Endocrine‐disrupting chemicals and male reproductive health

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Abstract

Background

A number of different types of endocrine‐disrupting chemicals (EDCs) including bisphenol A, phthalates, pesticides, and other environmental chemicals have been shown to adversely impact upon male reproductive health. Understanding the potential effects of EDCs on male reproductive health may enable the development of novel treatments and early prevention of the effects of EDCs on male infertility and their potential long‐term sequelae. This review critically evaluates the research performed in this area and explores potential harmful effects of EDCs in animals and humans, including the possibility of trans‐generational transmission.

Methods

A literature review was conducted using electronic databases using the following terms: ‘endocrine disrupt*’ OR ‘endocrine disruptors’ OR ‘endocrine disruptor chemicals’ OR ‘EDC’ AND ‘sperm*’ OR ‘spermatozoa’ OR ‘spermatozoon’ OR ‘male reproductive health’ OR’ male fertility’.

Main findings

Several studies have shown that EDCs have a variety of pathophysiological effects. These include failure of spermatogenesis, embryonic development, the association with testicular cancer, and long‐term metabolic effects.

Conclusions

Several studies observe correlations between chemical doses and at least one sperm parameter; however, such correlations are sometimes inconsistent between different studies. Mechanisms through which EDCs exert their pathophysiological effects have not yet been fully elucidated in human studies.

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Most cited references 73

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Concentrations of Urinary Phthalate Metabolites Are Associated with Increased Waist Circumference and Insulin Resistance in Adult U.S. Males

Richard Stahlhut, Edwin van Wijngaarden, Timothy Dye … (2007)

Background Phthalates impair rodent testicular function and have been associated with anti-androgenic effects in humans, including decreased testosterone levels. Low testosterone in adult human males has been associated with increased prevalence of obesity, insulin resistance, and diabetes. Objectives Our objective in this study was to investigate phthalate exposure and its associations with abdominal obesity and insulin resistance. Methods Subjects were adult U.S. male participants in the National Health and Nutrition Examination Survey (NHANES) 1999–2002. We modeled six phthalate metabolites with prevalent exposure and known or suspected antiandrogenic activity as predictors of waist circumference and log-transformed homeostatic model assessment (HOMA; a measure of insulin resistance) using multiple linear regression, adjusted for age, race/ethnicity, fat and total calorie consumption, physical activity level, serum cotinine, and urine creatinine (model 1); and adjusted for model 1 covariates plus measures of renal and hepatic function (model 2). Metabolites were mono-butyl phthalates (MBP), mono-ethyl phthalate (MEP), mono-(2-ethyl)-hexyl phthalate (MEHP), mono-benzyl phthalate (MBzP), mono-(2-ethyl-5-hydroxyhexyl) phthalate (MEHHP), and mono-(2-ethyl-5-oxohexyl) phthalate (MEOHP). Results In model 1, four metabolites were associated with increased waist circumference (MBzP, MEHHP, MEOHP, and MEP; p-values ≤ 0.013) and three with increased HOMA (MBP, MBzP, and MEP; p-values ≤ 0.011). When we also adjusted for renal and hepatic function, parameter estimates declined but all significant results remained so except HOMA-MBP. Conclusions In this national cross-section of U.S. men, concentrations of several prevalent phthalate metabolites showed statistically significant correlations with abdominal obesity and insulin resistance. If confirmed by longitudinal studies, our findings would suggest that exposure to these phthalates may contribute to the population burden of obesity, insulin resistance, and related clinical disorders.

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First trimester phthalate exposure and anogenital distance in newborns.

S H Swan, S. Sathyanarayana, E. S. Barrett … (2015)

Is first trimester phthalate exposure associated with anogenital distance (AGD), a biomarker of prenatal androgen exposure, in newborns? Concentrations of diethylhexyl phthalate (DEHP) metabolites in first trimester maternal urine samples are inversely associated with AGD in male, but not female, newborns. AGD is a sexually dimorphic measure reflecting prenatal androgen exposure. Prenatal phthalate exposure has been associated with shorter male AGD in multiple animal studies. Prior human studies, which have been limited by small sample size and imprecise timing of exposure and/or outcome, have reported conflicting results. The Infant Development and the Environment Study (TIDES) is a prospective cohort study of pregnant women recruited in prenatal clinics in San Francisco, CA, Minneapolis, MN, Rochester, NY and Seattle, WA in 2010-2012. Participants delivered 787 infants; 753 with complete data are included in this analysis. Any woman over 18 years old who was able to read and write English (or Spanish in CA), who was <13 weeks pregnant, whose pregnancy was not medically threatened and who planned to deliver in a study hospital was eligible to participate. Analyses include all infants whose mothers provided a first trimester urine sample and who were examined at or shortly after birth. Specific gravity (SpG) adjusted concentrations of phthalate metabolites in first trimester urine samples were examined in relation to genital measurements. In boys (N = 366), we obtained two measures of anogenital distance (AGD) (anoscrotal distance, or AGDAS and anopenile distance, AGDAP) as well as penile width (PW). In girls (N = 373), we measured anofourchette distance (AGDAF) and anoclitoral distance (AGDAC). We used multivariable regression models that adjusted for the infant's age at exam, gestational age, weight-for-length Z-score, time of day of urine collection, maternal age and study center. Three metabolites of DEHP were significantly and inversely associated with both measures of boys' AGD. Associations (β, 95% confidence interval (CI)) between AGDAS and (log10) SpG-adjusted phthalate concentrations were: -1.12 (-2.16, -0.07) for mono-2-ethylhexyl phthalate (MEHP), -1.43, (-2.49, -0.38) for mono-2-ethyl-5-oxohexyl phthalate (MEOHP), and -1.28 (-2.29, -0.27) for mono-2-ethyl-5-hydroxyhexyl (MEHHP). Associations were of similar magnitude for AGDAP. Associations were weaker and not statistically significant for PW. No other phthalate metabolites were associated with any genital measurement in boys. No phthalate metabolites were associated with either AGD measure in girls. Exposure assessment was based on a single first trimester urine sample, which may have introduced exposure misclassification. In addition, significant between-center differences suggest that this measurement is difficult to standardize. Our findings are consistent with multiple rodent studies and most human studies which were far smaller. The data we report here suggest that even at current low levels, environmental exposure to DEHP can adversely affect male genital development resulting in reproductive tract changes that may impact reproductive health later in life. These findings have important implications for public policy since most pregnant women are exposed to this ubiquitous chemical. Funding for TIDES was provided by the following grants from the National Institute of Environmental Health Sciences: R01ES016863-04 and R01 ES016863-02S4. The authors report no conflict of interest. © The Author 2015. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oup.com.

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Risk for animal and human health related to the presence of dioxins and dioxin‐like PCBs in feed and food

Helle Katrine Knutsen, Jan Alexander, Lars Barregård … (2018)

Abstract The European Commission asked EFSA for a scientific opinion on the risks for animal and human health related to the presence of dioxins (PCDD/Fs) and DL‐PCBs in feed and food. The data from experimental animal and epidemiological studies were reviewed and it was decided to base the human risk assessment on effects observed in humans and to use animal data as supportive evidence. The critical effect was on semen quality, following pre‐ and postnatal exposure. The critical study showed a NOAEL of 7.0 pg WHO2005‐TEQ/g fat in blood sampled at age 9 years based on PCDD/F‐TEQs. No association was observed when including DL‐PCB‐TEQs. Using toxicokinetic modelling and taking into account the exposure from breastfeeding and a twofold higher intake during childhood, it was estimated that daily exposure in adolescents and adults should be below 0.25 pg TEQ/kg bw/day. The CONTAM Panel established a TWI of 2 pg TEQ/kg bw/week. With occurrence and consumption data from European countries, the mean and P95 intake of total TEQ by Adolescents, Adults, Elderly and Very Elderly varied between, respectively, 2.1 to 10.5, and 5.3 to 30.4 pg TEQ/kg bw/week, implying a considerable exceedance of the TWI. Toddlers and Other Children showed a higher exposure than older age groups, but this was accounted for when deriving the TWI. Exposure to PCDD/F‐TEQ only was on average 2.4‐ and 2.7‐fold lower for mean and P95 exposure than for total TEQ. PCDD/Fs and DL‐PCBs are transferred to milk and eggs, and accumulate in fatty tissues and liver. Transfer rates and bioconcentration factors were identified for various species. The CONTAM Panel was not able to identify reference values in most farm and companion animals with the exception of NOAELs for mink, chicken and some fish species. The estimated exposure from feed for these species does not imply a risk.

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Author and article information

Contributors

Suks Minhas: suks.minhas@nhs.net

Journal

Journal ID (nlm-ta): Reprod Med Biol

Journal ID (iso-abbrev): Reprod. Med. Biol

Journal ID (doi): 10.1111/(ISSN)1447-0578

Journal ID (publisher-id): RMB2

Title: Reproductive Medicine and Biology

Publisher: John Wiley and Sons Inc. (Hoboken )

ISSN (Print): 1445-5781

ISSN (Electronic): 1447-0578

Publication date (Electronic): 14 April 2020

Publication date Collection: July 2020

Volume: 19

Issue: 3 ( doiID: 10.1111/rmb2.v19.3 )

Pages: 243-253

Affiliations

[ ¹ ] Section of Investigative Medicine Faculty of Medicine Imperial College London London UK

[ ² ] Imperial Centre for Andrology Imperial College Healthcare NHS Trust London UK

Author notes

[*] [* ] Correspondence

Suks Minhas, Imperial Centre for Andrology, Imperial College Healthcare NHS Trust, Charing Cross Hospital, London W6 8RF, UK.

Email: suks.minhas@ 123456nhs.net

Author information

Aditi Sharma https://orcid.org/0000-0002-3198-0879

Article

Publisher ID: RMB212326

DOI: 10.1002/rmb2.12326

PMC ID: 7360961

PubMed ID: 32684823

SO-VID: 804eba44-f053-471e-b9c0-0ccc59951156

License:

This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

History

Date received : 23 December 2019

Date revision received : 04 March 2020

Date accepted : 23 March 2020

Page count

Figures: 1, Tables: 2, Pages: 11, Words: 8538

Funding

Funded by: MRC , open-funder-registry 10.13039/501100000265;

Funded by: BBSRC , open-funder-registry 10.13039/501100000268;

Funded by: NIHR Imperial Biomedical Research Centre

Funded by: NHS

Funded by: NIHR

Funded by: Department of Health

Funded by: Imperial Health Charity

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source-schema-version-number 2.0

cover-date July 2020

details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_JATSPMC version:5.8.5 mode:remove_FC converted:15.07.2020

Keywords: endocrine‐disrupting chemicals,environmental,male infertility,semen quality,sperm

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Keywords: endocrine‐disrupting chemicals, environmental, male infertility, semen quality, sperm

Endocrine‐disrupting chemicals and male reproductive health

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Most cited references 73

Concentrations of Urinary Phthalate Metabolites Are Associated with Increased Waist Circumference and Insulin Resistance in Adult U.S. Males

First trimester phthalate exposure and anogenital distance in newborns.

Risk for animal and human health related to the presence of dioxins and dioxin‐like PCBs in feed and food

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