Summary box
Recent estimates of low birth weight (LBW) (weight <2500 g) indicate the burden to
be high; 20.5 million babies are born too small annually, although data from low-income
countries is sparse.
The WHO’s antenatal care guidelines recommend supplementation with ‘balanced energy
and protein’ (BEP) during pregnancy in undernourished settings (where >20% women are
too thin based on their body mass index).
Motivated by equity, we make the case for targeting individual, higher-risk women
for BEP supplementation, which would be safe, affordable and likely more impactful
by giving all vulnerable women access to this effective intervention.
Innovative, programmatic action using such a precision public health approach is needed
to improve women's health and accelerate progress towards the 2030 target for reducing
LBW by 30%.
The burden of maternal undernutrition is well defined, but global momentum and political
will to address it is lacking. Maternal nutrition has long been neglected largely
due to gender-based inequities in resource allocation. The first 1000 days, especially
the period from conception through birth (approximately the first 280 days), is a
critical window for future growth, development and resilience in the face of possible
adversity or disease. Despite this biological imperative, the bulk of resources allocated
to maternal and child health have been directed towards the child1—with little attention
to a woman’s nutritional status prior to or during pregnancy.
A recent estimate noted that 20.5 million babies are born ‘low birth weight’ (LBW
<2500 g) every year; 48% of these are born in South Asia and 24% in sub-Saharan Africa.2
Babies born small at birth have an increased risk of mortality, morbidity and suboptimal
growth and cognitive development throughout childhood, thus perpetuating the intergenerational
cycle of growth failure. Progress towards reducing LBW was somewhat rapid from 2000
to 2009, but it stalled in the past decade to only 1% average annual risk reduction
(AARR).2 The World Health Assembly target of 30% reduction in LBW by 2025 is unreachable
at this rate of change; the AARR must nearly triple to 2.7% to meet the global goal.
This high burden of LBW is biologically linked to the high burden of global maternal
undernutrition; 450 million women in low-income and middle-income countries (LMIC)
are estimated to have short stature,3 240 million are underweight (body mass index
(BMI) <18.5),4 and 468 million are anaemic.5 India faces the highest burden of maternal
undernutrition both proportionately and in absolute terms; 100 million adult women
in India have low BMI (<18.5).4 These maternal factors are causally linked with LBW
and its two underlying causes—preterm birth and small-for-gestational age (SGA) (figure
1), although it must be noted that having quality data for these requires accurate
gestational age assessment, which is relatively uncommon in LMIC.
Figure 1
Maternal nutrition and other factors influencing adverse birth outcomes. BMI, body
mass index; UTI, urinary tract infection; BV, bacterial vaginosis.
The WHO recently updated the guidelines for antenatal care for a ‘healthy pregnancy
experience’. These guidelines offer evidence-based recommendations to support nutrition
in pregnancy.6 WHO’s recommendations include nutrition counselling for a healthy diet
and adequate weight gain in pregnancy, daily use of iron–-folic acid supplement to
prevent anaemia, and calcium supplementation to reduce the risk of pre-eclampsia in
low calcium intake settings. Additionally, new evidence has demonstrated efficacy
and superiority of prenatal multiple micronutrient supplementation versus iron–folic
acid,7 8 calling for the need to revise current guidelines. Finally, based on a systematic
review of evidence,9 the guidelines also include a ‘context-specific’ recommendation
that pregnant women in ‘undernourished populations’ consume balanced energy and protein
(BEP) supplements. BEP refers to ready-to-use or ready-to-be-cooked foods provided
daily to supplement home-based diets to increase energy and protein intake in pregnancy.
This recommendation recognises that, in many LMIC settings, women begin a pregnancy
with low BMI. Women with chronically deficient diets are at higher risk for inadequate
weight gain in pregnancy; this is a modifiable risk factor linked to poor fetal growth.
Furthermore, nutritional requirements for protein, energy and many micronutrients
increase during pregnancy, and they are often unmet without substantially increased
dietary intake and improved dietary diversity. The BEP guideline is meant to address
these nutritional gaps. The systematic review showed BEP to reduce SGA by 21%,9 and
increase mean birth weight by 41 g; the impact of BEP on increasing birth weight was
higher in undernourished women (approximately 100 g).10
The WHO guideline recommends a population-based approach and suggests use of BEP where
the population prevalence of low BMI (<18.5) is greater than 20% (figure 2). This
recommendation arises in part from concerns related to global trends of increasing
BMI. Mean BMI in LMIC is rising.11 Except for Sub-Saharan Africa, this trend is as
common in rural contexts as it is in cities.12 While the obesity epidemic is an increasingly
important public health problem, there is not clear evidence that BEP during pregnancy
increases the risk of obesity. Further, the current guideline applies nationally to
only two countries—India and Bangladesh—where the prevalence of low maternal BMI is
>20%.4 This means that women in undernourished or food insecure regions of other countries
are not eligible for BEP; thus, the current guideline ignores the substantial sub-national
heterogeneity in maternal nutritional status. We advise more countries should consider
sub-national geographic targeting, but guidance on this is limited.
Figure 2
Recommended and alternative use cases for nutritious food supplements in pregnancy
in undernourished contexts. BMI, body mass index; LMIC, low-income and middle-income
countries.
Surprisingly, the current WHO guideline advises against identification and supplementation
of specific undernourished pregnant women. That recommendation likely arises from
a focus on equality and perceived ease of implementation. However, we argue that a
targeted, equity-focused approach is safe, may be more impactful and would potentially
be more affordable than a population-approach.
Using a person-specific guideline would facilitate implementation, impact and equity
through two additional use cases for BEP (figure 2). First, women could be targeted
for BEP based on their pre-pregnancy or early pregnancy BMI. One approach could be
to target only the most undernourished (<18.5 BMI), but arguably, this would not fully
address the entire burden of poor fetal growth as inadequate weight gain can occur
in women regardless of their baseline BMI. A meta-analysis that included pregnant
women in high-income and middle-income countries, showed that inadequate gestational
weight gain is associated with the highest risks of preterm birth among women with
pre-pregnancy BMI <25.13 Thus, we argue that women with BMI <25 are likely to benefit
from a food supplement in pregnancy in undernourished, food insecure contexts. Each
country should decide the upper cut-off of BMI, depending on the burden of maternal
undernutrition and related adverse pregnancy outcomes. A second targeting approach
might be based on inadequate gestational weight gain during pregnancy, which is estimated
to be high in LMICs.14 While this is a biologically sound approach to using BEP, there
is currently no evidence about the efficacy, feasibility, or acceptability of this
type of targeting strategy.
We posit three major motivations for adopting a maternal BMI targeted approach. First,
it would avoid concerns related to the risk of providing food supplements to overweight
and obese women. Second, evidence from efficacy trials categorised by high and low
burden of undernutrition would suggest that undernourished women are most likely to
benefit.10 Third, this approach would be more cost-effective and many more at-risk
women would have access to this effective intervention than is achievable with the
current guidelines. In a world that is increasingly heterogenous, we must question
global ‘one-size-fits all’ guidelines15; precision public health approaches are urgently
needed. Segmentation, targeting and applying an equity (not equality) lens is likely
to yield high impact, cost-effective outcomes that will aid us in reaching the Sustainable
Development Goal targets faster. The Bill & Melinda Gates Foundation is currently
funding ongoing research in South Asia and Africa testing ready-to-use food supplements
for pregnant (and lactating) women designed to meet the macro (protein and energy)
and micronutrient specifications as set by an expert group16 and targeting <25 BMI
women; these trials will generate further evidence on the impact on birth outcomes
(figure 2).
An increasing recognition of the intergenerational nature of health and development
may lead some to suggest that it is insufficient to simply improve nutrition in pregnancy,
arguing that improving health during preconception, adolescence, early childhood,
or even when the mother herself was a fetus is necessary to fully optimise health
in the future offspring. However, as argued by Garza,17 it is unlikely that growth
constraints in parents in utero or as children could explain a high proportion of
current child growth failure and that increases in growth can be achieved within a
generation with appropriate nutrition and care despite the adversities faced by the
previous generation.18 While social and economic development, as well as gender equity,
are essential for women and children to achieve their full potential, it is not a
reason to deprioritise an effective, ready-to-implement intervention that can begin
to address the intergenerational nature of growth failure. Applying an equity and
gender lens to the problem, many millions of women who become pregnant each year should
not be deprived the right and chance to have healthier babies.
Both as individuals and as influencers of the health and well-being of their families,
women and girls hold roles in their community that make them critical drivers of development.
Receiving the appropriate nutrition is essential for them to reach their potential
and meaningfully contribute to their communities—by succeeding in school, achieving
their maximum work productivity, and having their own healthy children, if they so
choose. We advocate for targeted balanced energy and protein supplementation for pregnant
(and lactating) women in low-income and food insecure contexts as an important strategy,
alongside use of micronutrient supplementation and nutrition counselling, for changing
the health trajectories of current and future generations.