Prepubertal Serum Concentrations of Organochlorine Pesticides and Age at Sexual Maturity in Russian Boys

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Abstract

Background

Few human studies have evaluated the impact of childhood exposure to organochlorine pesticides (OCP) on pubertal development.

Objective

We evaluated associations of serum OCP concentrations [hexachlorobenzene (HCB), β-hexachlorocyclohexane (βHCH), and p,p-dichlorodiphenyldichloroethylene ( p,p´-DDE)] with age at attainment of sexual maturity among boys.

Methods

From 2003 through 2005, 350 8- to 9-year-old boys from Chapaevsk, Russia, with measured OCPs were enrolled and followed annually for 8 years. We used multivariable interval-censored models to evaluate associations of OCPs (quartiles) with three physician-assessed measures of sexual maturity: Tanner stage 5 for genitalia growth, Tanner stage 5 for pubic hair growth, or testicular volume (TV) ≥ 20 mL in either testis.

Results

In adjusted models, boys with higher HCB concentrations achieved sexual maturity reflected by TV ≥ 20 mL a mean of 3.1 months (95% CI: –1.7, 7.8), 5.3 months (95% CI: 0.6, 10.1), and 5.0 months (95% CI: 0.2, 9.8) later for quartiles Q2, Q3, and Q4, respectively, compared with Q1 ( p trend = 0.04). Tanner stage 5 for genitalia growth was attained a mean of 2.2 months (95% CI: –3.1, 7.5), 5.7 months (95% CI: 0.4, 11.0), and 3.7 months (95% CI: –1.7, 9.1) later for quartiles Q2, Q3, and Q4, respectively, of βHCH compared with Q1 ( p trend = 0.09). Tanner stage 5 for pubic hair growth occurred 6–9 months later on average for boys in the highest versus lowest quartile for HCB ( p trend < 0.001), βHCH (trend p = 0.01), and p,p´-DDE ( p trend = 0.04). No associations were observed between p,p´-DDE and Tanner stage 5 for genitalia growth or TV ≥ 20 mL.

Conclusions and relevance

Higher prepubertal serum HCB and βHCH concentrations were associated with a later age at attainment of sexual maturity. Only the highest quartile of serum p,p´-DDE was associated with later pubic hair maturation.

Citation

Lam T, Williams PL, Lee MM, Korrick SA, Birnbaum LS, Burns JS, Sergeyev O, Revich B, Altshul LM, Patterson DG Jr, Hauser R. 2015. Prepubertal serum concentrations of organochlorine pesticides and age at sexual maturity in Russian boys. Environ Health Perspect 123:1216–1221; http://dx.doi.org/10.1289/ehp.1409022

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Most cited references 48

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Persistent DDT metabolite p,p'-DDE is a potent androgen receptor antagonist.

W R Kelce, C. Stone, S C Laws … (1995)

The increase in the number of reports of abnormalities in male sex development in wildlife and humans coincided with the introduction of 'oestrogenic' chemicals such as DDT (1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane) into the environment. Although these phenotypic alterations are thought to be mediated by the oestrogen receptor, they are also consistent with inhibition of androgen receptor-mediated events. Here we report that the major and persistent DDT metabolite, p,p'-DDE (1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene), has little ability to bind the oestrogen receptor, but inhibits androgen binding to the androgen receptor, androgen-induced transcriptional activity, and androgen action in developing, pubertal and adult male rats. The results suggest that abnormalities in male sex development induced by p,p'-DDE and related environmental chemicals may be mediated at the level of the androgen receptor.

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Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings.

Michelle M. Giddens, P Lee, Shanna Swan … (2008)

Whether children, especially girls, are entering and progressing through puberty earlier today than in the mid-1900s has been debated. Secular trend analysis, based on available data, is limited by data comparability among studies in different populations, in different periods of time, and using different methods. As a result, conclusions from data comparisons have not been consistent. An expert panel was asked to evaluate the weight of evidence for whether the data, collected from 1940 to 1994, are sufficient to suggest or establish a secular trend in the timing of puberty markers in US boys or girls. A majority of the panelists agreed that data are sufficient to suggest a trend toward an earlier breast development onset and menarche in girls but not for other female pubertal markers. A minority of panelists concluded that the current data on girls' puberty timing for any marker are insufficient. Almost all panelists concluded, on the basis of few studies and reliability issues of some male puberty markers, that current data for boys are insufficient to evaluate secular trends in male pubertal development. The panel agreed that altered puberty timing should be considered an adverse effect, although the magnitude of change considered adverse was not assessed. The panel recommended (1) additional analyses of existing puberty-timing data to examine secular trends and trends in the temporal sequence of pubertal events; (2) the development of biomarkers for pubertal timing and methods to discriminate fat versus breast tissue, and (3) establishment of cohorts to examine pubertal markers longitudinally within the same individuals.

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Chlorinated hydrocarbon levels in human serum: effects of fasting and feeding.

D L Phillips, J L Pirkle, V W Burse … (2015)

Twenty healthy adult humans had serum samples drawn on four occasions within a 24-hr period: after a 12 hr overnight fast, 4-5 hr after a high fat breakfast, at midafternoon, and the next morning after another 12 hr fast. Nonfasting samples had 22% to 29% higher mean concentrations (p less than 0.05) than did fasting samples for polychlorinated biphenyls (PCBs, 4.81 vs 3.74 ng/g serum wt), hexachlorobenzene (HCB, 0.163 vs 0.134 ng/g serum wt), and p,p'-dichlorodiphenyl-dichloroethylene (p,p'-DDE, 6.74 vs 5.37 ng/g serum wt) measured by electron capture gas liquid chromatography. Total serum lipids were estimated from measurements of total cholesterol, free cholesterol, triglycerides, and phospholipids and were 20% higher in nonfasting samples than in fasting samples (7.05 g/L vs 5.86 g/L). When PCBs, HCB, and p,p'-DDE concentrations were corrected by total serum lipids, results from fasting and non-fasting samples were not statistically different. Because of the differences in these chlorinated hydrocarbon concentrations observed with different sample collection regimens, meaningful comparison of analytical results requires standardizing collection procedures or correcting by total serum lipid levels.

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Author and article information

Journal

Journal ID (nlm-ta): Environ Health Perspect

Journal ID (iso-abbrev): Environ. Health Perspect

Journal ID (publisher-id): EHP

Title: Environmental Health Perspectives

Publisher: National Institute of Environmental Health Sciences

ISSN (Print): 0091-6765

ISSN (Electronic): 1552-9924

Publication date (Electronic): 22 May 2015

Publication date (Print): November 2015

Volume: 123

Issue: 11

Pages: 1216-1221

Affiliations

[1 ]Environmental and Occupational Medicine and Epidemiology Program, Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA

[2 ]Gradient, Cambridge, Massachusetts, USA

[3 ]Department of Biostatistics, and

[4 ]Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts, USA

[5 ]Pediatric Endocrine Division, Department of Pediatrics, and

[6 ]Department of Cell and Developmental Biology, University of Massachusetts Medical School, Worcester, Massachusetts, USA

[7 ]Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts, USA

[8 ]National Cancer Institute, National Institutes of Health, Department of Health and Human Services, Research Triangle Park, North Carolina, USA

[9 ]Department of Genomics and Human Genetics, Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, Russia

[10 ]Chapaevsk Medical Association, Chapaevsk, Samara Region, Russia

[11 ]Institute for Forecasting, Russian Academy of Sciences, Moscow, Russia

[12 ]Exposure, Epidemiology, and Risk Program, Department of Environmental Health, Harvard T.H. Chan, School of Public Health, Boston, Massachusetts, USA

[13 ]Environmental Health and Engineering Inc., Needham, Massachusetts, USA

[14 ]EnviroSolutions Consulting Inc., Auburn, Georgia, USA

[15 ]Axys Analytical Solutions, Sidney, British Columbia, Canada

[16 ]Exponent Inc., Maynard, Massachusetts, USA

Author notes

Address correspondence to R. Hauser, Environmental and Occupational Medicine and Epidemiology Program, Harvard T.H. Chan School of Public Health, 665 Huntington Ave., Building 1, Room 1409, Boston, MA 02115 USA. Telephone: (617) 432-3326. E-mail: rhauser@ 123456hsph.harvard.edu

Article

Publisher ID: ehp.1409022

DOI: 10.1289/ehp.1409022

PMC ID: 4629743

PubMed ID: 26009253

SO-VID: fe90dba2-3d98-4535-9e2f-c00fbd34deaa

License:

Publication of EHP lies in the public domain and is therefore without copyright. All text from EHP may be reprinted freely. Use of materials published in EHP should be acknowledged (for example, “Reproduced with permission from Environmental Health Perspectives”); pertinent reference information should be provided for the article from which the material was reproduced. Articles from EHP, especially the News section, may contain photographs or illustrations copyrighted by other commercial organizations or individuals that may not be used without obtaining prior approval from the holder of the copyright.

History

Date received : 31 July 2014

Date accepted : 19 May 2015

Date: 22 May 2015

Date: 01 November 2015

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Prepubertal Serum Concentrations of Organochlorine Pesticides and Age at Sexual Maturity in Russian Boys

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Abstract

Background

Objective

Methods

Results

Conclusions and relevance

Citation

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Global Health Next Generation Network

Most cited references 48

Persistent DDT metabolite p,p'-DDE is a potent androgen receptor antagonist.

Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings.

Chlorinated hydrocarbon levels in human serum: effects of fasting and feeding.

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Cited by 3

Most referenced authors 565