Screening and management options for severe thinness during pregnancy in India

This paper answers research questions on screening and management of severe thinness in pregnancy, approaches that may potentially work in India, and what more is needed for implementing these approaches at scale. A desk review of studies in the last decade in South Asian countries was carried out collating evidence on six sets of strategies like balanced energy supplementation (BEP) alone and in combination with other interventions like nutrition education. Policies and guidelines from South Asian countries were reviewed to understand the approaches being used. A 10‐point grid covering public health dimensions covered by World Health Organization and others was created for discussion with policymakers and implementers, and review of government documents sourced from Ministry of Health and Family Welfare. Eighteen studies were shortlisted covering Bangladesh, India, Nepal, and Pakistan. BEP for longer duration, preconception initiation of supplementation, and better pre‐supplementation body mass index (BMI) positively influenced birthweight. Multiple micronutrient supplementation was more effective in improving gestational weight gain among women with better pre‐supplementation BMI. Behavior change communication and nutrition education showed positive outcomes on dietary practices like higher dietary diversity. Among South Asian countries, Sri Lanka and Nepal are the only two countries to have management of maternal thinness in their country guidelines. India has at least nine variations of supplementary foods and three variations of full meals for pregnant women, which can be modified to meet additional nutritional needs of those severely thin. Under the National Nutrition Mission, almost all of the globally recommended maternal nutrition interventions are covered, but the challenge of reaching, identifying, and managing cases of maternal severe thinness persists. This paper provides four actions for addressing maternal severe thinness through available public health programs, infrastructure, and human resources.

Among pregnant women with normal pre-pregnancy weight, energy requirements increase by 350 kcal/day and protein by 7.6 g/ day in the second trimester, and 17.6 g/day in the third trimester as per Estimated Average Requirements 2020. 18 Pregnant women with severe thinness have higher nutrient requirements to achieve adequate gestational weight gain (GWG) compared to pregnant women with optimal BMI. In 2016, WHO recommended balanced energy and protein (BEP) supplementation for pregnant women in undernourished populations to reduce the risk of stillbirths and SGA neonates, and targeted counselling of severely thin pregnant women to increase energy-protein intake along with an array of nutritional interventions. 19 Earlier, in 2013, WHO recommended that pregnant women with active tuberculosis and moderate undernutrition, or with inadequate weight gain, should be provided with locally available nutrient-rich or fortified supplementary foods, as necessary, to achieve an average weekly minimum weight gain of approximately 300 g in the second and third trimesters. 20 In the absence of medical conditions, WHO recommended an outpatient food-by-prescription program for severely thin adolescents and adults. 21 In India, under the Integrated Child Development Service (ICDS) scheme, pregnant women and lactating mothers are entitled to take home ration (THR) or hot cooked food providing 600 kcal energy, 18-20 g protein, and half the daily requirement for nine essential micronutrients for 300 days a year. 22 However, there is no special nutritional support package for pregnant women who are thin or severely thin, except those afflicted with tuberculosis. 23 Maternal severe thinness screening and management remains suboptimally addressed in India's public health and nutrition programs. The searched studies were reviewed by two independent researchers and discrepancies about the inclusion of studies were resolved by discussion with a third reviewer. Relevant information on study title, authors, objectives, study setting and type of population, sample size, study design, methodology, intervention(s), outcome, and results were transcribed into a predesigned data collection form.

| Review of guidelines
The authors accessed guidelines on or related to maternal nutrition including antenatal care (ANC) from ministerial websites of all South Asian countries and carefully scanned for interventions that may be relevant to the management of severe thinness. Country or regional nutrition programs' review reports by UNICEF, Scaling up Nutrition, and related websites were also reviewed.

| Development of guidelines review grid and discussions with policymakers and implementers
A guideline review grid consisting of 10 blocks was constructed covering public health dimensions covered by WHO and others, such as availability and accountability for guidelines, plans and financing, demand creation, leadership and governance, partnerships, information systems/monitoring and evaluation, capacity building, supply, institutionalized mechanisms, research, and policy dialogue. The grid was used for discussion with policymakers and implementers of proposed Indian maternal nutrition guidelines to understand the current status and gaps against each of the blocks. All available documents, such as national ANC implementation guidelines, composition tables of supplementary foods or therapeutic foods being given to pregnant women in India, annual plan, and record of proceedings for measuring budget outlays were collated and reviewed to understand current provisions and gaps.
Severe thinness and severe underweight have been used interchangeably in operational definitions for this article.  or BMI < 18.5. 27,36,37,[39][40][41] In the remaining studies, there was a mixed sample of participants including both underweight and normal BMI. However, the prevalence of thinness was high, and only one among these reported a subgroup analysis for thin mothers. 29 None of the studies had subgroup analysis for severely thin pregnant women. Five studies involved women under pregnancy surveillance, 25,[28][29][30]32 whereas 13 studies recruited women who were already pregnant, and intervention was started after pregnancy confirmation. All studies, except one, included newborns for studying the effect of the intervention on outcome measures such as LBW and infant anthropometry.

| BEP supplementation
Three RCTs involving 6264 women evaluated the effect of BEP supplementation on neonatal, perinatal, and maternal outcomes. [25][26][27] Potdar et al. 25 reported a trend toward a higher birthweight for 1094 infants (+48 g; 95% CI, 1-96 g; P = 0.046) of women in the treatment group who received a treatment snack resembling local street food containing a mix of micronutrient-dense green leafy vegetables (such as spinach, coriander), milk powder, and dry fruits from more than 90 days before pregnancy until delivery. However, no overall positive effect on birth weight was observed for the entire cohort (26 g; 95% CI, -15 to 68 g; P = 0.22). The cluster RCT from Bangladesh involving 87 undernourished pregnant (defined as MUAC <22.1 cm) women treated until delivery with a locally produced BEP supplement found no significant differences in birth weight, whereas the MUAC of infants at 6 months of age was higher in the intervention group (12.83 ± 0.62 vs 12.01 ± 0.21 cm; P < 0.05). No significant difference was observed in other maternal and infant outcomes. 26 The study from Bangalore did not observe any significant difference in GWG, birthweight, birth length, or gestational age in 12 underweight pregnant women (BMI <18.5) who were provided a daily food supplement. 27

| MMN supplementation
Three studies involving 50 693 women with MMN supplementation found a significant increase in birthweight and reduction in the prevalence of LBW babies. [28][29][30] In the RCT from rural Nepal by Christian et al., 28  significantly higher in both groups (P = 0.012 and P < 0.001, respectively). There was no significant association between any of these supplements and neonatal or perinatal mortality. 28 Another RCT from Nepal reported that MMN supplementation (per UNIMMAP, a MMN tablet providing RDAs for thiamine, vitamin A, riboflavin, vitamin B6, vitamin B12, niacin, folic acid, vitamin C, iron, copper, iodine, selenium, vitamin D, vitamin E, and zinc) contributed to a 77 g increase (95% CI, 24-130; P = 0.04) in birthweight compared with the control arm with only IFA supplementation. 29 Mean birthweight was also higher in women with a BMI ≥18.5 (2804 g vs 2688 g) who received the intervention. In the analysis stratified by BMI, the difference in birthweight and LBW only remained significant for mothers with BMI ≥18.5 (birthweight: +83 g, 95% CI, 20-146; P = 0.010; reduction in LBW, OR 0.69; 95% CI, 0.52-0.93; P = 0.014).
No long-term benefits concerning child growth were noted.       study was included in the analysis. [31][32][33][34] The study by Matias et al. 31 in rural Bangladesh (Rang-din study), with 26% of the participants with BMI <18.5, reported no difference in overall outcomes (ma- 0.3 ± 3.7 kg in first, second, and third arms respectively; P < 0.001) and 32 weeks (6.9 ± 4.5, 6.4 ± 4.1, and 6.2 ± 4.4 kg in first, second, and third arms respectively; P < 0.001) of gestation compared with arms 2 and 3. The overall compliance was 87.2% for the LNS and 84%

| Combined BEP and MMN supplementation
for the BEP supplement. 32

The Bangladesh MINIMat (Maternal and Infant Nutrition
Interventions in MATLAB) study involving two food groups (early invitation to food supplementation and usual invitation to food sup-

| Nutrition education
Two studies evaluating the impact of nutrition education on the impact of nutritional status of pregnant women in India were identified. 35, 36 Garg and Kashyap 35 reported improvement in the quality and quantity of dietary intake (P < 0.001 for milk, cereals, green leafy vegetables, fruits, and fat; P < 0.05 for pulses, roots, and tubers) and nutrient intake (P < 0.001 for all nutrients) among mothers after counselling. However, improvement in maternal weight gain per week (0.40 kg) was not significant compared with control. 35 The study by Daniel et al. 36 reported significantly higher weight gain in the intervention group (8.8 ± 2.0 kg) compared with the control group (6.9 ± 1.4 kg; P < 0.0001) with only education. However, no significant difference in birth weight was observed. 36

| Combined BEP supplementation and nutrition education
Five studies involving 3027 women reported the use of nutrition education and BEP as interventions during pregnancy.

| Current policy, financial, and programmatic gaps to prevent, screen, and manage maternal severe thinness
A comparison of India's ANC nutritional interventions with global recommendations is presented in Table 3.
WHO recommends using pre-pregnancy BMI and MUAC to screen pregnant women for thinness and severe thinness. 49 The BMI Services currently include take-home supplementary food (providing 600 kcal, 18-20 g protein, and half the RDA for nine essential micronutrients) and hot cooked meals, health and nutrition education, and health check-ups delivered at Anganwadi or home. Table 4 provides a detailed description of the different kinds of supplementary food provided through different government programs.
There have been efforts to develop and test an algorithm As per policymakers'' and implementers' experiences and perspectives, there are several challenges in implementing these actions in the facility or community setting (Table 5).

| DISCUSS ION
This desk review explored the effect of nutritional interventions to manage severe thinness among pregnant women for maternal TA B L E 3 Maternal nutrition interventions recommended by WHO (2016), SAARC regional maternal nutrition guidance (forthcoming), and those covered under national programs/guidelines of India  4. Nutrition assessment and classification of nutrition risks has its challenges of data points, early enrolment, construct validity and time available with worker. Indian government has initiated programme feasibility-five integrated actions using a systems approach. This must be documented. Ongoing health systems/ social protection systems research on maternal nutrition must be replicated for feasibility and long-term implications.

| CON CLUS ION
More implementation research is needed to develop a standard service delivery package to manage severe thinness as medical nutrition therapy, some of which is ongoing in selected health facilities, NRCs, and community settings. Guidelines from neighboring Sri Lanka, drivers of maternal severe thinness, and successes (albeit limited) from intervention trials provide evidence for promoting a combination of interventions including comprehensive nutritional assessment and follow-up, diet and related counselling and nutrition education, and in some cases additional dietary supplementation.

ACK N OWLED G M ENTS
The research reported in this publication was developed from the working paper submitted to the Ministry of Health and Family Welfare, Government of India, and funded by the United Nations Children's Fund (UNICEF), New Delhi, India.

CO N FLI C T S O F I NTE R E S T
The authors have no conflicts of interest.

AUTH O R CO NTR I B UTI O N S
VS and AB conceptualized the paper and drafted it with contributions from TC. All other authors reviewed the manuscript and contributed to the interpretation of findings. All authors agreed the final version of the paper.