Endosulfan is a broad-spectrum organochlorine pesticide widely used in many developing countries despite its high toxicity potential. Endosulfan, listed as potent endocrine-disrupting chemical and xenoestrogen, gains importance for its potential to cause reproductive and developmental dysfunction. In females, endosulfan disrupts ovarian and uterine development, leading to infertility, miscarriage, and developmental toxicity. It acts by mimicking estrogen and interferes with estrogen and androgen pathways, impacting hormone regulation and gene expression, including estrogen receptor α (ERα) and progesterone receptors. Endosulfan triggers oxidative stress in ovaries, reduces follicle count, and impairs uterine differentiation, affecting embryo implantation. Additionally, it alters gene expression and causes epigenetic modifications, contributing to reproductive dysfunctions. In males, endosulfan affects spermatogenesis by causing oxidative stress, mitochondrial dysfunction, and lipid peroxidation. It reduces sperm quality, motility, and quantity, with effects on testicular tissues, sperm chromatin condensation, and enzymatic activity. Oxidative damage, increased reactive oxygen species (ROS), and disrupted energy metabolism are central to its toxicity. Epidemiological studies also link pesticide exposure to reduced sperm counts, higher DNA fragmentation, and infertility. Moreover, endosulfan can cross the placental barrier, leading to fetal resorption, malformations, and maternal toxicity. This review provides a comprehensive overview of the reproductive toxicity of endosulfan in males and females. We also highlight the various possible mechanisms of reproductive toxicity of endosulfan and its potential to impart deleterious effects over HPG axis, gonads, and uterine differentiation and development and implantation.
AbalisIMEldefrawiMEEldefrawiAT (1986) Effects of insecticides on GABA‐induced chloride influx into rat brain microsacs. Journal of Toxicology and Environmental Health, Part A Current Issues18(1): 13–23.
2.
AguilarHNMitchellBF (2010) Physiological pathways and molecular mechanisms regulating uterine contractility. Human Reproduction Update16(6): 725–744.
3.
AhmedTTripathiAKAhmedRS, et al. (2008) Endosulfan‐induced apoptosis and glutathione depletion in human peripheral blood mononuclear cells: attenuation by N‐acetylcysteine. Journal of Biochemical and Molecular Toxicology22(5): 299–304.
4.
AitkenRJRomanSD (2008) Antioxidant systems and oxidative stress in the testes. Oxid Med Cell Longev1(1): 15–24.
5.
AlarcónRVarayoudJLuqueEH, et al. (2019) Effect of neonatal exposure to endosulfan on myometrial adaptation during early pregnancy and labor in rats. Molecular and Cellular Endocrinology491: 110435.
6.
AmannRP (1986) Detection of alterations in testicular and epididymal function in laboratory animals. Environmental Health Perspectives70: 149–158.
7.
AntoniousGFByersMESnyderJC (1998) Residues and fate of endosulfan on field‐grown pepper and tomato. Pesticide Science54(1): 61–67.
8.
ATSDR (2000) Toxicological Profile for Endosulfan. Agency for Toxic Substances and Disease Registry.
9.
AugerJMesbahMHuberC, et al. (1990) Aniline blue staining as a marker of sperm chromatin defects associated with different semen characteristics discriminates between proven fertile and suspected infertile men. International Journal of Andrology13(6): 452–462.
10.
AzarniaMKoochesfahaniHMRajabiM, et al. (2008) Histological examination of endosulfan effects on follicular development of BALB/C mice. Bulgarian Journal of Veterinary Medicine12: 33–41.
11.
BagotCNTroyPJTaylorHS (2000) Alteration of maternal Hoxa10 expression by in vivo gene transfection affects implantation. Gene Therapy7(16): 1378–1384.
12.
BensonGVLimHPariaBC, et al. (1996) Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development122(9): 2687–2696.
13.
BlanksAMShmygolAThorntonS (2007) Regulation of oxytocin receptors and oxytocin receptor signaling. Seminars in Reproductive Medicine25(01): 052–059.
14.
BretveldRWThomasCMGScheepersPTJ, et al. (2006) Pesticide exposure: the hormonal function of the female reproductive system disrupted. Reproductive Biology and Endocrinology4: 1–14.
15.
BuettnerRG (2011) Superoxide dismutase in redox biology: the roles of superoxide and hydrogen peroxide. Anti-Cancer Agents in Medicinal Chemistry11(4): 341–346.
16.
CarlsenEGiwercmanAKeidingN, et al. (1992) Evidence for decreasing quality of semen during past 50 years. British Medical Journal305(6854): 609–613.
17.
CartaLSassoonD (2004) Wnt7a is a suppressor of cell death in the female reproductive tract and is required for postnatal and estrogen-mediated growth. Biology of Reproduction71(2): 444–454.
18.
CermikDSelamBTaylorHS (2003) Regulation of HOXA-10 expression by testosterone in vitro and in the endometrium of patients with polycystic ovary syndrome. Journal of Clinical Endocrinology and Metabolism88(1): 238–243.
19.
ChaJSunXDeySK (2012) Mechanisms of implantation: strategies for successful pregnancy. Nature Medicine18(12): 1754–1767.
20.
ChakrabartySRajakumarARaghuveerK, et al. (2012) Endosulfan and flutamide, alone and in combination, target ovarian growth in juvenile catfish, Clarias batrachus. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology155(3): 491–497.
21.
ChanMPMorisawaSNakayamaA, et al. (2005) Toxicokinetics of 14C‐endosulfan in male sprague–dawley rats following oral administration of single or repeated doses. Environmental Toxicology20(5): 533–541.
22.
ChenBFChanWY (2014) The de novo DNA methyltransferase DNMT3A in development and cancer. Epigenetics9(5): 669–677.
23.
ChitraKCLatchoumycandaneCMathurPP (1999) Chronic effect of endosulfan on the testicular functions of rat. DNA1(11.131): 35–206.
24.
ColeLMCasidaJE (1986) Polychlorocycloalkane insecticide-induced convulsions in mice in relation to disruption of the GABA-regulated chloride ionophore. Life Sciences39(20): 1855–1862.
25.
CollottaMBertazziPABollatiV (2013) Epigenetics and pesticides. Toxicology307: 35–41.
DaftaryGSTaylorHS (2006) Endocrine regulation of HOX genes. Endocrine Reviews27(4): 331–355.
28.
DalsenterPRDallegraveEMelloJR, et al. (1999) Reproductive effects of endosulfan on male offspring of rats exposed during pregnancy and lactation. Human & Experimental Toxicology18(9): 583–589.
29.
DalsenterPRdeAraújoSLda Silva de AssisHC, et al. (2003) Pre and postnatal exposure to endosulfan in Wistar rats. Human & Experimental Toxicology22(4): 171–175.
30.
DöringBShynlovaOTsuiP, et al. (2006) Ablation of connexin43 in uterine smooth muscle cells of the mouse causes delayed parturition. Journal of Cell Science119(9): 1715–1722.
31.
DuHTaylorHS (2016) The role of hox genes in female reproductive tract development, adult function, and fertility. Cold Spring Harbor Perspectives in Medicine6(1): a023002.
32.
DuanCGoldbergE (2003) Inhibition of lactate dehydrogenase C4 (LDH-C4) blocks capacitation of mouse sperm in vitro. Cytogenetic and Genome Research103(3-4): 352–359.
33.
DunlapKAFilantJHayashiK, et al. (2011) Postnatal deletion of Wnt7a inhibits uterine gland morphogenesis and compromises adult fertility in mice. Biology of Reproduction85(2): 386–396.
34.
DuttaHMArendsDA (2003) Effects of endosulfan on brain acetylcholinesterase activity in juvenile bluegill sunfish. Environmental Research91(3): 157–162.
35.
El-MounayriOTriplettJWYatesCW, et al. (2005) Triplett JW, yates CW, and herring BP. Regulation of smooth muscle-specific gene expression by homeodomain proteins, Hoxa10 and Hoxb8. Journal of Biological Chemistry280: 25854–25863.
36.
ElmesMSzyszkaAPauliatC, et al. (2015) Maternal age effects on myometrial expression of contractile proteins, uterine gene expression, and contractile activity during labor in the rat. Physiological Reports3(4): e12305.
37.
EmbrandiriASinghRPIbrahimHM, et al. (2012) An epidemiological study on the health effects of endosulfan spraying on cashew plantations in Kasaragod district, Kerala, India. Asian Journal of Epidemiology5(1): 22–31.
38.
Environmental Protection Agency (EPA) (1980) Ambient Water Quality Criteria for Endosulfan. Environmental Research Laboratory. Rept. No. 4405-80-046, p. 108.
39.
EvensonDPBaerRKJostLK, et al. (1986) Toxicity of thiotepa on mouse spermatogenesis as determined by dual-parameter flow cytometry. Toxicology and Applied Pharmacology82(1): 151–163.
40.
FavaroRRSalgadoRMRaspantiniPR, et al. (2010) Effects of long‐term diabetes on the structure and cell proliferation of the myometrium in the early pregnancy of mice. International Journal of Experimental Pathology91(5): 426–435.
41.
FischerCPKayisiliUTaylorHS (2011) HOXA10 expression is decreased in endometrium of women with adenomyosis. Fertility and Sterility95(3): 1133–1136.
42.
FranczakAWojciechowiczBKolakowskaJ, et al. (2014) Transcriptomic analysis of the myometrium during peri-implantation period and luteolysis–the study on the pig model. Functional & Integrative Genomics14(4): 673–682.
43.
FrazierLM (2007) Reproductive disorders associated with pesticide exposure. Journal of Agromedicine12(1): 27–37.
44.
FreireCKoifmanRJSarcinelliPN, et al. (2014) Association between serum levels of organochlorine pesticides and sex hormones in adults living in a heavily contaminated area in Brazil. International Journal of Hygiene and Environmental Health217(2-3): 370–378.
GhoshKChatterjeeBJayaprasadAG, et al. (2018) The persistent organochlorine pesticide endosulfan modulates multiple epigenetic regulators with oncogenic potential in MCF-7 cells. Science of the Total Environment624: 1612–1622.
47.
GhumanSPSRatnakaranUBediJS, et al. (2013) Impact of pesticide residues on fertility of dairy animals: a review. Indian Journal of Animal Sciences83(12): 1243–1255.
48.
GiulioniCMauriziVCastellaniD, et al. (2022) The environmental and occupational influence of pesticides on male fertility: a systematic review of human studies. Andrology10(7): 1250–1271.
49.
GoldmanJMStokerTECooperRL, et al. (1994) Blockade of ovulation in the rat by the fungicide sodium N-methyldithiocarbamate: relationship between effects on the luteinizing hormone surge and alterations in hypothalamic catecholamines. Neurotoxicology and Teratology16(3): 257–268.
50.
GoldmanJMParrishMBCooperRL, et al. (1997) Blockade of ovulation in the rat by systemic and ovarian intrabursal administration of the fungicide sodium dimethyldithiocarbamate. Reproductive Toxicology11(2-3): 185–190.
51.
GuoYJLiSGWangTX (1998) Enzymic cytochemical studies of LDH-C4 in infertile spermatozoa. Chinese Journal of Histochemistry and Cytochemistry3: 443–449.
52.
GuptaPKChandraSVSaxenaDK (1978) Teratogenic and embryotoxic effects of endosulfan in rats. Acta Pharmacologica et Toxicologica42(2): 150–152.
53.
HaffnerDSchecterA (2014) Persistent organic pollutants (POPs): a primer for practicing clinicians. Current Environmental Health Reports1(2): 123–131.
54.
HanukogluI (2006) Antioxidant protective mechanisms against reactive oxygen species (ROS) generated by mitochondrial P450 systems in steroidogenic cells. Drug Metabolism Reviews38(1-2): 171–196.
55.
HerrmannM (2002) Preliminary Risk Profile of Endosulfan. Umweltbundesamt.
56.
HiremathMBKaliwalBB (2002) Anti-implantation action of endosulfan in albino mice: possible mechanisms. Journal of Basic and Clinical Physiology and Pharmacology13(4): 329–342.
57.
HuangHFSNieschlagE (1984) Alteration of free sulphydryl content of rat sperm heads by suppression of intratesticular testosterone. Reproduction70(1): 31–38.
58.
IngaramoPIMilesiMMSchimpfMG, et al. (2016) Endosulfan affects uterine development and functional differentiation by disrupting Wnt7a and β-catenin expression in rats. Molecular and Cellular Endocrinology425: 37–47.
59.
JadaramkuntiUCKaliwalBB (1999) Effect of dicofol formulation on estrous cycle and follicular dynamics in albino rats. Journal of Basic and Clinical Physiology and Pharmacology10(4): 305–314.
60.
JadhavTJShaikhJD (2011) Histopathological changes in the ovary of freshwater crab (Barytelphusa cunicularis) exposed to endosulfan. DAV. International Journal of Science1: 139–140.
61.
JafferSShynlovaOLyeS (2009) Mammalian target of rapamycin is activated in association with myometrial proliferation during pregnancy. Endocrinology150(10): 4672–4680.
62.
JaiswalAPariharVKKumarMS, et al. (2005) 5-Aminosalicylic acid reverses endosulfan-induced testicular toxicity in male rats. Mutation Research, Genetic Toxicology and Environmental Mutagenesis585(1-2): 50–59.
63.
JayachandraS (2016) Impact of endosulfan on male reproductive functions-a review. Perspective in Medical Research4: 44–49.
64.
JeongJWLeeHSFrancoHL, et al. (2009) β-Catenin mediates glandular formation and dysregulation of β-catenin induces hyperplasia formation in the murine uterus. Oncogene28(1): 31–40.
65.
JiaHLiuLSunY, et al. (2010) Monitoring and modeling endosulfan in Chinese surface soil. Environmental Science and Technology44(24): 9279–9284.
66.
KalenderSKalenderYOgutcuA, et al. (2004) Endosulfan-induced cardiotoxicity and free radical metabolism in rats: the protective effect of vitamin E. Toxicology202(3): 227–235.
67.
KapdnisRRYadavBS (2011) Impact of organ pesticides for fresh water crab B. cunicularis. Biology and Medicine3(2): 282–283.
68.
KaraMÖztaşE (2020). Reproductive toxicity of insecticides. In: Faruk Aral, Rita Payan-Carreira and Miguel Quaresma (eds.), Animal Reproduction in Veterinary Medicine, IntechOpen, pp. 1–8.
69.
KhanPKSinhaSP (1994a) Vitamin C mediated amelioration of pesticide genotoxicity in murine spermatocytes. Cytobios80(323): 199–204.
70.
KocNDKayhanFESesalC, et al. (2009) Dose-dependent effects of endosulfan and malathion on adult wistar albino rat ovaries. Pakistan Journal of Biological Sciences12(6): 498–503.
71.
LawrenceLJCasidaJE (1984) Interactions of lindane, toxaphene and cyclodienes with brain-specific t-butylbicyclophosphorothionate receptor. Life Sciences35(2): 171–178.
72.
LeeJMMayallJRChevalierA, et al. (2018) Chlamydia muridarum infection differentially changes smooth muscle contractility and responses to prostaglandins in uterus and cervix. bioRxiv448340.
73.
LemaireGMnifWMauvaisP, et al. (2006) Activation of α-and β-estrogen receptors by persistent pesticides in reporter cell lines. Life Sciences79(12): 1160–1169.
74.
LimHMaLMaWG, et al. (1999) Hoxa-10 regulates uterine stromal cell responsiveness to progesterone during implantation and decidualization in the mouse. Molecular Endocrinology13(6): 1005–1017.
75.
LuFC (1995) A review of the acceptable daily intakes of pesticides assessed by WHO. Regulatory Toxicology and Pharmacology21(3): 352–364.
76.
MakkerAGoelMMNigamD, et al. (2017) Endometrial expression of homeobox genes and cell adhesion molecules in infertile women with intramural fibroids during window of implantation. Reproductive Sciences24(3): 435–444.
77.
MartinezEMSwartzWJ (1991) Effects of methoxychlor on the reproductive system of the adult female mouse 1. Gross and histologic observations. Reproductive Toxicology5(2): 139–147.
78.
MenezesRGQadirTFMoinA, et al. (2017) Endosulfan poisoning: an overview. Journal of Forensic and Legal Medicine51: 27–33.
79.
MesianoSWelshTN (2007) Steroid hormone control of myometrial contractility and parturition. Seminars in Cell & Developmental Biology18(3): 321–331.
80.
MilesiMMVarayoudJBosquiazzoVL, et al. (2012) Neonatal exposure to low doses of endosulfan disrupts the expression of proteins regulating uterine development and differentiation. Reproductive Toxicology33(1): 85–93.
81.
MilesiMMAlarcónRRamosJG, et al. (2015) Neonatal exposure to low doses of endosulfan induces implantation failure and disrupts uterine functional differentiation at the pre-implantation period in rats. Molecular and Cellular Endocrinology401: 248–259.
82.
MilesiMMVarayoudJRamosJG, et al. (2017) Uterine ERα epigenetic modifications are induced by the endocrine disruptor endosulfan in female rats with impaired fertility. Molecular and Cellular Endocrinology454: 1–11.
83.
MilesiMMDurandoMLorenzV, et al. (2020) Postnatal exposure to endosulfan affects uterine development and fertility. Molecular and Cellular Endocrinology511: 110855.
84.
MilesiMMLorenzVVarayoudJ (2022) Aberrant Hoxa10 gene methylation as a mechanism for endosulfan-induced implantation failures in rats. Molecular and Cellular Endocrinology547: 111576.
85.
MillerCSassoonDA (1998) Wnt-7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract. Development125(16): 3201–3211.
86.
MnifWHassineAIHBouazizA, et al. (2011) Effect of endocrine disruptor pesticides: a review. International Journal of Environmental Research and Public Health8(6): 2265–2303.
87.
MohamedOAJonnaertMLabelle-DumaisC, et al. (2005) Uterine Wnt/β-catenin signaling is required for implantation. Proceedings of the National Academy of Sciences102(24): 8579–8584.
88.
Mota-RojasDMartínez-BurnesJTrujilloME, et al. (2005a) Uterine and fetal asphyxia monitoring in parturient sows treated with oxytocin. Animal Reproduction Science86(1-2): 131–141.
89.
Mota-RojasDNava-OcampoAATrujilloME, et al. (2005b) Dose minimization study of oxytocin in early labor in sows: uterine activity and fetal outcome. Reproductive Toxicology20(2): 255–259.
90.
MuirDCTeixeiraCWaniaF (2004) Empirical and modeling evidence of regional atmospheric transport of current‐use pesticides. Environmental Toxicology and Chemistry23(10): 2421–2432.
91.
NaqviSMVaishnaviC (1993) Bioaccumulative potential and toxicity of endosulfan insecticide to non-target animals. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology105(3): 347–361.
92.
NarayanaKD’SouzaUJRaoKS (2002) Ribavirin-induced sperm shape abnormalities in wistar rat. Mutation Research, Genetic Toxicology and Environmental Mutagenesis513(1-2): 193–196.
93.
NarayanaKNarayanPD’SouzaUJA (2004) Is our drinking water a slow poison?Indian Journal of Medical Sciences58: 528–530.
94.
NayeemSBDharmarajanAKeelanJA (2015) Paracrine communication modulates production of Wnt antagonists and COX1-mediated prostaglandins in a decidual-trophoblast co-culture model. Molecular and Cellular Endocrinology405: 52–62.
95.
NobleKZhangJWrayS (2006) Lipid rafts, the sarcoplasmic reticulum and uterine calcium signalling: an integrated approach. The Journal of Physiology570(1): 29–35.
96.
OmurtagGZTozanAŞehirliAÖ, et al. (2008) Melatonin protects against endosulfan‐induced oxidative tissue damage in rats. Journal of Pineal Research44(4): 432–438.
97.
ÖzcanCÖzdamarÖGökbayrakME, et al. (2019) HOXA-10 gene expression in ectopic and eutopic endometrium tissues: does it differ between fertile and infertile women with endometriosis?European Journal of Obstetrics & Gynecology and Reproductive Biology233: 43–48.
98.
OzoeYMatsumuraF (1986) Structural requirements for bridged bicyclic compounds acting on picrotoxinin receptor. Journal of Agricultural and Food Chemistry34(1): 126–134.
99.
PalRAhmedTKumarV, et al. (2009) Protective effects of different antioxidants against endosulfan-induced oxidative stress and immunotoxicity in albino rats. Indian Journal of Experimental Biology47(9): 723–729.
100.
PathakRSukeSGAhmedT, et al. (2010) Organochlorine pesticide residue levels and oxidative stress in preterm delivery cases. Human & Experimental Toxicology29(5): 351–358.
101.
PerobelliJEMartinezMFda Silva FranchiCA, et al. (2010) Decreased sperm motility in rats orally exposed to single or mixed pesticides. Journal of Toxicology and Environmental Health, Part A73(13-14): 991–1002.
102.
PlowchalkDRSmithBJMattisonDR (1993) Assessment of toxicity to the ovary using follicle quantitation and morphometrics. Methods in Toxicology3(Part B): 37–38.
103.
PriyaKumarAAliM, et al. (2024) Endosulfan induces reproductive & genotoxic effect in male and female Swiss albino mice. Laboratory Animal Research40(1): 22.
104.
RaoMNarayanaKBenjaminS, et al. (2005) L-ascorbic acid ameliorates postnatal endosulfan induced testicular damage in rats. Indian Journal of Physiology & Pharmacology49(3): 331–336.
105.
RenNQZhangXDZhouGH, et al. (2008) Induced apoptosis and mechanism of endosulfan in mouse germ cells. Huan Jing ke Xue = Huanjing Kexue29(2): 386–390.
106.
RivasAFisherJSMcKinnellC, et al. (2002) Induction of reproductive tract developmental abnormalities in the male rat by lowering androgen production or action in combination with a low dose of diethylstilbestrol: evidence for importance of the androgen-estrogen balance. Endocrinology143(12): 4797–4808.
107.
RobertsDMKarunarathnaABuckleyNA, et al. (2003) Influence of pesticide regulation on acute poisoning deaths in Sri Lanka. Bulletin of the World Health Organization81(11): 789–798.
108.
RockwellLCPillaiSOlsonCE, et al. (2002) Inhibition of vascular endothelial growth factor/vascular permeability factor action blocks estrogen-induced uterine edema and implantation in rodents. Biology of Reproduction67(6): 1804–1810.
109.
SaidTMAgarwalASharmaRK, et al. (2005) Impact of sperm morphology on DNA damage caused by oxidative stress induced by β-nicotinamide adenine dinucleotide phosphate. Fertility and Sterility83(1): 95–103.
110.
SaiyedHDewanABhatnagarV, et al. (2003) Effect of endosulfan on male reproductive development. Environmental Health Perspectives111(16): 1958–1962.
111.
SalomonisNCotteNZambonAC, et al. (2005) Identifying genetic networks underlying myometrial transition to labor. Genome Biology6(2): 1–16.
112.
SamantaLRoyAChainyGBN (1999) Changes in rat testicular antioxidant defence profile as a function of age and its impairment by hexachlorocyclohexane during critical stages of maturation. Andrologia31(2): 83–90.
113.
SanbornBMKuCYShlykovS, et al. (2005) Molecular signaling through G-protein-coupled receptors and the control of intracellular calcium in myometrium. Journal of the Society for Gynecologic Investigation: JSGI12(7): 479–487.
114.
Sancewicz-PachKGroszekBPachD, et al. (1997) Acute pesticides poisonings in pregnant women. Przeglad Lekarski54(10): 741–744.
SaxenaRGargPJainDK (2011) In vitro anti-oxidant effect of vitamin E on oxidative stress induced due to pesticides in rat erythrocytes. Toxicology international18(1): 73.
117.
SaxenaSPKhareCFarooqA, et al. (1987) DDT and its metabolites in leiomyomatous and normal human uterine tissue. Archives of Toxicology59(6): 453–455.
118.
SebastianRRaghavanSC (2015) Exposure to endosulfan can result in male infertility due to testicular atrophy and reduced sperm count. Cell Death Discovery1(1): 1–10.
119.
SethunathanNMegharajMChenZ, et al. (2002) Persistence of endosulfan and endosulfan sulfate in soil as affected by moisture regime and organic matter addition. Bulletin of Environmental Contamination and Toxicology5(68): 725–731.
120.
SharmaAKaninathanADahalS, et al. (2022) Exposure to endosulfan can cause long term effects on general biology, including the reproductive system of mice. Frontiers in Genetics13: 1047746.
121.
ShawberCJLinLGnarraM, et al. (2015) Vascular notch proteins and notch signaling in the peri-implantation mouse uterus. Vascular Cell7(1): 1–17.
122.
ShenLWaniaFLeiYD, et al. (2005) Atmospheric distribution and long-range transport behavior of organochlorine pesticides in North America. Environmental Science and Technology39(2): 409–420.
123.
ShiotaK (2004) DNA methylation profiles of CpG islands for cellular differentiation and development in mammals. Cytogenetic and Genome Research105(2-4): 325–334.
124.
ShynlovaOOldenhofADoroginA, et al. (2006) Myometrial apoptosis: activation of the caspase Cascade in the pregnant rat myometrium at midgestation. Biology of Reproduction74(5): 839–849.
125.
ShynlovaOTsuiPDoroginA, et al. (2007) Insulin-like growth factors and their binding proteins define specific phases of myometrial differentiation during pregnancy in the rat. Biology of Reproduction76(4): 571–578.
126.
ShynlovaOTsuiPJafferS, et al. (2009) Integration of endocrine and mechanical signals in the regulation of myometrial functions during pregnancy and labor. European Journal of Obstetrics & Gynecology and Reproductive Biology144: S2–S10.
127.
SilvaMHGammonD (2009) An assessment of the developmental, reproductive, and neurotoxicity of endosulfan. Birth Defects Research Part B: Developmental and Reproductive Toxicology86(1): 1–28.
128.
SimonichSLHitesRA (1995) Global distribution of persistent organochlorine compounds. Science269(5232): 1851–1854.
129.
SinghSKPandeyRS (1990) Effect of sub-chronic endosulfan exposures on plasma gonadotrophins, testosterone, testicular testosterone and enzymes of androgen biosynthesis in rat. Indian Journal of Experimental Biology28(10): 953–956.
130.
SinghNDSharmaAKDwivediP, et al. (2007a) Citrinin and endosulfan induced teratogenic effects in wistar rats. Journal of Applied Toxicology: International Journal27(2): 143–151.
131.
SinghNDSharmaAKDwivediP, et al. (2007b) Citrinin and endosulfan induced maternal toxicity in pregnant wistar rats: pathomorphological study. Journal of Applied Toxicology: International Journal27(6): 589–601.
132.
SinhaNNarayanRShankerR, et al. (1995) Endosulfan-induced biochemical changes in the testis of rats. Veterinary & Human Toxicology37(6): 547–549.
133.
SinhaNNarayanRSaxenaDK (1997) Effect of endosulfan on the testis of growing rats. Bulletin of Environmental Contamination and Toxicology58(1): 79–86.
134.
SinhaNAdhikariNSaxenaDK (2001) Effect of endosulfan during fetal gonadal differentiation on spermatogenesis in rats. Environmental Toxicology and Pharmacology10(1-2): 29–32.
135.
SinhaASahayRKumarR, et al. (2016) Antidote effect of selenium against endosulfan induced toxicity in ovarian cells of mice. Austin Cell Biol2(1): 1005.
136.
SmithAG (1991) Chlorinated hydrocarbon insecticides. Handbook of Pesticide Toxicology2: 731–915.
137.
SotoAMChungKLSonnenscheinC (1994) The pesticides endosulfan, toxaphene, and dieldrin have estrogenic effects on human estrogen-sensitive cells. Environmental Health Perspectives102(4): 380–383.
138.
SpencerTE (2014) Biological roles of uterine glands in pregnancy. Seminars in Reproductive Medicine32(5): 346–357.
139.
SpencerTEDunlapKAFilantJ (2012) Comparative developmental biology of the uterus: insights into mechanisms and developmental disruption. Molecular and Cellular Endocrinology354(1-2): 34–53.
140.
SrinivasaJMaximPUrbanJ, et al. (2005) Effects of pesticides on male reproductive functions. Iranian Journal of Medical Sciences30(4): 153–159.
141.
SunYBWangJLSongYC, et al. (2005) Lipid peroxidation damnification on spleens of mice exposed to nicked sulfate. Chinese Journal of Public Health21(2): 187–188.
SweeneyTNicolLRocheJF, et al. (2000) Maternal exposure to octylphenol suppresses ovine fetal follicle-stimulating hormone secretion, testis size, and sertoli cell number. Endocrinology141(7): 2667–2673.
144.
TakhshidMATavasuliARHeidaryY, et al. (2012) Protective effect of vitamins E and C on endosulfan-induced reproductive toxicity in male rats. Iranian Journal of Medical Sciences37(3): 173–180.
145.
TomimatsuTMimuraKEndoM, et al. (2017) Pathophysiology of preeclampsia: an angiogenic imbalance and long-lasting systemic vascular dysfunction. Hypertension Research40(4): 305–310.
146.
VarayoudJRamosJGBosquiazzoVL, et al. (2008) Developmental exposure to bisphenol A impairs the uterine response to ovarian steroids in the adult. Endocrinology149: 5848–5860.
147.
VarayoudJRamosJGBosquiazzoVL, et al. (2011) Neonatal exposure to bisphenol A alters rat uterine implantation-associated gene expression and reduces the number of implantation sites. Endocrinology152(3): 1101–1111.
148.
VarayoudJRamosJGMuñoz-de-ToroM, et al. (2014) Long-lasting effects of neonatal bisphenol A exposure on the implantation process. Vitamins & Hormones94: 253–275.
149.
Velasco-SantamaríaYMHandyRDSlomanKA (2011) Endosulfan affects health variables in adult zebrafish (Danio rerio) and induces alterations in larvae development. Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology153(4): 372–380.
150.
WangNQianHYZhouXQ, et al. (2012) Mitochondrial energy metabolism dysfunction involved in reproductive toxicity of mice caused by endosulfan and protective effects of vitamin E. Ecotoxicology and Environmental Safety82: 96–103.
151.
WangNXuYZhouXQ, et al. (2016) Protective effects of testosterone propionate on reproductive toxicity caused by endosulfan in male mice. Environmental Toxicology31(2): 142–153.
152.
WeberJHalsallCJMuirD, et al. (2010) Endosulfan, a global pesticide: a review of its fate in the environment and occurrence in the arctic. Science of the Total Environment408(15): 2966–2984.
153.
WestonDPYouJLydyMJ (2004) Distribution and toxicity of sediment-associated pesticides in agriculture-dominated water bodies of California’s central valley. Environmental Science & Technology38(10): 2752–2759.
154.
WHO (2002) The WHO Recommended Classification of Pesticides by Hazard and Guidelines to Classification 2000–2002. World Health Organization, International Programme on Chemical Safety/Inter-Organisation Programme for Sound Management of Chemicals.
155.
WilsonVSLeBlancGA (1998) Endosulfan elevates testosterone biotransformation and clearance in CD-1 mice. Toxicology and Applied Pharmacology148(1): 58–168.
156.
WyrobekAJGordonLABurkhartJG, et al. (1983) An evaluation of the mouse sperm morphology test and other sperm tests in nonhuman mammals: a report of the US environmental protection agency gene-tox program. Mutation Research: Reviews in Genetic Toxicology115(1): 1–72.
157.
XuJQiuYDeMayoFJ, et al. (1998) Partial hormone resistance in mice with disruption of the steroid receptor coactivator-1 (SRC-1) gene. Science279(5358): 1922–1925.
158.
XuYWangNShiZX, et al. (2016) In vitro mechanistic study of endosulfan-induced spermatogenic cell apoptosis in the mouse. Toxicology and Industrial Health32(9): 1550–1563.
159.
YanJZhuWWangD, et al. (2019) Different effects of α-endosulfan, β-endosulfan, and endosulfan sulfate on sex hormone levels, metabolic profile and oxidative stress in adult mice testes. Environmental Research169: 315–325.
160.
YangYChenXSaravelosSH, et al. (2017) HOXA-10 and E-cadherin expression in the endometrium of women with recurrent implantation failure and recurrent miscarriage. Fertility and Sterility107(1): 136–143.
161.
ZamaAMUzumcuM (2010) Epigenetic effects of endocrine-disrupting chemicals on female reproduction: an ovarian perspective. Frontiers in Neuroendocrinology31(4): 420–439.
162.
ZenclussenAMeyerNSchumacherA, et al. (2017) Simultaneous ablation of natural killer cells and mast cells leads to poor uterine vascularization that compromises fetal-well being. The Journal of Immunology198(1): 149.14.
163.
ZervosIANikolaidisELavrentiadouSN, et al. (2011) Endosulfan-induced lipid peroxidation in rat brain and its effect on t-PA and PAI-1: ameliorating effect of vitamins C and E. Journal of Toxicological Sciences36(4): 423–433.
164.
ZhangGJ (2003) The effect of environmental anti-androgen and its mechanism. Foreign Medical Sciences30: 79–83.
165.
ZhangSLinHKongS, et al. (2013) Physiological and molecular determinants of embryo implantation. Molecular Aspects of Medicine34(5): 939–980.
166.
ZhangJZhangJLiuR, et al. (2016) Endocrine-disrupting effects of pesticides through interference with human glucocorticoid receptor. Environmental Science & Technology50(1): 435–443.
167.
ZhuXQZhengYFZhangQW, et al. (2002) Effects of endosulfan on the spermatogenesis and oxidative damage in rats. Chinese Journal of Pharmacology and Toxicology16(5): 391–395.
