Prevalence of intestinal parasitic infection in food handlers of Iran: A systematic review and meta‐analysis

Abstract Food handlers regardless of whether preparing or serving food, play key roles in the transmission of food‐borne infections. This study aimed to evaluate the prevalence of intestinal parasitic infections in food handlers in Iran. In the present study, a comprehensive literature search was carried out in electronic databases, including PubMed, Scopus, Google Scholar, Science Direct, Magiran, Scientific Information Database (SID), Iran Medex and Iran Doc, to identify all the published studies from 2000 to 31st April 2019. A total of 25 articles from different regions of Iran were identified and fulfilled our eligibility criteria. Totally, 140,447 cases were examined and 1163 cases were infected with intestinal parasites. Of all cases, 19,516 were male and 5901 were female with 1163 and 652 infected cases, respectively. The overall prevalence of intestinal parasitic infections was evaluated 14.0% [95% CI: 11.0‐17.0%]. It is revealed that protozoan, such as Giardia lamblia, with prevalence of 41.0% [95% CI: 25.0‐59.0%], Blastosystis hominis with 28.0% [95% CI: 15.0‐44.0%] and Entamoeba coli with 22.0% [95% CI: 16.0‐29.0%] had the highest prevalence while, Dientamoeba fragilis 5.0% [95% CI: 4.0‐7.0%], Iodamoeba bütschlii 5.0% [95% CI: 2.0‐8.0%], Chilomastix mesnili 5.0% [95% CI: 2.0‐9.0%] and Endolimax nana with 3.0% [95% CI: 1.0‐7.0%], were less prevalent. Infection with Ascaris lumbricoides7.0% [95% CI: 0.0‐29.0%] was more prevalent helminth followed with Enterobius vermicularis 3.0% [95% CI: 1.0‐5.0%], Hymenolepis nana 2.0% [95% CI: 1.0‐3.0%], Taenia spp. 2.0% [95% CI: 0.0‐7.0%] and Trichuris trichiura 1.0% [95% CI: 0.0‐1.0%]. The high prevalence of commensal parasites, such as Entamoeba coli, which does not need cure is indicating the importance of personal hygiene in food handlers. Our results revealed the high prevalence of intestinal parasitic infection in food handlers in Iran. Monitoring programs to prevent and controlling of transmission to individuals are needed.


INTRODUCTION
Intestinal parasitic infections are widespread in the world and transmitting directly or indirectly among populations (FeizHadad et al., 2017). In some cases, carriers without any symptoms of the disease are the main source of infection especially if they work as food handlers.
Given the high prevalence of 48.4 million cases of parasitic infections in the world, this fact is not reality. The importance of this issue emerges when those people work as food handlers and do not care about personal hygiene (Saki et al., 2012;Torgerson et al., 2015).
Although people are in constant contact with environmental pathogens, including parasites, they are not affected seriously since immunity is important in disease aetiology. Despite the good toleration of parasitic infection in healthiest individuals, some people are vulnerable to parasites (FeizHadad et al., 2017). The importance of parasitic infection is highlighted when the infected individual plays a major role in food handling or food industries.
Iran is a suitable region for most parasitesˊgrowth and distribution due to the geographic, socioeconomic and behavioural conditions.
Serious efforts to control parasitic infection have resulted in a burden decrease of parasitic infections, but contamination with intestinal parasites is still a concern for health-care services (Kusolsuk et al., 2011). Using animal and human faeces as fertilizers for agriculture and vegetable gardens, climatic conditions, traditions, and customs are considered the main reasons for the incidence of parasitic infections in some parts of the country. Direct transmission from person to person is another factor that complicates the parasite control programs. This kind of parasite transmission is markedly important in food handlers and particularly in oral-faecal parasites such as Giardia lamblia (G. lamblia), Hymenolepis nana (H. nana) and Enterobius vermicularis (E. vermicularis) (Kusolsuk et al., 2011;Kheirandish et al., 2014). If food handlers do not care about personal hygiene, they can contaminate dishes, salads and other food materials which finally results in the contamination of the customers (Koohsar et al., 2012).
Studies on transmitted parasites by food handlers indicate that Entamoeba coli (E. coli) is the most common non-pathogenic protozoa indicating a contamination with faecal materials and poor hygiene (Kassani et al., 2015). Also, zoonotic nature of some parasites, such as Enta- it is proven that they are associated with diarrhoea (Motazedian et al., 2016). Several studies have been conducted in different parts of the world regarding the prevalence of intestinal parasites in food handlers (Acilel et al., 2008;Abd Al-Muhsin AL-Khayat et al., 2017;Esparar et al., 2004;Kusolsuk et al., 2011;Wali et al., 2017). In this study, we performed a systematic review and meta-analysis to find out the pooled estimate of the prevalence of intestinal parasites, such as G. lamblia, E.
coli, B. hominis and H. nana, in food handlers, so the health-care officials discovered the routes to prevent and control the disease transmitted by parasites and also, the best and most practical method used in conducting experiments to achieve the best results.

Data collection
In the initial search of collected bibliographic references, 433 articles were found. After removing duplicated, irrelevant studies and studies out of Iran, finally, 25 articles with epidemiological parameters of interest fulfilled the inclusion criteria. Those articles reporting the prevalence of intestinal parasitic infections in food handlers in Iran were included to our study (Table 1).

Data extraction
Two authors screened the titles, abstracts and full text of literatures, independently. Any disagreements between two reviewers were resolved by discussion among researchers. Extracted data included first author name, the year of publication, prevalence rate, demographic information (age and gender), geographical region of study, diagnostic test, sample size (number of examined people), and the number of infected cases (Table 1).

Quality of study
To assess the quality of observational studies included in this metaanalysis using a checklist as in Review/guideline/editorial were omitted F I G U R E 1 PRISMA flowchart describing the study design process 'Yes = 1' and 'No = 0' . The sum of scores is 0 to 12 and for including study in meta-analysis a quality score of at least 8 is required.

Statistical analysis
After extracting the sample size and the number of positive infections for each study, the proportion of infection and standard error (SE) were computed. Before estimating pooled effect size, sensitivity analysis was used to explore the effect of each study on pooled effect size. Heterogeneity among studies assessed using both Q-test which is suggested by the Cochrane Handbook (p < 0.1 as substantial heterogeneity) and I-square index I 2 < 50%, as substantial heterogeneity).
If we found substantial heterogeneity, sub-group meta-analysis (fixed or random effect model) was performed to compute the pooled prevalence of infection based on a characteristic such as sex, country, education, pathogenicity and parasite species. In addition to meta-regression examined to find the source of heterogeneity. To detect sources of het-erogeneity, we performed meta-regression on publish year and sample size of studies.
To evaluate publication bias, we aided a funnel plot and egger's test as a statistical test (p < 0.1 as significant). If we detected a substantial publication bias, the trim and fill method was applied to estimate and adjust for the number of missing studies (due to publication bias) in a meta-analysis (Ebrahim, 2006

RESULTS
Among all searched databases (eight databases) and unpublished data studies that defined the gender of participants, a number of 19,516 cases were male and 5901 cases were female with 1163 (13.0%) infected cases in males and 652 (8.0%) infected in females, respectively (Table 1). There was a significant difference between infection among males 13.0% (10.0-15.0%) and females 8.0% (5.0-11.0%) (p = 0.027) ( Figure 5).
To evaluate the effect of each study on the pooled estimate of prevalence, by repeating the meta-analysis after omitting each study, the sensitivity of studies was depicted in Figure 2. All effect sizes of 25 studies were located in 95% confidence interval (95% CI). Therefore, none of the studies substantially affected the pooled prevalence of intestinal infection and we can include all studies in the meta-analysis ( Figure 2).  (Figure 3). In this review, some of the parasites were nonpathogenic (Tables 3,4).
The highest rate of infection was found in owners of the school cafeterias with 28.0% followed by 11.50% in butchers and 10.20%

DISCUSSION
Food-borne parasitic diseases are one of the main public-health concerns all around the world which may lead to morbidity and mortality in developing countries (Simsek et al., 2009 (Kusolsuk et al., 2013). Their results revealed insufficient hygiene in food preparation and our results indicated inappropriate personal hygiene. Our meta-analysis showed that the highest intestinal infection in food handlers was caused by protozoan parasites and the most frequent parasite (41.0%) was G. lamblia (Figure 3). These protozoa are among the most pathogenic parasites (Arora, 2015) which Also, training hygiene can affect the improvement of society's health (Kheirandish et al., 2011).

CONCLUSIONS
Our results revealed the high prevalence of intestinal parasitic infection in food handlers in Iran. This high prevalence is largely due to poor personal hygiene practice, poverty, lack of knowledge, insufficient environmental sanitation and inadequate health controlling services.
Although the food industry workers, food handlers, and anyone who is connected with the production, handling, storage, transportation, preparation, or else, is obliged to undergo routine medical examinations including stool microscopy for intestinal parasitic infections (once every 6 months) but, it seems that they are not sufficient. It is advised that some strict rules such as obligation in filling the stool container in the lab should be added. Also, if infected food handler cases are identified, immediate decisions for the exclusion of the career up the resolving all symptoms or completion of further investigations should be made. Additional programs, including education for changing attitude about infectious diseases requires more consideration.

CONFLICT OF INTEREST
The authors declare that they do not have any conflict of interest.

ETHICS APPROVAL
No ethical approval was required as this is a review article with no original research data.

DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.

PEER REVIEW
The peer review history for this article is available at https://publons. com/publon/10.1002/vms3.590