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Factors associated with the coexistence of anemia and undernutrition among children aged 6–59 months in Mali, 2023/24: A multilevel mixed-effects analysis

  • Halid Worku Jemil ,

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Supervision, Validation, Writing – original draft, Writing – review & editing

    halidworku288@gmail.com

    Affiliation Department of Health Informatics, College of Medicine and Health Science, Wollo University, Dessie, Ethiopia

  • Sonia Worku Semayneh,

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Resources, Writing – original draft, Writing – review & editing

    Affiliation Department of Oncology, Addis Ababa University College of Health Science Tikur Anbessa specialized hospital, Addis Ababa University, Addis Ababa, Ethiopia

  • Eyob Tilahun Abeje,

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Software, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, School of Public Health, College of Medicine and Health Sciences, Wollo University, Dessie, Ethiopia

  • Altaseb Beyene Kassaw,

    Roles Data curation, Investigation, Methodology, Project administration, Resources, Validation, Visualization, Writing – review & editing

    Affiliation Department of Biomedical Science, College of Medicine and Health Science, Wollo University, Dessie, Ethiopia

  • Gosa Mankelkl,

    Roles Conceptualization, Data curation, Funding acquisition, Methodology, Project administration, Resources, Validation, Writing – original draft, Writing – review & editing

    Affiliation Department of Biomedical Science, College of Medicine and Health Science, Wollo University, Dessie, Ethiopia

  • Anmut Endalkachew Bezie,

    Roles Conceptualization, Data curation, Methodology, Software, Validation, Writing – original draft, Writing – review & editing

    Affiliation Department of Occupational and Safety, College of Medicine and Health Science, Wollo University, Dessie, Ethiopia

  • Adisu Meles Kabtyimer

    Roles Data curation, Investigation, Resources, Writing – review & editing

    Affiliation Department of Epidemiology and Biostatistics, School of Public Health, College of Medicine and Health Sciences, Wollo University, Dessie, Ethiopia

Abstract

Introduction

coexistence of anemia and undernutrition is a major public health concern among children in Mali. However, there is a lack of study looking into the relationship between undernutrition and anemia among children in Mali. Therefore, this study was conducted by using multilevel analysis to identify significant factors associated with the coexistence of anemia and undernutrition among children.

Methods

A cross-sectional design was conducted from Mali Demographic and Health Survey data from 2023/24. STATA 17 was used for data summarization and analysis. The model was evaluated using the intra-class correlation coefficient (ICC), median odds ratio (MOR), likelihood ratio (LR), and deviance. Variables with a p-value less than 0.2 in the bi-variable logistic regression analysis were taken into account for the next multilevel analysis. In the multilevel analysis, significant factors were presented using the Adjusted Odds Ratio (AOR) along with the 95% Confidence Interval (CI).

Results

The prevalence of the coexistence of anemia and undernutrition among children was 26.3% (CI: 25.2%, 27.4%). According to the multilevel logistic regression result, mothers aged 25–34 years (AOR = 1.41; 95% CI: 1.01, 1.96), no education (AOR = 1.51; 95% CI: 1.19, 1.91), primary education (AOR = 1.39; CI: 1.05, 1.84), not covered by health insurance (AOR = 2.18; 95% CI: 1.05, 2.47), rural residents (AOR = 1.46; 95% CI: 1.16, 1.84), and short maternal stature (AOR = 1.83; 95% CI: 1.49, 2.27) were associated with an increased odds of the coexistence of anemia and undernutrition among children. In contrast, tall maternal stature (AOR = 0.29; 95% CI: 0.22, 0.36) and children aged 37–47 months (AOR = 0.70; 95% CI: 0.50, 0.96) were associated with decreasing the odds of the coexistence of anemia and undernutrition among children.

Conclusion

In Mali, the coexistence of anemia and undernutrition contributes to mortality and related complications among children. The finding from this study revealed that children whose mothers were aged 25–34, mothers without formal education, mothers without primary education, mothers whose health was not covered by health insurance, children who lived in rural areas, and maternal short stature were associated with increased odds of the coexistence of anemia and undernutrition among children. In contrast, tall maternal stature and children aged 37–47 were associated with decreasing the odds of the coexistence of anemia and undernutrition among children.

Introduction

Anemia is a condition in which red blood cell or hemoglobin levels fall below an average [1]. Undernutrition refers to a mild, moderate, or severe nutritional deficiency needed for body growth and development. It encompasses stunting, wasting, and underweight [2,3]. According to the WHO, anemia and undernutrition were indicators for assessing hemoglobin deficiency, and micro/macro-nutritional status in children, respectively [46]. Both anemia and undernutrition were caused by insufficient iron as well as nutritional deficiencies and recurrent infections [79]. Collectively, anemia and undernutrition result in negative health consequences like poor ability to carry oxygen in the blood [10], poor emotional well-being [11], delays in body growth [1215], impaired immune systems [1618], poor cognitive and mental development in children [17,19,20], an increased chance of chronic disease [21], and a higher susceptibility to infections and pathogens [22]. Generally, the combined effects of both anemia and undernutrition affect development, poor growth, and challenges in motor skills [23], and impair physical and social well-being [24,25].

According to the World Health Organization, in 2017, 41.7% of children worldwide under the age of five were affected by anemia [26,27]. In 2019, 89% of all disabilities in poor nations were caused by anemia, with 21%, 18%, and 1% of children suffering from mild, moderate, or severe anemia, respectively [28]. Additionally, the coexistence of anemia and undernutrition was more exacerbated in developing countries [29,30]. Similarly, the coexistence is higher in poor-income countries contribute to more than half of global deaths among children under five years [31]. Likewise, both anemia and undernutrition were significantly higher in Western Africa [29]. In 2018, the Mali Demographic and Health Survey reported that 88% of children under five are considered anemic [32]. According to the Mali Demographic and Health Survey, the prevalence of undernutrition among under-fives was a decreasing trend over time. In 2010, stunting (47%), underweight (13%), and wasting (4%) [33,34]. In 2015/16, stunting decreased to 37%, underweight (12%), and wasting (3%), and anemia declined from 73% in 2004 to 63% in 2010 and remained constant to 2015/16.

Anemia and undernutrition share a common strong bidirectional biological and phonological connections which needs a thorough examination. Although many studies have been conducted in Mali, most of them examined the risk factors of anemia and undernutrition individually. Hence, the relationship between anemia and undernutrition received little attention in most of the literature so far, and there is a few study looking into the relationship between undernutrition and anemia among children in Mali. Earlier research that examined these topics individually may not truly show how they are connected to one another [35]. A strong emphasis should be given to examining the link between anemia and undernutrition [29,30,35]. Therefore, this study was examined to investigate the coexistence of anemia and undernutrition among children in Mali using multilevel mixed-effect logistic regression analysis from the MDHS 2023/24 dataset.

Methods

Data source and data collection tools

We employed secondary data from the MDHS, 2023/24. The DHS is a nationally representative survey that provides overall data on different health and demographic indicators. The DHS contains information about the child’s health and nutrition, including vaccination profiles. The data collectors received training about the interviewing techniques, confidentiality, and respondent safety in Mali. In addition, before administering the questions, informed consent was gained from all respondents. DHS uses a standardized and validated questionnaire where hemoglobin levels are collected by measuring the hemoglobin levels using capillary blood samples obtained via finger or heel prick and analyzed on-site using a portable HemoCue Hb analyzer by using standardized procedures. Similarly, the anthropometric measurements were collected by measuring the children’s height and weight by professionals using calibrated measuring boards and digital scales, in alignment with the standards set by international protocols [36].

Study area and participants

This study was conducted in Mali; geographically, it is located between latitudes 10°N and 25°N and longitudes 12°W and 4°E. Its capital is Bamako. With a land area of roughly 1,240,192 km², Mali is the eighth-largest nation in Africa. The source population includes all children aged 6–59 months who reside in Mali, while the study population consists of those children who are present in Mali during the enumeration period.

Sampling method and sample size determination

The DHS used a cross-sectional design, with a two-stage stratified sampling technique was employed to select representative study participants. In the first stage, enumeration areas were selected using probability proportional to the size of each area, making sure the selection was done independently in every sampling group, stratified by region and urban/rural residence. Then, second, a fixed number of households were systematically chosen from each selected cluster. In DHS the probability of selecting women in households is not uniform; hence, we apply a sampling weight in all analyses to correct for unequal selection and to confirm representativeness. The main DHS indicators were collected from the Measure DHS program website, https://www.dhsprogram.com [37]. A weighted 15,631 children aged 6–59 months were included in this study. From those, 954 dead children and 8,386 children who did not take hemoglobin and anthropometric measurements during the enumeration period were excluded from the study. Finally, a total sample of 6,291 children were used for the final analysis (Fig 1).

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Fig 1. Sample extraction procedure for the coexistence of anemia and undernutrition among children in Mali 2023/24.

https://doi.org/10.1371/journal.pone.0351864.g001

Study variables and operational definition

The outcome variable was the coexistence of anemia and undernutrition (Co-AnUn), operationalized according to the WHO child growth reference standard as the presence of both low hemoglobin levels and inadequate nutritional status.

Stunting was dichotomized into a binary category if the child’s Z-score HAZ < −2 SD; the children were categorized as stunted, else not stunted [3840].

Wasting was dichotomized into a binary category; if the child’s WHZ score was less than −2 SD, the children were categorized as wasted, else not wasted [41,42].

Underweight was dichotomized into a binary category if the child WAZ-score < −2 SD the children were categorized as underweight, else not underweight [38,43,44].

Undernutrition dichotomized into a binary category by merging stunting (if the child’s HAZ is < −2 SD), wasting (WHZ score is < −2 SD), and underweight (WAZ score is < −2 SD). Children were considered undernourished if they met at least one anthropometric failure (HAZ, WHZ, and WAZ Z-scores were < -2 SD). and non-undernourished if their Z-score was >= -2 SD [30,38].

Anemia was classified in two binary categories as anemic if the child’s hemoglobin level is < 11 g/dl and not anemic if the hemoglobin level is > 11 g/dl [4547].

Coexistence of undernutrition and anemia they were merged if a child met the criteria for both anemia and at least one of the undernutrition indices (wasting, stunting, or underweight), Anemia ∩ undernutrition indices = Co-AneUn [48,49].

Independent variables

Individual-level variables mother’s occupation, mother’s age, mother’s education, marital status, wealth status, birth order, mother’s height, child age (S1 Fig).

Community-level variables place of residence, health insurance coverage, distance to health facility, toilet type, family size, and media exposure (S1 Fig).

Maternal height was categorized into three groups: short if a woman’s height is <= 1.50 m, normal if a woman’s height is between 1.5 m and 1.59 m, and tall if a woman’s height is >= 1.60 m [50].

Media exposure was dichotomized into two categories by merging three variables together: mothers listening to the radio, watching TV, or reading a magazine. If the mother was exposed to at least one of these, we consider her exposed to media; otherwise, we consider her not exposed to media [51].

Data management and analysis

To identify the associated factors of Co-AnUn, we first generated descriptive statistics and tabulated the proportion of Co-AnUn and selective independent factors. Similarly, we performed using STATA 17. Similarly, we adjusted the data for both the outcome and predictor variable using DHS sample weights for before analysis and to compute descriptive statics. This helps to correct for unequal probability of selection and to ensure a national representativeness of samples. The multicollinearity was checked before analysis. Further, variables with a p-value < 0.2 in the bivariable analysis were considered in the multilevel analysis.

Multilevel binary logistic regression analysis

The DHS used multistage sampling techniques from many levels of hierarchy. These methods naturally introduce a correlation among observations within the same cluster. This may give a biased parameter estimate and violate the independence assumption in traditional regression models. To account for this bias from individual and community-level variation, we applied a multilevel binary logistic regression model. We computed the intra-class correlation coefficient (ICC) to quantify the community-level variation. In addition, the Proportional Change in Variance (PCV) was calculated to evaluate the contribution of independent variables in explaining variability across clusters: PCV = [(VA − VB)/VA]100 Where VA = variance of the initial model and VB = variance of the model with more terms. Furthermore, we fitted the following four models (null model, Model II, Model III, and Model IV) sequentially. Model I (Null model): without explanatory variables, to assess baseline variation of Co-AnUn between clusters. Model II: We fit the model by adjusting for individual-level variables (mother’s occupation, mother’s age, mother’s education, marital status, wealth status, birth order, mother’s height, and child age). Model III: We fit the model for community-level variables (place of residence, covered by health insurance, distance to health facility, toilet type, family size, and media exposure) and Model IV (final model): We adjusted for both individual and community-level factors simultaneously. We applied deviance (−2 log likelihood) for model comparison, with the lowest deviance indicating a better model fit. Finally, variables’ with Adjusted Odds Ratios (AORs) with corresponding 95% Confidence Intervals (CIs) in the final model were used. The DHS used a multistage sampling method from many levels of hierarchy that results in a dependency among observations, so to avoid a bias from applying single-level statistical models, we used multilevel modeling techniques.

Ethical approval

The MDHS were presented without personal identifiers, which is publicly available and obtained from the Demographic and Health Surveys (DHS) Program website http://www.dhsprogram.com through online request. Furthermore, Furthermore, written conscent letter was obtained by the DHS Program Institutional Review Board (IRB).

Result

Sociodemographic characteristics of study participants

From 15,631 children, about 6.1% of children were dead and 53.1% of the children did not take hemoglobin and anthropometric measurements during the enumeration period (Fig 1). Most of the participants (mothers/caregivers) (46.19%) were aged 25–34 years, and 24.88% of them were aged 35–49 years. About 62.88% of women had not attained education, 20.49% had secondary education, and 16.63% had primary education. The majority of the participants (77.22%) live in rural areas, and 94% of the participants were not covered by health insurance. The majority of the children (58.70%) were aged 24–36. In addition, nearly half (52.31%) of the participants were not currently working. Regarding media exposure, 78.13% of participants had access to media while 21.87% did not. With respect to marital status, 95.26% were married, 1.61% were not married, and 2.13% were separated (Table 1).

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Table 1. Sociodemographic characteristics of the study participants, Mali 2023/24, (N = 6,291).

https://doi.org/10.1371/journal.pone.0351864.t001

Prevalence of undernutrition Indices and anemia

The prevalence of stunting, wasting, underweight, and anemia was 27.2% (95% CI: 26% − 28%), 6% (95% CI: 6% − 7.4%), 16% (95% CI: 15% − 17%), and 72.2% (95% CI: 71% − 73%), respectively. The overall prevalence of Co-AnUn was 26.3% (CI: 25.2%, 27.4%) (Fig 2).

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Fig 2. Prevalence of undernutrition Indices and anemia among Children in Mali, 2023/24.

https://doi.org/10.1371/journal.pone.0351864.g002

Random effect analysis

The results of the random-effects analysis in Table 2, the null model (M0), which contained no predictor variables, the between-cluster variance was 0.33, with an ICC of 9.1%, indicating modest clustering in the co-occurrence of anemia and undernutrition among children aged 6–59 months. The median odds ratio (MOR) was 1.73, suggesting considerable heterogeneity across clusters. When individual-level covariates were included in Model 1 (M1), the cluster variance slightly decreased to 0.19, with an ICC of 5.6% and an MOR of 1.51. This model showed a deviance reduction to 5722 compared with the null model. Model 2 (M2), which included only contextual-level variables, showed a reduction in community variance to 0.22, corresponding to an ICC of 6.3% and an MOR of 1.56. The PCV was 33.3%, indicating that contextual factors explained a notable portion of the variance between clusters.

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Table 2. Random effect analysis for coexistence of anemia and undernutrition among under five children in Mali, 2023/24.

https://doi.org/10.1371/journal.pone.0351864.t002

In the full model (M3), which incorporated both individual and contextual-level variables, the community-level variance was further reduced to 0.17. The ICC decreased to 4.9% with an MOR of 1.48, while the deviance was minimized (5697), suggesting the best model fit. The PCV in the full model was 48.4%, indicating that the combined effect of individual and contextual variables explained part of the between-cluster variance. Overall, the random-effects estimates demonstrate significant clustering of Co-AnUn at the community level. The contextual model explained the largest proportion of variance reduction, while the full model provided the best overall fit (Table 2).

The fixed effect analysis result

In the final multilevel mixed-effects logistic regression model, mothers aged 25–34 years, mothers living in rural areas, mothers with lower educational attainment, mothers without health insurance coverage, and mothers with short stature were significantly associated with an increased likelihood of Co-AnUn among children, whereas tall maternal stature and children aged between 37 and 47 months were associated with a lower likelihood of Co-AnUn among children (Table 3).

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Table 3. multi-level analysis of Factors associated with coexistence of anemia and undernutrition among under five children in Mali, 2023/24.

https://doi.org/10.1371/journal.pone.0351864.t003

Discussion

The overall prevalence of Co-AnUn among children in Mali was 26.3% (CI: 25.2%, 27.4%). We used the univariate, bivariate, and multilevel logistic regression models to assess the associated factors of coexistence of anemia with undernutrition among children. In the multilevel mixed-effect logistic regression model, mothers aged 25–34 years, rural residence, lower maternal educational attainment, lack of health insurance coverage, and short maternal stature were significantly associated with a higher likelihood of Co-AnUn among children. In contrast, tall maternal stature and children aged 37–44 months were associated with a lower likelihood of Co-AnUn among children.

As a result, children whose mothers aged between 25 and 34 years had 1.41 times higher odds of Co-AnUn among children compared to older mothers (AOR = 1.41; 95% CI: 1.01, 1.96). This finding is consistent with a cross-sectional study conducted in Ghana (2019), which reported that children whose mothers were aged below 20 years were 9 times more likely to be underweight and anemic (AOR = 9.455, p = 0.017) compared to mothers who were aged above 40 years [52]. This might be due to infants born from younger mothers being more likely to be born preterm and with a low birth weight, making them more vulnerable to infections and malnutrition [53,54]. This condition may increase the risks of developing anemia, malnutrition, and neonatal infections; these could further increase the risk of developing both anemia and undernutrition [55].

Additionally, children born from mothers without formal education had 1.51 times higher odds of having Co-AnUn compared to mothers with secondary and higher education (AOR = 1.51; 95% CI: 1.19, 1.91). These findings were similar to a study’s findings in Ethiopia from EDHS (2016), which reports that children whose mothers did not have formal education had 1.22 times higher odds of having Co-AnUn compared to mothers with secondary and higher education (AOR = 1.22, 95% CI: 0.73, 0.92) [55]. Similarly, a cross-sectional study conducted in Bangladesh (2016) reported that mothers without formal education had 1.98 times higher risk of having the coexistence of stunting, wasting, and underweight compared to mothers with secondary and higher education (RR = 1.98; 95% CI: 1.25–3.15) [31]. This might be explained by maternal education being essential for increasing mothers’ awareness of their infants’ health and nutrition, including topics such as exclusive breastfeeding and appropriate complementary feeding practices. Understanding proper feeding practices leads to a higher quality of health for a child [56], additionally, mothers’ educational backgrounds can have a positive impact on the health care and nutritional practices they apply to their children [57]. Furthermore, it is obvious that educated mothers have more control over allocating resources for their children’s well-being. This can also be linked to the better parenting procedures practiced by educated women compared to those who lack education [54].

In addition, children whose mothers’ health was not covered by insurance had 2.18 times higher odds of having Co-AnUn compared to mothers whose health was covered by insurance (AOR = 2.18; 95% CI: 1.05, 2.47). A cross-sectional study done in SSA found that mothers’ health insurance coverage decreases childhood stunting and underweight. Similarly, a systematic review and meta-analysis study in Ghana, report that health insurance was found to be a protective factor against anemia among children [58]. This might be due to inequalities in health care financing and lower access, despite equity being one of the key factors in health care systems. There is evidence that the impoverished experience more severe repercussions from morbidity and mortality and have less access to health care than the wealthy. Despite having greater health requirements and spending a larger percentage of their income on medical care, the poor use health care at lower rates than the wealthy [59]. Equity in health signifies that, in an ideal scenario, each individual should have an equal chance to prioritize their health in order to reach their complete health potential, and no one should be hindered from realizing this potential if it is preventable [60]. Furthermore, sustainability in health care finance refers to the relationship between generating revenue, pooling risks for financial security, and efficiently obtaining services to meet the requirements of all. To achieve sustainability, the three interrelated functions of the health financing system must be fulfilled: revenue collection, risk sharing, and health care service procurement [61].

Besides, children who lived in rural areas were 1.46 times higher odds of having Co-AnUn compared to children who lived in urban counters (AOR = 1.46; 95% CI: 1.16, 1.84).There was similar findings with a cross sectional study in Ethiopia from EDHS 2016 reports that Children who lived in rural areas were 1.41 times higher odds of having coexistence of anemia and stunting compared to children who lived in urban counters AOR: 1.41, 95% CI: (1.10, 1.82) [62]. Additionally, there were similar findings with a cross-sectional study in Ethiopia from EDHS 2016 reports: children who lived in rural areas had 1.28 times higher odds of coexistence of anemia and undernutrition compared to children who lived in urban areas (AOR = 1.28, 95% CI: 1.05, 1.57) [55]. This is because people living in rural areas are frequently at a disadvantage in terms of living conditions, economic position, and access to essential care services like vaccination and ANC care [63]. In urban areas, children are less likely to suffer from stunted growth, be underweight, or have any type of undernutrition if their mothers handle home tasks and their fathers work or operate their own businesses. On the other hand, children who have working mothers and fathers in business or service occupations are more likely to be underweight in metropolitan regions. This might be explained by the difficulty working women have finding enough time to provide a balanced meal for their kids [64].

Likewise, children of mothers with short stature were 1.84 times more likely to have Co-AnUn compared to mothers with normal stature (AOR = 1.83; 95% CI: 1.49–2.27). This finding was similar to a cross-sectional study conducted in Pakistan in 2019, which reported that short maternal stature had 1.90 times more likelihood of having coexisting forms of malnutrition compared to mothers with average stature (1.90 (1.02–3.51)) [65], There were findings similar to a cross-sectional study in Ethiopia from EDHS 2016, which reported that mothers with short stature were 2.04 times more likely to have the coexistence of anemia and stunting compared to mothers with tall stature [62], because of this, the association may be explained by an intergenerational cycle of malnutrition in which stunted women children grow up to become stunted mothers, who then give birth to stunted children [66]. Furthermore, due to the intergenerational cycle of stunting, underweight mothers are more likely to produce stunted children, and stunted children are more likely to be anemic. Hemoglobin (Hb) levels and HAZ were found to be positively correlated [40,67].

In contrast, tall maternal stature was 71% less likely to have Co-AnUn compared to mothers with average stature (AOR = 0.29; 95% CI: 0.22, 0.36). This finding is consistent with a cross-sectional study conducted in Pakistan in 2019, which reports that tall maternal stature had 47% fewer times the likelihood of having Co-AnUn compared to mothers with average stature (AOR = 0.53; 95% CI: 0.28–0.98) [65]. Similarly, a cross-sectional study done in 54 LMICs [68], reports that a 1 cm increase in maternal height was associated with a 1.2% reduction in underweight (RR = 0.968; 95% CI: 0.968–0.969) and a 3.2% reduction in stunting (RR = 0.968; 95% CI: 0.967–0.968) [68]. This might be explained by shorter maternal height tending to possess narrower pelvic structures, which raises the chances of cephalopelvic disproportion and difficulties during childbirth, resulting in obstructed labor [69]. Similarly, in shorter mothers who might possess reduced health reserves, the delivery of essential nutrients to the fetus may prove insufficient, causing intrauterine growth restriction and diminished birth weight, factors that can affect the health and survival of the offspring. For these mothers, a restricted supply of nutrients at the cellular level throughout their development may result in the prioritization of fundamental metabolic functions, thereby causing resources to be redirected from growth, which ultimately leads to retarded growth and reduced height [70].

Lastly, children aged 37–47 months were 30% less likely to have Co-AnUn compared to children with short stature (AOR = 0.70; 95% CI: 0.50–0.96). It is consistent with a cross-sectional study reported in Ethiopia, 2014, with lower odds of stunting among children aged 36–47 months (AOR  =  0.41; 95% CI: 0.22, 0.78) [71], similarly, a cross-sectional study in Ethiopia in 2016 reported 25% lower odds of anemia among children aged 36–47 months (AOR = 0.25, 95% CI: 0.20, 0.31) [72]. This could be explained by the finding that children between the ages of 37 and 47 months had less capacity to store nutrients than children older than 37 months. Children who have a low capacity for nutritional reserves and consistently consume low-quality supplemental meals are more likely to experience negative developmental outcomes. Early childhood is one of the most crucial stages in terms of the possibility of stunted growth and its long-term effects, according to additional studies [73].

Strengths and limitations

This study used standardized measurements from WHO and DHS guidelines for measuring undernutrition indices such as stunting, wasting, underweight, and anemia to determine Co-AnUn, which are internationally recognized and widely used by the WHO and other organizations as a standardized tool for measuring undernutrition indices. Subsequently, comparison of results across many studies will be possible. Additionally, the hierarchical nature of DHS data is conducted using an advanced model to take into account the clustering effect (mixed-effect logistic regression) for a reliable standard error and estimate.

However, the study design was cross-sectional; it does not show a causal relationship or long-term effects. The secondary nature of the dataset makes it difficult to obtain and analyze additional variables due to the absence of micronutrient intake data in the DHS dataset. Furthermore, DHS lacks dietary covariates, preventing analysis of micronutrient deficiencies, including zinc and vitamins, which are known drivers of Co-AnUn. The absence of nutritional covariates precludes any analysis of micronutrient deficiencies. Therefore, we recommend future research be conducted using longitudinal designs to track causal relationships and incorporation of dietary assessment tools.

Conclusion

The coexistence of anemia with undernutrition is still prevalent in Mali, which contributes to mortality and related complications among children. The finding from this study revealed that children whose mothers were aged 25–34, mothers without formal education, mothers without primary education, mothers whose health was not covered by health insurance, children who lived in rural areas, and maternal short stature were associated with increased odds of the coexistence of anemia and undernutrition among children. In contrast, tall maternal stature and children aged 37–47 were associated with decreasing the odds of the coexistence of anemia and undernutrition among children.

Implications of the study

The findings of this study carry significant implications for public health policy and nutritional intervention strategies in Mali. Improving equity of quality health services for limited healthcare access populations. Programs should prioritize the first 1,000 days of infants and newborn care by improving maternal education. Furthermore, the study highlights the critical importance for healthcare systems to integrate nutritional supplements with maternal and child health services, particularly targeting disadvantaged populations through community-based outreach programs for rural residents and providing insured maternal care services. Educational initiatives should focus on improving health literacy for mothers, while economic policies should address healthcare accessibility to remote areas.

Supporting information

S1 Fig. Conceptual framework for the Coexistence of Anemia and Undernutrition among children in Mali 2023/24 adapted from WHO 2017 and UNICEF 2013 framework.

https://doi.org/10.1371/journal.pone.0351864.s001

(TIF)

Acknowledgments

We are gratefully acknowledge the Measure DHS program for authorizing the datasets, and guidelines.

References

  1. 1. Pasricha S-R, Rogers L, Branca F, Garcia-Casal M-N. Measuring haemoglobin concentration to define anaemia: WHO guidelines. Lancet. 2024;403(10440):1963–6. pmid:38493792
  2. 2. Uzogara SG. Underweight, the less discussed type of unhealthy weight and its implications: a review. American Journal of Food Science and Nutrition Research. 2016;3(5):126–42.
  3. 3. Shetty P. Malnutrition and undernutrition. Medicine. 2006;34(12):524–9.
  4. 4. Engidaye G, Melku M, Yalew A, Getaneh Z, Asrie F, Enawgaw B. Under nutrition, maternal anemia and household food insecurity are risk factors of anemia among preschool aged children in Menz Gera Midir district, Eastern Amhara, Ethiopia: a community based cross-sectional study. BMC Public Health. 2019;19(1):968. pmid:31324244
  5. 5. Khurana R, Ravindrakumar A, Aggarwal AK, Thungapathra M, Sagar V. Magnitude of anaemia and micro-nutritional deficiencies (iron, folate, and vitamin B12) among outpatient clinic patients at a rural village-level health post in Haryana: An exploratory study: Micro-nutritional deficiencies at a health post in Haryana. International Journal of Health Systems and Implementation Research. 2025;9(1):14–30.
  6. 6. Akram HE, Al-Warid HS. Evaluation of Hematological Factors and Micronutrients Among Children Infected with Enterobius vermicularis. Iraqi Journal of Science. 2023;1625–34.
  7. 7. Ekholuenetale M, Okonji OC, Nzoputam CI, Barrow A. Inequalities in the prevalence of stunting, anemia and exclusive breastfeeding among African children. BMC Pediatr. 2022;22(1):333. pmid:35681131
  8. 8. McCarthy EK, Murray DM, Kiely ME. Iron deficiency during the first 1000 days of life: are we doing enough to protect the developing brain? Proc Nutr Soc. 2022;81(1):108–18. pmid:34548120
  9. 9. Barua S, Ciannella S, Tijani L, Gomez-Pastora J. Iron in blood cells: Function, relation to disease, and potential for magnetic separation. Biotechnol Bioeng. 2023;120(7):1707–24. pmid:36999568
  10. 10. Thakur M, Poojary S, Swain N. Green synthesis of iron oxide nanoparticles and its biomedical applications. Nanotechnology applications in health and environmental sciences. Springer. 2021:83–109.
  11. 11. Gedfie S, Getawa S, Melku M. Prevalence and Associated Factors of Iron Deficiency and Iron Deficiency Anemia Among Under-5 Children: A Systematic Review and Meta-Analysis. Glob Pediatr Health. 2022;9. pmid:35832654
  12. 12. Cheung WC, Shen S, Meadan H. Correlation between Motor, Socio-Emotional Skills, and Academic Performance between Young Children with and without Disabilities. J Dev Phys Disabil. 2021;34(2):211–31.
  13. 13. Ziegenfusz S, Paynter J, Flückiger B, Westerveld MF. A systematic review of the academic achievement of primary and secondary school-aged students with developmental language disorder. Autism Dev Lang Impair. 2022;7. pmid:36382072
  14. 14. Mulé D, Jeger I, Dötsch J, Breido F, Ferrari N, Joisten C. Correlation between Language Development and Motor Skills, Physical Activity, and Leisure Time Behaviour in Preschool-Aged Children. Children (Basel). 2022;9(3):431. pmid:35327803
  15. 15. Tamplain P, Cairney J. Low Motor Competence or Developmental Coordination Disorder? An Overview and Framework to Understand Motor Difficulties in Children. Curr Dev Disord Rep. 2024;11(1):1–7.
  16. 16. Obeagu EI, Obeagu GU, Ukibe NR, Oyebadejo SA. Anemia, iron, and HIV: decoding the interconnected pathways: A review. Medicine. 2024;103(2):e36937.
  17. 17. Zheng J, Liu J, Yang W. Association of Iron-Deficiency Anemia and Non-Iron-Deficiency Anemia with Neurobehavioral Development in Children Aged 6-24 Months. Nutrients. 2021;13(10):3423. pmid:34684422
  18. 18. Samson KLI, Fischer JAJ, Roche ML. Iron Status, Anemia, and Iron Interventions and Their Associations with Cognitive and Academic Performance in Adolescents: A Systematic Review. Nutrients. 2022;14(1):224. pmid:35011099
  19. 19. Osei RD, Lambon-Quayefio MP. Effects of Long-Term Malnutrition on Education Outcomes in Ghana: Evidence from a Panel Study. Eur J Dev Res. 2021;34(1):1–21.
  20. 20. Obeagu EI, Obeagu GU, Alum EU, Ugwu OPC. Anemia as a prognostic marker for disease progression in HIV infection. 2023.
  21. 21. Hacker K. The Burden of Chronic Disease. Mayo Clin Proc Innov Qual Outcomes. 2024;8(1):112–9. pmid:38304166
  22. 22. Safiri S, Kolahi AA, Noori M, Nejadghaderi SA, Karamzad N, Bragazzi NL. Burden of anemia and its underlying causes in 204 countries and territories, 1990–2019: results from the Global Burden of Disease Study 2019. Journal of Hematology & Oncology. 2021;14(1):185.
  23. 23. Iverson JM. Developing language in a developing body, revisited: The cascading effects of motor development on the acquisition of language. Wiley Interdiscip Rev Cogn Sci. 2022;13(6):e1626. pmid:36165333
  24. 24. Fouad HM, Yousef A, Afifi A, Ghandour AA, Elshahawy A, Elkhawass A, et al. Prevalence of malnutrition & anemia in preschool children; a single center study. Ital J Pediatr. 2023;49(1):75. pmid:37322509
  25. 25. Sartika RAD, Sari SL, Ningsih WM, Wirawan F. Prolonged Undernutrition and the Risk of Anemia in Indonesian Children. Journal of Health Research. 2024;38(3).
  26. 26. Fentaw W, Belachew T, Andargie A. Anemia and associated factors among 6 to 59 months age children attending health facilities in Kombolcha town, Northeast Ethiopia: a facility-based cross-sectional study. BMC Pediatr. 2023;23(1):209. pmid:37138229
  27. 27. Al-Jawaldeh A, Taktouk M, Doggui R, Abdollahi Z, Achakzai B, Aguenaou H, et al. Are Countries of the Eastern Mediterranean Region on Track towards Meeting the World Health Assembly Target for Anemia? A Review of Evidence. Int J Environ Res Public Health. 2021;18(5):2449. pmid:33801513
  28. 28. Azmeraw M, Kassaw A, Habtegiorgis SD, Tigabu A, Amare AT, Mekuria K, et al. Prevalence of anemia and its associated factors among children aged 6-23 months, in Ethiopia: a systematic review and meta analysis. BMC Public Health. 2023;23(1):2398. pmid:38042804
  29. 29. Dessie G, Li J, Nghiem S, Doan T. Prevalence and Determinants of Stunting-Anemia and Wasting-Anemia Comorbidities and Micronutrient Deficiencies in Children Under 5 in the Least-Developed Countries: A Systematic Review and Meta-analysis. Nutr Rev. 2025;83(2):e178–94. pmid:38820331
  30. 30. Asmare AA, Agmas YA. Determinants of coexistence of undernutrition and anemia among under-five children in Rwanda; evidence from 2019/20 demographic health survey: Application of bivariate binary logistic regression model. PLoS One. 2024;19(4):e0290111. pmid:38578819
  31. 31. Chowdhury MRK, Rahman MS, Billah B, Kabir R, Perera NKP, Kader M. The prevalence and socio-demographic risk factors of coexistence of stunting, wasting, and underweight among children under five years in Bangladesh: a cross-sectional study. BMC Nutr. 2022;8(1):84. pmid:35996184
  32. 32. Gebreegziabher T, Sidibe S. Prevalence and contributing factors of anaemia among children aged 6-24 months and 25-59 months in Mali. J Nutr Sci. 2023;12:e112. pmid:37964977
  33. 33. Chilinda ZB, Wahlqvist ML, Lee M-S, Huang Y-C. Higher maternal autonomy is associated with reduced child stunting in Malawi. Sci Rep. 2021;11(1):3882. pmid:33594098
  34. 34. Mandiwa C, Namondwe B, Makwinja A, Zamawe C. Factors associated with contraceptive use among young women in Malawi: analysis of the 2015-16 Malawi demographic and health survey data. Contracept Reprod Med. 2018;3:12. pmid:30250748
  35. 35. Asmare AA, Tegegne AS, Belay DB, Agmas YA. Coexisting predictors for undernutrition indices among under-five children in West Africa: application of a multilevel multivariate ordinal logistic regression model. BMC Nutr. 2025;11(1):112. pmid:40474304
  36. 36. Rutstein SO, Rojas G. Guide to DHS statistics. Calverton, MD: ORC Macro. 2006.
  37. 37. Croft TN, Marshall AM, Allen CK, Arnold F, Assaf S, Balian S. Guide to DHS statistics. Rockville: ICF. 2018.
  38. 38. Group UWWB, Estimates J C M JCM. Levels and trends in child malnutrition. 2021.
  39. 39. Organization WH, Fund UNCs. The UNICEF-WHO-World Bank Joint Child Malnutrition Estimates (JME) standard methodology: tracking progress on SDG Indicators 2.2. 1 on stunting, 2.2. 2 (1) on overweight and 2.2. 2 (2) on wasting. World Health Organization. 2024.
  40. 40. Jemil HW, Semayneh SW, Kassaw AB, Gashu KD. Predicting severe stunting and its determinants among under-five in Eastern African Countries: A machine learning algorithms. PLoS One. 2026;21(1):e0340221. pmid:41481593
  41. 41. Hossain MM, Abdulla F, Rahman A. Prevalence and determinants of wasting of under-5 children in Bangladesh: Quantile regression approach. PLoS One. 2022;17(11):e0278097. pmid:36417416
  42. 42. Mulama LA. Nutrition status of children under five years (during corona-19 pandemic) in Kibera informal settlement in Nairobi, Kenya. University of Nairobi. 2023.
  43. 43. Hossain MM, Abdulla F, Rahman A. Prevalence and risk factors of underweight among under-5 children in Bangladesh: Evidence from a countrywide cross-sectional study. PLoS One. 2023;18(4):e0284797. pmid:37093817
  44. 44. Oumer A, Fikre Z, Girum T, Bedewi J, Nuriye K, Assefa K. Stunting and Underweight, but not Wasting are Associated with Delay in Child Development in Southwest Ethiopia. Pediatric Health Med Ther. 2022;13:1–12. pmid:35046749
  45. 45. Kamruzzaman M. Is BMI associated with anemia and hemoglobin level of women and children in Bangladesh: A study with multiple statistical approaches. PLoS One. 2021;16(10):e0259116. pmid:34710186
  46. 46. Msaki RV, Lyimo E, Masumo RM, Mwana E, Katana D, Julius N, et al. Predictors of iron deficiency anaemia among children aged 6-59 months in Tanzania: Evidence from the 2015-16 TDHS-MIS cross-sectional household survey. PLOS Glob Public Health. 2022;2(11):e0001258. pmid:36962688
  47. 47. Zewude BT, Debusho LK. Multilevel proportional odds modeling of anaemia prevalence among under five years old children in Ethiopia. BMC Public Health. 2023;23(1):540. pmid:36949425
  48. 48. Sahiledengle B, Mwanri L, Petrucka P, Tadesse H, Agho KE. Co-existence of maternal overweight/obesity, child undernutrition, and anaemia among mother-child pairs in Ethiopia. PLOS Glob Public Health. 2024;4(3):e0002831. pmid:38452001
  49. 49. Dassie GA, Chala Fantaye T, Charkos TG, Sento Erba M, Balcha Tolosa F. Factors influencing concurrent wasting, stunting, and underweight among children under five who suffered from severe acute malnutrition in low- and middle-income countries: a systematic review. Front Nutr. 2024;11:1452963. pmid:39713780
  50. 50. Arendt E, Bhutta ZA, Singh NS, Campbell OMR. Effect of maternal height on caesarean section and neonatal mortality rates in sub-Saharan Africa: An analysis of 34 national datasets. PLOS ONE. 2018;13(2):e0192167. https://doi.org/10.1371/journal.pone.0192167
  51. 51. Raru TB, Merga BT, Mulatu G, Deressa A, Birhanu A, Negash B. Minimum dietary diversity among children aged 6-59 months in East Africa countries: A multilevel analysis. International Journal of Public Health. 2023;68:1605807.
  52. 52. Appiah CA, Mensah FO, Hayford FEA, Awuuh VA, Kpewou DE. Predictors of undernutrition and anemia among children aged 6–24 months in a low-resourced setting of Ghana: a baseline survey. JHR. 2020;35(1):27–37.
  53. 53. Ayele AW, Gabreyohannes E, Shiferaw YA. Under-nutrition and its associated factors among under-five children across urban and rural settings of Ethiopia: a cross-sectional comparative study. BMC Nutr. 2025;11(1):151. pmid:40731299
  54. 54. Darsene H, Geleto A, Gebeyehu A, Meseret S. Magnitude and predictors of undernutrition among children aged six to fifty nine months in Ethiopia: a cross sectional study. Arch Public Health. 2017;75:29. pmid:28694966
  55. 55. Aweke MN, Yitageasu G, Agimas MC, Yismaw GA, Baffa LD, Alemu GG. Co-occurrence of maternal anemia and child undernutrition in Ethiopia: multilevel analysis of analysis of EDHS data (2005-2016). BMC Public Health. 2025;25(1):2722. pmid:40790471
  56. 56. Gibson EL, Wardle J, Watts CJ. Fruit and vegetable consumption, nutritional knowledge and beliefs in mothers and children. Appetite. 1998;31(2):205–28. pmid:9792733
  57. 57. Vereecken CA, Keukelier E, Maes L. Influence of mother’s educational level on food parenting practices and food habits of young children. Appetite. 2004;43(1):93–103. pmid:15262022
  58. 58. Anaba EA, Tandoh A, Sesay FR, Fokukora T. Factors associated with health insurance enrolment among ghanaian children under the five years. Analysis of secondary data from a national survey. BMC Health Serv Res. 2022;22(1):269. pmid:35227256
  59. 59. Wagstaff A, O’Donnell O, Van Doorslaer E, Lindelow M. Analyzing health equity using household survey data: a guide to techniques and their implementation. World Bank Publications. 2007.
  60. 60. Braveman P, Gruskin S. Defining equity in health. J Epidemiol Community Health. 2003;57(4):254–8. pmid:12646539
  61. 61. Anarwat SG. Health Insurance for Economically Disadvantaged People in LMICs: What Are the Best Options? IntechOpen. 2022.
  62. 62. Sahiledengle B, Mwanri L, Petrucka P, Agho KE. Coexistence of Anaemia and Stunting among Children Aged 6-59 Months in Ethiopia: Findings from the Nationally Representative Cross-Sectional Study. Int J Environ Res Public Health. 2023;20(13):6251. pmid:37444099
  63. 63. Osadolor OO, Osadolor AJ, Osadolor OO, Enabulele E, Akaji EA, Odiowaya DE. Access to health services and health inequalities in remote and rural areas. Janaki Med Coll J Med Sci. 2022;10(2):70–4.
  64. 64. Nahar MZ, Zahangir MS. The role of parental education and occupation on undernutrition among children under five in Bangladesh: A rural-urban comparison. PLoS One. 2024;19(8):e0307257. pmid:39213314
  65. 65. Khaliq A, Nambiar S, Miller YD, Wraith D. Assessing the relationship of maternal short stature with coexisting forms of malnutrition among neonates, infants, and young children of Pakistan. Food Sci Nutr. 2024;12(4):2634–49. pmid:38628194
  66. 66. Prendergast AJ, Humphrey JH. The stunting syndrome in developing countries. Paediatr Int Child Health. 2014;34(4):250–65. pmid:25310000
  67. 67. de Novaes Oliveira M, Martorell R, Nguyen P. Risk factors associated with hemoglobin levels and nutritional status among Brazilian children attending daycare centers in Sao Paulo City, Brazil. Arch Latinoam Nutr. 2010;60(1):23–9. pmid:21090175
  68. 68. Ozaltin E, Hill K, Subramanian SV. Association of maternal stature with offspring mortality, underweight, and stunting in low- to middle-income countries. JAMA. 2010;303(15):1507–16. pmid:20407060
  69. 69. Rush D. Nutrition and maternal mortality in the developing world. Am J Clin Nutr. 2000;72(1 Suppl):212S-240S. pmid:10871588
  70. 70. Martorell R. Body Size, Adaptation and Function. Human Organization. 1989;48(1):15–20.
  71. 71. Fentahun W, Wubshet M, Tariku A. Undernutrition and associated factors among children aged 6-59 months in East Belesa District, northwest Ethiopia: a community based cross-sectional study. BMC Public Health. 2016;16:506. pmid:27297078
  72. 72. Jember TA, Teshome DF, Gezie LD, Agegnehu CD. Spatial variation and determinants of childhood anemia among children aged 6 to 59 months in Ethiopia: further analysis of Ethiopian demographic and health survey 2016. BMC Pediatr. 2021;21(1):497. pmid:34753442
  73. 73. Gigante DP, Rasmussen KM, Victora CG. Pregnancy increases BMI in adolescents of a population-based birth cohort. J Nutr. 2005;135(1):74–80. pmid:15623836