Pesticides, sexual development, reproduction, and fertility: Current perspective and future direction

Human and Ecological Risk Assessment

Volumn 13, Issue 5, 2007, Pages 1078-1110

  Colborn, Theo ^a   Carroll, Lynn E ^b  

^a UNIVERSITY OF FLORIDA   (United States)

^b THE ENDOCRINE DISRUPTION EXCHANGE   (United States)

Author keywords

Adverse effects; Agriculture; Endocrine disruption; Exposure; Fetal origin; Pesticides

Indexed keywords

EID: 34848860162     PISSN: 10807039     EISSN: 15497860     Source Type: Journal    
DOI: 10.1080/10807030701506405     Document Type: Article

References (108)

1. Allan BB, Brant R, Seidel JE, et al. 1997. Declining sex ratios in Canada. Can Med Assoc J 156:37-41
2. Anway MD, Cupp AS, Uzumcu M, et al. 2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308:1466-9
3. Arbuckle TE, Schrader SM, Cole D, et al. 1999. 2,4-Dichlorophenoxyacetic acid residues in semen of Ontario farmers. Reprod Toxicol 13:421-9
4. Arbuckle TE, Lin Z, and 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 109:851-7
5. Attaran A, Roberts DR, Curtis CF, et al. 2000. Balancing risks on the backs of the poor. Nat Med 6:729-31
6. Beard AP and Rawlings NC. 1998. Reproductive effects in mink (Mustela vison) exposed to the pesticides lindane, carbofuran and pentachlorophenol in a multigeneration study. J Reprod Fertil 113:95-104
7. Beard AP, Bartlewski PM, and Rawlings NC. 1999. Endocrine and reproductive function in ewes exposed to the organochlorine pesticides lindane or pentachlorophenol. J Toxicol Environ Health 56:23-46
8. Bell EM, Hertz-Picciotto I, and Beaumont JJ. 2001a. Case-cohort analysis of agricultural pesticide applications near maternal residence and selected causes of fetal death. Am J Epidemiol 154:702-10
9. Bell EM, Hertz-Picciotto I, and Beaumont JJ. 2001b. A case-control study of pesticides and fetal death due to congenital anomalies. Epidemiology 12:148-56
10. Benbrook CM. 2004 May. Minimizing Pesticide Dietary Exposure through Consumption of Organic Food. An Organic Center State of Science Review. Center for Organic Education and Promotion, Greenfield, MA, USA
11. Berkowitz GS, Lapinski RH, and Wolff MS. 1996. The role of DDE and polychlorinated biphenyl levels in preterm birth. Arch Environ Contam Toxicol 30:139-41
12. Bouwman H, Sereda B, and Meinhardt HM. 2006. Simultaneous presence of DDT and pyrethroid residues in human breast milk from a malaria endemic area in South Africa. Environ Pollut 144:902-17
13. Bradman A, Barr DB, Henn BGC, et al. 2003. Measurement of pesticides and other toxicants in amniotic fluid as a potential biomarker of prenatal exposure: A validation study. Environ Health Perspect 111:1779-82
14. Brock JW, Melnyk LJ, Caudill SP, et al. 1998. Serum levels of several organochlorine pesticides in farmers correspond with dietary exposure and local use history. Toxicol Ind Health 14:275-89
15. Cavieres MF, Jaeger J, and Porter W. 2002. Developmental toxicity of a commercial herbicide mixture in mice: I. Effects on embryo implantation and litter size. Environ Health Perspect 110:1081-5
16. CDC (Centers for Disease Control and Prevention). 2003 Jan. Second National Report on Human Exposure to Environmental Chemicals. NCEH Pub. No. 02-0716. National Center for Environmental Health, Atlanta, GA, USA
17. CDC. 2005. QuickStats: Leading causes of neonatal and postneonatal deaths: United States, 2002. MMWR Morb Mortal Wkly Rep 54:966
18. Chapin RE, Stevens JT, Hughes CL, et al. 1996. Endocrine modulation of reproduction. Fundam Appl Toxicol 29:1-17
19. CIA (US Central Intelligence Agency). 2005 November 1. Birth rate [by country]. Available at http://www.cia.gov/cia/publications/factbook/geos/xx. html; http://www.cia.gov/cia/publications/factbook/geos/us.html; http://www.cia.gov/cia/publications/factbook/ geos/ge.html; http://www.cia.gov/ cia/publications/factbook/geos/ja.html
20. Cohn BA, Cirillo PM, Wolff MS, et al. 2003. DDT and DDE exposure in mothers and time to pregnancy in daughters. Lancet 361:2205-06
21. Colborn T and Clement C, eds. 1992, Chemically Induced Alterations in Sexual and Functional Development: The Wildlife/Human Connection. Princeton Scientific Publishing Co., Inc., Princeton, NJ, USA
22. Cooper RL, Barrett MA, Goldman JM, et al. 1994. Pregnancy alterations following xenobiotic induced delays in ovulation in the female rat. Fundam Appl Toxicol 22:474-80
23. Coronado GD, Thompson B, Strong L, et al. 2004. Agricultural task and exposure to organophosphate pesticides among farmworkers. Environ Health Perspect 112:142-7
24. Curl CL, Fenske RA, and Elgethun K. 2003. Organophosphorus pesticide exposure of urban and suburban preschool children with organic and conventional diets. Environ Health Perspect 111:377-82
25. Davis DL, Gottlieb MB, and Stampnitzky JR. 1998. Reduced ratio of male to female births in several industrial countries - a sentinel health indicator. JAMA 279:1018-23
26. de Jager C, Farias P, Barraza A, et al. 2004. Seminal parameters after environmental DDT exposure in Mexico. In: Proceedings: 8th World Congress on Environmental Health, 22-27 February 2004, Durban, South Africa
27. de Jager C, Farias P, Barraza-Villarreal A, et al. 2006. Reduced seminal parameters associated with environmental DDT exposure and p , p′ -DDE concentrations in men from Chiapas, Mexico. J Androl 27:16-27
28. Derfoul A, Lin FJ, Awumey EM, et al. 2003. Estrogenic endocrine disruptive components interfere with calcium handling and differentiation of human trophoblast cells. J Cell Biochem 89:755-70
29. Doerge DR, Twaddle NC, Churchwell MI, et al. 2006. Lactational transfer of the soy isoflavone, genistein, in Sprague-Dawley rats consuming dietary genistein. Reprod Toxicol 21:307-12
30. Dorea JG, Cruz-Granja AC, Lacayo-Romero ML, et al. 2001. Perinatal metabolism of dichlorodiphenyldichloroethylene in Nicaraguan mothers. Environ Res 86:229-37
31. Duggan A, Charnley G, Chen W, et al. 2003. Di-alkyl phosphate biomonitoring data: assessing cumulative exposure to organophosphate pesticides [review]. Regul Toxicol Pharmacol 37:382-95
32. Fausto AM, Morera P, Margarit R, et al. 2001. Sperm quality and reproductive traits in male offspring of female rabbits exposed to lindane (γ̃HCH) during pregnancy and lactation. Reprod Nutr Dev 41:217-25
33. Foster W, Chan S, Platt L, et al. 2000. Detection of endocrine disrupting chemicals in samples of second trimester human amniotic fluid. J Clin Endocrinol Metab 85:2954-7
34. Gaido KW, Leonard LS, Maness SC, et al. 1999. Differential interaction of the methoxychlor metabolite 2,2-bis-(p-hydroxyphenyl)-1,1, 1-trichloroethane with estrogen receptors α and β. Endocrinology 140:5746-53
35. García-Rodríguez J, García-Martín M, Nogueras-Ocaña M, et al. 1996. Exposure to pesticides and cryptorchidism - Geographical evidence of a possible association. Environ Health Perspect 104:1090-5
36. Garry VF, Schreinemachers D, Harkins ME, et al. 1996. Pesticide appliers, biocides, and birth defects in rural Minnesota. Environ Health Perspect 104:394-9
37. Garry VF, Burroughs B, Tarone R, et al. 1999. Herbicides and adjuvants: an evolving view. Toxicol Ind Health 15:160-8
38. Garry VF, Harkins ME, Erickson LL, et al. 2002a. 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 (Suppl 3):441-9
39. Garry VF, Harkins ME, Lyubimov A, et al. 2002b. Reproductive outcomes in the women of the Red River Valley of the north. I. The spouses of pesticide applicators: Pregnancy loss, age at menarche, and exposures to pesticides. J Toxicol Environ Health A 65:769-86
40. Gladen BC and Rogan WJ. 1995. DDE and shortened duration of lactation in a northern Mexican town. Am J Public Health 85:504-8
41. Gladen BC, Ragan NB, and Rogan WJ. 2000. Pubertal growth and development and prenatal and lactational exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene. J Pediatr 136:490-6
42. Greenlee AR, Arbuckle TE, and Chyou PH. 2003. Risk factors for female infertility in an agricultural region. Epidemiology 14:429-36
43. Greenlee AR, Ellis TM, Berg RL, et al. 2005. Pregnancy outcomes for mouse preimplantation embryos exposed in vitro to the estrogenic pesticide o, p′-DDT. Reprod Toxicol 20:229-38
44. Hauser R, Singh NP, Chen Z, et al. 2003. Lack of an association between environmental exposure to polychlorinated biphenyls and p , p′-DDE and DNA damage in human sperm measured using the neutral comet assay. Hum Reprod 18:2525-33
45. Hediger ML, Overpeck MD, Ruan WJ, et al. 2002. Birthweight and gestational age effects on motor and social development. Paediatr Perinat Epidemiol 16:33-46
46. Hunt PA, Koehler KE, Susiarjo M, et al. 2003. Bisphenol A exposure causes meiotic aneuploidy in the female mouse. Curr Biol 13:546-53
47. Huwe JK, Clark GC, Chu AC, et al. 2003. CALUX and high resolution GC/MS analysis of dioxin-like compounds in chlorophenoxy pesticide formulations. Organohalogen Compounds 60:227-30
48. Jahnke GD, Choksi NY, Moore JA, et al. 2004. Thyroid toxicants: Assessing reproductive health effects. Environ Health Perspect 112:363-8
49. Jarrell JF, Villeneuve D, Franklin C, et al. 1993. Contamination of human ovariam follicular fluid and serum by chlorinated organic compounds in three Canadian cities. Can Med Assoc J 148:1321-7
50. Jefferson WN, Padilla-Banks E, and Newbold RR. 2005. Adverse effects on female development and reproduction in CD-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses. Biol Reprod 73:798-806
51. Jensen WD, Giwercman A, Carlsen E, et al. 1996. Semen quality among members of organic food associations in Zealand, Denmark. Lancet 347:1844
52. Kelce WR, Stone CR, Laws SC, et al. 1995. Persistent DDT metabolite p , p′-DDE is a potent androgen receptor antagonist. Nature 375:581-5
53. Kristensen P, Irgens LM, Andersen A, et al. 1997a. Birth defects among offspring of Norwegian farmers, 1967-1991. Epidemiology 8:537-44
54. Kristensen P, Irgens LM, Andersen A, et al. 1997b. Gestational age, birth weight, and perinatal death among births to Norwegian farmers, 1967-1991. Am J Epidemiol 146:329-38
55. Kristensen P, Irgens LM, and Bjerkedal T. 1997c. Environmental factors, reproductive history, and selective fertility in farmers sibships. Am J Epidemiol 145:817-25
56. Kurt-Karakus PB, Bidleman TF, Staebler RM, et al. 2006. Measurement of DDT fluxes from a historically treated agricultural soil in Canada. Environ Sci Technol 40:4578-85
57. Larsen SB, Spano M, Giwercman A, et al. 1999. Semen quality and sex hormones among organic and traditional Danish farmers. Occup Environ Med 56:139-44
58. Lin N and Garry VF. 2000. In vitro studies of cellular and molecular developmental toxicity of adjuvants, herbicides, and fungicides commonly used in Red River Valley, Minnesota. J Toxicol Environ Health A 60:423-39
59. Longnecker MP. 2005. Invited Commentary: Why DDT matters now. Am J Epidemiol 162:726-8
60. Longnecker MP, Klebanoff MA, Zhou H, et al. 2001. Association between maternal serum concentration of the DDT metabolite DDE and preterm and small-for-gestational-age babies at birth. Lancet 358:110-4
61. Longnecker MP, Klebanoff MA, Brock JW, et al. 2002. Maternal serum level of 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene and risk of cryptorchidism, hypospadias, and polythelia among male offspring. Am J Epidemiol 155(4):313-22
62. Lu C, Toepel K, Irish R, et al. 2005. Organic diets significantly lower children's dietary exposure to organophosphorus pesticides. Environ Health Perspect 114:260-3
63. Marcus M, Kiely J, Xu FJ, et al. 1998. Changing sex ratio in the United States, 1969-1995. Fertil Steril 70:270-3
64. Meeker JD, Ryan L, Barr DB, et al. 2004a. The relationship of urinary metabolites of carbaryl/ naphthalene and chlorpyrifos with human semen quality. Environ Health Perspect 112:1665-70
65. Meeker JD, Singh NP, Ryan L, et al. 2004b. Urinary levels of insecticide metabolites and DNA damage in human sperm. Hum Reprod 19:2573-80
66. Meeker JD, Ryan L, Barr DB, et al. 2006. Exposure to nonpersistent insecticides and male reproductive hormones. Epidemiology 17:61-8
67. Mizuno R. 2000. The male/female ratio of fetal deaths and births in Japan. Lancet 356:738-9
68. Mocarelli P, Gerthoux PM, Ferrari E, et al. 2000. Paternal concentrations of dioxin and sex ratio of offspring. Lancet 355:1858-63
69. Munger R, Isacson P, Hu S, et al. 1997. Intrauterine growth retardation in Iowa communities with herbicide-contaminated drinking water supplies. Environ Health Perspect 105:308-14
70. North K and Golding J. 2000. A maternal vegetarian diet in pregnancy is associated with hypospadias. BJU Int 85:107-13
71. Ouyang F, Perry MJ, Venners SA, et al. 2005. Serum DDT, age at menarche, and abnormal menstrual cycle length. Occup Environ Med 62:878-84
72. Panganiban L, Cortes-Maramba N, Dioquino C, et al. 2004. Correlation between blood ethylenethiourea and thyroid gland disorders among banana plantation workers in the Philippines. Environ Health Perspect 112:42-5
73. Pastore LM, Hertz-Picciotto I, and Beaumont JJ. 1997. Risk of stillbirth from occupational and residential exposures. Occup Environ Med 54:511-8
74. Petrelli G and Figà-Talamanca I. 2001. Reduction in fertility in male greenhouse workers exposed to pesticides. Eur J Epidemiol 17:675-7
75. Polder A, Odland JO, Tkachev A, et al. 2003. Geographic variation of chlorinated pesticides, toxaphenes and PCBs in human milk from sub-Arctic and Arctic locations in Russia. Sci Total Environ 306:179-95
76. Ralph JL, Orgebin-Crst M-C, Lareyre J-J, et al. 2003. Disruption of androgen regulation in the prostate by the environmental contaminant hexachlorobenzene. Environ Health Perspect 111:461-6
77. Regidor E, Ronda E, García AM, et al. 2004. Paternal exposure to agricultural pesticides and cause specific fetal death. Occup Environ Med 61:334-9
78. Rogan WJ, Gladen BC, McKinney JD, et al. 1987. Polychlorinated biphenyls (PCBs) and dichlorodiphenyl dichloroethene (DDE) in human milk: Effects on growth, morbidity, and duration of lactation. Am J Public Health 77:1294-7
79. Ryan JJ, Amirova Z, and Carrier G. 2002. Sex ratios of children of Russian pesticide producers exposed to dioxin. Environ Health Perspect 110:A699-A701
80. Salazar-García G, Gallardo-Díaz E, Cerón-Mireles P, et al. 2004. Reproductive effects of occupational DDT exposure among male malaria control workers. Environ Health Perspect 112:542-7
81. Savitz DA, Arbuckle T, Kaczor D, et al. 1997. Male pesticide exposure and pregnancy outcome. Am J Epidemiol 146:1025-36
82. Saxena MC, Siddiqui MKJ, Agarwal V, et al. 1983. A comparison of organochlorine insecticide contents in specimens of maternal blood, placenta, and umbilical-cord blood from stillborn and live-born cases. J Toxicol Environ Health 11:71-9
83. Schecter A, Papke O, Isaac J, et al. 1997. 2,3,7,8 chlorine substituted dioxin and dibenzofuran congeners in 2,4-D, 2,4,5-T and pentachlorophenol. Organohalogen Compounds 32:51-5
84. Schinas V, Leotsinidis M, Alexopoulos A, et al. 2000. Organochlorine pesticide residues in human breast milk from southwest Greece: Associations with weekly food consumption patterns of mothers. Arch Environ Health 55:411-7
85. Schreinemachers DM, Creason JP, and Garry VF . 1999. Cancer mortality in agricultural regions of Minnesota. Environ Health Perspect 107:205-11
86. Siddiqui MKJ, Srivastava S, Srivastava SP, et al. 2003. Persistent chlorinated pesticides and intra-uterine foetal growth retardation: A possible association. Int Arch Occup Environ Health 76:75-80
87. Simanainen U, Haavisto T, Tuomisto JT, et al. 2004. Pattern of male reproductive system effects after in utero and lactational 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) exposure in three differentially TCDD-sensitive rat lines. Toxicol Sci 80:101-8
88. Simonetti J, Berner J, and Williams K. 2001. Effects of p , p′-DDE on immature cells in culture at concentrations relevant to the Alaskan environment. Toxicol in Vitro 15:169-79
89. Stevens JT and Breckenridge CB. 2001. Crop protection chemicals. In: Hayes WA (ed), Principles and Methods of Toxicology, 4th ed., pp 565-648. Taylor and Francis, Philadelphia, PA, USA
90. Stoker TE, Goldman JM, and Cooper RL. 1993. The dithiocarbamate fungicide thiram disrupts the hormonal control of ovulation in the female rat. Reprod Toxicol 7:211-8
91. Stoker TE, Cooper RL, Goldman JM, et al. 1996. Characterization of pregnancy outcome following thiram-induced ovulatory delay in the female rat. Neurotoxicol Teratol 18:277-82
92. Swan SH, Brazil C, Drobnis EZ, et al. 2003a. Geographic differences in semen quality of fertile U.S. males. Environ Health Perspect 111:414-20
93. Swan SH, Kruse RL, Liu F, et al. 2003b. Semen quality in relation to biomarkers of pesticide exposure. Environ Health Perspect 111:1478-84
94. Swartz WJ and Eroschenko VP. 1998. Neonatal exposure to technical methoxychlor alters pregnancy outcome in female mice. Reprod Toxicol 12:565-73
95. Torres-Arreola L, Berkowitz G, Torres-Sanchez L, et al. 2003. Preterm birth in relation to maternal organochlorine serum levels. Ann Epidemiol 13:158-62
96. US Bureau of the Census. 2005 Apr 26. International Database. Table 028, Total Fertility Rate [global data]; Age-Specific Fertility Rates and Selected Derived Measures [US data]. Available at http://www.census.gov/ipc/www/idbnew. html; http://www.census.gov/cgibin/ipc/idbagg; http://www.census.gov/cgi-bin/ ipc/idbsprd
97. Vasiliu O, Muttineni J, and Karmaus W. 2004. In utero exposure to organochlorines and age at menarche. Hum Reprod 19:1506-12
98. Vaughan TL, Daling JR, and Starzyk PM. 1984. Fetal death and maternal occupation. An analysis of birth records in the State of Washington. J Occup Med 26:676-8
99. Venners SA, Korrick Z, Xu X, et al. 2005. Preconception serum DDT and pregnancy loss: A prospective study using a biomarker of pregnancy . Am J Epidemiol 162:709-16
100. Waliszewski SM, Aguirre AA, Infanzon RM, et al. 2002. Persistent organochlorine pesticide levels in maternal blood serum, colostrum, and mature milk. Bull Environ Contam Toxicol 68:324-31
101. Weidner IS, Moller H, Jensen TK, et al. 1998. Cryptorchidism and hypospadias in sons of gardeners and farmers. Environ Health Perspect 106:793-6
102. Welshons WV, Nagel SC, Thayer KA, et al. 1999. Low-dose bioactivity of xenoestrogens in animals: Fetal exposure to low doses of methoxychlor and other xenoestrogens increases adult prostate size in mice. Toxicol Ind Health 15:12-25
103. Whyatt RM and Barr DB. 2001. Measurement of organophosphate metabolites in postpartum meconium as a potential biomarker of prenatal exposure: A validation study. Environ Health Perspect 109:417-20
104. Windham GC, Lee D, Mitchell PI, et al. 2005. Exposure to organochlorine compounds and effects on ovarian function. Epidemiology 16:182-90
105. Wójtowicz AK, Gregoraszczuk EL, Ptak A, et al. 2004. Effect of single and repeated in vitro exposure of ovarian follicles to o,p'-DDT and p,p'-DDT and their metabolites. Pol J Pharmacol 56:465-72
106. Wu Y, Foster WG, and Younglai EV. 2006. Rapid effects of pesticides on human granulosa-lutein cells. Reproduction 131:299-310
107. Xiang HY, Nuckols JR, and Stallones L. 2000. A geographic information assessment of birth weight and crop production patterns around mother's residence. Environ Res 82:160-7
108. Younglai EV, Holloway AC, Lim GE, et al. 2004. Synergistic effects between FSH and 1,1-dichloro-2,2-bis(P-chlorophenyl)ethylene (P, P′-DDE) on human granulosa cell aromatase activity. Hum Reprod 19:1089-93