamini R, Negri E, La Vecchia C (2006) Occupational exposure to ultraviolet radiation and risk of non-Hodgkin lymphoma. Eur J Cancer Prev 15:453–457

    Article  PubMed  Google Scholar 

  32. Hartge P, Lim U, Freedman DM et al (2006) Ultraviolet radiation, dietary vitamin D, and risk of non-Hodgkin lymphoma (United States). Cancer Causes Control 17:1045–1052

    Article  PubMed  Google Scholar 

  33. Petridou ET, Dikalioti SK, Skalkidou A, Andrie E, Dessypris N, Trichopoulos D, Childhood Hematology-Oncology Group (2007) Sun exposure, birth weight, and childhood lymphomas: a case control study in Greece. Cancer Causes Control 18:1031–1037

    Article  PubMed  Google Scholar 

  34. Soni LK, Hou L, Gapstur SM, Evens AM, Weisenburger DD, Chiu BC (2007) Sun exposure and non-Hodgkin lymphoma: a population-based, case-control study. Eur J Cancer 43:2388–2395

    Article  PubMed  Google Scholar 

  35. Weihkopf T, Becker N, Nieters A et al (2007) Sun exposure and malignant lymphoma: a population-based case-control study in Germany. Int J Cancer 120:2445–2451

    Article  CAS  PubMed  Google Scholar 

  36. Zhang Y, Holford TR, Leaderer B et al (2007) Ultraviolet radiation exposure and risk of non-Hodgkin’s lymphoma. Am J Epidemiol 165:1255–1264

    Article  PubMed  Google Scholar 

  37. Grandin L, Orsi L, Troussard X et al (2008) UV radiation exposure, skin type and lymphoid malignancies: results of a French case-control study. Cancer Causes Control 19:305–315

    Article  CAS  PubMed  Google Scholar 

  38. Boffetta P, van der Hel O, Kricker A et al (2008) Exposure to ultraviolet radiation and risk of malignant lymphoma and multiple myeloma–a multicentre European case-control study. Int J Epidemiol 37:1080–1094

    Article  PubMed  Google Scholar 

  39. Kane EV, Painter D, Roman E, Allan J, Law G, Lightfoot T (2010) Melanocortin 1 receptor (MC1R), pigmentary characteristics and sun exposure: findings from a case-control study of diffuse large B-cell and follicular lymphoma. Cancer Epidemiol 34:136–141

    Article  PubMed  Google Scholar 

  40. Kelly JL, Friedberg JW, Calvi LM, van Wijngaarden E, Fisher SG (2010) A case-control study of ultraviolet radiation exposure, vitamin D, and lymphoma risk in adults. Cancer Causes Control 21:1265–1275

    Article  PubMed  PubMed Central  Google Scholar 

  41. Wong KY, Tai BC, Chia SE et al (2012) Sun exposure and risk of lymphoid neoplasms in Singapore. Cancer Causes Control 23:1055–1064

    Article  PubMed  Google Scholar 

  42. Kelly JL, Drake MT, Fredericksen ZS et al (2012) Early life sun exposure, vitamin D-related gene variants, and risk of non-Hodgkin lymphoma. Cancer Causes Control 23:1017–1029

    Article  PubMed  PubMed Central  Google Scholar 

  43. Lombardi C, Heck JE, Cockburn M, Ritz B (2013) Solar UV radiation and cancer in young children. Cancer Epidemiol Biomark Prev 22:1118–1128

    Article  CAS  Google Scholar 

  44. Coste A, Goujon S, Boniol M et al (2015) Residential exposure to solar ultraviolet radiation and incidence of childhood hematological malignancies in France. Cancer Causes Control 26:1339–1349

    Article  PubMed  Google Scholar 

  45. Wang SS, Luo J, Cozen W et al (2017) Sun sensitivity, indoor tanning and B-cell non-Hodgkin lymphoma risk among Caucasian women in Los Angeles County. Br J Haematol 177:153–156

    Article  PubMed  Google Scholar 

  46. Adami J, Gridley G, Nyrén O et al (1999) Sunlight and non-Hodgkin’s lymphoma: a population-based cohort study in Sweden. Int J Cancer 80:641–645

    Article  CAS  PubMed  Google Scholar 

  47. Håkansson N, Floderus B, Gustavsson P, Feychting M, Hallin N (2001) Occupational sunlight exposure and cancer incidence among Swedish construction workers. Epidemiology 12:552–557

    Article  PubMed  Google Scholar 

  48. Veierød MB, Smedby KE, Lund E, Adami HO, Weiderpass E (2010) Pigmentary characteristics, UV radiation exposure, and risk of non-Hodgkin lymphoma: a prospective study among Scandinavian women. Cancer Epidemiol Biomark Prev 19:1569–1576

    Article  Google Scholar 

  49. Freedman DM, Kimlin MG, Hoffbeck RW, Alexander BH, Linet MS (2010) Multiple indicators of ambient and personal ultraviolet radiation exposure and risk of non-Hodgkin lymphoma (United States). J Photochem Photobiol B 101:321–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Chang ET, Canchola AJ, Cockburn M et al (2011) Adulthood residential ultraviolet radiation, sun sensitivity, dietary vitamin D, and risk of lymphoid malignancies in the California Teachers Study. Blood 118:1591–1599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Bertrand KA, Chang ET, Abel GA et al (2011) Sunlight exposure, vitamin D, and risk of non-Hodgkin lymphoma in the Nurses’ Health Study. Cancer Causes Control 22:1731–1741

    Article  PubMed  PubMed Central  Google Scholar 

  52. Lin SW, Wheeler DC, Park Y et al (2012) Prospective study of ultraviolet radiation exposure and risk of cancer in the U.S. Int J Cancer 131:E1015-1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Cahoon EK, Pfeiffer RM, Wheeler DC et al (2015) Relationship between ambient ultraviolet radiation and non-Hodgkin lymphoma subtypes: a U.S. population-based study of racial and ethnic groups. Int J Cancer 136:E432-441

    Article  CAS  PubMed  Google Scholar 

  54. Bowen EM, Pfeiffer RM, Linet MS et al (2016) Relationship between ambient ultraviolet radiation and Hodgkin lymphoma subtypes in the United States. Br J Cancer 114:826–831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Grant WB (2003) Health benefits of solar UV-B radiation through the production of vitamin D: comment and response. Photochem Photobiol Sci 2:1307–1308 (discussion 1308–1310)

    Article  CAS  PubMed  Google Scholar 

  56. Hickish T, Cunningham D, Colston K et al (1993) The effect of 1,25-dihydroxyvitamin D3 on lymphoma cell lines and expression of vitamin D receptor in lymphoma. Br J Cancer 68:668–672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Chen S, Sims GP, Chen XX, Gu YY, Chen S, Lipsky PE (2007) Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J Immunol 179:1634–1647

    Article  CAS  PubMed  Google Scholar 

  58. Sánchez-Hidalgo M, Lee M, de la Lastra CA, Guerrero JM, Packham G (2012) Melatonin inhibits cell proliferation and induces caspase activation and apoptosis in human malignant lymphoid cell lines. J Pineal Res 53:366–373

    Article  PubMed  Google Scholar 

  59. Tordjman S, Chokron S, Delorme R et al (2017) Melatonin: pharmacology, functions and therapeutic benefits. Curr Neuropharmacol 15:434–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhu Y, Zheng T (2008) Clock-cancer connection in non-Hodgkin’s lymphoma. Med Hypotheses 70:788–792

    Article  PubMed  Google Scholar 

  61. Lahti TA, Partonen T, Kyyrönen P, Kauppinen T, Pukkala E (2008) Night-time work predisposes to non-Hodgkin lymphoma. Int J Cancer 123:2148–2151

    Article  CAS  PubMed  Google Scholar 

  62. Hoffman AE, Zheng T, Stevens RG et al (2009) Clock-cancer connection in non Hodgkin’s lymphoma: a genetic association study and pathway analysis of the circadian gene cryptochrome 2. Cancer Res 69:3605–3613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Weller RB, Wang Y, He J et al (2020) Does incident solar ultraviolet radiation lower blood pressure? J Am Heart Assoc 9:e013837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hussain SP, Trivers GE, Hofseth LJ et al (2004) Nitric oxide, a mediator of inflammation, suppresses tumorigenesis. Cancer Res 64:6849–6853

    Article  CAS  PubMed  Google Scholar 

  65. Huang J, Tatsumi T, Pizzoferrato E, Vujanovic N, Storkus WJ (2005) Nitric oxide sensitizes tumor cells to dendritic cell-mediated apoptosis, uptake, and cross-presentation. Cancer Res 65:8461–8470

    Article  CAS  PubMed  Google Scholar 

  66. van der Rhee H, Coebergh JW, de Vries E (2013) Is prevention of cancer by sun exposure more than just the effect of vitamin D? A systematic review of epidemiological studies. Eur J Cancer 49:1422–1436

    Article  PubMed  Google Scholar 

  67. Smolensky MH, Sackett-Lundeen LL, Portaluppi F (2015) Nocturnal light pollution and underexposure to daytime sunlight: Complementary mechanisms of circadian disruption and related diseases. Chronobiol Int 32:1029–1048

    Article  PubMed  Google Scholar 

  68. Vallèsa X, Alonsoa MH, López-Caleya JF et al (2018) Colorectal cancer, sun exposure and dietary vitamin D and calcium intake in the MCC-Spain study. Environ Int 12:428–434

    Article  Google Scholar 

  69. Gandini S, Boniol M, Haukka J et al (2011) Meta-analysis of observational studies of serum 25-hydroxyvitamin D levels and colorectal, breast and prostate cancer and colorectal adenoma. Int J Cancer 128:1414–1424

    Article  CAS  PubMed  Google Scholar 

  70. Ma Y, Zhang P, Wang F, Lin Z, Qin H (2011) Association between vitamin D and risk of colorectal cancer: a systematic review of prospective studies. J Clin Oncol 29:3775–3782

    Article  CAS  PubMed  Google Scholar 

  71. Ragan KR, Buchanan Lunsford N, Thomas CC, Tai EW, Sussell A, Holman DM (2019) Skin cancer prevention behaviors among agricultural and construction workers in the United States, 2015. Prev Chronic Dis 16:E15

    Article  PubMed  PubMed Central  Google Scholar 

  72. Rombaldi AJ, Canabarro LK, Neutzling MB, Silva MCD (2017) Prevalence and factors associated with exposure to sunlight and sunscreen among physical education teachers in Pelotas, southern Brazil. An Bras Dermatol 92:785–792

    Article  PubMed  PubMed Central  Google Scholar 

  73. Downs N, Parisi A, Schouten P (2011) Basal and squamous cell carcinoma risks for golfers: an assessment of the influence of tee time for latitudes in the Northern and Southern hemispheres. J Photochem Photobiol B 105:98–105

    Article  CAS  PubMed  Google Scholar 

  74. Cockburn M, Hamilton A, Mack T (2001) Recall bias in self-reported melanoma risk factors. Am J Epidemiol 153:1021–1026

    Article  CAS  PubMed  Google Scholar 

  75. Matsuoka LY, Ide L, Wortsman J, MacLaughlin JA, Holick MF (1987) Sunscreens suppress cutaneous vitamin D3 synthesis. J Clin Endocrinol Metab 64:1165–1168

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Won Seok, Park for conducting the literature search. We would also like to thank Editage (www.editage.co.kr) for English language editing.

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  1. Department of Family Medicine, Myongji Hospital, Hanyang University College of Medicine, Goyang, Republic of Korea

    Hong-Bae Kim

  2. Department of Family Medicine, Chung-ang University Medical Center, Chung-ang University College of Medicine, 102, Heukseok-ro, Dongjak-gu, Seoul, 06973, Republic of Korea

    Jung-Ha Kim

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Kim, HB., Kim, JH. Sunlight exposure in association with risk of lymphoid malignancy: a meta-analysis of observational studies. Cancer Causes Control 32, 441–457 (2021). https://doi.org/10.1007/s10552-021-01404-6

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