Prenatal and childhood exposure to chlordecone and sex-typed toy preference of 7-year-old Guadeloupean children.
Child development
Chlordecone
Endocrine-disrupting chemicals
French West Indies
Insecticides
Organochlorine
Sex-typed play behavior
Journal
Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
28
02
2019
accepted:
04
06
2019
pubmed:
3
7
2019
medline:
3
11
2020
entrez:
3
7
2019
Statut:
ppublish
Résumé
Chlordecone was used intensively as an insecticide in the French West Indies. Because of its high persistence, the resulting contamination of food and water has led to chronic exposure of the general population as evidenced by its presence in the blood of people of Guadeloupe, in particular in pregnant women and newborns, and in maternal breast milk. Chlordecone is recognized as a reproductive and developmental toxicant, is neurotoxic and carcinogenic in rodents, and is considered as an endocrine-disrupting compound with well-established estrogenic and progestogenic properties both in vitro and in vivo. The question arises of its potential consequences on child neurodevelopment following prenatal and childhood exposure, in particular on behavioral sexual dimorphism in childhood. We followed 116 children from the TIMOUN mother-child cohort study in Guadeloupe, who were examined at age 7. These children were invited to participate in a 7-min structured play session in which they could choose between different toys considered as feminine, masculine, or neutral. The play session was video recorded, and the percentage of the time spent playing with feminine or masculine toys was calculated. We estimated associations between playtime and prenatal exposure to chlordecone (assessed by concentration in cord blood) or childhood exposure (determined from concentrations in child blood obtained at the 7-year follow-up), taking into account confounders and co-exposures to other environmental chemicals. We used a two-group regression model to take into account sex differences in play behavior. Our results do not indicate any modification in sex-typed toy preference among 7-year-old children in relation with either prenatal or childhood exposure to chlordecone.
Identifiants
pubmed: 31264154
doi: 10.1007/s11356-019-05686-x
pii: 10.1007/s11356-019-05686-x
doi:
Substances chimiques
Insecticides
0
Chlordecone
RG5XJ88UDF
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
40971-40979Subventions
Organisme : French General Health Directorate
ID : DGS RMC11129NNA
Références
Alexander GM, Wilcox T, Woods R (2009) Sex differences in infants’ visual interest in toys. Arch Sex Behav 38:427–433. https://doi.org/10.1007/s10508-008-9430-1
doi: 10.1007/s10508-008-9430-1
Bell MR (2014) Endocrine-disrupting actions of PCBs on brain development and social and reproductive behaviors. Curr Opin Pharmacol 19:134–144. https://doi.org/10.1016/j.coph.2014.09.020
doi: 10.1016/j.coph.2014.09.020
Bernert JT, Turner WE, Patterson DG, Needham LL (2007) Calculation of serum “total lipid” concentrations for the adjustment of persistent organohalogen toxicant measurements in human samples. Chemosphere 68:824–831. https://doi.org/10.1016/j.chemosphere.2007.02.043
doi: 10.1016/j.chemosphere.2007.02.043
Birke LI, Sadler D (1983) Progestin-induced changes in play behaviour of the prepubertal rat. Physiol Behav 30:341–347. https://doi.org/10.1016/0031-9384(83)90136-1
doi: 10.1016/0031-9384(83)90136-1
Birke LI, Sadler D (1984) Modification of juvenile play and other social behaviour in the rat by neonatal progestins: further studies. Physiol Behav 33:217–219. https://doi.org/10.1016/0031-9384(84)90102-1
doi: 10.1016/0031-9384(84)90102-1
Boucher O, Simard MN, Muckle G, Rouget F, Kadhel P, Bataille H, Chajès V, Dallaire R, Monfort C, Thomé JP, Multigner L, Cordier S (2013) Exposure to an organochlorine pesticide (chlordecone) and development of 18-month-old infants. Neurotoxicology 35:162–168. https://doi.org/10.1016/j.neuro.2013.01.007
doi: 10.1016/j.neuro.2013.01.007
Caldwell BM, Bradley RH (2001) HOME inventory and administration manual, 3rd edn. University of Arkansas for Medical Sciences and University of Arkansas at Little Rock
Cannon SB, Veazey JM, Jackson et al (1978) Epidemic kepone poisoning in chemical workers. Am J Epidemiol 107:529–537. https://doi.org/10.1093/oxfordjournals.aje.a112572
doi: 10.1093/oxfordjournals.aje.a112572
Chajes V, Thiebaut ACM, Rotival M, Gauthier E, Maillard V, Boutron-Ruault MC, Joulin V, Lenoir GM, Clavel-Chapelon F (2008) Association between serum trans-monounsaturated fatty acids and breast cancer risk in the E3N-EPIC Study. Am J Epidemiol 167:1312–1320. https://doi.org/10.1093/aje/kwn069
doi: 10.1093/aje/kwn069
Collaer ML, Hines M (1995) Human behavioral sex differences: a role for gonadal hormones during early development? Psychol Bull 118:55–107. https://doi.org/10.1037/0033-2909.118.1.55
doi: 10.1037/0033-2909.118.1.55
Cooper JR, Vodicnik MJ, Gordon JH (1985) Effects of perinatal Kepone exposure on sexual differentiation of the rat brain. Neurotoxicology 6:183–190
Dallaire R, Muckle G, Rouget F, Kadhel P, Bataille H, Guldner L, Seurin S, Chajès V, Monfort C, Boucher O, Pierre Thomé J, Jacobson SW, Multigner L, Cordier S (2012) Cognitive, visual, and motor development of 7-month-old Guadeloupean infants exposed to chlordecone. Environ Res 118:79–85. https://doi.org/10.1016/j.envres.2012.07.006
doi: 10.1016/j.envres.2012.07.006
Debier C, Pomeroy P, Dupont C, Joiris C, Comblin V, le Boulengé E, Larondelle Y, Thomé JP (2003) Quantitative dynamics of PCB transfer from mother to pup during lactation in UK grey seals Halichoerus grypus. Mar Ecol Prog Ser 247:237–248. https://doi.org/10.3354/meps247237
doi: 10.3354/meps247237
Dubuisson C, Héraud F, Leblanc J-C, Gallotti S, Flamand C, Blateau A, Quenel P, Volatier JL (2007) Impact of subsistence production on the management options to reduce the food exposure of the Martinican population to Chlordecone. Regul Toxicol Pharmacol 49:5–16. https://doi.org/10.1016/j.yrtph.2007.04.008
doi: 10.1016/j.yrtph.2007.04.008
Faroon O, Kueberuwa S, Smith L, Derosa C (1995) Atsdr Evaluation of health effects of chemicals. Toxicol Ind Health 11:1–195. https://doi.org/10.1177/074823379501100601
doi: 10.1177/074823379501100601
Faroon O, Jones D, De Rosa C (2000) Effects of polychlorinated biphenyls on the nervous system. Toxicol Ind Health 16:305–333. https://doi.org/10.1177/074823370001600708
doi: 10.1177/074823370001600708
Frye C, Bo E, Calamandrei G, Calzà L, Dessì-Fulgheri F, Fernández M, Fusani L, Kah O, Kajta M, le Page Y, Patisaul HB, Venerosi A, Wojtowicz AK, Panzica GC (2012) Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J Neuroendocrinol 24:144–159. https://doi.org/10.1111/j.1365-2826.2011.02229.x
doi: 10.1111/j.1365-2826.2011.02229.x
Golombok S, Rust J (1993) The pre-school activities inventory: a standardized assessment of gender role in children. Psychol Assess 5:131–136. https://doi.org/10.1037/1040-3590.5.2.131
doi: 10.1037/1040-3590.5.2.131
Guldner L, Multigner L, Héraud F, Monfort C, Pierre Thomé J, Giusti A, Kadhel P, Cordier S (2010) Pesticide exposure of pregnant women in Guadeloupe: ability of a food frequency questionnaire to estimate blood concentration of chlordecone. Environ Res 110:146–151. https://doi.org/10.1016/j.envres.2009.10.015
doi: 10.1016/j.envres.2009.10.015
Guo YL, Lai TJ, Chen SJ, Hsu CC (1995) Gender-related decrease in Raven’s progressive matrices scores in children prenatally exposed to polychlorinated biphenyls and related contaminants. Bull Environ Contam Toxicol 55:8–13. https://doi.org/10.1007/BF00212382
doi: 10.1007/BF00212382
Hammond B, Katzenellenbogen BS, Krauthammer N, McConnell J (1979) Estrogenic activity of the insecticide chlordecone (Kepone) and interaction with uterine estrogen receptors. Proc Natl Acad Sci 76:6641–6645. https://doi.org/10.1073/pnas.76.12.6641
doi: 10.1073/pnas.76.12.6641
Hassett JM, Siebert ER, Wallen K (2008) Sex differences in rhesus monkey toy preferences parallel those of children. Horm Behav 54:359–364. https://doi.org/10.1016/j.yhbeh.2008.03.008
doi: 10.1016/j.yhbeh.2008.03.008
Kadhel P, Monfort C, Costet N, Rouget F, Thomé JP, Multigner L, Cordier S (2014) Chlordecone exposure, length of gestation, and risk of preterm birth. Am J Epidemiol 179:536–544. https://doi.org/10.1093/aje/kwt313
doi: 10.1093/aje/kwt313
Laessig SA, Auger AP, McCarthy MM, Silbergeld EK (2007) Effects of prenatal chlordecone on sexually differentiated behavior in adult rats. Neurotoxicol Teratol 29:255–263. https://doi.org/10.1016/j.ntt.2006.10.003
doi: 10.1016/j.ntt.2006.10.003
Lemaire G, Mnif W, Mauvais P, Balaguer P, Rahmani R (2006) Activation of α- and β-estrogen receptors by persistent pesticides in reporter cell lines. Life Sci 79:1160–1169. https://doi.org/10.1016/j.lfs.2006.03.023
doi: 10.1016/j.lfs.2006.03.023
Little RJA (1988) A test of missing completely at random for multivariate data with missing values. J Am Stat Assoc 83:1198–1202. https://doi.org/10.1080/01621459.1988.10478722
doi: 10.1080/01621459.1988.10478722
Lombardo MV, Ashwin E, Auyeung B, Chakrabarti B, Taylor K, Hackett G, Bullmore ET, Baron-Cohen S (2012) Fetal testosterone influences sexually dimorphic gray matter in the human brain. J Neurosci 32:674–680. https://doi.org/10.1523/JNEUROSCI.4389-11.2012
doi: 10.1523/JNEUROSCI.4389-11.2012
Mactutus CF, Tilson HA (1984) Neonatal chlordecone exposure impairs early learning and retention of active avoidance in the rat. Neurobehav Toxicol Teratol 6:75–83
Mactutus CF, Tilson HA (1985) Evaluation of long-term consequences in behavioral and/or neural function following neonatal chlordecone exposure. Teratology 31:177–186. https://doi.org/10.1002/tera.1420310202
doi: 10.1002/tera.1420310202
Mactutus CF, Unger K, Tilson HA (1982) Neonatal chlordecone exposure impairs early learning and memory in the rat on a multiple passive avoidance task. Neurotoxicology 3:27–44
McCarthy MM, Arnold AP (2011) Reframing sexual differentiation of the brain. Nat Neurosci 14:677–683. https://doi.org/10.1038/nn.2834
doi: 10.1038/nn.2834
Multigner L, Ndong JR, Giusti A, Romana M, Delacroix-Maillard H, Cordier S, Jégou B, Thome JP, Blanchet P (2010) Chlordecone exposure and risk of prostate cancer. J Clin Oncol 28:3457–3462. https://doi.org/10.1200/JCO.2009.27.2153
doi: 10.1200/JCO.2009.27.2153
Multigner L, Kadhel P, Rouget F, Blanchet P, Cordier S (2016) Chlordecone exposure and adverse effects in French West Indies populations. Environ Sci Pollut Res Int 23:3–8. https://doi.org/10.1007/s11356-015-4621-5
doi: 10.1007/s11356-015-4621-5
Muthén LK, Muthén BO (1998-2017) Mplus user’s guide, 8th edn. Muthén & Muthén, Los Angeles
Nordenström A, Servin A, Bohlin G, Larsson A, Wedell A (2002) Sex-typed toy play behavior correlates with the degree of prenatal androgen exposure assessed by CYP21 genotype in girls with congenital adrenal hyperplasia. J Clin Endocrinol Metab 87:5119–5124. https://doi.org/10.1210/jc.2001-011531
doi: 10.1210/jc.2001-011531
Pryor GT, Uyeno ET, Tilson HA, Mitchell CL (1983) Assessment of chemicals using a battery of neurobehavioral tests: a comparative study. Neurobehav Toxicol Teratol 5:91–117
Raven J, Raven JC, Court JH (2003) Manual for Raven’s progressive matrices and vocabulary scales. Section 1: General Overview. Harcourt Assessment, San Antonio
Rouget F, Lebreton J, Kadhel P, Monfort C, Bodeau-Livinec F, Janky E, Multigner L, Cordier S (2013) Medical and sociodemographic risk factors for preterm birth in a French Caribbean population of African descent. Matern Child Health J 17:1103–1111. https://doi.org/10.1007/s10995-012-1112-x
doi: 10.1007/s10995-012-1112-x
Schantz SL, Moshtaghian J, Ness DK (1995) Spatial learning deficits in adult rats exposed to ortho-substituted PCB congeners during gestation and lactation. Toxicol Sci. 26:117–126. https://doi.org/10.1093/toxsci/26.1.117
doi: 10.1093/toxsci/26.1.117
Scippo ML, Argiris C, Van De Weerdt C et al (2004) Recombinant human estrogen, androgen and progesterone receptors for detection of potential endocrine disruptors. Anal Bioanal Chem 378:664–669. https://doi.org/10.1007/s00216-003-2251-0
doi: 10.1007/s00216-003-2251-0
Servin A, Bohlin G, Berlin L (1999) Sex differences in 1-, 3-, and 5-year-olds’ toy-choice in a structured play-session. Scand J Psychol 40:43–48. https://doi.org/10.1111/1467-9450.00096
doi: 10.1111/1467-9450.00096
Seurin S, Rouget F, Reninger J-C, Gillot N, Loynet C, Cordier S, Multigner L, Leblanc JC, Volatier JL, Héraud F (2012) Dietary exposure of 18-month-old Guadeloupian toddlers to chlordecone. Regul Toxicol Pharmacol 63:471–479. https://doi.org/10.1016/j.yrtph.2012.05.009
doi: 10.1016/j.yrtph.2012.05.009
Squibb R, Tilson HA (1982) Effects of gestational and perinatal exposure to chlordecone (Kepone) on the neurobehavioral development of Fischer-344 rats. Neurotoxicology 3:17–26
Swan SH, Liu F, Hines M, Kruse RL, Wang C, Redmon JB, Sparks A, Weiss B (2010) Prenatal phthalate exposure and reduced masculine play in boys. Int J Androl 33:259–267. https://doi.org/10.1111/j.1365-2605.2009.01019.x
doi: 10.1111/j.1365-2605.2009.01019.x
Templ M, Hron K, Filzmoser P (2011) RobCompositions: an R-package for robust statistical analysis of compositional data. In: Pawlowsky-Glahn V, Buccianti A (eds) Compositional Data Analysis. Theory and Applications. John Wiley & Sons, Chichester (UK), pp 341–355
doi: 10.1002/9781119976462.ch25
Vonier PM, Crain DA, McLachlan JA et al (1996) Interaction of environmental chemicals with the estrogen and progesterone receptors from the oviduct of the American alligator. Environ Health Perspect 104:1318–1322. https://doi.org/10.1289/ehp.961041318
doi: 10.1289/ehp.961041318
Vreugdenhil HJI, Slijper FME, Mulder PGH, Weisglas-Kuperus N (2002) Effects of perinatal exposure to PCBs and dioxins on play behavior in Dutch children at school age. Environ Health Perspect 110:593–598
doi: 10.1289/ehp.021100593
Winneke G, Ranft U, Wittsiepe J, Kasper-Sonnenberg M, Fürst P, Krämer U, Seitner G, Wilhelm M (2014) Behavioral sexual dimorphism in school-age children and early developmental exposure to dioxins and PCBs: a follow-up study of the Duisburg cohort. Environ Health Perspect 122:292–298. https://doi.org/10.1289/ehp.1306533
doi: 10.1289/ehp.1306533