Skip to main content
Top
Published in: Environmental Health and Preventive Medicine 1/2021

Open Access 01-12-2021 | Testosterone | Research article

Chronic exposure of bisphenol S (BPS) affect hypothalamic-pituitary-testicular activities in adult male rats: possible in estrogenic mode of action

Authors: Hizb Ullah, Faizan Ullah, Owais Rehman, Sarwat Jahan, Tayyaba Afsar, Dara Al-Disi, Ali Almajwal, Suhail Razak

Published in: Environmental Health and Preventive Medicine | Issue 1/2021

Login to get access

Abstract

Background

The industrial revolution has resulted in increased synthesis and the introduction of a variety of compounds into the environment and their potentially hazardous effects have been observed in the biota. The present study was aimed to evaluate the potential endocrine-disrupting effects of chronic exposure to the low concentrations of bisphenol S (BPS) in male rats.

Methods

Weaning male Sprague-Dawley rats (22 days old) were either exposed to water containing 0.1% ethanol for control or different concentrations of BPS (0.5, 5, and 50 μg/L) in drinking water for 48 weeks in the chronic exposure study. After completion of the experimental period, animals were dissected and different parameters (hormone concentrations, histology of testis and epididymis, oxidative stress and level of antioxidant enzymes in the testis, daily sperm production (DSP), and sperm parameters) were determined.

Results

Results of the present study showed a significant alteration in the gonadosomatic index (GSI) and relative reproductive organ weights. Oxidative stress in the testis was significantly elevated while sperm motility, daily sperm production, and the number of sperm in epididymis were reduced. Plasma testosterone, luteinizing hormone (LH), and follicle-stimulating hormone (FSH) concentrations were reduced and estradiol levels were high in the 50 μg/L-exposed group. Histological observations involved a significant reduction in the epithelial height of the testis along with disrupted spermatogenesis, an empty lumen of the seminiferous tubules, and the caput region of the epididymis.

Conclusion

These results suggest that exposure to 5 and 50 μg/L of BPS for the chronic duration started from an early age can induce structural changes in testicular tissue architecture and endocrine alterations in the male reproductive system which may lead to infertility in males.
Literature
2.
go back to reference WHO/IPCS IPoCS. Global assessment of the state-of-the-science of endocrine disruptors; 2002. WHO/IPCS IPoCS. Global assessment of the state-of-the-science of endocrine disruptors; 2002.
3.
go back to reference Rubin BS. Bisphenol a: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol. 2011;127(1):27–34.PubMedCrossRef Rubin BS. Bisphenol a: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol. 2011;127(1):27–34.PubMedCrossRef
4.
5.
go back to reference Salian S, Doshi T, Vanage GJRT. Perinatal exposure of rats to bisphenol a affects fertility of male offspring—an overview. Reprod Toxicol. 2011;31(3):359–62.PubMedCrossRef Salian S, Doshi T, Vanage GJRT. Perinatal exposure of rats to bisphenol a affects fertility of male offspring—an overview. Reprod Toxicol. 2011;31(3):359–62.PubMedCrossRef
6.
go back to reference NTP-CERHR, National Toxicology Program, US Department of Health and Human Services. Monograph on the potential human reproductive and developmental effects of Bisphenol a. center for the evaluation of risks to human reproduction. Research Triangle Park: National Institute of Environmental Health; 2008. p. 157–395. NTP-CERHR, National Toxicology Program, US Department of Health and Human Services. Monograph on the potential human reproductive and developmental effects of Bisphenol a. center for the evaluation of risks to human reproduction. Research Triangle Park: National Institute of Environmental Health; 2008. p. 157–395.
7.
go back to reference FDA: 21 CFR part 175: Representative, Edward J. Markey; filing of food additive oetition; 2012. p. 41953. FDA: 21 CFR part 175: Representative, Edward J. Markey; filing of food additive oetition; 2012. p. 41953.
8.
go back to reference Canada Go. Order amending schedule i to the hazardous products act (bisphenol a), part II. In., vol. 144; 2010. p. 7. Canada Go. Order amending schedule i to the hazardous products act (bisphenol a), part II. In., vol. 144; 2010. p. 7.
9.
go back to reference Michałowicz J. Bisphenol A–sources, toxicity and biotransformation. Environ Toxicol Pharmacol. 2014;37(2):738–58.PubMedCrossRef Michałowicz J. Bisphenol A–sources, toxicity and biotransformation. Environ Toxicol Pharmacol. 2014;37(2):738–58.PubMedCrossRef
10.
go back to reference FDA. FaDA. Indirect food additives: adhesives and components of coatings. In., vol. 78; 2013. FDA. FaDA. Indirect food additives: adhesives and components of coatings. In., vol. 78; 2013.
11.
go back to reference Appleton. Nation’s largest maker of thermal receipt paper does not use BPA; 2010. Appleton. Nation’s largest maker of thermal receipt paper does not use BPA; 2010.
12.
go back to reference Biedermann S, Tschudin P, Grob K. Transfer of bisphenol a from thermal printer paper to the skin. Anal Bioanal Chem. 2010;398(1):571–6.PubMedCrossRef Biedermann S, Tschudin P, Grob K. Transfer of bisphenol a from thermal printer paper to the skin. Anal Bioanal Chem. 2010;398(1):571–6.PubMedCrossRef
13.
go back to reference Kuruto-Niwa R, Nozawa R, Miyakoshi T, Shiozawa T, Terao Y. Estrogenic activity of alkylphenols, bisphenol S, and their chlorinated derivatives using a GFP expression system. Environ Toxicol Pharmacol. 2005;19(1):121–30.PubMedCrossRef Kuruto-Niwa R, Nozawa R, Miyakoshi T, Shiozawa T, Terao Y. Estrogenic activity of alkylphenols, bisphenol S, and their chlorinated derivatives using a GFP expression system. Environ Toxicol Pharmacol. 2005;19(1):121–30.PubMedCrossRef
14.
go back to reference Chen MY, Ike M, Fujita M. Acute toxicity, mutagenicity, and estrogenicity of bisphenol-a and other bisphenols. Environ Toxicol. 2002;17(1):80–6.PubMedCrossRef Chen MY, Ike M, Fujita M. Acute toxicity, mutagenicity, and estrogenicity of bisphenol-a and other bisphenols. Environ Toxicol. 2002;17(1):80–6.PubMedCrossRef
15.
go back to reference Liao C, Liu F, Alomirah H, Loi VD, Mohd MA, Moon H-B, et al. Bisphenol S in urine from the United States and seven Asian countries: occurrence and human exposures. Environ Sci Technol. 2012;46(12):6860–6.PubMedCrossRef Liao C, Liu F, Alomirah H, Loi VD, Mohd MA, Moon H-B, et al. Bisphenol S in urine from the United States and seven Asian countries: occurrence and human exposures. Environ Sci Technol. 2012;46(12):6860–6.PubMedCrossRef
16.
go back to reference Rochester JR, Bolden AL. Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol a substitutes. Environ Health Perspect. 2015;123(7):643.PubMedPubMedCentralCrossRef Rochester JR, Bolden AL. Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol a substitutes. Environ Health Perspect. 2015;123(7):643.PubMedPubMedCentralCrossRef
17.
go back to reference Viñas R, Watson CS. Bisphenol S disrupts estradiol-induced nongenomic signaling in a rat pituitary cell line: effects on cell functions. Environ Health Perspect. 2013;121(3):352.PubMedPubMedCentralCrossRef Viñas R, Watson CS. Bisphenol S disrupts estradiol-induced nongenomic signaling in a rat pituitary cell line: effects on cell functions. Environ Health Perspect. 2013;121(3):352.PubMedPubMedCentralCrossRef
18.
go back to reference Cano-Nicolau J, Vaillant C, Pellegrini E, Charlier TD, Kah O, Coumailleau P. Estrogenic effects of several BPA analogs in the developing zebrafish brain. Front Neurosci. 2016;10:112-24. Cano-Nicolau J, Vaillant C, Pellegrini E, Charlier TD, Kah O, Coumailleau P. Estrogenic effects of several BPA analogs in the developing zebrafish brain. Front Neurosci. 2016;10:112-24.
19.
go back to reference Liao C, Liu F, Kannan K. Bisphenol S, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol a residues. Environ Sci Technol. 2012;46(12):6515–22.PubMedCrossRef Liao C, Liu F, Kannan K. Bisphenol S, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol a residues. Environ Sci Technol. 2012;46(12):6515–22.PubMedCrossRef
20.
go back to reference Zhang T, Xue J, Gao CZ, Qiu R-L, Li YX, Li X, et al. Urinary concentrations of bisphenols and their association with biomarkers of oxidative stress in people living near e-waste recycling facilities in China. Environ Sci Technol. 2016;50(7):4045–53.PubMedCrossRef Zhang T, Xue J, Gao CZ, Qiu R-L, Li YX, Li X, et al. Urinary concentrations of bisphenols and their association with biomarkers of oxidative stress in people living near e-waste recycling facilities in China. Environ Sci Technol. 2016;50(7):4045–53.PubMedCrossRef
21.
go back to reference Zhang R, Liu R, Zong W. Bisphenol S interacts with catalase and induces oxidative stress in mouse liver and renal cells. J Agric Food Chem. 2016;64(34):6630–40.PubMedCrossRef Zhang R, Liu R, Zong W. Bisphenol S interacts with catalase and induces oxidative stress in mouse liver and renal cells. J Agric Food Chem. 2016;64(34):6630–40.PubMedCrossRef
22.
go back to reference Liang S, Yin L, Shengyang Yu K, Hofmann M-C, Yu X. High-content analysis provides mechanistic insights into the testicular toxicity of bisphenol a and selected analogues in mouse spermatogonial cells. Toxicol Sci. 2017;155(1):43–60.PubMedCrossRef Liang S, Yin L, Shengyang Yu K, Hofmann M-C, Yu X. High-content analysis provides mechanistic insights into the testicular toxicity of bisphenol a and selected analogues in mouse spermatogonial cells. Toxicol Sci. 2017;155(1):43–60.PubMedCrossRef
23.
go back to reference Catanese MC, Vandenberg LN. Bisphenol S (BPS) alters maternal behavior and brain in mice exposed during pregnancy/lactation and their daughters. Endocrinology. 2017;158(3):516-30. Catanese MC, Vandenberg LN. Bisphenol S (BPS) alters maternal behavior and brain in mice exposed during pregnancy/lactation and their daughters. Endocrinology. 2017;158(3):516-30.
24.
go back to reference Clarkson ME. A stakeholder framework for analyzing and evaluating corporate social performance. Acad Manage Rev. 1995;20(1):92–117.CrossRef Clarkson ME. A stakeholder framework for analyzing and evaluating corporate social performance. Acad Manage Rev. 1995;20(1):92–117.CrossRef
25.
go back to reference Vandenberg LN. Non-monotonic dose responses in studies of endocrine disrupting chemicals: bisphenol a as a case study. Dose-response. 2014;12(2):dose-response. 13-020 Vandenberg.CrossRef Vandenberg LN. Non-monotonic dose responses in studies of endocrine disrupting chemicals: bisphenol a as a case study. Dose-response. 2014;12(2):dose-response. 13-020 Vandenberg.CrossRef
26.
go back to reference Ullah H, Jahan S, Ain QU, Shaheen G, Ahsan N. Effect of bisphenol S exposure on male reproductive system of rats: a histological and biochemical study. Chemosphere. 2016;152:383–91.PubMedCrossRef Ullah H, Jahan S, Ain QU, Shaheen G, Ahsan N. Effect of bisphenol S exposure on male reproductive system of rats: a histological and biochemical study. Chemosphere. 2016;152:383–91.PubMedCrossRef
28.
go back to reference Hulak M, Gazo I, Shaliutina A, Linhartova P. In vitro effects of bisphenol a on the quality parameters, oxidative stress, DNA integrity and adenosine triphosphate content in sterlet (Acipenser ruthenus) spermatozoa. Compar Biochem Physiol Part C: Toxicol Pharmacol. 2013;158(2):64–71. Hulak M, Gazo I, Shaliutina A, Linhartova P. In vitro effects of bisphenol a on the quality parameters, oxidative stress, DNA integrity and adenosine triphosphate content in sterlet (Acipenser ruthenus) spermatozoa. Compar Biochem Physiol Part C: Toxicol Pharmacol. 2013;158(2):64–71.
29.
go back to reference Ullah A, Pirzada M, Afsar T, Razak S, Almajwal A, Jahan S. Effect of bisphenol F, an analog of bisphenol a, on the reproductive functions of male rats. Environ Health Prev Med. 2019;24(1):41.PubMedPubMedCentralCrossRef Ullah A, Pirzada M, Afsar T, Razak S, Almajwal A, Jahan S. Effect of bisphenol F, an analog of bisphenol a, on the reproductive functions of male rats. Environ Health Prev Med. 2019;24(1):41.PubMedPubMedCentralCrossRef
30.
go back to reference Afsar T, Razak S, Almajwal A. Acacia hydaspica ethyl acetate extract protects against cisplatin-induced DNA damage, oxidative stress and testicular injuries in adult male rats. BMC Cancer. 2017;17(1):883.PubMedPubMedCentralCrossRef Afsar T, Razak S, Almajwal A. Acacia hydaspica ethyl acetate extract protects against cisplatin-induced DNA damage, oxidative stress and testicular injuries in adult male rats. BMC Cancer. 2017;17(1):883.PubMedPubMedCentralCrossRef
31.
go back to reference Ullah A, Pirzada M, Jahan S, Ullah H, Turi N, Ullah W, et al. Impact of low-dose chronic exposure to bisphenol a and its analogue bisphenol B, bisphenol F and bisphenol S on hypothalamo-pituitary-testicular activities in adult rats: a focus on the possible hormonal mode of action. Food Chem Toxicol. 2018;121:24–36.PubMedCrossRef Ullah A, Pirzada M, Jahan S, Ullah H, Turi N, Ullah W, et al. Impact of low-dose chronic exposure to bisphenol a and its analogue bisphenol B, bisphenol F and bisphenol S on hypothalamo-pituitary-testicular activities in adult rats: a focus on the possible hormonal mode of action. Food Chem Toxicol. 2018;121:24–36.PubMedCrossRef
32.
go back to reference Ullah H, Ambreen A, Ahsan N, Jahan S. Bisphenol S induces oxidative stress and DNA damage in rat spermatozoa in vitro and disrupts daily sperm production in vivo. Toxicol Environ Chem. 2017;99(5-6):953–65.CrossRef Ullah H, Ambreen A, Ahsan N, Jahan S. Bisphenol S induces oxidative stress and DNA damage in rat spermatozoa in vitro and disrupts daily sperm production in vivo. Toxicol Environ Chem. 2017;99(5-6):953–65.CrossRef
33.
go back to reference Yamasaki K, Noda S, Imatanaka N, Yakabe Y. Comparative study of the uterotrophic potency of 14 chemicals in a uterotrophic assay and their receptor-binding affinity. Toxicol Lett. 2004;146(2):111–20.PubMedCrossRef Yamasaki K, Noda S, Imatanaka N, Yakabe Y. Comparative study of the uterotrophic potency of 14 chemicals in a uterotrophic assay and their receptor-binding affinity. Toxicol Lett. 2004;146(2):111–20.PubMedCrossRef
34.
go back to reference Crump D, Chiu S, Williams KL. Bisphenol S alters embryonic viability, development, gallbladder size, and messenger RNA expression in chicken embryos exposed via egg injection. Environ Toxicol Chem. 2016;35(6):1541-9. Crump D, Chiu S, Williams KL. Bisphenol S alters embryonic viability, development, gallbladder size, and messenger RNA expression in chicken embryos exposed via egg injection. Environ Toxicol Chem. 2016;35(6):1541-9.
35.
go back to reference García MMS, Acquier A, Suarez G, Gomez NV, Gorostizaga A, Mendez CF, et al. Cisplatin inhibits testosterone synthesis by a mechanism that includes the action of reactive oxygen species (ROS) at the level of P450scc. Chem Biol Interact. 2012;199(3):185–91.PubMedCrossRef García MMS, Acquier A, Suarez G, Gomez NV, Gorostizaga A, Mendez CF, et al. Cisplatin inhibits testosterone synthesis by a mechanism that includes the action of reactive oxygen species (ROS) at the level of P450scc. Chem Biol Interact. 2012;199(3):185–91.PubMedCrossRef
36.
go back to reference Michałowicz J, Mokra K, Bąk A. Bisphenol a and its analogs induce morphological and biochemical alterations in human peripheral blood mononuclear cells (in vitro study). Toxicol In Vitro. 2015;29(7):1464–72.PubMedCrossRef Michałowicz J, Mokra K, Bąk A. Bisphenol a and its analogs induce morphological and biochemical alterations in human peripheral blood mononuclear cells (in vitro study). Toxicol In Vitro. 2015;29(7):1464–72.PubMedCrossRef
37.
go back to reference Molina-Molina J-M, Amaya E, Grimaldi M, Sáenz J-M, Real M, Fernandez MF, et al. In vitro study on the agonistic and antagonistic activities of bisphenol-S and other bisphenol-a congeners and derivatives via nuclear receptors. Toxicol Appl Pharmacol. 2013;272(1):127–36.PubMedCrossRef Molina-Molina J-M, Amaya E, Grimaldi M, Sáenz J-M, Real M, Fernandez MF, et al. In vitro study on the agonistic and antagonistic activities of bisphenol-S and other bisphenol-a congeners and derivatives via nuclear receptors. Toxicol Appl Pharmacol. 2013;272(1):127–36.PubMedCrossRef
38.
go back to reference Kitamura S, Suzuki T, Sanoh S, Kohta R, Jinno N, Sugihara K, et al. Comparative study of the endocrine-disrupting activity of bisphenol a and 19 related compounds. Compar Study. 2005;84(2):249–59. Kitamura S, Suzuki T, Sanoh S, Kohta R, Jinno N, Sugihara K, et al. Comparative study of the endocrine-disrupting activity of bisphenol a and 19 related compounds. Compar Study. 2005;84(2):249–59.
39.
go back to reference Ji K, Liu X, Lee S, Kang S, Kho Y, Giesy JP, et al. Effects of non-steroidal anti-inflammatory drugs on hormones and genes of the hypothalamic-pituitary-gonad axis, and reproduction of zebrafish. J Hazard Mater. 2013;254:242–51.PubMedCrossRef Ji K, Liu X, Lee S, Kang S, Kho Y, Giesy JP, et al. Effects of non-steroidal anti-inflammatory drugs on hormones and genes of the hypothalamic-pituitary-gonad axis, and reproduction of zebrafish. J Hazard Mater. 2013;254:242–51.PubMedCrossRef
40.
go back to reference Boucher JG, Ahmed S, Atlas E. Bisphenol S induces adipogenesis in primary human preadipocytes from female donors. Endocrinology. 2016;157(4):1397–407.PubMedCrossRef Boucher JG, Ahmed S, Atlas E. Bisphenol S induces adipogenesis in primary human preadipocytes from female donors. Endocrinology. 2016;157(4):1397–407.PubMedCrossRef
41.
go back to reference Del Moral LI, Le Corre L, Poirier H, Niot I, Truntzer T, Merlin J-F, et al. Obesogen effects after perinatal exposure of 4, 4′-sulfonyldiphenol (Bisphenol S) in C57BL/6 mice. Toxicology. 2016;357:11–20.CrossRef Del Moral LI, Le Corre L, Poirier H, Niot I, Truntzer T, Merlin J-F, et al. Obesogen effects after perinatal exposure of 4, 4′-sulfonyldiphenol (Bisphenol S) in C57BL/6 mice. Toxicology. 2016;357:11–20.CrossRef
42.
go back to reference Barber BJ, Blake NJ. Reproductive physiology. Dev Aquac Fish Sci. 2006;35:357–416.CrossRef Barber BJ, Blake NJ. Reproductive physiology. Dev Aquac Fish Sci. 2006;35:357–416.CrossRef
43.
go back to reference Blake CA, Ashiru OA. Disruption of rat estrous cyclicity by the environmental estrogen 4-tert-octylphenol. Proc Soc Exp Biol Med. 1997;216(3):446–51.PubMedCrossRef Blake CA, Ashiru OA. Disruption of rat estrous cyclicity by the environmental estrogen 4-tert-octylphenol. Proc Soc Exp Biol Med. 1997;216(3):446–51.PubMedCrossRef
44.
go back to reference Kaneto M, Kanamori S, Hishikawa A, Kishi K. Epididymal sperm motion as a parameter of male reproductive toxicity: sperm motion, fertility, and histopathology in ethinylestradiol-treated rats. Reprod Toxicol. 1999;13(4):279–89.PubMedCrossRef Kaneto M, Kanamori S, Hishikawa A, Kishi K. Epididymal sperm motion as a parameter of male reproductive toxicity: sperm motion, fertility, and histopathology in ethinylestradiol-treated rats. Reprod Toxicol. 1999;13(4):279–89.PubMedCrossRef
45.
go back to reference Goyal HO, Bartol FF, Wiley AA, Khalil MK, Chiu J, Vig MM. Immunolocalization of androgen receptor and estrogen receptor in the developing testis and excurrent ducts of goats. Anat Rec. 1997;249(1):54–62.PubMedCrossRef Goyal HO, Bartol FF, Wiley AA, Khalil MK, Chiu J, Vig MM. Immunolocalization of androgen receptor and estrogen receptor in the developing testis and excurrent ducts of goats. Anat Rec. 1997;249(1):54–62.PubMedCrossRef
46.
go back to reference Hess RA, Bunick D, Lee K-H, Bahr J, Taylor JA, Korach KS, et al. A role for oestrogens in the male reproductive system. Nature. 1997;390(6659):509–12.PubMedPubMedCentralCrossRef Hess RA, Bunick D, Lee K-H, Bahr J, Taylor JA, Korach KS, et al. A role for oestrogens in the male reproductive system. Nature. 1997;390(6659):509–12.PubMedPubMedCentralCrossRef
47.
go back to reference Vornberger W, Prins G, Musto NA, Suarez-Quian CA. Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis. Endocrinology. 1994;134(5):2307–16.PubMedCrossRef Vornberger W, Prins G, Musto NA, Suarez-Quian CA. Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis. Endocrinology. 1994;134(5):2307–16.PubMedCrossRef
48.
go back to reference Pelletier G, Labrie C, Labrie F. Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. J Endocrinol. 2000;165(2):359–70.PubMedCrossRef Pelletier G, Labrie C, Labrie F. Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. J Endocrinol. 2000;165(2):359–70.PubMedCrossRef
49.
go back to reference Chen D, Kannan K, Tan H, Zheng Z, Feng Y-L, Wu Y, et al. Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity a review. Environ Sci Technol. 2016;50(11):5438–53.PubMedCrossRef Chen D, Kannan K, Tan H, Zheng Z, Feng Y-L, Wu Y, et al. Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity a review. Environ Sci Technol. 2016;50(11):5438–53.PubMedCrossRef
50.
go back to reference Ullah H, Ambreen A, Ahsan N, Jahan S. Bisphenol S induces oxidative stress and DNA damage in rat spermatozoa in vitro and disrupts daily sperm production in vivo. Toxicol Environ Chem. 2016just-accepted:1–23. Ullah H, Ambreen A, Ahsan N, Jahan S. Bisphenol S induces oxidative stress and DNA damage in rat spermatozoa in vitro and disrupts daily sperm production in vivo. Toxicol Environ Chem. 2016just-accepted:1–23.
Metadata
Title
Chronic exposure of bisphenol S (BPS) affect hypothalamic-pituitary-testicular activities in adult male rats: possible in estrogenic mode of action
Authors
Hizb Ullah
Faizan Ullah
Owais Rehman
Sarwat Jahan
Tayyaba Afsar
Dara Al-Disi
Ali Almajwal
Suhail Razak
Publication date
01-12-2021
Publisher
BioMed Central
Keyword
Testosterone
Published in
Environmental Health and Preventive Medicine / Issue 1/2021
Print ISSN: 1342-078X
Electronic ISSN: 1347-4715
DOI
https://doi.org/10.1186/s12199-021-00954-0

Other articles of this Issue 1/2021

Environmental Health and Preventive Medicine 1/2021 Go to the issue