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Agricultural-related chemical exposures, season of conception, and risk of gastroschisis in Washington State

      Objective

      We sought to determine if periconceptional exposure to agrichemicals was associated with the development of gastroschisis.

      Study Design

      We conducted a retrospective, case-controlled study using Washington State Birth Certificate and US Geological Survey databases. Cases included all live-born singleton infants with gastroschisis. Distance between a woman's residence and site of elevated exposure to agrichemicals was calculated. Multivariate regression was used to estimate the association between surface water concentrations of agrichemicals and the risk of gastroschisis.

      Results

      Eight hundred five cases and 3616 control subjects were identified. Gastroschisis occurred more frequently among those who resided <25 km from a site of high atrazine concentration (odds ratio, 1.6). Risk was related inversely to the distance between the maternal residence and the closest toxic atrazine site. In multivariate analysis, nulliparity, tobacco use, and spring conception remained significant predictive factors for gastroschisis.

      Conclusion

      Maternal exposure to surface water atrazine is associated with fetal gastroschisis, particularly in spring conceptions.

      Key words

      The prevalence of gastroschisis has more than doubled over the last 30 years. Teratogens, organic chemicals, solvents, and cyclooxygenase inhibitors that are specifically related to the agricultural industry may be associated with the increased prevelance.
      • Heinig J.
      • Steinhard R.
      • Witteler R.
      • Schmitz R.
      • Kiesel L.
      • Klockenbusch W.
      Is there a seasonal variation in the frequency of gastroschisis?.
      • Saada J.
      • Oury J.F.
      • Vuillard E.
      • et al.
      Gastroschisis.
      • Mastroiacovo P.
      • Lisi A.
      • Castilla E.E.
      The incidence of gastroschisis: research urgently needs resources.
      • Loane M.
      • Dolk H.
      • Bradbury I.
      Increasing prevalence of gastroschisis in Europe 1980-2002: a phenomenon restricted to younger mothers?.
      • Root E.D.
      • Meyer R.E.
      • Emch M.E.
      Evidence of localized clustering of gastroschisis births in North Carolina, 1999-2004.
      • Collins S.R.
      • Griffin M.R.
      • Arbogast P.G.
      • et al.
      The rising prevalence of gastroschisis and omphalocele in Tennessee.
      Atrazine is an organic compound from the triazine family that is used mainly as a herbicide. It is used to stop the spread of weeds among agricultural crops.
      • Villanueva C.M.
      • Durand G.
      • Coutté M.B.
      • Chevrier C.
      • Cordier S.
      Atrazine in municipal drinking water and risk of low birth weight, preterm delivery, and small-for-gestational-age status.
      It does not tend to bioaccumulate in the environment, but its relative persistence (half-life of 35-125 days), especially in surface ground water, increases one's exposure. Animal data have shown that atrazine has embryotoxic and embryolethal effects in rodents. Furthermore in wildlife, male frogs that are exposed to water that has been polluted with atrazine at levels of >0.1 μg/L show hermaphroditism and retarded gonadal development because of its endocrine disrupting activity.
      • Villanueva C.M.
      • Durand G.
      • Coutté M.B.
      • Chevrier C.
      • Cordier S.
      Atrazine in municipal drinking water and risk of low birth weight, preterm delivery, and small-for-gestational-age status.
      In humans, atrazine can act as an endocrine-disrupting compound with effects on the central nervous system, the endocrine system, and the immune system. 2,4-Dichlorophenoxyacetic acid, a synthetic plant growth regulator, is the most widely used herbicide in the world. Nitrate, another agrichemical, is a salt of nitric acid and, in humans, is metabolized to ammonia that ultimately can lead to the dangerous condition of methameglobinemia. Nitrite, another nitric acid salt, is used frequently for curing meats because it prevents bacterial overgrowth.
      • Winchester P.D.
      • Huskins J.
      • Ying J.
      Agrichemicals in surface water and birth defects in the United States.
      • Manassaram D.M.
      • Backer L.C.
      • Moll D.M.
      A review of nitrates in drinking water: maternal exposure and adverse reproductive and developmental outcomes.
      • García A.M.
      Occupational exposure to pesticides and congenital malformations: a review of mechanisms, methods, and results.
      See related editorial, page 207
      Washington State has >80,000 live births with 2400-3200 reported defects annually. On average, there are 43 cases of gastroschisis in Washington State per year. The economy of eastern Washington counties is predominately agricultural; overall this industry employs >170,000 persons, which is 3% of the total state population.
      Washington State Department of Health
      Washington State Birth Defects Surveillance System, 1995-2004.
      April, aside from the winter months, has the highest mean monthly precipitation in Washington State according to the Western Regional Climate Center. Also, April is the month of highest atrazine use.
      Western Regional Climate Center
      Desert Research Institute.
      We hypothesized that an increased exposure in utero to herbicides is associated with the development of fetal gastroschisis. To test this hypothesis, we performed a retrospective, case-control study of pregnancies with and without gastroschisis and evaluated their periconceptional and first-trimester maternal exposure to atrazine and other agricultural chemicals.

      Materials and Methods

      We used Washington State birth certificate data that were linked with hospital discharge information from all nonfederal hospitals in the Comprehensive Hospital Abstract Reporting System in Washington State. Subjects were selected from all singleton live births in Washington State between 1987 and 2006. Birth records were linked with publicly available data from the United States Geological Survey Data on surface water concentrations of atrazine, 2,4-dichlorophenoxyacetic acid, nitrites, and nitrates in Washington State from 2001-2006. The Institutional Review Board of the Department of Social and Health Services of the State of Washington approved the study.
      Data were collected from the Comprehensive Hospital Abstract Reporting System file with the ICD-9 code 756.7 (gastroschisis) or 54.71 (abdominal wall defect repair). Cases included all deliveries of singleton infants with gastroschisis, excluding those cases with coexisting chromosomal anomalies, known genetic syndromes, fetal deaths, and no documented zip code at the time of delivery. Before 2003, abdominal wall defects, gastroschisis, and omphalocele had the same ICD-9 code. Taking this into account, once cases were identified, we increased the accuracy of the diagnosis by performing a brief review of the patients' hospitalization charts and outpatient records. We made study inclusion decisions based on the combination of ICD-9 codes and clinical evidence, including the results of amniocentesis, fetal echocardiograms, and the descriptive findings at the time of delivery.
      Control subjects were selected randomly from all Washington State singleton live births in a ratio of 4 controls per case and frequency matched to cases by year of birth. Gestational age was determined by maternal last menstrual period and calculated in weeks of gestation. Month of last menstrual period was used as a proxy for the time of conception.
      We collected information on parental demographic characteristics and maternal lifestyle characteristics from the birth certificate database to include age, race, smoking, and county of residence at the time of birth, longitude and latitude of primary residence during pregnancy, years of education, and occupation. Parental occupations were recorded in free text format on the birth certificate in response to the question “indicate type of work done during last year” and mutually exclusively categorized as agricultural, unemployed, <18 years old, and nonagricultural (all other occupations).
      The data for herbicide exposure were extracted from the Washington State Department of Agriculture database.
      USGS Washington Water Science Center
      Washington State Department of Agriculture.
      We obtained annual surface water concentrations by season of atrazine, nitrates, nitrites, and 2,4-dichlorophenoxyacetic acid from established sites in Washington State and calculated the average concentration for each site between 2001 and 2006. Data for Washington State are collected by the US Geological Survey, which operates 390 data collection sites. Surface water data were not available for the entire study population period; thus, we limited data to include 5 years. Then, we calculated the distance between each woman's residence using longitude and latitude of her known zip code and the closest geographic site of increased exposure to each of the individual agrichemicals with the use of the Haversine formula, which is an equation important in navigation that calculates great-circle distances between 2 points on a sphere from their longitudes and latitudes. High chemical exposure concentrations in surface water were defined according to the Environmental Protection Agency standards. The exposure limit for atrazine was >3 μg/L, for nitrates was >10 mg/L, for nitrites was >1 mg/L, and for 2,4-dichlorophenoxyacetic acid was >70 μg/L. Spring was defined as March, April, and May.
      Characteristics, exposures, and outcomes for cases and control subjects were compared with the use of the Student t test and χ2 test. Multivariate logistic and linear regressions were used to calculate odds ratios (ORs) and 95% confidence intervals (CIs) to evaluate the excess risk of gastroschisis that was associated with increased surface water levels of each agrichemical; adjustment was made for confounders and known risk factors that included age, parity, tobacco use, season of conception, and log transformed distance from exposure. The season of conception was compared for the cases with the use of the Mann-Whitney test. All statistical analyses were performed with statistical software (version 10; Stata Corporation, College Station, TX).

      Results

      We identified 805 cases and 3616 control subjects who met the inclusion criteria, for a total study population of 4421 infants who were born in Washington State between January 1, 1987, and December 31, 2006 (Table 1). We excluded 215 cases from the original population because of additional anomalies and genetic aneuploidy, which is a clinical diagnosis of omphalocele, and those cases with missing address information. We excluded 464 control subjects based on the same criteria. Within the case population, nulliparity, young maternal age, and tobacco use were associated significantly with gastroschisis. There was no difference between groups when we compared season of conception.
      TABLE 1Characteristics of the study population by case control status (n = 4421)
      CharacteristicGastroschisis status
      Cases (n = 805)Control subjects (n = 3616)P value
      Maternal age, y
      Data are presented as mean ± SD for continuous variables;
      24.4 ± 6.2 (13–45)27.4 ± 6.0 (13–46)< .001
      Married, n (%)439 (55)2606 (72)< .001
      Maternal race, n (%).005
       White584 (73)2746 (76)
       Black34 (4)129 (4)
       Asian49 (6)260 (7)
       Hispanic86 (11)342 (9)
       Native American32 (4)70 (2)
       Missing20 (2)69 (2)
      Maternal education, n (%)< .001
       ≤12 y386 (48)1309 (36)
       >12 y214 (27)1432 (40)
       Missing205 (25)875 (24)
      Nulliparity, n441 (55)1508 (42)< .001
      Smoked during pregnancy, n (%)182 (23)554 (15)< .001
      Income, $
      Data are given as median (interquartile range).
      36,204 (28,819–45,969)38,941 (30,780–50,544)< .001
      Paternal age, y
      Data are presented as mean ± SD for continuous variables;
      27.3 ± 6.930.3 ± 6.5< .001
      Season of conception, n (%).13
       Winter165 (21)797 (22)
       Spring171 (21)715 (20)
       Summer151 (19)843 (23)
       Fall168 (21)818 (23)
       Missing150 (19)443 (12)
      Gestational age, wk
      Data are presented as mean ± SD for continuous variables;
      36.6 ± 2.939.1 ± 1.7< .001
       Missing, n (%)74 (9)345 (10)
      Birthweight, g
      Data are presented as mean ± SD for continuous variables;
      2786 ± 7793444 ± 550< .001
       Missing, n (%)22 (3)11 (<1%)
      Male sex, n (%)443 (55)1886 (52).14
      Waller. Gastroschisis risk in Washington State. Am J Obstet Gynecol 2010.
      a Data are presented as mean ± SD for continuous variables;
      b Data are given as median (interquartile range).
      The association between agrichemical exposure and gastroschisis was determined by multivariate logistic regression. Each agrichemical was tested in a separate model, and all models were adjusted for maternal age, parity, and smoking status. Gastroschisis occurred more frequently among infants whose mothers resided <25 km from a site of high surface water contamination with atrazine (OR, 1.6; 95% CI, 1.1–2.3). Women who resided within 25-50 km of surface water sites with atrazine concentrations >3μg/L showed an increased risk as well (OR, 1.4; 95% CI, 1.2–1.7; Table 2). The risk of gastroschisis was related inversely to the distance between maternal residence and the closest increased atrazine site (P = .049) when distance was evaluated as a continuous variable (log scale). There was no associated increased risk for women who lived within 50 km of sites with increased concentrations of nitrates, nitrites, or 2,4-dichlorophenoxyacetic acid in this population.
      TABLE 2Logistic regression analysis for gastroschisis development (n = 4421)
      VariableOdds ratio (95% CI)P value
      High atrazine (>3 μg/L)
       <25 km1.60 (1.10–2.34).014
       25-50 km1.41 (1.19–1.66)< .001
       >50 km1.00 (Reference)
      High nitrate (>10 mg/L)
       <10 km0.79 (0.33–1.94)NS
       10-25 km1.17 (0.62–2.19)NS
       25-50 km1.10 (0.73–1.65)NS
       >50 km1.00 (Reference)
      High nitrite (>1 mg/L)
       <10 km0.83 (0.34–2.03)NS
       10-25 km1.13 (0.61–2.12)NS
       25-50 km1.10 (0.73–1.65)NS
       >50 km1.00 (Reference)
      High 2,4-dichlorophenoxyacetic acid (>70 μg/L)
       <10 km1.05 (0.81–1.37)NS
       10-25 km0.96 (0.77–1.21)NS
       25-50 km1.03 (0.86–1.25)NS
       >50 km1.00 (Reference)
      CI, confidence interval; NS, not significant.
      Each chemical was tested in separate model, and all models were adjusted for maternal age, parity, and smoking status. Risk estimate could not be calculated because there were no cases in this group (12 control subjects, 0 cases).
      Waller. Gastroschisis risk in Washington State. Am J Obstet Gynecol 2010.
      We observed a seasonal variation in the prevalence of gastroschisis, with a peak during spring conception (March-May; OR, 1.2; 95% CI, 1.1–1.5; Table 3). In multivariate analysis, nulliparity, tobacco use, and spring conception remained significant predictive factors for gastroschisis, as has been reported previously in the literature (Table 4). There was a trend toward a decreased risk of gastroschisis with increased distance from sites of higher atrazine concentrations.
      TABLE 3Odds of gastroschisis by season of conception (n = 3828)
      Time periodOdds ratio (95% CI)P value
      Month of conception
       January1.00 (Reference)
       February0.92 (0.60–1.43).72
       March1.00 (0.65–1.54)> .99
       April1.39 (0.92–2.11).12
       May1.11 (0.72–1.71).64
       June0.88 (0.58–1.36).57
       July0.91 (0.59–1.36).66
       August0.83 (0.54–1.29).40
       September1.34 (0.89–2.00).16
       October0.94 (0.60–1.45).77
       November0.71 (0.46–1.10).12
       December0.98 (0.65–1.48).94
      Season of conception
       Winter1.00 (Reference)
       Spring
      March, April, May.
      1.19 (0.94–1.52).15
       Summer0.90 (0.70–1.15).40
       Fall1.00 (0.79–1.29).94
      Spring conception (vs all other months)1.23 (1.01–1.50).039
      Month of conception and season of conception were tested in separate models; both models were adjusted for maternal age, parity, and smoking status.
      CI, confidence interval.
      Waller. Gastroschisis risk in Washington State. Am J Obstet Gynecol 2010.
      a March, April, May.
      TABLE 4Multivariate model for spring conception and atrazine exposure (n = 3828)
      VariableOdds ratio (95% CI)P value
      Maternal age0.92 (0.90–0.93)< .001
      Nulliparity1.20 (1.00–1.44).051
      Smoking during pregnancy1.34 (1.08–1.66).008
      Spring conception1.24 (1.01–1.51).036
      Distance to high atrazine site (log)0.80 (0.63–1.01).059
      CI, confidence interval.
      Waller. Gastroschisis risk in Washington State. Am J Obstet Gynecol 2010.

      Comment

      An increased prevalence of gastroschisis has been acknowledged around the world. The incidence of gastroschisis varies from 1-5 per 10,000 live births in the United States, depending on geographic location and is similar in male and female fetuses.
      • Mastroiacovo P.
      • Lisi A.
      • Castilla E.E.
      The incidence of gastroschisis: research urgently needs resources.
      • Loane M.
      • Dolk H.
      • Bradbury I.
      Increasing prevalence of gastroschisis in Europe 1980-2002: a phenomenon restricted to younger mothers?.
      The variation in prevalence is related primarily to maternal age and geographic location.
      • Martin R.W.
      Screening for fetal abdominal wall defects.
      Washington State has up to 2.2 times the number of observed to expected cases of gastroschisis, compared with US vital statistics.
      • Goldbaum G.
      • Daling J.
      • Milham S.
      Risk factors for gastroschisis.
      Our results indicate that exposure to elevated surface water atrazine concentrations possibly is associated with this increased prevalence, especially when conception occurs in the spring.
      In the early 1980s, several European studies saw a seasonal trend in the rates of gastroschisis.
      • Paulozzi L.
      • Milham S.
      Seasonality of omphalocele in Washington State.
      In 1990, Goldbaum et al
      • Goldbaum G.
      • Daling J.
      • Milham S.
      Risk factors for gastroschisis.
      suggested that unidentified environmental exposures may explain higher rates of gastroschisis during various seasons of the year. Then in 2007, Mattrix et al
      • Mattrix K.D.
      • Winchester P.D.
      • Scherer L.R.
      Incidence of abdominal wall defects is related to surface water atrazine and nitrate levels.
      found a positive correlation of abdominal wall defects and atrazine levels and a trend toward an increased prevalence with nitrite exposure in Indiana. This was later confirmed by researchers in Puerto Rico; however, researchers in Germany did not observe this trend in a retrospective database analysis.
      • Manassaram D.M.
      • Backer L.C.
      • Moll D.M.
      A review of nitrates in drinking water: maternal exposure and adverse reproductive and developmental outcomes.
      • de la Vega A.
      • López-Cepero R.
      Seasonal variations in the incidence of some congenital anomalies in Puerto Rico based on the timing of conception P R Health Sci J 2009;28:121-5.
      This study was limited by identifying only 17 cases.
      • Manassaram D.M.
      • Backer L.C.
      • Moll D.M.
      A review of nitrates in drinking water: maternal exposure and adverse reproductive and developmental outcomes.
      Finally in 2008, Winchester et al8 concluded that elevations in agrichemicals are highest between April and July of each year, which correlates with higher rates of anomalous fetuses who were conceived during the same period. The association between agrichemical exposure, seasonal variation, and increased risk of gastroschisis is consistent with previous studies. Our results endorse these findings, with a clear trend towards an increase in the rates of gastroschisis in the springtime. At this time, we do not have a clear understanding of the smaller peak that was seen in the fall season. It may be due to the need for increased drinking water in early fall and thus increased exposure. However, it may also be due to other agrichemicals or even a combination of various chemicals that accumulate over the course of a growing season.
      There exists retrospective evidence in today's literature that links agrichemical exposure in pregnancy to a remarkable increase in various birth defects. In 2006, the Centers for Disease Control and Prevention and the National Centers for Environmental Health examined the effects of nitrates on maternal health and found that there was moderate evidence within the animal literature that links exposure to increased rates of fetal loss, neonatal death, and developmental delay.
      • Manassaram D.M.
      • Backer L.C.
      • Moll D.M.
      A review of nitrates in drinking water: maternal exposure and adverse reproductive and developmental outcomes.
      Then in 2009, researchers in Indiana reexamined this hypothesis and found a statistically significant correlation between birth defects in 11 of 22 categories, nitrates, and time of conception.
      • Winchester P.D.
      • Huskins J.
      • Ying J.
      Agrichemicals in surface water and birth defects in the United States.
      Most recently, Lasserre et al
      • Lasserre J.P.
      • Fack F.
      • Revets D.
      • et al.
      Effects of the endocrine disruptors atrazine and PCB 153 on the protein expression of MCF-7 human cells.
      examined the proteomic effects of atrazine and found an 88% down-regulation of proteins when exposed the function of which primarily surrounds oxidative stress. We found that the prevalence of gastroschisis was increased during periods of high atrazine use. It is well-known by the agricultural industry that atrazine's herbicidal effects are maximized during the rainy season; thus, spring application is common and correlates with our observation of the highest rates of gastroschisis with spring conception.
      Birth certificate data can be a valuable resource for the analysis of maternal and child health issues; however, the retrospective nature of these records may be a limiting factor for the interpretation of the results that are obtained. It can have missing values that we encountered in our evaluation of conception and gestational age at delivery (20%) and that we observed in 25% of our case population who lacked address data. Also, it is well-known that relocation frequently occurs; therefore, documented residence at the periconceptional time may not be accurate. Furthermore, in our study, gastroschisis did not have an individual ICD-9 code before 2003 in Washington State. We adjusted for this issue by making study inclusion decisions based on the combination of ICD-9 codes and clinical evidence that was included within the birth record data that included the mode of delivery and additional anomalies. However, we may have included or even excluded a certain number of cases in our analyses because of this issue. The database has been used for multiple other retrospective analysis but has not been validated. The provision of birth certificate data is a complex and variable process that has undergone many changes in the last 20 years. General guidance is provided to the hospitals for data collection, but their own procedures and circumstances may take precedence. Finally, limitations arise from the means for which exposure was assessed. We used surface water concentrations of atrazine as a surrogate for maternal exposure; however, exposure to such herbicides can come from absorption and inhalation as well. In addition, most of a pregnant woman's exposure may come from outside of her primary residence, such as near her place of employment, which could not be evaluated with the available data.
      This study redemonstrates the observable association between exposure to agrichemicals that are used frequently by the agricultural industry and the development of gastroschisis during the periconceptional time. Further research must be carried out to define the acceptable limitations of exposure and to assess the effects of these chemicals on the development of other fetal anomalies.

      Acknowledgments

      We thank the Washington State Department of Health for providing the data and Beth Mueller and Mr Bill O'Brien for their assistance with the project.

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      Linked Article

      • Latest research from the 2010 meeting of the Society for Maternal-Fetal Medicine
        American Journal of Obstetrics & GynecologyVol. 202Issue 3
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          This month's issue includes 8 articles that describe research presented at the 2010 meeting of the Society for Maternal-Fetal Medicine (SMFM) in Chicago on February 4-6. From 1256 abstracts submitted, 86 were selected by the Society for oral presentation. Authors of these 86 abstracts were invited to submit their manuscripts through the “Fast-Track” process, in which AJOG reviewers provided rapid reviews in time to allow revision to meet the deadline for inclusion in this issue. These fast-track articles are easily identified by the checkered racing flags on the first page of each as well as next to their titles in the Contents section.
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      • Correction: March 2010 (vol. 202, no. 3, page 241)
        American Journal of Obstetrics & GynecologyVol. 203Issue 2
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          The authors of a research paper describing associations between atrazine exposure and fetal gastroschisis (Waller SA, Paul K, Peterson SE, Hitti J. Agricultural-related chemical exposures, season of conception, and risk of gastroschisis in Washington State. Am J Obstet Gynecol 2010;202:241.e1-6) wish to correct 2 errors.
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