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Prevalence of undernutrition among adult tuberculosis patients in Ethiopia: A

systematic review and meta-analysis

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DOI: 10.1016/j.jctube.2020.100211

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 Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 22 (2021) 100211

Contents lists available at ScienceDirect

Journal of Clinical Tuberculosis and Other

Mycobacterial Diseases
journal homepage: www.elsevier.com/locate/jctube

Prevalence of undernutrition among adult tuberculosis patients in Ethiopia:

A systematic review and meta-analysis
Adam Wondmieneh a, *, Getnet Gedefaw b, Addisu Getie a, Asmamaw Demis a
a
Department of Nursing, College of Health Sciences, Woldia University, P.O.Box: 400, Woldia, Ethiopia
b
Department of Midwifery, College of Health Sciences, Woldia University, P.O.Box: 400, Woldia, Ethiopia

A R T I C L E I N F O A B S T R A C T

Keywords: Background: Undernutrition and tuberculosis are the major public health problems of people living in middle and
Tuberculosis low-income countries. Even though single studies have been reported from different areas of Ethiopia, there is no
Undernutrition national-level study that estimates the overall burden of undernutrition among tuberculosis patients. Therefore,
Ethiopia
this study aimed to estimate the overall magnitude of undernutrition among adult tuberculosis patients in
Systematic review
Meta-analysis
Ethiopia.
Methods: We searched out records from databases such as PubMed/MEDLINE, HINARI, EMBASE, Scopus, Google
Scholar, and African journals and the online Ethiopian University repositories for published and unpublished
articles. The data were extracted using a standardized data extraction format. Meta-analysis was computed using
STATA version 11 software. The Cochrane Q-test and I2 with its corresponding p-value were used to assess the
heterogeneity of the study. The presence of publication bias was evaluated using Egger’s test and presented with
funnel plots. The random-effects meta-analysis model was computed to estimate the pooled prevalence of un­
dernutrition among adult tuberculosis patients.
Results: A total of Twelve observational studies with 4963 study participants were included in this systematic
review and meta-analysis. The pooled prevalence of undernutrition among tuberculosis patients in Ethiopia was
50.8% (95% CI 43.97, 57.63). The results of subgroup analysis showed that the highest prevalence of under­
nutrition among TB patients was observed from studies done in the Amhara region (65.63%). In this meta-
analysis, the pooled prevalence of undernutrition among TB-HIV co-infected patients was 45.45% (95%CI 21.85,
56.07).
Conclusion: The prevalence of undernutrition among TB patients in Ethiopia was noticeably high. The result of
this study showed that undernutrition is more severe in the Amhara regional state. Additionally, TB-HIV co-
infected patients are highly affected by undernutrition. Therefore, the Ministry of Health in collaboration with
clinicians should give special attention to provide nutritional care and support for TB patients as part of regular
care. Moreover, special nutritional support should be designed for TB-HIV co-infected patients.

1. Introduction estimated to be 24% of the 10 million global TB cases [1]. In Ethiopia,

TB is the leading cause of death from infectious diseases, and there were
Tuberculosis (TB) is a communicable disease caused by Mycobacte­ 30 thousand deaths due to TB every year [2].
rium tuberculosis and is the leading cause of death from a single infectious Undernutrition is a major public health problem for people living in
agent. The bacteria mainly affect the lungs but can also disseminate to underdeveloped regions of the world. According to the Food and Agri­
other sites of the body. According to the WHO 2019 Global tuberculosis culture Organization (FAO) 2016 estimate, 815 million people are un­
report, there were 10 million infections and 1.2 million deaths among dernourished with majorly living in developing countries, particularly
HIV-negative people. HIV infection increases the risk of TB and in 2018 Sub-Saharan Africa accounts for 22.7% [3]. In Ethiopia, 33% of adult
there were 251 thousand TB deaths among HIV-infected people [1]. The men aged 15–49 and 22% of adult women aged 14–49 exhibited un­
burden of TB infection is higher in Sub-Saharan Africa, which is dernourishment (Body Mass Index (BMI) < 18.5 kg/m2) [4]. TB-infected

Abbreviations: AOR, Adjusted Odds Ratio; BMI, Body Mass Index; CI, Confidence Interval; TB, Tuberculosis; WHO, World Health Organizations.
* Corresponding author.
E-mail address: [email protected] (A. Wondmieneh).

https://doi.org/10.1016/j.jctube.2020.100211

Available online 29 December 2020

2405-5794/© 2020 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
A. Wondmieneh et al. Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 22 (2021) 100211

individuals are more vulnerable to undernutrition compared to the Table 1

general population. Globally, one-quarter of TB infection is due to Searches in MEDLINE/PubMed, Google Scholar, and other databases for the
malnutrition [5]. Undernutrition and TB have a bidirectional relation­ prevalence of undernutrition among adult tuberculosis patients in Ethiopia.
ship. A person having active TB develops undernutrition and in turn, Databases Searching terms Number of
undernutrition increases the person’s susceptibility to developing TB studies
[5,6]. A comparative cross-sectional study conducted in the Amhara MEDLINE/PubMed “Prevalence” OR “magnitude” OR 280
region, Ethiopia, indicated that 33.8% of excess undernutrition was “proportion” OR “burden” AND
observed in TB patients compared with TB-free populations [7]. Un­ “undernutrition” OR “malnutrition”
OR “malnourishment” OR
dernutrition weakens the individual immune system, which increases
“underweight” AND “tuberculosis”
the risk of primary TB infection or activation of latent TB. Moreover, AND“adults” AND “Ethiopia”.
undernutrition increases the risk of mortality, poor treatment outcome,
Google Scholar “Undernutrition” OR “malnutrition” 248
and TB relapse [3,5,8].
OR “malnourishment” AND
The findings of previous studies showed that the morbidity and “Tuberculosis” AND “Adults”.
mortality of TB are mainly associated with undernutrition, low socio- HINARI, EMBASE, Scopus, 24
economic status, and poor immune function [9–11]. A retrospective African journals and online
Ethiopian University
cohort study conducted in Taipei, Taiwan, indicated that underweight
repository
(BMI < 18.5 kg/m2) was a significant predictor of all causes of TB Total retrieved articles 552
mortality [12]. Therefore, improving the nutritional status of TB pa­ Number of included studies 12
tients is a critical step towards the reduction of mortality due to TB [9].
Moreover, nutritional supplements that contain both macro-and
micronutrients could help people to resist TB infection, decrease the imported into the “EndNote reference software version 8 (Thomson
relapse of TB, and to increase TB treatment outcome through strength­ Reuters, Stamford, CT, USA) citation manager”. Then, duplicates were
ening their immune system [13,14]. In Ethiopia, different observational sorted and removed using EndNote software. Two investigators (AW and
studies were conducted to show the magnitude of undernutrition among AD) independently evaluated the individual study title and abstracts
TB patients. The results of these studies revealed that the prevalence of using predetermined inclusion criteria. Two investigators (AW and AD)
undernutrition among TB patients was ranged from 28.5% to 71.35% also have independently selected the full texts and assessed the eligi­
[15,16]. bility of the study for final analysis. The first author, year of publication,
In Ethiopia, no national-level studies are showing the burden of study area, study design, sample size, region in which the study was
undernutrition among TB patients. Estimating the overall pooled conducted, and prevalence of undernutrition were extracted. The dis­
magnitude of undernutrition among TB patients is very crucial to crepancies between the authors during the process were resolved
improve the quality of care through developing appropriate plans, pol­ through discussion with the other authors to agree. The data were
icies, and implementation programs. Therefore, this study aimed to es­ exported in Excel spreadsheets for further analysis.
timate the overall pooled prevalence of undernutrition among adult TB
patients in Ethiopia. 2.4. Inclusion and exclusion criteria

2. Methods and materials 2.4.1. Inclusion criteria

Studies only conducted in Ethiopia and meeting the following in­
2.1. The study protocol and registration clusion criteria were included in this systematic review and meta-
analysis.
For reporting the findings, we used the Preferred Reporting Items for
Systematic Review and Meta-analysis (PRISMA) guideline which is 2.4.1.1. Study design. All published and unpublished observational
provided as a Supplementary File (Table S1) [17]. The study protocol of studies (case-control, cohort, and cross-sectional) conducted among
this systematic review and meta-analysis has been submitted to the In­ adult tuberculosis patients in Ethiopia were included in the study.
ternational Prospective Register of Systematic Reviews (PROSPERO)
and assigned the submission number (ID 202843). 2.4.1.2. Language. Only studies reported in the English language were
included.
2.2. Databases and search strategy
2.4.1.3. Study period. Articles published from January 1, 2000, to July
We searched out records on PubMed/MEDLINE, HINARI, EMBASE, 30, 2020, were included in this study.
Scopus, Google Scholar, and African journals and the online Ethiopian
University repositories for published and unpublished articles. The 2.4.1.4. Study participants. Adult tuberculosis patients were included.
search was conducted from May 1st to July 30, 2020, and research ar­
ticles published until July 30, 2020, were included in the final meta- 2.4.1.5. Measurement of outcome. Studies reported the prevalence of
analysis (Table 1). Articles reporting undernutrition among adult undernutrition among tuberculosis patients and/or predictors were
tuberculosis patients and/or factors associated with undernutrition considered in this study and reported quality control methods.
among tuberculosis patients in Ethiopia were included in the analysis.
Searching was employed using the following keywords; “prevalence”, 2.4.2. Exclusion criteria
“magnitude”, “proportion”, “burden”, “undernutrition”, “malnutrition”, Articles reported in non-English language, case reports, trials, sys­
“malnourishment”, “underweight”, “tuberculosis”, “adults”, “Ethiopia”. tematic review, narrative review, policy and program evaluation,
The search strings were developed using “OR” and “AND” Boolean op­ statements, updates, and news were excluded from the study. Further­
erators. Moreover, the reference lists of all included studies were further more, qualitative studies and studies without full text were also
screened to identify more additional articles. excluded from the final analysis.

2.3. Screening and eligibility of the study

In the beginning, all articles retrieved from those databases were

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A. Wondmieneh et al. Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 22 (2021) 100211

2.5. Outcome measurement heterogeneity of the study. The values of I2, 25%, 50%, and 75%
represent low, moderate, and high heterogeneity, respectively [20]. We
In this systematic review and meta-analysis, the prevalence of un­ examined the source of heterogeneity through subgroup analysis based
dernutrition (BMI < 18.5 kg/m2) among adult tuberculosis patients was on (sample size, region, and publication year) and sensitivity analysis
determined by dividing the number of patients having undernutrition by was executed to investigate the potential source of heterogeneity
the total number of study subjects included in the final analysis. observed in the pooled prevalence of undernutrition among adult
tuberculosis patients. The presence of publication bias was evaluated by
using Egger’s test [21] and presented with funnel plots. A statistical test
2.6. Quality assessment
with a P value<0.05 was considered statistically significant.
Two independent authors (AW and AD) assessed the quality of the
studies using the critical quality assessment checklist recommended by 3. Results
the “Joanna Briggs Institute (JBI)” [18]. The disagreement between the
authors was resolved through discussion. The parameters of the quality A total of 552 articles were collected from the electronic databases
assessment criteria were clear inclusion criteria, details of the study using previously mentioned databases such as PubMed/MEDLINE,
population, and appropriate statistical analysis. At last, study articles Google Scholar, Scopus, EMBASE, CINHAL, HINARI, and Google. After
with a score of five and above were considered as having the good duplicates were removed, 258 articles remained. Then 204 articles were
quality to be included in the study. All authors independently assessed excluded through a reading of their titles and abstracts. Therefore, 54
the articles for consideration and inclusion in the study (Table S2). full-text articles were assessed for eligibility criteria, which results in the
further exclusion of 42 irrelevant articles. Finally, 12 studies were ful­
filled the inclusion criteria and included in this systematic review and
2.7. Data processing and analysis meta-analysis (Fig. 1).

The relevant information/data were extracted and further cleaned

using the standard format in Microsoft Excel sheets and the data were 3.1. Characteristics of included studies
exported into STATA version 11.0 (Stata Corporation, College Station,
Texas) software for further quantitative analysis. To estimate the pooled In the current meta-analysis, 12 studies with 4963 study participants
national prevalence of undernutrition among adult tuberculosis pa­ were included. All included studies were conducted among adult TB
tients, by considering the variation in true effect sizes across the popu­ patients in Ethiopia. The mean age of the study participants was 32.73
lation, a weighted inverse variance random-effects model was years old. More than half of the study participants were male (53.2%).
performed for analysis at 95%Cl [19]. The Cochrane Q-test and I2 sta­ More than three-fourths of the study participants have pulmonary
tistics with its corresponding p-value were used to assess the tuberculosis (71.38%), and the remaining one-third have

Fig. 1. Flow chart of study selection for systematic review and meta-analysis for the prevalence of undernutrition among adult tuberculosis patients in Ethiopia.

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A. Wondmieneh et al. Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 22 (2021) 100211

extrapulmonary tuberculosis (28.62%). From the included study par­ showed that the highest prevalence of undernutrition among TB patients
ticipants, 22.12% have TB-HIV co-infection. was observed from studies done in the Amhara region (65.63%),
Regarding study design, six were cross-sectional studies, four were whereas the lowest prevalence of undernutrition was observed from
case-control studies and two were cohort studies. Among them, eleven studies conducted in Addis Ababa (41.47%) (Fig. 4). Regarding one
articles were published in peer-reviewed journals between 2006 and publication year, the highest proportion of undernutrition was observed
2020, and one unpublished master’s thesis, which was conducted in in studies published before 2017 (52.24%) as compared to studies
2016. The sample size of the included studies ranged from 155 [22] to published after 2017 (48.8%). Finally, subgroup analysis was computed
1681 [7]. The included studies were reported from four regions and two based on sample size and the results showed that the highest prevalence
city administrations of the country. Four studies were conducted in of undernutrition was detected in studies with a sample size <300
Oromia regional state [15,23–25], three studies from Amhara regional (50.11%).
state [7,16,22], one study from Tigray regional state [26], one study
from South Nations Nationalities and Peoples regional state [27], two 3.5. Sensitivity analysis
studies from Addis Ababa city administration [8,28] and one study from
Dire Dawa city administration [29]. Five regions of the country, namely, We conducted a sensitivity analysis using a random-effects model.
Somali, Afar, Gambela, Harari, and Benishangul Gumuz, were not Hence, the results showed that no single study influenced the overall
included in this study due to the unavailability of studies (Table 2). pooled proportion of undernutrition among TB patients (Table 3).

3.2. The pooled prevalence of undernutrition among TB patients in 4. Discussion

Ethiopia
Undernutrition and tuberculosis are major public health problems
The results of this systematic review and meta-analysis showed that among people living in middle and low-income countries. As far as our
the overall estimated pooled prevalence of undernutrition among adult knowledge, this systematic review and meta-analysis is the first of its
TB patients in Ethiopia was 50.8% (95% CI 43.97, 57.63) (Fig. 2). The kind to estimate the pooled prevalence of undernutrition among tuber­
highest prevalence of undernutrition among TB patients (71.35%) was culosis patients in Ethiopia. Estimating the overall pooled prevalence of
reported from a study conducted in Gondar town, Amhara region, in undernutrition among TB patients is very crucial to improve the nutri­
2014 [16]. While the lowest prevalence (28.5%) was observed from a tional status of patients, which in turn increase TB treatment outcome
study done in Shashemene, Oromia region in 2016 [15]. In this meta- and decrease the morbidity and mortality of TB patients. The findings of
analysis, the pooled prevalence of undernutrition among TB-HIV co- this meta-analysis showed that more than half of TB patients in Ethiopia
infected patients was 45.45% (95%CI 21.85, 56.07). were undernourished 50.8 (95% CI 43.97, 57.63). Even though there
was no comparable meta-analysis study similar to this meta-analysis, the
3.3. Heterogeneity and publication bias result of this study is in line with studies conducted in Kenya (50.15%)
[30], Malawi (57%) [31], Ghana (51%) [32], Nepal (50%) [33], and
There was evidence of high heterogeneity among the included India 55.4% among women and 54.5% among men [34]. This similarity
studies according to Cochrane Q-test (P ≤ 0.001) and I2 test (I2 = might be due to the proportional socio-economic status of the countries.
99.7%). Therefore, we used a random-effects meta-analysis model to Additionally, those countries except Ghana and Malawi are listed in
estimate the overall pooled prevalence of undernutrition among TB WHO TB high burden countries [1].
patients. Publication bias was assessed using the funnel plot and Egger’s The finding of this review is higher than a study conducted in
regression test statistics. The funnel plot showed that there was an Bangladesh (36%) [35] and the United States of America (11.2%) [36].
asymmetrical distribution of the included studies through visual in­ The possible justification for this variation might be due to differences in
spection, which indicates there was potential publication bias (Fig. 3). the socioeconomic status of the countries. Ethiopia is grouped under a
However, The Egger regression test (p = 0.226) and Begg rank corre­ low-income country, whereas the USA is a high-income country and
lation statistics (p = 0.9) showed there was no evidence of potential Bangladesh is grouped under a middle-income country. Additionally,
publication bias. this difference might be due to variations in the residence of the study
participants. In Ethiopia, 78% of women and 80% of men live in rural
3.4. Subgroup analysis areas, and most of the rural population’s food intake habit was two times
per day [4].
There was evidence of high heterogeneity across the included The current study is lower than studies conducted in Brazil (70.6%)
studies. Therefore, subgroup analysis was employed to identify the [37] and West Bengal, India (61.9%) [38]. The possible explanation for
possible source of heterogeneity based on publication year, the region of the above variation might be due to variation in the number of study
the study conducted, and sample size. The results of subgroup analysis participants. Our study analyses the prevalence of undernutrition among

Table 2
Characteristics of included studies to assess the prevalence of undernutrition among adult TB patients in Ethiopia.
S. No Author Publication year Region Study Area Study design Sample size Prevalence %

1 Dargie et al [28] 2016 Addis Ababa Addis Ababa Cross-sectional 360 39.7
2 Feleke et al [7] 2019 Amhara Amhara region Cross-sectional 1681 57.17
3 Hussien et al [23] 2019 Oromia Bale zone Cross-sectional 372 63.2
4 G/meskel et al [27] 2018 SNNPR Hossana Cross-sectional 247 38.9
5 Guadie et al [24] 2016 Oromia Adama Cross-sectional 285 52.6
6 Tesfaye et al [15] 2016 Oromia Shashemene Cross-sectional 368 28.5
7 Seid et al [8] 2020 Addis Ababa Addis Ababa Cohort 284 46.8
8 Hassen et al [29] 2019 Dire Dawa Dire Dawa Case-control 285 37.9
9 Fisseha et al [26] 2014 Tigray Tigray region Case-control 230 56.08
10 Ephrem et al [25] 2015 Oromia Ambo Case-control 312 49.04
11 Kassu et al [22] 2006 Amhara Gondar Case-control 155 68.38
12 Wassie et al [16] 2014 Amhara Gondar Cohort 384 71.35

SNNPR = Southern Nation Nationalities and Peoples Region.

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A. Wondmieneh et al. Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 22 (2021) 100211

Fig. 2. The pooled prevalence of undernutrition among adult tuberculosis patients in Ethiopia.

Fig. 3. The funnel plots showing the presence of publication bias in the included studies undernutrition was detected from studies with a sample size<300 (50.11%).

TB patients at the national level with a large sample size, whereas the estimated 219,186 new TB Cases and 48,910 TB deaths in 2016 [39]. In
above-mentioned studies assess the prevalence of undernutrition among 2017, the Ethiopian ministry of Health updated the guideline for the
TB patients at a specific place of the country with small sample size. management of TB, drug resistance, TB, and Leprosy. This guideline
Additionally, the Brazil study was conducted among TB-HIV co-infected incorporated the management strategies of malnutrition in TB patients
participants and undernutrition is more severe in TB-HIV co-infected [40]. According to the guideline, TB patients who develop severe
patients [6]. malnutrition (BMI < 16 kg/m2) should be treated with Ready -to-Use
Ethiopia is one of the TB high burden countries with an annually Supplementary Foods (RUSF) for 03 months. Additionally, moderate

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A. Wondmieneh et al. Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 22 (2021) 100211

Fig. 4. Subgroup analysis showing the pooled prevalence of undernutrition among adult TB patients from different regions of Ethiopia.

infected patients was 45.45% (95% CI 21.85, 56.07). The result of this
Table 3
finding is higher than a study conducted in Brazil (27.3%) [37]. The
Sensitivity analysis of the prevalence of undernutrition among adult TB patients
possible justification for this result might be because TB-HIV co-infec­
in Ethiopia.
tion exacerbates undernutrition through increased body metabolic rate,
Study omitted Prevalence 95% CI
decrease absorption of nutrients, and increased protein and fat break­
Dargie et al. (2016) 51.81 44.72, 58.89 downs. Additionally, TB-HIV coinfection decreases the person’s appe­
Feleke et al. (2019) 50.22 41.2, 59.24 tite, which decreases nutritional intake and increases susceptibility to
Hussen et al. (2019) 49.67 42.21, 57.13
infection [43,44]. On the other hand, the result of this study is lower
G/meskel et al. (2018) 51.88 44.78, 58.97
Guadie et al. ((2016) 50.63 43.26, 58.01 than a study done in Tanzania (58%) [45]. This variation might be due
Tesfaye et al. (2016) 52.83 47.12, 58.34 to variation in the number of study participants. The above study was
Seid et al. (2020) 51.16 43.86, 58.46 conducted using 43 pregnant participants, but in this study, we used a
Hassen et al. (2019) 51.97 44.94, 59.01
large number of study participants.
Fisseha et al. (2014) 50.32 43.02, 57.61
Ephrem et al. (2015) 50.96 43.58, 58.34
The results of subgroup analysis showed that undernutrition among
Kassu et al. (2006) 49.2 42.05, 56.35 TB patients varies across regions of the country. A higher proportion of
Wassie et al. (2014) 48.93 41.95, 55.91 undernutrition was observed in Amhara regional state (65.63%), as
compared to other regions of the country. This variation might be due to
the topography of the Amhara region, in which the soil is suitable for
malnutrition (BMI < 17 kg/m2) in patients with TB-HIV co-infected
erosion and the productivity of land decreases from time to time.
individuals, MDR-TB, and pregnant and lactating mothers are also
Additionally, most of the people practice agriculture for a long time
indicated to take supplementary food [40]. The WHO 2017 guideline-
through traditional methods, and the farmers in the rural area live in
recommended treatment adherence support should include food,
poverty. In the Amhara region, approximately 26.1% of the population
financial incentives, and transportation access for patients with tuber­
lived below the country’s poverty line in 2016, and the region is highly
culosis. Moreover, psychological support including a home visit is
affected by poverty compared with other regions of the country [46].
mandatory to increase treatment adherence of tuberculosis patients
In the current review, the highest prevalence of undernutrition was
[41].
observed in studies published before 2017 (52.24%) as compared with
Tuberculosis is one of the most common causes of death for people
studies published after 2017 (48.8%). The possible justification for this
living with HIV; conversely, HIV increases the risk of TB infection and
variation might be due to the Ethiopian Ministry of Health updating
promotes the progression of latent TB into active TB [42]. Undernutri­
2012 TB treatment guideline in November 2017. The updated 2017 TB
tion becomes an additional burden for TB-HIV co-infected patients. In
treatment guideline incorporates management strategies for malnutri­
this study, the pooled prevalence of undernutrition among TB-HIV co-
tion for tuberculosis patients [40].

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A. Wondmieneh et al. Journal of Clinical Tuberculosis and Other Mycobacterial Diseases 22 (2021) 100211

Finally, subgroup analysis was computed based on the sample size. Consent for publication
The finding showed that the highest magnitude of undernutrition was
detected in studies with a sample size <300 compared with studies with Not applicable.
a sample size greater than 300. This variation could be explained by the
fact that when the sample size increases, the accuracy and precision of Appendix A. Supplementary data
the data would be increased.
Supplementary data to this article can be found online at https://doi.
5. The strength and limitations of the study org/10.1016/j.jctube.2020.100211.

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