Skip to main content
SpringerLink
Log in

Characterization of Pesticide Exposure in a Sample of Pregnant Women in Ecuador

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Few studies have detailed the prenatal pesticide exposure levels of women employed in or residing near large-scale agricultural industries. This study reports pesticide metabolite levels during and shortly after pregnancy in a pilot study of workers in Ecuador. Urine samples were collected for 16 rose workers and 10 nonagricultural workers enrolled into the study in early pregnancy. We measured six nonspecific organophosphatedialkylphosphate (DAP) pesticide metabolites, two alkylenebis-dithiocarbamate pesticide metabolites [ethylene thiourea (ETU) and propylene thiourea (PTU)], 3,5,6-trichloro-2-pyridinol (TCPy), malathion dicarboxylic acid, and two pyrethroid metabolites (2,2-dimethylcyclo propanecarboxylic acid and 3-phenooxybenzoic acid). We collected 141 urine samples (mean: 5.4 per woman). We observed high detection frequencies for five DAP metabolites and ETU, PTU, and TCPy. We report elevated levels of ETU in the entire sample (median 4.24 ng/mL, IQR 2.23, 7.18), suggesting other possible non-occupational pathways of exposure. We found no statistical differences in pesticide levels by current employment status, although the highest pesticide levels were among rose workers. We observed within-woman correlation in TCPy and PTU levels, but not in ETU or DAP levels. The present study is the first to characterize prenatal pesticide exposure levels among working women in Ecuador. Limitations include a small sample size and use of a convenience sample. Strengths include a longitudinal design and multiple urine samples per woman. Results provide an initial characterization of prenatal pesticide exposure levels and how these levels vary over pregnancy in a community impacted by agricultural industry and will inform further studies in the region.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Alavanja MC (2009) Introduction: pesticides use and exposure extensive worldwide. Rev Environ Health 24:303–309

    Article  CAS  Google Scholar 

  • Barr DB et al (1999) Strategies for biological monitoring of exposure for contemporary-use pesticides. Toxicol Ind Health 15:168–179

    Article  CAS  Google Scholar 

  • Barr DB et al (2004) Concentrations of dialkyl phosphate metabolites of organophosphorus pesticides in the U.S. population. Environ Health Perspect 112:186–200

    Article  CAS  Google Scholar 

  • Berman T, Hochner-Celnikier D, Barr D, Needham L, Amitai Y, Wormser U, Richter E (2011) Pesticide exposure among pregnant women in Jerusalem, Israel: results of a pilot study. Environ Int 37:198–203. doi:10.1016/j.envint.2010.09.002

    Article  CAS  Google Scholar 

  • Bradman A et al (2005) Organophosphate urinary metabolite levels during pregnancy and after delivery in women living in an agricultural community. Environ Health Perspect 113:1802–1807. doi:10.1289/ehp.7894

    Article  CAS  Google Scholar 

  • Bradman A et al (2013) Variability of organophosphorous pesticide metabolite levels in spot and 24-hr urine samples collected from young children during 1 week. Environ Health Perspect 21:118–124. doi:10.1289/ehp.1104808

    Google Scholar 

  • Breilh J (2007) New model of accumulation and agro-business: the ecological and epidemiological implications of the Ecuadorian cut flower production. Ciencia Saude Coletiva 12:91–104

    Article  Google Scholar 

  • Breilh J et al. (2005) Floriculture and the health divide: a struggle for fair and ecological flowers. In: CEAS (ed) Latin American Health Watch: Alternative Latin American Health Report. Global Health Watch, Quito

  • Castorina R et al (2010) Comparison of current-use pesticide and other toxicant urinary metabolite levels among pregnant women in the CHAMACOS cohort and NHANES. Environ Health Perspect 118:856–863. doi:10.1289/ehp.0901568

    Article  CAS  Google Scholar 

  • CDC (2001) National Report on Human Exposure to Environmental Chemicals. Centers for Disease Control and Prevention, National Center Environmental Health, Atlanta

    Google Scholar 

  • CDC (2003) Second national report on human exposure to environmental chemicals. Centers for Disease Control and Prevention, National Center Environmental Health, Atlanta

    Google Scholar 

  • CDC (2013a) Biomonitoring summary: ethylenethiourea propylenethiourea. Centers for Disease Control and Prevention, Atlanta

    Google Scholar 

  • CDC (2013b) Fourth national report on human exposure to environmental chemicals. Centers for Disease Control and Prevention, Atlanta

    Google Scholar 

  • Cole DC, Carpio F, Julian J, Leon N, Carbotte R, De Almeida H (1997) Neurobehavioral outcomes among farm and nonfarm rural Ecuadorians. Neurotoxicol Teratol 19:277–286

    Article  CAS  Google Scholar 

  • Colosio C et al (2003) Occupational exposure to fungicides in floriculture in Ecuador. Giornale Italiano di Medicina del Lavoro ed Ergonomia 25(Suppl):107–108

    Google Scholar 

  • Direccion de Inteligencia Comercial e Inversiones (2011) Analisis Sectorial de Flores ProEcuador. Instituto de Promocion de Exportaciones e Inversiones. Ministerio de Relaciones Exteriores Comercio e Integracion, Quito. http://www.proecuador.gob.ec/wp-content/uploads/downloads/2012/01/PROEC-AS2011-FLORES.pdf

  • Ecobichon D (2001) Pesticide use in developing countries. Toxicology 160(1–3):6

    Google Scholar 

  • Engel SM et al (2007) Prenatal organophosphate metabolite and organochlorine levels and performance on the Brazelton Neonatal Behavioral Assessment Scale in a multiethnic pregnancy cohort. Am J Epidemiol 165:1397–1404. doi:10.1093/aje/kwm029

    Article  Google Scholar 

  • Eskenazi B et al (2004) Association of in utero organophosphate pesticide exposure and fetal growth and length of gestation in an agricultural population. Environ Health Perspect 112:1116–1124. doi:10.1289/ehp.6789

    Article  CAS  Google Scholar 

  • Eskenazi B et al (2007) Organophosphate pesticide exposure and neurodevelopment in young Mexican-American children. Environ Health Perspect 115:792–798. doi:10.1289/ehp.9828

    Article  CAS  Google Scholar 

  • Eskenazi B et al (2008) Pesticide toxicity and the developing brain. Basic Clin Pharm Toxicol 102:228–236. doi:10.1111/j.1742-7843.2007.00171.x

    Article  CAS  Google Scholar 

  • Fenske RA, Kissel JC, Lu C, Kalman DA, Simcox NJ, Allen EH, Keifer MC (2000) Biologically based pesticide dose estimates for children in an agricultural community. Environ Health Perspect 108:515–520

    Article  CAS  Google Scholar 

  • Grandjean P, Landrigan PJ (2014) Neurobehavioural effects of developmental toxicity. Lancet Neurol 13:330–338. doi:10.1016/S1474-4422(13)70278-3

    Article  CAS  Google Scholar 

  • Hallam D, Liu P, Lavers G, Pikauskas P, Rapsomanikis G, Claro J (2004) The market for non-traditional agricultural exports. Raw Material, Tropical and Horticultural Products Service Commodities and Trade Division

    Google Scholar 

  • Handal AJ, Lozoff B, Breilh J, Harlow SD (2007a) Effect of community of residence on neurobehavioral development in infants and young children in a flower-growing region of Ecuador. Environ Health Perspect 115:128–133. doi:10.1289/ehp.9261

    Article  Google Scholar 

  • Handal AJ, Lozoff B, Breilh J, Harlow SD (2007b) Neurobehavioral development in children with potential exposure to pesticides. Epidemiology 18:312–320. doi:10.1097/01.ede.0000259983.55716.bb

    Article  Google Scholar 

  • Handal AJ, Lozoff B, Breilh J, Harlow SD (2007c) Sociodemographic and nutritional correlates of neurobehavioral development: a study of young children in a rural region of Ecuador. Pan Am J Public Health 21:292–300

    Article  Google Scholar 

  • Handal AJ, Harlow SD, Breilh J, Lozoff B (2008) Occupational exposure to pesticides during pregnancy and neurobehavioral development of infants and toddlers. Epidemiology 19:851–859. doi:10.1097/EDE.0b013e318187cc5d

    Article  Google Scholar 

  • Handal AJ, McGough-Maduena A, Paez M, Skipper B, Rowland AS, Fenske RA, Harlow SD (2014) A pilot study comparing observational and questionnaire surrogate measures of pesticide exposure among residents impacted by the Ecuadorian flower industry. Arch Environ Occupational Health. doi:10.1080/19338244.2013.879563

    Google Scholar 

  • Harari R et al (2004) Seguridad, Salud, y Ambiente en la Floricultura. IFA-Promesa, Quito

    Google Scholar 

  • Houeto P, Bindoula G, Hoffman JR (1995) Ethylenebisdithiocarbamates and ethylenethiourea: possible human health-hazards. Environ Health Perspect 103:568–573. doi:10.2307/3432432

    Article  CAS  Google Scholar 

  • Huen K, Bradman A, Harley K, Yousefi P, Barr DB, Eskenazi B, Holland N (2012) Organophosphate pesticide levels in blood and urine of women and newborns living in an agricultural community. Environ Res 117:8–16. doi:10.1016/j.envres.2012.05.005

    Article  CAS  Google Scholar 

  • Jurewicz J, Hanke W (2008) Prenatal and childhood exposure to pesticides and neurobehavioral development: review of epidemiological studies. Int J Occup Med Environ Health 21:121–132. doi:10.2478/v10001-008-0014-z

    Article  Google Scholar 

  • Kissel JC et al (2005) Comparison of organophosphorus pesticide metabolite levels in single and multiple daily urine samples collected from preschool children in Washington State. J Exp Anal Environ Epidemiol 15:164–171. doi:10.1038/sj.jea.7500384

    Article  CAS  Google Scholar 

  • Kongtip P, Nankongnab N, Woskie S, Phamonphon A, Tharnpoophasiam P, Wilaiwan K, Srasom P (2014) Organophosphate urinary metabolite levels during pregnancy, delivery and postpartum in women living in agricultural areas in Thailand. J Occup Health 55:367–375

    Article  Google Scholar 

  • Kromann P, Pradel W, Cole DC, Taipe A, Forbes GA (2011) Use of the environmental impact quotient to estimate health and environmental impacts of pesticide usage in peruvian and Ecuadorian potato production. J Environ Protect 2:581–591

    Article  Google Scholar 

  • Lentza-Rizos C (1990) Ethylenethiourea (ETU) in relation to use of ethylenebisdithiocarbamate (EBDC) fungicides. Rev Environ Contam Toxicol 115:1–37

    CAS  Google Scholar 

  • Llop S et al (2013) Prenatal and postnatal insecticide use and infant neuropsychological development in a multicenter birth cohort study. Environ Int 59:175–182. doi:10.1016/j.envint.2013.06.010

    Article  CAS  Google Scholar 

  • London L, de GS, Wesseling C, Kisting S, Rother HA, Mergler D (2002) Pesticide usage and health consequences for women in developing countries: out of sight, out of mind? Int J Occup Environ Health 8:46–59. doi:10.1179/oeh.2002.8.1.46

    Article  Google Scholar 

  • Lu C, Bravo R, Caltabiano LM, Irish RM, Weerasekera G, Barr DB (2005) The presence of dialkylphosphates in fresh fruit juices: implication for organophosphorus pesticide exposure and risk assessments. J Toxicol Environ Health Part A 68:209–227. doi:10.1080/15287390590890554

    Article  CAS  Google Scholar 

  • Lubin JH et al (2004) Epidemiologic evaluation of measurement data in the presence of detection limits. Environ Health Perspect 112:1691–1696

    Article  CAS  Google Scholar 

  • Montesano MA, Olsson AO, Kuklenyik P, Needham LL, Bradman AS, Barr DB (2007) Method for determination of acephate, methamidophos, omethoate, dimethoate, ethylenethiourea and propylenethiourea in human urine using high-performance liquid chromatography-atmospheric pressure chemical ionization tandem mass spectrometry. J Expo Sci Environ Epidemiol 17:321–330

    Article  CAS  Google Scholar 

  • National Health and Nutrition Examination Survey Data (2008) U.S. Department of Health and Human Services; Centers for Disease Control and Prevention. http://www.cdc.gov.libproxy.unm.edu/nchs/about/major/nhanes/datalink.htm Accessed 25 May 2014

  • Olsson AO et al (2004) A liquid chromatography–tandem mass spectrometry multiresidue method for quantification of specific metabolites of organophosphorus pesticides, synthetic pyrethroids, selected herbicides, and deet in human urine. Anal Chem 76:2453–2461. doi:10.1021/ac0355404

    Article  CAS  Google Scholar 

  • Orozco F, Cole DC, Munoz V, Altamirano A, Wanigaratne S, Espinosa P, Munoz F (2007) Relationships among production systems, preschool nutritional status, and pesticide-related toxicity in seven ecuadorian communities: a multi-case study approach. Food Nutr Bull 28:S247–S257

    Article  Google Scholar 

  • Orozco FA, Cole DC, Forbes G, Kroschel J, Wanigaratne S, Arica D (2009) Monitoring adherence to the international code of conduct: highly hazardous pesticides in central Andean agriculture and farmers’ rights to health. Int J Occup Environ Health 15:255–268. doi:10.1179/oeh.2009.15.3.255

    Article  CAS  Google Scholar 

  • Panganiban L, Cortes-Maramba N, Dioquino C, Suplido ML, Ho H, Francisco-Rivera A, Manglicmot-Yabes A (2004) Correlation between blood ethylenethiourea and thyroid gland disorders among banana plantation workers in the Philippines. Environ Health Perspect 112:42–45

    Article  CAS  Google Scholar 

  • Prapamontol T et al (2014) Cross validation of gas chromatography-flame photometric detection and gas chromatography-mass spectrometry methods for measuring dialkylphosphate metabolites of organophosphate pesticides in human urine. Int J Hyg Environ Health 217:554–566. doi:10.1016/j.ijheh.2013.10.005

    Article  CAS  Google Scholar 

  • Quiros-Alcala L et al (2012) Organophosphorous pesticide breakdown products in house dust and children’s urine. J Exp Sci Environ Epidemiol 22:559–568. doi:10.1038/jes.2012.46

    Article  CAS  Google Scholar 

  • Rauch SA et al (2012) Associations of prenatal exposure to organophosphate pesticide metabolites with gestational age and birth weight. Environ Health Perspect 120:1055–1060. doi:10.1289/ehp.1104615

    Article  CAS  Google Scholar 

  • Rauh VA et al (2006) Impact of prenatal chlorpyrifos exposure on neurodevelopment in the first 3 years of life among inner-city children. Pediatrics 118:E1845–E1859. doi:10.1542/peds.2006-0338

    Article  Google Scholar 

  • Reilly TJ, Smalling KL, Orlando JL, Kuivila KM (2012) Occurrence of boscalid and other Selectedfungicides in surface water and groundwater in three targeted use areas in the United States. Chemosphere 89(3):228–234

    Article  CAS  Google Scholar 

  • Ribeiro MG, Colasso CG, Monteiro PP, Pedreira Filho WR, Yonamine M (2012) Occupational safety and health practices among flower greenhouses workers from Alto Tiete region (Brazil). Sci Total Environ 416:121–126. doi:10.1016/j.scitotenv.2011.11.002

    Article  CAS  Google Scholar 

  • Rice D, Barone S (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108:511–533. doi:10.2307/3454543

    Article  Google Scholar 

  • Rosas LG, Eskenazi B (2008) Pesticides and child neurodevelopment. Curr Opin Pediatr 20:191–197. doi:10.1097/MOP.0b013e3282f60a7d

    Article  Google Scholar 

  • Sawers L (2005) Nontraditional or new traditional exports: Ecuador’s flower boom. Latin Am Res Rev 40(3):28

    Article  Google Scholar 

  • Scheuplein R, Charnley G, Dourson M (2002) Differential sensitivity of children and adults to chemical toxicity. I. Biological basis. Regul Toxicol Pharmacol 35:429–447. doi:10.1006/trph.2002.1558

    Article  CAS  Google Scholar 

  • Schutz L (2014) Survey of agricultural practices and alternatives to pesticide use to conserve water resources in the Mojanda Watershed, Ecuador. Future Food J Food Agric Soc 2:76–92

    Google Scholar 

  • Smalling KL et al (2013) Environmental fate of fungicides and other current-use pesticides in a Central California estuary. Mar Pollut Bull 73:144–153

    Article  CAS  Google Scholar 

  • Tobin J (1958) Estimation of relationships for limited dependent variables. Econometrica 26:24–36

    Article  Google Scholar 

  • Wendel de Joode van B et al (2014) Aerial application of mancozeb and urinary ethylene thiourea (ETU) concentrations among pregnant women in Costa Rica: The Infants’ Environmental Health Study (ISA). Environ Health Perspect 12(12):1321–1328

    Google Scholar 

  • Wessels D, Barr DB, Mendola P (2003) Use of biomarkers to indicate exposure of children to organophosphate pesticides: implications for a longitudinal study of children’s environmental health. Environ Health Perspect 111:1939–1946

    Article  CAS  Google Scholar 

  • Whyatt RM et al (2002) Residential pesticide use during pregnancy among a cohort of urban minority women. Environ Health Perspect 110:507–514

    Article  CAS  Google Scholar 

  • World Bank (2005) In: Aksoy MA, Behgin JC (eds) Global agricultural trade and developing countries. World Bank, Washington DC

    Google Scholar 

  • World Health Organization (1990) Public health impact of pesticides used in agriculture. WHO, Geneva

    Google Scholar 

  • Ye XB et al (2009) Levels of metabolites of organophosphate pesticides, phthalates, and bisphenol A in pooled urine specimens from pregnant women participating in the Norwegian Mother and Child Cohort Study (MoBa). Int J Hygiene Environ Health 212:481–491. doi:10.1016/j.ijheh.2009.03.004

    Article  CAS  Google Scholar 

  • Zhang Y et al (2014) Prenatal exposure to organophosphate pesticides and neurobehavioral development of neonates: a birth cohort study in Shenyang, China. PloS One 9:e88491. doi:10.1371/journal.pone.0088491

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank their consortium partners in Ecuador: Dr. William Waters, Director of the Research Institute for Health and Nutrition-Universidad de San Francisco de Quito (USFQ), and the USFQ Center for Technology Development and Transfer (USFQ-CTT). They thank their study team, including study nurse, Katty Turqueres, and field coordinator, Luis Pena, and also the staff at the Casa Campesina Cayambe, the members of the Community Advisory Board, the local community leaders, and local hospital and clinic staff, and, most of all, the study participants. Dr. Handal was supported by a National Institute of Environmental Health Sciences (NIEHS) Grant #5R21ES19285-2 and faculty field research grants from the University of New Mexico Latin American and Iberian Institute (LAII). This project also was supported in part by the Dedicated Health Research Funds from the University of New Mexico School of Medicine.

Author information

Authors and Affiliations

  1. Public Health Program, Department of Family and Community Medicine, University of New Mexico, Albuquerque, NM, 87131, USA

    Alexis J. Handal, Samantha Bear & Carolyn Greenberg

  2. Biostatistics and Epidemiology, Department of Family and Community Medicine, University of New Mexico, Albuquerque, NM, 87131, USA

    Lauren Hund

  3. College of Health Sciences, Universidad San Francisco de Quito, Cumbaya, Ecuador

    Maritza Páez

  4. Department of Environmental and Occupational Health Sciences, University of Washington, Seattle, WA, 98195, USA

    Richard A. Fenske

  5. Rollins School of Public Health, Emory University, Atlanta, GA, 30322, USA

    Dana Boyd Barr

Authors
  1. Alexis J. Handal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lauren Hund
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maritza Páez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Samantha Bear
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carolyn Greenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Richard A. Fenske
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dana Boyd Barr
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexis J. Handal.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Handal, A.J., Hund, L., Páez, M. et al. Characterization of Pesticide Exposure in a Sample of Pregnant Women in Ecuador. Arch Environ Contam Toxicol 70, 627–639 (2016). https://doi.org/10.1007/s00244-015-0217-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-015-0217-9

Keywords

Search

Navigation