Abstract
Organopesticides (OPs) are a group of various synthetic chemicals prevalently used in agriculture and homestead plantations. OPs were originally developed to remove insects, weeds, and other pests from agricultural fields for improving crop yields. Modern pesticides including organochlorine pesticides, organophosphorus pesticides, and amido-formyl ester are closely related to our lives. Many people are exposed to various OPs during farming practice. OPs can cause adverse effects and provoke serious impacts on normal reproductive functions of humans, resulting in loss of fertility. The effects of OPs in the reproductive system include association with fluctuation in the levels of sex hormones, delayed menstrual cycle, ovarian dysfunction, alteration in ovary weight, changes of follicle growth, altered oocyte feasibility, and changed the quality of spermatogenesis. Current literature clearly states that exposure to various OPs can impair the fertility of women and cause a high risk of reproductive potential. However, investigations on OPs exposure to woman fertility remain scarce. This review highlights effects of exposure to OPs on the fertility of occupational women and mechanisms of action involved in such effects on the reproductive function of women along with their related impacts.
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Akkina J, Reif J, Keefe T, Bachand A (2004) Age at natural menopause and exposure to organochlorine pesticides in Hispanic women. J Toxicol Environ Health A 67:1407–1422
Alahmar AT (2019) Role of oxidative stress in male infertility: an updated review. J Hum Reprod Sci 12(1):4–18
Al-Shamary NM, Al-Ghouti MA, Al-Shaikh I, Al-Meer SH, Ahmad TA (2016) Evaluation of pesticide residues of organochlorine in vegetables and fruits in Qatar: statistical analysis. Environ Monit Assess 188(3):198
Axmon A, Rylander L, Strömberg U, Hagmar L (2000) Miscarriages and stillbirths in women with a high intake of fish contaminated with persistent organochlorine compounds. Int Arch Occup Environ Health 73(3):204–208
Baligar PN, Kaliwal BB (2001) Induction of gonadal toxicity to female rats after chronic exposure to mancozeb. Ind Health 39(3):235–243
Bindali BB, Kaliwal BB (2002) Anti-implantation effect of carbamate fungicide mancozeb in albino mice. Ind Health 40:191–197
Blanco-Muñoz J, Morales MM, Lacasaña M, Aguilar-Garduño C, Bassol S, Cebrián ME (2010) Exposure to organophosphate pesticides and male hormone profile in floriculturist of the state of Morelos, Mexico. Human Reprod 25(7):1787–1795
Boesch P, Weber-Lotfi F, Ibrahim N, Tarasenko V, Cosset A, Paulus F, Lightowlers RN, Dietrich A (2011) DNA repair in organelles: pathways, organization, regulation, relevance in disease and ageing. Biochim Biophys Acta 1813:186–200
Bolognesi C, Creus A, Ostrosky-Wegman P, Marcos R (2011) Micronuclei and pesticide exposure. Mutagenesis 26:19–26
Bretveld RW, Thomas CM, Scheepers PT, Zielhuis GA, Roeleveld N (2006) Pesticide exposure: The hormonal function of the female reproductive system disrupted. Reprod Biol Endocrinol 4:30
Briz V, Molina-Molina JM, Sánchez-Redondo S, Fernández MF, Grimalt JO, Olea N, Rodríguez-Farré E, Suñol C (2011) Differential estrogenic effects of the persistent organochlorine pesticides dieldrin, endosulfan and lindane in primary neuronal cultures. Toxicol Sci 120(2):413–427
Buah-Kwofie A, Humphries MS, Pillay L (2019) Dietary exposure and risk assessment of organochlorine pesticide residues in rural communities living within catchment areas of iSimangaliso World Heritage Site, South Africa. Environ Sci Pollut Res Int 26(17):17774–17786
Bulger WH, Muccitelli RM, Kupfer D (1978) Studies on the in vivo and in vitro estrogenic activities of methoxychlor and its metabolites. Role of hepatic mono-oxygenase in methoxychlor activation. Biochem Pharmacol 27:2417–2423
Calaf GM, Ponce-Cusi R, Aguayo F, Muñoz JP, Bleak TC (2020) Endocrine disruptors from the environment affecting breast cancer. Oncol Lett 20(1):19–32
Carvalho FP, Fowler SW, Readman JW, Mee LD (1992) Pesticide residues in tropical coastal lagoons: the use of 14C-labelled compounds to study cycling and fates of agrochemicals in applications of isotopes and radiation in conservation of the environment. Proceed Int Symposium, IAEA, Vienna, 637–653
Carvalho FP, Villeneuve JP, Cattini C, Tolosa I, Montenegro-Guillén S, Lacayo M, Cruz A (2002a) Ecological risk assessment of pesticide residues in coastal lagoons of Nicaragua. J Environ Monit 4:778–787
Carvalho FP, Gonzalez-Farias F, Villeneuve JP, Cattini C, Hernandez-Garza M, Mee LD, Fowler SW (2002b) Distribution, fate and effects of pesticide residues in tropical coastal lagoons of the northwest of Mexico. Environ Technol 23:1257–1270
Chadwick RW, Cooper RL, Chang J, Rehnberg GL, McElroy WK (1988) Possible antiestrogenic activity of lindane in female rats. J Biochem Toxicol 3:147–158
Chang GR (2018) Persistent organochlorine pesticides in aquatic environments and fishes in Taiwan and their risk assessment. Environ Sci Pollut Res Int 25(8):7699–7708
Chapin RE, Harris MW, Davis BJ, Ward SM, Wilson RE, Mauney MA, Lockhart AC, Smialowicz RJ, Moser VC, Burka LT, Collins BJ (1997) The effects of perinatal/juvenile methoxychlor exposure on adult rat nervous, immune, and reproductive system function. Fundam Appl Toxicol 40:138–157
Chevrier J, Eskenazi B, Holland N, Bradman A, Barr DB (2008) Effects of exposure to polychlorinated biphenyls and organochlorine pesticides on thyroid function during pregnancy. Am J Epidemiol 168(3):298–310
Chevrier C, Warembourg C, Gaudreau E, Monfort C, Le Blanc A, Guldner L, Cordier S (2013) Organochlorine pesticides, polychlorinated biphenyls, seafood consumption, and time-to pregnancy. Epidemiology 24:251–260
Chiu YH, Williams PL, Gillman MW, Gaskins AJ, Mínguez-Alarcón L, Souter I, Toth TL, Ford JB, Hauser R, Chavarro JE, EARTH Study Team (2018) Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology. JAMA Intern Med 178(1):17–26
Cohn BA, Cirillo PM, Wolff MS, Schwingl PJ, Cohen RD, Sholtz RI, Ferrara A, Christianson RE, van den Berg BJ, Siiteri PK (2003) DDT and DDE exposure in mothers and time to pregnancy in daughters. Lancet 361(9376):2205–2206
Cohn BA, Cirillo PM, Christianson RE (2010) Prenatal DDT exposure and testicular cancer: a nested case-control study. Arch Environ Occup Health 65(3):127–134
Cooper RL, Barrett MA, Goldman JM, Rehnberg GR, McElroy WK, Stoker TE (1994) Pregnancy alterations following xenobiotic-induced delays in ovulation in the female rat. Fundam Appl Toxicol 22:474–480
Costa LG, Olibet G, Murphy SD (1988) Alpha 2-adrenoceptors as atarget for formamidine pesticides: in vitro and in vivo studies in mice. Toxicol Appl Pharmacol 93:319–328
Craig ZR, Hannon PR, Flaws JA (2013) Pregnenolone co-treatment partially restores steroidogenesis, but does not prevent growth inhibition and increased atresia in mouse ovarian antral follicles treated with mono-hydroxy methoxychlor. Toxicol Appl Pharmacol 272:780–786
Cummings AM (1997) Methoxychlor as a model for environmental estrogens. Crit Rev Toxicol 27(4):367–379
Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, Zoeller RT, Gore AC (2009) Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev 30(4):293–342
EEA (2013) Late lessons from early warnings: science, precaution, innovation. European Environment Agency, Report No 1/2013. EEA, Copenhagen
Eldridge JC, Fleenor-Heyser DG, Extrom PC, Wetzel LT, Breckenridge CB, Gillis JH, Luempert LG III, Stevens JT (1994) Short-term effects of chlorotriazines on estrus in female Sprague-Dawley and Fischer 344 rats. J Toxicol Environ Health 43:155–167
Eskenazi B, Marks AR, Bradman A, Fenster L, Johnson C, Barr DB, Jewell NP (2006) In utero exposure to dichlorodiphenyltrichloroethane (DDT) and dichlorodiphenyldichloroethylene (DDE) and neurodevelopment among young Mexican American children. Paediatrics 118:233–241
Fan J, Otterlei M, Wong HK, Tomkinson AE, Wilson DM (2004) 3rd. XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res 32:2193–2201
Farr SL, Cooper GS, Cai J, Savitz DA, Sandler DP (2004) Pesticide use and menstrual cycle characteristics among premenopausal women in the Agricultural Health Study. Am J Epidemiol 160:1194–1204
Farr SL, Cai J, Savitz DA, Sandler DP, Hoppin JA, Cooper GS (2006) Pesticide exposure and timing of menopause: the Agricultural Health Study. Am J Epidemiol 163:731–742
Gaido KW, Maness SC, McDonnell DP, Dehal SS, Kupfer D, Safe S (2000) Interaction of methoxychlor and related compounds with estrogen receptor α and β, and androgen receptor: structure-activity studies. Mol Pharmacol 58(4):852–858
Gerhard I, Monga B, Krähe J, Runnebaum B (1999) Chlorinated hydrocarbons in infertile women. Environ Res 80(4):299–310
Germain P, Staels B, Dacquet C, Spedding M, Laudet V (2006) Overview of nomenclature of nuclear receptors. Pharmacol Rev 58(4):685–704
Gojmerac T, Kartal B, Curic S, Zuric M, Kusevic S, Cvetnic Z (1996) Serum biochemical changes associated with cystic ovarian degeneration in pigs after atrazine treatment. Toxicol Lett 85:9–15
Goode EL, Ulrich CM, Potter JD (2002) Polymorphisms in DNA repair genes and associations with cancer risk. Cancer Epidemiol Biomarkers Prev 11(12):1513–1530
Grandjean P, Bellinger D, Bergman A, Cordier S, Davey-Smith G, Eskenazi B, Gee D, Gray K, Hanson M, van den Hazel P, Heindel JJ, Heinzow B, Hertz-Picciotto I, Hu H, Huang TT, Jensen TK, Landrigan PJ, McMillen IC, Murata K, Ritz B, Schoeters G, Skakkebaek NE, Skerfving S, Weihe P (2008) The Faroes statement: human health effects of developmental exposure to chemicals in our environment. Basic Clin Pharmacol Toxicol 102(2):73–75
Gray LE Jr, Wolf C, Lambright C, Mann P, Price M, Cooper RL, Ostby J (1999) Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p,p'-DDE, and ketoconazole) and toxic substances (dibutyl- and diethylhexyl phthalate, PCB 169, and ethane dimethane sulphonate) during sexual differentiation produces diverse profiles of reproductive malformations in the male rat. Toxicol Ind Health 15:94–118
Gray LE, Ostby J, Furr J, Wolf CJ, Lambright C, Parks L, Veeramachaneni DN, Wilson V, Price M, Hotchkiss A, Orlando E, Guillette L (2001) Effects of environmental anti-androgens on reproductive development in experimental animals. Hum Reprod Update 7:248–264
Greenlee AR, Arbuckle TE, Chyou PH (2003) Risk factors for female infertility in an agricultural region. Epidemiology 14(4):429–436
Guo Z, Qiu H, Wang L, Wang L, Wang C, Chen M, Zuo Z (2017) Association of serum organochlorine pesticides concentrations with reproductive hormone levels and polycystic ovary syndrome in a Chinese population. Chemosphere 171:595e600
Haake J, Kelley M, Keys B, Safe S (1987) The effects of organochlorine pesticides as inducers of testosterone and benzo[a]pyrene hydroxylases. Gen Pharmacol 18:165–169
Hart RW, Hall KY, Daniel FB (1978) DNA repair and mutagenesis in mammalian cells. Photochem Photobiol 28:131–155
Hass U, Christiansen S, Axelstad M, Scholze M, Boberg J (2017) Combined exposure to low doses of pesticides causes decreased birth weights in rats. Reprod Toxicol 72:97–105
Hayes TB, Case P, Chui S, Chung D, Haeffele C, Haston K, Lee M, Mai VP, Marjuoa Y, Parker J, Tsui M (2006) Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environ Health Perspect 114(1):40–50
Hayes TB, Khoury V, Narayan A, Nazir M, Park A, Brown T, Adame L, Chan E, Buchholz D, Stueve T, Gallipeau S (2010) Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopuslaevis). Proc Natl Acad Sci USA 107(10):4612–4617
Hirsch KS, Weaver DE, Black LJ, Falcone JF, MacLusky NJ (1987) Inhibition of central nervous system aromatase activity: a mechanism for fenarimol-induced infertility in the male rat. Toxicol Appl Pharmacol 91(2):235–245
Hu Y, Ji L, Zhang Y, Shi R, Han W, Tse LA, Pan R, Wang Y, Ding G, Xu J, Zhang Q, Gao Y, Tian Y (2018) Organophosphate and pyrethroid pesticide exposures measured before conception and associations with time to pregnancy in Chinese couples enrolled in the Shanghai birth cohort. Environ Health Perspect 126(7):077001
Idrovo AJ, Sanìn LH, Cole D, Chavarro J, Cáceres H, Narváez J, Restrepo M (2005) Time to first pregnancy among women working in agricultural production. Int Arch Occup Environ Health 78(6):493–500
Jayaraj R, Megha P, Sreedev P (2016) Organochlorine pesticides, their toxic effects on living organisms and their fate in the environment. Interdiscip Toxicol 9(3-4):90–100
Kaiser J (2000) Endocrine disruptors: Panel cautiously confirms low-dose effects. Science 290:695–697
Kaur K, Kaur R (2018) Occupational pesticide exposure, impaired DNA repair, and diseases. Indian J Occup Environ Med 22:74–81
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
Kettles MK, Browning SR, Prince TS, Horstman SW (1997) Triazine herbicide exposure and breast cancer incidence: an ecologic study of Kentucky counties. Environ Health Perspect 105(11):1222–1227
Kumar R, Uppal RP (1986) Effect of malathion on estrous cycle and reproductive performance of rats. J Environ Biol 7:35–39
Kumar S, Sharma A, Kshetrimayum C (2019) Environmental & occupational exposure & female reproductive dysfunction. Indian J Med Res 150(6):532–545
Latif Y, Sherazi STH, Bhanger MI (2011) Assessment of pesticide residues in commonly used vegetables in Hyderabad, Pakistan. Ecotoxicol Environ Saf 74(8):2299–2303
Lee S, Kim S, Lee HK, Lee IS, Park J, Kim HJ, Lee JJ, Choi G, Choi S, Kim S, Kim SY, Choi K, Kim S, Moon HB (2013a) Contamination of polychlorinated biphenyls and organochlorine pesticides in breast milk in Korea: time-course variation, influencing factors, and exposure assessment. Chemosphere 93(8):1578–1585
Lee HR, Jeung EB, Cho MH, Kim TH, Leung PC, Choi KC (2013b) Molecular mechanism(s) of endocrine-disrupting chemicals and their potent oestrogenicity in diverse cells and tissues that express oestrogen receptors. J Cell Mol Med 17(1):1–11
Lee JE, Jung HW, Lee YJ, Lee YA (2019) Early-life exposure to endocrine-disrupting chemicals and pubertal development in girls. Ann Pediatr Endocrinol Metab 24(2):78–91
Leemans M, Couderq S, Demeneix B, Fini JB (2019) Pesticides with potential thyroid hormone-disrupting effects: A review of recent data. Front Endocrinol 9(10):743
Li AJ, Chen Z, Lin TC, Buck Louis GM, Kannan K (2020) Association of urinary metabolites of organophosphate and pyrethroid insecticides, and phenoxy herbicides with endometriosis. Environ Int 136:105456
Loizou JI, El-Khamisy SF, Zlatanou A, Moore DJ, Chan DW, Qin J, Sarno S, Meggio F, Pinna LA, Caldecott KW (2004) The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks. Cell 117(17):28
Lu C, Toepel K, Irish R, Fenske RA, Barr DB, Bravo R (2006) Organic diets significantly lower children's dietary exposure to organophosphorus pesticides. Environ Health Perspect 114(2):260–263
Luderer U, Kesner JS, Fuller JM, Krieg EF Jr, Meadows JW, Tramma SL, Yang H, Baker D (2013) Effects of gestational and lactational exposure to heptachlor epoxide on age at puberty and reproductive function in men and women. Environ Res 121:84–94
Lushchak VI, Matviishyn TM, Husak VV, Storey JM, Storey KB (2018) Pesticide toxicity: a mechanistic approach. Excli J 17:1101–1136
Ma J, Lin F, Zhang R, Yu W, Lu N (2004) Differential sensitivity of two green algae, Scenedesmus quadricauda and Chlorella vulgaris, to 14 pesticide adjuvants. Ecotoxicol Environ Saf 58(1):61–67
Marks AR, Harley K, Bradman A, Kogut K, Barr DB, Johnson C, Calderon N, Eskenazi B (2010) Organophosphate pesticide exposure and attention in young Mexican-American children: the CHAMACOS study. Environ Health Perspect 118(12):1768–1774
Marques-Pinto A, Carvalho D (2013) Human infertility: are endocrine disruptors to blame? Endocr Connect 2(3):R15–R29
Marsin S, Vidal AE, Sossou M, Ménissier-de Murcia J, Le Page F, Boiteux S, de Murcia G, Radicella JP (2003) Role of XRCC1 in the coordination and stimulation of oxidative DNA damage repair initiated by the DNA glycosylase hOGG1. J Biol Chem 278:44068–44074
Martenies SE, Perry MJ (2013) Environmental and occupational pesticide exposure and human sperm parameters: a systematic review. Toxicology 307:66–73
Martinez EM, Swartz WJ (1991) Effects of methoxychlor on the reproductive system of the adult female mouse. 1. Gross and histologic observations. ReprodToxicol 5:139–147
Meeker JD, Maity A, Missmer SA, Williams PL, Mahalingaiah S, Ehrlich S, Berry KF, Altshul L, Perry MJ, Cramer DW, Hauser R (2011) Serum concentrations of polychlorinated biphenyls in relation to in vitro fertilization outcomes. Environ Health Perspect 119(7):1010–1016
Mulder TA, van den Dries MA, Korevaar TIM, Ferguson KK, Peeters RP, Tiemeier H (2019) Organophosphate pesticides exposure in pregnant women and maternal and cord blood thyroid hormone concentrations. Environ Int 132:105124
Nandipati S, Litvan I (2016) Environmental exposures and Parkinson's disease. Int J Environ Res Public Health 13(9):E881
Nash RA, Caldecott KW, Barnes DE, Lindahl T (1997) XRCC1 protein interacts with one of two distinct forms of DNA ligase III. Biochemistry 36(17):5207–5211
Ngoula F, Watcho P, Kenfack A, Manga JN, Defang HF, Pierre K, Joseph T (2014) Effect of dimethoate (an organophosphate insecticide) on the reproductive system and fertility of adult male rat. Am J Pharmacol Toxicol 9(1):75–83
Nicolopoulou-Stamati P, Pitsos MA (2001) The impact of endocrine disrupters on the female reproductive system. Hum Reprod Update. 7(3):323–330
Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L (2016) Chemical pesticides and human health: the urgent need for a new concept in agriculture. Front Public Health 4:148
Oduma JA, Wango EO, Oduor-Okelo D, Makawiti DW, Odongo H (1995) In vivo and in vitro effects of graded doses of the pesticide heptachlor on female sex steroid hormone production in rats. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 111:191–196
Olisah C, Okoh OO, Okoh AI (2020) Occurrence of organochlorine pesticide residues in biological and environmental matrices in Africa: a two-decade review. Heliyon 6:03518
Ostby J, Kelce WR, Lambright C, Wolf CJ, Mann P, Gray LE (1999) The fungicide procymidone alters sexual differentiation in the male rat by acting as an androgen-receptor antagonist in vivo and in vitro. Toxicol Ind Health 15:80–93
Oyeyiola AO, Fatunsin OT, Akanbi LM, Fadahunsi DE, Moshood O (2017) Human health risk of organochlorine pesticides in foods grown in Nigeria. J Health Pollut 7(15):63–70
Palanza P, Parmigiani S, Liu H, vom Saal FS (1999) Prenatal exposure to low doses of the estrogenic chemicals diethylstilbestrol and o,p'-DDT alters aggressive behavior of male and female house mice. Pharmacol Biochem Behav 64:665–672
Pandey AK, Nagpure NS, Trivedi SP, Kumar R, Kushwaha B (2011) Profenofos induced DNA damage in freshwater fish, Channa punctatus (Bloch) using alkaline single cell gel electrophoresis. Mutat Res 726:209–214
Parveen A, Vasanta N (1986) Effects of endosulfan on the nucleic acid content in different tissues of freshwater fish, Clariasbatrachus. Proc 7th Nat Symp Ind Soc Life Sci 31-38
Patel S (2017) Disruption of aromatase homeostasis as the cause of a multiplicity of ailments: A comprehensive review. J Steroid Biochem Molecular Biol 168:19–25
Philippe V, Neveen A, Marwa A, Ahmad Basel AY (2021) Occurrence of pesticide residues in fruits and vegetables for the Eastern Mediterranean region and potential impact on public health. Food Control 119:107457
Pizzorno J (2018) Environmental toxins and infertility. Integr Med 17(2):8–11
Prakash N, Narayana K, Murthy GS, Moudgal NR, Honnegowda (1992) The effect of malathion, an organophosphate, on the plasma FSH, 17 beta-estradiol and progesterone concentrations and acetylcholinesterase activity and conception in dairy cattle. Vet Hum Toxicol 34:116–119
Priyanka R, Pranay Kumar P, Debojit C, Surajeet B (2017) Pesticides, insecticides and male infertility. Int J Reprod Contracept Obstet Gynecol 6(8):3387–3391
Rattan S, Zhou C, Chiang C, Mahalingam S, Brehm E, Flaws JA (2017) Exposure to endocrine disruptors during adulthood: Consequences for female fertility. J Endocrinol 233(3):R109–R129
Rekhadevi PV, Rahman MF, Mahboob M, Kumari SI, Chinde S, Bhanuramya M, Naresh D, Grover P (2017) Assessment of genotoxicity in female agricultural workers exposed to pesticides. Biomarkers 22(5):446–454
Rim KT (2017) Reproductive toxic chemicals at work and efforts to protect workers' health: a literature review. Saf Health Work 8(2):143–150
Rishi KK, Grewal S (1995) Chromosome aberration test for the insecticide, dichlorvos, on fish chromosomes. Mutat Res 344(1-2):1–4
Rusiecki JK, Baccarelli A, Bollati V, Tarantini L, Moore LE, Bonefeld-Jorgenson EC (2008) Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic unit. Environ Health Perspect 116:1547–1552
Sanderson JT, Seinen W, Giesy JP, van den Berg M (2000) 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity inH295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol Sci 54:121–127
Schmidt CW (2017) Age at menopause: Do chemical exposures play a role? Environ Health Perspect 125(6):062001
Sebastian R, Raghavan SC (2015) Exposure to endosulfan can result in male infertility due to testicular atrophy and reduced sperm count. Cell Death Discov 1:15020
Semu E, Tindwa H, Singh BR (2019) Heavy metals and organopesticides: Ecotoxicology, health effects and mitigation options with emphasis on sub-Saharan Africa. J Toxicol Cur Res 3:010
Sengupta P, Banerjee R (2014) Environmental toxins: Alarming impacts of pesticides on male fertility. Hum Exp Toxicol 33(10):1017–1039
Sharma T, Banerjee BD, Mazumdar D, Tyagi V, Thakur G, Guleria K, Ahmed RS, Tripathi AK (2015) Association of organochlorine pesticides and risk of epithelial ovarian cancer: a case control study. J Reprod Health Med 1:76–82
Silvestroni L, Palleschi S (1999) Effects of organochlorine xenobiotics on human spermatozoa. Chemosphere 39:1249–1252
Snedeker SM (2001) Pesticides and breast cancer risk: a review of DDT, DDE, and dieldrin. Environ Health Perspect 109(Suppl 1):35–47
Su Y, Dai Y, Lin Y, Gao X, Han Y, Zhao B (2012) Serum organochlorine pesticide residues and risk of gallstone disease: a case-control study in Xiamen. Annals Epidemiology 22(8):592–597
Sutton P, Wallinga D, Perron J, Gottlieb M, Sayre L, Woodruff T (2011) Reproductive health and the industrialized food system: a point of intervention for health policy. Health Aff (Millwood) 30:888–897
Tebourbi O, Sakly M, Rhouma KB (2011) Molecular mechanisms of pesticide toxicity K.B. Rhouma (Ed.), Pesticides in the Modern World – Pests Control and Pesticides Exposure and Toxicity Assessment, Intech, pp. 297-332
Teodoro M, Briguglio G, Fenga C, Costa C (2019) Genetic polymorphisms as determinants of pesticide toxicity: Recent advances. Toxicol Rep 6:564–570
Toft G, Axmon A, Giwercman A, Thulstrup AM, Rignell-Hydbom A, Pedersen HS, Ludwicki JK, Zvyezday V, Zinchuk A, Spano M, Manicardi GC, Bonefeld-Jørgensen EC, Hagmar L, Bonde JP, INUENDO (2005) Fertility in four regions spanning large contrasts in serum levels of widespread, persistent organochlorines: a cross-sectional study. Environ Health 4:26
Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268
Toporova L, Balaguer P (2020) Nuclear receptors are the major targets of endocrine-disrupting chemicals. Mol Cell Endocrinol 502:110665
Tully DB, Cox VT, Mumtaz MM, Davis VL, Chapin RE (2000) Six high-priority organochlorine pesticides, either singly or in combination, are nonestrogenic in transfected HeLa cells. Reprod Toxicol 14:95–102
Turusov V, Rakitsky V, Tomatis L (2002) Dichlorodiphenyltrichloroethane (DDT): ubiquity, persistence, and risks. Environ Health Perspect 110(2):125–128
Vinggaard AM, Hnida C, Breinholt V, Larsen JC (2000) Screening of selected pesticides for inhibition of CYP19 aromatase activity in vitro. Toxicol Vitro 14:227–234
Vonier PM, Crain DA, McLachlan JA, Guillette LJ Jr, Arnold SF (1996) Interaction of environmental chemicals with the estrogen and progesterone receptors from the oviduct of the American alligator. Environ Health Perspect 104:1318–1322
Waliszewski SM, Carvajal O, Infanzon RM, Trujillo P, Aguirre AA, Maxwell M (2004) Levels of organochlorine pesticides in soils and rye plant tissues in a field study. J Agric Food Chem 52:7045–7050
Welch RM, Levin W, Kuntzman R, Jacobson M, Conney AH (1971) Effect of halogenated hydrocarbon insecticides on the metabolism and uterotropic action of estrogens in rats and mice. Toxicol Appl Pharmacol 19:234–246
Wójtowicz AK, Kajta M, Gregoraszczuk EŁ (2007) DDT- and DDE-induced disruption of ovarian steroidogenesis in prepubertal porcine ovarian follicles: a possible interaction with the main steroidogenic enzymes and estrogen receptor beta. J Physiol Pharmacol 58(4):873–885
Ye M, Beach J, Martin JW, Senthilselvan A (2017) Pesticide exposures and respiratory health in general populations. J Environ Sci 51:361–370
Zhang J, Zhang J, Liu R, Gan J, Liu J, Liu W (2016) Endocrine-disrupting effects of pesticides through interference with human glucocorticoid receptor. Environ Sci Technol 50(1):435–443
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B.V, U.S, G.R,. I.M.C, and M.T conceived the review idea and focus, drafted the article, and critically revised the article. R.S and M.A.S were involved in the reference collection, drawing figures, and writing the article. All authors have read and agreed to the published version of the manuscript.
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Venkidasamy, B., Subramanian, U., Samynathan, R. et al. Organopesticides and fertility: where does the link lead to?. Environ Sci Pollut Res 28, 6289–6301 (2021). https://doi.org/10.1007/s11356-020-12155-3
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DOI: https://doi.org/10.1007/s11356-020-12155-3