Factors associated with concurrent wasting and stunting among children 6–59 months in Karamoja, Uganda

Abstract Children with concurrent wasting and stunting (WaSt) and children with severe wasting have a similar risk of death. Existing evidence shows that wasting and stunting share similar causal pathways, but evidence on correlates of WaSt remains limited. Research on correlates of WaSt is needed to inform prevention strategies. We investigated the factors associated with WaSt in children 6–59 months in Karamoja Region, Uganda. We examined data for 33,054 children aged 6–59 months using June 2015 to July 2018 Food Security and Nutrition Assessment in Karamoja. We defined WaSt as being concurrently wasted (weight‐for‐height z‐scores <−2.0) and stunted (height‐for‐age z‐score <−2.0). We conducted multivariate mixed‐effect logistic regression to assess factors associated with WaSt. Statistical significance was set at p < 0.05. In multivariate analysis, being male (adjusted odds ratio [aOR] = 1.79; 95% confidence interval [CI] [1.60–2.00]), aged 12–23 months (aOR = 2.25; 95% CI [1.85–2.74]), 36–47 months (aOR = 0.65; 95% CI [0.50–0.84]) and 48–59 months (aOR = 0.71; 95% CI [0.54–0.93]) were associated with WaSt. In addition, acute respiratory infection (aOR = 1.30; 95% CI [1.15–1.48]), diarrhoea (aOR = 1.25; 95% CI [1.06–1.48]) and malaria/fever (aOR = 0.83; 95% CI [0.73–0.96]) episodes were associated with WaSt. WaSt was significantly associated with maternal underweight (body mass index <18.5 kg/m2), short stature (height <160 cm), low mid‐upper arm circumference (MUAC <23 cm) and having ≥4 live‐births. WaSt was prevalent in households without livestock (aOR = 1.30; 95% CI [1.13–1.59]). Preventing the occurrence of WaSt through pragmatic and joint approaches are recommended. Future prospective studies on risk factors of WaSt to inform effective prevention strategies are recommended.


| INTRODUCTION
Wasting and stunting are the commonest forms of undernutrition in children under 5 years. Annually, one-third of all deaths in children under 5 years are attributed to undernutrition .
Due to the joint adverse effects of wasting and stunting, children with concurrent wasting and stunting (WaSt) have increased risk of death compared with being wasted alone or stunted alone (Garenne et al., 2019;McDonald et al., 2013;Myatt et al., 2018). The prevalence of WaSt is reported to range from 0% to 8.0% among children aged 6-59 months across 84 countries in Asia, Africa, Europe, Latin America and Oceania . Children with WaSt should be considered as a public health priority group for prevention and curative interventions.
Literature indicates that wasting and stunting share similar causal pathways and consequences (Briend, Khara, & Dolan, 2015;Harding, Aguayo, & Webb, 2018). A pooled odds ratio of 1.4 was estimated for being stunted if wasted and vice versa . Some reports indicate that child age and sex, as well as exposure to food insecurity, are significantly associated with WaSt (Garenne et al., 2019;Myatt et al., 2018;Schoenbuchner et al., 2019). Other studies have focused on factors associated with multiple anthropometric deficits (Fentahun, Belachew, & Lachat, 2016;Hondru et al., 2019). According to Fentahun et al., factors associated with multiple anthropometric deficits are being female, a suboptimal dietary diversity and not being fed special foods during illness (Fentahun et al., 2016). Another study found that children who were concurrently wasted, stunted and underweight were two times more likely to have prolonged days of illness than those who were wasted or stunted (Hondru et al., 2019).
Understanding the correlates of WaSt is important for identifying and designing prevention and treatment strategies. Factors associatedwith the different categories of undernutrition in children have been widely studied. Undernutrition is attributed to complex and interconnected factors; poor dietary intake and morbidity are the proximal factors. Distal factors include poverty and socioeconomic status (UNICEF, 1990). However, few studies have focussed on factors associated with WaSt. We need more information on the correlates of WaSt to support integrated approaches to prevent and treat WaSt, and ultimately to avoid the occurrence of WaSt in children under 5 years. This study aimed to assess the factors associated with WaSt in children 6-59 months in Karamoja Region, Uganda.

| Data source
We conducted secondary data analysis of the June 2015 to July 2018 Food Security and Nutrition Assessment (FSNA) cross-sectional survey datasets conducted in all the seven districts of the Karamoja Region in North-Eastern Uganda. Data was pooled from seven FSNA datasets for the current study. These datasets have been described in detail elsewhere (Odei Obeng- Amoako, Myatt, et al., 2020 (Golden et al., 2006). The FSNA employed a two-stage cluster sampling approach. First, a probability proportional to size sampling Weight and height measurements were collected from nonpregnant women with children aged 0-59 months in the household.
Mid-upper arm circumference (MUAC) was measured for both pregnant and nonpregnant women with children aged 0-59 months.
Weight, height and MUAC measurements were collected from children aged 6-59 months found in the household. Recumbent length was measured for children <24 months old. Bilateral pitting oedema and haemoglobin levels among children aged 6-59 months were also examined. Child age in months was obtained from the child health cards or by maternal recall using a local event calendar.

| Definition of childhood growth indices
We defined wasted as weight for height z-score (WHZ) <−2.0, stunted as height for age z-score (HAZ) <−2.0, and underweight as weight for age z-score (WAZ) <−2.0 based on z-scores of the 2006 World Health Organization (WHO) growth standards (WHO, 2006).
Degrees of anthropometric deficits were defined as no deficit as zscores ≥−2; moderate deficits as z-scores <−2 and ≥−3 and severe deficits as <−3 z-scores. We defined acute malnutrition as wasting

| Study variables
The outcome of our study was WaSt among children aged 6-59 months. We defined WaSt as concurrently having WHZ <−2 and HAZ <−2 . We explored a range of factors likely to be associated with WaSt in children aged 6-59 months in this analysis based on previous literature and on the UNICEF conceptual framework for under-nutrition (UNICEF, 1990). These explanatory variables were classified as child level, maternal level (i.e., caregivers) and household characteristics as well as markers of the food security seasons during which the surveys were conducted.

| Ethical considerations
We received approval to access the Karamoja FSNA datasets from the Office of the Prime Minister, Uganda. We used a de-identified dataset for this analysis. We obtained a waiver of consent to use the

| Child level factors
Child level factors included in the study were age in months, sex and morbidity. We categorized the age of children into 6-11, 12-23, 24-35, 36-47 and 48-59 months (Garenne et al., 2019). Childhood morbidity was reported by the caregivers. The presence of infectious disease was defined as ARI, malaria/fever, and diarrhoea episodes in the last 2 weeks before the survey.

| Household factors and season of survey
The socioeconomic factors included in the analysis were household heads' sex, maternal and household heads' educational level, wealth index, livestock ownership, access to land for cultivation and season of survey. Similar to maternal educational level, we described household head's educational level as no education, 1-7 years (primary) and ≥8 years (secondary and above). We used principal component analysis to generate a wealth index based on household assets ownership (Rutstein & Staveteig, 2014). These household assets were bed, table, chair, mattress, radio/tape, cell phone, sewing machine, bicycle, automobile, motorcycle, television, axe, panga/machete, hoe, oxplough, water tank, seed and food stores (UNICEF, DFID, WFP, FAO, & IBFAN, 2018). We categorized the wealth index from the lowest to the highest as poorest, poor, middle, rich and the richest households using quintiles.
We used household livestock ownership and access to land for cultivation as an independent factor for wealth given that Karamoja is an agro-pastoral setting. Household food consumption scores reflect the diversity and frequency of food items from the different food groups reportedly consumed over the previous 7 days. The food items were grouped into main staples, pulses, vegetables, fruits, meat/fish, milk, sugar and oil. The food consumption scores We evaluated the presence of a latrine in a household as a probable factor associated with WaSt. Sources of drinking water were defined as improved water sources (piped/tap, protected well/spring and borehole fitted with a hand-pump) and unimproved water sources (surface water, river, dam, runoff, rainwater collected in a tank and water from open well/spring) (WHO & UNICEF, 2006). The association between food security seasons and the occurrence of WaSt was also examined. FSNA surveys were conducted in May/June for the lean (hunger or preharvest) and in November/December for the nonlean (postharvest) seasons.

| Study population
Children aged 6-59 months were included in the analysis. We used WHO flags for outliers; HAZ <−6 and HAZ >6, WAZ <−6 and WAZ >5, and WHZ <−5 and WHZ >5 were excluded as biologically implausible z-scores values (WHO, 2009). Given that WaSt was the outcome variable, children with incomplete data on WHZ or HAZ or both were excluded from the study. Children with bilateral pitting oedema, height <45 and >120 cm and MUAC >20 cm were also excluded from the dataset (MoH Uganda & UNICEF, 2016). The maternal MUAC measurements which were out of range of upper quartile +3.0× interquartile range (IQR) and lower quartile −3.0× IQR were censored as outliers (Healy, Chambers, Cleveland, Kleiner, & Tukey, 1984).

| Data management and analysis
All statistical analyses were conducted using STATA 13.0. We also analysed anthropometric z-scores per WHO growth standards in STATA (Leroy, 2011). We used descriptive statistics to summarize continuous variables using medians and IQRs and categorical variables using percentages.
We used multivariate mixed-effect logistic regression to assess child level, maternal and household level, socioeconomic and seasons factors associated with WaSt. Mixed-effect logistic regression method adjusted for the clustering effect of the multistage sampling design used in the FSNA survey. In the multivariate analysis we only included explanatory variables with p < 0.2 from the bivariate regression analysis. Multicollinearity of the variables was assessed by using the variance inflation factor (VIF > 10). In the multivariate analysis, we used a backward stepwise method to remove the nonsignificant variables (p > 0.05). To identify variables with interaction effects in the model, we assessed the significance (p > 0.05) of each interaction term one at a time in the basic model, but none of the interaction terms was conceptually meaningful. We found no confounding factors in our model after testing for a ≥10% change in the effect measure in the presence of another variable. We retained maternal stature and season of the survey in the final model although they were dropped during the backward stepwise process based on literature Harding et al., 2018). Akaike information criterion (AIC) and Bayesian information criterion (BIC) methods were used to assess for the goodness of fit of our model.
Factors associated with WaSt were reported by adjusted odds ratio (aOR) at 95% confidence interval (CI). We set statistical significance at p < 0.05 in this analysis.

| Characteristics of the study participants
The study involved 33,054 children aged 6-59 months with available data on sex, wasting and stunting ( Figure 1). About half (50.4%) of the children in the study sample were females. The median age of the children was 26 months (IQR: 15, 38), and about 44.3% were in the age group 6-23 months (Table 1). About 9.9% of the children had a diarrhoea episode and 26.0% had acute respiratory infection (ARI) in the 2 weeks before the survey. Nearly 59.6% of the children had caregivers with no formal education and about 27.0% of the caregivers were underweight (BMI < 18.5 kg/m 2 ) (  (Table 2). WaSt was more common among children aged <36 months than those aged >36 months.
Stunting was the most prevalent form of undernutrition across the different age groups (Figure 2).

| Factors associated with WaSt
Several child-level, maternal, household, socioeconomic and seasonal variables were associated with WaSt at bivariate and multivariate analyses (Table 3) (Victora, de Onis, Hallal, Blossner, & Shrimpton, 2010). These findings highlight the need to target younger children particularly those <36 months for infant and young child feeding, growth monitoring and promotion interventions.
In our analysis, recent morbidity of ARI and diarrhoea infections in the past 2 weeks prior to the survey increased the odds of WaSt in children. Our results are in line with previous studies, which showed that children with multiple anthropometric deficits were more likely to experience any morbidity including ARI (Fentahun et al., 2016). The relationship between undernutrition and infections is synergistic; undernutrition is a risk factor for infection and vice versa (Scrimshaw & SanGiovanni, 1997). It is well established that diarrhoea is associated with undernutrition (Guerrant, Schorling, McAuliffe, & de Souza, 1992). An analysis of nine longitudinal datasets showed that the odds of stunting increased by 1.13 for every five episodes of diarrhoea and 25% of all stunting was attributed to five previous episodes of diarrhoea (Checkley et al., 2008). In another analysis, diarrhoea episode was attributed to weight loss, and a small but measurable decrease in linear growth over the long term (Richard et al., 2013).
Furthermore, we found that children with malaria/fever had a reduced risk of having WaSt. Evidence on the relationship between malaria and undernutrition remains inconclusive as some studies have found no influence of malaria on the occurrence of wasting and stunting (Das et al., 2018). Studies in Ethiopia and Uganda found malaria/fever infection to be strongly associated with stunting and wasting (Gari, Loha, Deressa, Solomon, & Lindtjorn, 2018;Wamani, Astrom, Peterson, Tumwine, & Tylleskar, 2006). A recent analysis showed that children with concurrent wasting, stunting and underweight had 1.34 odds of experiencing prolonged days of illness (Hondru et al., 2019). These findings show that children with WaSt are at high risk of morbidity. Therefore, prompt treatment and prevention of infections through integrated approaches to improve caregivers' care practices, household socioeconomic status and environmental health are recommended (Dodos et al., 2018).
Children of caregivers who had over four live-births were more likely to experience WaSt compared with children who had caregivers with less than three live-births. WaSt was strongly associated with low maternal BMI, stature and low MUAC in this analysis. These findings resonate with a previous analysis that shows that low maternal BMI and stature were associated with wasting and stunting (Martorell & Young, 2012). In another study, children whose is evidence that foetal growth is restricted during pregnancy in women of short stature and low BMI . Pregnant women with low BMI, short stature and low MUAC had a high risk of maternal, neonatal and child death and low birth weight Christian et al., 2008;Nyamasege et al., 2018;Ververs et al., 2013). Poor maternal nutritional status could be an indication of poor household feeding practices.
In the present study, we also found that the children whose caregivers were overweight were 0.38 times less likely to be WaSt, although this effect was not statistically significant. These findings imply that in protracted food insecure contexts there could be some overweight/obese caregivers, probably food secure with high socioeconomic status who could afford to feed their children adequately.
Maternal and child undernutrition are interconnected and have longterm and intergenerational consequences (Victora et al., 2008).
Wasting and stunting co-exist at birth and persist concurrently over time in some children . Therefore, interventions targeted at improving maternal and child nutrition, health and wellbeing should focus on the first 1,000 days (i.e., from conception until 24 months) of a child's life (Schwarzenberg & Georgieff, 2018).  Wamani et al., 2006). Parental education especially the mother's education and household wealth index are important socioeconomic correlates of undernutrition; these characteristics may influence child feeding and care practices and the enabling environment for child growth and development (Akombi et al., 2017;Wamani et al., 2006).
The risk of WaSt was higher among children in a household without livestock. A previous report showed that a 10-fold increase in household livestock ownership had a significant association with lower stunting prevalence in Ethiopia and Uganda, but not in Kenya (Mosites et al., 2015). Karamoja is predominantly pastoralist and agro-pastoralist, and household livestock ownership is indicative of wealth, resilience and livelihood. Apart from being used as food, livestock rearing is a financial livelihood that can serve as credit, asset-based insurance and agricultural labour for land traction (Behnke & Arasio, 2019). Actions for improving livestock productivity in Karamoja should be a priority because of the beneficial effects on child nutrition and well-being.
Our analysis showed no significant association between seasons and WaSt. However, earlier analyses showed that food security seasons were predictors for wasting and stunting in a Gambian longitudinal study (Schoenbuchner et al., 2019) and a cross-sectional study conducted in Somalia (Kinyoki et al., 2016). Karamoja is chronically food insecure and prone to recurrent drought and sporadic flooding. These harsh living conditions make children susceptible to malnutrition and infectious diseases. In such a setting, persistent stunting will be more common than persistent wasting (Richard et al., 2012). The actual burden of wasting may not be revealed in cross-sectional data; this may be because wasting is an acute condition and wasted children die or recover over a short period. Wasting is appropriately measured by incidence (Isanaka, Boundy, Grais, Myatt, & Briend, 2016 approaches to prevent and treat simultaneous wasting and stunting in children (Bergeron & Castleman, 2012). Future programmatic and policy decision making should consider interventions that promote linear and ponderal growth at the same time (Harding et al., 2018). In the context of high undernutrition burden, children with WaSt should be recognized as a public health priority group for treatment given the heightened risk of death associated with WaSt.

| Strengths and limitations
Previous analyses reported on factors associated with the different forms of nutrition outcomes. To the best of our knowledge this is the first study to assess factors associated with WaSt, a useful composite indicator for wasting and stunting .
However, the interpretation of our study should consider some limitations commonly associated with a secondary dataset. The likelihood of random error because of a fixed sample size may have been offset by the large sample used in the present analysis. We may have introduced selection bias by excluding about 21% of the children with incomplete data, missing data, and implausible anthropometric data. Nevertheless, children who were excluded from the study had similar sex distribution patterns, though they were younger.
Missing data and erroneous anthropometric measurements by field enumerators were probable sources of information bias in the FSNA dataset. However, information bias was likely to be minimal due to the regular and standardized training of field enumerators and the use of standard operating procedures for sampling and data collection during each round of the survey.
Given that the present study was based on existing dataset, we were limited to explore the effects of the variables found in the FSNA dataset. We could not easily infer causality of WaSt because the dataset was cross-sectional. Moreover, wasting has a shorter duration and is more seasonally variable compared with stunting.
Therefore the true burden of wasting may be under-reported in prevalence data (Khara & Dolan, 2014). However, the results presented in this report could be useful baseline information for future studies on factors associated with WaSt and provide useful evidence for decision making on interventions for the prevention and treatment of WaSt.

| CONCLUSION
WaSt was significantly associated with the child's age, sex, ARI and diarrhoea episodes especially among children whose caregivers had low BMI, short stature, low MUAC, ≥4 live-births and low socioeconomic status. Cost-effective interventions aimed at preventing and treating childhood illnesses and improving prenatal and maternal nutrition, women empowerment and socioeconomic status will be beneficial for early childhood nutrition and well-being. Existing programmes and interventions such as community-based management of acute malnutrition (CMAM) designed solely for the treatment of wasting, food and micronutrient supplementation, infant and young child feeding programme, social safety net, and hygiene and sanitation promotion for stunting prevention should be adapted to address both conditions, especially in high burden settings like Karamoja. There is a need to identify and test how integrated packages of nutrition-sensitive and nutrition-specific interventions can be targeted at reducing wasting and stunting in children. Future prospective studies on the risk factors of WaSt are needed to improve our understanding of the causality of WaSt.

ACKNOWLEDGMENTS
We are grateful to all staff of UNICEF, WFP, the Makerere University

CONFLICTS OF INTEREST
The authors declare no conflicts of interest.