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Articles

Evaluation of glyphosate exposure on testosterone among U.S. adult men

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Pages 902-915 | Received 26 Nov 2022, Accepted 21 Mar 2023, Published online: 25 Apr 2023

References

  • Andreotti G, Koutros S, Hofmann JN, Sandler DP, Lubin JH, Lynch CF, Lerro CC, De Roos AJ, Parks CG, Alavanja MC, et al. 2018. Glyphosate use and cancer incidence in the agricultural health study. J Natl Cancer Inst. 110(5):509–516. doi:10.1093/jnci/djx233.
  • Brookes G, Taheripour F, Tyner WE. 2017. The contribution of glyphosate to agriculture and potential impact of restrictions on use at the global level. GM Crops Food. 8(4):216–228. doi:10.1080/21645698.2017.1390637.
  • Connolly A, Coggins MA, Galea KS, Jones K, Kenny L, McGowan P, Basinas I. 2019. Evaluating glyphosate exposure routes and their contribution to total body burden: a study among amenity horticulturalists. Ann Work Expo Health. 63(2):133–147. doi:10.1093/annweh/wxy104.
  • Dai P, Hu P, Tang J, Li Y, Li C. 2016. Effect of glyphosate on reproductive organs in male rat. Acta Histochem. 118(5):519–526. doi:10.1016/j.acthis.2016.05.009.
  • de Araújo-Ramos AT, Passoni MT, Romano MA, Romano RM, Martino-Andrade AJ. 2021. Controversies on endocrine and reproductive effects of glyphosate and glyphosate-based herbicides: a mini-review. Front Endocrinol (Lausanne). 12:627210. doi:10.3389/fendo.2021.627210.
  • Defarge N, Takács E, Lozano VL, Mesnage R, Spiroux de Vendômois J, Séralini GE, Székács A. 2016. Co-formulants in glyphosate-based herbicides disrupt aromatase activity in human cells below toxic levels. Int J Environ Res Public Health. 13(3):264. doi:10.3390/ijerph13030264.
  • Del Giudice F, Glover F, Belladelli F, De Berardinis E, Sciarra A, Salciccia S, Kasman AM, Chen T, Eisenberg ML. 2021. Association of daily step count and serum testosterone among men in the United States. Endocrine. 72(3):874–881. doi:10.1007/s12020-021-02631-2.
  • Dziewirska E, Hanke W, Jurewicz J. 2018. Environmental non-persistent endocrine-disrupting chemicals exposure and reproductive hormones levels in adult men. Int J Occup Med Environ Health. 31(5):551–573. doi:10.13075/ijomeh.1896.01183.
  • Fu H, Gao F, Wang X, Tan P, Qiu S, Shi B, Shan A. 2021. Effects of glyphosate-based herbicide-contaminated diets on reproductive organ toxicity and hypothalamic-pituitary-ovarian axis hormones in weaned piglets. Environ Pollut. 272:115596. doi:10.1016/j.envpol.2020.115596.
  • Gillezeau C, van Gerwen M, Shaffer RM, Rana I, Zhang L, Sheppard L, Taioli E. 2019. The evidence of human exposure to glyphosate: a review. Environ Health. 18(1):2. doi:10.1186/s12940-018-0435-5.
  • Glover FE, Caudle WM, Del Giudice F, Belladelli F, Mulloy E, Lawal E, Eisenberg ML. 2022. The association between caffeine intake and testosterone: NHANES 2013–2014. Nutr J. 21(1):33. doi:10.1186/s12937-022-00783-z.
  • Glover FE, Del Giudice F, Belladelli F, Ryan PB, Chen T, Eisenberg ML, Caudle WM. 2022. The association between 2,4-D and serum testosterone levels: NHANES 2013–2014. J Endocrinol Invest. 45(4):787–796. doi:10.1007/s40618-021-01709-y.
  • Gorga A, Rindone GM, Centola CL, Sobarzo CM, Pellizzari EH, Camberos MDC, Marín-Briggiler CI, Cohen DJ, Riera MF, Galardo MN, et al. 2021. Low doses of glyphosate/roundup alter blood-testis barrier integrity in juvenile rats. Front Endocrinol (Lausanne). 12:615678. doi:10.3389/fendo.2021.615678.
  • Holt SK, Lopushnyan N, Hotaling J, Sarma AV, Dunn RL, Cleary PA, Braffett BH, Gatcomb P, Martin C, Herman WH, et al. 2014. Prevalence of low testosterone and predisposing risk factors in men with type 1 diabetes mellitus: findings from the DCCT/EDIC. J Clin Endocrinol Metab. 99(9):E1655–1660. doi:10.1210/jc.2014-1317.
  • Jarrell ZR, Ahammad MU, Benson AP. 2020. Glyphosate-based herbicide formulations and reproductive toxicity in animals. Vet Anim Sci. 10:100126. doi:10.1016/j.vas.2020.100126.
  • Jia H, Sullivan CT, McCoy SC, Yarrow JF, Morrow M, Borst SE. 2015. Review of health risks of low testosterone and testosterone administration. World J Clin Cases. 3(4):338–344. doi:10.12998/wjcc.v3.i4.338.
  • Johansson HKL, Schwartz CL, Nielsen LN, Boberg J, Vinggaard AM, Bahl MI, Svingen T. 2018. Exposure to a glyphosate-based herbicide formulation, but not glyphosate alone, has only minor effects on adult rat testis. Reprod Toxicol. 82:25–31. doi:10.1016/j.reprotox.2018.09.008.
  • Kanissery R, Gairhe B, Kadyampakeni D, Batuman O, Alferez F. 2019. Glyphosate: its environmental persistence and impact on crop health and nutrition. Plants (Basel). 8(11):499. doi:10.3390/plants8110499.
  • Köhn FM. 2006. Testosterone and body functions. Aging Male. 9(4):183–188. doi:10.1080/13685530601060396.
  • Lu L, Liu JB, Wang JQ, Lian CY, Wang ZY, Wang L. 2022. Glyphosate-induced mitochondrial reactive oxygen species overproduction activates parkin-dependent mitophagy to inhibit testosterone synthesis in mouse leydig cells. Environ Pollut. 314:120314. doi:10.1016/j.envpol.2022.120314.
  • Malik J, Barry G, Kishore G. 1989. The herbicide glyphosate. Biofactors. 2(1):17–25.
  • Manservisi F, Lesseur C, Panzacchi S, Mandrioli D, Falcioni L, Bua L, Manservigi M, Spinaci M, Galeati G, Mantovani A, et al. 2019. The Ramazzini Institute 13-week pilot study glyphosate-based herbicides administered at human-equivalent dose to Sprague Dawley rats: effects on development and endocrine system. Environ Health. 18(1):15. doi:10.1186/s12940-019-0453-y.
  • Marouani N, Tebourbi O, Cherif D, Hallegue D, Yacoubi MT, Sakly M, Benkhalifa M, Ben Rhouma K. 2017. Effects of oral administration of 2,4-dichlorophenoxyacetic acid (2,4-D) on reproductive parameters in male Wistar rats. Environ Sci Pollut Res Int. 24(1):519–526. doi:10.1007/s11356-016-7656-3.
  • Mohammadi K, Sani MA, Safaei P, Rahmani J, Molaee-Aghaee E, Jafari SM. 2022. A systematic review and meta-analysis of the impacts of glyphosate on the reproductive hormones. Environ Sci Pollut Res Int. 29(41):62030–62041. doi:10.1007/s11356-021-16145-x.
  • Moore LJ, Fuentes L, Rodgers JH, Bowerman WW, Yarrow GK, Chao WY, Bridges WC. 2012. Relative toxicity of the components of the original formulation of Roundup® to five North American anurans. Ecotoxicol Environ Saf. 78:128–133. doi:10.1016/j.ecoenv.2011.11.025.
  • Peixoto F. 2005. Comparative effects of the Roundup and glyphosate on mitochondrial oxidative phosphorylation. Chemosphere. 61(8):1115–1122. doi:10.1016/j.chemosphere.2005.03.044.
  • Pham TH, Derian L, Kervarrec C, Kernanec PY, Jégou B, Smagulova F, Gely-Pernot A. 2019. Perinatal exposure to glyphosate and a glyphosate-based herbicide affect spermatogenesis in mice. Toxicol Sci. 169(1):260–271. doi:10.1093/toxsci/kfz039.
  • Prevention CfDCa. 2020a. NHANES 2013-2014 questionnaire data overview. August 24 2020. https://wwwn.cdc.gov/nchs/nhanes/ContinuousNhanes/OverviewQuex.aspx?BeginYear=2013.
  • Prevention CfDCa. 2020b. NHANES survey methods and analytic guidelines. Retrieved October 26 from https://wwwn.cdc.gov/nchs/nhanes/analyticguidelines.aspx.
  • Richmond ME. 2018. Glyphosate: a review of its global use, environmental impact, and potential health effects on humans and other species. J Environ Stud Sci. 8(4):416–434. doi:10.1007/s13412-018-0517-2.
  • Rivas AM, Mulkey Z, Lado-Abeal J, Yarbrough S. 2014. Diagnosing and managing low serum testosterone. Proc (Bayl Univ Med Cent). 27(4):321–324. doi:10.1080/08998280.2014.11929145.
  • Romano MA, Romano RM, Santos LD, Wisniewski P, Campos DA, de Souza PB, Viau P, Bernardi MM, Nunes MT, de Oliveira CA. 2012. Glyphosate impairs male offspring reproductive development by disrupting gonadotropin expression. Arch Toxicol. 86(4):663–673. doi:10.1007/s00204-011-0788-9.
  • Romano RM, Romano MA, Bernardi MM, Furtado PV, Oliveira CA. 2010. Prepubertal exposure to commercial formulation of the herbicide glyphosate alters testosterone levels and testicular morphology. Arch Toxicol. 84(4):309–317. doi:10.1007/s00204-009-0494-z.
  • Ross A, Bhasin S. 2016. Hypogonadism: its prevalence and diagnosis. Urol Clin North Am. 43(2):163–176. doi:10.1016/j.ucl.2016.01.002.
  • Seralini GE, Jungers G. 2021. Endocrine disruptors also function as nervous disruptors and can be renamed endocrine and nervous disruptors (ENDs). Toxicol Rep. 8:1538–1557. doi:10.1016/j.toxrep.2021.07.014.
  • Soares D, Silva L, Duarte S, Pena A, Pereira A. 2021. Glyphosate use, toxicity and occurrence in food. Foods. 10(11):2785. doi:10.3390/foods10112785.
  • Song HY, Kim YH, Seok SJ, Gil HW, Hong SY. 2012. In vitro cytotoxic effect of glyphosate mixture containing surfactants. J Korean Med Sci. 27(7):711–715. doi:10.3346/jkms.2012.27.7.711.
  • Tarazona JV, Court-Marques D, Tiramani M, Reich H, Pfeil R, Istace F, Crivellente F. 2017. Glyphosate toxicity and carcinogenicity: a review of the scientific basis of the European Union assessment and its differences with IARC. Arch Toxicol. 91(8):2723–2743. doi:10.1007/s00204-017-1962-5.
  • Teleken JL, Gomes ECZ, Marmentini C, Moi MB, Ribeiro RA, Balbo SL, Amorim EMP, Bonfleur ML. 2020. Glyphosate-based herbicide exposure during pregnancy and lactation malprograms the male reproductive morphofunction in F1 offspring. J Dev Orig Health Dis. 11(2):146–153. doi:10.1017/s2040174419000382.
  • Vardakas P, Veskoukis AS, Rossiou D, Gournikis C, Kapetanopoulou T, Karzi V, Docea AO, Tsatsakis A, Kouretas D. 2022. A mixture of endocrine disruptors and the pesticide roundup(®) induce oxidative stress in rabbit liver when administered under the long-term low-dose regimen: reinforcing the notion of real-life risk simulation. Toxics. 10(4):190. doi:10.3390/toxics10040190.
  • Walsh LP, McCormick C, Martin C, Stocco DM. 2000. Roundup inhibits steroidogenesis by disrupting steroidogenic acute regulatory (StAR) protein expression. Environ Health Perspect. 108(8):769–776. doi:10.1289/ehp.00108769.
  • Wang W, Ma Y, Chen J, Peng L, Gao X, Lin L, Zhang F, Xiong Y, Qin F, Yuan J. 2022. The association between 2, 4-dichlorophenoxyacetic acid and erectile dysfunction. Front Public Health. 10:910251. doi:10.3389/fpubh.2022.910251.
  • Wang Y, Aimuzi R, Nian M, Zhang Y, Luo K, Zhang J. 2021. Bisphenol A substitutes and sex hormones in children and adolescents. Chemosphere. 278:130396. doi:10.1016/j.chemosphere.2021.130396.
  • Xia Y, Yang X, Lu J, Xie Q, Ye A, Sun W. 2020. The endoplasmic reticulum stress and related signal pathway mediated the glyphosate-induced testosterone synthesis inhibition in TM3 cells. Environ Pollut. 260:113949. doi:10.1016/j.envpol.2020.113949.
  • Zhao L, Zhang J, Yang L, Zhang H, Zhang Y, Gao D, Jiang H, Li Y, Dong H, Ma T, et al. 2021. Glyphosate exposure attenuates testosterone synthesis via NR1D1 inhibition of StAR expression in mouse Leydig cells. Sci Total Environ. 785:147323. doi:10.1016/j.scitotenv.2021.147323.

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