Effects of exposure to pesticides during pregnancy on placental maturity and weight of newborns: A cross-sectional pilot study in women from the Chihuahua State,Mexico

Abstract

It is known that pesticides cross the placental barrier and can cause alterations in the development of placental structures resulting in adverse effects in reproduction. The objectives of this study were to investigate the effects of pesticide exposure during pregnancy on placental maturity and to evaluate the relationship between placental maturity, gestational age and birth weight. We collected the placentas from singleton pregnancies from women exposed (n = 9) and non-exposed (n = 45 full-term and n = 31 preterm) to pesticides as evaluated geographically, by questionnaire and by acetylcholinesterase levels. Placental morphometry from the central and peripheral regions was examined by microscopy and staining with hematoxylin and eosin. The placental maturity index (PMI) was estimated by dividing the number of epithelial plates in terminal villi to their thickness in 1 mm² of the placental parenchyma. Gestational age, birth weight and the following characteristics of the mother were also recorded: pre-pregnancy body mass index, weight gain during pregnancy and hemoglobin concentrations. Birth weight and the gestational age were correlated with PMI (r = .54 and r = .44, respectively; p < .01). Pesticide exposure was associated with a higher PMI (beta = 7.38, p = .01) after adjusting by variables related to placental maturity. In conclusion, the results suggest a relationship between prenatal exposure to pesticides and placental maturity and may potentially affect the nutrient transport from the mother to the fetus.

Keywords

Pesticides placental maturity birth weight gestational age

References

Sharara FI , Seifer DB , Flaws JA Environmental toxicants and female reproduction. Fertil Steril 1998; 70: 613—622.

Jaga K. , Dharmani C. Sources of exposure to and public health implications of organophosphate pesticides . Pan Am J Public Health 2003; 14: 171—185.

Bolognesi C. Genotoxicity of pesticides: a review of human biomonitoring studies. Mutat Res 2003; 543: 251—272.

Stillerman KP , Mattison DR , Giudice LC , Woodruff TJ Environmental exposures and adverse pregnancy outcomes: a review of the science. Reprod Sci 2008; 15: 631—650.

Ye X. , Pierik FH , Hauser R. , et al. Urinary metabolite concentrations of organophosphorous pesticides, bisphenol A, and phthalates among pregnant women in Rotterdam, the Netherlands: the Generation R study. Environ Res 2008; 108: 260—267.

Bradman A. , Eskenazi B. , Barr DB , et al. Organophosphate urinary metabolite levels during pregnancy and after delivery in women living in an agricultural community. Environ Health Perspect 2005; 113: 1802—1807.

Torres-Arreola L. , Berkowitz G. , Torres-Sánchez L. , et al. Preterm birth in relation to maternal organochlorine serum levels. Ann Epidemiol 2003; 3: 158—162.

Berkowitz GS , Wetmur JG , Birman-Deych E. , et al. In utero pesticide exposure, maternal paraoxonase activity, and head circumference. Environ Health Perspect 2004; 112: 388—391.

Sesline DH , Jackson RJ The effect of the prenatal exposure to pesticides. In: Needleman HLBD (ed.) Prenatal exposure to toxicants. Baltimore: Johns Hop-kins, 1994, p.223—248.

10.

Gupta RC Environmental agents and placental toxicity: anticholinesterases and other insecticides. In: Sastry BV (ed.) Placental toxicology. Tennessee: CRC Press, Inc, 1995, p.257 —278.

11.

Schneider H. The role of the placenta in nutrition of the human fetus. Am J Obstet Gynecol 1991; 164: 967—973.

12.

Janowiak Z. , Mazerski J. New criterion of placental barrier maturity . Zentralbl Gynakol 1992; 114: 292—295.

13.

Benjaminov O. , Hoffer E. , Taitelman U. , Urbach J. , Brandes JM Parathion transfer and acetylcholinesterase activity in an in-vitro perfused term human placenta . Vet Hum Toxicol 1992; 34: 10—12.

14.

Srivastava MK, Raizada RB. Development effect of technical dimethoate in rats: maternal and fetal toxicity evaluation. Indian J Exp Biol 1996; 34: 329—333. 15. Wessler I, Kilbinger H, Bittinger F, Unger R, Kirkpatrick CJ. The non-neuronal cholinergic system in humans: expression, function and pathophysiology. Life Sci 2003; 72: 2055—2061.

15.

Lotti M. Organophosphorus compounds. In: Spencer P , Schaumburg H (ed.) Experimental and clinical neurotoxicology. New York: Oxford University Press Inc, 2000, p.898—925.

16.

Sastry BV Human placental cholinergic system. Biochem Pharmacol 1997; 53: 1577—1586.

17.

Lewis SH , Benirschke K. Overwiew of the placental pathology and justification for examination of the placenta. In: Lewis SH , Perrin E (eds.). Pathology of the placenta . Philadelphia: Churchill Livingstone , 1991, p.1—26.

18.

Maly A. , Goshen G. , Sela J. , Pinelis A. , Stark M. , Maly B. Histomorphometric study of placental villi vascular volume in toxemia and diabetes. Hum Pathol 2005; 36: 1074—1079.

19.

Egbor M. , Ansari T. , Morris N. , Green CJ , Sibbons PD Morphometric placental villous and vascular abnormalities in early- and late-onset pre-eclampsia with and without fetal growth restriction. BJOG 2006; 113: 580—589.

20.

Biagini G. , Vasi V. , Pugnaloni A. , et al. Morphological development of the human placenta in normal and complicated gestation: a quantitative and ultrastructural study. Gynecol Obstet Invest 1989; 28: 62—69.

21.

Murthy NV , Bhatnagar OP , Ganguly AK Placental acetylcholine and toxaemias of pregnancy. Indian J Med Res 1977; 65: 523—527.

22.

Sastry BV , Olubadewo J. , Harrison RD , Schmidt DE Human placental cholinergic system. Occurrence, distribution and variation with gestational age of acetylcholine in human placenta. Biochem Pharmacol 1976; 25: 425—431.

23.

Stoz F. , Schuhmann RA , Schebesta B. The development of the placental villus during normal pregnancy: morphometric data base. Arch Gynecol Obstet 1988; 244: 23—32.

24.

Benirschke K. , Kaufmann P. Architecture of normal villous trees. In: Benirschke K , Kaufmann P (eds.) Pathology of the human placenta. New York: Springer, 2000, p.116—154.

25.

Levario-Carrillo M. , Chávez-Corral D. , Ramos-Martínez E. , Solis F. , González-Horta C. , Sanin LH Exposición de mujeres a plaguicidas organofosforados durante el embarazo y alteraciones en la placenta. Rev Bras Toxicol 2002; 15: 79—85.

26.

White FMM , Choen FG , Sherman G. , McCurdy R. Chemicals birth defects and stillbirths in New Brunswick: associations with agricultural activity. CMAJ 1988; 138: 117—124.

27.

Lagunes-Tejeda A. , Rodríguez-Maciel JC , Mota-Sánchez D. Combate químico de plagas agrícolas en México. Colegio de Postgraduados en Ciencias Agrícolas. Consejo Nacional Consultivo Fitosanitario. México, D.F.; 1994.

28.

Levario-Carrillo M. , Amato D. , Ostrosky-Wegman P. , Gonzalez-Horta C. , Corona Y. , Sanin LH Relation between pesticide exposure and intrauterine growth retardation. Chemosphere 2004; 55: 1421—1427.

29.

Ellman GL , Courtney KD , Andres V. Jr , Feather-Stone RM A new and rapid colorimetric determination of acetylcholinesterase activity . Biochem Pharmacol 1961; 7: 88—95.

30.

Centro panamericano de ecología humana y salud: Paquete espectofotométrico para medir la actividad de la colinesterasa. Metepec/México, Organización mundial de la salud, 1986, p.1—19.

31.

Benirschke K. , Kaufmann P. Classification of villus maldevelopment . In: Benirschke K , Kaufmann P (eds.) Pathology of the human placenta . New York: Springer, 2000, p.449—450.

32.

Popek EJ Normal anatomy and histology of the placenta. In: Lewis SH , Perrin E (eds.) Pathology of the placenta. Philadelphia: Churchill Livingstone, 1991, p.49—88.

33.

Fajardo-Gutierrez A. , Yamamoto-Kimura LT , Garduño-Espinoza J. , Hernandez-Hernandez DM , Martinez-Garcia MC The consistency and validity of a measurement in clinical pediatric research . Its definition, evaluation and interpretation. Bol Med Hosp Infant Mex 1991; 48: 367—381.

34.

Prieto L. , Lamarca R. , Casado A. Assessment of the reliability of clinical findings: the intraclass correlation coefficient. Med Clin (Barc) 1998; 110: 142—145.

35.

Mc Kenna D. , Tharmaratnam S. , Mahsud S. , Dornan J. Ultrasonic evidence of placental calcification at 36 weeks’ gestation: maternal and fetal outcomes. Acta Obstet Gynecol Scand 2005 ; 84: 7—10.

36.

Kingdom J. , Huppertz B. , Seaward G. , Kaufmann P. Development of the placental villous tree and its consequences for fetal growth . Eur J Obstet Gynecol Reprod Biol 2000; 92: 35—43.

37.

Little RE , Zadorozhnaja TD , Hulchiy OP , et al. Placental weight and its ratio to birthweight in a Ukrainian city. Early Hum Dev 2003; 71: 117—127.

38.

Leyland A. , Pritchard C. Fetal growth and ratio of placental weight to birth weight. BMJ 1992; 304: 1052—1053.

39.

Honda M. , Toyoda C. , Nakabayashi M. , Omori Y. Quantitative investigations of placental terminal villi in maternal diabetes mellitus by scanning and transmission electron microscopy. Tohoku J Exp Med 1992; 167: 247—257.

40.

González-García B. , Olave ME , Ramos-Martínez E. , González-Horta C. , Levario-Carrillo M. , Sánchez-Ramirez B. Decrease of muscarinic cholinergic receptors expression in placenta from rats exposed to methyl parathion. Hum Exp Toxicol 2008; 27: 241—246.

41.

Woodruff TJ , Carlson A. , Schwartz JM , Giudice LC Proceedings of the summit on environmental challenges to reproductive health and fertility: executive summary. Fertil Steril 2008; 89: e1—e20.

42.

Eskenazi B. , Harley K. , Bradman A. , et al. Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect 2004; 112: 1116—1124.

43.

Ostrea EM , Bielawski DM , Posecion NC , et al.Combined analysis of prenatal (maternal hair and blood) and neonatal (infant hair cord blood and meconuim) matrices to detect fetal exposure to environmental pesticides. Environ Res 2009 ; 109: 116—122.

44.

Capurro H. , Konichezky S. , Fonseca D. , Caldeyro-Barcia R. A simplified method for diagnosis of gestational age in the newborn infant . J Pediatr 1978; 93: 120—122.