Log in

Effects of Glyphosate Exposure on Reproductive Health: A Systematic Review of Human, Animal and In-Vitro Studies

  • Review Paper
  • Published:
Exposure and Health Aims and scope Submit manuscript

Abstract

Glyphosate is the most widely used herbicide in the world. We examined whether and how human populations exposed to glyphosate at any age are at risk of develo** reproductive health effects. Protocol was developed following the recommendations of the PRISMA guidelines. Original research published in indexed journals was included with direct and indirect exposure to glyphosate, from any country/region, without publication year restriction, in English or Spanish. We included observational studies in humans, as well as experiments in vitro or in animal models. Studies were searched in four databases. The scoring assignments were based on the guidelines for conducting systematic reviews in the development of toxicity factors. The findings on the agent and exposure assessment were retrieved and summarized in a narrative synthesis. After eliminating duplicates among the identified articles and reviewing the inclusion and exclusion criteria, 80 were included in the narrative synthesis, i.e., 20 human studies, 44 animal studies, and 16 using in vitro models. This review shows strong experimental evidence, in animal models and in vitro studies, of glyphosate toxicity in reproduction and development as well as related metabolic and disease consequences. Several of these studies show significant health consequences for mothers, fetuses, and offspring, even several generations after exposure. Human studies, in contrast, are scarce and controversial. Nevertheless, we believe that the evidence is sufficient to, under the precautionary principle, define policies to prevent exposure of women, their partners, and their children to glyphosate.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Data Availability

Not applicable.

Code Availability

Not applicable.

References

  • Abarikwu SO, Akiri OF, Durojaiye MA, Adenike A (2015) Combined effects of repeated administration of bretmont wipeout (glyphosate) and ultrazin (atrazine) on testosterone, oxidative stress and sperm quality of wistar rats. Toxicol Mech Methods 25(1):70–80. https://doi.org/10.3109/15376516.2014.989349

    Article  CAS  Google Scholar 

  • Agostini LP, Dettogni RS, Dos Reis RS, Stur E, Dos Santos EV, Ventorim DP, Garcia FM, Cardoso RC, Graceli JB, Louro ID (2020) Effects of glyphosate exposure on human health: insights from epidemiological and in vitro studies. Sci Total Environ 705:135808

    Article  CAS  Google Scholar 

  • Alarcon R, Ingaramo PI, Rivera OE, Dioguardi GH, Repetti MR, Demonte LD, Milesi MM, Varayoud J, Munoz-de-Toro M, Luque EH (2019) Neonatal exposure to a glyphosate-based herbicide alters the histofunctional differentiation of the ovaries and uterus in lambs. Mol Cell Endocrinol 482:45–56. https://doi.org/10.1016/j.mce.2018.12.007

    Article  CAS  Google Scholar 

  • Almeida LL, Teixeira Áa, Soares AF, Cunha FMD, Silva VADJ, Vieira FLD, Wanderley-Teixeira V (2017) Effects of melatonin in rats in the initial third stage of pregnancy exposed to sub-lethal doses of herbicides. Acta Histochem 119(3):220–227

    Article  CAS  Google Scholar 

  • Anifandis G, Amiridis G, Dafopoulos K, Daponte A, Dovolou E, Gavriil E, Gorgogietas V, Kachpani E, Mamuris Z, Messini CI, Vassiou K, Psarra AG (2017) The in vitro impact of the herbicide roundup on human sperm motility and sperm mitochondria. Toxics 6(1):2. https://doi.org/10.3390/toxics6010002

    Article  CAS  Google Scholar 

  • Anifandis G, Katsanaki K, Lagodonti G, Messini C, Simopoulou M, Dafopoulos K, Daponte A (2018) The effect of glyphosate on human sperm motility and sperm DNA fragmentation. Int J Environ Res Public Health 5(30):1117

    Article  CAS  Google Scholar 

  • Arbuckle TE, Lin Z, Mery LS (2001) An exploratory analysis of the effect of pesticide exposure on the risk of spontaneous abortion in an Ontario farm population. Environ Health Perspect 109(8):851–857. https://doi.org/10.1289/ehp.01109851

    Article  CAS  Google Scholar 

  • Aris A, Leblanc S (2011) Maternal and fetal exposure to pesticides associated to genetically modified foods in Eastern Townships of Quebec, Canada. Reprod Toxicol 31(4):528–533

    Article  CAS  Google Scholar 

  • Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur 28(1):3. https://doi.org/10.1186/s12302-016-0070-0

    Article  CAS  Google Scholar 

  • Beuret CJ, Zirulnik F, Gimenez MS (2005) Effect of the herbicide glyphosate on liver lipoperoxidation in pregnant rats and their fetuses. Reprod Toxicol 19(4):501–504. https://doi.org/10.1016/j.reprotox.2004.09.009

    Article  CAS  Google Scholar 

  • Bolognesi C, Carrasquilla G, Volpi S, Solomon KR, Marshall EJP (2009) Biomonitoring of genotoxic risk in agricultural workers from five Colombian regions: association to occupational exposure to glyphosate. J Toxicol Environ Health-Part A-Current Issues 72(15–16):986–997. https://doi.org/10.1080/15287390902929741

    Article  CAS  Google Scholar 

  • Bonvallot N, Canlet C, Blas YEF, Gautier R, Tremblay-Franco M, Chevolleau S, Cordier S, Cravedi JP (2018) Metabolome disruption of pregnant rats and their offspring resulting from repeated exposure to a pesticide mixture representative of environmental contamination in Brittany. PLoS ONE 13(6):e0198448. https://doi.org/10.1371/journal.pone.0198448

    Article  CAS  Google Scholar 

  • Camacho A, Mejia D (2017) The health consequences of aerial spraying illicit crops: the case of Colombia. J Health Econ 54:147–160. https://doi.org/10.1016/j.jhealeco.2017.04.005

    Article  Google Scholar 

  • Carmichael SL, Yang W, Roberts EM, Kegley SE, Wolff C, Guo L, Lammer EJ, English P, Shaw GM (2013) Hypospadias and residential proximity to pesticide applications. Pediatrics 132(5):e1216–e1226. https://doi.org/10.1542/peds.2013-1429

    Article  Google Scholar 

  • Cattani D, De Liz Oliveira Cavalli VL, Heinz Rieg CE, Domingues JT, Dal-Cim T, Tasca CI, Mena Barreto Silva FR, Zamoner A (2014) Mechanisms underlying the neurotoxicity induced by glyphosate-based herbicide in immature rat hippocampus: involvement of glutamate excitotoxicity. Toxicology 320:34–45. https://doi.org/10.1016/j.tox.2014.03.001

    Article  CAS  Google Scholar 

  • Cattani D, Cesconetto PA, Tavares MK, Parisotto EB, De Oliveira PA, Heinz Rieg CE, Leite MC, Schroder Prediger RD, Wendt NC, Razzera G, Wilhelm Filho D, Zamoner A (2017) Developmental exposure to glyphosate-based herbicide and depressive-like behavior in adult offspring: Implication of glutamate excitotoxicity and oxidative stress. Toxicology 387:67–80. https://doi.org/10.1016/j.tox.2017.06.001

    Article  CAS  Google Scholar 

  • Cassault-Meyer E, Gress S, Séralini G-É, Galeraud-Denis I (2014) An acute exposure to glyphosate-based herbicide alters aromatase levels in testis and sperm nuclear quality. Environ Toxicol Pharmacol 38(1):131–140. https://doi.org/10.1016/j.etap.2014.05.007

  • Cooney MA, Louis GMB, Sundaram R, McGuiness BM, Lynch CD (2009) Validity of self-reported time to pregnancy. Epidemiology 20(1):56

    Article  Google Scholar 

  • 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. https://doi.org/10.1016/j.acthis.2016.05.009

  • Dallegrave E, Mantese FD, Coelho RS, Pereira JD, Dalsenter PR, Langeloh A (2003) The teratogenic potential of the herbicide glyphosate-roundup in Wistar rats. Toxicol Lett 142(1–2):45–52

    Article  CAS  Google Scholar 

  • Dallegrave E, Mantese FD, Oliveira RT, Andrade AJM, Dalsenter PR, Langeloh A (2007) Pre- and postnatal toxicity of the commercial glyphosate formulation in Wistar rats. Arch Toxicol 81(9):665–673. https://doi.org/10.1007/s00204-006-0170-5

  • Daruich J, Zirulnik F, Gimenez MS (2001) Effect of the herbicide glyphosate on enzymatic activity in pregnant rats and their fetuses. Environ Res 85(3):226–231

    Article  CAS  Google Scholar 

  • De Joaquim AO, Spinosa HS, Macrini DJ, Rodrigues PA, Ricci EL, Artiolli TS, Moreira N, Suffredini IB, Bernardi MM (2012) Behavioral effects of acute glyphosate exposure in male and female balb/c mice. Braz J Vet Res Anim Sci 49(5):367–376

    Article  Google Scholar 

  • De Liz Oliveira Cavalli VL, Cattani D, Heinz Rieg CE, Pierozan P, Zanatta L, Benedetti Parisotto E, Wilhelm Filho D, Mena Barreto Silva FR, Pessoa-Pureur R, Zamoner A (2013) Roundup disrupts male reproductive functions by triggering calcium-mediated cell death in rat testis and Sertoli cells. Free Radic Biol Med 65:335–346. https://doi.org/10.1016/j.freeradbiomed.2013.06.043

    Article  CAS  Google Scholar 

  • De Roos AJ, Blair A, Rusiecki JA, Hoppin JA, Svec M, Dosemeci M, Sandler DP, Alavanja MC (2005) Cancer incidence among glyphosate-exposed pesticide applicators in the agricultural health study. Environ Health Perspect 113(1):49–54. https://doi.org/10.1289/ehp.7340

    Article  CAS  Google Scholar 

  • de Souza JS, Kizys MM, da Conceicao RR, Glebocki G, Romano RM, Ortiga-Carvalho TM, Giannocco G, da Silva ID, Dias da Silva MR, Romano MA, Chiamolera MI (2017) Perinatal exposure to glyphosate-based herbicide alters the thyrotrophic axis and causes thyroid hormone homeostasis imbalance in male rats. Toxicology 377:25–37. https://doi.org/10.1016/j.tox.2016.11.005

    Article  CAS  Google Scholar 

  • de Souza JS, Laureano-Melo R, Herai RH, da Conceicao RR, Oliveira KC, da Silva I, Dias-da-Silva MR, Romano RM, Romano MA, Maciel RMB, Chiamolera MI, Giannocco G (2019) Maternal glyphosate-based herbicide exposure alters antioxidant-related genes in the brain and serum metabolites of male rat offspring. Neurotoxicology 74:121–131. https://doi.org/10.1016/j.neuro.2019.06.004

    Article  CAS  Google Scholar 

  • Dechartres J, Pawluski JL, Gueguen M-M, Jablaoui A, Maguin E, Rhimi M, Charlier TD (2019) Glyphosate and glyphosate-based herbicide exposure during the peripartum period affects maternal brain plasticity, maternal behaviour and microbiome. J Neuroendocrinol 31:e12731

    Article  CAS  Google Scholar 

  • Duong A, Steinmaus C, McHale CM, Vaughan CP, Zhang L (2011) Reproductive and developmental toxicity of formaldehyde: a systematic review. Mutat Res/rev Mutat Res 728(3):118–138

    Article  CAS  Google Scholar 

  • ECHA (2017) Glyphosate not classified as a carcinogen by ECHA—all news—ECHA. https://echa.europa.eu/-/glyphosate-not-classified-as-a-carcinogen-by-echa. Accessed 2 May 2021

  • Gallegos CE, Bartos M, Bras C, Gumilar F, Antonelli MC, Minetti A (2016) Exposure to a glyphosate-based herbicide during pregnancy and lactation induces neurobehavioral alterations in rat offspring. Neurotoxicology 53:20–28

    Article  CAS  Google Scholar 

  • Gallegos CE, Baier CJ, Bartos M, Bras C, Dominguez S, Monaco N, Gumilar F, Gimenez MS, Minetti A (2018) Perinatal glyphosate-based herbicide exposure in rats alters brain antioxidant status, glutamate and acetylcholine metabolism and affects recognition memory. Neurotox Res 34(3):363–374. https://doi.org/10.1007/s12640-018-9894-2

    Article  CAS  Google Scholar 

  • Garry VF, Harkins ME, Erickson LL, Long-Simpson LK, Holland SE, Burroughs BL (2002) Birth defects, season of conception, and sex of children born to pesticide applicators living in the Red River Valley of Minnesota, USA. Environ Health Perspect 110:441–449. https://doi.org/10.1289/ehp.02110s3441

    Article  Google Scholar 

  • Geller AM, Zenick H (2005) Aging and the environment: a research framework. Environ Health Perspect 113(9):1257–1262

    Article  Google Scholar 

  • Guerrero Schimpf M, Milesi MM, Ingaramo PI, Luque EH, Varayoud J (2017) Neonatal exposure to a glyphosate based herbicide alters the development of the rat uterus. Toxicology 376:2–14. https://doi.org/10.1016/j.tox.2016.06.004

    Article  CAS  Google Scholar 

  • Guerrero Schimpf M, Milesi MM, Luque EH, Varayoud J (2018) Glyphosate-based herbicide enhances the uterine sensitivity to estradiol in rats. J Endocrinol 239(2):197–213. https://doi.org/10.1530/joe-18-0207

  • Halwachs S, Schaefer I, Kneuer C, Seibel P, Honscha W (2016) Assessment of ABCG2-mediated transport of pesticides across the rabbit placenta barrier using a novel MDCKII in vitro model. Toxicol Appl Pharmacol 305:66–74. https://doi.org/10.1016/j.taap.2016.06.007

    Article  CAS  Google Scholar 

  • Hamdaoui L, Naifar M, Rahmouni F, Harrabi B, Ayadi F, Sahnoun Z, Rebai T (2018) Subchronic exposure to kalach 360 SL-induced endocrine disruption and ovary damage in female rats. Arch Physiol Biochem 124(1):27–34

    Article  CAS  Google Scholar 

  • Hao Y, Zhang Y, Ni H, Gao J, Yang Y, Xu W, Tao L (2019) Evaluation of the cytotoxic effects of glyphosate herbicides in human liver, lung, and nerve. J Environ Sci Health Part B Pestic Food Contam Agric Wastes 54(9):737–744. https://doi.org/10.1080/03601234.2019.1633215

  • IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2017) Some organophosphate insecticides and herbicides. IARC, Lyon

    Google Scholar 

  • Ingaramo PI, Varayoud J, Milesi MM, Guerrero Schimpf M, Munoz-de-Toro M, Luque EH (2016) Effects of neonatal exposure to a glyphosate-based herbicide on female rat reproduction. Reproduction 152(5):403–415. https://doi.org/10.1530/rep-16-0171

    Article  Google Scholar 

  • Ingaramo PI, Varayoud J, Milesi MM, Guerrero Schimpf M, Alarcón R, Muñoz-de-Toro M, Luque EH (2017) Neonatal exposure to a glyphosate-based herbicide alters uterine decidualization in rats. Reprod Toxicol 73:87–95. https://doi.org/10.1016/j.reprotox.2017.07.022

    Article  CAS  Google Scholar 

  • Ji H, Xu L, Wang Z, Fan X, Wu L (2018) Differential microRNA expression in the prefrontal cortex of mouse offspring induced by glyphosate exposure during pregnancy and lactation. Exp Ther Med 15(3):2457–2467. https://doi.org/10.3892/etm.2017.5669

    Article  CAS  Google Scholar 

  • Jiang X, Zhang N, Yin L, Zhang W, Han F, Liu W, Chen H, Cao J, Liu J (2018) A commercial roundup (R) formulation induced male germ cell apoptosis by promoting the expression of XAF1 in adult mice. Toxicol Lett 296:163–172. https://doi.org/10.1016/j.toxlet.2018.06.1067

  • Joffe M, Key J, Best N, Keiding N, Scheike T, Jensen TK (2005) Studying time to pregnancy by use of a retrospective design. Am J Epidemiol 162(2):115–124

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Koyyada A, Orsu P (2020) Role of hypothyroidism and associated pathways in pregnancy and infertility: clinical insights. Tzu Chi Med J 32(4):312. https://doi.org/10.4103/tcmj.tcmj_255_19

    Article  Google Scholar 

  • Kubsad D, Nilsson EE, King SE, Sadler-Riggleman I, Beck D, Skinner MK (2019) Assessment of glyphosate induced epigenetic transgenerational inheritance of pathologies and sperm epimutations: generational toxicology. Sci Rep. https://doi.org/10.1038/s41598-019-42860.0

    Article  Google Scholar 

  • Kwiatkowska M, Huras B, Bukowska B (2014) The effect of metabolites and impurities of glyphosate on human erythrocytes (in vitro). Pestic Biochem Physiol 109:34–43. https://doi.org/10.1016/j.pestbp.2014.01.003

    Article  CAS  Google Scholar 

  • Kwiatkowska M, Reszka E, Wozniak K, Jablonska E, Michalowicz J, Bukowska B (2017) DNA damage and methylation induced by glyphosate in human peripheral blood mononuclear cells (in vitro study). Food Chem Toxicol 105:93–98. https://doi.org/10.1016/j.fct.2017.03.051

  • Ling C, Liew Z, von Ehrenstein OS, Heck JE, Park AS, Cui X, Cockburn M, Wu J, Ritz B (2018) Prenatal exposure to ambient pesticides and preterm birth and term low birthweight in agricultural regions of California. Toxics. https://doi.org/10.3390/toxics6030041

    Article  Google Scholar 

  • Lioi MB, Scarfi MR, Santoro A, Barbieri R, Zeni O, Di Berardino D, Ursini MV (1998) Genotoxicity and oxidative stress induced by pesticide exposure in bovine lymphocyte cultures in vitro. Mutat Res 403(1–2):13–20. https://doi.org/10.1016/s0027-5107(98)00010-4

    Article  CAS  Google Scholar 

  • Lorenz V, Milesi MM, Guerrero Schimpf M, Luque EH, Varayoud J (2019) Epigenetic disruption of estrogen receptor alpha is induced by a glyphosate-based herbicide in the preimplantation uterus of rats. Mol Cell Endocrinol 480:133–141. https://doi.org/10.1016/j.mce.2018.10.022

    Article  CAS  Google Scholar 

  • Malagoli C, Costanzini S, Heck JE, Malavolti M, De Girolamo G, Oleari P, Palazzi G, Teggi S, Vinceti M (2016) Passive exposure to agricultural pesticides and risk of childhood leukemia in an Italian community. Int J Hyg Environ Health 219(8):742–748. https://doi.org/10.1016/j.ijheh.2016.09.015

    Article  CAS  Google Scholar 

  • Manrique-Zuluaga V, Carmona-Alert P (2019) Glifosato en qué consiste el debate? Observatorio Iberoamericano de Cultivos y Drogas Ilícitas, Boletin, p 25

    Google Scholar 

  • Manservisi F, Lesseur C, Panzacchi S, Mandrioli D, Falcioni L, Bua L, Manservigi M, Spinaci M, Galeati G, Mantovani A, Lorenzetti S, Miglio R, Andrade AM, Kristensen DM, Perry MJ, Swan SH, Chen J, Belpoggi F (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: Global Access Sci Source 18(1):15. https://doi.org/10.1186/s12940-019-0453-y

  • Mao Q, Manservisi F, Panzacchi S, Mandrioli D, Menghetti I, Vornoli A, Bua L, Falcioni L, Lesseur C, Chen J, Belpoggi F, Hu J (2018) The Ramazzini Institute 13-week pilot study on glyphosate and Roundup administered at human-equivalent dose to Sprague Dawley rats: effects on the microbiome. Environ Health. https://doi.org/10.1186/s12940-018-0394-x

  • Marc J, Mulner-Lorillon O, Belle R (2004) Glyphosate-based pesticides affect cell cycle regulation. Biol Cell 96(3):245–249. https://doi.org/10.1016/j.biolcel.2003.11.010

    Article  CAS  Google Scholar 

  • Martinez A, Al-Ahmad AJ (2019) Effects of glyphosate and aminomethylphosphonic acid on an isogeneic model of the human blood-brain barrier. Toxicol Lett 304:39–49. https://doi.org/10.1016/j.toxlet.2018.12.013

    Article  CAS  Google Scholar 

  • Martínez MA, Ares I, Rodríguez JL, Martínez M, Martínez-Larrañaga MR, Anadón A (2018) Neurotransmitter changes in rat brain regions following glyphosate exposure. Environ Res 161:212–219. https://doi.org/10.1016/j.envres.2017.10.051

    Article  CAS  Google Scholar 

  • Mesnage R, Bernay B, Séralini GE (2013) Ethoxylated adjuvants of glyphosate-based herbicides are active principles of human cell toxicity. Toxicology 313(2–3):122–128

    Article  CAS  Google Scholar 

  • Mesnage R, Phedonos A, Biserni M, Arno M, Balu S, Corton JC, Ugarte R, Antoniou MN (2017) Evaluation of estrogen receptor alpha activation by glyphosate-based herbicide constituents. Food Chem Toxicol 108:30–42. https://doi.org/10.1016/j.fct.2017.07.025

  • Milesi MM, Lorenz V, Pacini G, Repetti MR, Demonte LD, Varayoud J, Luque EH (2018) Perinatal exposure to a glyphosate-based herbicide impairs female reproductive outcomes and induces second-generation adverse effects in Wistar rats. Arch Toxicol 92(8):2629–2643

    Article  CAS  Google Scholar 

  • Monge P, Wesseling C, Guardado J, Lundberg I, Ahlbom A, Cantor KP, Weideroass E, Partanen T (2007) Parental occupational exposure to pesticides and the risk of childhood leukemia in Costa Rica. Scand J Work Environ Health 33(4):293–303. https://doi.org/10.5271/sjweh.1146

    Article  CAS  Google Scholar 

  • Monroy CM, Cortés AC, Sicard DM, de Restrepo HG (2005) Citotoxicidad y genotoxicidad en células humanas expuestas in vitro a glifosato. Biomedica 25(3):335–345

    Article  Google Scholar 

  • Nardi J, Moras PB, Koeppe C, Dallegrave E, Leal MB, Rossato-Grando LG (2017) Prepubertal subchronic exposure to soy milk and glyphosate leads to endocrine disruption. Food Chem Toxicol Int J Pub British Indust Biol Res Assoc 100:247–252. https://doi.org/10.1016/j.fct.2016.12.030

  • Owagboriaye FO, Dedeke GA, Ademolu KO, Olujimi OO, Ashidi JS, Adeyinka AA (2017) Reproductive toxicity of Roundup herbicide exposure in male albino rat. Exp Toxicol Pathol Off J Ges Fur Toxikol Pathol 69(7):461–468. https://doi.org/10.1016/j.etp.2017.04.007

  • Paganelli A, Gnazzo V, Acosta H, Lopez SL, Carrasco AE (2010) Glyphosate-based herbicides produce teratogenic effects on vertebrates by impairing retinoic acid signaling. Chem Res Toxicol 23(10):1586–1595. https://doi.org/10.1021/tx1001749

    Article  CAS  Google Scholar 

  • Parvez S, Gerona RR, Proctor C, Friesen M, Ashby JL, Reiter JL, Lui Z, Winchester PD (2018) Glyphosate exposure in pregnancy and shortened gestational length: a prospective Indiana birth cohort study. Environ Health 17(1):23

    Article  CAS  Google Scholar 

  • Paz-Y-Miño C, Sánchez ME, Arévalo M, Muñoz MJ, Witte T, De-La-Carrera GO, Leone PE (2007) Evaluation of DNA damage in an Ecuadorian population exposed to glyphosate. Genet Mol Biol 30(2):456–460

    Article  Google Scholar 

  • Peillex C, Pelletier M (2020) The impact and toxicity of glyphosate and glyphosate-based herbicides on health and immunity. J Immunotoxicol 17(1):163–174. https://doi.org/10.1080/1547691X.2020.1804492

    Article  CAS  Google Scholar 

  • Perego MC, Schutz LF, Caloni F, Cortinovis C, Albonico M, Spicer LJ (2017) Evidence for direct effects of glyphosate on ovarian function: glyphosate influences steroidogenesis and proliferation of bovine granulosa but not theca cells in vitro. JAT 37(6):692–698

    CAS  Google Scholar 

  • Pham TH, Derian L, Kervarrec C, Kernanec PY, Jegou 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. https://doi.org/10.1093/toxsci/kfz039

  • Racz PI, Wildwater M, Rooseboom M, Kerkhof E, Pieters R, Yebra-Pimentel ES, Dirks RP, Spaink HP, Smulders C, Whale GF (2017) Application of Caenorhabditis elegans (nematode) and Danio rerio embryo (zebrafish) as model systems to screen for developmental and reproductive toxicity of Piperazine compounds. Toxicol Vitro 44:11–16

    Article  CAS  Google Scholar 

  • Rappazzo KM, Warren JL, Davalos AD, Meyer RE, Sanders AP, Brownstein NC, Luben TJ (2019) Maternal residential exposure to specific agricultural pesticide active ingredients and birth defects in a 2003–2005 North Carolina birth cohort. Birth Defects Res 111(6):312–323. https://doi.org/10.1002/bdr2.1448

    Article  CAS  Google Scholar 

  • Razi M, Najafi G, Feyzi S, Karimi A, Shahmohamadloo S, Nejati V (2012) Histological and histochemical effects of gly-phosate on testicular tissue and function. Iran J Reprod Med 10(3):181–192

  • 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

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1007/s00204-011-0788-9

    Article  CAS  Google Scholar 

  • Rull RP, Ritz B, Shaw GM (2006) Neural tube defects and maternal residential proximity to agricultural pesticide applications. Am J Epidemiol 163(8):743–753

    Article  Google Scholar 

  • Sanin LH, Carrasquilla G, Solomon KR, Cole DC, Marshall EJ (2009) Regional differences in time to pregnancy among fertile women from five Colombian regions with different use of glyphosate. J Toxicol Environ Health A 72(15–16):949–960

    Article  CAS  Google Scholar 

  • Savitz DA, Arbuckle T, Kaczor D, Curtis KM (1997) Male pesticide exposure and pregnancy outcome. Am J Epidemiol 146(12):1025–1036

    Article  CAS  Google Scholar 

  • Schaefer HR, Myers JL (2017) Guidelines for performing systematic reviews in the development of toxicity factors. Regul Toxicol Pharmacol 91:124–141

    Article  Google Scholar 

  • Schatten H, Constantinescu GM (2017) Animal models and human reproduction. Wiley, New Jersy

    Book  Google Scholar 

  • Schneider K, Schwarz M, Burkholder I, Kopp-Schneider A, Edler L, Kinsner-Ovaskainen A, Hartung T, Hoffmann S (2009) “ToxRTool”, a new tool to assess the reliability of toxicological data. Toxicol Lett 189(2):138–144

    Article  CAS  Google Scholar 

  • Shaw W (2017) Elevated urinary glyphosate and clostridia metabolites with altered dopamine metabolism in triplets with autistic spectrum disorder or suspected seizure disorder: a case study. Integr Med 16(1):50–57

    Google Scholar 

  • Shrestha S, Parks CG, Goldner WS, Kamel F, Umbach DM, Ward MH, Lerro CC, Koutros S, Hofmann JN, Beane Freeman LE, Sandler DP (2018) Pesticide use and incident hypothyroidism in pesticide applicators in the agricultural health study. Environ Health Perspect 126(9):97008–97008

    Article  CAS  Google Scholar 

  • Siviková K, Dianovsky J (2006) Cytogenetic effect of technical glyphosate on cultivated bovine peripheral lymphocytes. Int J Hyg Environ Health 209(1):15–20

    Article  CAS  Google Scholar 

  • Solomon KR, Anadón A, Carrasquilla G, Cerdeira AL, Marshall EJP, Sanin L-H (2007) Coca and poppy eradication in Colombia: environmental and human health assessment of aerially applied glyphosate. In: Ware GW, Whitacre DM, Gunther FA (eds) Reviews of environmental contamination and toxicology: continuation of residue reviews. Springer, New York, pp 43–125

    Chapter  Google Scholar 

  • Sosa B, Fontans-Álvarez E, Romero D, da Fonseca A, Achkar M (2019) Analysis of scientific production on glyphosate: an example of politicization of science. Sci Total Environ 681:541–550. https://doi.org/10.1016/j.scitotenv.2019.04.379

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1007/s00204-017-1962-5

    Article  CAS  Google Scholar 

  • 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 Develop Origins Health Dis 11(2):146–153. https://doi.org/10.1017/S2040174419000382

  • Thongprakaisang S, Thiantanawat A, Rangkadilok N, Suriyo T, Satayavivad J (2013) Glyphosate induces human breast cancer cells growth via estrogen receptors. Food Chem Toxicol 59:129–136. https://doi.org/10.1016/j.fct.2013.05.057

  • UNICEF (2018) Understanding the impact of pesticides on children. A discussion paper. New York, 2018. http://www.ounipestiziden.lu/uploads/2/2/4/8/22480338/2018_01_xx_understanding_the_impact_of_pesticides_on_children-unicef.pdf. Accessed 2 May 2021

  • UNODC (2018) Coca crops in Colombia at all-time high, UNODC report finds. United Nations office on drugs and crime. http://www.unodc.org/unodc/en/frontpage/2018/September/coca-crops-in-colombia-at-all-time-high--unodc-report-finds.html?ref=fs1. Accessed 2 May 2021

  • Upadhyay J, Rana M, Bisht SS, Rana A, Durgapal S, Juyal V (2019) Biomarker responses (serum biochemistry) in pregnant female Wistar rats and histopathology of their neonates exposed prenatally to pesticides. Braz J Pharm Sci. https://doi.org/10.1590/s2175-97902019000118194

    Article  Google Scholar 

  • USEPA (1996) Guidelines for reproductive toxicity risk assessment. https://www.epa.gov/risk/guidelines-reproductive-toxicity-risk-assessment. Accessed 2 May 2021

  • Varayoud J, Durando M, Ramos JG, Milesi MM, Ingaramo PI, Munoz-de-Toro M, Luque EH (2017) Effects of a glyphosate-based herbicide on the uterus of adult ovariectomized rats. Environ Toxicol 32(4):1191–1201. https://doi.org/10.1002/tox.22316

    Article  CAS  Google Scholar 

  • von Ehrenstein OS, Ling C, Cui X, Cockburn M, Park AS, Yu F, Wu J, Ritz B (2019) Prenatal and infant exposure to ambient pesticides and autism spectrum disorder in children: population based case-control study. BMJ. https://doi.org/10.1136/bmj.l962

    Article  Google Scholar 

  • Watts M, Clausing P, Lyssimachou A, Schutte G, Gudagnini R, Marquez E (2016) The glyphosate monograph. A comprehensive new review of the science documenting the adverse human health and environmental impacts of glyphosate and glyphosate based herbicides. Pesticide Action Network International, UK

    Google Scholar 

  • Weselak M, Arbuckle TE, Wigle DT, Krewski D (2007) In utero pesticide exposure and childhood morbidity. Environ Res 103(1):79–86. https://doi.org/10.1016/j.envres.2006.09.001

    Article  CAS  Google Scholar 

  • Williams AL, Watson RE, DeSesso JM (2012) Developmental and reproductive outcomes in humans and animals after glyphosate exposure: a critical analysis. J Toxicol Environ Health Part B 15(1):39–96

    Article  CAS  Google Scholar 

  • World Health Organization (2006) Reproductive health indicators: guidelines for their generation, interpretation and analysis for global monitoring. World Health Organization, Geneva

    Google Scholar 

  • World Health Organization (2011) Introduction to reproductive health and the environment. World Health Organization, Geneva

    Google Scholar 

  • Yousef MI, Salem MH, Ibrahim HZ, Helmi S, Seehy MA, Bertheussen K (1995) Toxic effects of carbofuran and glyphosate on semen characteristics in rabbits. J Environ Sci Health Part B 30(4):513–534

    Article  CAS  Google Scholar 

  • Yu N, Tong Y, Zhang D, Zhao S, Fan X, Wu L, Ji H (2018) Circular RNA expression profiles in hippocampus from mice with perinatal glyphosate exposure. Biochem Biophys Res Commun 501(4):838–845

    Article  CAS  Google Scholar 

  • Zhang J-W, Xu D-Q, Feng X-Z (2019) The toxic effects and possible mechanisms of glyphosate on mouse oocytes. Chemosphere 237:124435–124435

    Article  CAS  Google Scholar 

  • Zimdahl RL (2003) WEEDS | weed technology and control. In: Thomas B (ed) Encyclopedia of applied plant sciences. Elsevier, Amsterdam, pp 1508–1516

    Chapter  Google Scholar 

Download references

Funding

This work was funded by the Universidad del Valle and a grant from the Center for Reproductive Rights.

Author information

Authors and Affiliations

Authors

Contributions

FM, JO and NA conceptualised the study design. Search for articles in databases and screening was conducted by JO. Final selection of articles was revised by all authors. Data extraction and analysis were conducted by FM, JO and NA. The writing, editing and proofreading of the final manuscript was performed by all authors.

Corresponding author

Correspondence to Fabian Mendez.

Ethics declarations

Conflict of interest

All authors certify they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mendez, F., Ordoñez-Betancourth, J. & Abrahams, N. Effects of Glyphosate Exposure on Reproductive Health: A Systematic Review of Human, Animal and In-Vitro Studies. Expo Health 14, 635–669 (2022). https://doi.org/10.1007/s12403-021-00442-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12403-021-00442-4

Keywords

Navigation