Prevalence of undernutrition and associated factors among adults taking antiretroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis

Awole Seid; Omer Seid; Yinager Workineh; Getenet Dessie; Zebenay Workneh Bitew

doi:10.1371/journal.pone.0283502

. 2023 Mar 24;18(3):e0283502. doi: 10.1371/journal.pone.0283502

Prevalence of undernutrition and associated factors among adults taking antiretroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis

Awole Seid ^1,^2,^*, Omer Seid ³, Yinager Workineh ⁴, Getenet Dessie ^1,⁵, Zebenay Workneh Bitew ^2,⁶

Editor: Joel Msafiri Francis⁷

PMCID: PMC10038308 PMID: 36961844

Abstract

Background

Undernutrition (Body Mass Index < 18.5 kg/m2) is a common problem and a major cause of hospital admission for patients living with HIV. Though sub-Saharan Africa is the most commonly affected region with HIV and malnutrition, a meta-analysis study that estimates the prevalence and correlates of undernutrition among adults living with HIV has not yet been conducted. The objective of this study was to determine the pooled prevalence of undernutrition and associated factors among adults living with HIV/AIDS in sub-Saharan Africa.

Methods

Studies published in English were searched systematically from databases such as PubMed, Google Scholar, and gray literature, as well as manually from references in published articles. Observational studies published from 2009 to November 2021 were included. The data extraction checklist was prepared using Microsoft Excel and includes author names, study area, publication year, sample size, prevalence/odds ratio, and confidence intervals. The results were presented and summarized in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) standard. Heterogeneity was investigated using the Q test, I², τ², τ and predictive interval. STATA version 17 was used to analyze the data. A meta-analysis using a random-effects model was used to determine the overall prevalence and adjusted odds ratio. The study has been registered in PROSPERO with a protocol number of CRD42021268603.

Results

In this study, a total of 44 studies and 22,316 participants were included. The pooled prevalence of undernutrition among adult people living with HIV (PLWHIV) was 23.72% (95% CI: 20.69–26.85). The factors associated with undernutrition were participants’ age (AOR = 0.5, 95% CI: 0.29–0.88), gender (AOR = 2.08, 95% CI: 0.22–20.00), World Health Organization (WHO) clinical stage (AOR = 3.25, 95% CI: 2.57–3.93), Cluster of Differentiation 4 (CD4 count) (AOR = 1.94, 95% CI: 1.53–2.28), and duration of ART (AOR = 2.32, 95% CI: 1.6–3.02).

Conclusion

The pooled prevalence of undernutrition among adult PLWHIV in sub-Saharan Africa remained high. WHO clinical stage, CD4 count, duration of ART treatment, age, and sex were found to be the factors associated with undernutrition. Reinforcing nutrition counseling, care, and support for adults living with HIV is recommended. Priority nutritional screening and interventions should be provided for patients with advanced WHO clinical stages, low CD4 counts, the male gender, younger age groups, and ART beginners.

Introduction

According to the United Nations Program on HIV/AIDS (UNAIDS) 2021 fact sheet, there were 38.4 million people living with HIV, of whom 36.7 million were adults (15 years of age or older). Seventy-six percent of adults living with HIV had access to ART treatment [1]. Sub-Saharan Africa accounted for 57% of all new HIV infections in 2019 [2]. Similarly, Eastern and Southern Africa constituted the largest number of AIDS-related deaths (280,000) globally in 2021 [1]. Despite progress in HIV care, the overall life expectancy among adults living with HIV is 5 to 10 years less than that of uninfected adults [3]. Malnutrition takes the lion’s share in increasing the risk of mortality and the occurrence of other opportunistic infections among adults living with HIV [4, 5].

Poor nutrition and HIV have bidirectional relationships and exacerbate one another [6]. In resource-limited countries like sub-Saharan Africa, many people living with HIV (PLWHIV) on long-term ART follow-up lack adequate nutrition [7, 8], and, undernutrition is an indicator of a poor prognosis of HIV care [9]. Similarly, malnutrition is among the major causes of hospital admission in PLWHIV [10]. Meanwhile, HIV affects nutritional status in three distinct ways. It decreases food consumption (through poor appetite and inability to eat and swallow), raises energy needs (up to 20% more energy), and hinders the body’s ability to absorb nutrients. All these factors predispose patients to undernutrition and finally to wasting syndrome [11]. Thus, identifying and treating malnutrition in people living with HIV can fasten recovery from infection, enhance immunity, and possibly slow the progression to AIDS [12].

A meta-analysis study in Ethiopia showed the pooled prevalence of undernutrition among adults receiving ART was 26%. Undernutrition among people living with HIV is associated with socio-demographic and clinical factors such as age, WHO clinical stage, CD4 count, duration of ART treatment, and food security [13, 14]. There is a need to estimate the overall prevalence of undernutrition in Sub-Saharan Africa, as the region remains the world’s epicenter of HIV transmission. Similarly, several studies indicated that the region is affected by food insecurity, which is directly linked to undernutrition for individuals, households, and communities affected by HIV [15–18]. Beside this, several nutritional programs to address undernutrition in adults living with HIV in sub-Saharan Africa have been instituted without consolidated evidence on the overall estimates of the prevalence and correlates of undernutrition [19]. Moreover, the available primary studies in sub-Saharan Africa lack consistency and are not conclusive. Therefore, the purpose of this meta-analysis study was to determine the pooled (overall) prevalence of undernutrition and its associated factors among adults living with HIV in sub-Saharan Africa. This study will help policymakers devise evidence-based nutrition intervention programs for patients living with HIV in sub-Saharan Africa.

Methods

Inclusion and exclusion criteria

Both published and unpublished observational studies (i.e., cross-sectional, case-control, and cohort) conducted among HIV-positive adults in SSA countries were included. Articles published only in the English language were included. On the other hand, studies with no free full texts, and studied only pregnant women were excluded. For clarity, the topic is described using a PICO format as follows:

Population (P): Adult patients (> 15 year, as defined by UNAIDS and other studies) [20].
Intervention or exposure (I): Living with HIV
Comparison or control (C): Living without HIV
Outcome (O): Undernutrition (prevalence)

Information source and search strategy

We used the databases mainly PubMed, Google Scholar, and Gray (unpublished) literature, university repositories, and manual searches of references from a list of included articles. Articles published from 2009 to November 10, 2021, were included. We used 2009 as there was a previous study among women living with HIV and published in 2008. However, our study also included male adults. Articles identified through the electronic searches were exported and managed using EndNote Version 8 reference manager. Articles from PubMed were accessed using the following keywords (Table 1).

Table 1. The search strategy used in the PubMed database, 2021.

Key variables	Searching words in PubMed
Prevalence of undernutrition	“Proportion” or “Prevalence” or “Magnitude” or “Burden” AND “Malnutrition” OR “Undernutrition” OR “Under-weight” OR “Wasting” OR “Malnourished” AND “Adult” AND “Living with HIV” OR “HIV-positive” OR “HIV-infected” OR “Anti-Retroviral Therapy” AND (Each country) sub-Saharan Africa”.
Associated factors	“Associated factors” OR “Determinants” OR “Predictors” OR “Correlates” AND “Malnutrition” OR “Undernutrition” OR “Under-weight” OR “Wasting” OR “Malnourished” AND “Adult” AND “Living with HIV” OR “HIV-positive” OR “HIV-infected” OR “Anti-Retroviral Therapy AND (Each country) in sub-Saharan Africa”.

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Studies were selected after two reviewers (AS) and (OS) independently screened for inclusion eligibility. A third author (GD) was involved in resolving disagreements between the two authors.

Data collection process and data items

The authors prepared data extraction using Microsoft Excel. All relevant data for this review were extracted by two reviewers (AS and OS). The disparities between reviewers at the time of data abstraction were resolved through discussion with the third author (ZWB).

The data extraction sheet included primary authors, publication year, country, study design, sample size, response rate, study setting, study population, proportion, 95% confidence interval, and the logarithm of proportion S1 Table.

Effect measures

We include studies that measure under-weight (undernutrition) using BMI < 18.5 Kg/m². Underweight was utilized as an indicator of advanced malnutrition, despite the fact that it does not reliably indicate the nutritional status of adults [21]. The proportion of undernutrition was calculated by dividing the number of individuals under-nourished by the total sample of study subjects included in the final analysis. We used the adjusted odds ratio (AOR) as an effect measure to find associated factors of undernutrition.

Risk of bias assessment

Newcastle Ottawa Scale (NOS) adapted for cross-sectional studies was used to assess the quality of the studies. NOS has three categories and has a maximum score of 10 for cross-sectional studies. The categories are selection (maximum of 5 stars), comparability (maximum of 2 stars), and study outcome (maximum of 3 stars). Each study was independently appraised by two authors. Disagreements between authors were resolved through discussion with a third author. Finally, the quality score of each study was calculated as the sum of scores, thus ranging from zero to ten for cross-sectional studies, and zero to nine for cohort and case-control studies. A score of greater or equal to 6 points was considered “good” and included in the study [22]. Additionally, publication bias was assessed using Egger’s regression test, funnel plot, and sensitivity analysis.

Synthesis methods

Data analysis was performed using STATA (version 17) software. We employed a random effect model to find the pooled prevalence and associated factor estimates of under-nutrition. Heterogeneity of effect sizes was assessed using I², τ²,τ and prediction interval. Subgroup and trim and fill were performed to deal with the potential source of heterogeneity. Sensitivity analysis was also performed. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist is used for data presentation S2 Table [23].

Results

Study selection and characteristics

A total of 3,477 articles were identified from PubMed, Google scholar, and gray literature in the initial search. After the removal of 1,220 duplicates, 2,257 articles were screened for title and abstract. In the next step, 2,194 articles were excluded based on titles and abstracts. The full texts of 62 articles were downloaded and assessed against inclusion criteria. Thus, 18 articles were excluded for the following reasons: 7 studies did not report data on the outcome variable [5, 24–29], six studies were review papers [4, 14, 30–33], three studies focused on children [30, 34, 35], one study was conducted out of SSA [36], one study focused on pregnant women [37], and one study lacks full text [38]. Finally, 44 studies were included in final systematic review and meta-analysis (Fig 1) [23]. No studies were excluded after appraising the quality using NOS.

In this study, a total of 22,316 adults living with HIV were included. The sample size of the included studies ranged from 145 in Botswana to 3,993 in Tanzania. Of the 44 included studies, only one was a retrospective cohort and the rest were carried out using cross-sectional study designs. The largest number of articles (33 studies) were reported from Ethiopia [8, 39–70] and only one article is reported from Kenya [71], Botswana [72], Ghana [73], Democratic Republic of Congo (DRC) [74], Senegal [75], Uganda [76], and Zimbabwe [77]. Four articles were from each of South Africa [78, 79] and Tanzania [13, 80]. Regarding the publication year, studies were published from 2009 to 2021 and the majority of the studies (11), were reported in 2020, followed by nine in 2017, and five in each of 2018 and 2015 (Tables 2 and 3).

Table 2. Study characteristics included in meta-analysis of undernutrition among adult PLWHIV in sub-Saharan Africa, 2009–2021.

S. N	Authors	Publication Year	Country		Sample Size	Study design	Mean/ age range (year)	ART Status	No of cases	P	95% CI	NOS
1	Adal M, Howe R, Kassa D et al	2018	Ethiopia		594	Cross-sectional	34	Pre-ART	87	15.1	12.2–17.9	6
2	Akilimali PZ, Musumari PM, Kashala-Abotnes E et al	2016	DRC		583	Cross-sectional	41	On ART	141	24.1	20.6–27.6	8
3	Amza L, Demissie T, Halala Y.	2017	Ethiopia		519	Cross-sectional	18–45+	On ART	133	26.6	22.8–30.4	8
4	Asnakew M.	2015	Ethiopia		340	Cross-sectional	35	On ART	103	31.2	26.3–30.1	7
5	Benzekri NA, Sambou J, Diaw B,	2015	Senegal		109	Cross-sectional	45	On ART	25	22.9	15.0–30.8	6
6	Birhane M, Loha E, Alemayehu FR.	2015	Ethiopia		389	Cross-sectional	40	On ART	60	25	20.7–29.3	8
7	Daka DW, Ergiba MS.	2020	Ethiopia		1062	Cross-sectional	16–50+	On ART	357	34	31.1–36.8	8
8	Daniel M, Mazengia F, Birhanu D.	2013	Ethiopia		408	Cross-sectional	18–45+	Pre & on ART	104	25.5	21.3–29.7	8
9	M Dedha, M Damena, G Egata et al	2017	Ethiopia		459	Cross-sectional	35	On ART	131	30	25.8–34.2	7
10	Fentie M, Wassie MM, Tesfahun A,	2017	Ethiopia		317	Cross-sectional	39	On ART	57	18.3	14.0–22.6	6
11	Fufa H, Umeta M, Taffesse S et al	2009	Ethiopia		153	Cross-sectional	27	Pre-ART	27	18	11.9–24.1	7
12	Gebru TH, Mekonen HH, Kiros KG.	2020	Ethiopia		394	Cross-sectional	41	On ART	169	42.9	38.0–47.8	7
13	Gedle D, Gelaw B, Muluye D,	2015	Ethiopia		305	Cross-sectional	40	On ART	77	25.2	20.3–30.1	8
14	Girma M, Motuma A, Negasa L.	2017	Ethiopia		502	Cross-sectional	24	Pre & on ART	133	26.5	22.6–30.4	8
15	Gebremichael DY, Hadush KT, Kebede EM, et al	2018	Ethiopia		512	Cross-sectional	34	On ART	119	23.6	19.9–27.3	8
16	Hadgu TH, Worku W, Tetemke D, et al	2013	Ethiopia		276	Cross-sectional	33	On ART	159	42.3	36.5–48.1	6
17	Hailemariam S, Bune GT, Ayele HT et al	2013	Ethiopia		520	Cross-sectional	34	On ART	64	12.3	9.4–15.1	8
18	Kabalimu TK, Sungwa E, Lwabukuna WC.	2018		Tanzania	125	Cross-sectional	20–60+	On ART	24	19.4	12.5–26.3	6
19	Kenea MA, Garoma S, Gemede HF.	2015		Ethiopia	423	Cross-sectional	15–50+	On ART	112	26.47	22.3–30.7	7
20	Getaw Kume	2017		Ethiopia	457	Cross-sectional	41	On ART	53	12.3	9.3–15.3	8
21	Mahlangu K, Modjadji P, Madiba S.	2020		South Africa	480	Cross-sectional	35	On ART	62	13	9.9–16.0	7
22	Mitiku A, Ayele TA, Assefa M, et al	2016		Ethiopia	452	Cross-sectional	35	On ART	105	23.2	19.3–27.1	7
23	Motuma A, Abdeta T.	2021		Ethiopia	502	Cross-sectional	37	On ART	133	26.5	22.6–30.4	8
24	Mulu H, Hamza L, Alemseged F.	2016		Ethiopia	109	Cross-sectional	33	On ART	51	46.8	37.4–56.2	6
25	Naidoo K, Yende-Zuma N, Augustine S	2018		South Africa	1000	Retrospective cohort	NR	On ART	149	15.7	13.5–17.9	7
26	Nanewortor BM, Saah FI, Appiah PK, et al	2021		Ghana	152	Cross-sectional	39	On ART	21	13.8	8.3–19.3	6
27	Nigusso FT, Mavhandu-Mudzusi AH	2020		Ethiopia	390	Cross-sectional	36	On ART	232	60	55.1–64.9	7
28	Nnyepi MB	2009		Botswana	145	Cross-sectional	33	Pre & on ART	41	28.5	21.2–35.9	6
29	Odwee A, Kasozi KI, Acup CA,	2020		Uganda	253	Cross-sectional	39	On ART	26	10.28	6.5–14.0	7
30	Oumer B, Boti N, Hussen S, et al	2019		Ethiopia	333	Cross-sectional	33	On ART	79	23.72	19.2–28.3	7
31	Regassa TM, Gudeta TA.	2020		Ethiopia	1007	Cross-sectional	18–50+	On ART	154	16	13.7–18.3	8
32	Sahile AT, Ayehu SM, Fanta SF.	2021		Ethiopia	319	Cross-sectional	31–41+	On ART	61	19.1	14.8–23.4	6
33	Saito A, Karama M, Kamiya Y.	2020		Kenya	251	Cross-sectional	38	On ART	21	8.3	4.9–11.7	6
34	Saliya MS, Azale T, Alamirew A,	2018		Ethiopia	428	Cross-sectional	36	On ART	97	24.1	20.1–28.2	7
35	Shifera N, Molla A, Mesafint G, et al	2020		Ethiopia	402	Cross-sectional	34	On ART	115	29.2	24.8–33.6	7
36	Sunguya BF, Ulenga NK, Siril H,et al	2017		Tanzania	3993	Cross-sectional	38	Pre-ART	1106	27.7	26.3–29.1	9
37	Takarinda KC, Mutasa-Apollo T, Madzima B, et al	2017		Zimbabwe	1,242	Cross-sectional	41	On ART	122	10	8.3–11.7	8
38	Takele AE, Engida AR.	2017		Ethiopia	295	Cross-sectional	34	On ART	71	24	19.1–28.9	7
39	Teklu T, Chauhan NM, Lemessa F, et al	2020		Ethiopia	519	Cross-sectional	41	On ART	95	18.3	14.9–21.6	7
40	Teshome	2017		Ethiopia	302	Cross-sectional	36	On ART	81	27.2	22.2–32.2	6
41	Wasie B, Kebede Y, Yibre A.	2010		Ethiopia	331	Cross-sectional	34	On ART	92	27.8	22.9–32.6	6
42	Wasihun Y, Yayehrad M, Dagne S et al	2020		Ethiopia	350	Cross-sectional	35	On ART	85	26.9	22.3–31.6	6
43	Yitbarek GY, Engidaw MT, Ayele BA, et al	2020		Ethiopia	263	Cross-sectional	38	On ART	30	11.9	7.9–15.8	6
44	Zemede Z, Tariku B, Kote M, et al	2019		Ethiopia	351	Cross-sectional	40	On ART	64	18.23	14.2–22.3	7

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DRC: Democratic Republic of Kongo

ART: Antiretroviral therapy, NR: Not reported

Table 3. Sub-group analysis of the prevalence of undernutrition among adults living with HIV in sub-Saharan Africa by country, study design, and publication year, 2009–2021.

Variables	Responses	No of studies	Pooled prevalence (95% CI)	I² (p-value)
Country	Ethiopia	33	25.8% (22.4–29.3)	95.9% (0.001)
	Tanzania	2	24.3% (16.3–32.3)	81.08% (0.022)
	South Africa	2	14.5% (14.9–17.2)	49.33% (0.16)
	Kenya	1	8.3% (4.9–11.7)	-
	DRC	1	24.1% (20.6–27.6)	-
	Senegal	1	22.9% (15.0–30.8)	-
	Botswana	1	28.5% (21.2–35.9)	-
	Ghana	1	13.8% (8.3–19.3)	-
	Uganda	1	10.3% (6.5–14.0)	-
	Zimbabwe	1	10% (8.3–11.6)	-
Study design	Cross-sectional	43	23.9% (20.9–26.9)	96.67% (0.001)
Study design	Retrospective cohort	1	15.7% (13.4–17.9)	-
Publication year	2009–2015	11	25.8% (21.3–30.3)	89.72% (0.001)
Publication year	2016–2021	33	23.1% (19.4–26.8)	97.52% (0.001)
ART characteristics	Pre-ART	3	20.5% (12.6–28.3)	95.32% (0.001)
	Both “on & pre” ART	3	26.4% (23.7–29.1)	0.00% (0.783)
	On ART	38	23.8 (20.4–27.2)	96.84% (0.001)

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NB: meta-analysis works when two or more effect estimates are reported

Quality appraisal results

The heterogeneity test of the study revealed I² = 96.8%, τ² = 98.83, τ = 9.94, prediction interval (13.8–33.68%), and 95% confidence interval of the average estimate (20.69–26.79%). The source of high I2 is not identified, though it is expected to rise in a meta-analysis of proportions in different countries, and the result should be interpreted conservatively [81]. Furthermore, the study also demonstrated a wide prediction interval, a direct and easily interpretable indicator as compared to the confidence interval, implying evidence of high heterogeneity. Regarding the publication bias, Egger’s regression test (B1 = 5.72, p = 0.002) showed there was publication bias but studies looked relatively symmetrical in the funnel plot (Fig 2). However, these indicators of publication bias were developed in the context of comparative data and may not be reliable indicators of publication bias in a meta-analysis of proportions [82].

Sub-group analysis and trim and fill analysis were also performed to deal with the publication bias and heterogeneity S3 Table. A sensitivity analysis was performed and all estimates were within the confidence interval limit, and no individual study contributed to the publication bias. Consequently, it is unnecessary to exclude studies from the final meta-analysis.

Meta-analysis results

Prevalence of undernutrition among adult PLWHIV in sub-Saharan Africa

Of the 44 studies that reported a proportion of undernutrition, the highest prevalence (60%) was reported in Ethiopia [58], whereas the lowest (8.3%) was reported in Kenya [71]. Majority of the studies are reported from Ethiopia (33 studies), cross-sectional design (43 studies), carried out during 2016–2021 (33 studies), and on patients taking ART (38 studies).

In this study, the pooled prevalence of undernutrition using a random-effect model meta-analysis was found to be 23.74% (95% CI: 20.77–26.73) (Fig 3). Sub-group analysis by country showed 25.8% (95% CI: 22.4–29.3) in Ethiopia, 14.5% (95% CI: 14.9–17.2) in South Africa, and 24.3% (95% CI: 16.3–32.3) in Tanzania. Additional sub-group analysis by ART status, by study design, and by publication year also carried out (Table 3).

Factors associated with undernutrition among adults of PLWHIV in sub-Saharan Africa

From the searched published articles 16 reported “WHO clinical stage” [13, 39, 41–43, 45, 47, 50, 52, 57, 59, 60, 64–66, 68, 83], four studies reported “CD4 count” [40, 43, 47, 55, 57, 59, 60, 80, 83], four studies reported patient’s “age” [13, 39, 55, 56, 60, 77], four studies reported “sex” [40, 56, 64, 80, 83], and four articles reported “duration of ART treatment” [8, 59, 64, 67, 68] as factors associated with undernutrition among adult PLWHIV in sub-Saharan Africa (Table 4). Patients living with HIV and WHO clinical stage III/IV were 3.25 (AOR, 95% CI: 2.57–3.93) times higher odds of developing undernutrition as compared to WHO clinical stage I/II (Fig 4). Similarly, patients whose CD4 count was less than 200cells/mm³ were 1.94 times (AOR = 1.94, 95% CI: 1.53–2.28) with higher odds of developing undernutrition as compared to their counterparts (CD4 ˃500cells/mm³) (Fig 5).

Table 4. Summary of the factors associated with undernutrition among adults living with HIV in sub-Saharan Africa, 2021.

Factor	No of included studies	Pooled AOR (95% CI)	I² (p-value)	Reference category
WHO clinical stage	16	3.25 (2.57–3.94)	I² = 0.0% (0.233)	WHO clinical Stage I
CD4 count	10	1.91 (1.53–2.29)	I² = 0.0% (0.535)	CD4 ˃ 500 cells /mm³
Age	4	0.51 (0.31–0.71)	I² = 31.2% (0.11)	19–30 years
Sex	4	2.11 (1.52–2.7)	I² = 0.0% (0.534)	Females
ART duration	4	2.31 (1.6–3.02)	I² = 0.0% (0.001)	≥12 months

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Regarding the age of study participants, patients aged 40 years and above had 49% lower odds of developing undernutrition as compared to those aged 19 to 30 years (AOR = 0.51, 95% CI: 0.26–0.76) (Fig 6). Furthermore, the odds of developing undernutrition among males living with HIV were 2 times (AOR = 2.11, 95% CI: 1.52–2.7) higher as compared to female patients (Fig 7). Similar to this, patients receiving ART for less than 12 months had 2.68 times the risk of developing undernutrition compared to individuals taking it for more than 12 months (Fig 8). This implies that the longer the duration of patients’ taking ART, the lower the risk of developing under-nutrition.

Discussion

Despite the improvement of comprehensive HIV care, sub-Saharan Africa continues to be an epicenter of HIV transmission and has a high prevalence of malnutrition among adults living with HIV. This study aimed to investigate the pooled prevalence and correlates of undernutrition among adults living with HIV/AIDS. The result shows a significant number of adults living with HIV are malnourished, and several socio-demographic and clinical factors have been associated with undernutrition.

In this meta-analysis, the pooled prevalence of undernutrition (adult BMI <18.5kg/m²) among adults living with HIV was high (23.74%) and interpreted as a serious situation according to WHO nutrition landscape information system cut-off values (20–39%) [84]. It is serious because studies have shown that undernutrition increases the risk of opportunistic infections (OIs) and mortality [4, 85]. The pooled prevalence slightly decreased from 25.8% in 2009–2015 to 23% in 2015–2021. This might be attributed to the expansion of nutrition intervention programs and the improvement of comprehensive HIV care in Africa. This finding is in line with a previous meta-analysis study in Ethiopia, in which the pooled prevalence was reported as 26% (95% CI: 22–30%) [14].

In contrast, our finding is higher as compared to a previous meta-analysis study conducted on women living with HIV in sub-Saharan Africa: 10.3% (95% CI: 7.4%–14.1%). The study used secondary data from the DHS and analyzed the reported estimate of only 11 sub-Saharan African countries. The disparity might be explained by the fact that over the last 13 years, there have been changes in socio-demography, the trend of HIV incidence, food insecurity, and other population factors that might have been associated with undernutrition. Moreover, the study was carried out only among women, which may have affected the result. Nevertheless, our study also asserts that men living with HIV are at a higher risk of developing malnutrition as compared to women [37], even though the biological mechanism is not clear.

We also found that patients with an advanced WHO clinical stage, a lower CD4 count, being of male sex, a younger age, and a shorter duration of ART treatment had a higher likelihood of developing undernutrition in adults living with HIV. The factor regarding the WHO clinical stage was also reported in a meta-analysis report in Ethiopia [86]. This may be due to the advanced WHO clinical stage and low CD4 count, which are indicators of severe immune deficiency are directly linked to undernutrition, especially protein and energy malnutrition. Thus, it is important to give due emphasis to nutrition counseling and supplementation with high-energy and protein foods during the follow-up visit.

Furthermore, young adults and ART beginners were identified as being at risk for malnutrition. The reason for the younger ages might be due to the poor emotional readiness to accept the disease condition and the failure to receive comprehensive HIV care at an early age. On the other hand, increasing age may improve acceptance and the perceived benefits of adherence to recommendations by health care providers. However, the result for younger ages requires further exploration. In spite of this, although it is acknowledged that receiving ART improves nutritional status, the impact of HIV on nutrition begins even before diagnosis and needs a longer course of therapy in order to be reversed, and noticed by anthropometric measurements.

Limitation of the study

The possible limitation for this review was the inability of accessing some databases like EMBASE, CINHAL, and Scopus. This was compensated by searching for published articles in broad databases like Google scholar. The other limitation is the absence of similar meta-analysis studies for comparison of our result. There is an uneven distribution of included studies among countries, a large number of which were reported from Ethiopia. Additionally, there is high heterogeneity, and studies published only in English were included.

Conclusion

Supporting information

S1 Table. Data extraction sheet used in the meta-analysis of the prevalence and associated factors of undernutrition among adults taking antiretroviral therapy in sub-Saharan Africa, 2009–2021.

(XLSX)

Click here for additional data file.^{(34.4KB, xlsx)}

S2 Table. PRISMA statement presentation of systematic review and meta-analysis of undernutrition among adults taking ART in SSA, 2009–2021.

(DOCX)

Click here for additional data file.^{(32.6KB, docx)}

S3 Table. Trim and fill analysis of prevalence of undernutrition and associated factors among adult PLWHIV in SSA, 2009–2021.

(DOCX)

Click here for additional data file.^{(32.9KB, docx)}

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

The authors received no specific funding for this work.

References

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PONE-D-21-36754Prevalence and associated factors of under-nutrition among adults taking anti-retroviral therapy in sub-Saharan Africa: A systematic review and meta-analysisPLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: No

Reviewer #2: No

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Prevalence and associated factors of under-nutrition among adults taking anti-retroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis

1. General comment: Relevant topic, consolidating evidence about the relationship between under-nutrition and ART.

However, the whole article needs to be revisited to make sure that English language is well written especially writing the article in a past tense. The authors should define abbreviations used for the first time

2. Abstract:

Background: Lacks the research gap and the broad aim/objective of conducting the study. Method: Some sentences written in present tense instead of past tense.

3. Main body:

Introduction: Revisit the first sentence in the first paragraph (Probably the authors meant that the rate of new HIV infection is decreasing Worldwide). 5th and 6th paragraphs talked about previous studies which also determined prevalence of under-nutrition and associated factors with HIV. However, the authors did not show the gap intended to be filled by the current study. It is not clear why the current meta-analysis was done as there were already some meta-analysis done as indicated in the literature review. However, the rationale is well stated.

Method: Include a table showing the PICO of the systematic review. Search words shown are only those for PubMed. I suggest you list all the search words considered in every search engine without giving the details of how the different search words were related (OR/AND). Give initials for the third author.

Results: Arrange the table and figures e.g. the PRISMA as they are discussed in the results section.

Discussion: Avoid repeating results in the discussion section

Reviewer #2: This was a systematic review to estimate pooled prevalence of under nutrition and associated factors among PLHIV in sSA.

Comment:

Overall:

Manuscript need English proof reading. Several areas past tense have not been used, conjunction missing. Message not clearly communicated

Title: Consider revising it to “Prevalence of under-nutrition and its associated factors among adults taking anti-retroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis”

Define HIV appropriately as Human immunodeficiency virus. Do dot prefer people as HIV infected, you may consider using people living with HIV as the former is regarded as stigmatizing

Introduction:

There are about 7 paragraphs. Not clearly aligned. Consider reducing number of paragraphs to about 4 and each should carry specific message. Stating bidirectional relationship between ART and undernutrition without describing it not enough.

22 times more likely, if the study did not use risk ration, interpretation is not right.

Methods:

Needs English proof reading

Issues such as ‘The review is aimed……’; ‘databases are accessed…..’ needs revision to past tense. The word on the other had was used severally in the manuscript but not showing clear contrast

‘…..to find associated factors of under-nutrition’ could be factors associated with under-nutrition

Results.

There is unnecessary bolding of numbers or reference (eg figure xxx) , a total of 22316 etc

‘Sensitivity analysis is performed…..’ Needs to be past tense through out the manuscript

Odds ratios were not appropriately interpreted. The odds of X is 2 times that of Y. Not 2 times higher

‘……1.94 times more likely ….’ Is not appropriate, can be written 1.94 higher odds of having under-nutrition. This is not a risk ratio, you can’t say more likely

Discussion:

Needs revision

Like introduction, consider few paragraph with specific message

1- Paragraph- summarize main findings

2-3 Paragraphs- consider main factors to expand

4- para- consider limitations and strength

5- conclusion

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6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

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PLoS One. 2023 Mar 24;18(3):e0283502. doi: 10.1371/journal.pone.0283502.r002

Author response to Decision Letter 0

14 May 2022

Response to reviewer #1

General comment: the whole article needs to be revisited to make sure that English language is well written especially writing the article in a past tense. The authors should define abbreviations used for the first time. The authors should define abbreviations used for the first time.

Response: We noted several English proofreading problems in the manuscript. We have made corrections word by word. I also invited English language editors to minimize language problems. Grammatical errors are also corrected.

Yes abbreviations should be defined in the first use and we made corrections.

Comment on abstract:

Background: Lacks the research gap and the broad aim/objective of conducting the study. Method: Some sentences written in present tense instead of past tense.

Response: We incorporate the research gap and objective in the background section of the abstract. We changed verbs to past tense in the method section.

Comment

1. Main body:

Response: The first and second paragraphs are merged and paraphrased. Meta-analysis was done in Ethiopia, not at the sub-Sahara Africa level. There are a number of studies but lacks consistency. Besides, we believe a single country figure will not represent the region. Therefore, this is the first review in sub-Sahara Africa and this statement is incorporated in the paragraph.

Comment

Response: Thank you for this comment and PICO table is incorporated and makes the study more clear. Search words and Mesh terms were used only for PubMed because it is an open access database. We have no institutional access to Embase, Scopus and other databases which is described under limitation. Therefore, we didn’t use different search words for these databases. However, we searched articles in Google scholar which is comprehensive and include articles indexed in those databases.

Comment on results: Arrange the table and figures e.g. the PRISMA as they are discussed in the results section.

Response: We arranged and make results in line with the PRISMA chart.

Comment on discussion: Avoid repeating results in the discussion section

Response: We noted some repetition of results in the discussion section and removed it.

Response to reviewer #2

Overall comment:

Manuscript need English proof reading. Several areas past tense have not been used, conjunction missing. Message not clearly communicated

Title: Consider revising it to “Prevalence of under-nutrition and its associated factors among adults taking anti-retroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis”. Define HIV appropriately as Human immunodeficiency virus. Do dot prefer people as HIV infected, you may consider using people living with HIV as the former is regarded as stigmatizing

Response: We admit the manuscript had language problems and we undergo thorough revision and language editors were also invited to help us communicate the message clearly. The comment on title sounds more logical if the title is rephrased and done as indicated by the reviewer. The abbreviation HIV is defined appropriately. We also accept the comment of stigmatizing expression of “HIV infected…” We corrected the expression throughout the manuscript.

Comment

Introduction:

Response:

The paragraphs in the introduction are abridged to four and each carries specific messages. Regarding the interpretation of the odds ratio, we agree it is preferable to interpret as indicated and we modified throughout the manuscript.

Comment

Methods:

Needs English proof reading

There is unnecessary bolding of numbers or reference (e.g. figure xxx) , a total of 22316 etc

Response:

We changed the tenses in methodology and other sections as commented.

Unnecessary bolding of words or numbers are avoided. We tried to correct the grammatical errors made throughout the manuscript including in the result section.

Comments

Discussion:

Needs revision

Like introduction, consider few paragraph with specific message

1- Paragraph- summarize main findings

2-3 Paragraphs- consider main factors to expand

4 - para- consider limitations and strength

5 – Conclusion

Response:

In the discussion section, we also merge paragraphs with similar messages. Even though there are few studies that limit the discussion, we tried to add other interpretation guides.

Attachment

Submitted filename: Response to reviewers.docx

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PLoS One. doi: 10.1371/journal.pone.0283502.r003

Decision Letter 1

Joel Msafiri Francis

21 Jun 2022

PONE-D-21-36754R1Prevalence of under-nutrition and associated factors among adults taking antiretroviral therapy in sub-Saharan Africa: A systematic review and meta-analysisPLOS ONE

Dear Dr. Ali,

Please submit your revised manuscript by Aug 05 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Joel Msafiri Francis, MD, MS, PhD

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #3: (No Response)

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2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Yes

Reviewer #3: No

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #3: No

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4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: Yes

Reviewer #3: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: Yes

Reviewer #3: Yes

**********

6. Review Comments to the Author

Reviewer #1: Introduction:

• Third sentence, first paragraph: Look for more than one proof for food insecurity in Africa or better look for a systematic review

• Make sure you define all the abbreviation when used for the first time e.g. ART

• Second paragraph: The bi-directionality was not shown; you only showed that malnutrition worsens HIV. The effect of HIV on malnutrition is missing

Reviewer #3: General comment

The interpretation of this review has a bias towards comparing outcomes for Ethiopia with other published outcomes about Ethiopia. Given that all the authors are from Ethiopia, perhaps the authors want to reframe this study title and objectives to having a particular focus on Ethiopia

Specific comments

Wherever point estimates are provided confidence intervals should be included – for both this study, and the supporting background text

Methods

Inclusion criteria – prospective studies were not included?

How was undernutrition defined?

NewCastle Ottawa is good but it is stated that “A score of greater or equal to 6 points was considered “good” and included in the study”. Summary scores are a misleading way to assess quality.

Further, if this was done, the number of studies excluded because they were not considered “good” should be included in the flow diagram and results section narrative

A funnel plot is noted in the abstract and results, but not in the methods.

Subgroup and sensitivity analyses are described in the results, but not the methods.

12 is not the most appropriate test for heterogeneity when the outcome measure is a proportion. As such, it is unsurprising that 12 is >90%. (Tau2 would have been better)

The search strategy is not highly sensitive (eg “Anti-Retroviral Therapy” is a very limited term) and this should be noted as a limitation. Preferably, standard search terms would have been used (eg see search terms used by Cochrane, or search strings used by other reviews cited by this review, eg ref 10.)

Also, the search strategy has two sets of terms

“Proportion” or “Prevalence” or “Magnitude” AND“Malnutrition” OR “Under-nutrition” OR “Under-weight” OR “Wasting” AND “HIV-positive” OR “HIV-infected” OR “Anti-Retroviral Therapy” AND “Adults” AND “ (each country) in subSaharan Africa”.

AND

“Associated factors” OR “Determinants” OR “Predictors” OR “Correlates” AND “malnutrition” OR “under-nutrition” OR “under-weight” OR “Wasting” AND “HIV-positive” OR “HIV-infected” OR “Anti-Retroviral Therapy” AND “Adults” AND “ (each country) Sub-Saharan Africa”

These two sets of terms have duplicate terms. Limiting the search to studies that contain the words “Proportion” or “Prevalence” or “Magnitude” or “Correlates” is quite a crude limitation, as studies could report these outcomes without using these terms.

Results

“Regarding the publication year, 11 articles were published in 2020 followed by 9 articles in 2017. Besides, only one article was reported in 2010”

This is an anecdotal way of describing year of publication, given that 44 studies were included. Please reconsider how to present these data

Tables need legends to explain the acronyms

Figure 3

This is a very unconventional forest plot that does not display pooled estimates and confidence intervals well

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #3: No

**********

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PLoS One. 2023 Mar 24;18(3):e0283502. doi: 10.1371/journal.pone.0283502.r004

Author response to Decision Letter 1

18 Jul 2022

Response to reviewer #1

Comment: Third sentence, first paragraph: Look for more than one proof for food insecurity in Africa or better look for a systematic review

Response: I have included additional systematic review and primary studies to strengthen the evidence.

Comment: Make sure you define all the abbreviation when used for the first time e.g. ART

Response: Abbreviations are defined in the first usage throughout the manuscript.

Comment: Second paragraph: The bi-directionality was not shown; you only showed that malnutrition worsens HIV. The effect of HIV on malnutrition is missing.

Response: The effect of HIV on malnutrition is presented in detail.

Response to reviewer # 3

Comment: The interpretation of this review has a bias towards comparing outcomes for Ethiopia with other published outcomes about Ethiopia. Given that all the authors are from Ethiopia, perhaps the authors want to reframe this study title and objectives to having a particular focus on Ethiopia.

Response: The use of systematic reviews and meta-analysis studies reported from Ethiopia for interpretation and comparison was due to a lack of similar or related studies in other countries, not the authors' origins in Ethiopia. We tried our best to search for meta-analysis results conducted elsewhere outside of Africa too. Of course, we added one meta-analysis study conducted on a similar topic but carried out only among women for additional comparison and interpretation. Notably, 11 out of 44 studies were conducted outside of Ethiopia, and as long as studies are systematically searched and no eligible studies were left in the final analysis, the result can be taken as representative of sub-Sahara African region. In spite of that, we mentioned the dominancy of studies from Ethiopia under the “limitation of the study”.

Comment: Wherever point estimates are provided confidence intervals should be included – for both this study, and the supporting background text.

Response: It is accepted and we included confidence intervals for different point estimates presented in the manuscript.

Comment: Inclusion criteria –prospective studies were not included?

Response: All observational studies reporting prevalence, incidence, and/or determinants were searched. But we didn’t find studies with prospective cohort designs, and only one retrospective cohort study was included.

Comment: How was under-nutrition defined?

Response: Even though there is no single indicator of nutritional status in adults, a low body mass index (BMI) of < 18.5 kg/m2 or underweight is an indicator of advanced malnutrition. The risk becomes higher when patients have chronic diseases like HIV. If it is not prevented or early detected, it will lead to "wasting syndrome," a sign of an advanced immune-compromised state. It was also demonstrated that starting antiretroviral therapy (ART) accelerated mortality (6 months) if the patient's BMI was less than 18. An additional point regarding definition of under-nutrition is added in the manuscript. All of the studies used a BMI of < 18.5kg/m2 to define under-nutrition.

(Koethe, John R., and Douglas C. Heimburger. "Nutritional aspects of HIV-associated wasting in sub-Saharan Africa." The American journal of clinical nutrition 91.4 (2010): 1138S-1142S.

https://emedicine.medscape.com/article/2058483-overview

Comment: Newcastle Ottawa Scale is good but it is stated that “A score of greater or equal to 6 points was considered “good” and included in the study”. Summary scores are a misleading way to assess quality. Further, if this was done, the number of studies excluded because they were not considered “good” should be included in the flow diagram and results section narrative

Response: The Newcastle Ottawa Scale, JBI, and Cochrane risk of bias assessment are the commonly used tools to screen the quality of published studies. When using NOS, it is difficult to make a qualitative judgment for eligibility without a cut-off point. The domain of assessment uses the star method, which is rated out of 10 points for cross-sectional studies. There are also studies published in PLOS ONE using similar judgment. We agree that studies that were not considered "good" should be reported in the flowchart. However, no study is excluded from the analysis due to poor quality.

Comment: A funnel plot is noted in the abstract and results, but not in the methods.

Response: It is incorporated in the method section as indicated.

Comment: Subgroup and sensitivity analyses are described in the results, but not the methods.

Response: It is incorporated in method section too.

Comment: I2 is not the most appropriate test for heterogeneity when the outcome measure is a proportion. As such, it is unsurprising that I2 is >90%. (Tau2 would have been better).

Yes it is true that both Q test with p value and I2 are a relative measure of heterogeneity. They don’t tell us exactly the magnitude of variation of effect sizes among the studies. Therefore, high I2 in the context of proportional meta-analysis does not necessarily mean that data is inconsistent. As such, the results of this test should be interpreted conservatively. It is advised to use I2 as a criterion for a decision whether a subgroup analysis or moderato analysis is indicated.

On the other hand, τ2 or Tau2 is an estimate of the between-study variance in a random-effects meta-analysis. The square root of this number (i.e. tau) is the estimated standard deviation of underlying effects across studies. T2 is not used itself as a measure of heterogeneity but is used in two other ways: (1) it is used to compute Tau; and (2) it is used to assign weights to the studies in the meta-analysis under the random-effects model. Tau is used for computing the prediction interval. Tau is a useful first indication of the extent of this dispersion. However, the prediction interval is a more direct and more easily interpretable indicator.

Michael Borenstein et al. (2009), Introduction to Meta-Analysis, Chichester (UK): Wiley.

Therefore, in our meta-analysis study the following is incorporated.

Tau2 = 98.83, Tau = 9.94, prediction interval (13.8 – 33.68), 95% CI confidence interval, (20.69 – 26.79)

With high heterogeneity, prediction intervals will be wider than confidence intervals, and can be considered a more conservative way to incorporate uncertainty in the analysis. Where possible, it is suggested estimation of prediction intervals alongside with confidence intervals, especially for prevalence and incidence estimates and we include this concept.

Barker, Timothy Hugh, et al. "Conducting proportional meta-analysis in different types of systematic reviews: a guide for synthesis of evidence." BMC Medical Research Methodology 21.1 (2021): 1-9.

Comment: The search strategy is not highly sensitive (e.g. “Anti-Retroviral Therapy” is a very limited term) and this should be noted as a limitation. Preferably, standard search terms would have been used (e.g. see search terms used by Cochrane, or search strings used by other reviews cited by this review, e.g. ref 10).

Response: We believe that we have searched enough articles using sufficient key words. We were having difficulty finding alternative search terms for the key word "Anti-Retroviral Therapy". Even the suggested reference by the reviewer didn’t include this word. We accept that truncations were not used. Additionally, the Cochrane handbook for systematic review recommends to avoid using too many different search concepts but a wide variety of search terms. (www.training.cochrane.org/handbook). However, we don’t mean that the recommendation for maximizing the number of alternative key words is not important in our future work. Regarding duplication of terms, the second search strategy connected by “AND” was used to access potential case-control and retrospective cohort studies that might only report the associated factors (determinants) without the prevalence or incidence of under-nutrition. We believe that no study is leftover other than based on eligibility criteria in our final meta-analysis and it may not be necessary to put the search strategy as a crude limitation.

Comment: Results “Regarding the publication year, 11 articles were published in 2020 followed by 9 articles in 2017. Besides, only one article was reported in 2010” This is an anecdotal way of describing year of publication, given that 44 studies were included. Please reconsider how to present these data.

Response: This result is rephrased in a more informative way. The detail is displayed in table 2 and description is reserved only for the majority of studies and range of year of publication.

Comment: Tables need legends to explain the acronyms

Response: Legends are added in some tables to avoid confusions. For example “ART” in table 2.

Comment: Figure 3. This is a very unconventional forest plot that does not display pooled estimates and confidence intervals well.

Response: Figure 3 is a sensitivity analysis graph. It, like the funnel plot, serves as a visual guide to publication bias. The graph shows estimates are within the confidence interval limit and removal of studies to minimize publication bias is not required. The sensitivity analysis indirectly supports the risk of bias assessment, which was arbitrarily assessed using NOS.

Attachment

Submitted filename: Response to reviewers #2.docx

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PLoS One. doi: 10.1371/journal.pone.0283502.r005

Decision Letter 2

Joel Msafiri Francis

21 Dec 2022

PONE-D-21-36754R2Prevalence of under-nutrition and associated factors among adults taking antiretroviral therapy in sub-Saharan Africa: A systematic review and meta-analysisPLOS ONE

Dear Dr. Ali,

Please submit your revised manuscript by Feb 04 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Joel Msafiri Francis, MD, MS, PhD

Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #4: (No Response)

Reviewer #5: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #4: Partly

Reviewer #5: Partly

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #4: Yes

Reviewer #5: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #4: Yes

Reviewer #5: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #4: Yes

Reviewer #5: Yes

**********

6. Review Comments to the Author

Reviewer #4: Thank you for inviting me to review this systematic review on the prevalence of under-nutrition among people living with HIV in sub-Saharan Africa. While this topic is of high interest, and the authors have already improved their manuscript during the revision process, I feel the article is not yet ready for publication, and need further details, especially on the methods, results and discussion. Please see below my point-by-point review:

Title: it seems the review includes adults living with HIV, whatever their ART status, fig5 showing sub-analysis by ART status, I would therefore suggest changing the title to fit better with the review.

Abstract:

- Undernutrition has several definitions (low BMI, low weight, small mid-upper arm circumference, micronutrients deficiencies), this needs to be defined clearly in the abstract, especially as the background talks also about food insecurity which can be confusing. There are many terms used (malnutrition, wasting etc..) in the abstract and throughout the paper, which needs to be harmonized

- Methods section needs to be a bit more detailed (inclusion criteria, study period, study design and data extracted, especially related to the associated factors)

- Results section could start with the number of total records identified with the search strategy before to give the final number.

- Given the heterogeneity of the selected studies, whether in terms of study design, population, context, year etc.., I would be extremely careful while comparing the prevalence by country or years. I would rather focus on the HIV-related associated factors, which can be the more useful to target to further improve the nutritional status of people living with HIV.

Introduction: overall this part lacks a bit of structure and justification

- First paragraph should explain the HIV epidemic among adults, and challenges of HIV care, especially in sub-Saharan Africa, I don’t think the part about food insecurity should be there

- Second paragraph about the relationship between nutrition and HIV: ok

- Third paragraph, before objectives and perspectives, about the knowledge gaps on this topic and why it is important to study them: we need to estimate the burden of under-nutrition among people living with HIV in sub-Saharan Africa and understand what are the main risk factors for this population. If the focus in on adults among ART (which again is not clear in the title and abstract), this has to be better justified too

Methods:

- I don’t understand the comparison/control group here. Most studies selected don’t compare the prevalence of under-nutrition by HIV status, and the following results will not really display this. Does the comparative sample was really a criterion of the search strategy?

- Age threshold at age 16 years also need justification, why include youth for which nutritional and growth outcomes are still evolving greatly compared to adults?

- What was the period of time selected for the searching strategy? It is said until November 2021 but no information about the beginning, only in the title of the figures (2009), what is the justification for this threshold?

- I would suggest creating a table for the search strategy rather than putting it in the text, to better highlight it.

Results: Need further details for the reader to understand and have the full picture

- Table 2: Results should be much more specific and includes for each selected article: gender/sex distribution, ART duration (at least +/- 6 months on ART), the type of setting (urban, semi-urban, rural), median age or age range if available, the associated factors measured (so we know for each pooled analysis how many articles you included). I don’t think the response rate is useful here. Add the prevalence with its 95% confidence interval or interquartile range (fig 3 seems to display it but is not easy to read and I would suggest to delete it).

- Fig5: can this figure be stratified also by duration on ART? (whether +/- 6 months, 1 year or 5 years, depending on your results)

- Fig 6,7 and 8: it is not specific what was the reference group for each study. For example for WHO clinical stage, does all the studies compared stage 3-4 with stage 1-2? What was the comparison groups for CD4 count used to calculate the odds ratio? Same question for age and sex, how were the estimates calculated? If the definition and comparison were heterogeneous between studies I don’t see the point of doing a pooled analysis, this could be a narrative review only for this part, with a table explaining the detailed results.

Discussion: overall this part needs to be reinforced and better structured

- 1st paragraph: should summarised the results of the review first, not giving general messages, better suitable for the introduction of the end of the conclusion

- 2nd paragraph: I don’t understand why comparing the results with a population of pregnant women, this is a specific topic. Also, why discussing the effects of undernutrition on mortality here? This outcome was not taken into account in the review.

- In 3rd paragraph, you are discussing and comparing results by sex but this information is not well highlighted in you own article. What was the pooled prevalence by sex in your review? The comparison with results found on children are not necessary here. This will be more relevant to compare with the estimates of under-nutrition among the general population, to see if people living with HIV are more affected by this, and how much more affected.

- Ref28: why discussing of discrepancy with your study while this review measured food insecurity and not under-nutrition, which are, as you said yourself, two different markers?

- Further in the same paragraph, comparing with studies focused on overweight and obesity seems not relevant as well, unless you incorporate those results in your definition of the study outcomes and describe it.

- You briefly described the difference of prevalence per year in your results, I wonder if it would not be worth it to see and discuss if the prevalence has evolved over time, or at least comparing 2009-2015 and 2015-2021 for example. There might have been very few improvements, which is a result in itself, worthwhile to highlight.

- Other limitations need to be highlighted: heterogeneity and lack of comparative group. You should also discuss the risk of publication bias and how you mitigated it.

Reviewer #5: I have reviewed manuscript titled "Prevalence of under-nutrition and associated factors among adults taking antiretroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis"

General comments : Few areas in the manuscript require proof reading. Correct the sentence on page 4, paragraph 1, " For example, a study......times higher odds.............."

If possible remove table 1 and you can just define the PICO questions by text. For this case, P can stand for population, I intervention and C: Comparison..... Also correct the sentence under population to read 16 years instead of 16 year... Also be consistent, is it grey literature or gray literature?

Under Effect measures : Make sure you write that sentence in past tense "We included......"

Methodology : Properly explain why I2 is high

Discussion: Page 13, correct those 2 sentences " Conversely.........." " The study used....

The second paragraph towards the end, you are discussing about children. This article is on adults.

Thank you

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Reviewer #4: No

Reviewer #5: No

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PLoS One. 2023 Mar 24;18(3):e0283502. doi: 10.1371/journal.pone.0283502.r006

Author response to Decision Letter 2

30 Dec 2022

Response to reviewers #4

First, I would like to thank the reviewers for taking the time to provide us with invaluable comments that enrich the quality of the manuscript.

Comment: Title: it seems the review includes adults living with HIV, whatever their ART status, fig5 showing sub-analysis by ART status, I would therefore suggest changing the title to fit better with the review.

Response: Yes, the manuscript includes adults living with HIV irrespective of their ART status, and the pooled prevalence is reported in the document. However, subgroup analysis by different relevant characteristics is common in order to better understand the results by different categories. The sub-group analysis was made to look into whether taking ART has made a difference in nutritional status. There is evidence that taking ART improves nutritional status. Sub-group analysis is made for description, not inference. We believe sub-group analysis by different variables will not demand changing the title.

Abstract:

Comment- Undernutrition has several definitions (low BMI, low weight, small mid-upper arm circumference, micronutrients deficiencies), this needs to be defined clearly in the abstract, especially as the background talks also about food insecurity which can be confusing. There are many terms used (malnutrition, wasting etc..) in the abstract and throughout the paper, which needs to be harmonized

Response: Though malnutrition also includes overnutrition, in this study and commonly, malnutrition, undernutrition, underweight, wasting, and malnourishment are all used in the same context. All of the studies included in this meta-analysis defined malnutrition as low BMI (less than or equal to 18.5 kg/m2), as indicated in the main text. Food security was mentioned as one of the causes of malnutrition in SSA. However, as it is not the scope of this study, we removed it from the statement. We put the operational definition in the first statement in brackets.

Comment: Methods section needs to be a bit more detailed (inclusion criteria, study period, study design and data extracted, especially related to the associated factors)

Response: Accepted and we add some details in methods part.

Comment: Results section could start with the number of total records identified with the search strategy before to give the final number.

Response: Different articles present the results in different ways in their abstracts. Overall, we used the PRISMA 2020 Abstracts Checklist to structure our abstract. Because the details are described in text and using a flow chart in the main result section, we prefer not to present the number of total records here.

Comment: Given the heterogeneity of the selected studies, whether in terms of study design, population, context, year etc.., I would be extremely careful while comparing the prevalence by country or years. I would rather focus on the HIV-related associated factors, which can be the more useful to target to further improve the nutritional status of people living with HIV.

Response: Thank you for the concern. Sub-group analysis is used in meta-analysis to describe phenomena by different segments rather than for inference. It is also used to identify the source of heterogeneity. Inference is made based on the major objective of the study, i.e., the pooled estimate of prevalence and associated factors. Therefore, we removed the sub-group result from the abstract as it was not our major finding. Additionally, we avoid comparison statements like "the highest" for the sub-group results presented in the main text.

Introduction: overall this part lacks a bit of structure and justification

Comment: First paragraph should explain the HIV epidemic among adults, and challenges of HIV care, especially in sub-Saharan Africa, I don’t think the part about food insecurity should be there.

Response: We really appreciate the comment on the structural organization of the contents presented in the introduction. A number of literatures on food insecurity were added as per previous reviewers’ comments on why the "sub-Saharan Africa region" was selected as the study area. It was to show the high burden of food insecurity and HIV transmission in SSA, which puts these patients at high risk for malnutrition. However, we abridged the statements on food insecurity and brought them to the third paragraph, where the evidence gaps are presented. Similarly, we added some statements describing the epidemiology of HIV among adults and the challenges of HIV care in SSA as background statements in the first paragraph.

Comment: Third paragraph, before objectives and perspectives, about the knowledge gaps on this topic and why it is important to study them: we need to estimate the burden of under-nutrition among people living with HIV in sub-Saharan Africa and understand what are the main risk factors for this population. If the focus in on adults among ART (which again is not clear in the title and abstract), this has to be better justified too.

Response: In the third paragraph, we presented a summary of previous key findings related to the topic and showed the evidence gap and how our study contributed to filling it. The reason for categorizing based on ART status is that there is evidence that indicates taking ART improves nutritional status, and sub-group analysis by ART status will enable us to appreciate the proportion separately.

Methods:

Comment- I don’t understand the comparison/control group here. Most studies selected don’t compare the prevalence of under-nutrition by HIV status, and the following results will not really display this. Does the comparative sample was really a criterion of the search strategy?

Response: In cross-sectional studies, the comparator group is identified by context or assumption. The results are interpreted under this assumption. However, in case-control and cohort studies, the control groups are those who are HIV-negative adults. The comparative sample was not a criterion of the search strategy but a context for interpretation.

Comment: Age threshold at age 16 years also need justification, why include youth for which nutritional and growth outcomes are still evolving greatly compared to adults?

Response: The lowest age categories for adults in the included studies were 15 years, 16 years, 18 years, and 20 years. Adults are defined as people over the age of "15 years" by the UNAIDS definition. It is corrected in the PICO. https://www.unaids.org/en/resources/fact-sheet

Comment: What was the period of time selected for the searching strategy? It is said until November 2021 but no information about the beginning, only in the title of the figures (2009), what is the justification for this threshold?

Response: Accepted. We include the commencement period. The reason was that there was a previous meta-analysis study on the prevalence of undernutrition among women living with HIV published in 2008. To avoid redundancy and add evidence to existing knowledge, we took published studies starting in 2009 and included both adult males and females. https://bmcpublichealth.biomedcentral.com/articles/10.1186/1471-2458-8-226

Comment- I would suggest creating a table for the search strategy rather than putting it in the text, to better highlight it.

Response: It is possible to present search strategy in table.

Results: Need further details for the reader to understand and have the full picture

Comment- Table 2: Results should be much more specific and includes for each selected article: gender/sex distribution, ART duration (at least +/- 6 months on ART), the type of setting (urban, semi-urban, rural), median age or age range if available, the associated factors measured (so we know for each pooled analysis how many articles you included). I don’t think the response rate is useful here. Add the prevalence with its 95% confidence interval or interquartile range (fig 3 seems to display it but is not easy to read and I would suggest to delete it).

Response: We include some of the suggested variables, like 95% CI and mean/median age, but inserting all variables will overwhelm the table and make it unattractive. Studies on ART duration were conducted in both categories, i.e., no study was conducted on either the -6 or +6 month separately. Most importantly, the data on the associated factors, including ART duration, are extracted on a separate Excel sheet. I will attach it as a supplementary file for further clarity. The response rate is added to show the credibility of the reported estimate. The forest plot for each associated factor would tell us the number of studies included there. For better understanding, we created a table that summarizes the points related to the associated factors (Table 4).

Figure 3 is a sensitivity analysis graph. It, like the funnel plot, serves as a visual guide to publication bias. The graph shows the effect estimates (indicated by small circles) are within the confidence interval limit, and no outlier is detected. Thus, the removal of studies to minimize publication bias is not required. The sensitivity analysis indirectly supports the risk of bias assessment, which was arbitrarily assessed using NOS. We believe adding this graph will enhance the quality of this manuscript.

Comment: Fig5: can this figure be stratified also by duration on ART? (whether +/- 6 months, 1 year or 5 years, depending on your results)

Response: No, it is not possible. In order to stratify by the duration of ART, individual studies should study patients with a specific category of treatment duration. Studies were not conducted with a certain limit on treatment duration. Most importantly, the pooled estimate of the adjusted odds ratio between "duration of ART" and "undernutrition" is presented in the "results" section and was 2.68.

Comment: Fig 6,7 and 8: it is not specific what was the reference group for each study. For example, for WHO clinical stage, does all the studies compared stage 3-4 with stage 1-2? What was the comparison groups for CD4 count used to calculate the odds ratio? Same question for age and sex, how were the estimates calculated? If the definition and comparison were heterogeneous between studies, I don’t see the point of doing a pooled analysis, this could be a narrative review only for this part, with a table explaining the detailed results.

Response: We appreciate this outlook. We did not combine heterogenous comparison groups. We include the reference group that the majority of the studies used. We exclude articles that report on a completely different reference group. This is the major problem that researchers face during meta-analysis of determinants (associated factors) with outcome variables. We used the reported adjusted odds ratio to determine the strength of the association. We prefer to present a short summary of the associated factors and comparison group using a table format. (Table 4).

Discussion: overall this part needs to be reinforced and better structured

Comment: 1st paragraph: should summarized the results of the review first, not giving general messages, better suitable for the introduction of the end of the conclusion.

Response: We generally agree with the comment. We also understand that the first paragraph in the discussion summarizes major concepts outlined in the introduction and provides a logical linkage of the results with the original question or objectives. We make amendments based on the above.

Comment: 2nd paragraph: I don’t understand why comparing the results with a population of pregnant women, this is a specific topic. Also, why discussing the effects of undernutrition on mortality here? This outcome was not taken into account in the review.

Response: The comment is fully accepted. This was added due to the scarcity of similar meta-analysis studies for comparison with our findings. However, rather than compare with a different population and outcome variable, we decided to remove the comparators and mention the shortage of evidence under the limitation of study section.

Comment: In 3rd paragraph, you are discussing and comparing results by sex but this information is not well highlighted in you own article. What was the pooled prevalence by sex in your review? The comparison with results found on children are not necessary here. This will be more relevant to compare with the estimates of under-nutrition among the general population, to see if people living with HIV are more affected by this, and how much more affected.

Response: We presented the sex, age, ART duration, WHO clinical stage, and CD4 count in the result section under the sub-heading “Factors associated with under-nutrition”. Describing the prevalence by subgroup is different from determining the strengths of association between the factors and outcome variable. The pooled adjusted odds ratio is separately estimated for each above-mentioned factor. For clarity we will attach the data extraction excel sheet for all factors as a supplementary file.

Comment: Ref28: why discussing of discrepancy with your study while this review measured food insecurity and not under-nutrition, which are, as you said yourself, two different markers?

Response: Again, we also removed this section. It was inserted as food insecurity is closely related and leads to under-nutrition in majority of the studies. Similarly, this was used due to shortage of meta-analysis studies exactly carried out on under-nutrition.

Comment: Further in the same paragraph, comparing with studies focused on overweight and obesity seems not relevant as well, unless you incorporate those results in your definition of the study outcomes and describe it.

Response: Again, this comment is accepted. It was used for the above similar reason.

Comment: You briefly described the difference of prevalence per year in your results, I wonder if it would not be worth it to see and discuss if the prevalence has evolved over time, or at least comparing 2009-2015 and 2015-2021 for example. There might have been very few improvements, which is a result in itself, worthwhile to highlight.

Response: We appreciate you suggesting this perspective for interpretation, and we will include it in the result and discussion.

Comment: Other limitations need to be highlighted: heterogeneity and lack of comparative group. You should also discuss the risk of publication bias and how you mitigated it.

Response: High heterogeneity is expected in the meta-analysis of proportions reported from different countries. The source of heterogeneity was explored by sub-group analysis but not identified. The inter-country difference in population characteristics is obvious. It is also mentioned in the document under the sub-heading of quality appraisal results as "this result should be interpreted cautiously." We will include it in the limitation section. Regarding the publication bias, studies look symmetrically distributed in the funnel plot (Figure 2) but not by the Eggers statistical test. The sensitivity analysis graph (Figure 3) did not show outlier studies to be removed from the analysis. Trim and fill analysis is also another method, but it is not recommended as it provides artificial estimates. Additionally, the small study size effect is not the problem of this study, as 44 articles have been included in the analysis. Therefore, it is acceptable to run the analysis based on available studies, and publication bias will not be the limitation of this study.

Response to reviewer #5

General comments: Few areas in the manuscript require proof reading. Correct the sentence on page 4, paragraph 1, " For example, a study......times higher odds.............."

Response: Okay, accepted.

Comment: If possible, remove table 1 and you can just define the PICO questions by text. For this case, P can stand for population, I intervention and C: Comparison..... Also correct the sentence under population to read 16 years instead of 16 year... Also be consistent, is it grey literature or gray literature?

Response: Accepted. PICO questions can be formatted by texts using bullets. Though the words “grey” and “gray” can be used interchangeably we will use one of the terms throughout the paper.

Comment: Under Effect measures: Make sure you write that sentence in past tense "We included......"

Response: Accepted.

Comment: Methodology: Properly explain why I2 is high.

Response: Still, the source is not identified, but high heterogeneity is expected when combining proportions reported from different countries. The only thing we can do is add the statement "The result should be interpreted cautiously" and mention high heterogeneity under the limitation of the study section.

Comment: Discussion: Page 13, correct those 2 sentences " Conversely.........." " The study used....

Response: Okay, Accepted.

Comment: The second paragraph towards the end, you are discussing about children. This article is on adults.

Response: The paragraph on children was added due to scarcity of available similar studies on adults. However, we delete it as it is beyond the scope of our study defined in the PICO.

Attachment

Submitted filename: Response to reviewers V_3.docx

Click here for additional data file.^{(23.2KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0283502.r007

Decision Letter 3

Joel Msafiri Francis

12 Mar 2023

Prevalence of under-nutrition and associated factors among adults taking antiretroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis

PONE-D-21-36754R3

Dear Dr. Ali,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Additional Editor Comments (optional):

Please format the figures - and would be helpful to drop Figure 3. It is not informative. It would would be helpful to proof read the English grammar prior to publication.

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #5: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #5: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #5: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #5: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #5: Yes

**********

6. Review Comments to the Author

Reviewer #5: Thank you for responding to reviewers comments. Please verify that UNAIDS identify adults as those aged above 15.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #5: No

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PLoS One. doi: 10.1371/journal.pone.0283502.r008

Acceptance letter

Joel Msafiri Francis

16 Mar 2023

PONE-D-21-36754R3

Prevalence of undernutrition and associated factors among adults taking antiretroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis

Dear Dr. Seid:

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Thank you for submitting your work to PLOS ONE and supporting open access.

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on behalf of

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Table. Data extraction sheet used in the meta-analysis of the prevalence and associated factors of undernutrition among adults taking antiretroviral therapy in sub-Saharan Africa, 2009–2021.

(XLSX)

Click here for additional data file.^{(34.4KB, xlsx)}

S2 Table. PRISMA statement presentation of systematic review and meta-analysis of undernutrition among adults taking ART in SSA, 2009–2021.

(DOCX)

Click here for additional data file.^{(32.6KB, docx)}

S3 Table. Trim and fill analysis of prevalence of undernutrition and associated factors among adult PLWHIV in SSA, 2009–2021.

(DOCX)

Click here for additional data file.^{(32.9KB, docx)}

Attachment

Submitted filename: SUmmary of comments.docx

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Attachment

Submitted filename: Nutrition.docx

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Attachment

Submitted filename: Response to reviewers.docx

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Attachment

Submitted filename: Comments.docx

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Attachment

Submitted filename: Response to reviewers #2.docx

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Attachment

Submitted filename: Response to reviewers V_3.docx

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Data Availability Statement

All relevant data are within the paper and its Supporting Information files.

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PERMALINK

Prevalence of undernutrition and associated factors among adults taking antiretroviral therapy in sub-Saharan Africa: A systematic review and meta-analysis

Awole Seid

Omer Seid

Yinager Workineh

Getenet Dessie

Zebenay Workneh Bitew

Roles

Abstract

Background

Methods

Results

Conclusion

Introduction

Methods

Inclusion and exclusion criteria

Information source and search strategy

Table 1. The search strategy used in the PubMed database, 2021.

Data collection process and data items

Effect measures

Risk of bias assessment

Synthesis methods

Results

Study selection and characteristics

Fig 1. Flow chart showing the sequence of study selection on undernutrition among adult PLWHIV in sub-Saharan Africa, 2009–2021.

Table 2. Study characteristics included in meta-analysis of undernutrition among adult PLWHIV in sub-Saharan Africa, 2009–2021.

Table 3. Sub-group analysis of the prevalence of undernutrition among adults living with HIV in sub-Saharan Africa by country, study design, and publication year, 2009–2021.

Quality appraisal results

Fig 2. Funnel plot of studies on undernutrition among adult PLWHIV in SSA, 2009–2021.

Meta-analysis results

Prevalence of undernutrition among adult PLWHIV in sub-Saharan Africa

Fig 3. Forest plot of pooled prevalence of undernutrition among adult PLWHIV in sub-Saharan Africa 2021.

Factors associated with undernutrition among adults of PLWHIV in sub-Saharan Africa

Table 4. Summary of the factors associated with undernutrition among adults living with HIV in sub-Saharan Africa, 2021.

Fig 4. The pooled effect of “WHO clinical stage” on undernutrition among adult PLWHIV in sub-Saharan Africa, 2021.

Fig 5. Pooled effect of “CD4 count” on undernutrition among adult PLWHIV in sub-Saharan Africa, 2021.

Fig 6. Pooled effect of “age” of study participants on undernutrition among adult PLWHIV in sub-Saharan Africa, 2021.

Fig 7. Pooled effect of “sex” on undernutrition among adult PLWHIV in sub-Saharan Africa, 202.

Fig 8. Pooled effect of “ART duration” on undernutrition among adult PLWHIV in sub-Saharan Africa, 2021.

Discussion

Limitation of the study

Conclusion

Supporting information

Data Availability

Funding Statement

References

Decision Letter 0

Joel Msafiri Francis

Roles

Author response to Decision Letter 0

Decision Letter 1

Joel Msafiri Francis

Roles

Author response to Decision Letter 1

Decision Letter 2

Joel Msafiri Francis

Roles

Author response to Decision Letter 2

Decision Letter 3

Joel Msafiri Francis

Roles

Acceptance letter

Joel Msafiri Francis

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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