The relationship between wasting and stunting in young children: A systematic review

Abstract In 2014, the Emergency Nutrition Network published a report on the relationship between wasting and stunting. We aim to review evidence generated since that review to better understand the implications for improving child nutrition, health and survival. We conducted a systematic review following PRISMA guidelines, registered with PROSPERO. We identified search terms that describe wasting and stunting and the relationship between the two. We included studies related to children under five from low‐ and middle‐income countries that assessed both ponderal growth/wasting and linear growth/stunting and the association between the two. We included 45 studies. The review found the peak incidence of both wasting and stunting is between birth and 3 months. There is a strong association between the two conditions whereby episodes of wasting contribute to stunting and, to a lesser extent, stunting leads to wasting. Children with multiple anthropometric deficits, including concurrent stunting and wasting, have the highest risk of near‐term mortality when compared with children with any one deficit alone. Furthermore, evidence suggests that the use of mid‐upper‐arm circumference combined with weight‐for‐age Z score might effectively identify children at most risk of near‐term mortality. Wasting and stunting, driven by common factors, frequently occur in the same child, either simultaneously or at different moments through their life course. Evidence of a process of accumulation of nutritional deficits and increased risk of mortality over a child's life demonstrates the pressing need for integrated policy, financing and programmatic approaches to the prevention and treatment of child malnutrition.


| INTRODUCTION
Undernutrition remains a major public health concern in many countries and an underlying cause of almost half of global child mortality (Black et

Key messages
• A significant proportion of wasting and stunting is present at birth and can contribute to further growth failure during subsequent infancy and childhood. Improving maternal health and nutrition in pregnancy and early life could have a critical role in the prevention of wasting and stunting.
• Periods of wasting leave a child more likely to experience stunting and, to a lesser extent, vice versa. Common risk factors drive an accumulation of vulnerabilities. This underlines the need for cohesive policies and the implementation of services and activities to prevent both wasting and stunting.
• Concurrently wasted and stunted children have an elevated risk of death and should be considered as a highrisk group in the targeting of treatment.
• A combination of weight-for-age Z score and mid-upperarm circumference may be the most effective way to identify children at highest risk of mortality, including those concurrently wasted and stunted. Further evidence is needed to understand the operational implications.

| Search strategy
We identified search terms to describe wasting and stunting and the relationship between the two conditions, including implications for ponderal and linear growth. The search terms are listed in Figure 1.

We searched Medline, Embase and global health databases through
Ovid, applying limits for studies published after 2012 to allow for any studies that may have been missed in the 2014 review and for the age of the individuals included in studies. We also issued a call for studies known to the WaSt TIG members in May 2020. The final search was conducted in June 2020. Both the search strategy and the eligibility criteria were guided by the Population, Intervention, Comparison, Outcome (PICO) framework in order to delineate the question of focus for the review and to define inclusion and exclusion criteria. The PICO is presented in Table 1.

| Eligibility criteria
We reviewed studies from low-and middle-income countries (LMICs) where wasting and stunting are most prevalent. As wasting and stunting commonly occur in children under 5 years of age, we applied age limits from 0 to 59 months. We considered studies in the review that assessed both ponderal growth/wasting and linear growth/ stunting as well as the association between the two. Included studies focused on prevalence, physiological mechanisms and outcomes related to growth and mortality. We included all types of studies that involved primary research (case control studies, cross-sectional studies and secondary data analyses). We also included reviews if they presented pooled analysis or new insights into the relationship between wasting and stunting. Both peer-reviewed papers and grey literature identified through the search were considered for inclusion.
We excluded studies that assessed wasting and stunting separately and that did not report on either condition in relation to the other. Also excluded were studies that focused on obesity,  We identified three main themes before extraction: physiological understanding of the similarities in wasting and stunting, the interrelationship between the two conditions and the implications of this relationship and then extracted data along these lines. We extracted data into an Excel spreadsheet including information on authors, titles, dates of publication, sample size, data/information relevant to each theme and any research recommendations and conclusions.

| Risk of bias assessment
We assessed the quality of included studies using an adapted version of the SIGN checklists (https://www.sign.ac.uk/what-we-do/ methodology/checklists/). We selected the SIGN checklists as they provide a checklist of items for case-control and cohort studies, study designs commonly used in the studies selected for this review. Adaptation was necessary due to the varied nature of the studies included.
We assessed factors such as clearly defined objectives, study design, definition of participants, exposures and outcomes, statistical methods, addressing of bias and potential confounders and the presentation of results.

| Study selection
The results of the search process are presented in Figure 2. The database search identified 2486 studies and reports and an additional 12 studies came from WaSt TIG members. After removing duplicates, 983 studies and reports remained, of which 867 were excluded following initial screening. One hundred and sixteen full text studies and reports were assessed for eligibility of which 71 were excluded. The reasons for exclusion are given in Figure 2. We included a total of 45 studies and reports in our final review.

| Study characteristics and risk of bias
We present the characteristics of each included study or report in

| Interconnected physiological processes
We reviewed studies that considered the physiological processes underlying the potential interaction between wasting and stunting, either as the primary objective or within the discussion.

Priority research questions for wasting and stunting identified
Research is needed into wasting and stunting in order to inform global health efforts to address undernutrition 2 ✓ The highest incidence of stunting onset occurred from birth to 3 months of age. From 0 to 15 months of age, less than 5% of children per month reversed their stunting status and, among those who did, stunting relapse was common.
Preventive intervention within prenatal and early postnatal phases, coupled with continued delivery of postnatal interventions through the first 1000 days of life, are key to overcoming the early occurrence and low reversal rates of stunting.
3 ✓ No incidence of overweight or adiposity.
Children age ≥6 months with a height less than 65 cm will not become overweight or obese following RUTF treatment with MUAC as admission and discharge criteria.

4
✓ Fat loss and muscle mass loss are associated with both wasting and stunting. Hormones produced by fat play a crucial role in immune function and bone growth which might explain reduced linear growth in the case of low WHZ.
Crucial to prevent both wasting and stunting in order to reduce malnutrition related mortality.

5
LBW was associated with higher odds of wasting, stunting and underweight. Control of stunting likely a result of control of infectious disease. Increase in reduced WHZ requires further investigation.

9
✓ ✓ ✓ Wasting and stunting are correlated. Concurrent wasting and stunting peaks around 30 months and is higher in boys than girls, but this difference could not be explained by muscle mass or fat mass measured by arm or muscle circumference, triceps or subscalpular skinfold.
Concurrent wasting and stunting is a strong risk factor for mortality.

10
Key determinants of child stunting are also significant determinants of child wasting in Asia.
The co-occurrence of wasting and stunting requires more integrated interventions. That is, programmes aimed at preventing LBW and poor IYCF to avert stunting should be linked more effectively with actions aimed at the management of wasting.

11
LBW strongly associated with wasting and wasting and stunting.
Programmes aimed at preventing LBW and poor IYCF (to reduce stunting) should be linked with actions aimed at the management of wasting. CMAM programmes should adapt to consider stunting as well as wasting.

13
✓ High burden of stunting in wasting treatment programme. Stunting did not impair response to treatment. There was limited linear growth in this population.
There is a direct relationship whereby inadequate weight is associated with slowed linear growth. Wasting contributes to stunting.

Half of weight gained by children during SAM treatment was fat free mass (FFM) and the FFM of treated children at recovery was similar to community controls indicating incomplete FFM recovery during SAM treatment.
There is no evidence from this study of a differential effect of a reduced RUTF dose on the tissue accretion of treated children when compared with standard treatment suggesting that, in a relatively food secure context, a reduction in the RUTF dose can result in similar body composition by recovery.

15
Underweight was associated with both stunting and wasting. There was no association between stunting and wasting. There is no a three way interaction among stunting, wasting and underweight.
Wasting, stunting and underweight should be considered simultaneously to estimate the actual burden of childhood undernutrition.

16
✓ Concurrent wasting and stunting highest in 12-24 months age group and males. Fragile and conflict affected states have higher concurrence than stable countries.
Concurrent wasting and stunting represents a high risk group. Investigations needed to ensure this group is being reached.

17
Determinants of wasting are similar but patterns in correlation are variable.
Wasting, stunting and underweight have common risk factors. Joined up programming is required to address wasting and stunting.

18
Higher burdens of enteropathogens were associated with elevated biomarker concentrations of gut and systemic inflammation and indirectly associated with both reduced linear and ponderal growth.
The strongest evidence for environmental enteropathy was the association between enteropathogens and linear growth mediated through systemic inflammation.

19
✓ More stunting found in case group. Sitting height was similar across groups suggesting preservation of torso growth. SAM has long term adverse effects on growth and body composition.

20
Hazarad ratio for stunting, wasting and underweight was 12.3. Children with multiple anthropometric deficits are at increased risk of mortality.

21
✓ Children who experienced early ponderal or linear growth failure were at higher risk of persistent growth failure and were more likely to die by age 24 months.
A focus on pre-conception and pregnancy is key for preventive interventions.
T A B L E 2 (Continued) Wasting incidence is five-fold higher than prevalence estimates suggest. Peak incidence is between 0 and 3 months.

No
New focus is required to extend preventive interventions for child wasting to pregnant and lactating mothers and children below age 6 months.

23
Concurrent wasting and stunting is prevalent in Southeast Asia.
Both preventive and curative approaches are needed to address wasting in Southeast Asia.

24
✓ MUAC and WAZ detected all near-term deaths associated with anthropometric deficits, including concurrent wasting and stunting.
Therapeutic feeding programmes should consider WAZ and MUAC admission criteria.

25
✓ ✓ Children who are wasted and stunted are also underweight. Concurrently wasted and stunted children have a high risk of mortality.
Therapeutic feeding programmes should include concurrent wasting and stunting given the high risk of mortality.

26
The CIAF supports the assessment of the relationship between malnutrition, morbidity and poverty.
Efforts to reduce poverty and increase living standards are needed to support reduction of malnutrition.

27
✓ No significant increase in HAZ at 1 year follow-up after inpatient treatment for complicated SAM, despite MUAC growth and weight gain. Linear growth was associated with less severe wasting and more stunted and with fewer comorbidities at admission.
Intensive nutritional rehabilitation did not resolve stunting.

28
Associations found between wasting and underweight and stunting and underweight but no association found between wasting and stunting.
Wasting, stunting and underweight are valid measures which cannot represent each other.

29
✓ MUAC was the strongest predictor of mortality followed by WAZ.
MUAC is a better predictor of mortality in this study population.

30
✓ ✓ All concurrent wasted and stunted children were also underweight. Concurrent wasting and stunting prevalence of 5% raises public health concerns. WaSt was more common among younger children and males, but the majority of WaSt children with low MUAC were female.
Consider the integration of WAZ into therapeutic feeding programmes to detect and treat concurrent wasting and stunting.

31
✓ ✓ ✓ High number of stunted children in wasting treatment programme.
Existing therapeutic feeding protocols can be used to detect and effectively treat children with concurrent wasting and stunting.

34
✓ Infants born with growth deficits will likely continue to have growth deficits as they progress along growth trajectories.
Research is needed to understand causal pathways to growth faltering.

35
A small sub-sample of the population was found to be both wasted and stunted.
The study makes recommendations for programme-specific data and measurementrelated improvements to enable more meaningful analysis.

36
Children with wasting only in early life had similar LAZ at 18-24 months than those with no wasting. More recent wasting was associated with lower LAZ.
Wasting is associated with the process of stunting. Prevention of wasting could increase attained stature in children.

37
✓ ✓ MUAC <125 mm should not be used as a standalone criteria for wasting given its strong association with age, sex and stunting and its low sensitivity to detect slim children.
Further research is needed to better understand the clinical and physiological outcomes of the various anthropometric indicators of malnutrition.

38
Children who were wasted were more at risk of stunting.
WHZ relates to linear growth. Stunting and wasting share common determinants therefore prevention of both wasting and stunting will positively influence linear growth.

39
✓ Associations that were insignificant for wasting and stunting individually were significant for concurrent wasting and stunting. Mosquito nets and lack of diarrhoea in the last two weeks were both protective of concurrent wasting and stunting.
Concurrent wasting and stunting should be a key consideration for nutrition programming in Guinea-Bissau.

40
✓ ✓ ✓ Being wasted was predictive of stunting, even accounting for current stunting. Boys more likely to be wasted, stunted and underweight than girls, and are more susceptible to seasonally driven growth deficits.
Stunting is in part a biological response to previous wasting highlighting the policy implications of recognising the importance of wasting.

41
Children who have a low WHZ but a MUAC above the cut-off would be omitted from diagnosis and treatment. In addition to simple tools for case finding, the use of WHZ should be used whenever possible.       Were the number of participants at each stage of the study (including loss to follow-up) well described?

42
Were characteristics of the study participants described?
Were outcome indicators clearly reported? Have estimates (adjusted where relevant) and associated confidence intervals been reported?
Were study limitations recognised?

| Evidence for the relationship between wasting and stunting
Population  Table 2

| Stunting leading to wasting
We also identified evidence to support a direct relationship whereby

| Concurrent wasting and stunting
Some studies conducted since the 2014 review have focused on identifying the burden and implications of concurrent wasting and stunting. We identified studies that explored the prevalence and

| Mortality implications of concurrent wasting and stunting
We identified six studies that explored the mortality implications of

| Wasting treatment outcomes and stunting
As stated above, stunting is highly prevalent among wasted children admitted to therapeutic feeding programmes (

| Ongoing research priorities on the relationship between wasting and stunting
We identified one study that focused on the identification of research priorities for concurrent wasting and stunting (Bhutta et al., 2016).

| CONCLUSION
The ongoing accumulation of evidence since the 2014 review demonstrates progress in improving the understanding and awareness of the relationship between wasting and stunting. The findings of this review are supportive of a strong relationship between these two manifestations of undernutrition and provide a better understanding of which groups should be considered at risk and therefore prioritised for treatment.
Evidence on the cumulative effects of nutritional deficits, and therefore risk over the life course of a child beginning in-utero, demonstrates the need for a more integrated approach to prevention and treatment strategies in order to interrupt this process. To achieve this, further progress is needed to overcome the divide that has typified undernutrition policy, programme, financing and research initiatives.