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      Arsenic is associated with reduced effect of folic acid in myelomeningocele prevention: a case control study in Bangladesh

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          Abstract

          Background

          Arsenic induces neural tube defects in several animal models, but its potential to cause neural tube defects in humans is unknown. Our objective was to investigate the associations between maternal arsenic exposure, periconceptional folic acid supplementation, and risk of posterior neural tube defect (myelomeningocele) among a highly exposed population in rural Bangladesh.

          Methods

          We performed a case–control study that recruited physician-confirmed cases from community health clinics served by Dhaka Community Hospital in Bangladesh, as well as local health facilities that treat children with myelomeningocele. Controls were selected from pregnancy registries in the same areas. Maternal arsenic exposure was estimated from drinking water samples taken from wells used during the first trimester of pregnancy. Periconceptional folic acid use was ascertained by self-report, and maternal folate status was further assessed by plasma folate levels measured at the time of the study visit.

          Results

          Fifty-seven cases of myelomeningocele were identified along with 55 controls. A significant interaction was observed between drinking water inorganic arsenic and periconceptional folic acid use. As drinking water inorganic arsenic concentrations increased from 1 to 25 μg/L, the estimated protective effect of folic acid use declined (OR 0.22 to 1.03), and was not protective at higher concentrations of arsenic. No main effect of arsenic exposure on myelomeningocele risk was identified.

          Conclusions

          Our study found a significant interaction between drinking water inorganic arsenic concentration from wells used during the first trimester of pregnancy and reported intake of periconceptional folic acid supplements. Results suggest that environmental arsenic exposure reduces the effectiveness of folic acid supplementation in preventing myelomeningocele.

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          Most cited references41

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          Effect of community-based newborn-care intervention package implemented through two service-delivery strategies in Sylhet district, Bangladesh: a cluster-randomised controlled trial.

          Neonatal mortality accounts for a high proportion of deaths in children under the age of 5 years in Bangladesh. Therefore the project for advancing the health of newborns and mothers (Projahnmo) implemented a community-based intervention package through government and non-government organisation infrastructures to reduce neonatal mortality. In Sylhet district, 24 clusters (with a population of about 20 000 each) were randomly assigned in equal numbers to one of two intervention arms or to the comparison arm. Because of the study design, masking was not feasible. All married women of reproductive age (15-49 years) were eligible to participate. In the home-care arm, female community health workers (one per 4000 population) identified pregnant women, made two antenatal home visits to promote birth and newborn-care preparedness, made postnatal home visits to assess newborns on the first, third, and seventh days of birth, and referred or treated sick neonates. In the community-care arm, birth and newborn-care preparedness and careseeking from qualified providers were promoted solely through group sessions held by female and male community mobilisers. The primary outcome was reduction in neonatal mortality. Analysis was by intention to treat. The study is registered with ClinicalTrials.gov, number 00198705. The number of clusters per arm was eight. The number of participants was 36059, 40159, and 37598 in the home-care, community-care, and comparison arms, respectively, with 14 769, 16 325, and 15 350 livebirths, respectively. In the last 6 months of the 30-month intervention, neonatal mortality rates were 29.2 per 1000, 45.2 per 1000, and 43.5 per 1000 in the home-care, community-care, and comparison arms, respectively. Neonatal mortality was reduced in the home-care arm by 34% (adjusted relative risk 0.66; 95% CI 0.47-0.93) during the last 6 months versus that in the comparison arm. No mortality reduction was noted in the community-care arm (0.95; 0.69-1.31). A home-care strategy to promote an integrated package of preventive and curative newborn care is effective in reducing neonatal mortality in communities with a weak health system, low health-care use, and high neonatal mortality.
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            Neurology of the newborn.

            J Volpe (1980)
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              Updated Estimates of Neural Tube Defects Prevented by Mandatory Folic Acid Fortification — United States, 1995–2011

              In 1992, the U.S. Public Health Service recommended that all women capable of becoming pregnant consume 400 μg of folic acid daily to prevent neural tube defects (NTDs) (1). NTDs are major birth defects of the brain and spine that occur early in pregnancy as a result of improper closure of the embryonic neural tube, which can lead to death or varying degrees of disability. The two most common NTDs are anencephaly and spina bifida. Beginning in 1998, the United States mandated fortification of enriched cereal grain products with 140 μg of folic acid per 100 g (2). Immediately after mandatory fortification, the birth prevalence of NTD cases declined. Fortification was estimated to avert approximately 1,000 NTD-affected pregnancies annually (2,3). To provide updated estimates of the birth prevalence of NTDs in the period after introduction of mandatory folic acid fortification (i.e., the post-fortification period), data from 19 population-based birth defects surveillance programs in the United States, covering the years 1999–2011, were examined. After the initial decrease, NTD birth prevalence during the post-fortification period has remained relatively stable. The number of births occurring annually without NTDs that would otherwise have been affected is approximately 1,326 (95% confidence interval = 1,122–1,531). Mandatory folic acid fortification remains an effective public health intervention. There remain opportunities for prevention among women with lower folic acid intakes, especially among Hispanic women, to further reduce the prevalence of NTDs in the United States. In August 2014, a total of 19 population-based birth defects surveillance programs in the United States reported to CDC the number of cases of spina bifida (International Classification of Diseases, 9th Revision, Clinical Modification codes 741.0 and 741.9) and anencephaly (codes 740.0–740.1) among deliveries occurring during 1995–2011 among non-Hispanic whites, non-Hispanic blacks, and Hispanics, as well as all racial/ethnic groups combined. Surveillance programs were grouped by whether they systematically conducted prenatal ascertainment to capture diagnosed cases (eight sites: Arkansas, Georgia, Iowa, New York, Oklahoma, Puerto Rico, South Carolina, and Utah) or did not (11 sites: Arizona, California, Colorado, Illinois, Kentucky, Maryland, New Jersey, North Carolina, Texas, West Virginia, and Wisconsin). Programs with prenatal ascertainment monitored birth defects among live births, stillbirths, and elective terminations, and included collection of information from prenatal sources, such as prenatal diagnostic facilities. The birth prevalences of spina bifida, anencephaly, and both NTDs combined were estimated as the total number of cases divided by the total number of live births during the pre-fortification (1995–1996) and post-fortification periods (1999–2011). These prevalence estimates were multiplied by the average number of live births in the United States for the selected periods to estimate the annual number of NTD cases nationwide. Prevalence estimates were also calculated by type of surveillance program (i.e., programs with prenatal ascertainment and programs without prenatal ascertainment) and maternal race/ethnicity (i.e., non-Hispanic white, non-Hispanic black, and Hispanic). The estimated annual number of NTDs prevented was calculated as the difference between the estimated annual number during the pre-fortification period and the estimated annual number during the post-fortification period using prevalence estimates from programs with prenatal ascertainment. A decline in NTDs was observed for all three of the racial/ethnic groups examined between the pre-fortification and post-fortification periods (Figure). The post-fortification prevalence has remained relatively stable. During the observed periods, Hispanics consistently had a higher prevalence of NTDs compared with the other racial/ethnic groups, whereas non-Hispanic blacks generally had the lowest prevalence. The birth prevalences of anencephaly and spina bifida during the pre-fortification (1995–1996) and post-fortification periods (biennial from 1999–2008, last 3 years of available data from 2009–2011, and all years from 1999–2011) for programs with and without prenatal ascertainment were estimated. Overall, a 28% reduction in prevalence was observed for anencephaly and spina bifida using data from all participating programs; a greater reduction (35%) was observed among programs with prenatal ascertainment than for programs without prenatal ascertainment (21%) (Table). The prevalence reported for anencephaly from programs with prenatal ascertainment was consistently higher across all racial/ethnic groups than for programs without prenatal ascertainment, whereas the difference in the observed prevalence of spina bifida was not as pronounced between the two types of programs. Based on data from programs that collect prenatal ascertainment information, an updated estimate of the number of births occurring annually without NTDs that would otherwise have been affected is 1,326 (95% confidence interval = 1,122–1,531). Discussion The birth prevalence of NTDs during the post-fortification period has remained relatively stable since the initial reductions observed during 1999–2000, immediately after mandatory folic acid fortification in the United States. The updated estimate of approximately 1,300 NTD-affected births averted annually during the post-fortification period is slightly higher than the previously published estimate (3). Factors that could have helped contribute to the difference include a gradual increase in the number of annual live births in the United States during the post-fortification period and data variations caused by differences in surveillance methodology. The lifetime direct costs for a child with spina bifida are estimated at $560,000, and for anencephaly (a uniformly fatal condition), the estimate is $5,415 (4); multiplying these costs by the NTD case estimates translates to an annual saving in total direct costs of approximately $508 million for the NTD-affected births that were prevented. The reduction in NTD cases during the post-fortification period inversely mirrors the increase in serum and red blood cell (RBC) folate concentrations among women of childbearing age in the general population. Fortification led to a decrease in the prevalence of serum folate deficiency from 30% to 1,000 nmol/L were sufficient to substantially attenuate the risk for NTDs at a population level (6). Using data from the National Health and Nutrition Examination Survey for 1988–2010 (5) and adjusting for assay differences, the estimated mean RBC folate concentration in women aged 15–44 years in the United States is 1,290–1,314 nmol/L, which appears to indicate that for many women of childbearing age, current strategies are preventing a majority of folic acid–sensitive NTDs (5,6). However, almost a quarter (21.6%) of women of childbearing age in the United States still do not have RBC folate concentrations associated with a lower risk for NTDs, and targeted strategies might be needed to achieve RBC folate concentrations >1,000 nmol/L in this group (7). Although a reduction in the birth prevalence of NTDs has been observed for all three of the racial/ethnic groups examined, the prevalence among Hispanics is consistently greater than that among other racial/ethnic groups. Possible reasons could include differences in folic acid consumption and genetic factors affecting the metabolism of folic acid. Fewer Hispanic women (17%) than non-Hispanic white women (30%) report consuming ≥400 μg of folic acid per day through fortified food or supplements (8). A common genetic polymorphism in Hispanics, the methylenetetrahydrofolate reductase T allele, has been associated with relatively lower plasma folate and RBC folate concentrations compared with those without this polymorphism (9). Persons with this polymorphism have more genetic susceptibility to a folate insufficiency. To target Hispanics who might need additional folic acid intake to prevent NTDs, one strategy under consideration in the United States is to fortify corn masa flour with folic acid at the same level as enriched cereal grain products. Implementation of corn masa flour fortification would likely prevent an additional 40 cases of NTDs annually (10). What is already known on this topic? A decline in the prevalence of neural tube defects (NTDs) was reported during the period immediately after mandatory folic acid fortification in the United States, which translated to approximately 1,000 births occurring annually without anencephaly or spina bifida that would otherwise have been affected. What is added by this report? The prevalence of NTDs during the post-fortification period has remained relatively stable since the initial reduction observed immediately after mandatory folic acid fortification in the United States. Using the observed prevalence estimates of NTDs during 1999–2011, an updated estimate of the number of births occurring annually without NTDs that would otherwise have been affected is 1,300. What are the implications for public health practice? Current fortification efforts should be maintained to prevent folic acid–sensitive NTDs from occurring. There are still opportunities for prevention among women with lower folic acid intakes, especially among Hispanic women, to further reduce the prevalence of NTDs in the United States. The findings in this report are subject to at least one limitation. The prevalence data used in this study might not be generalizable to the entire United States, but only to the extent that NTD prevalence in other states/territories not examined could differ from NTD prevalence in the states/territories represented in this analysis. The initial decline in NTD prevalence reported immediately after mandatory folic acid fortification has been maintained after more than a decade since implementation. Mandatory folic acid fortification remains an effective public health policy intervention.
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                Author and article information

                Contributors
                maitreyi.mazumdar@childrens.harvard.edu
                sharif_paed@yahoo.com
                rezina.hamid@gmail.com
                liv839@mail.harvard.edu
                ligi.paul_pottenplackel@tufts.edu
                jacob.selhub@tufts.edu
                emarod@hsph.harvard.edu
                fareesa.silva@childrens.harvard.edu
                dch@bangla.net.bd
                mostofa07@gmail.com
                qzaman07@gmail.com
                dcht87@gmail.com
                dchris@hsph.harvard.edu
                Journal
                Environ Health
                Environ Health
                Environmental Health
                BioMed Central (London )
                1476-069X
                10 April 2015
                10 April 2015
                2015
                : 14
                : 34
                Affiliations
                [ ]Department of Neurology, Boston Children’s Hospital, 300 Longwood Avenue, Boston, MA USA
                [ ]Department of Environmental Health, Harvard School of Public Health, 665 Huntington Avenue, Boston, MA USA
                [ ]Dhaka Community Hospital, 190/1 Baro Moghbazar, Wireless Railgate, Dhaka, 1217 Bangladesh
                [ ]Bangladesh Medical College, 14/A Dhanmondi, Dhaka, 1209 Bangladesh
                [ ]Department of Biostatistics, Harvard School of Public Health, 655 Huntington Avenue, Boston, MA USA
                [ ]Jean Mayer USDA Human Nutrition Research Center on Aging, Tufts University, 711 Washington Street, Boston, MA USA
                Article
                20
                10.1186/s12940-015-0020-0
                4404044
                25885259
                0e8df446-b71a-42f2-88ab-669d7eb7c712
                © Mazumdar et al.; licensee BioMed Central. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 5 January 2015
                : 20 March 2015
                Categories
                Research
                Custom metadata
                © The Author(s) 2015

                Public health
                arsenic,neural tube defect,myelomeningocele,birth defect,folate deficiency
                Public health
                arsenic, neural tube defect, myelomeningocele, birth defect, folate deficiency

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