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Journal of Occupational & Environmental Medicine:
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Association Between Congenital Anomalies and Paternal Exposure to Agricultural Pesticides Depending on Mother’s Employment Status

Ronda, Elena MPH; Regidor, Enrique MPH; García, Ana M. MPH; Domínguez, Vicente MPH

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From the Department of Public Health, Universidad de Alicante; Department of Preventive Medicine and Public Health, Universidad Complutense de Madrid; and Department of Preventive Medicine and Public Health, Universidad de Valencia, Spain.

Address correspondence to: Dr Elena Ronda. Department of Public Health, University of Alicante, Ap. Correos 99, E03080, Alicante, Spain. E-mail: elena.ronda@ua.es.

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Abstract

Objective: We analyzed the association between fetal death from congenital anomalies and paternal agricultural occupation in mothers who were employed and in housewives.

Materials and Methods: The data consist of individual records from the Spanish Birth Register (1995-1999).

Results: The adjusted relative risk of fetal death in agricultural workers compared with nonagricultural was 1.24 (95% confidence interval = 0.38- 4.02) in mothers who were employed and 1.68 (95% confidence interval = 1.03-2.73) in housewives.

Conclusion: The risk of fetal death in the offspring of agricultural workers exposed to pesticides around the time of conception was higher than in the offspring of nonagricultural workers in mothers who were housewives but not in mothers who worked outside the home.

Different studies have found an association between the exposure of women to pesticides in the first trimester of pregnancy and the occurrence of congenital anomalies in their offspring.1–5 In a previous study, we found evidence supporting the existence of an association between paternal exposure to pesticides during the first trimester of pregnancy and the risk of congenital anomalies.6 We showed that paternal agricultural work increases the risk of fetal death from congenital anomalies in fetuses conceived during periods of maximum pesticide use.

Our results did not support the mutation of germ cells in fathers caused by pesticide exposure as the pathogenic mechanism for congenital anomalies, and we pointed out the possible implication of the mother because the routes of exposure to pesticides include inhalation, absorption through the skin, contamination of the water, contamination of the husband’s clothes, ingestion of residues present in food, or a combination of all of these.7

To support this indirect maternal exposure to pesticides as the mechanism that mediates the excess risk of fetal death from congenital anomalies among the offspring of fathers exposed to pesticides in agricultural use, this study presents a new analysis of the data, which distinguishes between the wives of agricultural workers who work outside the home and those who are housewives.

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Materials and Methods

The data consist of individual records from the Stillbirth and Birth National Register of Spain for the period 1995 to 1999. This register contains information on all pregnancies in Spain ending in live birth or late fetal death, ie, stillbirth at 26 weeks or more of gestation. For legal reasons, the register also includes infant deaths within 24 hours of birth. Fetal deaths are defined as stillbirths at 26 weeks or more of gestation plus deaths in the first day of life. The variables included are year and month of birth, weeks of gestation, sex and weight of the product of conception, cause of late fetal death or of death in the first 24 hours of life, and parental information (age, marital status, mother’s and father’s occupation). Mother’s and father’s occupation are coded according to the first digit of the 1968 International Standard Classification of Occupations (ISCO). The analysis was restricted to live births and stillbirths occurring in southern and eastern Spain. During the period of study, pesticide use in these two areas represented two thirds of all pesticides used in Spain.

The mother’s employment status was classified into two categories: works outside the home-if the mother had an ISCO occupation-and housewife. In 312,975 observations, the mother worked outside the home, and in 371,595 the mother was a housewife. Fifteen percent of the observations were excluded from the analysis because of a lack of information on birth weight, weeks of gestation, or the father’s occupation. This percentage was similar in mothers who worked outside the home and in housewives. The total number of stillbirths and live births included in the study was 587,360.

For both mothers who worked outside the home and those who were housewives, we calculated the rate and relative risk of fetal death from congenital anomalies by father’s occupation—agricultural workers versus non-agricultural workers—by Poisson regression. Crude and adjusted relative risks were estimated. We first calculated the rate and relative risk of fetal death in fetuses conceived between April and September, which is the period of highest use of pesticides in agriculture. We then calculated the rate and relative risk of fetal death in fetuses conceived during the rest of the year. The month of conception was estimated based on the data available on weeks of gestation and month of birth.

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Results

Table 1 shows the rate and relative risk of fetal death from congenital anomalies according to father’s occupation and mother’s economic activity by period of conception. The adjusted relative risk of fetal death in agricultural workers compared with nonagricultural workers among births conceived between April and September was 1.24 (95% confidence interval [CI] = 0.38-4.02) in mothers who worked outside the home and 1.68 (95% CI = 1.03-2.73) in housewives. The adjusted relative risk of fetal death in agricultural workers compared with nonagricultural workers among births conceived during the rest of the year was 0.53 (95% CI = 0.07-3.86) in mothers who worked outside the home and 0.88 (95% CI = 0.47-1.64) in housewives. In both periods the rate of fetal death from congenital anomalies was higher in the offspring of housewives.

Table 1
Table 1
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Discussion

The results of this analysis show an association between paternal exposure to pesticides in agricultural workers around the time of conception and risk of fetal death from congenital anomalies in mothers who were housewives, but not in mothers who worked outside the home. These findings suggest that the association observed in the previous study between paternal exposure to pesticides in agricultural workers and the development of congenital anomalies is due to the large percentage of the wives of agricultural workers who are housewives. Only 26% of the wives of agricultural workers worked outside the home, as compared with 52% of the wives of non-agricultural workers.

A probable mechanism mediating the excess risk of congenital anomalies in the offspring of fathers exposed to agricultural pesticides around the time of conception could be maternal exposure to pesticides. Because agricultural workers usually live in the same area where they farm,8 housewives inhale or absorb through the skin a larger amount of pesticides than the wives of agricultural workers who work outside the home. This probably occurs because housewives are likely to have more prolonged contact with their husbands’ contaminated clothes and with work equipment stored at home than wives who work outside the home. Some evidence exists of “para-occupational” exposures in workers’ family members when toxic substances are carried home. Children living with pesticide applicators have been shown to present higher urinary levels of organophosphorus metabolites than reference children in the same community.9 This mechanism is consistent with studies that have found a relation between proximity of maternal residence to pesticide applications in the first trimester of pregnancy and the appearance of congenital anomalies.3–5

One limitation of this study could be the measure of pesticide use. Although it is an ecologic measure, the estimate of the results by time period minimizes this disadvantage. In fact, the rate of fetal death is similar in nonagricultural workers in the two periods, whereas in agricultural workers it is higher in the period of greatest pesticide use. Another limitation of this study is the possibility of uncontrolled confounding to impact these results, that is to say, it is not possible exclude the exposition to other potential risk factors to congenital malformations other than pesticides during spraying season.

In addition, one risk factor for fetal death that was not taken into account in this study is smoking. Although women who work outside the home smoke more than housewives, the percentage is unlikely to differ by husband’s occupation and is highly unlikely to differ in the two time periods studied.

Another important finding of this study, although not one of its objectives, is the higher risk of fetal death from congenital anomalies in housewives than in mothers who work outside the home. Higher perinatal mortality has been described in non-employed mothers than in those who are employed.10 In the future, it will be necessary to ascertain the causes of the excess risk of fetal and perinatal death in housewives if this excess risk varies depending on the cause of fetal and perinatal deaths.

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References

1. García AM, Fletcher T, Benavides FG, Orts E. Parental agricultural work and selected congenital malformations. Am J Epidemiol. 1999;149:64–74.

2. Nurminen T, Rantala K, Kurppa K, Holmberg PC. Agricultural work during pregnancy and selected malformations in Finland. Epidemiology. 1995;6:23–30.

3. Pastore LM, Hertz-Piccioto I, Beaumont JJ. Risk of stillbirth from occupational and residential exposures. Occup Environ Med. 1997;54:511–18.

4. Zang J, Cai WW, Lee DJ. Occupational hazards and pregnancy outcomes. Am J Ind Med. 1992;21:397–408.

5. Bell EM, Hertz-Piccioto I, Beaumont JJ. A case-control study of pesticides and fetal death due to congenital anomalies. Epidemiology. 2001;12:148–156.

6. Regidor E, Ronda E, García AM, Domínguez V. Paternal exposure to agricultural pesticides and cause-specific fetal death. Occup Environ Med. 2004;61:334–339.

7. Rowland AS. Pesticides and birth defects. Epidemiology. 1995;6:6–7.

8. Gómez C, González JJ, Sancho R. Identidad y profesión en la agricultura familiar. Madrid: CIS;1999.

9. Loewenherz C, Fenske RA, Simcox NJ, Bellamy G, Kalman D. Biological monitoring of organophosphorus pesticide exposure among children of agricultural workers in Central Washington State. Environ Health Perspect. 1997;105:1344–53.

10. Murphy FF, Dauncey M, Newcombe R. Employment in pregnancy: prevalence, maternal characteristics, perinatal outcome. Lancet. 1984;1:1163–1166.

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