American Journal of Epidemiology Advance Access originally published online on March 8, 2006
American Journal of Epidemiology 2006 163(7):662-669; doi:10.1093/aje/kwj089
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Original Contribution |
Pregnancy Outcomes, Infant Mortality, and Arsenic in Drinking Water in West Bengal, India
1 School of Public Health, University of California, Berkeley, CA
2 Institute for Postgraduate Medical Education and Research, Kolkata, India
3 Division of Environmental and Occupational Disease Control, California Department of Health Services, Oakland, CA
4 Research and Evaluation, Kaiser Permanente Southern California, Pasadena, CA
5 School of Public Health and Community Medicine, University of Washington, Seattle, WA
Reprint requests to Dr. Allan H. Smith, Arsenic Health Effects Research Program, University of California School of Public Health, 140 Warren Hall, Berkeley, CA 94720-7360 (e-mail: ahsmith{at}berkeley.edu).
Received for publication July 25, 2005. Accepted for publication November 7, 2005.
| ABSTRACT |
|---|
|
|
|---|
Between 2001 and 2003, the authors studied pregnancy outcomes and infant mortality among 202 married women in West Bengal, India. Reproductive histories were ascertained using structured interviews. Arsenic exposure during each pregnancy, including all water sources used, was assessed; this involved measurements from 409 wells. Odds ratios for spontaneous abortion, stillbirth, neonatal mortality, and infant mortality were estimated with logistic regression based on the method of generalized estimating equations. Exposure to high concentrations of arsenic (
200 µg/liter) during pregnancy was associated with a sixfold increased risk of stillbirth after adjustment for potential confounders (odds ratio (OR) = 6.07, 95% confidence interval (CI): 1.54, 24.0; p = 0.01). Arsenic-related skin lesions were found in 12 women who had a substantially increased risk of stillbirth (OR = 13.1, 95% CI: 3.17, 54.0; p = 0.002). The odds ratio for neonatal death was 2.81 (95% CI: 0.73, 10.8). No association was found between arsenic exposure and spontaneous abortion (OR = 1.01, 95% CI: 0.38, 2.70) or overall infant mortality (OR = 1.33, 95% CI: 0.43, 4.04). This study adds to the limited evidence that exposure to high concentrations of arsenic during pregnancy increases the risk of stillbirth. However, there was no indication of the increased rates of spontaneous abortion and overall infant mortality that have been reported in some studies.
arsenic; India; infant mortality; pregnancy outcomes; stillbirth; water pollutants
Abbreviations: CI, confidence interval; GEE, generalized estimating equations; OR, odds ratio
| INTRODUCTION |
|---|
|
|
|---|
Worldwide, millions of people are currently drinking groundwater that contains inorganic arsenic in concentrations above 10 µg/liter, the US Environmental Protection Agency maximum contaminant level and the standard recommended by the World Health Organization (1
Health effects associated with long-term consumption of arsenic-contaminated water include cancers of the bladder, kidney, lung, and skin (9
12
), as well as chronic nonmalignant conditions, the most frequently observed being characteristic skin lesions (13
, 14
). Although recently more attention has been focused on the reproductive health effects of arsenic, the findings are still inconclusive (15
20
). A few investigations have related arsenic concentrations above 50 µg/liter in drinking water to increased risks of spontaneous abortion, stillbirth, preterm delivery, and infant mortality (15
19
). In Taiwan and Chile, average birth weight was lower in regions with increased arsenic in drinking water (18
, 21
). Recently, one study from Bangladesh suggested that increases in spontaneous abortion, stillbirth, and neonatal death rates were associated with levels of arsenic in drinking water greater than 50 µg/liter (22
).
We conducted a study of the relation of arsenic exposure during pregnancy to pregnancy outcome and infant mortality among 202 married women in West Bengal, India. To our knowledge, this was the first pregnancy-outcome study of drinking-water arsenic considering spontaneous abortion, stillbirth, and infant mortality that employed detailed interviews concerning all drinking-water sources used during each pregnancy and had water measurements from the majority of them.
| MATERIALS AND METHODS |
|---|
|
|
|---|
Study design and selection of participants
This study was carried out between 2001 and 2003. Women were selected on the basis of a 19951996 cross-sectional survey of 7,683 people conducted in 21 villages in West Bengal, India (South 24-Parganas district) (23
The details of participant selection are somewhat complex, because the study was conducted in parallel with a study of chronic respiratory disease. In the respiratory disease study, groups of "high-exposure" and "low-exposure" participants were identified from the cross-sectional survey conducted in 19951996. In the respiratory disease study, all participants from the 19951996 survey who had drinking-water arsenic concentrations greater than 400 µg/liter and also showed signs of arsenic-caused skin lesions were selected for the "high-exposure" group. Participants placed in the "low-exposure" group in the respiratory disease study had drinking water containing less than 50 µg/liter of arsenic and were not found to have arsenic-caused skin lesions. For each "high-exposure" participant, a "low-exposure" participant was randomly selected, matched by age (within 5 years) and gender.
For the pregnancy outcome study, we selected participants from the chronic respiratory disease study to obtain high- and low-exposure groups in the following manner. If a participant in the respiratory disease study was a married woman in the age range 2040 years, she was invited to participate in the pregnancy study. If not, married women in the same household or close female neighbors who had drunk the same water in 19951996 and were currently aged 2040 years were invited to participate. In general, the pregnancy study participants were daughters-in-law, wives, or (occasionally) close neighbors of the respiratory disease study participants who were using the same tube wells for drinking water.
We identified and approached 205 eligible women matching the selection criteria. Informed consent was obtained from all subjects. The study was approved by the institutional review boards of the Institute of Postgraduate Medical Research and Education (Kolkata, India) and the University of California, Berkeley (Berkeley, California).
Interviews
In-depth face-to-face structured interviews were conducted in the participants' homes by a female physician who was blind to the water concentrations of arsenic in tube wells used by participants during their pregnancies. We assessed reproductive histories in detail, including each pregnancy and its outcome, identifying spontaneous abortions, therapeutic abortions, stillbirths, livebirths, and neonatal and infant deaths. The interview also included probing with different wording and the use of contextual questions to trigger participants' memories; for example, participants were asked about "miscarriages" and missed menstrual periods and the duration of time intervals without menstrual periods. The correct timing of events was assessed using milestones such as the assassination of former Prime Minister Indira Gandhi. Information from birth certificates, if available, was recorded. Residential and job history, lifetime smoking history, and demographic variables, including education and type of housing material (mud, mixed, or concrete), were assessed. Dietary intake was also assessed but is not discussed in this paper.
Physical examination for skin lesions
Following the assessment of reproductive history, a careful examination of the skin was conducted by a trained field physician in a well-lit area outdoors under natural light. Visible or palpable dermal lesions were documented, with the field physician noting the location and appearance and whether the patterns were characteristic of arsenic-induced skin toxicity. Lesions were classified by the field physician into one of four categories: definitely, probably, possibly, or not related to arsenic.
Exposure assessment
The field team collected water samples from all functioning tube wells that had been used by participants for at least 6 months since their first pregnancy. Some wells had been closed because of damaged filters or other mechanical problems or because they were known to have arsenic contamination. When available, such measurements were incorporated into data analysis. For many of these closed tube wells, we located past arsenic concentration measurements obtained before the wells were closed (n = 48). We collected samples from 361 functioning tube wells in the 21 villages in the study region. Private tube wells were sometimes used by just one household, whereas government tube wells were used by multiple families. Water samples were stored in a cooler containing an ice block and transported to the laboratory in Kolkata on the same day. The water samples were then kept frozen at 20°C until they were analyzed. Total water arsenic level was measured by flow injection analysis using atomic fluorescence detection with in-line photooxidation and continuous hydride generation (24
). The lower limit of quantification was less than 1 µg/liter. We provided the results of drinking-water arsenic measurements to the women and their families.
Statistical analyses
Women's histories of arsenic exposure since their first pregnancy were constructed on the basis of information about tube well usage at each residence and work site, if applicable, and the results of the arsenic measurements. A few participants reported that they had, at times, used surface pond water for drinking. Because concentrations of arsenic in pond test samples were very low or nondetectable (ranging from less than 0.2 µg/liter to 4.2 µg/liter), we used zero as the concentration for all pond water sources. Annual average water arsenic concentrations were first calculated for participants for each calendar year on the basis of measured concentrations in each tube well used in that year and the fraction of their drinking water participants had obtained from the respective source in that year (e.g., 75 percent from one tube well and 25 percent from another tube well). Arsenic exposure during each pregnancy was then calculated using the annual averages, weighting them for the time fraction of each pregnancy period that fell into a particular calendar year. For livebirths, average arsenic levels were calculated likewise for the first 12 months of life or until the month of death if the child died within this time period. Pregnancies and first-year-of-life periods with no exposure information were excluded from further analyses. The arsenic value was unknown for fractions of 11 prenatal time periods and two first-year-of-life time periods, so for those time periods, the known average arsenic value of the remaining time period was applied.
Reproductive and other characteristics of the study population were first assessed in univariate analyses. The associations between prenatal arsenic exposure (in categories: 049 µg/liter, 50199 µg/liter, and
200 µg/liter) and adverse pregnancy outcomes (spontaneous abortion and stillbirth), neonatal death (death occurring in the first month after birth), and infant death (death occurring in the first 12 months of life) were assessed in stratified analyses using chi-squared tests. The stratification of arsenic at 50 µg/liter was chosen because this was the drinking water standard in India, and the stratification at 200 µg/liter was chosen to achieve sufficient numbers in the first stratum above the drinking water standard. We additionally assessed infant mortality in relation to drinking-water arsenic concentration during the first 12 months of life (or until the month of the child's death). We also compared the frequencies of adverse outcomes according to whether or not the mother had arsenic-caused skin lesions. The denominator used for calculating the rate of spontaneous abortion was all pregnancies; that used for calculation of stillbirths was all livebirths plus stillbirths; and that used for calculation of neonatal death and infant death was all livebirths.
For further evaluation of the association between adverse pregnancy outcomes, infant mortality, and prenatal and first-year-of-life (for infant mortality) arsenic exposure, we used logistic regression models based on the method of generalized estimating equations (GEE) to calculate crude and adjusted odds ratios with 95 percent confidence intervals, accounting for multiple pregnancies in the same subject (25
). Pregnancies and first-year-of-life periods for which there was no exposure information were excluded from the regression analysis. Indicator variables were used for the different arsenic exposure categories. After univariate analyses, all potentially confounding factors for which we had data were included in the full multivariate models. Potentially confounding factors were known risk factors for the outcomes or factors, such as socioeconomic status, that might reasonably be assumed to be related to the outcomes. The full models included mother's age at the child's birth, body mass index (weight (kg)/height (m)2), maternal education, education of the head of the household (no formal education, primary school, secondary school or higher), and type of housing material (mud, brick, mixed materials) as a measure of socioeconomic status. We also evaluated smoking status and occupational history. Smoking was not included in the model, because only one woman reported ever smoking; occupational history was not included either, because only one woman reported ever having had a job other than homemaker.
There were only 12 women with skin lesions, so crude GEE-based odds ratios were estimated for their adverse outcomes, and Fisher's exact test was used to assess significance. All p values shown are two-sided. All data analyses were carried out using the SAS statistical program (version 8.0e; SAS Institute, Inc., Cary, North Carolina).
| RESULTS |
|---|
|
|
|---|
Of the 205 women who were identified and approached, 203 (99 percent) agreed to participate in the pregnancy study. One woman was excluded from the analyses of reproductive outcomes because she reported having had no pregnancies. General and reproductive characteristics of the study population are summarized in table 1. Approximately 32 percent of the women reported having one or two pregnancies; more than half of the women reported having three or four pregnancies; and 16 percent reported having five or more pregnancies. Complete information about arsenic concentrations in the drinking water used during pregnancy was obtained for 633 of the 660 pregnancies (95.9 percent). For an additional 11 of the 660 pregnancies, arsenic values were available for part of the pregnancy period. Similarly, complete information on arsenic exposure was obtained for the first year of life for 522 of 540 livebirths (96.7 percent), with partial information being available for two additional livebirths. The average prenatal concentration of arsenic in drinking water was 101.7 µg/liter, with 18.2 percent of pregnant women being exposed to levels greater than or equal to 200 µg/liter (table 2).
|
|
In the GEE-based logistic regression models, increased concentrations of arsenic in drinking water during pregnancy were related to an almost fivefold increase in risk of stillbirth at the highest exposure level of
200 µg/liter in comparison with levels below 50 µg/liter. Further adjustment for socioeconomic variables, mother's age at child's birth, and body mass index led to an adjusted odds ratio for stillbirth of 6.07 (95 percent confidence interval (CI): 1.54, 24.0; p = 0.01). No increase in risk of stillbirth was seen at levels between 50 µg/liter and 199 µg/liter (adjusted odds ratio (OR) = 0.80, 95 percent CI: 0.10, 6.66). The risk of neonatal death was increased more than twofold at exposure levels of
200 µg/liter compared with levels below 50 µg/liter after adjustment for potential confounders, but the confidence interval was wide and included unity (OR = 2.81, 95 percent CI: 0.73, 10.8). An association between arsenic and spontaneous abortion was not found (adjusted OR = 1.01, 95 percent CI: 0.38, 2.70). No increase in overall infant mortality was seen with prenatal arsenic exposure (table 3) or exposure during the first year of life (data not shown). Disentangling prenatal arsenic exposure and arsenic exposure during the first 12 months of life was difficult, since water sources generally did not change directly after birth.
|
Separately, we analyzed the associations between mothers' arsenic-related skin lesions and adverse outcomes (table 4). Using the GEE-based regression model, the risk of stillbirth was substantially elevated among all pregnancies in mothers who had arsenic-related skin lesions (OR = 14.4, 95 percent CI: 3.59, 58.1; p < 0.001). Removing multiple stillbirths in the same woman by considering the number of women who had ever had a stillbirth similarly demonstrated increased risks (OR = 13.1, 95 percent CI: 3.17, 54.0; p = 0.002). Further adjustment could not be carried out because of the small numbers of women with skin lesions. No effect on spontaneous abortion was seen, and no neonatal deaths occurred among women with skin lesions. Furthermore, the presence of skin lesions was not associated with overall infant mortality when we compared numbers of deaths among all livebirths in mothers with (2/43) and without (19/497) skin lesions (OR = 1.23, 95 percent CI: 0.20, 7.62). Both recorded deaths of infants of mothers with skin lesions occurred during the postneonatal period. Considering only this period, an increase in risk was seen (2/43 vs. 7/497; OR = 3.42, 95 percent CI: 0.5, 23.0), but the confidence interval was very wide.
|
| DISCUSSION |
|---|
|
|
|---|
We investigated the association of pregnancy outcomes and infant mortality with arsenic exposure during pregnancy and during the 12 months after birth in a highly arsenic-affected area in West Bengal, India. We found a sixfold increase in risk of stillbirth at high arsenic levels of
200 µg/liter, after adjusting for socioeconomic variables and other potential confounders. Women with arsenic-related skin lesions had a 13 times' higher risk of ever having a stillbirth than women without skin lesions, although the number of women was small (n = 12). Weaker effects were seen for neonatal death, while no association with arsenic concentrations was found for spontaneous abortion or overall infant mortality prenatally or during the 12 months after birth.
Only a few investigators have considered pregnancy outcomes and infant death in relation to arsenic levels in drinking water (15
17
, 19
, 22
), and so far none of these studies have individually assessed arsenic concentrations in all water sources used during each pregnancy in relation to spontaneous abortion, stillbirth, and infant mortality. Recently, a study conducted in Bangladesh showed an increased risk of stillbirth for women with current arsenic levels greater than 100 µg/liter, although the risk estimates (OR = 2.9, 95 percent CI: 1.5, 5.9) were smaller than those in our study. The authors further reported effects for spontaneous abortion, which we did not see in our study in West Bengal (OR = 2.5, 95 percent CI: 1.5, 4.4) (22
). No information on arsenic exposure during pregnancy was available, and high exposure levels of
200 µg/liter were not considered separately in that study. One earlier cross-sectional study from Bangladesh compared rates of spontaneous abortion, stillbirth, and preterm delivery between 96 women in one village who were exposed to more than 100 µg/liter of arsenic with rates among 96 women in another village who were exposed to less than 20 µg/liter, and found that rates were 23 times higher among exposed women (15
). Both Bangladeshi studies reported a relation to overall duration of women's exposure without taking into account exposure during the actual time period of their pregnancies (15
, 22
). Neonatal death risks were investigated only in the recent study by Milton et al. (22
), who found risks similar to those observed in our study. In an ecologic study carried out in Chile, stillbirths (rate ratio = 1.7, 95 percent CI: 1.5, 1.9) and neonatal and postneonatal infant mortality were found to be increased in the high-arsenic-exposure city of Antofagasta as compared with the low-exposure city of Valparaiso (16
).
In rural West Bengal, no medical records on adverse pregnancy outcomes and infant deaths are available. Therefore, self-reported reproductive histories are the only source of information. The reliability of retrospectively assessed reproductive histories depends on the completeness of mothers' reports and the accuracy of their recall and reporting of dates. Women in rural West Bengal do not necessarily have accurate information on the timing of past events in relation to calendar years, but other important events are recalled accurately. Our questionnaire-based interview involved the use of salient events as milestones, such as the death of Indira Gandhi, which is a significant date for all Indians and can be used as a memory anchor as well as for determining the timing of events.
In contrast to wells in Bangladesh, wells in West Bengal have not been color-marked (red) for high arsenic exposure. The women had little information about their drinking-water arsenic exposure currently or earlier in life; therefore, self-reports are highly unlikely to have been differentially related to exposure in our study. We assessed detailed exposure histories of women considering all water sources used for at least 6 months since their first pregnancy, allowing the determination of exposure levels during the months of each pregnancy. If differential recall bias had been operating, overreporting of all considered adverse pregnancy outcomes would have occurred. Spontaneous abortions are much more susceptible to recall bias than discrete events known to the whole family and neighbors, such as a stillbirth. However, we did not find an association between spontaneous abortion and arsenic, which further supports the notion that differential recall was not operating and cannot account for the large effect estimate we found for stillbirth.
In an earlier study from Argentina, Concha et al. (26
) reported that breastfeeding protected infants from high levels of arsenic in drinking water. We found no difference in risk of infant mortality between first-year-of-life arsenic exposure and prenatal arsenic exposure. Unfortunately, we did not have adequate data on breastfeeding with which to assess breastfeeding in this analysis.
In most countries, non-livebirths are underascertained in surveys and medical assessments (27
). The incidence rates for neonatal mortality (22.2 per 1,000 livebirths) and infant mortality (38.9 per 1,000 livebirths) overall were lower in our study than rates reported for rural West Bengal in the Indian National Family Health Survey for the time period 19941998 (27
). The ratio of neonatal mortality to overall infant mortality in our study was 0.57, which was slightly lower than the rate of 0.69 reported in the Indian National Family Health Survey. Rates of reported spontaneous abortion and stillbirth were somewhat higher in our study (45.5 per 1,000 livebirths and 32.3 per 1,000 livebirths, respectively) than in the Indian National Family Health Survey (40 per 1,000 livebirths and 18 per 1,000 livebirths, respectively) (27
), potentially reflecting the effect of arsenic in our study area, but lower than the rates reported from an arsenic-affected area in Bangladesh (22
).
Because of the small number of women with skin lesions (n = 12), we could not reasonably adjust the estimates for any other variable; related findings are limited and must be interpreted cautiously, as indicated by the wide 95 percent confidence intervals. Although women with skin lesions were older at the time of the interview (median age, 37 years) than women without skin lesions (median age, 31 years), this difference is unlikely to have biased the estimates towards higher risks of stillbirth, since all stillbirths in our study were reported at maternal ages below 30 years; no difference in age was found between exposed and unexposed women or according to skin lesion status. For the purpose of this analysis, we defined arsenic-related skin lesions on the basis of the field physician's diagnosis as "definitely," "probably," or "possibly" due to arsenic exposure. Findings did not change if we excluded from the analyses those subjects with "possibly" arsenic-related skin lesions.
The reproductive toxicity of inorganic arsenic has been well documented in many animal studies, usually after very few high doses (28
32
). Arsenic metabolites have been found in umbilical cord blood and the placenta (33
). The biologic effect mechanism by which arsenic may affect the developing fetus is still unclear, and whether differences in arsenic methylation during pregnancy may be related to particular susceptibility of the fetus to arsenic is unknown.
In conclusion, we observed pronounced effects of drinking-water arsenic on stillbirth rates at relatively high concentrations, with an approximately sixfold risk increase; and although numbers were small, women with arsenic-related skin lesions appeared to be especially at risk. There was little evidence for other adverse pregnancy outcomes or increased infant mortality. The findings concerning stillbirth need to be confirmed, ideally in a prospective pregnancy study, but the existing evidence warrants preventive actions designed to reduce the exposure of childbearing-age women in regions with high levels of arsenic in water.
| ACKNOWLEDGMENTS |
|---|
This study was supported by award SSA/INDQ/00003082 from the United Nations Children's Fund (New York, New York); grant P42 ES04705 from the US National Institute of Environmental Health Sciences (Research Triangle Park, North Carolina); the University of California Center for Occupational and Environmental Health (Berkeley, California); and grant D43 TW00815 from the Fogarty International Center, US National Institutes of Health (Bethesda, Maryland).
Conflict of interest: none declared.
| References |
|---|
|
|
|---|
- Frost FJ, Muller T, Petersen HV, et al. Identifying US populations for the study of health effects related to drinking water arsenic. J Expo Anal Environ Epidemiol 2003;13:2319.[CrossRef][Web of Science][Medline]
- Ayotte JD, Montgomery DL, Flanagan SM, et al. Arsenic in groundwater in eastern New England: occurrence, controls, and human health implications. Environ Sci Technol 2003;37:207583.[Medline]
- World Health Organization. Guidelines for drinking-water quality. Geneva, Switzerland: World Health Organization, 2004.
- Nordstrom DK. Public health. Worldwide occurrences of arsenic in ground water. Science 2002;296:21435.
[Abstract/Free Full Text] - United Nations Children's Fund. Plan of action to combat situation arising out of arsenic contamination in drinking water: plan to assist government of West Bengal. New York, NY: United Nation Children's Fund, 1998.
- Bagla P, Kaiser J. India's spreading health crisis draws global arsenic experts. Science 1996;274:1745.[CrossRef][Web of Science][Medline]
- Khan AW, Ahmed SK, Sayed MH, et al. Arsenic contamination in ground water and its effect on human health with particular reference to Bangladesh. J Prev Soc Med 1997;16:6573.
- Chakraborti D, Mukherjee SC, Pati S, et al. Arsenic groundwater contamination in Middle Ganga Plain, Bihar, India: a future danger? Environ Health Perspect 2003;111:1194201.[Web of Science][Medline]
- Chen CJ, Chen CW, Wu MM, et al. Cancer potential in liver, lung, bladder and kidney due to ingested inorganic arsenic in drinking water. Br J Cancer 1992;66:88892.[Web of Science][Medline]
- Tsuda T, Babazono A, Yamamoto E, et al. Ingested arsenic and internal cancer: a historical cohort study followed for 33 years. Am J Epidemiol 1995;141:198209.
[Abstract/Free Full Text] - Hopenhayn-Rich C, Biggs ML, Smith AH. Lung and kidney cancer mortality associated with arsenic in drinking water in Cordoba, Argentina. Int J Epidemiol 1998;27:5619.
[Abstract/Free Full Text] - Smith AH, Goycolea M, Haque R, et al. Marked increase in bladder and lung cancer mortality in a region of northern Chile due to arsenic in drinking water. Am J Epidemiol 1998;147:6609.
[Abstract/Free Full Text] - Haque R, Mazumder DN, Samanta S, et al. Arsenic in drinking water and skin lesions: dose-response data from West Bengal, India. Epidemiology 2003;14:17482.[CrossRef][Web of Science][Medline]
- National Research Council, National Academy of Sciences. Arsenic in drinking water: 2001 update. Washington, DC: National Academy Press, 2001.
- Ahmad SA, Sayed MH, Barua S, et al. Arsenic in drinking water and pregnancy outcomes. Environ Health Perspect 2001;109:62931.[Web of Science][Medline]
- Hopenhayn-Rich C, Browning SR, Hertz-Picciotto I, et al. Chronic arsenic exposure and risk of infant mortality in two areas of Chile. Environ Health Perspect 2000;108:66773.[Web of Science][Medline]
- Borzsonyi M, Bereczky A, Rudnai P, et al. Epidemiological studies on human subjects exposed to arsenic in drinking water in southeast Hungary. Arch Toxicol 1992;66:778.[CrossRef][Web of Science][Medline]
- Yang CY, Chang CC, Tsai SS, et al. Arsenic in drinking water and adverse pregnancy outcome in an arseniasis-endemic area in northeastern Taiwan. Environ Res 2003;91:2934.[Medline]
- Aschengrau A, Zierler S, Cohen A. Quality of community drinking water and the occurrence of spontaneous abortion. Arch Environ Health 1989;44:28390.[Web of Science][Medline]
- Ihrig MM, Shalat SL, Baynes C. A hospital-based case-control study of stillbirths and environmental exposure to arsenic using an atmospheric dispersion model linked to a geographical information system. Epidemiology 1998;9:2904.[CrossRef][Web of Science][Medline]
- Hopenhayn C, Ferreccio C, Browning SR, et al. Arsenic exposure from drinking water and birth weight. Epidemiology 2003;14:593602.[CrossRef][Web of Science][Medline]
- Milton AH, Smith WP, Rahman B, et al. Chronic arsenic exposure and adverse pregnancy outcomes in Bangladesh. Epidemiology 2005;16:826.[CrossRef][Web of Science][Medline]
- Mazumder DN, Das Gupta J, Santra A, et al. Chronic arsenic toxicity in West Bengalthe worst calamity in the world. J Indian Med Assoc 1998;96:47, 18.[Medline]
- Atallah RH, Kalman DA. On-line photo-oxidation for the determination of organoarsenic compounds by atomic-absorption spectrometry with continuous arsine generation. Talanta 1991;38:16773.[CrossRef]
- Liang KY, Zeger SL. Longitudinal data analysis using generalized linear models. Biometrika 1986;73:1322.
[Abstract/Free Full Text] - Concha G, Vogler G, Nermell B, et al. Low-level arsenic excretion in breast milk of native Andean women exposed to high levels of arsenic in the drinking water. Int Arch Occup Environ Health 1998;71:426.[CrossRef][Web of Science][Medline]
- International Institute for Population Sciences and Macro International, Inc. National Family Health Survey (NFHS-2), India, 199899: West Bengal. Mumbai, India and Washington, DC: International Institute for Population Sciences and Macro International, Inc, 2001.
- Golub MS, Macintosh MS, Baumrind N. Developmental and reproductive toxicity of inorganic arsenic: animal studies and human concerns. J Toxicol Environ Health B Crit Rev 1998;1:199241.[Web of Science][Medline]
- Golub MS. Maternal toxicity and the identification of inorganic arsenic as a developmental toxicant. Reprod Toxicol 1994;8:28395.[CrossRef][Web of Science][Medline]
- Holson JF, Stump DG, Clevidence KJ, et al. Evaluation of the prenatal developmental toxicity of orally administered arsenic trioxide in rats. Food Chem Toxicol 2000;38:45966.[CrossRef][Web of Science][Medline]
- DeSesso JM, Jacobson CF, Scialli AR, et al. An assessment of the developmental toxicity of inorganic arsenic. Reprod Toxicol 1998;12:385433.[CrossRef][Web of Science][Medline]
- Lindgren A, Danielsson BR, Dencker L, et al. Embryotoxicity of arsenite and arsenate: distribution in pregnant mice and monkeys and effects on embryonic cells in vitro. Acta Pharmacol Toxicol (Copenh) 1984;54:31120.[Medline]
- Concha G, Vogler G, Lezcano D, et al. Exposure to inorganic arsenic metabolites during early human development. Toxicol Sci 1998;44:18590.
[Abstract/Free Full Text]
This article has been cited by other articles:
![]() |
A. Rahman, M. Vahter, A. H. Smith, B. Nermell, M. Yunus, S. El Arifeen, L.-A. Persson, and E.-C. Ekstrom Arsenic Exposure During Pregnancy and Size at Birth: A Prospective Cohort Study in Bangladesh Am. J. Epidemiol., February 1, 2009; 169(3): 304 - 312. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. P. Stillerman, D. R. Mattison, L. C. Giudice, and T. J. Woodruff Environmental Exposures and Adverse Pregnancy Outcomes: A Review of the Science Reproductive Sciences, September 1, 2008; 15(7): 631 - 650. [Abstract] [PDF] |
||||
![]() |
D. Mondal, A. Hegan, L. Rodriguez-Lado, M. Banerjee, A. K. Giri, and D. A. Polya Multiple regression analysis of As ground-water hazard and assessment of As-attributable human health risks in Chakdha Block, West Bengal Mineralogical Magazine, February 1, 2008; 72(1): 461 - 465. [Full Text] [PDF] |
||||
![]() |
K. Kordas, B. Lonnerdal, and R. J. Stoltzfus Interactions between Nutrition and Environmental Exposures: Effects on Health Outcomes in Women and Children J. Nutr., December 1, 2007; 137(12): 2794 - 2797. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Marshall, C. Ferreccio, Y. Yuan, M. N. Bates, C. Steinmaus, S. Selvin, J. Liaw, and A. H. Smith Fifty-Year Study of Lung and Bladder Cancer Mortality in Chile Related to Arsenic in Drinking Water J Natl Cancer Inst, June 20, 2007; 99(12): 920 - 928. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Rahman, M. Vahter, E.-C. Ekstrom, M. Rahman, A. H. M. Golam Mustafa, M. A. Wahed, M. Yunus, and L.-A. Persson Association of Arsenic Exposure during Pregnancy with Fetal Loss and Infant Death: A Cohort Study in Bangladesh Am. J. Epidemiol., June 15, 2007; 165(12): 1389 - 1396. [Abstract] [Full Text] [PDF] |
||||
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
, West Bengal, India, 20012003



