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Chlordecone Exposure and Risk of Prostate Cancer

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Chlordecone Exposure and Risk of Prostate Cancer VOLUME 28 ⅐ NUMBER 21 ⅐ JULY 20 2010 JOURNAL OF CLINICAL ONCOLOGY ORIGINAL REPORT Chlordecone Exposure and Risk of Prostate Cancer Luc Multigner, Jean Rodrigue Ndong, Arnaud Giusti, Marc Romana, Helene Delacroix-Maillard, Sylvaine Cordier, Bernard Je´gou, Jean Pierre Thome, and Pascal Blanchet From the Institut National de la Sante´ et de la Recherche Me´ dicale (Inserm) U ABSTRACT 625, Pointe a` Pitre; Inserm U 763; Centre d’Examens de Sante´ Sainte Purpose Genevie` ve; Service d’Urologie, Centre Determining whether environmental estrogens are associated with the risk of prostate cancer may Hospitalier Universitaire de la Guade- have important implications for our general understanding of this disease. The estrogenic loupe; Universite´ des Antilles et de la insecticide chlordecone was used extensively in the French West Indies, contaminating the Guyane, Pointe a` Pitre, Guadeloupe, population for more than 30 years. We analyzed the relationship between exposure to chlordecone French West Indies; Inserm U 625, and the risk of prostate cancer. Rennes; Universite´ Rennes 1, Rennes, France; and the Laboratoire d’Ecologie Patients and Methods Animale et d’Ecotoxicologie, Center for We investigated 623 men with prostate cancer and 671 controls. Exposure was analyzed Analytical and Research Technology, according to case-control status, using either current plasma concentration or a cumulative Universite´ de Lie` ge, Lie` ge, Belgium. exposure index based on years of exposure. We genotyped two single-nucleotide polymorphisms Submitted November 28, 2009; (rs3829125 and rs17134592) in the gene encoding chlordecone reductase. accepted May 4, 2010; published online ahead of print at www.jco.org on June Results 21, 2010. We found a significant increase in the risk of prostate cancer with increasing plasma chlordecone concentration (odds ratio [OR], 1.77; 95% CI, 1.21 to 2.58 for the highest tertile of values above Supported by the Programme Hospi- ϭ talier de Recherche Clinique, the Plan the limit of detection [LD]; P trend .002) and for cumulative exposure index (OR, 1.73; 95% CI, Pluri-Formation from the French Minis- 1.04 to 2.88 for the highest quartile; P trend ϭ .004). Stronger associations were observed among try of Education and Research, the those with a positive family history of prostate cancer and among those who had lived in a French Ministry of Overseas Territories, Western country. The rs3829125 and rs17134592 allele variants were in complete linkage the French Agency for Environmental disequilibrium and were found at low frequency (0.04). Among subjects with plasma chlordecone and Occupational Health Safety, the concentrations above the LD, carriers of the allele variants had a higher risk of prostate cancer (OR, Guadeloupean Division of Social, Health, and Welfare Affairs Directorate, 5.23; 95% CI, 0.82 to 33.32). the National Health Directorate, the Conclusion Association pour la Recherche sur le These findings support the hypothesis that exposure to environmental estrogens increases the Cancer, the Comite´ Guadeloupe Ligue risk of prostate cancer. contre le Cancer; Grant No. 212844 from the European Union (Developmen- tal Effects of Environment on Repro- J Clin Oncol 28:3457-3462. © 2010 by American Society of Clinical Oncology ductive Health). Authors’ disclosures of potential con- Chlordecone (also known as Kepone) is an or- flicts of interest and author contribu- INTRODUCTION tions are found at the end of this ganochlorine insecticide with well defined estro- 5,6 article. Prostate cancer is the most commonly diagnosed genic properties. It was extensively used from Corresponding author: Luc Multigner, cancer among men in developed countries. How- 1973 to 1993 in the French West Indies, to control MD, Institut National de la Sante´etde ever, little is known about the risk factors associ- the banana root borer. A few years after the intro- la Recherche Me´ dicale U625, Faculte´ de Me´ decine, Campus de Fouillole, ated with this cancer. Advancing age, ethnic duction of chlordecone, the widespread pollution of BP145, 97154 Pointe a` Pitre, Guade- origins, and a family history of prostate cancer are soils, river water, wild animals, and vegetables grow- loupe, French West Indies; e-mail: the only established risk factors.1,2 Many lifestyle- ing in polluted soils was reported.7,8 This pesticide [email protected]. related risk factors have been implicated, but their undergoes no significant biotic or abiotic degrada- © 2010 by American Society of Clinical roles in prostate cancer etiology remain unclear.1,2 tion in the environment, so permanently polluted Oncology The effect of exposure to synthetic chemicals in the soils and waters have remained the primary source 0732-183X/10/2821-3457/$20.00 environment on prostate cancer development re- of foodstuffs contamination, and human beings DOI: 10.1200/JCO.2009.27.2153 mains a matter of debate with implications for pub- continue to be exposed to this chemical.9-13 lic health. Chemicals with hormonal properties, also Chlordecone is a potential carcinogen and has called endocrine disruptors, are thought to be in- been shown to cause hepatic tumors in laboratory volved.3,4 However, no epidemiologic evidence of a rats and mice.14 The carcinogenic and hormonal positive link between environmental exposure to properties of chlordecone and its long biologic half- endocrine chemicals and prostate cancer has yet life raise the possibility of long-term effects, such as been established. cancer. We tested the hypothesis that chlordecone © 2010 by American Society of Clinical Oncology 3457 Downloaded from ascopubs.org by 37.58.186.129 on February 8, 2017 from 037.058.186.129 Copyright © 2017 American Society of Clinical Oncology. All rights reserved. Multigner et al exposure in adulthood, over a 30-year period, favors the development Categorical covariates, including missing data as an additional response, were of prostate cancer in the French West Indies, where the incidence of modeled as dummy variables representing the different levels. Confounding this disease is particularly high.15 Chlordecone reductase catalyzes covariates were included into the logistic model if they modified the OR the reduction of chlordecone to chlordecone alcohol, increasing the estimates by more than 10%. Tests for linear trend across exposure categories 16 were performed, with the natural log-transformed chlordecone concentration biliary excretion of chlordecone and decreasing its toxicity. We treated as a continuous variable. For values equal to or below the LD, we therefore hypothesized that the prostate cancer-causing effects of assigned a value of the LD divided by 2. We tested for a modifier effect, by chlordecone would be stronger in individuals with functional variants creating an interaction term based on the cross product of these variables and of the chlordecone reductase gene, rs3829125 and rs17134592, result- exposure categories (treated as a continuous variable). Interactions were ex- ing in the production of a protein with low levels of enzymatic activity. amined by entering the interaction terms into the logistic regression model. We report the results of a case-control study in which chlorde- We quantified the significance of the interaction term using the Wald test. We used polytomous logistic regression to estimate risk simultaneously among cone exposure was evaluated by measuring its concentration in controls and non ordered subgroups of cases, as a function of age at onset the blood. (Ͻ60 vϾ60) and prostate cancer stage (local vregional/distant stage). We also used a composite index of prostate cancer aggressiveness at diagnosis: high aggressive potential (PSA Ͼ 30 ng/mL or regional/distant stage or Gleason PATIENTS AND METHODS score of 4 ϩ3 and higher) and low aggressive potential (PSA Ͻ30 ng/mL, local stage, and Gleason score of 3 ϩ 4 and lower).17 P values lower than .05 were Study Population considered significant. All statistical tests were two tailed and were carried out This study was conducted in Guadeloupe, a French archipelago in the with SAS version 9.1 (SAS Institute Inc, Cary, NC). Caribbean, most of the 405,000 inhabitants of which are of African descent. This study was carried out on 709 consecutive incident cases of histologically confirmed prostate cancer (June 2004 to December 2007) and 723 controls RESULTS without prostate cancer (January 2005 to December 2006). For details of the selection of cases and controls, see the Appendix (online only). Trained nurses obtained information for both patients and controls, The results presented here were obtained from a study population concerning demographic characteristics, anthropometrics, periods and places comprising 623 of the 709 eligible prostate cancer cases and 671 of the of residence since birth, lifestyle, occupational data, family history of prostate eligible 722 controls, from whom we were able to obtain blood sam- cancer, medical background, use of medication, and prostate cancer screening history. Weight, height, and the circumferences of the waist and hips were ples and determinations of plasma chlordecone concentration. The measured at the end of the face-to-face interview. Participants were also asked baseline characteristics of the study participants are summarized in to provide a blood sample. The study was approved by the Guadeloupean Table 1. Chlordecone was detected in the plasma of 68.7% of the cases ethics committee for studies involving human subjects. Each participant pro- and 66.8% of the controls. vided
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