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Mengistu Et Al 2022 Bacteriological Quality and Public Health Risk of Ready To Eat Foods in Developing Countries

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1113916

research-article2022
MBI0010.1177/11786361221113916Microbiology InsightsMengistu et al

Bacteriological Quality and Public Health Risk of Microbiology Insights


Volume 15: 1–11

Ready-to-Eat Foods in Developing Countries: © The Author(s) 2022


Article reuse guidelines:

Systematic Review and Meta Analysis sagepub.com/journals-permissions


DOI: 10.1177/11786361221113916
https://doi.org/10.1177/11786361221113916

Dechasa Adare Mengistu1 , Desi Debelu Belami1,


Alemayehu Aschalew Tefera2 and Yohanis Alemeshet Asefa1
1Department of Environmental Health, College of Health and Medical Science, Haramaya
University, Harar, Ethiopia. 2Institutional Development and Facility Management, College of Health
and Medical Science, Haramaya University, Harar, Ethiopia.

ABSTRACT

Background: Ready-to-eat foods are foods that are consumed at the point of sale or later, without any further processing or treatment.
Foodborne diseases are on the rise worldwide, involving a wide range of diseases caused by pathogenic bacteria, and are becoming a pub-
lic health problem. Therefore, this study sought to identify and determine the bacteriological quality and public health risks in ready-to-eat
foods in developing countries.

Methods: The studies published from 2012 to 2020 were identified through systematic searches of various electronic databases such as
Google Scholar, PubMed and MEDLINE, MedNar, EMBASE, CINAHL, Scopus, and Science Direct. The articles were searched using a
Boolean logic operator (“AND,” “OR,” “NOT”) combination with Medical Subject Headings (MeSH) terms and keywords. All identified key-
words and an index term were checked in all included databases. In addition, a quality assessment is performed to determine the relevance
of the article, and then the data are extracted and analyzed.

Results: The current study found that the pooled prevalence of Staphylococcus aureus, Enterobacter species, Klebsiella, Escherichia coli,
Salmonella, Bacillus cereus, Pseudomonas species, and Shigella in ready-to-eat foods was 30.24% (95% CI: 18.8, 44.65), 11.3% (95% CI:
6.6, 18.7), 9.1% (95% CI: 7.0, 11.8), 23.8% (95% CI: 17.5, 31.5), 17.4% (95% CI: 11.6, 25.31)], 26.8% (95% CI: 13.7, 45.9), 6.1% (95% CI: 2.8,
12.6), 34.4% (95% CI: 18.1-55.4), respectively.

Conclusions: Most of the reviewed articles reported on various pathogenic bacterial species that are potentially harmful to human
health, such as Staphylococcus aureus, Salmonella, Shigella, and Escherichia coli in ready-to-eat food above the maximum allowable limit.
Therefore, relevant national and international organizations must take corrective measures to prevent foodborne diseases and protect human
health.

Keywords: Ready-to-eat foods, microbiological quality, street-vended foods, microbiological contamination, and public health

RECEIVED: December 28, 2021. ACCEPTED: June 27, 2022. Declaration of conflicting interests: The author(s) declared no potential
conflicts of interest with respect to the research, authorship, and/or publication of this
Type: Review article.
Funding: The author(s) received no financial support for the research, authorship, and/or CORRESPONDING AUTHOR: Dechasa Adare Mengistu, Department of Environmental
publication of this article. Health, College of Health and Medical Science, Haramaya University, PO.Box 235, Harar,
Ethiopia. Emails: Dechasa.Adare@haramaya.edu.et; dechasaadare@gmail.com

Introduction Due to the negligence of regulatory agencies and weak law


Ready-to-eat (RTE) foods are foods and beverages consumed enforcement, which has affected food quality and led to the
at the point of sale or at a later time without any further pro- provision of unsafe food to consumers, the hygiene and safety
cessing or treatment in such a way that may significantly reduce practices of most food suppliers have not been supervised or
the microbial load and could be raw or cooked, hot or chilled.1,2 monitored.9 According to estimates by the World Health
RTE foods can be fruits and fruit products,3 meat and its prod- Organization,10 eating contaminated food can cause/spread
ucts, eggs and the like.4-6 more than 200 different types of disease, and sometimes they
RTE foods provide an important source of readily available can cause long-term health problems, especially for vulnerable
and nutritious meals for consumers. Today, the increasing groups such as the elderly, pregnant women, and babies.
demand for RTE foods has led to an increase in the amount of Even in developed countries, it is estimated that one-third
food and different types of food that consumers can easily of the population is affected by microbial foodborne diseases
obtain.7 RTE foods are convenient meals for today’s lifestyle every year.11 According to Scallan et al,12 from 2000 to 2010,
because they do not require cooking or further preparation. In there were approximately 47.8 million foodborne illnesses in
addition to its benefits, the incidence of foodborne diseases is the United States each year, of which 9.4 million were caused
increasing globally, involving a wide range of diseases caused by by 31 known and identified pathogens. In United States alone,
pathogenic organisms, and becoming a public health problem food-borne diseases caused an estimated of 76 million illnesses,
that requires urgent response.8 325 000 hospitalizations, and 5000 deaths annually.13

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2 Microbiology Insights 

In developing countries, food-borne or water-borne Information sources and search strategy


microbial pathogens are the main cause of disease.11 Feglo
This review takes into account articles published in 2012 to
and Sakyi14 identified various types of microorganisms in
2020 that provide quantitative results and written in English.
RTE foods, such as Staphylococcus aureus, Bacillus, Klebsiella
The search was done based on keywords and Medical Subject
pneumoniae, and Escherichia coli (E.coli) in different types of
Headings (MeSH) terms in combination with “AND” or “OR”
RTE foods. Furthermore, Gizaw, also identified various
(Boolean logic operators) or individually from various elec-
bacterial species that cause food poisoning and foodborne
tronic databases such as Google Scholar, PubMed/MEDLINE,
diseases such as Salmonella, Shigella, E. coli, Clostridium,
Med Nar, EMBASE, CINAHL, Web of Science, Scopus, and
Staphylococcus, Campylobacter, and Vibrio from RTE foods,
Science direct. The authors then checked the identified key-
some of which are common bacteria that cause food-related
words and an index term in the included databases.
illness.15 Similarly, according to the study conducted in
The following is a search term the authors (DAM, DDB,
china using national food-borne disease outbreak surveil-
AAT and YAA) used in the initial search: ((((((“microbiologi-
lance system data (2003-2017), 19 517 food borne out-
cal quality” [MeSH Terms] OR (“microbiological” [All Fields]
breaks were reported, which resulted in 235 754 illnesses,
AND “quality” [All Fields]) OR “microbiological quality” [All
107 470 hospitalizations, and 1457 deaths. Of 13 307 out-
Fields]) AND (((“Public health” [MeSH Terms] OR (“public”
breaks with known etiology, about 6.8%, 4.2%, and 3.0% of
[All Fields] AND “health” [All Fields]) OR “public health”
outbreaks were caused by Salmonella, Staphylococcus aureus,
[All Fields])) AND ((((“risk” [MeSH Terms] OR “risk” [All
and Bacillus cereus, respectively.16
Fields] OR “risks” [All Fields])) OR ((“implication” [MeSH
In general, illness and death from diseases caused by con-
Terms] OR “implication” [All Fields] OR “implications” [All
taminated food are a threat to public health and a significant
Fields]) OR (((“hazard” [MeSH Terms] OR “hazard” [All
impediment to socio-economic development. Foodborne dis-
Fields] OR “hazards” [All Fields])) AND (((((((“ready-to-eat
ease outbreaks are common and cause considerable morbidity
food” [MeSH Terms] OR (“Ready-to-eat” [All Fields] AND
and mortality.17
“foods” [All Fields]) OR “ready-to-eat food” [All Fields])))
This indicates the need to determine the microbial load or
AND (((((“developing countries” [MeSH Terms] OR (“devel-
status of RTE foods to prevent foodborne diseases and pro-
oping” [All Fields] AND “countries” Fields]) OR “low-and
mote health and well-being. Therefore, this study sought to
middle-income countries” [MeSH Terms] OR (“low-and mid-
determine the microbiological quality and public health risks
dle-income” [All Fields] AND “countries” [All Fields])))))).
of RTE foods in developing countries.
Finally, the keywords and index terms were checked by
Methods authors (DAM, DDB, AAT, and YAA) across the included
This systematic review was conducted according to the electronic databases. Furthermore, a manual search was done
Preferred Reporting Items for Systematic Reviews and Meta- for further studies to cover other published articles not included
Analysis (PRISMA) guidelines.18 in the selected electronic databases. The last literature search
was conducted in December 2020.

Eligibility criteria
Study selection
This review included articles that met the following predeter-
mined inclusion criteria. The authors used ENDNOTE software version X5 (Thomson
Reuters, USA) to remove duplicate articles. Then the authors
(DAM, DDB, AAT, and YAA) independently screened the
i.  opulation: Any type of RTE foods carried out in
P studies by using the inclusion criteria based on their abstract
developing countries based on the World Bank. and titles. A disagreement between the authors was resolved by
ii. O utcome: Articles reported the quantitative out- taking the mean score of the 2 reviewers after repeating the
come (prevalence or magnitude) of selected bac- procedure and discussing the rationale for the differences.
terial species (Salmonella, Shigella, Staphylococcus Finally, the review included 23 articles that met the inclusion
aurous, Bacillus cereus, Pseudomonas, Entrobacter spe- criteria to determine the microbiological quality and public
cies, E. coli, and Klebsiella). health risk of RTE foods sold in developing countries.
iii. 
Study design: A cross-sectional study that provides
quantitative results.
Data extraction and quality assessment
iv. Study location: Full-text articles conducted in devel-
oping countries The authors (DAM, DDB, AAT, and YAA) used a predeter-
v.  Publication issue: Articles published in peer-reviewed mined data extraction form under the following key points/
journals from 2012 to 2020 headings: author, publication year, country where the study was
vi. Language: Full-text articles written in English. conducted, study design, and primary outcome. For articles
Mengistu et al 3

Record identified through database searches


(N= 3230). Google scholar (562)
PubMed/MEDLINE (1795), MedNar (233), Record identified through additional
Identification EMBASE (119), CINAHL (166), Scopus (129), search (N=133)
Web of Science (158), and Science direct (68).

Record after duplication


removed (n=2597).
Excluded articles (n =1,256)
Screening

 Review articles (n=48).


 Editorial reports (n=29].
Record screened by title and
 Not conducted in developing country (n=1,179).
abstract (n=1341).

Excluded articles (n=1142)


Full-text articles assessed for
Eligibility

Eligibility (n=199).  Non-relevant articles (n= 237).


 Published before 2012 (n=700)
 Small sample size(n=18)
 Not available in full texts (n=187)

Studies included in a
systematic review (n=23). Excluded articles (n=176)
Included

 Not reported outcome of the interest (n=134)


 Unclear objectives (n=26)
Studies included in Meta-  Unclear methods (n=16)
analysis (n=23).

Figure 1. Flow diagram that shows the selection process of studies for a systematic review and meta-analysis.

that met the inclusion criteria, the abstracts and methodology Results
were read and evaluated to establish their relevance and to Study selection
assess the quality of the included articles.
Furthermore, to assess and determine the quality of each A total of 3363 articles published between 2012 and 2020 were
article, the authors performed a rigorous and independent eval- searched from various electronic databases such as Google
uation using standardized critical evaluation tools, Joanna Scholar, PubMed/MEDLINE, MedNar, EMBASE, CINAHL,
Briggs Institute ( JBI) Critical Appraisal tools.19 Then the and Science direct. Following the search for articles, 766 dupli-
mean score was taken for each included article and classified as cate articles were excluded. Furthermore, 1256 articles were
high (80% and above), moderate (65%-80%), and low (less excluded after initial screening and 176 articles were excluded
than 65%) quality. Disagreements made among the authors after full-text articles were assessed for eligibility, of which 23
(DAM, DDB, AAT, and YAA) on what to be extracted and on articles were included in the systematic review and meta-analy-
quality assessment were resolved by discussion after repeating sis (Figure 1).
the same procedure and by taking a mean score of reviewers.
Characteristics of the included studies
Data analysis and statistical procedures
In this study, a total of 1959 RTE food samples were included
The pooled prevalence of selected bacterial species in RTE in 23 articles conducted in developing countries and published
foods was performed using Comprehensive Meta-Analysis between 2012 and 2020. Regarding the included articles, 7
(CMA) version 3.0 statistical software. Furthermore, the forest (30.43%) articles5,6,20-24 conducted in Nigeria, 4 (17.39%) arti-
plot and random effects models were used to determine the cles25-28 in Ethiopia, 2 (8.7%) articles29,30 in Bangladesh, 2
pooled prevalence of selected bacterial species in RTE foods. (8.7%) in India31,32, 2 (8.7%) articles in Ghana,14,33 and 1 arti-
Cochran’s Q test, (Q) and (I squared test) I2 statistics were used cle in Egypt,34 1 in Sudan,35 1 in South Africa,36 1 in Benin,37
to evaluate heterogeneity among included articles. The publi- 1 in Pakistan,38 and 1 in Saudi Arabia.39 The included studies
cation bias of the included studies was evaluated using funnel were cross-sectional studies with a sample size ranging from
plots and a P-value of <.05 was considered evidence of publi- 1223 to 25236 RTE foods samples. Based on the JBI Critical
cation bias. Finally, the results were presented using text, tables, Appraisal tool,19 all included articles had a low risk of bias. The
and graphs/figures. prevalence of Entrobacter, Klebsiella, B. cereus, S. aureus, E. coli,
4 Microbiology Insights 

Salmonella, Shigella, and Pseudomonas in RTE foods was ranged Discussion


from 5.36%22 to 41.6%,37 5.6%28 to 18.0%,14 5.0%25 to 93.3%,33 This study reviewed studies conducted in developing countries
not detected37 to 89.8%,28 not-detected36 96.7%,33 not to determine the microbiological quality and public health risk
detected36-38 to 100%,35 2%20 to 76.7%33 and 2.2%14 to 25.0%,23 of RTE foods. A total of 23 articles conducted on the bacterio-
respectively (Table 1). logical quality or contamination of RTE foods were included
in the systematic review and meta-analysis. The included arti-
Microbiological status of ready-to-eat foods cles reported various pathogenic bacterial species higher than
the recommended standard set for RTE foods.40
Prevalence of Staphylococcus aureus in ready-to-eat foods. The Currently, food-borne diseases represent a significant
pooled prevalence of Staphylococcus aureus in RTE foods was health problem for individuals, communities, and food indus-
30.24% [95% CI 18.8-44.65 and a P-value of .008] and tries41 and remain a global public health challenge.42
I2 = 95.26% with a P-value < .001 (Figure 2). Salmonella, E. coli, Shigella, Clostridium, Staphylococcus, and
Vibrio are among the most common bacteria species that
Prevalence of Entrobacter species in ready-to-eat foods. The cause food-related illness.43-45
overall prevalence of Entrobacter species in RTE food was However, the current study found the pooled prevalence of
11.3% [95% CI: 6.6-18.7 and a P-value < .001]; I2 = 87.37% selected pathogenic bacterial species in RTE foods such as
with a P-value < .001 (Figure 3). Staphylococcus aureus (30.24%), E. coli (23.8%), and Shigella
(34.4%). This indicates that at least 1 in 4 RTE food samples
Prevalence of Klebsiella in ready-to-eat foods. The total mean
were contaminated with at least one pathogenic bacterial spe-
prevalence of Klebsiella in RTE food was 9.1% [95% CI: 7.0-
cies and potential risk to consumer health. There is high risk of
11.8 and P-value < .001]; I2 = 31.73% with a P-value = .16
to be effected by food borne disease as the result of consuming
(Figure 4).
contaminated RTE foods, which can be highly complex, reach-
ing far beyond acute gastroenteritis and lead to a variety of
Prevalence of Escherichia coli in ready-to-eat foods. The pooled
health outcomes.46
prevalence of E. coli in RTE food was 23.8% [95% CI: 17.5-
Furthermore, the current study found the pooled preva-
31.5 and a P-value < .001]; I2 = 88.34% with a P-value < .001
lence of bacterial species in RTE foods such as Entrobacter
(Figure 5).
species (11.3%), Klebsiella (9.1%), Bacillus cereus (26.8%) and
Pseudomonas species (6.1%). Contamination of food with
Prevalence of Salmonella in ready-to-eat foods. The pooled
these microorganisms is beyond the standard limit and poses
prevalence of Salmonella in RTE food was 17.4% [95% CI:
a risk to human health. This was in line with various studies
11.6-25.3 and P-value < .001]; I2 = 84.59% with a
reporting various foodborne pathogenic bacterial species in
P-value < .001 (Figure 6).
foods such as B. cereus, C. perfringens, S. aureus, and Salmonella
Prevalence of Bacillus cereus in ready-to-eat foods. The pooled species.47,48
prevalence of Bacillus cereus in RTE food was 26.8% [95% CI: Gizaw also reported that different disease-causing bacteria
13.7-45.9 and a P-value = .019]; I2 = 93.5% with a P-value < .001 species were identified, mainly Salmonella species, E. coli,
(Figure 7). Klebsiella species, Shigella species, Enterobacter species,
Staphylococcus aureus, Bacillus cereus, and Pseudomonas species15
Prevalence of Pseudomonas species in ready-to-eat foods. The that was in line with the current study.
pooled prevalence of Pseudomonas species in RTE food was In general, foodborne illness is a major public health con-
6.1% [ 95% CI: 2.8-12.6 and a P-value < .001]; I2 = 84.24% cern and a common cause of illness and death worldwide.49
with a P-value < .001 (Figure 8). Foodborne diseases can occur as single cases or outbreaks and
sometimes as in the case of cholera spread around the world to
Prevalence of Shigella in ready-to-eat foods. The pooled preva- cause pandemics.50
lence of Shigella in RTE food was 34.4% [95% CI: 18.1-55.4]; This study indicated that the consumption of RTE foods
I2 = 87.47% with a P-value < .001 (Figure 9). contaminated with pathogenic bacterial species continues to be
a major risk to consumer health in developing countries.
Particularly, old, very young, immune-compromised, and
Subgroup analysis of the pooled prevalence of healthy people exposed to a very high dose of pathogenic
selected bacteria species ready-to-eat foods microorganisms, including bacterial species are at high risk of
The subgroup analysis of the pooled prevalence of E. coli, S. to be effected by food borne disease.51
aureus, B. cereus, Salmonella spp., Shigella spp., Entrobacter spp., Therefore, to prevent foodborne diseases and protect public
Klebsiella, and Pseudomonas species is presented in Table 2 health, it is crucial to apply food hygiene and safety measures
below with 95% CI and P-value (Table 2). that include, but are not limited to, good practices, proper
Table 1. Overall characteristics of the articles included in the systematic review and meta-analysis.

Authors Publication N Entrobacter Klebsiella B. cereus S. aureus E. coli Salmonella Shigella Pseudomonas Samples Country
year (%) (%) (%) (%) (%) (%) (%) (%)
Mengistu et al

Bello Olorunjuwon et al6 2014 120 0.06 0.08 0.08 0.14 0.06 0.06 NA 0.03 Juice Nigeria

Oje et al20 2018 35 NA 0.17 0.2 0.23 0.09 0.18 0.02 0.06 Meat pie, egg roll, roasted Nigeria
groundnut, and fried fish

Iqbal et al38 2016 90 NA NA 0.6637 0.2168 0.1194 ND NA NA Juice Pakistan

Geta et al25 2019 40 0.1 0.075 0.05 0.15 0.1 NA NA NA Juice Ethiopia

Mahfuza et al29 2016 50 NA 0.09 0.25 0.24 0.36 NA NA NA Fresh-cut fruits, salad vegetables Bangladesh
and juices

Reddi et al31 2015 150 NA NA NA 0.733 0.426 NA 0.486 NA Juice India

Abd-El-Malek34 2014 100 NA NA 0.2 0.4 NA 0.07 0.23 NA Liver sandwiches (kibda) Egypt

Amare et al26 2019 72 0.1587 NA NA 0.5396 0.238 NA NA NA Sanbusa, donat, bombolino and Ethiopia
bread

Dashen et al21 2020 100 NA NA NA 0.76 0.36 0.15 NA 0.08 Meat Nigeria

Alharbi et al39 2019 155 NA NA NA 0.07 0.18 0.15 NA NA Vegetable salad, falafel, kibtha Saudi Arabia
and shawarma

Igbinosa et al22 2020 210 0.0536 0.089 NA NA 0.411 0.214 NA 0.1786 Fried rice, jollof rice, moi-moi, Nigeria
salad, oil beans, non-oil beans,
and African salad

Sabuj et al30 2018 72 NA NA NA 0.4 0.333 0.267 NA NA Shingara, samosa, piazu, puri, Bangladesh
potato chop and beguni

Singh32 2015 15 NA NA 0.27 NA 0.4 0.13 NA NA Juice India

Elhag et al35 2017 30 NA NA NA 0.55 0.733 1.0 NA NA Juice Sudan

Nyenje et al36 2012 252 0.18 0.08 NA 0.032 ND ND NA 0.024 Vegetables, potatoes, rice, pies, South Africa
beef and chicken stew

Bristone et al23 2018 12 NA NA NA 0.375 0.5 0.375 0.375 0.25 Awara (soybean cheese) Nigeria

El-Hassan et al24 2018 15 NA NA NA 0.435 0.13 0.217 0.217 NA Meat Product (Tsire) Nigeria

Abakari et al33 2018 30 NA NA 0.933 NA 0.967 0.733 0.767 NA Vegetable salads Ghana

Leul and Kibret 27 2012 90 0.114 0.057 NA NA 0.143 0.2 NA 0.029 Juice Ethiopia

Abera et al28 2016 126 0.056 0.056 NA 0.898 0.315 0.176 NA NA Milk Ethiopia

Feglo and Sakyi14 2012 60 0.067 0.18 0.215 0.237 0.022 NA NA 0.022 Ice-kenkey, cocoa drink, Ghana
ready-to-eat red pepper, salad
and macaroni.

Anihouvi et al37 2019 60 0.416 NA 0.542 ND 0.25 ND NA NA Fresh pork and processed pork Benin
meat

Adesetan et al5 2013 75 NA NA 0.053 0.134 0.067 NA NA NA Street vended fruits Nigeria

Abbreviations: N, sample size; ND, not detected; S. aureus, Staphylococcus aureus; B. cereus, Bacillus cereus; E. coli, Escherichia coli.
5
6 Microbiology Insights 

Study name Statistics for each study Event rate and 95% CI

Event Lower Upper Z- p-


rate limit limit Value Value
Bello et al 0.140 0.089 0.214 -6.900 0.000
Oje et al 0.230 0.120 0.396 -3.008 0.003
Iqbal et al 0.217 0.144 0.314 -5.021 0.000
Geta et al 0.150 0.069 0.296 -3.917 0.000
Mahfuza et al 0.240 0.142 0.377 -3.481 0.000
Reddi, et al 0.733 0.657 0.798 5.472 0.000
Malek 0.400 0.309 0.499 -1.986 0.047
Amare et al 0.540 0.424 0.651 0.671 0.502
Dashen et al 0.760 0.667 0.834 4.923 0.000
Alharbi et al 0.070 0.039 0.122 -8.217 0.000
Sabuj et al 0.400 0.294 0.517 -1.685 0.092
Singh et al 0.270 0.106 0.536 -1.710 0.087
Elhag et al 0.550 0.373 0.715 0.547 0.585
Nyenje et al 0.032 0.016 0.063 -9.526 0.000
Bristone et al 0.375 0.157 0.659 -0.857 0.392
EL-Hassan et al 0.435 0.217 0.681 -0.502 0.616
Abera et al 0.898 0.832 0.940 7.390 0.000
Feglo and Sakyi 0.237 0.146 0.360 -3.851 0.000
Anihouvi et al 0.008 0.001 0.118 -3.377 0.001
Adesetan et al 0.134 0.074 0.231 -5.505 0.000
Overall 0.302 0.188 0.446 -2.641 0.008
Heterogeneity (I2) = 95.26 % with a p -value < 0.001 -1.00 -0.50 0.00 0.50 1.00
Random effect model
Figure 2. Forest plot shows the pooled prevalence of Staphylococcus aureus in ready-to-eat foods in developing countries.

Study name Statistics for each study Event rate and 95% CI
Event Lower Upper
rate limit limit Z-Value p-Value
Bello et al 0.060 0.029 0.119 -7.158 0.000
Geta et al 0.100 0.038 0.238 -4.169 0.000
Amare et al 0.159 0.091 0.262 -5.171 0.000
Igbinosa 0.054 0.030 0.094 -9.371 0.000
Nyenje et al 0.180 0.137 0.232 -9.248 0.000
Leul and kibret 0.114 0.063 0.198 -6.182 0.000
Abera et al 0.056 0.027 0.113 -7.290 0.000
Feglo and Sakyi 0.067 0.025 0.165 -5.101 0.000
Anihouvi et al 0.416 0.299 0.543 -1.295 0.195
Overall 0.113 0.066 0.187 -6.885 0.000
Heterogeneity (I2) = 87.37% with a p -value < 0.001 -1.00 -0.50 0.00 0.50 1.00
Random effect model
Figure 3. Forest plot shows the pooled prevalence of Entrobacter species in ready-to-eat foods in developing countries.
Mengistu et al 7

Study name Statistics for each study Event rate and 95% CI
Event Lower Upper
rate limit limit Z- p-Value
Value
Bello et al 0.080 0.043 0.144 -7.258 0.000
Oje et al 0.170 0.078 0.331 -3.524 0.000
Geta et al 0.075 0.024 0.208 -4.185 0.000
Mahfuza et al 0.090 0.036 0.207 -4.682 0.000
Igbinosa, 0.089 0.058 0.136 -9.597 0.000
Nyenje et al 0.080 0.052 0.121 -10.518 0.000
Leul and Kibret 0.057 0.024 0.128 -6.172 0.000
Abera et al 0.056 0.027 0.113 -7.290 0.000
Feglo and Sakyi 0.180 0.102 0.298 -4.513 0.000
0.091 0.070 0.118 -15.844 0.000
Heterogeneity (I2) = 31.73% with a p -value = 0.16 -1.00 -0.50 0.00 0.50 1.00
Random effect model
Figure 4. Forest plot shows the pooled prevalence of Klebsiella in ready-to-eat foods in developing countries.

Study name Statistics for each study Event rate and 95% CI

Event Lower Upper


rate limit limit Z-Value p-Value

Bello et al 0.060 0.029 0.119 -7.158 0.000


Oje et al 0.090 0.030 0.239 -3.917 0.000
Iqbal et al 0.119 0.067 0.204 -6.147 0.000
Geta et al 0.100 0.038 0.238 -4.169 0.000
Mahfuza et al 0.360 0.240 0.501 -1.953 0.051
Reddi, et al 0.426 0.349 0.506 -1.806 0.071
Amare et al. 0.238 0.154 0.349 -4.205 0.000
Dashen et al 0.360 0.272 0.458 -2.762 0.006
Alharbi et al 0.180 0.127 0.249 -7.253 0.000
Igbinosa, 0.411 0.346 0.479 -2.566 0.010
Sabuj et al 0.333 0.234 0.449 -2.778 0.005
Singh et al 0.400 0.192 0.652 -0.769 0.442
Elhag et al 0.733 0.550 0.860 2.447 0.014
Nyenje et al 0.002 0.000 0.031 -4.397 0.000
Bristone et al 0.500 0.244 0.756 0.000 1.000
EL-Hassan et al 0.130 0.032 0.402 -2.476 0.013
Abakari et al 0.967 0.798 0.995 3.305 0.001
Leul and kibret 0.143 0.085 0.231 -5.947 0.000
Abera et al 0.315 0.240 0.401 -4.051 0.000
Feglo and Sakyi 0.022 0.004 0.112 -4.311 0.000
Anihouvi et al 0.250 0.157 0.374 -3.685 0.000
Adesetan et al 0.067 0.028 0.151 -5.703 0.000
Overall 0.238 0.175 0.315 -5.878 0.000
2
Heterogeneity (I ) = 88.34% with a p -value < 0.001 -1.00 -0.50 0.00 0.50 1.00
Random effect model
Figure 5. Forest plot shows the pooled prevalence of Escherichia coli in ready-to-eat foods in developing countries.
8 Microbiology Insights 

Study name Statistics for each study Event rate and 95% CI

Event Lower Upper


rate limit limit Z-Value p-Value

Bello et al 0.060 0.029 0.119 -7.158 0.000


Oje et al 0.180 0.085 0.342 -3.446 0.001
Iqbal et al 0.005 0.000 0.082 -3.666 0.000
Malek 0.070 0.034 0.140 -6.600 0.000
Dashen et al 0.150 0.092 0.234 -6.194 0.000
Alharbi et al 0.150 0.102 0.215 -7.711 0.000
Igbinosa, 0.214 0.164 0.275 -7.732 0.000
Sabuj et al 0.267 0.178 0.380 -3.791 0.000
Singh et al 0.130 0.032 0.402 -2.476 0.013
Elhag et al 0.984 0.789 0.999 2.883 0.004
Nyenje et al 0.002 0.000 0.031 -4.397 0.000
Bristone et al 0.375 0.157 0.659 -0.857 0.392
EL-Hassan et al 0.217 0.075 0.486 -2.049 0.040
Abakari et al 0.733 0.550 0.860 2.447 0.014
Leul and kibret 0.200 0.130 0.295 -5.261 0.000
Abera et al 0.176 0.119 0.253 -6.599 0.000
Anihouvi et al 0.008 0.001 0.118 -3.377 0.001
Overall 0.174 0.116 0.253 -6.425 0.000

Heterogeneity (I2) = 84.59% with a p -value < 0.001 -1.00 -0.50 0.00 0.50 1.00
Random effect model
Figure 6. Forest plot shows the pooled prevalence of Salmonella in ready-to-eat foods in developing countries.

Study name Statistics for each study Event rate and 95% CI

Event Lower Upper


rate limit limit Z-Value p-Value

Bello et al 0.080 0.043 0.144 -7.258 0.000


Oje et al 0.200 0.098 0.364 -3.281 0.001
Iqbal et al 0.664 0.560 0.753 3.047 0.002
Geta et al 0.050 0.013 0.179 -4.059 0.000
Mahfuza et al 0.250 0.149 0.387 -3.364 0.001
Malek 0.200 0.133 0.290 -5.545 0.000
Abakari et al 0.933 0.769 0.983 3.607 0.000
Feglo and Sakyi 0.215 0.129 0.336 -4.121 0.000
Anihouvi et al 0.542 0.416 0.663 0.650 0.516
Adesetan et al 0.053 0.020 0.133 -5.594 0.000
Overall 0.268 0.137 0.459 -2.349 0.019

Heterogeneity (I2) = 95.3% with a p -value < 0.001 -1.00 -0.50 0.00 0.50 1.00
Random effect model
Figure 7. Forest plot shows the pooled prevalence of Bacillus cereus in ready-to-eat foods in developing countries.
Mengistu et al 9

Study name Statistics for each study Event rate and 95% CI

Event Lower Upper


rate limit limit Z-Value p-Value

Bello et al 0.030 0.011 0.081 -6.496 0.000


Oje et al 0.060 0.016 0.205 -3.866 0.000
Dashen et al 0.080 0.041 0.152 -6.626 0.000
Igbinosa, 0.179 0.133 0.236 -8.469 0.000
Nyenje et al 0.024 0.011 0.052 -9.003 0.000
Bristone et al 0.250 0.083 0.552 -1.648 0.099
Leul and kibret 0.029 0.009 0.093 -5.589 0.000
Feglo and Sakyi 0.022 0.004 0.112 -4.311 0.000
Ovelall 0.061 0.028 0.126 -6.700 0.000

Heterogeneity (I2) = 84.24% with a p -value < 0.001 -1.00 -0.50 0.00 0.50 1.00
Random effect model
Figure 8. Forest plot shows the pooled prevalence of Pseudomonas species in ready-to-eat foods in developing countries.

Study name Statistics for each study Event rate and 95% CI

Event Lower Upper


rate limit limit Z-Value p-Value

Oje et al 0.020 0.002 0.179 -3.223 0.001


Reddi et al 0.486 0.407 0.566 -0.343 0.732
Malek 0.230 0.158 0.322 -5.085 0.000
Bristone et al 0.375 0.157 0.659 -0.857 0.392
Hassan et al 0.217 0.075 0.486 -2.049 0.040
Abakari et al 0.767 0.585 0.885 2.759 0.006
0.344 0.181 0.554 -1.470 0.142
Heterogeneity (I2) = 87.47% with a p-value < 0.001
-1.00 -0.50 0.00 0.50 1.00
Random effect model
Figure 9. Forest plot shows the pooled prevalence of Shigella in ready-to-eat foods in developing countries.

Table 2. Subgroup analysis of the pooled prevalence of selected bacterial species in ready-to-eat foods in developing countries.

Selected bacteria Based on study area (Country) Based on publication year


species Pooled 95% CI P-value I2 Pooled 95% CI P-value I2
Prevalence (%) LCI UCL prevalence LCI UCL

E. coli 29.5 26.2 33.2 <.001 88.34 29.2 25.8 32.8 <.001 88.34

Staphylococcus aureus 23.7 20.1 27.7 <.001 95.26 47.3 36.7 50 <.001 95.26

Bacillus cereus 36.2 31 41.8 <.001 93.5 16.5 11.3 23.6 <.001 93.5

Salmonella species 19.1 16.3 22.4 <.001 84.59 14.3 11 18.5 <.001 84.59

Shigella species 42.1 36.2 48.3 =.012 87.47 39.3 33.2 45.6 =.001 87.47
Entrobacter species 14.9 12.5 17.8 <.001 87.37 7.9 5.9 10.6 <.001 87.37

Klebsiella 9 7.3 11.2 <.001 31.75 8.8 6.9 11.3 <.001 31.75

Pseudomonas species 4.2 2.6 6.8 <.001 84.24 4.4 2.9 6.7 <.001 84.24

Abbreviations: CI, confidence interval; E. coli, Escherichia coli; LCI, lower confidence interval; UCI, upper confidence interval.
10 Microbiology Insights 

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