Environmental Research Section A 80, 158—164 (1999)Article ID enrs.1998.3878, available online at http://www.idealibrary.com on

Acute Health Effects Associated with Nonoccupational PesticideExposure in Rural El Salvador1

Lenore S. Azaroff* and Lucas M. Neas-

*Department of Work Environment, University of Massachusetts—Lowell, One University Avenue, Lowell, Massachusetts 01854; and-Department of Epidemiology, Harvard School of Public Health, 665 Huntington Avenue, Boston, Massachusetts 02115

Received September 26, 1997

Little is known about the health effects of nonoc-cupational pesticide exposure in agricultural com-munities of poor countries. Therefore, this studyinvestigated acute symptoms associated withnonoccupational exposure to organophosphate in-secticides (OPs) in rural El Salvador, a regionknown for intensive pesticide use. In the five com-munities studied, 2-week prevalences of severalacute symptoms were associated with living witha farmer who had recently applied methyl para-thion. These included cramps in limbs (odds ratio2.1, 95% confidence interval 1.2–3.7), chest pressure(OR 2.3, 95% CI 1.3–4.0), change in defecation (OR2.3, 95% CI 1.3–4.1), feeling dazed (OR 2.4, 95% CI1.3–4.4), and eyes tearing (OR 2.5, 95% CI 1.4–4.5).Associations were found regardless of whether theindividuals reporting the symptoms had themselvesperformed field labor. These results suggest thatliving in areas where pesticides are used on cropsmay represent an environmental health concern,especially for children. ( 1999 Academic Press

Key Words: child; environmental exposure; insec-ticides, organophosphate; methyl parathion; ruralhealth.

INTRODUCTION

Studies of nonoccupational pesticide exposurehave typically addressed pesticides used in the home

1 This work was supported by an Inter-American FoundationDoctoral Field Research Grant, a Harvard University SinclairKennedy Traveling Fellowship, a Harvard University Committeeon Latin American and Iberian Studies Summer Field ResearchFellowship, and NIH grants ES05947 and ES00002. Laboratoryspace and supplies were donated by Petros Koutrakis and P.Barry Ryan. Standard compounds were donated by Isao Saito.This study was conducted in accordance with U.S. and HarvardSchool of Public Health guidelines for the protection of humansubjects.

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0013-9351/99 $30.00Copyright ( 1999 by Academic PressAll rights of reproduction in any form reserved.

or yard, residues left on commercial foods, or sui-cides and accidents (Goldman, 1995; USNRC, 1993;Muldoon and Hodgson, 1992; Fenske et al., 1990;Immerman and Schaum, 1990; Zwiener and Gin-sburgh, 1988). However, recent findings support theconcern that nonoccupational exposure due to resi-dence in agricultural areas may have significantpublic health consequences (Simcox et al., 1995).

California residents exposed to paraquat driftfrom aerial spraying of fields half a mile away re-ported significantly increased 2-week prevalence ofcough, diarrhea, eye irritation, headache, nausea,rhinitis, throat irritation, trouble breathing, un-usual tiredness, and wheezing. The highest oddsratios (ORs) were 5.90 for diarrhea and 3.10 fornausea (Ames et al., 1993).

A study of kibbutz residents exposed to organo-phosphate pesticide spray drift near their homesfound a significant dose response relationship be-tween levels of urinary organophosphate meta-bolites and unsolicited complaints of at least onesymptom, including nausea, abdominal pain, diar-rhea, headache, and dizziness (Richter et al., 1992).

Residents of cotton-growing communities in Cali-fornia have experienced significant (60%—100%) in-creases in prevalence of symptoms associated withliving within 1 mile of cotton fields sprayed aeriallywith mixtures of organophosphates, paraquat, andother pesticides. Associated symptoms included fa-tigue, eye irritation, throat irritation, nausea, anddiarrhea (Scarborough et al., 1989).

At least four episodes of rural community expo-sure to agricultural methyl bromide and chloropicrinsoil fumigation in california were documented be-tween 1973 and 1984. In each episode, up to severaldozen residents were found to exhibit symptoms ofintoxication, including weakness, headache, eye andthroat irritation, cough, shortness of breath, nausea,and others (Goldman et al., 1987).

EFFECTS OF NONOCCUPATIONAL PESTICIDE EXPOSURE 159

Few studies have investigated the health effectson children of environmental exposure to agricul-tural pesticides, especially the neurotoxic effects oflow-level exposure (Simcox et al., 1995). However,children are thought to be liable to particularly severeacute and chronic developmental, immunological,and neurological symptoms from pesticides. In par-ticular, exposure to neurotoxins at levels that wouldbe safe for adults may cause permanent loss of brainfunction in infants and toddlers (USNRC, 1993).

Several recent studies have addressed the healtheffects of childhood exposure from pesticide use inhomes and yards. These identified positive associ-ations with childhood incidence of brain tumors,leukemias, and soft tissue sarcomas (Leiss and Sav-itz, 1995). In addition, several recent epidemiologicstudies have demonstrated increased incidence ofcancer in children exposed to agricultural pesticidesin developed countries (Moses et al., 1993). Fathers’occupational pesticide use has been found to bestrongly associated with incidence of Ewing’s bonetumors, lymphomas, and leukemia in children(Holly et al., 1992, Mulder et al., 1994).

Given that children in developed countries sufferlong-term health effects of nonoccupational pesticideexposure, it is reasonable to expect that children inpoor countries might be exposed at the greater levelsthat cause acute effects. It is widely suspected thatexposure to highly toxic compounds is of sufficientmagnitude to cause frequent illness among the poor.In many poor areas, including rural El Salvador,farmers spray acutely toxic pesticides from backpacksprayers in fields immediately bordering theirhomes, then return to their homes and yards withcontaminated skin, clothing, and equipment (Mur-ray, 1994; Calderon and Ramos, 1992; Thrupp, 1988;Copplestone, 1985; Bull, 1982; Weir and Schapiro,1981).

Poor people who are exposed to pesticides may beat greater risk of adverse health effects than weal-thier people due to lack of access to medical care andto their already compromised health status. Forexample, malnutrition and infectious disease maycontribute to the severity of symptoms among thepoor in both industrialized and poor countries (Bul-usu and Chakravarty, 1984; Chakravarty andSreedhar, 1982; Forget, 1991; Jamall and Davis,1991; WHO, 1990; Mahaffey and Vanderveen, 1979).Dehydration, whether due to inadequate fluid in-take, tropical climate, alcohol consumption, or diar-rheal disease, may also intensify symptoms (Baetjer,1983).

This study therefore aimed to test the hypothesisthat, in poor countries, farmers’ family members can

be exposed to pesticides at levels sufficient to beassociated with acute health symptoms even if theythemselves do not perform fieldwork. The researchwas performed among farmers’ families in rural ElSalvador, a country known for intensive use of high-ly toxic compounds (Castillo, 1993; Calderon andRamos, 1992; Mejıa Guerra, 1992; Lopez Zepedaet al., 1989).

MATERIALS AND METHODS

Study Population

The study population consisted of families in fiveagricultural communities served by a Salvadorannongovernmental organization, The Foundation forthe Promotion of Cooperatives (FUNPROCOOP).The residents of these villages are demographicallytypical of the mestizo (mixed Indian and European)poor rural population of El Salvador. Eligible sub-jects included all household members 8 years andolder. Subjects in three communities were system-atically selected to be representative (every secondhouse or every house along the central road). Due togreater population dispersal in two other com-munities, households there were chosen byFUNPROCOOP staff based on expected cooperation.Field work was conducted in June and July 1995.

In the three communities where households werechosen to be representative, more than 90% offamilies approached agreed to participate, and morethan 87% of eligible members of these householdsparticipated. A total of 103 households took part,comprising 358 individuals. Of these, 136 were un-der 18. Forty-two of the 136 children were reportednot to have performed fieldwork within the past2 weeks.

Of the 358 participants, 247 had complete datacollected, including biomarker presence in urine,fieldwork performed, and pesticides used by theirhousehold farmers. Data on organophosphate (OP)metabolites in urine and fieldwork performed wereavailable for 259 subjects. The first author was ableto gather only partial data (e.g., only urine samplesor only interviews on their own work) from the re-maining subjects due to the difficulty of locatingindividuals repeatedly. Prevalence of detectable OPmetabolites was not significantly different betweensubjects who were and were not interviewed (datanot shown).

Of the 80 farmers interviewed, 22 reported ap-plying methyl parathion to crops in the past 2weeks. Other commonly used pesticides included theherbicide paraquat and the OP methamidophos. Of358 urine samples analyzed, nearly half contained

160 AZAROFF AND NEAS

detectable levels of at least one alkyl phosphate (AP),indicating recent OP exposure (Dillon and Ho, 1987).These results were similar for adults and children.Further data on agricultural and household pesticideuse as well as collection and storage of urine samplesand analysis for OP metabolites are described else-where (see companion paper by Azaroff, this issue).

Surveys

An oral informed consent script was read to alladult subjects and parents of participating childrenbefore proceeding with interviews and sample collec-tion. Farmers were asked specifically about use of 14named pesticides, and to report use of other pestici-des. They were asked about use during the previous2 weeks and during the previous year. Mothers wereasked about the age and sex of household membersand the numbers of days each person had washedclothes or worked in the fields during the past2 weeks. Mothers were also asked to name pesticidesused in or near the house.

All subjects were interviewed regarding specifiedsymptoms experienced within the preceding2 weeks. Symptom surveys were based on the WorldHealth Organization questionnaire for symptoms re-lated to organophosphate exposure (WHO, 1987),with questions added to reflect paraquat-relatedsymptoms. Three symptoms not known to be asso-ciated with pesticide exposure were included forquality control purposes.

Preliminary drafts of all questionnaires wereedited by professional staff at FUNPROCOOP andthen by several rural health promoters. The sub-sequent drafts were field tested with approximately30 families in four communities and edited furtherbefore the study was conducted.

Data Analysis

All data were entered into a database constructedin EpiInfo (CDC, 1994). Data were entered twice andthe two entries cross checked for discrepancies,which were corrected by comparison with hard copy.Odds ratios (ORs) between potential predictor vari-ables and reported symptoms were identified withlogistic regression models using SAS (SAS Institute,1989). Models of reported symptoms controlled forgender, age (18, and the interaction between thesetwo variables. In all cases the reference populationfor ORs between a given predictor variable and out-come was composed of all study subjects with com-plete data for those predictor and outcome variablesand negative for the predictor.

Where nonindependence of observations withinhousehold was suspected, the EpiInfo CSAMPLEprogram was used to evaluate design effect withhousehold as the clustering variable. A design effectdiffering from 1 by more than 0.2 was found only forchange in defecation (design effect"1.67), and thisdesign effect was used to adjust the findings in thecase of this symptom.

Five symptoms similar to those found by Richterto be associated with nonoccupational OP exposurewere examined as a group: headache, nausea, stom-ach ache, dizziness, and changes in defecation (Rich-ter et al., 1992). T tests were used to compareaverage numbers of these symptoms betweengroups.

RESULTS

Acute Symptoms Associated withOccupational Exposure

Two-week prevalences of several self-reportedsymptoms were strongly associated with the interac-tion between performing fieldwork and excreting de-tectable levels of a urinary AP. These includedcoughing (OR 3.4, 95% confidence interval 1.1—10),coughing several times (OR 7.3, 95% CI 1.5—16),feeling weak or unusually tired (OR 5.0, 95% CI1.5—16), and experiencing difficulty in thinking sev-eral times (OR 5.0, 95% CI 1.6—16). The interactionof performing fieldwork with excreting specificallyethylated metabolites was associated with feelingloss of strength in hands or feet once or twice (OR 13,95% CI 2.1—118) or several times (OR 17, 95% CI2.2—368) (Table 1).

The interaction between performing fieldwork andexcreting detectable metabolite levels was asso-ciated with experiencing at least one central nervoussystem symptom (convulsions, feeling dazed/dizzy,difficulty sleeping, difficulty thinking, confusion,feeling angry for no reason, feeling sad for no reason)several times (OR 4.3, 95% CI 1.3—15). This interac-tion was also associated with experiencing at leastone muscle symptom (feeling weak, difficulty mov-ing limbs, loss of strength in limbs, trembling inhands or feet, tingling in hands or feet, leg cramps)several times (OR 8.8, 95% CI 2.5—32).

Acute Symptoms Associated withNonoccupational Exposure

Some symptoms were associated with living witha farmer who had applied methyl parathion withinthe past 2 weeks, regardless of one’s own age, gen-der, or work history. These included limb cramps

TABLE 1Associations between Apparently Occupational Exposure to Organophosphates and Acute Symptoms Reported

Outcome of interest (2-week prevalence) Predictor variablesa OR 95% CI P value

Coughing Reporting fieldwork within past 2 weeks 1.0 0.4—2.1 [0.1Detectable level of a urinary alkyl phosphate 0.5 0.2—1.3 [0.1Reporting fieldwork within past 2 weeks anddetectable level of a urinary alkyl phosphate 3.4 1.1—10 (0.05

Coughing more than twice Reporting fieldwork within past 2 weeks 0.5 0.2—1.1 (0.1Detectable level of a urinary alkyl phosphate 0.4 0.1—1.0 (0.05Reporting fieldwork within past 2 weeks anddetectable level of a urinary alkyl phosphate 7.3 1.5—16 (0.01

Feeling weak or unusually tiredmore than twice

Reporting fieldwork within past 2 weeks 1.2 0.5—2.9 [0.1Detectable level of a urinary alkyl phosphate 0.4 0.2—1.1 (0.1Reporting fieldwork within past 2 weeks anddetectable level of a urinary alkyl phosphate 5.0 1.5—16 (0.01

Difficulty thinking more than twice Reporting fieldwork within past 2 weeks 0.7 0.3—1.6 [0.1Detectable level of a urinary alkyl phosphate 0.4 0.1—0.9 (0.05Reporting fieldwork within past 2 weeks anddetectable level of a urinary alkyl phosphate 5.0 1.6—16 (0.01

Feeling loss of strength in hands or feetb Reporting fieldwork within past 2 weeks 1.4 0.7—2.9 [0.1Detectable level of an ethylated urinary alkyl phosphate 0.3 0.04—1.3 [0.1Reporting fieldwork within past 2 weeks anddetectable level of an ethylated urinary alkyl phosphate 13 2.1—118 (0.01

Feeling loss of strength in hands orfeet more than twiceb

Reporting fieldwork within past 2 weeks 1.6 0.7—3.5 [0.1Detectable level of an ethylated urinary alkyl phosphate 0.2 0.01—1.6 [0.1Reporting fieldwork within past 2 weeks anddetectable level of an ethylated urinary alkyl phosphate 17 2.2—368 (0.05

Note. n"259.a Odds ratios and significance measures obtained by including both predictor variables in logistic regression models. Models were run in

SAS using proc logistic. All models control for potential confounders gender, age (18, and interaction of gender and age (18.b n"258 for analyses of ethylated metabolites due to contamination of one sample.

EFFECTS OF NONOCCUPATIONAL PESTICIDE EXPOSURE 161

(OR 2.1, 95% CI 1.2—3.7), chest pressure (OR 2.3,1.3—4.0), change in defecation such as diarrhea orconstipation (OR 2.3, 95% CI 1.2—4.1), feelingdazed/dizzy (OR 2.4, 95% CI 1.3—4.4), and eyes tear-ing (OR 2.5, 95% CI 1.4—4.5). This exposure was alsomarginally significantly associated with difficultythinking and with stomach ache (ORs 1.7 and 1.9,P(0.1) (Table 2). Household farmer’s parathion usewas not significantly protective for any pesticide-related symptom.

Females of all ages who performed no fieldworkexperienced a significantly increased number of thefive symptoms grouped according to Richter if headhousehold farmers had applied methyl parathion tocrops within the past 2 weeks (mean number 3.4 vs.2.6 symptoms, mode 5 vs. 2, P(0.02).

The interaction between age less than 18 yearsand excreting detectable levels of ethylated metab-olites was associated with wheezing (OR 5.9, 95% CI1.0—41) and chest pain (OR 2.4, 95% CI 1.1—5.4),regardless of fieldwork performed.

The household farmer’s reported use of otheracutely toxic pesticides, including paraquat, was notassociated with reported acute symptoms. Threesymptoms not known to be associated with pesticideexposure were not found to be associated with expo-sures as measured by reported pesticide use or bio-marker levels.

DISCUSSION AND CONCLUSIONS

These data suggest that a large proportion of thestudy population, including children, experiencesacute health effects due to pesticide exposure.Prevalence of several symptoms was associated withthe interaction of field labor and excretion of OPmetabolites, suggesting occupational exposure.However, several symptoms were associated notwith fieldwork, but with living with a farmer usingmethyl parathion. This exposure was also associatedwith higher numbers of symptoms among femalesnot engaged in fieldwork.

TABLE 2Associations between Farmers’ Use of Methyl Parathion and Acute Symptoms Reported by Household Members

Outcome of interest (2-week prevalence) Predictor variablesa OR 95% CI P value

Difficulty thinking Reporting fieldwork within past 2 weeks 0.9 0.5—1.8 [0.1Parathion applied to crops within past 2 weeks 1.7 1.0—3.1 (0.1

Stomach ache Reporting fieldwork within past 2 weeks 0.8 0.4—1.7 [0.1Parathion applied to crops within past 2 weeks 1.9 1.0—3.7 (0.1

Cramps in limbs Reporting fieldwork within past 2 weeks 1.0 0.5—1.9 [0.1Parathion applied to crops within past 2 weeks 2.1 1.2—3.7 (0.05

Pressure in chest Reporting fieldwork within past 2 weeks 0.8 0.4—1.6 [0.1Parathion applied to crops within past 2 weeks 2.3 1.3—4.0 (0.01

Defecation change Reporting fieldwork within past 2 weeks 0.6 0.3—1.2 [0.1b

Parathion applied to crops within past 2 weeks 2.3 1.2—4.1 (0.01b

Feeling dazed/dizzy Reporting fieldwork within past 2 weeks 1.2 0.6—2.5 [0.1Parathion applied to crops within past 2 weeks 2.4 1.3—4.4 (0.01

Eyes tearing Reporting fieldwork within past 2 weeks 1.4 0.7—2.8 [0.1Parathion applied to crops within past 2 weeks 2.5 1.4—4.5 (0.01

Note. n"247.a Odds ratios and significance measures obtained by including both predictor variables in logistic regression models. Models were run in

SAS using proc logistic. All models control for potential confounders gender, age (18, and interaction of gender and age (18.b Corrected for design effect of clustering of defecation change within household.

162 AZAROFF AND NEAS

Although reported use of many different pestici-des was examined for association with reportedacute symptoms, only methyl parathion use produc-ed significant associations. This is consistent withthe known extreme acute toxicity of this compound.

However, associations were found between bio-markers of exposure to pesticides other than methylparathion and acute symptoms. Children excretingdetectable levels of ethylated alkyl phosphates, re-flecting exposure to ethylated compounds ratherthan the methylated methyl parathion, experiencedincreased odds of wheezing and chest pain. Thesefindings may reflect a putative link between pesti-cide exposure and asthma (Senthilselvan et al.,1992). Also, this finding suggests a potential effect ofexposure to diazinon, the ethylated organophos-phate most frequently used by farmers in this studygroup. Diazinon has been reported to produce toxico-logical effects in addition to those resulting fromacetylcholinesterase inhibition (Wagner and Or-wick, 1994, Kojima et al., 1992).

Nonoccupational pesticide exposure in the studypopulation may result from any number of exposureroutes (Simcox et al., 1995; Nigg et al., 1990).Farmers spray fields immediately bordering homesand wells, then bring home their contaminatedclothes and sprayers. Residents walk through,handle, pick, and eat recently sprayed crops. Thus,

dermal contact, respiration of drift, and ingestionmay all contribute to exposure (Plimmer, 1990). Themost significant routes of exposure could not bedetermined with the data produced by this study.

This study has several other limitations. It wascross sectional, so that putative chronic healtheffects such as cancer, birth defects, abortion, still-birth, and neurological impairment could not beexamined. Sampling of subjects was not uniformlyrepresentative. Children under 5 years, who arethought to be most at risk from environmental pesti-cide exposure due to their developing neurologicaland immune systems, were not studied for practicalreasons.

Nevertheless, the results of this study support thehypothesis that members of farmers’ families, in-cluding children, can be exposed to levels of pestici-des sufficient to be associated with acute healtheffects even if they do not perform fieldwork. It maybe expected that these findings of exposure and asso-ciated symptoms would apply more strongly to thevery young.

ACKNOWLEDGMENTS

This work was supported by an Inter-American FoundationDoctoral Field Research Grant, a Harvard University SinclairKennedy Traveling Fellowship, a Harvard University Committee

EFFECTS OF NONOCCUPATIONAL PESTICIDE EXPOSURE 163

on Latin American and Iberian Studies Summer Field ResearchFellowship, and NIH grants ES05947 and ES00002. Laboratoryspace and supplies were donated by Petros Koutrakis and P.Barry Ryan. The author thanks Isao Saito of the Aichi PrefecturalInstitute for his generous donation of alkyl phosphate standards.Logistic support and consulting were provided by the Foundationfor the Promotion of Cooperatives (FUNPROCOOP), especiallyIsrael Pineda Henrrıquez, Antonio Lemus, Fidel Angel ParadaBerrios, Nelly Susana Rivera, and David Vasquez. Field testing ofsurveys and introduction to the communities were performed bythe health promoter teams of Las Americas, El Papaturro,Marianela, Milingo, and El Barillo. All laboratory analysis wasperformed at John Clark’s Massachusetts Pesticide Analysis La-boratory at the University of Massachusetts Amherst by AndrewS. Curtis, Jeffrey Doherty, Raymond Putnam, and Gerard R. Roy.Technical support was provided by Robert Weker and J. MikhailWolfson. Comments and general support were provided by DavidChristiani.

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