Full length article| Volume 220, P39-43, January 2018

The effect of follicullar fluid pesticides and polychlorinated biphenyls concentrations on intracytoplasmic sperm injection (ICSI) embryological and clinical outcome

Published:November 02, 2017DOI:



      The present study evaluated the correlation between the concentrations of polychlorinated biphenyls (PCBs) and pesticides in the follicular fluid (FF) obtained during intracytoplasmic sperm injection (ICSI) with the ovarian response, endometrial thickness, and embryological and clinical outcomes.


      Cross-sectional observational study.

      Materials and methods

      Women aged 20 to 38 years (300 infertile couples) presenting to a university-affiliated fertility center were approached to participate in the study. Only 150 couples that underwent ICSI for male factor infertility agreed to participate, and 94 of them had retrieved enough FF samples suitable for laboratory testing. The FF sample was obtained, centrifuged, and stored in liquid nitrogen. Two organochlorine pesticides (OCPs), Lindane and DDT;three organophosphates (OPs);chlorpyrifos;Diazinon; malathion; one Chloroacetanilide (Pretilachlor);two pyrethroids(Bioallethrin and β-cyfluthrin); and the concentrations of four PCBs, 28, 52, 138, 180, were estimated in the obtained FF samples by using gas chromatography/mass spectrometry. SPSS statistical analysis program (version 17) was used for analysis. Multiple regression analysis was used to correlate the PCBs and pesticides with ICSI outcomes.


      There were significant negative correlations between FF concentrations of the eight examined pesticides and the four PCBs on the endometrial thickness. However, Pretilachlor, chlorpyrifos, β-cyfluthrin, and Diazinon were the only toxic agents that negatively correlated with the number of the oocytes retrieved. Fertilization and early embryo cleavage rates were negatively correlated with Pretilachlor and β-cyfluthrin. Moreover, high concentrations of Lindane,DDT, Diazinon,and chlorpyrifos were significantly associated lower implantation rate. PCB 28 and 180 concentration in the FF was associated with a lower number of retrieved oocytes and fertilization rate, respectively. The number of implanted embryos was negatively correlated with PCB 52 FF concentration. However, the clinical pregnancy rate did not reach the level of significance.


      Higher concentrations of any studied PCBs and pesticides are associated with thinner endometrial thickness. The higher the level of Pretilachlor, β-cyfluthrin, PCB 28 and 180, the lower the retrieval, fertilization, and embryo cleavage rates. High PCB and pesticide concentrations in the FF adversely affected embryological ICSI outcomes. However, more data are needed to evaluate their effect on the clinical outcome.


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        • Rivas A.
        • Fernandez M.F.
        • Cerrillo I.
        • et al.
        Human exposure to endocrine disrupters: standardisation of a marker of estrogenic exposure in adipose tissue.
        APMIS. 2001; 109: 185-197
        • Tiemann U.
        In vivo and in vitro effects of the organochlorine pesticides DDT, TCPM, methoxychlor, and lindane on the female reproductive tract of mammals: a review.
        Reprod Toxicol. 2008; 25: 316-326
        • Brown J.F.
        Determination of PCB metabolic, excretion, and accumulation rates for use as indicators of biological response and relative risk.
        Environ Sci Technol. 1994; 28: 2295-2305
        • Freels S.
        • Chary L.K.
        • Turyk M.
        • et al.
        Congener profiles of occupational PCB exposure versus PCB exposure from fish consumption.
        Chemosphere. 2007; 69: 435-443
        • Harrad S.
        • Ren J.
        • Hazrati S.
        • Robson M.
        Chiral signatures of PCB#s 95 and 149 in indoor air, grass, duplicate diets and human faeces.
        Chemosphere. 2006; 63: 1368-1376
        • Herrick R.F.
        PCBs in school-persistent chemicals, persistent problems.
        New Solut. 2010; 20: 115-126
        • Kohler M.
        • Tremp J.
        • Zennegg M.
        • et al.
        Joint sealants: an overlooked diffuse source of polychlorinated biphenyls in buildings.
        Environ Sci Technol. 2005; 39: 1967-1973
        • Martinez A.
        • Norstrom K.
        • Wang K.
        • Hornbuckle K.C.
        Polychlorinated biphenyls in the surficial sediment of indiana harbor and ship canal, lake michigan.
        Environ Int. 2010; 36: 849-854
        • Wingfors H.
        • Selden A.I.
        • Nilsson C.
        • Haglund P.
        Identification of markers for PCB exposure in plasma from Swedish construction workers removing old elastic sealants.
        Ann Occup Hyg. 2006; 50: 65-73
        • Heinddel J.J.
        Role of exposure to environmental chemicals in the developmental basis of reproductive disease and dysfunction.
        Semin Reprod Med. 2006; 24: 168-177
        • De Felip E.
        • di Domenico A.
        • Miniero R.
        • Silvestroni L.
        Polychlorobiphenyls and other organochlorine compounds in human follicular fluid.
        Chemosphere. 2004; 54: 1445-1449
        • Meeker J.D.
        • Missmer S.A.
        • Vitonis A.F.
        • Cramer D.W.
        • Hauser R.
        Risk of spontaneous abortion in women with childhood exposure to parental cigarette smoke.
        Am J Epidemiol. 2007; 166: 571-575
        • Younglai E.V.
        • Foster W.G.
        • Hughes E.G.
        • Trim K.
        • Jarrell J.F.
        Levels of environmental contaminants in human follicular fluid, serum, and seminal plasma of couples undergoing in vitro fertilization.
        Arch Environ Contam Toxicol. 2002; 43: 121-126
        • Wade M.G.
        • Foster W.G.
        • Younglai E.V.
        • et al.
        Effects of subchronic exposure to a complex mixture of persistent contaminants in male rats: systemic, immune, and reproductive effects.
        Toxicol Sci. 2002; 67: 131-143
        • Mes J.
        • Marchand L.
        • Davies D.J.
        Organochlorine residues in adipose tissue of Canadians.
        Bull Environ Contam Toxicol. 1990; 45: 681-688
        • Polishuk Z.W.
        • Wassermann D.
        • Wassermann M.
        • Cucos S.
        • Ron M.
        Organochlorine compounds in mother and fetus during labor.
        Environ Res. 1977; 13: 278-284
        • Polishuk Z.W.
        • Ron M.
        • Wassermann M.
        • Cucos S.
        • Wassermann D.
        • Lemesch C.
        Organochlorine compounds in human blood plasma and milk.
        Pestic Monit J. 1977; 10: 121-129
        • Covaci A.
        • Jorens P.
        • Jacquemyn Y.
        • Schepens P.
        Distribution of PCBs and organochlorine pesticides in umbilical cord and maternal serum.
        Sci Total Environ. 2002; 298: 45-53
        • Toft G.
        • Thulstrup A.M.
        • Jonsson B.A.
        • et al.
        Fetal loss and maternal serum levels of 2,2',4,4',5,5'-hexachlorbiphenyl (CB-153) and 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene (p,p'-DDE) exposure: a cohort study in Greenland and two European populations.
        Environ Health. 2010; 9: 22
        • Mallozzi M.
        • Bordi G.
        • Garo C.
        • Caserta D.
        The effect of maternal exposure to endocrine disrupting chemicals on fetal and neonatal development: a review on the major concerns Birth defects research Part C.
        Embryol Today Rev. 2016; 108: 224-242
        • Bornman R.
        • de Jager C.
        • Worku Z.
        • Farias P.
        • Reif S.
        DDT and urogenital malformations in newborn boys in a malarial area.
        BJU Int. 2010; 106: 405-411
        • Liu Y.
        • Peterson K.E.
        Maternal exposure to synthetic chemicals and obesity in the offspring: recent findings.
        Curr Environ Health Rep. 2015; 2: 339-347
        • Langer P.
        • Kocan A.
        • Tajtakova M.
        • et al.
        Possible effects of polychlorinated biphenyls and organochlorinated pesticides on the thyroid after long-term exposure to heavy environmental pollution.
        J Occup Environ Med. 2003; 45: 526-532
        • Drbohlav P.
        • Bencko V.
        • Masata J.
        • et al.
        [Detection of cadmium and zinc in the blood and follicular fluid in women in the IVF and ET program].
        Ceska Gynekol. 1998; 63: 292-300
        • Younglai E.V.
        • Wu Y.
        • Foster W.G.
        Rapid action of pesticides on cytosolic calcium concentrations in cultures of human umbilical vein endothelial cells.
        Reprod Toxicol. 2006; 21: 271-279
        • Tsukimori K.
        • Tokunaga S.
        • Shibata S.
        • et al.
        Long-term effects of polychlorinated biphenyls and dioxins on pregnancy outcomes in women affected by the Yusho incident.
        Environ Health Perspect. 2008; 116: 626-630
        • Venners S.A.
        • Korrick S.
        • Xu X.
        • et al.
        Preconception serum DDT and pregnancy loss: a prospective study using a biomarker of pregnancy.
        Am J Epidemiol. 2005; 162: 709-716
        • Ouyang F.
        • Perry M.J.
        • Venners S.A.
        • et al.
        Serum DDT, age at menarche, and abnormal menstrual cycle length.
        Occup Environ Med. 2005; 62: 878-884
        • Jirsova S.
        • Masata J.
        • Jech L.
        • Zvarova J.
        Effect of polychlorinated biphenyls (PCBs) and 1,1,1-trichloro-2,2,-bis (4-chlorophenyl)-ethane (DDT) in follicular fluid on the results of in vitro fertilization-embryo transfer (IVF-ET) programs.
        Fertil Steril. 2010; 93: 1831-1836
        • Mahalingaiah S.
        • Missmer S.A.
        • Maity A.
        • et al.
        Association of hexachlorobenzene (HCB), dichlorodiphenyltrichloroethane (DDT), and dichlorodiphenyldichloroethylene (DDE) with in vitro fertilization (IVF) outcomes.
        Environ Health Perspect. 2012; 120: 316-320
        • CDC (Centers for Disease Control and Prevention)
        Fourth National Report on Human Exposure to Environmental Chemicals.
        Atlanta, GA, 2009
        • Perry M.J.
        • Ouyang F.
        • Korrick S.A.
        • et al.
        A prospective study of serum DDT and progesterone and estrogen levels across the menstrual cycle in nulliparous women of reproductive age.
        Am J Epidemiol. 2006; 164: 1056-1064
        • Rusiecki J.A.
        • Matthews A.
        • Sturgeon S.
        • et al.
        A correlation study of organochlorine levels in serum, breast adipose tissue, and gluteal adipose tissue among breast cancer cases in India.
        Cancer Epidemiol Biomarkers Prev. 2005; 14: 1113-1124
        • Kelce W.R.
        • Gray L.E.
        • Wilson E.M.
        Antiandrogens as environmental endocrine disruptors.
        Reprod Fertil Dev. 1998; 10: 105-111
        • Bonefeld-Jorgensen E.C.
        • Andersen H.R.
        • Rasmussen T.H.
        • Vinggaard A.M.
        Effect of highly bioaccumulated polychlorinated biphenyl congeners on estrogen and androgen receptor activity.
        Toxicology. 2001; 158: 141-153
        • Scippo M.L.
        • Argiris C.
        • Van De Weerdt C.
        • et al.
        Recombinant human estrogen, androgen and progesterone receptors for detection of potential endocrine disruptors.
        Anal Bioanal Chem. 2004; 378: 664-669
        • Rignell-Hydbom A.
        • Rylander L.
        • Giwercman A.
        • et al.
        Exposure to PCBs and p,p'-DDE and human sperm chromatin integrity.
        Environ Health Perspect. 2005; 113: 175-179
        • Pflieger-Bruss S.
        • Schill W.B.
        Effects of chlorinated hydrocarbons on sperm function in vitro.
        Andrologia. 2000; 32: 311-315