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American Journal of Epidemiology Advance Access originally published online on March 10, 2007
American Journal of Epidemiology 2007 165(12):1389-1396; doi:10.1093/aje/kwm025
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American Journal of Epidemiology Copyright © 2007 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

Association of Arsenic Exposure during Pregnancy with Fetal Loss and Infant Death: A Cohort Study in Bangladesh

Anisur Rahman1,2, Marie Vahter3, Eva-Charlotte Ekström2, Mahfuzar Rahman1, Abu Haider Mohammad Golam Mustafa1, Mohammad Abdul Wahed1, Mohammed Yunus1 and Lars-Åke Persson2

1 International Centre for Diarrhoeal Disease Research, Bangladesh, Mohakhali, Dhaka, Bangladesh
2 International Maternal and Child Health, Department of Women's and Children's Health, Uppsala University, University Hospital, Uppsala, Sweden
3 Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden

Correspondence to Dr. Lars-Åke Persson, International Maternal and Child Health, Department of Women's and Children's Health, Uppsala University, University Hospital, SE-75185 Uppsala, Sweden (e-mail: lars-ake.persson{at}kbh.uu.se).

Received for publication May 9, 2006. Accepted for publication December 4, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The authors evaluated the effect of arsenic exposure on fetal and infant survival in a cohort of 29,134 pregnancies identified by the health and demographic surveillance system in Matlab, Bangladesh, in 1991–2000. Arsenic exposure, reflected by drinking water history and analysis of arsenic concentrations in tube-well water used by women during pregnancy, was assessed in a separate survey conducted in 2002–2003. Data on vital events, including pregnancy outcome and infant mortality, were collected by monthly surveillance at the household level. The risk of fetal loss and infant death in relation to arsenic exposure was estimated by a Cox proportional hazards model. Drinking tube-well water with more than 50 µg of arsenic per liter during pregnancy significantly increased the risks of fetal loss (relative risk = 1.14, 95% confidence interval: 1.04, 1.25) and infant death (relative risk = 1.17, 95% confidence interval: 1.03, 1.32). There was a significant dose response of arsenic exposure to risk of infant death (p = 0.02). Women of reproductive age should urgently be prioritized for mitigation activities where drinking water is contaminated by arsenic.

arsenic; Bangladesh; fetal death; infant; mortality; pregnancy outcome; water

Abbreviations: AsMat, health consequences of arsenic exposure in Matlab; CI, confidence interval; HDSS, health and demographic surveillance system; ICDDR,B, International Centre for Diarrhoeal Disease Research, Bangladesh; RR, relative risk


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Contamination of ground water by inorganic arsenic, a documented potent human toxicant and carcinogen, is an increasing global health concern (1–3). Many regions worldwide have ground water with elevated concentrations of arsenic (>10 µg/liter), including parts of Europe and the United States (2). Bangladesh is one of the most affected countries. Nearly 90 percent of the population drinks water from tube wells, and it has been estimated that more than a quarter of those wells have arsenic concentrations above the local standard of 50 µg/liter (4–6). Despite the facts that arsenic readily passes the human placenta (7) and that high doses of arsenic are known to cause detrimental effects on the developing fetus in various animal species (2, 8), little is known about the effects of arsenic exposure on human reproductive outcome. Human studies are needed, as there are no suitable animal models for studying arsenic toxicity (2, 9).

A few human studies are indicative of adverse effects on reproductive outcome and child health. Increased risk of spontaneous abortion, stillbirth, preterm birth, and neonatal death was suggested in two studies in Bangladesh, including 192 and 533 women, respectively (10, 11). However, exposure levels were not measured for individual pregnancies, and outcomes were assessed by recall. A recent study in West Bengal, India, indicated a pronounced effect of arsenic exposure during pregnancy on stillbirth, although with wide confidence intervals of the estimate (odds ratio = 6.07, 95 percent confidence interval (CI): 1.54, 24.0) (12). Increased spontaneous abortions and stillbirths were also reported in villages with high arsenic concentrations in drinking water in Hungary (13), but detailed information was not provided. In northern Chile, fetal, neonatal, and postneonatal mortality rates were reported to be elevated in Antofagasta, compared with Valparaiso, during a period with increased arsenic concentration (from 90 to 800 µg/liter) in the drinking water (14). All the mentioned studies were either ecologic or cross-sectional in design and had potential biases in the assessment of exposure and outcome. Therefore, within a large cohort of pregnant women, our aim was to assess the effect of individual arsenic exposure through drinking water on fetal and infant survival.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study area
The study area, Matlab, is located 53 km southeast of the capital Dhaka, in Bangladesh. Matlab is one of the areas that have been most affected by arsenic contamination of tube-well water. The International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR,B), has been running a health and demographic surveillance system (HDSS) in the area since 1966 that covers a population of about 220,000. The study area is divided into two parts. One is the ICDDR,B service area, where an extensive Maternal, Child Health, and Family Planning Program has been operating. The other is the government service area, where the population receives health services from the government facilities as in other parts of the country. Community health research workers visit every household on a monthly basis to update information on demographic events, that is, marriage, pregnancy, birth, death, and in- and outmigration, as well as to collect information on the morbidity of children below 5 years of age and of women of childbearing age. Socioeconomic information, including education and household assets, is also recorded by periodic censuses.

Study design and subjects
This cohort study used prospectively collected HDSS data on pregnancies that occurred during the period from 1991 to 2000. Information on exposure to arsenic was based on data obtained in a separate study of the health consequences of arsenic exposure in Matlab (AsMat study) performed in the HDSS area in 2002–2003 (15). Pregnant women were identified by history of missing menstrual period during the monthly home visit of community health workers. On identification of pregnancy, usually around 8 weeks of gestation, women were advised to visit their respective health facility in the area for antenatal care. Similarly, information on pregnancy outcome was collected by the monthly household surveillance. Pregnancies identified by HDSS were included in the analysis if information on drinking water history and concentration of arsenic in the tube-well water used during pregnancy was available. Out of 51,500 pregnancies, tube-well water was not used as drinking water in 5,059 (9.8 percent) pregnancies. This was mainly because of financial reasons (not being able to afford investing in a tube well) but may also include some women who preferred the taste of surface water instead of the often iron-tasting tube-well water. In total, 29,134 pregnancies qualified for analysis (figure 1). The study was approved by the ethical review committee of ICDDR,B, Dhaka, Bangladesh.


Figure 1
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  		FIGURE 1. Study participation of the pregnancy cohort based on availability of arsenic concentrations in tube-well water in Matlab, Bangladesh, 1991–2000. AsMat, health consequences of arsenic exposure in Matlab; TW, tube well.

 
Arsenic exposure assessment
In the AsMat study, teams of field workers collected information on lifetime drinking water sources for all inhabitants above 4 years of age in the study area by moving from household to household and interviewing the family members. Another team subsequently visited the area and collected water samples from all functioning tube wells for analysis of total arsenic by hydride generation atomic absorption spectrophotometry (model AA6800 spectrophotometer; Shimadzu Corporation, Kyoto, Japan) in the ICCDR,B laboratory (15). Arsenic exposure for individual pregnancies was based on the concentration of arsenic in the tube-well water used by the women during pregnancy.

Outcome and covariate information
Information on pregnancies and type of outcomes, as well as on related covariates, was obtained from the monthly updated HDSS databases. Dates of the last menstrual period and pregnancy outcome were extracted. In the HDSS, a woman is identified as pregnant if she is not having menstrual periods. Subsequently, pregnancy is confirmed, and the date and type of pregnancy outcome are recorded for all pregnancies by monthly home visits unless the women have migrated out. Early fetal loss was defined as loss of a fetus within 28 weeks of pregnancy, excluding "menstrual regulation" (vacuum aspiration within 10 weeks following a missed menstrual period) or induced abortion. Late fetal loss or stillbirth was defined as birth of a dead fetus after 28 weeks of gestation. An infant death was defined as death of a child before 12 months of age. A neonatal death was defined as death of an infant within 28 days, and a postneonatal death was defined as death of an infant after 28 days but before 12 months of age.

Data on maternal education and economic status were obtained from HDSS. Economic status was categorized into quintiles of assets based on a model relevant for assets in this rural setting (16), category 1 representing the poorest and 5 the richest. We also extracted information on women's date of birth, order of pregnancy, geographic location, locally recognized seasons, and any loss to follow-up such as outmigration of infants.

Quality control of data
The HDSS has a careful quality control system in the field and at the data entry level. Supervisors check the data by random field visits. A quality control team repeats collection of a subset of data to check for consistency. In the AsMat study, a quality control team made random controls on data collection and checked the validity of the data collected by the field workers. Information about drinking water sources was validated by use of census information collected in 1974, 1982, and 1996 that contained information on whether or not a tube well was used as a source for drinking water. This information was included on the printed forms used in the interviews for cross-checking of lifetime drinking water sources. Water samples were analyzed in duplicate for arsenic concentrations. The quality of analytical results was assured by use of standard reference materials and interlaboratory comparison of a subset of samples (15).

Statistical analysis
The risk of fetal loss and infant death in relation to arsenic exposure was estimated by a Cox proportional hazards model. Arsenic exposure was divided into quintiles, and the first quintile corresponded relatively well with the World Health Organization guideline value of 10 µg/liter (17). We also stratified by exposure levels of less than 50 and 50 or more µg/liter to determine the effect size related to the current Bangladesh drinking water standard. Covariates (mother's age at pregnancy, order of pregnancy, mother's education, socioeconomic status by asset score, six locally recognized seasons, calendar year of outcome, and mother's location according to service area) were evaluated for association with exposure and outcomes. Associations were determined by Spearman's correlation coefficient, {chi}2, or analysis of variance appropriate for the type of data being analyzed. Potential confounders, associated with exposure and outcome at a p ≤ 0.10 significance level, were identified, and those found to change the effect estimation by 5 percent or more were included in the final multivariate model. The last menstrual period date and birth date were set at time = 0 for fetal and infant survival, respectively. Follow-up was censored if an outcome event did not happen by the end of follow-up or if the child migrated out of the area.

An individual woman could contribute with more than one pregnancy to the cohort, raising the concern of ties between pregnancies and error in the estimates of effect. To adjust for multiple pregnancies in single subjects, we also evaluated the effect of arsenic exposure on fetal loss and infant death by use of logistic regression, using generalized estimating equation models.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
The mean age at pregnancy was 27 years, and about half of the pregnancy cohort consisted of illiterate women. Twenty-six percent of the pregnant women were primigravid (table 1). No woman in the study area smoked or used alcohol. The 29,134 pregnancies resulted in 2,444 fetal losses (1,615 early fetal losses and 829 late fetal losses), 1,096 induced abortions (including menstrual regulation), 850 neonatal deaths, and 523 postneonatal deaths.


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  		TABLE 1. Characteristics of the pregnant women studied, Matlab, Bangladesh, 1991–2000

 
The arsenic concentration in the drinking water used during pregnancy showed a wide variation, with a mean concentration of 239 µg/liter (median: 224 µg/liter; 10th percentile: <1 µg/liter; 90th percentile: 513 µg/liter). About 80 percent of the pregnant women used water with an arsenic concentration exceeding 10 µg/liter (table 2). It was found that, in 1,308 of 29,134 pregnancies (4.5 percent), there had been a shift in tube well from before pregnancy compared with the water source during pregnancy.


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  		TABLE 2. Concentrations of arsenic in tube-well water consumed by pregnant women, Matlab, Bangladesh, 1991–2000

 
No covariates confounded the association between arsenic exposure and fetal loss. Of the available covariates, order of pregnancy, mother's education, socioeconomic status by asset score, calendar year of outcome, and mother's location according to service area (ICDDR,B service area and government service area) were found to be associated with arsenic exposure during pregnancy as well as infant death (table 3). Calendar year of birth was found negatively associated with infant mortality, indicating a strong time trend. A marked decrease of the mean arsenic concentration in the years 1998–2000 indicated that a mitigation process had already started in the study area. Calendar year was also found to be negatively associated with gravidity and positively associated with education and asset score (data not shown). Among the available covariates, only calendar year was found to change the risk estimate of infant death due to arsenic exposure and was therefore adjusted for in the analysis.


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  		TABLE 3. Associations between background factors and infant death and arsenic exposure in the pregnancy cohort, Matlab, Bangladesh, 1991–2000

 
There was a tendency of increased risk of fetal loss for higher quintiles of water arsenic concentrations, although the increased risk was not statistically significant until the fourth quintile (table 4).


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  		TABLE 4. Risk of fetal loss in relation to arsenic exposure via tube-well water during pregnancy, Matlab, Bangladesh, 1991–2000

 
The risk of infant death increased significantly with increasing arsenic exposure during pregnancy in a dose-dependent way (plinear trend = 0.02). The adjusted risk of infant death was highest (relative risk (RR) = 1.29, 95 percent CI: 1.08, 1.53) for the group exposed to water arsenic concentrations of 276–408 µg/liter during pregnancy compared with the lowest exposure group (table 5). The results indicate that most of the risk increase already occurred at the level of the local drinking water standard (figure 2).


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  		TABLE 5. Risk of infant death in relation to arsenic exposure via tube-well water during pregnancy, Matlab, Bangladesh, 1991–2000

 

Figure 2
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  		FIGURE 2. Infant survival plot in relation to maternal exposure to arsenic during pregnancy by a Cox proportional hazards model of a cohort of pregnancies in Matlab, Bangladesh, 1991–2000. The curves represent exposure categories defined by water arsenic levels. Birth was set at time = 0. Follow-up was censored at 12 months if the outcome of interest (infant death) did not happen or at the age of outmigration, if applicable (plinear trend = 0.02).

 
We evaluated the risk of death in the neonatal and postneonatal periods, and the risk estimates were relatively homogeneous across the group (table 6). Similarly, stratification for calendar period (1991–1995 and 1996–2000) and mother's location according to service area did not modify the pattern of relative risks of infant deaths in relation to arsenic exposure (data not shown). We did not observe any difference in the risk of infant death due to arsenic exposure by gender.


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  		TABLE 6. Risk of neonatal and postneonatal death in relation to arsenic exposure among the pregnancy cohort livebirths, Matlab, Bangladesh, 1991–2000

 
If exposure was dichotomized below and above the Bangladesh local drinking water standard (<50 and ≥50 µg/liter), there was a 17 percent increased risk of infant death (RR = 1.17, 95 percent CI: 1.03, 1.32) if the mothers had been drinking water with the higher arsenic concentrations during pregnancy. With the same exposure, there was a 14 percent increase in the risk of fetal loss (RR = 1.14, 95 percent CI: 1.04, 1.25). The effect estimates for the above categories based on logistic regression with generalized estimating equations revealed almost the same results, that is, 16 percent increased risk of infant death (odds ratio = 1.16, 95 percent CI: 1.02, 1.31) and 15 percent increased risk of fetal loss (odds ratio = 1.15, 95 percent CI: 1.05, 1.26) for exposed pregnancies. Similar estimates for fetal loss and infant deaths were also observed when exposure was divided into quintiles (data not shown).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
We have provided evidence that arsenic exposure via drinking water during pregnancy increases the risk of infant death and, to a lesser extent, fetal loss. The risk estimate for fetal loss in relation to arsenic exposure was lower than those reported in previous studies in Bangladesh and West Bengal, India (10–12). However, those studies were either ecologic or cross-sectional in design and included only a few hundred women, and reproductive outcomes were collected by recall.

After clinical recognition of pregnancy, the rate of early fetal loss reportedly varies between 10 and 15 percent (18), although much lower rates have also been observed (19). These rates vary with data collection methods and are usually low if based on regular vital statistics data (20). The early pregnancy loss rate (5.8 percent) found in our study is quite similar to rates based on recalls (4.5–7 percent) (10–12). However, we might have underestimated the effect, if arsenic also caused losses at an early stage of fetal development where pregnancy was not accounted for by the monthly surveillance. It should be noted that the monthly household surveillance in Matlab most likely identifies pregnancies and pregnancy losses more efficiently than any retrospective interviews considering the data collection methods and sociocultural context of the study site. In the recent study in West Bengal, India, the association between arsenic exposure and infant mortality had a size that corresponds well with the result of our study, although the sample size and power of that study were small (odds ratio = 1.33, 95 percent CI: 0.43, 4.04) (12).

The strengths of our study are the large sample size, the collection of information on individual arsenic exposure in pregnancy, and the prospectively collected outcome data from the HDSS databases. Selection and information biases were minimized by combining outcome data from the regular monthly surveillance at the household level with exposure data from the cross-sectional survey of arsenic concentrations in all tube wells and interviews about drinking water history at the individual level. To minimize recall errors, we asked the participants to recall their drinking water history in relation to momentous life events. In addition, the data on drinking water sources were validated by use of data from previous HDSS socioeconomic censuses in which information on tube-well water use was available. Misclassification of exposure, if any, is likely to be randomly distributed.

We assume that the arsenic concentration in the tube-well water, as determined in 2002–2003, had remained similar during the study period of pregnancy outcomes in 1991–2000. Information on temporal variation in water arsenic concentrations is limited. However, repeated water analyses in an area with high water arsenic contents in drinking water were found to be fairly stable over a 3-year period (21). Further, the British Geological Survey analyzed random samples from all over the country for a 1.5-year period without showing any time trends (4). In well water in northern Argentina and western Nevada in the United States, the water arsenic concentrations remained about the same over periods of 10–20 years (22, 23). Moreover, in the study area, when following 61 randomly selected tube wells three times per year over a 3-year period, no systematic time trends could be shown (p = 0.11; unpublished data). We observed that the absolute majority (95.5 percent) had used the same tube well the year before compared with the period of pregnancy. The proportion changing water source corresponded to the general variation of water sources in society at that time.

It is known that arsenic readily passes through the placenta to the fetus but not to breast milk (24). As most women in Matlab practice breastfeeding for 12 months or more, the arsenic exposure of infants was probably limited. Therefore, the observed arsenic-associated decrease in infant survival was, most likely, an effect of prenatal exposure rather than postnatal exposure. It may be a result of compromised fetal development. Previous epidemiologic studies have suggested an association between arsenic exposure during pregnancy and low birth weight (25, 26). Arsenic was found to affect the T-cell subpopulation (helper T cells) from women ex vivo and also maturation of normal immune effector cells (27). The exact mode of action of arsenic is not known but may involve oxidative stress, interference with hormones, especially glucocorticoids and estrogen, perturbation of DNA methylation, increased telomerase activity, and modulation of signal transduction pathways (2, 28–32), all of which are important for intrauterine programming and fetal development (33, 34).

Taken together, we have shown an association between arsenic exposure via tube-well water and increased mortality in early human development. Similar risk estimates in different strata of infants (neonatal and postneonatal), calendar year, and mother's location by service area reflect the robustness of our findings. The increased risk of infant death is relevant to many countries around the world including Bangladesh, where pregnant women are exposed to arsenic through contaminated drinking water. Therefore, there is an urgent need to strengthen arsenic mitigation programs and to prioritize women in reproductive ages in that process.


   ACKNOWLEDGMENTS
 
This study was conducted at the ICDDR,B with the support of the Swedish International Development Agency (ICDDR,B GR-00123, GR-00211, GR-00212, U11 BB/1.5.5-3, 1998-05440, U11 BB/1.5.5-3/A); World Health Organization (ICDDR,B GR-00024, SE/01/037664); and the US Agency for International Development (ICDDR,B GR-00118, 388-G-00-02-00125-00). The Matlab HDSS is supported primarily by the Department for International Development (ICDDR,B GR-00210).

ICDDR,B acknowledges with gratitude the commitment of the Swedish International Development Agency, World Health Organization, US Agency for International Development, and Department for International Development to the Centre's research efforts.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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