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For Bangladeshi gamers accessing the system mostly using mobile phone– which describes the majority of the on the internet pc gaming audience in the nation– this architectural clearness translates into a functional benefit over platforms where mobile usability feels secondary to the desktop computer experience. We hope to validate the findings from this study with future follow-up genetic studies in humans and animals through existing collaborations, and to explore how folate status and arsenic exposure potentially modify the relationship between genetics and spina bifida risk. Although we were not able to confirm previously identified associations between spina bifida risk and genetic variants restricted to certain biological pathways, such as folate metabolism, we were able to identify novel variants that may impact biological processes involved in early development. Due to the small sample size of the current study, we were not able to perform linkage analysis that could have provided greater insight into genomic regions affecting disease risk and to perform predictive statistical models that could indicate causal variants for disease.

Results

However, the large variation in neural tube defect prevalence is not solely attributable to folic-acid based prevention strategies, and affected pregnancies occur in regions with ubiquitous folic acid fortification and to women known to have taken folic acid supplements (Centers for Disease Control and Prevention, 2010). Over the past several decades, multiple studies have demonstrated that periconceptional folic acid intake, either through food fortification or supplementation, can reduce neural tube defect risk (Blencowe et al., 2010; Crider et al., 2022). Cranial neural tube defects, including craniorachischisis and anencephaly, result in infant death (Molloy et al., 2017), while individuals with spina bifida may survive, albeit many individuals experience life-long health consequences such as neurological impairment and gastrointestinal disorders (Greene & Copp, 2014). We performed genetic association analyses to compare allele frequencies between 112 case and 121 control children, 272 mothers, and 128 trios.

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The data that support the findings of this study are available to researchers trained in human subjects research and privacy protections upon reasonable request from the corresponding author. The Bangladesh Medical Research Council and the Human Research Committees at Boston Children’s Hospital and the National Institute of Neurosciences & Hospital approved all study protocols, which were conducted in accordance with the Declaration of Helsinki. The data analysis was performed with the computational resources provided by the Research Computing Group at Boston Children’s Hospital and Harvard Medical School (Boston, MA), including High-Performance Computing Clusters Enkefalos 2 (E2), Massachusetts Green High-Performance Computing Center (MGHPCC), and the BioGrids scientific software made available for data analysis. We are grateful to the field staff at the National Institute of Neurosciences and Hospital (NINS) and study participants for their contributions. We have shared biospecimens and data from the project with investigators focused on neural tube defect research and are planning to be involved in future genetic analyses across studies from multiple geographic areas.

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DNA extraction of saliva samples from children and their parents was performed using the Maxwell® RSC Buccal Swab DNA kit (Promega, Madison, WI, USA), adhering to the manufacturer’s protocol. Saliva samples were shaken for 5 seconds and stored at room temperature until shipped to Boston for long-term storage and DNA extraction. ASeven samples failed the Broad Institute QC due to call rates less than 97% and/or as a result of a sex mismatch. The Bangladesh Medical Research Council and the Human Research Committees at Boston Children’s Hospital and NINS approved all study protocols, and informed consent was obtained from parents prior to enrollment. We included individuals with lipomeningocele, which is characterized by fatty tissue connected to the spinal cord (Agopian et al., 2012), and their families in the control group as this defect is believed to occur at different developmental stages than myelomeningocele and meningocele (Agopian et al., 2012; Chan et al., 2017).

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We previously performed candidate gene analysis to examine the interactions between polymorphisms in folate pathway genes and drinking water arsenic, and the influence of these interactions on spina bifida risk, in a separate, pilot study conducted in Bangladesh between April and November of 2013 (Mazumdar et al., 2015). Genetic association studies, including case-control and child-parent trio designs, have been implemented to explore the relationship between genetic variants and neural tube defect risk in humans. Arsenic modifies the effect of folic acid in spina bifida prevention, a large hospital-based case-control study in Bangladesh. First, recall bias may arise since information about folic acid use and drinking water sources was collected after occurrence of spina bifida and might be influenced by differential recall between mothers of cases and mothers of controls. Prenatal folic acid use among our study population was low, but consistent with other reports from Bangladesh; 27,28,29 only 16.7% of mothers of cases in our study and 22.1% of mothers of controls reported using folic acid during pregnancy.

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Although our study is the first to our knowledge to report an association between a variant in the ASB2 gene and neural tube defect risk, this gene has previously been implicated in early developmental processes, specifically heart defects. This study adds to the limited, but growing, research focusing on comprehensive scans of the genome, rather than examining a small subset of genes, for risk variants for spina bifida. Characteristics of the study participants, including children with spina bifida, controls, and their parents, for each of the statistical models (mean ± SD, except where noted). For family-based association, standard transmission disequilibrium chi-square tests (TDT; --tdt) were performed on trio samples for 370,617 variants. Standard case/control allelic association tests were performed using PLINK software (Purcell et al., 2007) to determine the relationship between genetic variants and spina bifida case status. Five children, two fathers, and three mothers included in at least one of the analysis models of the current study belonged to a case family and were later reassigned to be categorized as control families after surgery on the child revealed an updated diagnosis of lipomeningocele.

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Our previous study discovered that higher water arsenic concentrations reduced the effectiveness of folic acid in spina bifida prevention . A recent systematic review showed there was inadequate evidence to determine the relationship between prenatal arsenic exposure and prevalence of NTDs , but the review did not address potential interactions between arsenic and folic acid that may affect spina bifida risk. Mother’s arsenic exposure modified the protective association of folic acid with spina bifida.

The primary aim of the study was to assess the relationship between environmental arsenic exposure and spina bifida risk, and the details regarding recruitment and evaluation have been previously published (Tindula et al., 2021). From December 2016 through December 2022, we enrolled cases, controls, and their parents in a case-control study based in Bangladesh (Tindula et al., 2021). Case-control genetic association studies compare the frequency of genetic variants between cases and controls and are helpful in studies of rare outcomes, including NTDs (Lupo et al., 2017). Association analyses comparing cases and controls, as well as models that included their mothers, did not identify genome-wide significant variants. Our findings raise important questions about the risk of spina bifida in arsenic-endemic areas and the effectiveness of folic acid supplements alone as the strategy to prevent spina bifida in high-arsenic areas of the world.