The secondary exposure to pesticides among infants, children and adolescents study (ESPINA: Estudio de la exposición secundaria a plaguicidas en infantes, Niños y adolescentes)

Abstract

INTRODUCTION: Children of agricultural workers are at risk of pesticide contamination through secondary routes (e.g. take-home pathway). Animal and human studies suggest that organophosphate and carbamate pesticide intoxication in early childhood can affect childhood development but it is not clear whether secondary pesticide exposures, which tend to be chronic but in low amounts, are sufficient to affect physiologic processes and development in children. Objectives: The Secondary Exposure to Pesticides among Infants, Children and Adolescents (ESPINA) study (Spanish: Estudio de la Exposición Secundaria a Plaguicidas en Infantes,Niños y Adolescentes) evaluated the effects of secondary pesticide exposure on childhood growth and neurobehavioral development among children living in Pedro Moncayo County, Ecuador, a county with an active fresh-cut flower industry. The following hypotheses were addressed: compared to children without secondary pesticide exposure (operationalized as flower plantation worker (flower worker) cohabitation), exposed children have: 1) lower acetylcholinesterase (AChE) activity, 2) lower neurobehavioral development scores, 3) lower systolic blood pressure, 4) lower resting heart rate and 5) slower growth. METHODS: ESPINA included socio-economic, demographic and anthropometric (height and weight) information of children from 0 to 5 years of age who participated in 2004 in the Survey of Access and Demand of Health Services in the County of Pedro Moncayo (SAHS-PM 2004). Pedro Moncayo County, Pichincha, Ecuador, has one of the highest concentrations of flower plantations per capita worldwide and the flower industry employs 21% of adults of Pedro Moncayo. In 2008, ESPINA examined children, 4 to 10 years of age, who participated in the SAHS-PM 2004 and new volunteers living in the County to obtain anthropometric measurements, a neurobehavioral developmental assessment and hemoglobin concentration and AChE activity. Study Design: This study is composed of: 1) a cross-section of 2004 to assess growth, 2) a cross-section of 2008 to assess neurobehavioral development, growth, heart rate, blood pressure and blood AChE levels; and 3) a longitudinal component (2004-2008) to assess growth. RESULTS: a) Participant Characteristics: From the SAHS-PM 2004, 922 (51% female) children were included. The mean age was 2.3 y (standard deviation (SD): 1.4 y), 63% cohabited with ≥1 flower worker with a mean of 2.0 flower workers at home. In ESPINA (2008), 313 (49% female, 78% mestizo) children participated; the mean age was 6.6y (SD=1.6 y), and 55% of participants cohabited with ≥1 flower worker. Flower worker cohabitants had a mean duration of cohabitation of 5.3 years and a mean of 1.5 flower workers at home. A total of 230 (49% female, 74% mestizo) children were examined in 2004 and 2008; the mean age was 6.4 years (SD=1.4 y) and 59% cohabited with at least one flower worker. Flower worker cohabitants had a mean duration of cohabitation of 5.1 years and a mean of 1.5 flower workers at home in 2008. b) Flower worker cohabitation and AChE activity: Mean acetylcholinesterase activity was 3.14 U/ml, standard deviation (SD): 0.49. It was lower by 0.09 U/ml (95% confidence interval (CI) -0.19, -0.001) in children of flower workers (57% of participants) than non-flower workers’ children, after adjustment for gender, age, height-for-age, hemoglobin concentration, income, pesticide use within household lot, pesticide use by contiguous neighbors, examination date and residence distance to nearest flower plantation. Using a 4 level polychotomous acetylcholinesterase activity dependent variable, flower worker cohabitation (vs. not) had odds ratio 3.39 (95% CI 1.19, 9.64) for being <15th percentile compared to the highest tertile. Children cohabitating for ≥5 years (vs. never) had OR of 4.11 (95% CI: 1.17, 14.38) of AChE activity within <15th percentile compared to the highest tertile. c) Secondary Pesticide Exposure and Neurobehavioral Development: The range of scores among 13 NEPSY-II subtests was 5.9-10.9 units (SD: 2.8-4.9). Boys with AChE activity in the lowest vs. the highest tertile had adjusted odds ratios (OR) of 7.40 (95%CI 1.71-32.05), 9.39 (95%CI 2.36-37.38) and 2.35 (95%CI 1.03-5.34) of low scores (<9th percentile) of Attention and Executive Functioning Domain, inhibitory control and long term memory, respectively, after adjusting for age, gender, race, height-for-age z-score, household income, flower worker cohabitation status, maternal education, hemoglobin concentration. Children’s cohabitation with a FW (vs. not) was associated with OR of low auditory attention score of 1.63 (95%CI 0.79,-3.37). AChE and FW cohabitation were not associated with other measures of neurobehavioral development. d) Secondary Pesticide Exposure and Blood Pressure (and Heart Rate) among Children living in Agricultural Communities in Ecuador: AChE activity was directly associated with blood pressure: every U/ml decrease was associated with a mean decrease in SBP of 1.54 mmHg (95%CI -2.68, -0.40) and DBP of 1.52 mmHg (95% CI -2.55, -0.50), after adjustment for age, gender, race, height-for-age z-score, heart rate, hemoglobin concentration, income, residence distance to nearest flower plantation edge, pesticide use within household lot, pesticide use by contiguous neighbors and examination date. Flower worker cohabitation was associated with lower systolic blood pressure (SBP) by 1.79 mmHg (95%CI -3.57, -0.01). Every year of cohabitation was associated with an adjusted decrease of SBP of 0.32 mmHg (95%CI 0.02, 0.64). Further adjustment for AChE weakened these associations. Cohabitation with a flower worker was not related to diastolic blood pressure (DBP); resting heart rate was not associated with flower worker cohabitation or AChE activity. e) Secondary Pesticide Exposure and Growth Cross-sectionally in 2004 (n=853), flower worker cohabitation was not associated with growth after adjusting for demographic and socio-economic factors. Longitudinally, child cohabitation with a flower worker was associated with decreased mean BMI-for-age (-0.36 standard deviations (SD), 95% CI: -0.66, -0.06) and weight-for-age (-0.33 SD, 95% CI: -0.61, -0.05). In 2008, flower worker cohabitation and lower AChE activity (per U/ml, mean=3.13 U/ml, SD=0.49) were both associated with larger head circumference (0.37 cm, 95% CI: 0.003, 0.74 and 0.75 cm, 95% CI: 0.30, 1.19, respectively). CONCLUSIONS: a) Cohabitation with a flower worker was related to lower AChE activity in children; this supports the hypothesis that indirect pesticide exposure from flower workers suffices to depress AChE activity, with greater suppression due to longer exposure. b) Low AChE activity was associated with deficits on tasks reflecting memory, attention and inhibitory control in boys. These are critical cognitive skills that affect learning and academic performance c) Our findings reflect physiologic reactivity in children with subclinical secondary exposures to pesticides and suggest vasodilation as an important mechanism of decreased blood pressure of cholinesterase inhibitors in this population. Although lower BP in isolation might be a beneficial effect of secondary pesticide exposure, the finding needs to be viewed with caution, as part of a pattern of generally adverse physiologic responses to pesticides. d) Our findings suggest that indirect pesticide exposures (estimated by AChE activity and cohabitation with a flower worker) can affect growth and head circumference in children living in agricultural communities. RECOMMENDATIONS: Our findings support the hypothesis that take-home pesticide exposures have physiologic effects in children of flower plantations workers. This investigation reinforces the importance of reducing the amounts of pesticides introduced into the homes by agricultural workers. Interventions to reduce secondary exposures targeting flower plantation workers and their families are needed. It is important to not only educate agricultural workers to adequately handle pesticides to reduce their contamination and that of their families, but also to provide adequate infrastructure to promote healthy practices including providing sufficient showers or and washing work clothes in the plantation.