Skip to main content

Advertisement

Log in

The potential reproductive toxicity of tannery effluent to the estrous cycle and ovarian follicular dynamics of female Swiss mice

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Although the toxic effects of tannery effluent (TE) on tanning-industry workers have been reported in many studies, its effects on females’ reproductive system are unknown. We aimed at evaluating the effects of direct contact with TE on the “emotional” status, estrous cycle (during 15 consecutive exposure days), and ovarian follicular dynamics of female Swiss mice at the end of the experiment to broaden the knowledge about the toxicity of this pollutant. The herein adopted exposure protocol simulated tanning-industry workers’ exposure to TE. The test animals were subjected to 45 exposure days, for 1 h a day, 5 days a week (from Monday to Friday). Based on the collected data, female mice exposed to TE recorded high anxiety index in the elevated plus maze test, although we did not observe changes in their estrous cycle. The smaller total and specific number of ovarian follicles (types 1 to 6) and the higher frequency of degenerating follicles (atresic) in female mice exposed to TE marked the folliculogenesis reduction in them. Therefore, our study was the first to provide evidences that the exposure to TE can cause reproduction issues in female mice, as well as the first experimental insight about the impact of unhealthy work activities in tanning industries on women’s reproductive system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • American Public Health Association (APHA). Standard methods for the examination of water and wastewater. 20. ed. New York: APHA, AWWA, WPCR, 1194, 1997

  • Ateeq M, Rehman HU, Kiani BH, Zareen S, Maqbool T, Ilyas BS, Rasheed, Akbar NU (2017) Toxic effect of hexavalent chromium on the works employed in chrome plating. J Entomology Zoology Studies 5(1):221–223

    Google Scholar 

  • Baldridge MG, Stahl RL, Gerstenberger SL, Tripoli V, Hutz RJ (2004) In utero and lactational exposure of Long-Evans rats to ammonium perchlorate (AP) disrupts ovarian follicle maturation. Reprod Toxicol 19:155–161

    Article  CAS  Google Scholar 

  • Brazilian Leather Exporting added value. Available in: http://www.cicb.org.br/brazilian-leather/en/industry-data. Accessed on 7 May 2018.

  • Byers SL, Wiles MV, Dunn SL, Taft RA (2012) Mouse estrous cycle identification tool and images. PLosS One 7(4):e35538

    Article  CAS  Google Scholar 

  • Cardoso LS, Estrela FN, Chagas TQ, da Silva WAM, Costa DRO, Pereira I, Vaz BG, Rodrigues ASL, Malafaia G (2018) The exposure to water with cigarette residue changes the anti-predator response in female Swiss albino mice. Environ Sci Pollut Res Int 25(9):8592–8607. https://doi.org/10.1007/s11356-017-1150-4 Epub 2018 Jan 9

    Article  Google Scholar 

  • Chagas TQ, Rabelo LM, Alvarez TGS, Guimarães AT, Rodrigues ASL, Cardoso LS, Ferreira RO, Malafaia G (2018) Precopulatory sexual behavior of male mice is changed by the exposure to tannery effluent. Chemosphere 195:312–324. https://doi.org/10.1016/j.chemosphere.2017.12.087 Epub 2017 Dec 19

    Article  CAS  Google Scholar 

  • Chandrasekaran V, Dilara K, Padmavathi R (2014) Pulmonary functions in tannery workers—a cross sectional study. Indian J Physiol Pharmacol 58:206–210

    Google Scholar 

  • Costantini AS, Paci E, Miligi L, Buiatti E, Martelli C, Lenzi S (1989) Cancer mortality among workers in the Tuscan tanning industry. Br J Ind Med 46(6):384–388

    CAS  Google Scholar 

  • Cuberos E, Rodriguez AI, Pietro E (2009) Niveles de cromo y alteraciones de salud en una población expuesta a las actividades de curtiembres en Bogotá, Colombia. Revista de Salud Pública 11(2):278–289

    Article  Google Scholar 

  • Daniels R (2007) Tannery effluent and reedbeds: working with nature. J Am Leather Chemists Assoc 102(8):248–253

    CAS  Google Scholar 

  • Drummond AE, Findlay JK (1999) The role estrogen in folliculogenesis. Mol Cell Endocrinol 51:57–64

    Article  Google Scholar 

  • Faridah H. Were, M. Charles Moturi, and Godfrey A. Wafula (2014) chromium exposure and related health effects among tannery workers in Kenya. J Health Pollution: October 2014, Vol. 4, No. 7, pp. 25–35.

  • Febriana SA, Jungbauer F, Soebono H, Coenraads PJ (2012) Inventory of the chemicals and the exposure of the workers’ skin to these at two leather factories in Indonesia. Int Arch Occup Environ Health 85(5):517–526. https://doi.org/10.1007/s00420-011-0700-1 Epub 2011 Sep 22

    Article  CAS  Google Scholar 

  • Gowd SS, Govil PK (2008) Distribution of heavy metals in surface water of Ranipet industrial area in Tamil Nadu, India. Environ Monitoring Assessment 136(1–3):197–207

    CAS  Google Scholar 

  • Greene LE, Riederer AM, Marcus M (2007) Associations of fertility and pregnancy outcomes with leather tannery work in Mongolia: a pilot study. Int J Occup Med Environ Health 16:60–68

    Article  Google Scholar 

  • Guimarães ATB, de Oliveira Ferreira R, de Lima Rodrigues AS, Malafaia G (2017) Memory and depressive effect on male and female Swiss mice exposed to tannery effluent. Neurotoxicol Teratol 61:123–127. https://doi.org/10.1016/j.ntt.2017.03.003 Epub 2017 Mar 10

    Article  CAS  Google Scholar 

  • Guimarães ATB, Ferreira RO, Rabelo LM, Silva BC, Souza JM, Silva WAM, Menezes IPP, Rodrigues ASL, Vaz BG, Costa DRO, Pereira I, Silva AR, Malafaia G (2016) The C57BL/6J mice offspring originated from a parental generation exposed to tannery effluents shows object recognition deficits. Chemosphere 164:593–602

    Article  Google Scholar 

  • Hannon PR, Brannick KE, Wang W, Gupta RK, Flaws JA (2015) Di(2-ethylhexyl) phthalate inhibits antral follicle growth, induces atresia, and inhibits steroid hormone production in cultured mouse antral follicles. Toxicol Appl Pharmacol 284(1):42–53. https://doi.org/10.1016/j.taap.2015.02.010 Epub 2015 Feb 18

    Article  CAS  Google Scholar 

  • Hu J, Xiao Z, Zhou R, Deng W, Wang M, Ma S (2011) Ecological utilization of leather tannery waste with circular economy model. J Clean Prod 19(2):221–228

    Article  CAS  Google Scholar 

  • Hu Y, Yuan DZ, Wu Y, Yu LL, Xu LZ, Yue LM, Liu L, Xu WM, Qiao XY, Zeng RJ, Yang ZL, Yin WY, Ma YX, Nie Y, Bisphenol A (2018) Initiates excessive premature activation of primordial follicles in mouse ovaries via the PTEN signaling pathway. Reprod Sci 25(4):609–620. https://doi.org/10.1177/1933719117734700 Epub 2017 Oct 5

    Article  CAS  Google Scholar 

  • Hu YC, Wang PH, Yeh S, Wang RS, Xie C, Xu Q, Zhou X, Chao HT, Tsai MY, Chang C (2004) Subfertility and defective folliculogenesis in female mice lacking androgen receptor. Proc Natl Acad Sci U S A 101(31):11209–11214 Epub 2004 Jul 26

    Article  CAS  Google Scholar 

  • Islam R, Hossain S, Siddique AB (2017) Occupational health hazards and safety practices among the workers of tannery industry in Bangladesh. J Biol Sci 6(1):13–22

    Google Scholar 

  • Issever H, Ozdilli K, Ozyildirim BA, Hapcioglu B, Ince N, Ince H, Isik E, Akçayy E, Yegenoglu Y, Erelel E, Çalak B, Agbas N (2007) Respiratory problems in tannery workers in Istanbul. Indoor Built Environ 16:177–183

    Article  CAS  Google Scholar 

  • Johansson HKL, Jacobsen PR, Hass U, Svingen T, Vinggaard AM, Isling LK, Axelstad M, Christiansen S, Boberg J (2016) Perinatal exposure to mixtures of endocrine disrupting chemicals reduces female rat follicle reserves and accelerates reproductive aging. Reprod Toxicol 61:186–194

    Article  CAS  Google Scholar 

  • Joseph K, Nithya N (2009) Material flows in the life cycle of leather. J Clean Prod 17(7):676–682

    Article  CAS  Google Scholar 

  • Kamijima M, Ichihara G, Kitoh J, Tsukamura H, Maeda K, Yu X, Xie Z, Nakajima T, Asaeda N, Hisanaga N, Takeuchi Y (1997) Ovarian toxicity of 2-bromopropane in the non-pregnant female rat. J Occup Health 39:144–149

    Article  CAS  Google Scholar 

  • Khan DA, Mushtaq S, Khan FA, Khan MQA, Khan DA, Mushtaq S, Khan FA, Khan MQA (2012) Toxic effects of chromium on tannery workers at Sialkot (Pakistan). Toxicol Ind Health 29(2):209–215

    Article  Google Scholar 

  • Kolibianakis EM, Papanikolaou EG, Fatemi HM, Devroey P (2005) Estrogen and folliculogenesis: is one necessary for the other? Curr Opin Obstet Gynecol 17(3):249–253

    Article  Google Scholar 

  • Komada M, Takao K, Miyakawa T (2008) Elevated plus maze for mice. J Vis Exp 22:1088

    Google Scholar 

  • Krezel W, Dupont S, Krust A, Chambon P, Chapman PF (2001) Increased anxiety and synaptic plasticity in estrogen receptor beta-deficient mice. Proc Natl Acad Sci U S A 98(21):12278–12282 Epub 2001 Oct 2

    Article  CAS  Google Scholar 

  • Kumar V, Majumdar C, Roy P (2008) Effects of endocrine disrupting chemicals from leather industry effluents on male reproductive system. J Steroid Biochem Mol Biol 111(3):208–216

    Article  CAS  Google Scholar 

  • Lai FN, Liu JC, Li L, Ma JY, Liu XL, Liu YP, Zhang XF, Chen H, De Felici M, Dyce PW, Shen W (2017) Di (2-ethylhexyl) phthalate impairs steroidogenesis in ovarian follicular cells of prepuberal mice. Arch Toxicol 91(3):1279–1292. https://doi.org/10.1007/s00204-016-1790-z Epub 2016 Jul 12

    Article  CAS  Google Scholar 

  • Li J, Kim JS, Abejuela VA, Lamano JB, Klein NJ, Christian CA (2017) Disrupted female estrous cyclicity in the intrahippocampal kainic acid mouse model of temporal lobe epilepsy. Epilepsia Open 2(1):39–47

    Article  Google Scholar 

  • Linos A, Petralias A, Christophi CA, Christoforidou E, Kouroutou P, Stoltidis M, Veloudaki A, Tzala E, Makris KC, Karagas MR (2011) Oral ingestion of hexavalent chromium through drinking water and cancer mortality in an industrial area of Greece—an ecological study. Environ Health 10:50. https://doi.org/10.1186/1476-069X-10-50

    Article  CAS  Google Scholar 

  • Lohff JC, Christian PJ, Marion SL, Arrandale A, Hoyer PB (2005) Characterization of cyclicity and hormonal profile with impending ovarian failure in a novel chemical-induced mouse model of perimenopause. Comp Med 55:523–527

    CAS  Google Scholar 

  • Maguire JL, Stell BM, Rafizadeh M, Mody I (2005) Ovarian cycle-linked changes in GABA(a) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8(6):797–804 Epub 2005 May 15

    Article  CAS  Google Scholar 

  • Matos MHT, Lima-Verde IB, Luque MCA, Maia JE Jr, Silva JRV, Celestino JJH, Martins FS, Báo SN, Lucci AM, Figueiredo JR (2007) Essential role of follicle stimulating hormone in the maintenance of caprine preantral follicle viability in vitro. Zygote 15:173–182

    Article  CAS  Google Scholar 

  • Mayer LP, Pearsall NA, Christian PJ, Devine PJ, Payne CM, McCuskey MK, Marion SL, Sipes IG, Hoyer PB (2002) Long-term effects of ovarian follicular depletion in rats by 4-vinylcyclohexene diepoxide. Reprod Toxicol 16(6):775–781

    Article  CAS  Google Scholar 

  • Mora S, Dussaubat N, Díaz-Véliz G (1996) Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 21(7):609–620

    Article  CAS  Google Scholar 

  • Morgan S, Lopes F, Gourley C, Anderson RA, Spears N (2013 Jul 29) Cisplatin and doxorubicin induce distinct mechanisms of ovarian follicle loss; imatinib provides selective protection only against cisplatin. PLoS One 8(7):e70117. https://doi.org/10.1371/journal.pone.0070117.Print2013.

    Article  CAS  Google Scholar 

  • Myagmartseren P, Geater A, Sriplung H (2017) Exposure to leather tanning factories lowers semen quality in Mongolian men. Central Asian J Medical Sci 3(3):243–249

    Google Scholar 

  • Nihila M (1999) Marginalisation of women workers leather tanning industry in Tamil Nadu. Econ Polit Wkly 34(16–17):WS21–WS27

    Google Scholar 

  • Pacheco JWF, Ferrari WA (2014) Guia Técnico Ambiental de Curtumes. 2. ed. v. 1. CETESB, São Paulo

    Google Scholar 

  • Palter SF, Tavares AB, Hourvitz A, Veldhuis JD, Adashi EY (2001) Are estrogens of import to primate/human ovarian folliculogenesis? Endocr Rev 22(3):389–424

    CAS  Google Scholar 

  • Pasquali R (2012) The hypothalamic–pituitary–adrenal axis and sex hormones in chronic stress and obesity: pathophysiological and clinical aspects. Ann N Y Acad Sci 1264:20–35. https://doi.org/10.1111/j.1749-6632.2012.06569.x Epub 2012 May 21

    Article  CAS  Google Scholar 

  • Pedersen T, Peters H (1968) Proposal for a classification of oocytes and follicles in the mouse ovary. J Reprod Fert 17:555–557

    Article  CAS  Google Scholar 

  • Ramzan M, Malik MA, Iqbal Z, Arshad N, Khan SY, Arshad M (2011 Oct) Study of hematological indices in tannery workers exposed to chromium in Sheikhupura (Pakistan). Toxicol Ind Health 27(9):857–864

    Article  CAS  Google Scholar 

  • Rastogi SK, Amit P, Sachin T (2008) Occupational health risks among the workers employed in leather tanneries at Kanpur. Indian J Occupational Environ Med 12(3):132

    Article  Google Scholar 

  • Ray RR (2016) Adverse hematological effects of hexavalent chromium: an overview. Interdiscip Toxicol 9(2):55–65

    Article  CAS  Google Scholar 

  • Rodgers RJ, Dalvi A (1997) Anxiety, defence and the elevated plus-maze. Neurosci Biobehav Rev 21(6):801–810

    Article  CAS  Google Scholar 

  • Sabumon PC (2016) Perspectives on biological treatment of tannery effluent. Advances Recycling Waste Management 1:3–10

    Google Scholar 

  • Saner G, Yüzbașiyan V, Çigdem S (1984) Hair chromium concentration and chromium excretion in tannery workers. Br J Ind Med 41:263–266

    CAS  Google Scholar 

  • Saraiva MVA, Celestino JJH, Chaves RN, Martins FS, Bruno JB, Lima-Verde IB, Matos MHT, Silva GM, Porfirio EP, Báo SN, Campello CC, Silva JRV, Figueiredo JR (2008) Influence of different concentrations of LH and FSH on in vitro caprine primordial ovarian follicle development. Small Rumin Res 78:87–95

    Article  Google Scholar 

  • Shahzad K, Akhtar S, Mahmud S (2006) Prevalence and determinants of asthma in adult male leather tannery workers in Karachi, Pakistan: a cross sectional study. BMC Public Health 6(1):292

    Article  Google Scholar 

  • Singletary SJ, Kirsch AJ, Watson J, Karim BO, Huso DL, Hurn PD, Murphy SJ (2005) Lack of correlation of vaginal impedance measurements with hormone levels in the rat. Contemp. Top. Lab. Anim. Sci. 44, 37–42

  • Siqueira IR, Vanzella C, Bianchetti P, Rodrigues MAS, Stülp S (2011) Anxiety-like behaviour in mice exposed to tannery wastewater: the effect of photoelectrooxidation treatment. Neurotoxicol Teratol 33:481–484

    Article  CAS  Google Scholar 

  • Sirotkin AV, Makarevich AV (2002) Growth hormone can regulate functions of porcine ovarian granulosa cells through the cAMP/protein kinase a system. Anim Reprod Sci 70:111–126

    Article  CAS  Google Scholar 

  • Souza JM, Mendes BO, Guimarães ATB, Rodrigues ASL, Chagas TQ, Rocha TL, Malafaia G. Zinc oxide nanoparticles in predicted environmentally relevant concentrations leading to behavioral impairments in male Swiss mice. Sci Total Environ 2018 Feb 1;613–614:653–662. doi: https://doi.org/10.1016/j.scitotenv.2017.09.051. Epub 2017 Sep 26, 613-614.

  • Tatem KS, Quinn JL, Phadke A, Yu Q, Gordish-Dressman H, Behavioral NK (2014) Locomotor measurements using an open field activity monitoring system for skeletal muscle diseases. J Vis Exp 91:51785

    Google Scholar 

  • United Nations Industrial Development Organization. Occupational safety and health in the tanning industry in South East Asia (2000). Available in: https://leatherpanel.org/sites/default/files/publications-attachments/occupational_safety_and_health_in_the_tanning_industry_se_asia.pdf. Access on: 7 may 2018

  • Vasumathi A, Prithi S (2018) Work life balance of women workers in tannery industry, Tamil Nadu - an empirical bivariate study, International Journal of Services and Operations Management, 29, issue 3, p. 420–438

  • Veyalkin I, Gerein V (2006) Retrospective cohort study of cancer mortality at the Minsk leather tannery. Ind Health 44:69–74

    Article  Google Scholar 

  • Veyalkin IV, Alexander AM (2003a) Proportionate cancer mortality among workers in the Belarussian tanning industry. Am J Ind Med 44(6):637–642

    Article  Google Scholar 

  • Veyalkin IV, Alexander AM (2003b) Proportionate cancer mortality among workers in the Belarussian tanning industry. Am J Ind Med 44(6):637–642

    Article  Google Scholar 

  • Walf AA, Frye CA (2007) The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc 2(2):322–328

    Article  CAS  Google Scholar 

  • Weller BK, Atan SU, Metin M (2017) Effects of cadmium on female fertility parameters: an experimental study. Studies on Ethno-Medicine 11(1):63–69

    Article  Google Scholar 

  • Were FH, Moturi MC, Wafula GM (2014) Chromium exposure and related health effects among tannery workers in Kenya. J Health Pollution 7:25–35

    Article  Google Scholar 

  • World Health Organization (1993) WHO's drinking water standards 1993. Available in: https://www.lenntech.nl/toepassingen/drinkwater/normen/who-s-drinking-water-standards.htm. Access on: 26 oct 2018

Download references

Acknowledgments

The authors are grateful to the Brazilian National Council for Research (CNPq) (Brazilian research agency) (Proc. No 467801/2014-2) and to Instituto Federal Goiano for the financial support (Proc. No 23219000096/2018-93). Moreover, the authors are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) and Fundação de Amaparo à Pesquisa do Estado de Goiás (FAPEG, Brazil) for granting the scholarship to the student who developed the current study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Guilherme Malafaia.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Oliveira Ferreira, R., Guimarães, A.T.B., Rocha, T.L. et al. The potential reproductive toxicity of tannery effluent to the estrous cycle and ovarian follicular dynamics of female Swiss mice. Environ Sci Pollut Res 25, 36355–36367 (2018). https://doi.org/10.1007/s11356-018-3527-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-3527-4

Keywords

Navigation