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. 2024 Apr 5;10(7):e29308. doi: 10.1016/j.heliyon.2024.e29308

Effects of undernutrition on mortality of HIV-infected children after initiation of antiretroviral therapy in Ethiopia: A systematic review and meta-analysis

Amare Kassaw a,⁎, Bogale Chekole b, Muluken Chanie Agimas c, Molla Azmeraw d, Biruk Beletew d, Shegaw Zeleke e, Worku Necho Asferi f, Solomon Demis f, Habtamu Shimeles Hailemeskel f, Wubet Alebachew Bayih f, Ermias Sisay Chane a, Demewoz Kefale a, Tigabu Munye Aytenew e
PMCID: PMC11004412  PMID: 38601598

Abstract

Background

Undernutrition is the leading cause of mortality among children infected with HIV particularly in resource-deprived settings. Despite several studies were disclosed the effect of undernutrition on mortality of children living with HIV in Ethiopia, the findings were fragmented and inconclusive. Therefore, this review aimed to determine the pooled effects of undernutrition on mortality of children infected with HIV in Ethiopia.

Methods

The search were performed using international online electronic data bases (MEDLINE/though PubMed, Google scholar, Hinari, Scopus and open Google). The review included only retrospective/prospective cohort studies reporting the effects of undernutrition on mortality of children infected with HIV. Heterogeneity between included studies was assessed using Cochrane Q-test and the I2 statistics. Sub-group analysis was done by study regions, sample size and publication year.

Results

A total of 1345 articles were identified from databases. Among these, 14 studies met the inclusion criteria and included in the study. Meta-analysis of 4 studies revealed that stunting has a significant effect on mortality of children infected with HIV (AHR: 3.36; 95 % CI: 2.95–3.77). Of 14 included studies, 6 articles indicated that wasting has a significant effect on mortality in children infected with HIV (AHR: 3.93; 95 % CI: 2.56–5.30) as compared to their counterparts. Furthermore, the pooled effect of 8 studies showed that underweight has 3.4 times hazard of death among children who lived with HIV as compared to well-nourished children.

Conclusion

This review revealed that undernutrition has deleterious effect on mortality of children infected with HIV/AIDS by disease progression and prone the children to serious opportunistic infections. From the study, the authors recommended that nutritional status of children on antiretroviral therapy need to be evaluated regularly.

Keywords: Children living with HIV, Undernutrition, Effect, Ethiopia

1. Introduction

Human Immunodeficiency Virus (HIV) is still remaining a major public health concern [1,2] which cause the death of 40.1 million people worldwide since the start of the epidemic [3]. Globally, at the end of 2021, there were an estimated 38.4 million people living with HIV, of which 1.7 million were children aged less than 15 years [4]. Sub-Saharan Africa is heavily affected region in the globe which is home to two-thirds of all people living with HIV [5].

Children and adolescents are among the most victimized groups of all populations for infection, morbidity and mortality of HIV/AIDS. Worldwide, about 5 percent of all people living with HIV are under 15 years of age, and 15 percent of all AIDS-related deaths [6,7]. Although the use of Antiretroviral Therapy (ART) sunstanicially decrease AIDS-related mortality [8], in resource-limited settings the mortality risk due to HIV/AIDS is still high among children [9]. Evidences indicated that among HIV-infected children who admitted to hospital, about 14 % were died [10]. A similar evidence also disclosed that the overall mortality of HIV-infected children were 24 % [9]. A systematic review and meta-analysis studies conducted in Sub-Saharan Africa showed that the pooled proportion of mortality among HIV-infected children was 7.9 % [1].

Undernutrition in the form of (wasting, stunting and underweight) is the leading cause of morbidity, low survival and mortality among children infected with HIV particularly in resource-deprived settings [[11], [12], [13]].In fact, initiation of ART dramatically reduce HIV/AIDS-related morbidity, mortality, and boost survival rate [[14], [15], [16]]. However, the responses of HIV-infected children for HAART(Highly Active Antiretroviral Therapy) are not similar to adults, because of deleterious impacts of the virus on the immature immunity system, nutritional status and negative consequence on the immunologic response of children living with HIV [8,17]. Undernutrition, especially severe acute malnutrition (SAM) decreased the numbers of T-helper cells, cytotoxic T-cells, and natural killer cells and predisposing children to opportunistic infections [18,19].

HIV- infection and undernutrion coexists in a viscous cycle and deadly duo with each one fuelling the other [11,20]. Children living with HIV are more vulnerable to undernutrition [21] due to several mechanisms: HIV- infection exposed children for decreased appetite [22], increase energy needs as a result of infection, exacerbating of gastrointestinal infections, enteropathy and food insecurity [20]. Moreover, children with HIV are prone to undernutrion due to reduced food intake resulting from decreased appetite [23], poor absorption of nutrients that result of recurrent or chronic diarrhea [24], increased energy needs as a result of virus replication and opportunistic infections [25]. Undernutrition on its part increases susceptibility to infection by causing immune dysfunction in manifold ways and it adds fuel to the fire by accelerating the progress of HIV- infection to AIDS [11,19].

Ethiopia has been planned and endorsed nutritional care and support program as a cost-effective strategy in the management of HIV/AIDS patients to reduce morbidity and mortality [25,26]. Despite these interventions, undernutrition is continued to be a major predictor of morbidity and mortality of people with HIV, particularly children are among the most victimized populations [12,15,24,27]. Even though there is common understanding that HIV and undernutrion are intricate and intertwined to predict mortality and decrease survival rate, there is a lacking of comprehensive nationally pooled evidence estimating the pooled effects of undernutrition on mortality among children living with HIV.

In Ethiopia several studies were conducted and disclosed the effect of undernutrition on mortality of children with HIV [12,[28], [29], [30], [31], [32], [33], [34], [35]]. However, there were a fragment and inconclusive among studies finding. Therefore, the review aimed to determine the pooled effects of undernutrition on mortality among children living with HIV in Ethiopia. Evidences reported from this study will be used as one input for program planners and decision-makers in designing strategies to halt undernutrition related mortality among children living with HIV and to achieve the target held by 2025.

2. Methods

2.1. Search strategy

The search were performed using international online electronic data bases (MEDLINE/though PubMed, Google scholar, Hinari, Scopus and open Google). Additionally, unpublished papers were reviewed out from research centers and library sources as well as the hand search of reference lists of eligible articles were also searched. Searches were limited to full text articles, human studies and English language studies. Using pre-determined search terms/keywords and MeSH terms, the following search map was built: Undernutrition OR malnutrition OR “nutritional deficienc*” OR malnourish* OR "Nutritional Status"[Mesh] OR “nutritional status” OR stunting OR Wasting OR underweight OR “micronutrient deficienc*” OR “Thinness"[Mesh] AND "Mortality"[Mesh] OR Mortality OR survival OR “death rate” OR “risk factors” OR “time to death” OR “case fatality rate” OR “mortality rate” AND "Child"[Mesh] OR child* OR pediatric* OR paediatric* AND "Antiretroviral Therapy” OR “Highly Active"[Mesh] OR "anti-retroviral agents" OR "anti-retroviral agents"[MeSH] OR “antiretroviral treatment” OR “anti-retroviral therapy” AND "Ethiopia"[Mesh] OR Ethiopia (S1 Table). To access the eligible articles, the adapted PICO framework was used. This review was prospectively registered at the Prospero with a registration number of CRD42023448563.

2.2. Inclusion and exclusion criteria

The review included only retrospective/prospective cohort studies that report the adjusted pooled effects of undernutrition on mortality of children with HIV. However, articles with no full texts, case series, case reports, case control, cross-sectional and qualitative studies were excluded from this study. The study was selected if their publication period is between 2008 and 2023 as the revised version of national guidelines for HIV/AIDS and nutrition developed in 2008 [25].

2.3. Outcome measurement

This study primarily focuses on the pooled effect of undernutrition (stunting, wasting and underweight) reported from primary studies on mortality and survival of children infected with HIV. Stunting(height for age < −2Zscore), wasting (Weight for height < -2Z score) and underweight (Weight for age < −2Z score) [36].

2.4. Quality assessment

The quality of included studies were appraised using the Joanna Briggs Institute (JBI) critical appraisal checklists for cohort studies [37]. Accordingly, all eligible studies were critically appraised by two independent reviewers (TMA and SZ) and scored for the validity of their results. Arguments between reviewers were settled through discussion. Based on this, among 14 included articles nine studies were scored 9 out of 11 questions 82 %(low risk).Whereas, 4 of them scored 8 out of 11 questions 73 %(low risk) and one study score 7 out of 11 questions(low risk)(S1 checklist). Studies were considered to be low risk when scored 50 % or higher on the quality assessment tools [37]. Thus, the quality of all the included studies was high.

2.5. Data extraction

The relevant data were extracted by two authors (AK& DK) by using standardized JBI data extraction format [38]. Any discrepancies between two authors were handled by discussion. For each included study; first author name, publication year, study region, study design, study setting, sample size, adjusted hazard ratio with 95 % confidence intervals (CI),standard error and follow-up period were extracted on Microsoft excel spread sheet.

2.6. Statistical analysis

STATA version17 software was used for meta-analysis of extracted data to determine the pooled effect size. The presence of heterogeneity between included studies was assessed using Cochrane Q-test and the I2 statistics [39]. To adjust random variation in the presence of significant heterogeneity between primary studies, sub-group analysis was done by study regions, sample size and publication year. Furthermore, the presence of publication bias was checked through graphical (funnel plot) and statistical (Egger's) test.

3. Results

3.1. Study identification

A total of 1345 articles were identified from different electronic databases and other approach of searching methods. After removal of 456 duplicate studies, 889 studies were remained for the next screening. Reading the title and abstracts, 764 articles were removed as they are not relevant for this systematic review. Again after evaluating full text articles, 125 reports were retrieved. Next, 62 studies were removed as studies did not report data on the outcome interest, report only descriptive statics and studies focused on adults and pregnant women. Finally, 14 studies were included for analysis after removal of 49 studies with reasons (Fig. 1).

Fig. 1.

Fig. 1

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PRISMA flow diagram of article selection for systematic review and meta-analysis of the Effects of undernutrion on mortality of children after initiation of Antiretroviral Therapy in Ethiopia.

3.2. Characteristics of included studies

This systematic review included 14 studies from different regions of Ethiopia with a total sample size of 5491 children living with HIV and all are retrospective cohort studies. The sample size was ranged from 222 in South Nation and Nationalities and Peoples Regional States (SNNPRS) [40] to 721 in Benishangul Gumuz regional state [31].The highest mortality rate was reported as (22.9 %) in Amhara region [14] while the least (4.2 %) was reported from study done in Benishangul Gumuz region [31]. Concerning the study settings, six studies were from Amhara region [12,14,34,35,41,42], one from Oromia [32], four studies from SNNPRS [29,30,40,43], two from Addis Ababa [28,33] and one study from Benishangul Gumuz region [31](Table 1).

Table 1.

Characteristics of the included studies of effects of undernutrion on mortality of children living with HIV in Ethiopia.

S.N Author/year Study region Study
Design		 Sample size Overall mortality (%) Quality score
1 Adem, A.k. et al.,[2014] [32] Oromia Retrosp-cohort 560 43(7.6) Low risk
2 Alebel, A. et al.,[2018] [12] Amhara Retrosp-cohort 390 38(9.7) Low risk
3 Alebel, A. et al.,[2020] [34] Amhara Retrosp-cohort 538 38(7.1) Low risk
4 Arage, G. et al.,[2019] [14] Amhara Retrosp-cohort 426 97(22.9) Low risk
5 Ashagre, S. et al.,[2012] [40] SNNPRS Retrosp-cohort 222 26(11.7) Low risk
6 Bitew, s. et al.,[2017] [27] SNNPRS Retrosp-cohort 228 16(7) Low risk
7 Biyazin, Y. et al.,[2022] [35] Amhara Retrosp-cohort 251 16(6.4) Low risk
8 Chekole,B. et al., [2022] [41] Amhara Retrosp-cohort 588 27(4.6) Low risk
9 Ebsa, G. et al.,[2015] [33] Addis Ababa Retrosp-cohort 253 58(10.4) Low risk
10 Marie, B.T. et al. [2022] [42] Amhara Retrosp-cohort 376 21(5.6) Low risk
11 Molla, M. et al.,[2022] [31] Benishangul Retrosp-cohort 721 30(4.2) Low risk
12 Omer, A. et al.,[2019] [30] SNNPRS Retrosp-cohort 242 13(5.3) Low risk
13 Sidemo, N.B. and S.H. Hebo,[2019] [29] SNNPRS Retrosp-cohort 421 65(15.4) Low risk
14 Taye,B. et al.,[2010] [28] Addis Ababa Retrosp-cohort 475 42(8.8) Low risk
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3.3. Meta-analysis of the effects of undernutrition on mortality of children living with HIV

Among the total of 14 retrospective cohort studies included in the review, twelve studies were reporting nutritional status as well-nourished and undernourished (stunting, wasting and underweight). The remaining two studies reporting undernutrition based on the three categories of mild, moderate and severe undernutrition [14,42].

3.4. The effects of stunting on mortality of children living with HIV

A total of four [12,31,34,40] cohort studies revealed that stunting has a significant effect on mortality of children infected with HIV. The pooled AHR (adjusted hazard ratio) of these studies disclosed that stunted children living with HIV were 3.36 times hazard of death (AHR: 3.36; 95 % CI: 2.95–3.77) as compared to their counterparts. Since studies included in this meta-analysis were exhibited no heterogeneity (I2 = 36.16 %, p = 0.195), fixed effect model was undertaken (Fig. 2).

Fig. 2.

Fig. 2

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Forest plot showing of the effects of stunting on mortality among children living with HIV in Ethiopia.

3.5. The effects of wasting on mortality of children living with HIV

Among seven included [12,27,28,31,34,35,40] studies, six articles indicated that wasting has a significant effect on mortality in children infected with HIV. From random effects model, statistical heterogeneity was observed among studies (I2 = 93.35 %, P-value<0.001) and there was no single study that excessively influenced the pooled effects of wasting on mortality. Egger's statistical test revealed that there is evidence of publication bias (P-value = 0.0206). After trim and fill analysis (Fig. 3), wasting had negative impact on mortality of children with HIV. Therefore, from trimfill analysis the pooled hazard effects of mortality among wasted children living with HIV were 3.93 times as compared to well-nourished children with HIV(AHR: 3.93; 95 % CI: 2.56–5.30) (Fig. 4).

Fig. 3.

Fig. 3

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Trim and fill analysis of funnel plot for effects of wasting on mortality among children living with HIV.

Fig. 4.

Fig. 4

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Forest plot showing of the effects of wasting on mortality among children infected with HIV in Ethiopia.

3.6. The effects of underweight on mortality of children living with HIV

Eight studies [12,[29], [30], [31], [32], [33],35,41] were included in the meta-analysis of this category. Of these four studies showed that underweight has a significant effect on mortality in children living with HIV while four of them reported that underweight has no significant effect on mortality. However, the pooled effect of all 8 studies showed that underweight has 3.4 times hazard of death among children who lived with HIV as compared to their compartments. Statistical heterogeneity was observed among studies (I2 = 96.06 %, P-value<0.001) (Fig. 5) and there was no single study that excessively influenced the pooled effects of underweight on mortality of children with HIV. Egger's statistical test revealed that there is no evidence of publication bias (P-value = 0.2679). Additionally, the remaining two [14,42] studies reporting undernutrition interms of mild, moderate and severe which were not suitable for meta-analysis in this study. The studies indicated that children with severe undernutrion were more likely to die than children with mild undernutrion.

Fig. 5.

Fig. 5

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Forest plot showing of the effects of underweight on mortality among children living with HIV in Ethiopia.

3.7. Subgroup analyses of effects of wasting on mortality of children living with HIV

From random effects pooled estimate, significant heterogeneity was observed. To handle this heterogeneity, Subgroup analyses was performed based on the region, sample size and publication year (Table 2).The result of this analysis showed that wasting has higher effect(AHR: 5.33; 95%CI: 2.13–8.54]) on mortality among studies done SNNPRS as compared to other parts of the country [27,40]. The Sub-group analyses based on sample size indicated that wasting has more effect (AHR: 4.62; 95%CI: 3.05–6.19) among studies conducted with sample size less than 450 [12,27,35,40] compared to their counterparts. Furthermore, subgroup analyses also evidenced that wasting has a more effect on mortality in studies published before 2019 [12,27,28,40] as compared to studies published after 2019.

Table 2.

Summary of sub-group analysis on effects of wasting among children living with HIV in Ethiopia by region, sample size and publication year.

Variables Sub-group Included studies AHR Heterogeneity (I2 %, p-value)
Region Amhara 3 3.61[2.50–4.73] 72.85,p = 0.03
SNNPRS 2 5.33[2.13–8.54] 89.99, p < 0.001
Others 2 3.03[2.81–6.87] 98.36,p < 0.001
Sample size <450 4 4.62[3.05–6.19] 85.30,p < 0.001
≥450 3 3.05[0.67–5.43] 96.73, p < 0.001
Publication year <2019 4 4.57[3.17–5.97] 87.26, p < 0.001
≥2019 3 3.04[0.89–5.19] 93.87, p < 0.001
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NB: others; Oromia, Benishangul and Addis Ababa.

3.8. Sub-group analyses of effects of underweight on mortality of children living with HIV

To handle heterogeneity, a sub-group analysis was performed using sample size and publication year. The effect of underweight on mortality of children living with HIV was higher (AHR:4.23; 95 % CI:1.72–6.73) among studies done with sample size less than 450 [12,29,30,33,35] compared with studies conducted with sample size greater than 450. The result of sub-group analyses also disclosed that underweight has an exaggerated effect (AHR: 4.58; 95%CI: 1.17–8.99) on mortality among studies published before 2019 (Table 3).

Table 3.

Summary of sub-group analysis on effects of underweight on mortality among children living with HIV in Ethiopia by sample size and publication year.

Variables Sub-group Included studies AHR Heterogeneity (I2,p-value)
Sample size <450 5 4.23[1.72–6.73] 96.63, p < 0.001
≥450 3 2.11[1.14–3.08] 82.07, p < 0.001
Publication year <2019 3 4.58[1.17–8.99] 98.43, p < 0.001
≥2019 5 2.75[1.45–4.05] 91.75, p < 0.001
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4. Discussion

Despite several interventions undertaken regarding to HIV/AIDS related mortality, undernutrition (wasting, stunting and underweight) is continued to be a major predictors of mortality among HIV-infected children. Therefore, this review aimed to estimate the pooled effects of undernutrition on mortality among children living with HIV in Ethiopia.

The finding of this systematic review and meta-analysis indicated that undernutrition has significant role to increases the risk of mortality in children living with HIV/AIDS.

The review disclosed that stunted children living with HIV were 3.36 times more likely to die as compared to well-nourished children. This is reasoned by bidirectional relationship nature of chronic undernutrition and HIV- infection [44]. The coexistence of HIV-infection and stunting further compromises the immune system [45,46]. Studies evidenced that nutritional status, immune system and HIV are intricate and intertwined [19]. As immunity system weakened, the risk for acquiring of opportunistic infections increased [47].Decreased immunity also complicates the treatment of HIV by interfere with intestinal absorption of drugs and various nutrients [48] and thereby increases the progression HIV to AIDS which finally hastens morbidity and mortality rate of children infected with HIV [46].

This study also showed that HIV-infected children complicated with acute undernutrition were more hazards to die than well-nourished children. It is supported by a study done in Tanzania, Malawi, low income countries and a systematic review and meta-analysis study conducted in Sub-Saharan Africa and East Africa [[48], [49], [50], [51], [52], [53]]. Similarly, an evidence from elsewhere also revealed that HIV- infected children with severe acute malnutrition(SAM) were nine times risk of death compared with their normal peers. This is due to the double burden of acute malnutrition/wasting and HIV which results in increased incidence and severity of concurrent infections, making clinical management more challenging [54]. SAM on the background of HIV prone children for further complications, electrolyte disorders, micronutrient deficiencies, lethal opportunistic infections like tuberculosis, persistent diarrhea, pneumonia which contribute to high mortality [55].

Furthermore, the review indicated that underweight is major predictor of mortality and low survival among children with HIV. Our finding is in line with the study done in Zambia, Kenya and democratic Republic of Congo [[56], [57], [58]]. This is justified by HIV-infected children who is manifested with low weight for age ratio is a marker of disease progression and significant factors to low survival and premature death [59]. Nutritional deficiency/underweight and HIV/AIDS are jeopardized conditions that exposed children delayed immune recovery and life threatening medical complications which increase the risk of death [13].

Sub-group analyses based on publication year also disclosed that undernutrion has an exaggerated effect on mortality among studies published before 2019.This is explained by that the country has planned and implemented different strategies to reduce morbidity and mortality of people due to HIV/AIDS afterwards [60]. Moreover, the result of sub-group analysis based on the sample size revealed that stunting and underweight have significant effect on mortality of children living with HIV among studies done with sample size less than 450.

4.1. Strength and limitation of the study

This is the first review to determine the pooled effects of undernutrion on the mortality of children infected with HIV in Ethiopia. Sub-group analysis was done to minimize statistically significant heterogeneity and all the included studies were cohort study design which better identifies cause and effect relationship. Although the above strength of the study, it has some drawbacks that the reader should consider. Qualitative studies and articles published other than English language was excluded. The study included some studies with small sample size and significant heterogeneity which might affect the pooled effect estimates. The review included a small number of primary studies which minimize the strength of representativeness.

5. Conclusion

This Meta-analysis and systematic review revealed that undernutrition (stunting, wasting and underweight) has deleterious effect on mortality of children infected with HIV/AIDS by disease progression and prone the children to serious opportunistic infections. From the study, the authors recommended that nutritional status of children on antiretroviral therapy need to be evaluated regularly. In addition, parents/care providers are counseled to nourish the recommended balance diet and the complex nature of undernutrion and HIV-infections.

Funding statement

This research did not receive any specific grant.

Ethics statement

Ethical clearance is not applicable for this systematic review and meta-analysis, because we extracted the data from previous primary studies.

Data availability statement

All data are available on the manuscript and supporting files.

CRediT authorship contribution statement

Amare Kassaw: Writing – review & editing, Writing – original draft, Visualization, Validation, Supervision, Software, Resources, Methodology, Investigation, Formal analysis, Conceptualization. Bogale Chekole: Writing – review & editing, Writing – original draft, Methodology. Muluken Chanie Agimas: Writing – review & editing, Writing – original draft, Software, Project administration. Molla Azmeraw: Writing – review & editing, Writing – original draft, Resources. Biruk Beletew: Writing – review & editing, Writing – original draft. Shegaw Zeleke: Writing – review & editing, Writing – original draft, Visualization, Software. Worku Necho Asferi: Writing – review & editing, Writing – original draft. Solomon Demis: Writing – review & editing, Writing – original draft, Investigation. Habtamu Shimeles Hailemeskel: Writing – review & editing, Writing – original draft, Validation. Wubet Alebachew Bayih: Writing – review & editing, Writing – original draft. Ermias Sisay Chane: Writing – review & editing, Writing – original draft. Demewoz Kefale: Writing – review & editing, Writing – original draft. Tigabu Munye Aytenew: Writing – review & editing, Writing – original draft, Visualization, Validation.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.heliyon.2024.e29308.

Abbreviations

HIV

Humane Immune Virus

AIDS

Acquired Immune Deficiency Virus

HAART

Highly Active Antiretroviral Therapy

ART

Antiretroviral Therapy

SAM Severe acute Malnutrition
AHR

Adjusted Hazard Ratio

CI

Confidence Interval

Appendix A. Supplementary data

The following are the Supplementary data to this article:

Multimedia component 1
mmc1.docx (19.6KB, docx)
Multimedia component 2
mmc2.docx (17.2KB, docx)

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