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Abstract
Objective To estimate the prevalence of neural tube defects among all birth outcomes in Odisha during 2016–2022. Additionally, to estimate the identification rate of neural tube defects during Pradhan Mantri Surakshit Matritva Abhiyan sessions.
Design A population-based cross-sectional study with a household survey for neural tube defects using pictorial card as well as a hospital-based study for antenatal ultrasonography data.
Setting The sample population was selected through multistage random sampling. In the first stage, one district from each zone was selected randomly. In the second stage, using simple random sampling, one community health centre and one urban primary health centre were selected from each district. In the third stage, the population from a block and ward were picked from the selected rural and urban settings, respectively.
Participants All married women in the reproductive age group (18–49 years) residing in these cluster villages in the selected districts were enrolled.
Results The study surveyed 49 215 women and recorded 50 196 birth outcomes, including 49 174 live births, 890 stillbirths and 132 medical terminations of pregnancy. A total of 30 neural tube defect cases were detected. The overall prevalence rate of neural tube defect was 0.59 per 1000 birth outcomes. Spina bifida was the most prevalent neural tube defect with the prevalence of, followed by anencephaly and encephalocele. Despite 26 860 mothers receiving antenatal ultrasonography Pradhan Mantri Surakshit Matritva Abhiyan session, data on neural tube defects and other birth defects detected through these scans is unavailable.
Conclusion This study found a low prevalence of neural tube defect in Odisha, which is far lower compared with the older studies from India. There is an urgent need to strengthen the quality of antenatal care services provided under Pradhan Mantri Surakshit Matritva Abhiyan through better training regarding anomaly scans and better data keeping at public healthcare facilities.
Trial registration number CTRI/2021/06/034487.
- epidemiology
- antenatal
- health surveys
- health services administration & management
- prenatal diagnosis
- community child health
Data availability statement
Data are available upon reasonable request. All data relevant to the study are included in the article or uploaded as supplementary information.
This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.
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- epidemiology
- antenatal
- health surveys
- health services administration & management
- prenatal diagnosis
- community child health
Strengths and limitations of this study
This is one of the largest studies conducted in India, covering an entire state, to detect the prevalence of neural tube defects (NTD).
This is among the few studies conducted to assess the Pradhan Mantri Surakshit Matritva Abhiyan programme in terms of antenatal identification of congenital anomalies, especially NTD on the antenatal ultrasonography.
A limitation of the study may be that it does not include the unmarried women of the study, and some cases may have been missed.
Introduction
Neural tube defects (NTD) are preventable public health problems, and they cause significant morbidity and mortality worldwide. A systematic review article on the prevalence of NTD worldwide reveals that 120 out of 194 WHO member states did not have any data on NTD prevalence, and where available, the prevalence tends to vary widely.1 Approximately 400 000 births with neural NTD occur each year, resulting in an estimated 270 000 newborn deaths worldwide or more than 10% of all newborn deaths.2 The prevalence seems to be higher in countries where folic acid supplementation is not available, and this prevalence ranges between 0.5 and 2 per 1000 births.2 The reported incidence of NTDs in India varies from 0.5 to 18.2 per 1000 total births. The overall pooled birth prevalence is calculated to be 4.5 per 1000 total births which is very high compared with other regions in the world.3
NTD continue to be a problem with significant public health impact in low-income and middle-income countries. Ultrasonographic diagnosis of NTD typically occurs during the second trimester of pregnancy. The diagnostic sensitivity of prenatal ultrasonography (USG) for the identification of NTD in high-risk populations is approximately 97–98% with 100% specificity.4 Determining the site and extent of a spinal lesion correlates well with neurological outcome; more severe neurological dysfunction is associated with higher and larger lesions.
In July 2016, the Government of India launched the Pradhan Mantri Surakshit Matritva Abhiyan (PMSMA) to provide essential antenatal care services to pregnant women in their second and third trimesters on the 9th of each month.5 6 This initiative also focuses on early identification of fetal anomalies and high-risk pregnancies through obstetric USG services. Despite the availability of such guidelines and programmes, many debilitating NTD are not detected antenatally and we continue to see many of these cases in our daily practices.
Although there are a few studies with small sample sizes and a few with pooled data from meta-analysis, but there is no large population-based study from India covering an entire state. Also, there is a paucity of data regarding the prevalence of NTD in Eastern India. Our main study objectives are to estimate the prevalence of NTD among all birth outcomes in Odisha during 2016–2022. We also aimed to estimate the identification rate of NTD through PMSMA programme during this study period of the sampled population by antenatal USG.
Methodology
This was a population-based cross-sectional study carried out in the state of Odisha covering a period of 6 years (2016–2022).
Study population
The sample population was selected using multistaged random sampling. Odisha has 30 districts and 32 district headquarter hospitals (DHH). In the first stage, the 30 districts were divided into four zones (representing different geographical areas of Odisha). In the second stage, one district from each zone was selected randomly. In the second stage, using simple random sampling, the population from one block from rural settings and one ward from urban settings were selected from each district. In the third stage, population of a sector/ward was picked from the selected block and ward, respectively. The study was conducted in both the urban and rural areas. The study was carried out among all married women in the reproductive age group (18–49) years residing in these cluster villages in the selected districts. The detailed of multistage random sampling was represented in a figure mentioned below with the overall population number (figure 1).
Flow chart of multistage random sampling of the study. CHC, community health centres; PHC, primary health centres.
Study procedure (data collection)
A well-structured data collection protocol was implemented. Initial communication transpired between the Principal and Co-Principal Investigators and the Chief District Medical and Public Health Officers, with subsequent approval obtained through an official letter from the district hospital headquarters. Following this, the study team conducted a detailed explanation of the research objectives to the participants in the selected study areas, securing written consent before proceeding. Before commencing data collection, a 1-day capacity-building session was conducted by the research team to the Accredited Social Health Activists (ASHA) and Anganwadi Workers (AWW) associated with the selected community health centres (CHC) and urban primary health centres (UPHC). A pictorial card aided in avoiding any confusion during the identification process. Informed written consent, signed by the mothers of NTD children, was obtained. Thorough inquiries were made to determine if similar cases had occurred within the family, involving cross-verification through family members, neighbours, village ASHA and AWW, in case of denial by the mothers. A team comprising trained field assistants conducted door-to-door surveys in each cluster village, engaging with women who had been pregnant within the last 6 years in each household. The data collection tool was developed by the research assistant by first identifying the construct and item of the tool by doing an extensive review of the literature to identify the articles related to the identification and prevalence of NTD. We also searched relevant guidelines and programme documents to further supplement the published literature. The initial tool was shared with experts and study investigators and each expert was expected to rate items on a scale of 1–5 based on the relevance of the item to the study objective. The item was removed from the tool if at least one expert rated it as not relevant. The updated tool was then pretested on 10 eligible participants and further modified based on the responses. The final tool was pilot-tested in one of the clusters in the study areas to assess the feasibility and time taken for each interview. The cluster chosen for pilot testing was not included in the random list for the main study.
Using a pretested and structured questionnaire, the data collection process was organised into three parts. The first part sought comprehensive information on maternal age, number of pregnancies and various birth outcomes such as live births, stillbirths, medical termination of pregnancy (MTP), miscarriages and children with NTDs. The second part was exclusively administered to mothers with children having birth defects, while the third part was designated for mothers with children specifically diagnosed with NTDs. The collected data encompassed demographic details, folic acid usage, medications during or early pregnancy, underlying maternal diseases, time and place of USG and the timing of NTD diagnosis.
Data collection tools: A pictorial card depicting 11 coloured photographs of different types of NTDs was used to show the married woman and her family members to detect NTDs. These photographs include anencephaly, craniorachischisis, iniencephaly, frontal encephalocele, occipital encephalocele, myelomeningocele (cervical, thoracic, lumbar, sacral), spina bifida occulta and associated hydrocephalus.
Confirmation of NTD: All the cases detected during the data collection were confirmed by the primary investigators paediatric surgeons.
Data collection from the hospital (primary health centres (PHC)/CHC/Sub-divisional hospital (SDH)/DHH): The health workers visited each selected hospital to collect data regarding the effectiveness of the PMSMA programme including the provided facility of PMSMA programme and the outcome of antenatal USG, identification of NTD if any (details).
Data entry and analysis
Data were collected using Epicollect5 software. All data were entered in Microsoft Excel 2019 and analysed using the software IBM Statistical Packages for Social Sciences (SPSS) V.22.0. We estimated the prevalence of NTD in all ever-married women aged (18–49) who were pregnant during the last 6 years (2016–2022) residing in four selected districts. The quantitative variable is expressed in frequency and percentage. The prevalence rate was calculated using the total number of identified NTD cases as the numerator and the number of birth outcomes as the denominator. The 95% CIs were estimated. We have collected the data of socio-demographic, hospital record of the mother of NTD cases and some characteristics of NTD child. These quantitative variables were descriptively summarised.
Results
During the study period from 1 Aug 2021 to 30 July 2022, a number of 41 243 women were interviewed in the study out of which a total of 49 174 live birth (LB), 890 stillbirth (SB) and 132 numbers of MTP were identified. A total number of 30 NTD cases were detected. Out of which 19 cases were LB, 4 were SB and 7 mothers underwent MTP following antenatal diagnosis. The overall prevalence rate of NTD in our study was 0.59 per 1000 birth outcomes with 95% CI (0.4187 to 0.853). The prevalence of NTD among LB was 0.3/1000 LB 95% CI (0.2474 to 0.6034); similarly, the prevalence of NTD among SB and the prevalence of MTP was 4.4/1000 95% CI (1.749 to 11.5) and 53.03/1000 95% CI (25.92 to 105.4), respectively.
Distribution and types of NTD: In the years 2016–2022, a total of 30 cases of NTD were analysed. The most prevalent NTD was spina bifida, with the prevalence 0.33 per 1000 birth 95% CI (0.2115 to 0.5423) followed by anencephaly 0.19 per 1000 birth 95% CI (0.1082 to 0.3667), occipital encephalocele with a prevalence of 0.03 per 1000 birth 95% CI (0.01093 to 0.1453) and lastly craniorachischisis 0.01 per 1000 95% CI (0.0035 to 0.1128).
Socio-demographic and obstetrical characteristics of mothers having NTD child: A detailed overview of various factors was associated with a cohort of 30 pregnancies, offering insights into maternal characteristics, medical history, folic acid consumption, antenatal care, USG evaluations and the professionals involved in the process. Maternal age distribution indicated that the majority of participants fell within the 20–24 age range (46.7%), followed by 31–35 (26.7%). Parity analysis revealed that half of the pregnancies were from women with a parity of 1 (50.0%), with decreasing frequencies for higher parities. Medical history during pregnancy highlighted diverse conditions such as fever, cold, cough, anticonvulsant consumption, gestational diabetes, anaemia, acidity, mental disorders and thyroid issues, each with varying prevalence.
Regarding folic acid consumption, 46.7% of participants took iron folic acid, while 53.3% did not. The timing of folic acid intake varied, with 30.0% taking it regularly during pregnancy. Antenatal check-ups were more commonly conducted in private facilities (63.3%), with 36.7% opting for government facilities. Surprisingly, all participants were not aware of the PMSMA scheme. All pregnancies were singleton, and USG examinations were commonly performed, with 66.7% of reports indicating abnormalities. The number of USG examinations varied, with the impression of reports suggesting normal findings in 33.3% of cases. Obstetric and gynaecologists and radiologists were the primary professionals performing antenatal USG scans, with a slight majority being obstetrical and gynaecological specialists (table 1).
Socio-demographic and obstetrical characteristics of women reported with a pregnancy with neural tube defect
The provided table summarised key variables related to a study population of 30 individuals, shedding light on the demographic and clinical characteristics of the sample. In terms of gender distribution, the population exhibited a relatively balanced representation, with 53.3% being men and 46.7% women. Birth order analysis revealed that half of the individuals were firstborns (50.0%), while the second birth order constituted 40.0% of the sample. Notably, there was a decreasing frequency with higher birth orders (6.7% for the third and 3.3% for the fifth). Examination of birth years demonstrated variability, with peaks in 2019 and 2021 (both at 30.0%), contrasting with fewer cases in 2016, and 2020. However, in 2017, no NTD cases were detected. Delivery settings predominantly favoured hospitals (96.7%), underscoring the importance of institutional birthing environments. Regarding birth outcomes, the majority resulted in LB (63.3%), with 13.3% ending in SB and 23.3% in MTP. Furthermore, the table outlined the distribution of NTD types, revealing spina bifida as the most prevalent (56.6%), followed by anencephaly (33.3%). Occipital encephalocele and craniorachischisis were less common, comprising 6.7% and 3.3%, respectively (table 2).
Demographic characteristics and hospital record of neural tube defects identified cases
For identification of the number of NTD cases through USG in the health facilities during PMSMA (Pradhan Mantri Surakshit Matritva Abhiyan) sessions during our study period, to know the impressions of USG regarding NTD in four districts: Khordha, Mayurbhanj, Sambalpur and Koraput, the data indicated that the selected CHC and UPHC in these districts did not perform USG facilities during that specified study period. However, DHH in all districts had the necessary equipment for conducting USG.
The number of pregnant women who performed for USG during PMSMA sessions varied across the districts. Khordha, Mayurbhanj, Sambalpur and Koraput had 4686, 13 298, 4603 and 4273, respectively. However, no USG reports record were available for the USG impression of any birth NTD cases.
Discussion
The present study identified 30 NTD cases between 2016 and 2022 across four districts in Odisha, resulting in a prevalence of 0.59 per 1000 births. This figure is significantly lower than the pooled NTD prevalence in India (4.5 per 1000 births) and falls within the range observed in the USA and Canada.3
As per a meta-analysis, the prevalence at birth was highest in Northern India at 7.7 cases per 1000 births, while the prevalence in the eastern region was 1.1 cases per 1000 births.3 Such variation is explained by different factors such as type of study (hospital-based or population-based), poor study designs, non-random samples, lack of use of standard definitions, lack of defined denominators and non-standard methods of reporting data.3 7 Compliance with folic acid supplementation, variation in diet and other sociocultural factors play a significant role too. Most of the available studies in India between 1992 and 2014 were hospital-based studies which are heavily affected by selection bias and referral bias.7 8 Moreover, it does not include residents outside of the geographical location of the hospital. Community-based population study designs are far superior, and when collected from a larger population with a wider time frame, they are proven to be more accurate.8 9
The prevalence of 1.1 cases per 1000 births in the eastern region was based on only one study, which was a hospital-based retrospective study.1 10 Hence, it is justifiable to argue that this does not reflect the true prevalence of NTD in Eastern India. Moreover, systematic reviews and meta-analyses may give flawed results when there is insufficient data and fewer previous studies available. Our results reflect the true prevalence of NTD in Eastern India, as ours was a prospective cross-sectional study conducted as a door-to-door survey, and we have included the entire state and districts from different zones of the state.
In our study, spina bifida (56.6%) was the most common anomaly, followed by anencephaly and encephalocele. This pattern is similar to earlier studies across the globe. However, anencephaly was the most common anomaly in one systematic review from India.11 This can be explained by geographical differences, which may have contributed to variations in different types of NTDs. Also, being a systematic review that includes many hospital-based studies, the data may not represent the entire picture.
The occurrence of NTDs in any population may have a multifactorial cause. It can be due to hereditary or environmental factors or their interactions. Maternal folate deficiency is the most important environmental factor linked to NTD causation.7 Periconceptional intake of folic acid reduces the risk of having an infant affected by NTD. According to some studies, there is 60–100% reduction in the risk of NTD pregnancy after folic acid intervention among pregnant women with prior NTD-affected pregnancies.12 Observational studies of folic acid efficacy in preventing NTD in pregnant women without a prior NTD-affected pregnancy showed a 0–75% reduction in risk.12 In the present study, 16 (53.3%) mothers with an NTD child have not at all consumed folic acid during their entire pregnancy, and the others took folic acid during the first two trimesters but irregularly. One had a family history of NTD and three had previous birth history of NTD. Despite this high-risk history, none of the women took folic acid in the periconceptional period. Pregnant women are still not aware of the advantages of periconceptional folic acid, despite several government initiatives. Though this fact of not taking folic acid, does not reflect a rise in NTD cases in our population. The lower prevalence of NTD in the current study may be explained by other environmental factors and the dietary patterns of the people of Odisha. However, the present study did not explore these factors, which were beyond the scope of this study.
Traditionally, it has been assumed that, in India, the cases of NTD seem to be higher as compared with other developed countries because of unplanned pregnancies, unawareness regarding the benefits of periconceptional folate supplementation, improper USG and the absence of prenatal diagnostic tests, which means parents only become aware of their malformed infant after birth. While India has made considerable progress in the reduction of maternal and infant mortality, every year approximately 44 000 women still die due to pregnancy-related causes and approximately 6.6 lakhs infants die within the first 28 days of life. Many of these deaths are preventable and many lives can be saved if quality care is provided to pregnant women during their antenatal period and high-risk factors such as severe anaemia, pregnancy-induced hypertension, etc are detected on time and managed well.5 The PMSMA was launched by the Ministry of Health and Family Welfare, Government of India in July 2016, which aims to provide assured, comprehensive and quality antenatal care, free of cost, universally to all pregnant women on the 9th day of every month. PMSMA guarantees a minimum package of antenatal care services to women in their second/third trimesters of pregnancy at designated government health facilities. Through PMSMA every pregnant woman will receive at least one check-up in second/third trimester of pregnancy by an Obstetrics and gynaecology (OBG) specialist or medical officer at the designated government health facilities.5 6
As antenatal ultrasonography (ANUSG) is a routine antenatal check-up during PMSMA days, any birth defect or NTD if present should be diagnosed earlier. In order, to find out the effectiveness of ANUSG during PMSMA in identifying NTD, we did a secondary data collection using the data of PMSMA sessions conducted in the selected UPHC and CHC. On the PMSMA reports, the total number of pregnant women was limited to those who had undergone ANUSG during the PMSMA sessions. However, there were no records available about the impression from the ANUSG or whether any congenital anomalies, including NTD, were detected. An antenatal care service was sought by all 30 women with an NTD child, and all of them had undergone ANUSG. In the majority of cases (21, 70%), ANUSG were conducted in a private setting (hospital clinic) and in 83.3% of cases, ANUSG were performed by an obstetrician or a radiologist. None of the affected pregnant women were aware of the PMSMA programme, healthcare facilities providing the PMSMA or had undergone ANUSG under PMSMA. Though 20 (66.7%) NTD cases were detected by ANUSG, none of them were detected before 24 weeks (second trimester), which is the cut-off for doing an MTP. In 10 cases, the NTD was not detected on any of the ANUSG which raises a serious concern about the knowledge and training of the medical practitioners performing the ANUSG. The routine ANUSG only focuses on the identification of the amniotic fluid levels and fetal heartbeat and specific record is maintained for high-risk pregnancies.
According to the WHO, an estimated 240 000 newborns die worldwide within 28 days of birth every year due to congenital disorders. Congenital disorders cause a further 170 000 deaths of children between the ages of 1 month and 5 years.13 Hence, timely antenatal identification will be largely helpful in managing this issue. ANUSG can detect the majority of lethal and complex congenital anomalies including NTD and proper training is needed to conduct an anomaly scan to detect these conditions. Though the PMSMA programme has included the provision of ANUSG in its arsenal, proper training for the healthcare providers especially treating obstetricians should be included. Record keeping is another issue that needs to be addressed. There is no record keeping of the details of the ANUSG findings in any of the government healthcare facilities. A recent study on the assessment of the quality of antenatal care services in public sector facilities in India found that the quality of antenatal care (ANC) services under PMSMA was grossly inadequate and needs urgent attention to improve maternal and neonatal health outcomes.14 Our study also echoes the same findings and demands further strengthening of the PMSMA programme through coverage, quality training and record keeping.
Our study had several strengths. First, it was a population-based cross-sectional study covering an entire state which is a first-of-its-kind study in India. Second, it included information on all possible outcomes of pregnancy that is, LB, SB and MTP. Third, the confirmation of NTD was done by showing pictures of various NTD on a tablet phone, which were validated by paediatric surgeons. We collected and verified the ANUSG reports for antenatal identification of NTD and the MTP records for NTD in SB. Fourth, the time frame of the NTD identification was kept at 6 years to negate the problem of recall bias and loss of physical documents such as ANUSG reports and medical records. The study had a few limitations. The study relied on self-reported occurrences of NTDs. Hence, under-reporting due to social desirability bias (taboo) could be a possibility. We tried to overcome this issue by asking other women in the family and in the neighbourhood. Though the study covered the entire state by dividing the state into four zones and randomly selecting CHC, urban and rural PHC and villages, it is not possible to collect data from each village in the state in a door-to-door survey. Many NTD cases may have been missed as the villages were not included in the study. However, the sample population was selected by multistage sampling strategy which is a valid method to cover a larger population. Additionally, we have compared our data with the (Rashtriya Bal Swasthya Karyakram) RBSK data of the same region which were similar. In fact, we were able to detect more cases over RBSK as we have taken MTP and stillborn data whereas RBSK only takes LB data. We have not discussed the details of this as this was beyond the scope of this paper.
Conclusion
This study investigated the prevalence of NTD in four districts of Odisha from 2016 to 2022, revealing a rate of 0.59 per 1000 birth outcomes, significantly lower than previous studies. The identification of risk factors, particularly the association with inadequate folic acid intake, underscores the critical need for enhanced primary prevention strategies. Emphasising the importance of folic acid supplementation during the preconception phase and promoting healthy dietary habits through existing government initiatives are essential interventions. While acknowledging the positive impact of the PMSMA programme initiated by the Government of India, our findings highlight areas requiring urgent attention in improving data management practices of fetal anomalies during ANUSG in healthcare facilities involved in the PMSMA programme is imperative for accurate monitoring and assessment. In conclusion, addressing the relatively low prevalence of NTDs and optimising the effectiveness of existing initiatives demand a multifaceted approach. The integration of enhanced preventive measures, comprehensive training programmes and improved data management practices will contribute to the overall success of public health efforts in reducing the burden of NTDs in these districts and serve as a model for broader initiatives in maternal and child health.
Data availability statement
Data are available upon reasonable request. All data relevant to the study are included in the article or uploaded as supplementary information.
Ethics statements
Patient consent for publication
Ethics approval
This study involves human participants and an ethical clearance was obtained from the Institute Ethics Committee of All India Institute of Medical Sciences (AIIMS), Bhubaneswar (IEC-EMF/Ped.Surg/20/11) and the Additional Chief Secretary to Government of Odisha, Health and Family Welfare Department (letter No. 16616/MS-2-IV-04/2020 (PT) dated (21 August 2021). Written consent was obtained from the women who gave birth to an NTD child or have done MTP of having NTD before collecting the data from them.
Acknowledgments
We would like to thank all our field assistants (Harapriya Jena, Manish Kumar Dutta, Namrata Mohanta, Rashmita Jena) for their exceptional door-to-door survey and data collection. We would like to thank the Anganwadi workers and ASHA workers from different districts for their help and input regarding data collection. We would like to thank the CDMO and all medical officers in charge of different district, CHC and PHC involved in data collection.
Footnotes
X @santosh25
Contributors SKM and AKS developed the study protocol with inputs from ABP. Door-to-door survey, supervision of filed assistants and compilation of data were conducted by SM and LR. SM and LR further analysed the data and created the first draft of the manuscript. SKM, AKS and ABP further modified the draft to prepare the final manuscript. All authors provided critical comments on drafts, and read and approved the final manuscript. All authors contributed to revisions of the paper. SKM as guarantor accepts full responsibility for the finished work and the conduct of the study, had access to the data and controlled the decision to publish.
Funding The project got approval from Indian Council of Medical Research (ICMR), New Delhi, as an ad hoc project and got a funding of INR 3 020 471. The sanction letter number: 5/7/91/MH/Adhoc/2020-RBMCH.
Disclaimer The views expressed in this publication are those of the author(s) and not necessarily those of AIIMS Bhubaneswar or ICMR.
Competing interests None declared.
Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.
Provenance and peer review Not commissioned; externally peer reviewed.