Citrus intake and risk of skin cancer in the European Prospective Investigation into Cancer and Nutrition cohort (EPIC).


Journal

European journal of epidemiology
ISSN: 1573-7284
Titre abrégé: Eur J Epidemiol
Pays: Netherlands
ID NLM: 8508062

Informations de publication

Date de publication:
Nov 2020
Historique:
received: 11 02 2020
accepted: 16 07 2020
pubmed: 28 7 2020
medline: 16 12 2020
entrez: 26 7 2020
Statut: ppublish

Résumé

Citrus intake has been suggested to increase the risk of skin cancer. Although this relation is highly plausible biologically, epidemiologic evidence is lacking. We aimed to examine the potential association between citrus intake and skin cancer risk. EPIC is an ongoing multi-center prospective cohort initiated in 1992 and involving ~ 520,000 participants who have been followed-up in 23 centers from 10 European countries. Dietary data were collected at baseline using validated country-specific dietary questionnaires. We used Cox proportional hazards regression models to compute hazard ratios (HR) and 95% confidence intervals (CI). During a mean follow-up of 13.7 years, 8448 skin cancer cases were identified among 270,112 participants. We observed a positive linear dose-response relationship between total citrus intake and skin cancer risk (HR = 1.10, 95% CI 1.03-1.18 in the highest vs. lowest quartile; P

Identifiants

pubmed: 32710289
doi: 10.1007/s10654-020-00666-9
pii: 10.1007/s10654-020-00666-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1057-1067

Subventions

Organisme : European Research Council (ERC)
ID : ERC-2009-AdG 232997
Organisme : Regional Governments of Andalucía, Asturias, Basque Country, Murcia and Navarra
ID : Murcia (No. 6236)
Organisme : ISCIII RETIC (RD06/0020) and the Catalan Institute of Oncology (Spain)
ID : RD06/0020
Organisme : Norwegian Cancer Society
ID : 6823329
Organisme : Cancer Research UK
ID : 14136 to EPIC-Norfolk
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C570/A16491
Pays : United Kingdom
Organisme : Cancer Research UK
ID : C8221/A19170 for EPIC-Oxford
Pays : United Kingdom
Organisme : Medical Research Council
ID : 1000143 to EPIC-Norfolk, MR/M012190/1 to EPIC-Oxford
Pays : United Kingdom

Références

Wu S, Han J, Feskanich D, Cho E, Stampfer MJ, Willett WC, et al. Citrus Consumption and risk of cutaneous malignant melanoma. J Clin Oncol. 2015;33:2500–8.
pubmed: 26124488 pmcid: 4979231
Wu S, Cho E, Feskanich D, Li W-Q, Sun Q, Han J, et al. Citrus consumption and risk of basal cell carcinoma and squamous cell carcinoma of the skin. Carcinogenesis. 2015;36:1162–8.
pubmed: 26224304 pmcid: 4834848
Melough MM, Wu S, Li W-Q, Eaton C, Nan H, Snetselaar L, et al. Citrus consumption and risk of cutaneous malignant melanoma in the women’s health initiative. Nutr Cancer. 2020;72:568–75.
pubmed: 31335211
Dowdy JC, Sayre RM. Melanoma risk from dietary furocoumarins: How much more evidence is required? J Clin Oncol. 2016;34:636–7.
pubmed: 26729442
Lehrer S, Green S, Rosenzweig KE. melanoma risk and citrus consumption. J Clin Oncol. 2016;34:636.
pubmed: 26729433
Wu S, Cho E, Qureshi AA. Reply to S. Lehrer et al and J.C. Dowdy and R.M.Sayre. J Clin Oncol. 2016;34:637–8.
pubmed: 26729435
Dugrand A, Olry A, Duval T, Hehn A, Froelicher Y, Bourgaud F. Coumarin and furanocoumarin quantitation in citrus peel via ultraperformance liquid chromatography coupled with mass spectrometry (UPLC-MS). J Agric Food Chem. 2013;61:10677–84.
pubmed: 24117278
Griffin AC, Hakim RE, Knox J. The wave length effect upon erythemal and carcinogenic response in psoralen treated mice. J Investig Dermatol. 1958;31:289–95.
pubmed: 13598936
Sun W, Rice MS, Park MK, Chun OK, Melough MM, Nan H, et al. Intake of furocoumarins and risk of skin cancer in 2 prospective US cohort studies. J Nutr. 2020;150:1535–44.
pubmed: 32221600
Parrish JA, Fitzpatrick TB, Tanenbaum L, Pathak MA. Photochemotherapy of psoriasis with oral methoxsalen and longwave ultraviolet light. N Engl J Med. 1974;291:1207–11.
pubmed: 4422691
Stern RS, PUVA Follow up Study. The risk of melanoma in association with long-term exposure to PUVA. J Am Acad Dermatol. 2001;44:755–61.
pubmed: 11312420
Stern RS, Nichols KT, Väkevä LH. Malignant melanoma in patients treated for psoriasis with methoxsalen (psoralen) and ultraviolet A radiation (PUVA). The PUVA Follow-Up Study. N Engl J Med. 1997;336:1041–5.
pubmed: 9091799
Alcalay J, Bucana C, Kripke ML. Cutaneous pigmented melanocytic tumor in a mouse treated with psoralen plus ultraviolet A radiation. Photodermatol Photoimmunol Photomed. 1990;7:28–31.
pubmed: 2371167
Sayre RM, Dowdy JC. The increase in melanoma: Are dietary furocoumarins responsible? Med Hypotheses. 2008;70:855–9.
pubmed: 17881138
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;5:1113–24.
pubmed: 12639222
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.
pubmed: 9126529
Margetts BM, Pietinen P. European prospective investigation into cancer and nutrition: validity studies on dietary assessment methods. Int J Epidemiol. 1997;26(Suppl 1):S1–5.
pubmed: 9126528
Cust AE, Smith BJ, Chau J, van der Ploeg HP, Friedenreich CM, Armstrong BK, et al. Validity and repeatability of the EPIC physical activity questionnaire: a validation study using accelerometers as an objective measure. Int J Behav Nutr Phys Act. 2008;5:33.
pubmed: 18513450 pmcid: 2424075
Caini S, Masala G, Saieva C, Kvaskoff M, Savoye I, Sacerdote C, et al. Coffee, tea and melanoma risk: findings from the European prospective investigation into cancer and nutrition. Int J Cancer. 2017;140:2246–55.
pubmed: 28218395 pmcid: 6198927
Fortes C, Mastroeni S, Melchi F, Pilla MA, Antonelli G, Camaioni D, et al. A protective effect of the mediterranean diet for cutaneous melanoma. Int J Epidemiol. 2008;37:1018–29.
pubmed: 18621803
FAO. FAOSTAT. 2018; Citrus, http://faostat.fao.org/ . Available from: http://www.fao.org/3/a-i8092e.pdf .
Mullen MP, Pathak MA, West JD, Harrist TJ, Dall’Acqua F. Carcinogenic effects of monofunctional and bifunctional furocoumarins. Natl Cancer Inst Monogr. 1984;66:205–10.
pubmed: 6531030
Cartwright LE, Walter JF. Psoralen-containing sunscreen is tumorigenic in hairless mice. J Am Acad Dermatol. 1983;8:830–6.
pubmed: 6863646
Wagstaff DJ. Dietary exposure to furocoumarins. Regul Toxicol Pharmacol. 1991;14:261–72.
pubmed: 1771268
Guth S, Habermeyer M, Schrenk D, Eisenbrand G. Update of the toxicological assessment of furanocoumarins in foodstuffs (Update of the SKLM statement of 23/24 September 2004)—opinion of the senate commission on food safety (SKLM) of the German research foundation (DFG). Mol Nutr Food Res. 2011;55:807–10.
pubmed: 21433281
Dunnick JK, Forbes PD, Eustis SL, Hardisty JF, Goodman DG. Tumors of the skin in the HRA/Skh mouse after treatment with 8-methoxypsoralen and UVA radiation. Fundam Appl Toxicol. 1991;16:92–102.
pubmed: 2019354
Archier E, Devaux S, Castela E, Gallini A, Aubin F, Le Maître M, et al. Carcinogenic risks of psoralen UV-A therapy and narrowband UV-B therapy in chronic plaque psoriasis: a systematic literature review. J Eur Acad Dermatol Venereol. 2012;26(Suppl 3):22–31.
pubmed: 22512677
Stern RS, Liebman EJ, Väkevä L. Oral psoralen and ultraviolet-A light (PUVA) treatment of psoriasis and persistent risk of nonmelanoma skin cancer. PUVA Follow-up Study. J Natl Cancer Inst. 1998;90:1278–84.
pubmed: 9731734
Stern RS, Lunder EJ. Risk of squamous cell carcinoma and methoxsalen (psoralen) and UV-A radiation (PUVA). A meta-analysis. Arch Dermatol. 1998;134:1582–5.
pubmed: 9875197
Bickers DR, Pathak MA. Psoralen pharmacology: studies on metabolism and enzyme induction. Natl Cancer Inst Monogr. 1984;66:77–84.
pubmed: 6531043
Melough MM, Chun OK. Dietary furocoumarins and skin cancer: a review of current biological evidence. Food Chem Toxicol. 2018;122:163–71.
pubmed: 30316841
Scott BR, Pathak MA, Mohn GR. Molecular and genetic basis of furocoumarin reactions. Mutat Res. 1976;39:29–74.
pubmed: 13299
Derheimer FA, Hicks JK, Paulsen MT, Canman CE, Ljungman M. Psoralen-induced DNA interstrand cross-links block transcription and induce p53 in an ataxia-telangiectasia and rad3-related-dependent manner. Mol Pharmacol. 2009;75:599–607.
pubmed: 19064630
Laskin JD, Lee E, Yurkow EJ, Laskin DL, Gallo MA. A possible mechanism of psoralen phototoxicity not involving direct interaction with DNA. Proc Natl Acad Sci USA. 1985;82:6158–62.
pubmed: 3862124
Ortelli D, Edder P, Corvi C. Pesticide residues survey in citrus fruits. Food Addit Contam. 2005;22:423–8.
pubmed: 16019813
Dennis LK, Lynch CF, Sandler DP, Alavanja MCR. Pesticide use and cutaneous melanoma in pesticide applicators in the agricultural heath study. Environ Health Perspect. 2010;118:812–7.
pubmed: 20164001 pmcid: 2898858
Parhiz H, Roohbakhsh A, Soltani F, Rezaee R, Iranshahi M. Antioxidant and anti-inflammatory properties of the citrus flavonoids hesperidin and hesperetin: an updated review of their molecular mechanisms and experimental models. Phytother Res. 2015;29:323–31.
pubmed: 25394264
Aune D, Giovannucci E, Boffetta P, Fadnes LT, Keum N, Norat T, et al. Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality-a systematic review and dose-response meta-analysis of prospective studies. Int J Epidemiol. 2017;46:1029–56.
pubmed: 28338764 pmcid: 5837313
Linseisen J, Rohrmann S, Miller AB, Bueno-de-Mesquita HB, Büchner FL, Vineis P, et al. Fruit and vegetable consumption and lung cancer risk: updated information from the European prospective investigation into cancer and nutrition (EPIC). Int J Cancer. 2007;121:1103–14.
Perez-Cornago A, Travis RC, Appleby PN, Tsilidis KK, Tjønneland A, Olsen A, et al. Fruit and vegetable intake and prostate cancer risk in the European prospective investigation into cancer and nutrition (EPIC). Int J Cancer. 2017;141:287–97.
pubmed: 28419475 pmcid: 5488166
Zamora-Ros R, Béraud V, Franceschi S, Cayssials V, Tsilidis KK, Boutron-Ruault M-C, et al. Consumption of fruits, vegetables and fruit juices and differentiated thyroid carcinoma risk in the European prospective investigation into cancer and nutrition (EPIC) study. Int J Cancer. 2018;142:449–59.
pubmed: 28688112
Chaudhary PR, Jayaprakasha GK, Patil BS. Ethylene degreening modulates health promoting phytochemicals in Rio Red grapefruit. Food Chem. 2015;188:77–83.
pubmed: 26041167
Chaudhary PR, Jayaprakasha GK, Porat R, Patil BS. Low temperature conditioning reduces chilling injury while maintaining quality and certain bioactive compounds of ‘Star Ruby’ grapefruit. Food Chem. 2014;153:243–9.
pubmed: 24491726
Gorgus E, Lohr C, Raquet N, Guth S, Schrenk D. Limettin and furocoumarins in beverages containing citrus juices or extracts. Food Chem Toxicol. 2010;48:93–8.
pubmed: 19770019

Auteurs

Yahya Mahamat-Saleh (Y)

CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris Saclay, 94 805, Villejuif, France.
Inserm UMR1018, Gustave Roussy, 114 Rue Edouard Vaillant, F-94805, Villejuif, France.

Iris Cervenka (I)

CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris Saclay, 94 805, Villejuif, France.
Inserm UMR1018, Gustave Roussy, 114 Rue Edouard Vaillant, F-94805, Villejuif, France.

Marie Al-Rahmoun (M)

CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris Saclay, 94 805, Villejuif, France.
Inserm UMR1018, Gustave Roussy, 114 Rue Edouard Vaillant, F-94805, Villejuif, France.

Francesca R Mancini (FR)

CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris Saclay, 94 805, Villejuif, France.
Inserm UMR1018, Gustave Roussy, 114 Rue Edouard Vaillant, F-94805, Villejuif, France.

Gianluca Severi (G)

CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris Saclay, 94 805, Villejuif, France.
Inserm UMR1018, Gustave Roussy, 114 Rue Edouard Vaillant, F-94805, Villejuif, France.

Reza Ghiasvand (R)

Oslo Centre for Biostatistics and Epidemiology, Department of Biostatistics, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway.

Marit B Veierod (MB)

Oslo Centre for Biostatistics and Epidemiology, Department of Biostatistics, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway.

Saverio Caini (S)

Cancer Risk Factors and Lifestyle Epidemiology Unit, Cancer Research, Prevention and Clinical Network Institute (ISPRO), Florence, Italy.

Domenico Palli (D)

Cancer Risk Factors and Lifestyle Epidemiology Unit, Cancer Research, Prevention and Clinical Network Institute (ISPRO), Florence, Italy.

Edoardo Botteri (E)

Department of Bowel Cancer Screening, Cancer Registry of Norway, Oslo University Hospital, Oslo, Norway.
Norwegian National Advisory Unit for Women's Health, Women's Clinic, Oslo University Hospital, Oslo, Norway.

Carlotta Sacerdote (C)

Piedmont Reference Centre for Epidemiology and Cancer Prevention (CPO Piemonte), Turin, 10126, Italy.

Fulvio Ricceri (F)

Epidemiology Unit, ASL TO3, Piedmont Region, Grugliasco, 10095, Italy.

Antonia Trichopoulou (A)

Hellenic Health Foundation, Athens, Greece.

Eleni Peppa (E)

Hellenic Health Foundation, Athens, Greece.

Carlo La Vecchia (C)

Hellenic Health Foundation, Athens, Greece.
Department of Clinical Sciences and Community Health, Università degli Studi di Milano, Milan, Italy.

Kim Overvad (K)

Department of Public Health, Aarhus University, Aarhus, Denmark.
Department of Cardiology, Aalborg University Hospital, Aalborg, Denmark.

Christina C Dahm (CC)

Department of Public Health, Aarhus University, Aarhus, Denmark.

Anja Olsen (A)

Danish Cancer Society Research Center, Copenhagen, Denmark.

Anne Tjønneland (A)

Danish Cancer Society Research Center, Copenhagen, Denmark.
Department of Public Health, University of Copenhagen, Copenhagen, Denmark.

Aurora Perez-Cornago (A)

Cancer Epidemiology Unit, Nuffield Department of Population Health, University of Oxford, Oxford, UK.

Paula Jakszyn (P)

Unit of Nutrition and Cancer, Cancer Epidemiology Research Programme, Catalan Institute of Oncology, ĹHospitallet de Llobregat, Barcelona, Spain.
Facultat de Ciències de la Salut Blanquerna, Universitat Ramón Llull, Barcelona, Spain.

Sara Grioni (S)

Epidemiology and Prevention Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy.

Matthias B Schulze (MB)

Department of Molecular Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke, Nuthetal, Germany.
Institute of Nutritional Sciences, University of Potsdam, Nuthetal, Germany.

Guri Skeie (G)

Department of Community Medicine, University of Tromsø, The Arctic University of Norway, Tromsø, Norway.

Cristina Lasheras (C)

Department of Functional Biology, University of Oviedo, Asturias, Spain.

Sandra Colorado-Yohar (S)

Department of Epidemiology, Murcia Regional Health Council, IMIB-Arrixaca, Murcia, Spain.
CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
Research Group on Demography and Health, National Faculty of Public Health, University of Antioquia, Medellín, Colombia.

Miguel Rodríguez-Barranco (M)

CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
Andalusian School of Public Health (EASP), Granada, Spain.
Instituto de Investigación Biosanitaria de Granada (ibs.GRANADA), Universidad de Granada, Granada, Spain.

Tilman Kühn (T)

Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Verena A Katzke (VA)

Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Pilar Amiano (P)

CIBER Epidemiología y Salud Pública (CIBERESP), Madrid, Spain.
Public Health Division of Gipuzkoa, BioDonostia Research Institue, Donostia-San Sebastian, Spain.

Rosario Tumino (R)

Cancer Registry and Histopathology Department, Civic-M. P. Arezzo Hospital, ASP Ragusa, Ragusa, Italy.

Salvatore Panico (S)

Dipartimento di Medicina Clinica e Sperimentale, Federico II University, Naples, Italy.

Ana Ezponda (A)

Clínica Universidad de Navarra, Pamplona, Spain.

Emily Sonestedt (E)

Nutritional Epidemiology, Department of Clinical Sciences Malmö, Lund University, Malmö, Sweden.

Augustin Scalbert (A)

Biomarkers Group, International Agency for Research on Cancer, Lyon, France.

Elisabete Weiderpass (E)

International Agency for Research on Cancer, World Health Organization, Lyon, France.

Marie-Christine Boutron-Ruault (MC)

CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris Saclay, 94 805, Villejuif, France.
Inserm UMR1018, Gustave Roussy, 114 Rue Edouard Vaillant, F-94805, Villejuif, France.

Marina Kvaskoff (M)

CESP, Fac. de médecine - Univ. Paris-Sud, Fac. de médecine - UVSQ, INSERM, Université Paris Saclay, 94 805, Villejuif, France. Marina.KVASKOFF@gustaveroussy.fr.
Inserm UMR1018, Gustave Roussy, 114 Rue Edouard Vaillant, F-94805, Villejuif, France. Marina.KVASKOFF@gustaveroussy.fr.

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