Skip to main content
SpringerLink
Log in

Environmental Toxicants and Sperm Production in Men and Animals

  • Conference paper
  • First Online:
XIIIth International Symposium on Spermatology

  • 383 Accesses

Abstract

In malaria-endemic areas in South Africa, traditional huts are sprayed with 1,1,1-trichloro-2,2-bis(chlorodiphenyl)ethane (DDT) while modern structures are sprayed with pyrethroid insecticides. With modernization of housing and DDT sourcing costs, spray programs have changed. Coupled with this is an increase in agricultural pesticide use, creating another source of exposure. However, DDT and pyrethroids are considered endocrine disrupting chemicals (EDCs). Exposure to complex mixtures of EDCs is associated with adverse male reproductive health including a decline in sperm and semen quality. Thus, the aim of the study was to investigate the impact of exposure to a complex mixture of EDCs, DDT pyrethroids and other agricultural pesticides, on seminal parameters, hormonal regulation and sperm chromatin integrity. In a cross-sectional study conducted between 2003 and 2008 (n = 544, from three DDT-sprayed villages—n = 310, three non-DDT sprayed villages—n = 234) and 2012–2017 (n = 431 young males from three DDT-exposed—n = 236; three non-DDT exposed—n = 195); young males were recruited from a malaria endemic area in Limpopo Province, South Africa where DDT was used in indoor residual spraying. Exposure levels of DDT (measured in blood plasma) pyrethroids and other pesticides (measured in urine) were determined and a semen analysis was conducted according to WHO standards. Linear regression models were examined to evaluate DDT/DDE effects on different reproductive outcomes. In sprayed villages p,p′-DDE exposure levels were significantly lower between 2012 and 2017 (mean ± SD: 5.80 ± 6.6 μg/g) compared to the 2003–2008 (216.9 ± 210.6 μg/g) period (P < 0.001). In the non-sprayed villages p,p′-DDE exposure levels were significantly lower between 2012 and 2017 (mean ± SD: 1.47 ± 3.68 μg/g) compared to the 2003–2008 (2.81 ± 4.26 μg/g) period (P < 0.001). Sperm counts were significantly lower (P = 0.04) in the 2012–2017 period (45.30 ± 49.20 mil/ml) compared to 2003–2008 (51.91 ± 48.25 mil/ml). Analysis showed that 3,5,6-trichloro-2-pyridinol (TCPY), 1,2,3-benzotriazine-4-one (BTA) a herbicide and 3-(2,2-dichlororvinyl)-2,2-dimethyl-cyclopropane-1-carboxylic acid (Trans/DCCA) were the most common metabolites. Despite the decline in exposure levels over time, seminal parameters and chromatin integrity were still affected. While still dependent on DDT and pyrethroids for malaria vector control, a more sustainable approach is needed towards malaria elimination, involving transdisciplinary approaches.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aneck-Hahn NH, Schulenburg GW, Bornman MS, Farias P, de Jager C (2007) Impaired semen quality associated with environmental DDT exposure in young men living in a malaria area in the Limpopo Province, South Africa. J Androl 28(3):423–434. https://doi.org/10.2164/jandrol.106.001701

    Article  CAS  PubMed  Google Scholar 

  • ASTDR (2002) Toxicological profile for DDT, DDE and DDD. ASTDR, Atlanta, GA

    Google Scholar 

  • Bergman A, Heindel JJ, Jobling S, Kidd KA, Zoeller RT (2013) State of the science of endocrine disrupting chemicals 2012. United Nations Environment Programme and the World Health Organization, Geneva, Switzerland

    Google Scholar 

  • Boberg J, Johansson HK, Hadrup N, Dreisig K, Berthelsen L, Almstrup K et al (2015) Perinatal exposure to mixtures of anti-androgenic chemicals causes proliferative lesions in rat prostate. Prostate 75(2):126–140. https://doi.org/10.1002/pros.22897

    Article  CAS  PubMed  Google Scholar 

  • Bornman MS, Barnhoorn IEJ, Genthe B, van Vuuren JH, Pieterse GM, Aneck-Hahn NH et al (2010) DDT for malaria control: effects in indicators and health risk. Retrieved from Pretoria

    Google Scholar 

  • Bornman MS, Delport R, Farias P, Aneck-Hahn NH, de Jager C (2011) Hormonal changes associated with DDT uptake in young males. Paper presented at the International Society for Environmental Epidemiology, Barcelona

    Google Scholar 

  • Bornman M, Delport R, Farias P, Aneck-Hahn N, Patrick S, Millar RP, de Jager C (2018) Alterations in male reproductive hormones in relation to environmental DDT exposure. Environ Int 113:281–289. https://doi.org/10.1016/j.envint.2017.12.039

    Article  CAS  PubMed  Google Scholar 

  • Bouwman H (2004) South Africa and the Stockholm convention on persistent organic pollutants. S Afr J Sci 100(7/8):323–328

    Google Scholar 

  • Colborn T, Vom Saal FS, Soto AM (1993) Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101(5):378–384

    Article  CAS  Google Scholar 

  • Dalvie MA, Myers JE, Thompson ML, Robins TG, Dyer S, Riebow J et al (2004) The long-term effects of DDT exposure on semen, fertility, and sexual function of malaria vector-control workers in Limpopo Province, South Africa. Environ Res 96(1):1–8. https://doi.org/10.1016/j.envres.2003.09.002

    Article  CAS  PubMed  Google Scholar 

  • Danzo BJ (1997) Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ Health Perspect 105(3):297–301

    Article  Google Scholar 

  • de Jager C, Farias P, Barazza-Villarreal A, Avilla MH, Ayotte P, Dewailly E et al (2006a) Breakthroughs in andrology: reduced seminal parameters associated with environmental DDT exposure and p,p′-DDE concentrations in men in Chiapas, Mexico: a cross-sectional study. J Androl 27(1):16–27

    Article  Google Scholar 

  • de Jager C, Farias P, Barraza-Villarreal A, Avila MH, Ayotte P, Dewailly E et al (2006b) Reduced seminal parameters associated with environmental DDT exposure and p,p′-DDE concentrations in men in Chiapas, Mexico: a cross-sectional study. J Androl 27(1):16–27. https://doi.org/10.2164/jandrol.05121

    Article  CAS  PubMed  Google Scholar 

  • de Jager C, Aneck-Hahn NH, Bornman MS, Farias P, Leter G, Eleuteri P et al (2009) Sperm chromatin integrity in DDT-exposed young men living in a malaria area in the Limpopo Province, South Africa. Hum Reprod 24(10):2429–2438. https://doi.org/10.1093/humrep/dep249

    Article  CAS  PubMed  Google Scholar 

  • Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM et al (2009) Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30(4):293–342. https://doi.org/10.1210/er.2009-0002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • ESHRE (1998) Guidelines on the application of CASA technology in the analysis of spermatozoa. Hum Reprod 13:142–145

    Article  Google Scholar 

  • Evenson D (2016) The sperm chromatin structure assay (SCSA) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility. Anim Reprod Sci 169:56–75

    Article  CAS  Google Scholar 

  • Evenson D, Jost LK (2000) Sperm chromatin structure assay is useful for fertility assessment. Methods Cell Sci 22:169–189

    Article  CAS  Google Scholar 

  • Fielden MR, Halgren RG, Fong CJ, Staub C, Johnson L, Chou K, Zacharewski TR (2002) Gestational and lactational exposure of male mice to diethylstibestrol causes long-term effect on testis, sperm fertilizing ability in vitro and testicular gene expression. Endocrinology 8:3044–3059

    Article  Google Scholar 

  • Hsieh MH, Breyer BN, Eisenberg ML, Baskin LS (2008) Associations among hypospadias, cryptorchidism, anogenital distance, and endocrine disruption. Curr Urol Rep 9(2):137–142

    Article  Google Scholar 

  • Kaneko H (2011) Pyrethroids: mammalian metabolism and toxicity. J Agric Food Chem 59(7):2786–2791. https://doi.org/10.1021/jf102567z

    Article  CAS  PubMed  Google Scholar 

  • Kelce WR, Stone CR, Laws SC, Gray LE, Kemppainen JA, Wilson EM (1995) Persistent DDT metabolite p,p′-DDE is a potent androgen receptor antagonist. Nature 375:581–585

    Article  CAS  Google Scholar 

  • Kirman CR, Aylward LL, Hays SM, Krishnan K, Nong A (2011) Biomonitoring equivalents for DDT/DDE. Regul Toxicol Pharmacol 60(2):172–180. https://doi.org/10.1016/j.yrtph.2011.03.012

    Article  CAS  PubMed  Google Scholar 

  • Martenies SE, Perry MJ (2013) Environmental and occupational pesticide exposure and human sperm parameters: a systematic review. Toxicology 307:6–73

    Article  Google Scholar 

  • Meeker JD, Barr DB, Hauser R (2008) Human sperm quality and sperm DNA damage in relation to urinary metabolites of pyrethroid insecticides. Hum Reprod 23(8):1932–1940

    Article  CAS  Google Scholar 

  • Meeker JD, Barr DB, Hauser R (2009) Pyrethroid insecticide metabolites are associated with serum hormone levels in adult men. Reprod Toxicol 27(2):155–160

    Article  CAS  Google Scholar 

  • Metcalf RL (1995) Insect control technology. In: Kroschwitz J, Howe-Grant M (eds) Kirk-Othmer encyclopedia of chemical technology, vol 14. Wiley, New York, pp 524–602

    Google Scholar 

  • Mnif W, Hassine AIH, Bouaziz A, Bartegi A, Thomas O, Roig B (2011) Effect of endocrine disruptor pesticides: a review. Int J Environl Res Public Health 8:2265–2303

    Article  CAS  Google Scholar 

  • Moline JM, Golden AL, Bar-Chama N, Smith E, Rauch ME, Chapin RE et al (2000) Exposure to hazardous substances and male reproductive health: a research framework. Environ Health Perspect 108(9):803–813

    Article  CAS  Google Scholar 

  • Mortimer D (1994) Practical laboratory andrology. Oxford University Press, Oxford

    Google Scholar 

  • Mortimer D, Barratt LR, Björndahl L, de Jager C, Jequier AM, Muller CH (2013) What should it take to describe a substance or product as “sperm-safe”? Hum Reprod Update 19(Suppl 1):i1–i45

    Article  Google Scholar 

  • Morton S, Pencheon D, Squires N (2017) Sustainable development goals (SDGs), and their implementation: a national global framework for health, development and equity needs a systems approach at every level. Br Med Bull 124(1):81–90. https://doi.org/10.1093/bmb/ldx031

    Article  PubMed  Google Scholar 

  • NAFA (2002) Manual on basic semen analysis. Retrieved from www.ki.se/org/nafa

  • Nieschlag E, Behre H (1998) Testosterone: action, deficiency, substitution, 2nd edn. Springer, Germany

    Book  Google Scholar 

  • O’Connor JC, Frame SR, Davis LG, Cook JC (1999) Detection of the environmental antiandrogen p,p′-DDE in CD and Long-Evans rats using a Tier 1 screening battery and a Hershberger Assay. Toxicol Sci 51:44–53

    Article  Google Scholar 

  • OECD (1983) OECD Guidelines for the testing of chemicals. One-generation reproductive toxicity study (Protocol 415) (415). Retrieved from http://www.oecd.org/document/22/0,2340,en_2646_34377_1916054_1_1_1_1,00.html

  • Palanza P, Parmigiani S, Vom Saal FS (2001) Effects of prenatal exposure to low doses of diethylstilbestrol, o,p′-DDT, and methoxychlor on postnatal growth and neurobehavioural development in male and female mice. Horm Behav 40:252–265

    Article  CAS  Google Scholar 

  • Patrick SM, Bornman MS, Joubert AM, Pitts N, Naidoo V, de Jager C (2016) Effects of environmental endocrine disruptors, including insecticides used for malaria vector control on reproductive parameters of male rats. Reprod Toxicol 61:19–27. https://doi.org/10.1016/j.reprotox.2016.02.015

    Article  CAS  PubMed  Google Scholar 

  • Phillips KP, Tanphaichitr N (2008) Human exposure to endocrine disrupters and semen quality. J Toxicol Environ Health B Crit Rev 11(3–4):188–220

    Article  CAS  Google Scholar 

  • Raman J, Morris N, Frean J, Brooke B, Blumberg L, Kruger P et al (2016) Reviewing South Africa’s malaria elimination strategy (2012–2018): progress, challenges and priorities. Malar J 15(1):438. https://doi.org/10.1186/s12936-016-1497-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Rhind SM, Rae MT, Brooks AN (2001) Effects of nutrition and environmental factors on the fetal programming of the reproductive axis. Reproduction 122:205–214

    Article  CAS  Google Scholar 

  • Russell LD, Griswold MD (1993) The sertoli cell, 1st edn. Cache River Press, Clearwater, FL

    Google Scholar 

  • Rylander L, Nilsson-Ehle P, Hagmar L. A simplified precise method for adjusting serum levels of persistent organohalogen pollutants to total serum lipids. Chemosphere. 2006 Jan;62(3):333–336. https://doi.org/10.1016/j.chemosphere.2005.04.107. Epub 2005 Jul 11. PMID: 16005493

  • Sadeghi MR, Mahshid H, Lakpour N, Arefi S, Amirannati N, Modarresi T et al (2009) Effects of sperm chromatin integrity on fertilization rate and embryo quality following intracytoplasmic sperm injection. Avicenna J Med Biotechnol 1(3):173–180

    PubMed  PubMed Central  Google Scholar 

  • Saillenfait MA, Ndiye D, Sabate JP (2015) Pyrethroids: exposure and health effects - an update. Int J Hyg Environ Health 218:281–292

    Article  CAS  Google Scholar 

  • Schug TT, Janesick A, Blumberg B, Heindel JJ (2011) Endocrine disrupting chemicals and disease susceptibility. J Steroid Biochem Mol Biol 127(3–5):204–215. https://doi.org/10.1016/j.jsbmb.2011.08.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharpe R (2009) Male reproductive health disorders and the potential role of exposure to environmental chemicals. Retrieved from United Kingdom

    Google Scholar 

  • Sikka SC, Wang R (2008) Endocrine disruptors and estrogenic effects on male reproductive axis. Asian J Androl 10(1):134–145. https://doi.org/10.1111/j.1745-7262.2008.00370.x

    Article  CAS  PubMed  Google Scholar 

  • Silva E, Rajapakse N, Kortenkamp A (2002) Something from “nothing” - eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects. Environ Sci Technol 36:1751–1756

    Article  CAS  Google Scholar 

  • Spano M, Toft G, Hagmar L, Eleuteri P, Rescia M, Rignell-Hydbom A et al (2005) Exposure to PCB and p,p′-DDE in European and Inuit populations: impact on human sperm chromatin integrity. Hum Reprod 20(12):3488–3499. https://doi.org/10.1093/humrep/dei297

    Article  CAS  PubMed  Google Scholar 

  • Svechnikov K, Stukenborg JB, Savchuck I, Soder O (2014) Similar causes of various reproductive disorders in early life. Asian J Androl 16(1):50–59. https://doi.org/10.4103/1008-682x.122199

    Article  PubMed  Google Scholar 

  • Swan SH, Sathyanarayana S, Barrett ES, Janssen S, Liu F, Nguyen RHN, Redmon JB (2015) First trimester phthalate exposure and anogenital distance in newborns. Hum Reprod 30:963. https://doi.org/10.1093/humrep/deu363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tavares RS, Amaral S, Paiva C, Baptista M, Ramalho-Santos J (2015) In vitro exposure to the organochlorine p,p′-DDE affects functional human sperm parameters. Chemosphere 120:443–446. https://doi.org/10.1016/j.chemosphere.2014.08.075

    Article  CAS  PubMed  Google Scholar 

  • Turusov V, Rakitsky V, Tomatis L (2002) Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect 110(2):125–127

    Article  CAS  Google Scholar 

  • Van Dyk JC, Bouwman H, Barnhoorn IEJ, Bornman MS (2010) DDT contamination from indoor residual spraying for malaria control. Sci Total Environ 408(13):2745–2752. https://doi.org/10.1016/j.scitotenv.2010.03.002

    Article  CAS  PubMed  Google Scholar 

  • WHO (1999) WHO laboratory manual for the examination of human semen and sperm-cervical musuc interaction, 4th edn. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • WHO (2006) Indoor residual spraying - an operational manual for indoor residual spraying (IRS) for malaria transmission control and elimination. WHO, Geneva, Switzerland

    Google Scholar 

  • WHO (2019) World malaria report. WHO, Geneva, Switzerland

    Google Scholar 

  • Zoeller RT, Brown TR, Doan LL, Gore AC, Skakkebaek NE, Soto AM et al (2012) Endocrine disrupting chemicals and public health protection: a statement of principles from the Endocrine Society. Endocrinology 153(9):4097–4110

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Health Systems and Public Health, Environmental Chemical Pollution and Health Research Unit, University of Pretoria Institute for Sustainable Malaria Control (UP ISMC), Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa

    C. de Jager, S. M. Patrick, N. H. Aneck-Hahn & M. S. Bornman

  2. Department of Urology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa

    N. H. Aneck-Hahn

Authors
  1. C. de Jager
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. M. Patrick
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. H. Aneck-Hahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. S. Bornman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. de Jager .

Editor information

Editors and Affiliations

  1. Andrology Laboratory, ANOVA Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden

    Lars Björndahl

  2. Andrology Laboratory, ANOVA Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden

    John Flanagan

  3. Andrology Laboratory, ANOVA Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden

    Rebecka Holmberg

  4. Andrology Laboratory, ANOVA Karolinska University Hospital and Karolinska Institutet, Stockholm, Sweden

    Ulrik Kvist

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this paper

Check for updates. Verify currency and authenticity via CrossMark

Cite this paper

de Jager, C., Patrick, S.M., Aneck-Hahn, N.H., Bornman, M.S. (2021). Environmental Toxicants and Sperm Production in Men and Animals. In: Björndahl, L., Flanagan, J., Holmberg, R., Kvist, U. (eds) XIIIth International Symposium on Spermatology. Springer, Cham. https://doi.org/10.1007/978-3-030-66292-9_6

Download citation

Publish with us

Policies and ethics

Search

Navigation