Prevalence and Associated Risk Factors of Intestinal Parasites and Enteric Bacterial Infections among Selected Region Food Handlers of Ethiopia during 2014–2022: A Systematic Review and Meta-Analysis

Food-borne disease due to intestinal parasites (IPs) and enteric bacterial infections (EBIs) remain a major public health problem. Food handlers, individuals involved in preparing and serving food, working with poor personal hygiene could pose a potential threat of spreading IPs and EBIs to the public. The aim of this study was to examine the overall prevalence and risk factors of IPs and EBIs among food handlers in four selected regions of Ethiopia. Scientific articles written in English were recovered from PubMed, ScienceDirect, Web of Science, Google Scholar, Cochrane Library, and other sources from Google Engine and University Library Databases. “Prevalence,” “Intestinal Parasites,” “Enteric Bacterial Infections,” “Associated Factors,” “Food Handlers,” and “Ethiopia” were the search terms used for this study. For critical appraisal, PRISMA 2009 was applied. Stata software version 16 was used to perform the meta-analysis. Heterogeneity and publication bias were evaluated using Cochran's Q, inverse variance (I2), and funnel plot asymmetry tests. A random-effects model was used to calculate the pooled burden of IPs and EBIs and its associated factors among food handlers, along with the parallel odds ratio (OR) and 95% confidence interval (CI). For this meta-analysis, a total of 5844 food handlers were included in the 20 eligible studies. The overall pooled prevalence of IPs and EBIs among food handlers in four selected regions of Ethiopia was 29.16% (95% CI: 22.61, 35.71), with covering (25.77%) and (3.39%) by IPs and EBIs, respectively. Ascaris lumbricoides, Entamoeba histolytica/dispar, Giardia lamblia, and hookworm were the most prevalent IPs among food handlers with a pooled prevalence of 7.58%, 6.78%, 3.67%, and 2.70%, respectively. Salmonella and Shigella spp. were the most prevalent EBIs among food handlers with a pooled prevalence of 2.78% and 0.61%, respectively. A high prevalence of IPs and EBIs among food handlers was observed in Oromia (38.56%; 95% CI: 29.98, 47.14), while a low prevalence was observed in the Tigray region (19.45%; 95% CI: 6.08, 32.82). Food handlers who had not taken food hygiene training (OR: 0.68, 95% CI: −0.34, 1.69), untrimmed finger nail (OR: 2.23, 95% CI: 1.47, 2.99), lack of periodic medical checkup (OR: 1.52, 95% CI: 0.41, 2.64), lack of handwashing habits (OR: 1.97, 95% CI: 0.53, 3.41), and eating raw vegetables and meat (OR: 2.63, 95% CI: 0.92, 4.34) were factors significantly associated with the prevalence of IPs and EBIs. The prevalence of IPs and EBIs was high in the selected Ethiopian region (Amhara, Oromia, SNNPR, and Tigray) food handlers along an increasing prevalence trend from 2014 to 2022. Therefore, this study recommends the provision of proper health education and training regarding personal hygiene, hand washing, food handling, medical checks, as well as raw vegetable and meat safety.


Introduction
Food-borne diseases are illnesses caused by ingesting pathogenic microorganisms (bacteria, fungi, viruses, and parasites) or their toxins (for bacteria and fungi) [1,2]. Food-borne outbreaks can result in both health and economic losses. According to the World Health Organization (WHO) [3], 600 million people worldwide become severely ill each year, with 420,000 dying as a result of food contamination. Food-borne infections affect an estimated 48 million people in the United States each year, resulting in 128,000 hospitalizations and 3,000 fatalities [4,5]. Food-borne and waterborne infections were also projected to cause approximately 700,000 deaths each year in Africa [6] and cause both short-term (nausea, vomiting, and diarrhea) and long-term (tissue damage, cancer, kidney or liver failure, brain disorders, and neural disorders) disorders.
Gastrointestinal parasitic infections are prevalent throughout the world, with the highest prevalence in poorer nations due to poor personal hygiene, environmental sanitation, socioeconomic, demographic, and health-related behaviors [7]. e most common way for intestinal parasitic infections to spread is through contaminated food and water, but they can further transmit from person-to-person through fecal-oral contact [8]. In the world, intestinal parasites infect approximately one-third of the total population, with the tropics and subtropics bearing the greatest load [9]. Ascaris lumbricoides, Trichuris trichiura, hookworm, Entamoeba histolytica, and Giardia lamblia infect an estimated 1.2 billion, 795 million, 740 million, 500 million, and 2.8 million people worldwide [10,11]. In Ethiopia, the burden of intestinal parasites (IPs) is extremely high. A third (26 million), a quarter (21 million), and one in every eight (11 million) Ethiopians are infected with Ascaris lumbricoides, Trichuris trichiura, and hookworm [12], respectively. As a result, Ethiopia has the second, third, and fourth largest burdens of ascariasis, hookworm, and trichuriasis, in sub-Saharan Africa, respectively.
Enteric bacterial infection (EBI)-causing microbes, namely, the genus of Salmonella (Salmonellosis) and Shigella (Shigellosis) are also the most important sources of foodborne diseases. As a result, they continue to be significant public health issues. Furthermore, clinical prevention and control of typhoid fever are difficult, particularly in Africa, due to the development of antibiotic resistance, and vaccines are not immunogenic to young children. Globally, there are 93.8 million cases of gastroenteritis caused by Salmonella species each year, with 155,000 deaths. An estimated 80.3 million of these cases were food-borne [13]. Shigella species are more common in temperate and tropical areas. Shigella species causes an estimated 80-165 million cases of disease and 600,000 deaths worldwide each year [14,15].
Food handlers are individuals engaged in preparing and serving foods, infected with gastrointestinal parasitic and bacterial infections, and practicing poor personal hygiene could be serious sources of transmission of IPs and EBIs to the public. Since food handlers infected with IPs and EBIs exhibit subclinical symptoms and are asymptomatic carriers, they are unaware of their possible role in the spread of infection, hinders the pathogens, and challenges in the integrated control and elimination of infections [8]. Furthermore, food handlers have a large impact on the spread of IPs and EBIs as they can directly or indirectly transmit infections to a large number of foods and drink consumers in food service establishments namely restaurants, hotels, factories, canteens, schools, hospitals, prisons, or other places where food is prepared and served to a range of users [16,17].
Aside from socioeconomic issues, other factors including the availability of clean water, the survival of pathogenic parasites and bacteria in different environmental conditions, and personal and public hygiene habits all play an important role in the transmission of IPs and EBIs [18,19]. Ethiopia has one of the lowest rates of clean water supply and toilet coverage [20]. Ethiopian studies on personal hygiene factors, for example, hand washing after toilet use, medical cheek examinations including stool exams, eating raw vegetables and meat, hand washing before food handling and meal, finger nail status, food hygiene training, and knowledge of enteric parasites and bacteria were found to contribute to the prevalence of IPs and EBIs among food handlers [12,21,22].
Numerous studies have been conducted in Africa, to investigate the prevalence of intestinal parasitic and enteric bacterial infections among handlers of food. In Ethiopia, the risk of Salmonella and Shigella infection among food handlers ranged from 1 to 7.5% [21,23,24]. However, the prevalence of intestinal parasitic infections among food handlers varied and was inconsistent across studies: 10.9 to 45.3% in Ethiopian university cafeterias [25][26][27][28][29][30], 43.9% in street dwellers [31], 48.1% in prisons [32], 35% in orphanage centers [33,34], 32.3% in public hospitals [34], and 14.5 to 44% in restaurants and cafeterias [12,22]. IPs and EBIs are one of the common public health issues in Ethiopia, with varying levels of prevalence throughout the country. In Ethiopia, only one systematic review and meta-analysis study were conducted on the prevalence of IPs among food handlers by Yimam et al. [12]. However, the prevalence and risk factors of both IPs and EBIs among selected region food handlers is not collected, well-organized, or recorded as a systematic review and meta-analysis. As a result, the objective of this study was to provide tangible evidence on the overall prevalence and risk factors for IPs and EBIs among food handlers using previously conducted research articles in four (Amhara, Oromia, SNNPR, and Tigray) regions of Ethiopia. Furthermore, the results obtained in the current investigation could significantly contribute to healthcare providers, users, and policy makers.

Profile of the Country.
Ethiopia measures 1,104,300 square kilometers and is located in the Horn of Africa (total land area is 1,000,000 square kilometers) (386,102 square miles). Ethiopia is bordered in the north by Eritrea, in the east by Djibouti and Somalia, in the west by Sudan and South Sudan, and in the south by Kenya. According to Worldometer's elaboration of the most recent United Nations data, Ethiopia's current population was 113,881,451 in 2020, which is comparable to 1.47%. Furthermore, according to the aforementioned report, approximately, 21.3% of the population (24, 463, 423) will live in urban areas by 2020 [35,36].

Search Strategy.
is systematic review and metaanalysis were performed according to the Guidelines and checklists for Preferred Reporting Items for Systematic 2 e Scientific World Journal Review and Meta-Analysis (PRISMA) 2009 [37]. An extensive search was conducted in international databases (PubMed, ScienceDirect, Web of Science, Google Scholar, and Cochrane Library) and other sources (Google Engine and University Library Databases). Articles were searched using MeSH key terms and phrases in combination or separate using Boolean operators ("OR"/"AND") such as "Prevalence," "Intestinal Parasites," "Enteric Bacterial Infections," "Associated Factors," "Food Handlers," and "Ethiopia." e study was carried out from November 2021 to June 2022. e search process was presented following PRISMA flow chart 2009 guidelines along the studies included and excluded with reasons of exclusion ( Figure 1).

Criteria for Inclusion and Exclusion of Studies.
In this systematic and meta-analysis review, institutional and hospital-based studies were included. Articles collected through the searches were evaluated for inclusion in the meta-analysis based on the following criteria: (i) Selected However, reports about knowledge and practice of food handlers towards IPs and EBIs, investigation on patterns of antimicrobial resistance of EBIs only, studies conducted outside selected regions and duplicate publications or extensions of analysis from original studies, as well as studies that were incompletely presented, were excluded from the review process. Four Ethiopian regions were included in the study due to their large population size, increasing urbanization and cover a wide range of geographical locations, along with many infrastructures, namely, hotels, resorts, cafeterias, and organizations (governmental and nongovernmental). Among many of the previously published articles, only 20 met the meta-analysis selection criteria ( Figure 1).

Data Extraction.
e data extraction protocol consists of the name of the country, author and year of publication, study setting, study area, sample size, number of positive cases, prevalence and their associated risk factors. If the study was conducted over a range of years, then the latest year of the stated range was used. e period from January 1 to March 30, 2022, was used for study selection, quality evaluation, and data extraction.

Quality Assessment of Individual Studies.
e general quality of the evidence was assessed using the GRADE approach (Grading of Recommendations Assessment, Development, and Evaluation) [38]. Using the three (methodological quality, comparability, and the outcome and statistical analysis of the study) main assessment tools, the quality of each study was determined. High-quality publications received five up to six points, moderate-quality publications received four points, and low-quality articles received zero up to three points. e choice and evaluation of the articles' quality were performed independently by the two reviewers (AG and AA). e articles were added after agreement was reached and the discrepancies between the reviewers were resolved through discussion.

Risk of Publication Bias.
Using funnel plot symmetry, Cochran's Q test, and the I 2 test, the risks of publication bias in articles were analyzed.

Statistical Analysis.
e pooled prevalence of IPs and EBIs among food handlers was calculated by dividing the total positive cases by the total study subjects included in this meta-analysis and multiplying by a factor of a hundred. We used a random-effects model to estimate the pooled effect size. To sort out the causes of heterogeneity, subgroup analysis was conducted based on sample size, region of the study, year of publication, and study area. e Cochran Q statistic with inverse variance and funnel plot symmetry was used to assess the existence of statistical heterogeneity. A log odds ratio was used to decide the association between IPs and EBIs with the associated risk factors among food handler respondents included in the studies. Meta-analysis was performed using Stata software version 16, where P ≤ 0.05 was considered statistically significant.

Results
A total of 131 articles on the prevalence and associated risk factors of IPs and EBIs among food handlers in Ethiopia were recovered.
irty-eight of these articles were excluded due to duplicates. Of the remaining 93 articles, 54 were excluded based on specific criteria included in the inclusion criteria and the data extraction protocol. Of the remaining 39 articles, 19 articles were further excluded due to the fact that they did not have OR, 95% CI, and the number of positive cases (meaning the report was based only on the estimated prevalence percentage). erefore, only 20 of the studies met the eligibility criteria and were included in the final systematic review and meta-analysis study (Figure 1). e prevalence of intestinal parasites among Ethiopian food handlers were assessed from 20 eligible studies conducted from 2014 to 2022 (9 year study). Helminthes, protozoan, and enteric bacteria were the most prevalent intestinal parasites and enteric bacterial infections among Ethiopian food handlers with a pooled prevalence of 13.89%, 11.88%, and 3.39%, respectively. 7.58%, 6.78%, 3.67%, 2.78%, and 2.70% was, respectively, the pooled prevalence of Ascaris lumbricoides, Entamoeba histolytica/dispar, Giardia lamblia, Salmonella spp., and hookworm (Table 1).  Figure 3). High heterogeneity in the prevalence of IPs and EBIs was observed across studies within and between three regions (Amhara, SNNPR, and Tigray) (I 2 > 96% and P < 0.001) (Figure 3)

Factors Associated with IPs and EBIs among Food Handlers in Ethiopia.
In this meta-analysis, food hygiene training, finger nail status, medical checkup, hand washing before food handling, hand washing before meals, and eating raw vegetables and meat were significantly associated with IPs and EBIs among food handlers (S4, S5, S6, S7, S8, and S9).
e results from five studies revealed that food hygiene training was strongly associated with IPs and EBIs. Food handlers who did not receive food hygiene training were 0.68 times more likely to have IPs and EBIs than those who had received food hygiene training (OR: 0. 68 Fourteen studies (70.0%) obtained high-quality scores, whereas six (30.0%) had medium-quality scores when it came to risk bias assessment (Table 1). e most common e Scientific World Journal 5 biases observed were representation and case definition. To know the effect of medium-quality studies, the pooled prevalence was calculated without involving it. e pooled prevalence estimates with and without these studies had confidence intervals that overlapped, indicating that there was no meaningful difference between them (Figure 4). Based on these findings, the majority of the primary study authors met high-quality standards (Figure 4). is gives the current study more credibility for healthcare providers, users, and policy makers.

Discussion
Food-borne parasitic and enteric bacterial illnesses are major public health concerns around the world, causing morbidity and mortality, especially in undeveloped countries like Ethiopia [59]. Personal sanitation and education of food handlers are as important as hygienic food preparation and delivery. is group of persons is involved in the handling, storage, transportation, processing, and preparation of food for users on a variety of levels. Knowing the exact pooled prevalence of intestinal parasites (IPs) and enteric bacterial infections (EBIs) among Ethiopian food handlers is useful as a guide for both governmental and nongovernmental policymakers and stakeholders to control food-related diseases. e overall prevalence of IPs and EBIs among four region food handlers was 29 [83], respectively. is variation within a country regions may be due to differences in study area, year of study, urbanization, food safety, and hygiene awareness and sociodemographic characteristics of the society.
In the current investigation, Ascaris lumbricoides was the most prevalent intestinal parasite with a pooled prevalence of 7.58%. is was consistent with the findings of a similar study conducted in South Asia [84], South Africa [85], Nigeria [86], and in different regions of Ethiopia [21,25,30,[87][88][89]. e current study found a high prevalence of A. lumbricoides, which could be attributed to the high level of environmental contamination caused by a number of infected people, the durability of Ascaris eggs under varying environmental conditions, the high fertility, and the sticky nature of the Ascaris egg shell, which aids in its attachment to human hands, fruits, and vegetables.
In this meta-analysis, the pooled prevalence of Entamoeba histolytica/dispar was 6.78%. It comparatively agrees with the reports from Mexico (5%) by Quihui et al. [77], Ethiopia (6.4%) by Yeshanew et al. [56], and Cameroon (7.3%) by Nsagha et al. [79]. However, the outcome of this investigation was higher than that of previous studies conducted by Walana et al. [72] in Ghana (0.21%), Bahrami et al. [90] in Iran (0.6%), Sanprasert et al. [69] in ailand (0.73%), and Ismail [64] in Saudi Arabia (2%). In comparison, the findings of the current study were lower than those of previous investigations conducted in Sudan (31.2%) by Suliman et al. [73], in Côte d'Ivoire (56%) by Coulibaly et al. [65], in Burkina Faso (66.5%) by Erismann et al. [80], and in Iraq (88%) by Hamady obeid Al-Taei [82]. e variance could be attributed to the quality of the food and water of the various study locations, as well as their ambient conditions. Since E. histolytica/dispar is a pollutant in drinking water and food as such it can easily spread through drinking polluted water and eating contaminated vegetables and foods. e pooled prevalence of G. lamblia in this metaanalysis was 3.67%, which is comparatively consistent with previous investigations conducted by Ismail [64] in Saudi Arabia (3%), Nsagha et al. [79] in Cameroon (3.3%), Rahi and Majeed, [91] in Iraq (4%), Sanprasert et al. [69] in ailand (4.2%), Ghenghesh et al. [92] in Libya (4.9%), Okyay et al. [93] in Turkey (6.1%), and Kimosop et al. [75] in Kenya (6.5%). However, it was  8 e Scientific World Journal lamblia (3.67%) in this study was significantly higher than that of Punsawad et al. [97] in ailand (0.6%) and Bahrami et al. [90] in Iran (1.7%). e discrepancy might be attributed to educational status, insufficient sanitary surveillance by the regulatory team, and a lack of hand washing facilities in the workplace. e pooled prevalence of hookworm was 2.70%, which is in agreement with other Ethiopian studies by Aklilu et al. [25] in Addis Ababa (2.1%) and Sahlemariam and Mekete [30] in Jimma (2.9%). e high frequency of such parasite could be attributed to poor personal hygiene and the parasite's simple mode of transmission, which is commonly found in contaminated soil, or surfaces contaminated with feces. Additionally, the disparity between studies could be explained by differences in eating habits, climate conditions, and other sociocultural variances between the location of the research and the year.
In this finding, the pooled prevalence of Shigella was 0.61%, which is comparatively in line with the findings of Dire Dawa city (1.7%) by Tadesse et al. [100], Motta Town (1.6%) by Yesigat et al. [54], and Bahir Dar University (1.2%) by Abera et al. [42]. As compared to the current study, a higher prevalence of Shigella was reported from Gondar University (2.7%) by Dagnew et al. [101] and Gondar town (10.1%) by Getie et al. [102]. is difference could be attributed to the culture medium used and to the geographical distribution.
Food handlers who did not receive food hygiene training were 0.68 times more likely to have IPs and EBIs than those who had received food hygiene training. It is supported by other studies conducted elsewhere in Ethiopia by Abera et al. [103], Nigusse et al. [21], and Gizaw et al. [104]. is could be due to differences in the number of institutions engaged in safety, employers' proclivity to hire food handlers without considering a health certificate as a basic criterion, and low monthly wage (paid) for food handlers in other study locations.
e pooled results showed that food handlers with untrimmed fingernail and poor cleanness habits were 2.23 times more likely to be infected with IPs and EBIs than their counterparts. is finding is supported by studies conducted in Ethiopia by Tegen et al. [35], by Eshetu et al. [105] in Sri Lanka by Galgamuwa et al. [106] and in Nepal by Sah et al. [107]. Due to the difficulties of cleaning, untrimmed fingernails among food handlers could serve as a vehicle for transporting IPs and EBIs from source to food. Food handlers with untrimmed fingernails may also contaminate food while serving customers if they are infected, and they can be identified as possible public health threats. Furthermore, this may most likely owing to a lack of awareness, poor hygiene practices, and sociodemographic characteristics among the food handlers. e probability of IPs and EBIs was 1.52 times higher among food handlers who did not attend a medical checkup than among their counterparts. It agrees with earlier studies conducted in Ethiopia by Marami et al. [29] and Gezehegn et al. [43]. erefore, it is better Ethiopian food handlers to update their medical certificates every three months that reduces the prevalence of IPs and EBIs among them and the wide customers. e odds of having IPs and EBIs were 1.97 times higher among food handlers who did not wash their hands before food handling with soap and water than among people who wash their hands. is finding was in line with the previous study conducted in Ethiopia by Tegen et al. [35], in Nigeria by Amuta et al. [108], in Indonesia by Pasaribu et al. [76], and in Cameroon by Tchakounté et al. [109]. is could be due to effective hand washing techniques interrupt the chain of transmission for IPs and EBIs. e odds of having IPs and EBIs were 2.63 times higher among food handlers who had habits of eating raw meat and vegetables as compared with the counterparts. It agrees with the findings conducted in Ethiopia by Tolera and Dufera [110] and Alemu et al. [111] and outside in Sri Lanka by Galgamuwa et al. [106] and in Libya by Osman et al. [81]. is could be due to raw meat and unwashed vegetables can carry IPs and EBIs causing pathogens.

Limitation of the Study.
A small number of published papers met the inclusion criteria and were involved in the current finding.

Conclusion
e pooled prevalence of IPs and EBIs was 29.16%. Ascaris lumbricoides, Entamoeba histolytica/dispar, Giardia lamblia, e Scientific World Journal and hookworm were the most prevalent IPs among food handlers with a pooled prevalence of 7.58%, 6.78%, 3.67%, and 2.70%, respectively. Salmonella and Shigella spp. were the most prevalent EBIs among Ethiopian food handlers with a pooled prevalence of 2.78% and 0.61%, respectively. Food handlers who did not receive food hygiene training, untrimmed finger nail, eating raw vegetables and meat, lack of periodic medical checkup and hand washing habits were factors significantly associated with the prevalence of IPs and EBIs. Increasing food handler's knowledge about personal hygienic conditions and periodic medical checkup for IPs and EBIs could consider an appropriate intervention measure.

AOR:
Adjusted odds ratio CI: Confidence interval EBIs: Enteric bacterial infections GRADE: Grading of Recommendations Assessment, Development and Evaluation IPs: Intestinal parasites PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analyses SNNPR: Southern Nations, Nationalities, and Peoples' Region STATA: Statistical software for data science.

Data Availability
All data sets have been presented within the manuscript and on supplementary data. e dataset supporting the conclusions of this article is available from the correspondence author upon a formal request.

Conflicts of Interest
e authors declare that theyhave no conflicts of interest regarding the publication of this paper.

Authors' Contributions
e authors designed the project and actively participated in study selection, quality evaluation, and data extraction, AG and AA analyzed the data, and AA wrote the manuscript and edited by AG. All the authors have read and approved the final manuscript.

Supplementary Materials
S1: pooled prevalence of IPs and EBIs among food handlers by sample size. S2: pooled prevalence of IPs and EBIs among food handlers from 2014 to 2022. S3: pooled prevalence of IPs and EBIs among food handlers by study area. S4: food hygiene training as an associated risk factor for IPs and EBIs among food handlers. S5: fingers nail status as an associated risk factor for IPs and EBIs among food handlers. S6: medical checkup as an associated risk factor for IPs and EBIs among food handlers. S7: hand washing habit before food handling as an associated risk factor for IPs and EBIs among food handlers. S8: eating raw vegetables and meat as an associated risk factor for IPs and EBIs among food handlers. (Supplementary Materials)