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Intestinal parasites among food handlers in Iran: A systematic review and meta-
analysis

Aref Teimouri, Hossein Keshavarz, Sina Mohtasebi, Fatemeh Goudarzi, Fattaneh

Mikaeili, Alireza Borjian, Mahya Allahmoradi, Yonas Yimam, Mohammad Javad
Abbaszadeh Afshar
PII: S0740-0020(20)30292-6
DOI: https://doi.org/10.1016/j.fm.2020.103703
Reference: YFMIC 103703

To appear in: Food Microbiology

Received Date: 19 August 2020

Revised Date: 26 November 2020
Accepted Date: 27 November 2020

Please cite this article as: Teimouri, A., Keshavarz, H., Mohtasebi, S., Goudarzi, F., Mikaeili, F., Borjian,
A., Allahmoradi, M., Yimam, Y., Abbaszadeh Afshar, M.J., Intestinal parasites among food handlers in
Iran: A systematic review and meta-analysis, Food Microbiology (2021), doi: https://doi.org/10.1016/
j.fm.2020.103703.

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1 Intestinal parasites among food handlers in Iran: A systematic review and meta-
2 analysis
3 Aref Teimouria, Hossein Keshavarzb, Sina Mohtasebib, Fatemeh Goudarzib, Fattaneh Mikaeilia,
4 Alireza Borjianb, Mahya Allahmoradib, Yonas Yimamb,c, Mohammad Javad Abbaszadeh
5 Afsharb,d*
6
a
7 Department of Parasitology and Mycology, School of Medicine, Shiraz University of Medical
8 Sciences, Shiraz, Iran

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b
9 Department of Medical Parasitology and Mycology, School of Public Health, Tehran University

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10 of Medical Sciences, Tehran, Iran
c
11 Woldia University, Woldia, Ethiopia -p
d
12 Department of Medical Parasitology and Mycology, School of Medicine, Jiroft University of
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13 Medical Sciences, Jiroft, Iran
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15 Corresponding author:
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16 Mohammad Javad Abbaszadeh Afshar, Department of Medical Parasitology and Mycology,

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17 School of Medicine, Jiroft University of Medical Sciences, Jiroft, Iran

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18 Email: Mj.afshar1990@gmail.com

19 Tel: +989136393293

20 ORCID iD: 0000-0002-8723-6432

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2 Abstract
3 Regarding preparing and serving foods, food handlers have an influential role in the spreading
4 of foodborne infections. Due to the great potential to cause foodborne infections, intestinal
5 parasites (IPs) are considered a significant public health problem in today's societies. In Iran,
6 despite several regional reports, national data on IPs prevalence in food handlers are lacking.
7 The aim of the present study, therefore, is to estimate the pooled prevalence of IPs infections
8 and associated pooled odds ratio of educational level among food handlers in Iran. PubMed,

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9 Web of Science, Scopus, Embase, and Google Scholar databases (international) and SID and
Magiran databases (national) were systematically searched for studies that reporting the

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11 prevalence of IPs in food handlers in Iran, published between 2000 and 2020. Pooled
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prevalence was estimated using a random-effects model with a 95% confidence interval (CI)
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13 and depicted as a forest plot, while heterogeneity was evaluated using Cochran’s Q-test. The
14 overall pooled prevalence estimate for IPs was 19.3% (95% CI=14.9 to 23.7%). Prevalence of the
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15 protozoan parasites (20%, 95% CI=13.7 to 26.3%) was significantly higher than that of the
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16 helminthic parasites (1.6%, 95% CI=1.1 to 2.0%). Giardia lamblia (5.2%), Entamoeba coli (5.0%),
17 and Blastocystis spp. (4.4%), as protozoan parasites, and Ascaris lumbricoides (1.4%), Enterobius
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18 vermicularis (0.9%), and Hymenolepis nana (0.5%), as helminthic parasites, were the most
commonly reported species. Food handlers with low educational levels were 20% more
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20 exposed to IPs infection, compared to those with high educational levels (OR=1.21, 95% CI=0.88
21 to 1.65). The prevalence of IPs infections among food handlers in Iran is significant. Besides
22 taking into account this epidemiologic information, a holistic approach, including periodic stool
23 screening, health education, and treatment of infected food handlers, will help in the control of
24 these infections in Iran.
25 Keywords: Food handlers, Intestinal parasites, Iran, Systematic review, Meta-analysis
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2 1. Background
3 Regarding preparing and serving foods, food handlers have an influential role in the spreading
4 of foodborne infections. Due to the great potential to cause foodborne infections, intestinal
5 parasites (IPs) are considered a significant public health problem in today's societies (Acco et
6 al., 2003; Pozio, 2020).

7 Human societies have always fought against infectious diseases, some of which are caused by

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8 IPs (Alum et al., 2010). IPs have a widespread distribution, especially among the developing
9 communities where limited sanitation facilities and poor personal hygiene have contributed to

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10 a notable prevalence of these agents. Around one billion people across the world are infected
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by at least one of the common IPs species, including Giardia lamblia, Entamoeba
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12 histolytica/dispar, Ascaris lumbricoides, Trichuris trichiura, and hookworms (Karshima, 2018;
13 Yimam et al., 2020).
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14 Spreading of infectious diseases by food handlers is a commonly persistent challenge

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15 worldwide. Food handlers with poor personal hygiene from food service establishments such as
16 restaurants, hotels, factories, canteens, schools, hospitals, and prisons could be potential
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17 sources of infections since they may introduce pathogens in the food during production,
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18 processing, distribution, and handling. Due to subclinical infections in most food handlers, they
19 can play important roles as healthy carriers to spread infectious agents through society (Yimam
20 et al., 2020). On the other hand, nowadays, the modern lifestyle leads to more consumption of
21 ready-to-eat (fast) foods that rolled up the pieces of IPs transmission puzzle through food
22 handlers (Abate et al., 2013).

23 Several studies have been carried out to assess IPs infections in food handlers from various
24 regions of Iran. Due to differences in socioeconomic, geographic, sanitary/hygiene, cultural, and
25 educational statuses, a wide range of IPs prevalence has been reported from 1 to 76% (Fallah et
26 al., 2004; Heydari-Hengami et al., 2018). In a developing country like Iran, with a population of
27 over 80 million people with limited resources, cost-effectiveness in the control of IPs infections
28 is essential to ensure efficient allocation of resources and achievement of high impact. Hence, it

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1 is important to provide useful national and comprehensive epidemiological information on IPs
2 prevalence in food handlers, as a super-spreader population, which help to implementation of
3 an effective control program. Thus, the main objective of this systematic review and meta-
4 analysis was to estimate the pooled prevalence of IPs and associated pooled odds ratio of
5 educational level among food handlers of foodservice establishments in Iran.

6 2. Material and methods

7 The present study followed the preferred reporting items for systematic reviews and meta-
8 analysis (PRISMA) guideline (Moher et al., 2009) (Additional file 1). The infection of Iranian food

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9 handlers with IPs was the outcome of interest.

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10 2.1. Search strategy

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Four international databases of PubMed, Web of Science, Scopus, and Embase and two national
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12 databases of SID and Magiran were respectively searched for English and Persian articles
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13 published between 1st January 2000 and 5th July 2020. Furthermore, Google Scholar database
14 was used for proofing the search. Relevant articles were found using the following search
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15 terms: (‘intestinal parasites’ or ‘parasitic intestinal disease’ or ‘intestinal protozoa’ or ‘intestinal

16 helminths’) and (‘food handlers’) and (‘Iran’). Bibliographic lists of the relevant studies were
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17 searched in-depth to find other associated articles that were not found through database
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18 searching. All searched articles were imported to EndNote X8 software (Thompson Reuter, CA,
19 USA) for management.

20 2.2. Eligibility criteria and study selection

21 After removing duplicated articles, the studies were screened through title and abstract for
22 relevance. This was followed by a detailed full-text review to determine the presence of the
23 outcome of interest and other inclusion requirements. Two investigators (FG and AB) assessed
24 the eligibility, independently, then, discrepancies were removed following discussion with the
25 third reviewer (MA). Eligibility for the inclusion of a study was based on the following
26 conditions: (a) it was carried out in Iran, (b) it was reported IPs infections among Iranian food
27 handlers, (c) it was published in English or Persian, (d) it was a cross-sectional study, (e) sample
28 size and the number of positive cases were clearly stated, (f) it was published in a peer-
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1 reviewed journal, and (g) parasites were identified at least to the genus level. Studies that did
2 not meet these inclusion criteria were excluded.

3 2.3. Data extraction

4 Data extracted from the eligible studies were: first author, publication year, year(s) of
5 conduction (study period), sample size, number of infected subjects, type of the intestinal
6 parasites, educational levels of food handlers, region of study, and diagnostic method.

7 2.4. Quality assessment

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8 Quality assessment of the included studies was carried out using Joanna Briggs Institute (JBI)

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9 critical appraisal instrument for studies reporting prevalence data (Munn et al., 2015). This tool
10 included nine items with four options of ‘yes’, ‘no’, ‘unclear’, and ‘not applicable’. The ‘yes’
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answers were used to calculate the final score of each article. Included studies were
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12 categorized as presenting ‘high risk of bias’ (scores equal or lower than 5), ‘moderate risk of
13 bias’ (scores higher than 5 to 7), and ‘low risk of bias’ (scores above 7) (Martins et al., 2020).
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14 2.5. Data synthesis and statistical analysis

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15 Preliminary analyses including summations, subtractions, divisions, multiplications and

estimation of percentages were conducted using Microsoft Excel. Statistical and meta-analyses
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17 were carried out using STATA statistical software v.14 (Stata Corp, College Station, TX, USA).
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18 2.6. Pooling, sub-group and heterogeneity analyses

19 Overall pooled prevalence of the intestinal parasites (95% confidence interval, CI) was
20 calculated, using random-effects model, and presented as a forest plot (Hedges and Vevea,
21 1998). Sub-group analysis was carried out based on the geographical regions, year(s) of
22 conduction (study period), sample size, diagnostic methods, risk of bias (quality), and type of
23 the reported intestinal parasites (protozoa/helminth).

24 Heterogeneity, which is the measure of variability between studies analyzed was evaluated
25 using Cochran’s Q-test while percentage variation in prevalence estimate due to heterogeneity
26 was quantified using the I2 statistic. I2 values of 0, 25, 50, and 75% were considered as ‘no’,
27 ‘low’, ‘moderate’, and ‘high’ heterogeneities respectively (Higgins and Thompson, 2002).

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1 2.7. Publication bias, sensitivity and meta-regression analyses
2 Publication bias was assessed using Egger's intercept and visual inspection of the funnel plot
3 (Egger et al., 1997). A sensitivity analysis was carried out using random-effect model through
4 step-by-step omitting of a single study to evaluate robustness of the pooled prevalence
5 estimate (Copas and Shi, 2000). Moreover, meta-regression was carried out by considering the
6 publication year and sample size to detect the potential source of heterogeneity.

7 3. Results
8 3.1. Literature search and eligible studies

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9 Of the 206 studies identified, 202 were retrieved through the search of databases and four

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10 from the lists article references. One hundred thirty-four studies were removed because of
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duplication. Seventy-two studies were subjected to title and abstract review, where 35 studies
were excluded. Full text of 37 remains studies assessed, and five studies excluded because of
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13 the inconsistency in the information (n=1) and insufficient data on sample sizes and the number
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14 of cases (n=4). Finally, 32 studies were found eligible for the final analysis (Fig. 1).
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15 3.2. Characteristics of the eligible studies

16 Table 1 presents the characteristics of the 32 eligible studies meta-analyzed. Studies were
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17 conducted between 1994 and 2018 and published between 2000 and 2019. Prevalence of IPs
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18 infections among eligible studies ranged between 1 and 76%. Most of the studies were
19 reported from the center (n=9) and south (n=7) regions. Also, most of the studies were
20 conducted between 2011 and 2015 while only one study was conducted before 2000. For the
21 pooled prevalence estimate of IPs infections, a total of 127,162 food handlers were involved.
22 Regarding the risks of bias assessments, 27 studies (84%) had low risks of bias, four studies
23 (13%) included medium risks of bias, and one study (3%) included high risks of bias.

24 3.3. Pooling, sub-group and heterogeneity analyses

25 Pooled prevalence of the IPs in food handlers was estimated at 19.3% (95% CI=14.9 to 23.7%)
26 (Fig. 2). Pooled prevalence estimates for sub-groups including region, study period, sample size,
27 diagnostic method, and risk of bias are presented in Table 2. The highest and lowest pooled
28 prevalence estimates were recorded in center [24.6% (95% CI=17.3 to 31.8%)] and west [10.0%

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1 (95% CI=6.0 to 14.0%)] regions, respectively. Pooled prevalence estimate of IPs has risen from
2 44.6% (95% CI=26.0 to 63.3%) in 2001-2005 interval to 7.4% (95 CI=5.7 to 9.1%) in 2016-2020
3 interval. Also, in terms of the diagnostic method studies which implementation direct wet-
4 mount and concentration methods together record the highest pooled prevalence estimate
5 [22.0% (95% CI=17.4 to 26.5%)] while the lowest, records in the studies which use only direct
6 method [3.8% (95% CI=1.5 to 6.2%)]. Chi2 test was highly significant (p<0.001) and I2 statistic
7 was 99.88%, indicating high heterogeneity in the results of the included studies.

8 3.3.1. IPs species-specific pooled prevalence

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9 Sub-group analysis also revealed that pooled prevalence estimates for the intestinal protozoa

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10 and helminths were 20% (95% CI=13.7 to 26.3%) and 1.6% (95% CI=1.1 to 2.0%), respectively.
11 For intestinal protozoa, G. lamblia (5.2%, 95% CI=4.3 to 6.1%), Entamoeba coli (5.0%, 95%
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12 CI=4.2 to 5.9%), and Blastocystis spp. (4.4%, 95% CI=3.1 to 5.8%) were the most prevalent
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13 species. In terms of helminthic agents, the most prevalent species were A. lumbricoides [1.4%
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14 (95% CI=0.8 to 1.9%)] followed by Enterobius vermicularis [(0.9%, 95% CI=0.3 to 1.5%)] and
15 Hymenolepis nana [(0.5%, 95% CI=0.3 to 0.7%)] (Table 3).
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16 3.4. Publication bias, sensitivity and meta-regression analyses

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17 Symmetrical funnel plot visual inspection (Fig. 3) showed absence of publication bias, which
18 was statistically verified by Egger’s test (p=0.16). Sensitivity analysis was carried out by
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19 excluding each study step-by-step from the meta-analysis and comparing the point prevalence
20 estimates before and after removing a single study. Removing a single study did not alter the
21 pooled prevalence estimate considerably, with sensitivity analysis ranging from 17.40% [when
22 (Fallah et al., 2004) was removed] to 20.03% [when (Salary and Safizadeh, 2013) was removed]
23 (Fig. 4). A univariate meta-regression between the infection prevalence and the year of
24 publication showed statistically significant correlations (p<0.01). However, the sample size
25 showed no statistically significant correlations (p>0.93) (Table 4).

26 3.5. Pooled odds ratio of educational level

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1 In terms of the correlation between IPs infections and educational level, food handlers with low
2 educational levels were 20% more exposed to IPs infection, compared to those with high
3 educational levels (OR=1.21, 95% CI=0.88 to 1.65) (Fig. 5).

4 4. Discussion
5 The present study was designed to provide comprehensive epidemiological information on
6 endemic species of IPs and their national and regional prevalence among food handlers in Iran
7 that will serve as a guide for a targeted and cost-effective control program.

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8 The pooled prevalence estimate (19.3%) revealed in this study is lower than the 33.6% reported
9 in Ethiopia (Yimam et al., 2020). Since there are no other available systematic reviews and

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10 meta-analysis conducted on IPs in food handlers worldwide, our study shows a lower
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prevalence compared with the primary studies conducted in Qatar (33.9%) (Abu-Madi et al.,
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12 2008) and Jordan (48.0%) (al-Lahham et al., 1990) in the Middle East. However, this is higher
13 than that of Saudi Arabia (12.8%) (Kalantan et al., 2001), Iran's southern neighbor. These
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14 variations firstly could be attributable to the fact that this study is a systematic review and
meta-analysis which combined several primary studies to estimate the pooled prevalence and
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16 secondly, differences in climatic conditions, socioeconomic conditions of the population, levels
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17 of sanitation and hygiene as well as the specificity and sensitivity of the diagnostic methods
18 employed by the individual studies may be related to the above variations.
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19 Urbanization and consequently, population density in the center of Iran may explain the higher
20 prevalence of IPs infections in this region. The higher prevalence in the north-west and south
21 regions also could be due to a lack of sanitation infrastructures and poor health education in
22 these regions.

23 Sub-group analysis based on the study period revealed a more than 37% decline in the
24 prevalence of IPs infections in Iranian food handlers during the past two decades. According to
25 the National Food Safety Standards in Iran, all food handlers should receive health certificates
26 annually. So, food handlers must go under annual microbial examination and should take part
27 in training courses regarding food safety before receive their health certificate (Nasrolahei et
28 al., 2017). It seems the dramatic decrease in IPs infections among food handlers could be

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1 attributable to promote personal hygiene practices and training courses regarding food safety
2 among food handlers.

3 The higher pooled prevalence estimates in the studies which employed concentration and
4 staining methods besides direct wet-mount reflect the fact that implementation of these
5 methods together enhanced the sensitivity of IPs detection (Garcia et al., 2018). Co-
6 implementation of these methods should be considered in the annual medical checkups of food
7 handlers in Iran.

Interestingly, sub-group analysis revealed that the prevalence of protozoan parasites was

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9 significantly higher than that of helminthic ones in food handlers in Iran. The prevalence of the

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10 intestinal helminths has decreased sharply in recent decades, compared to that of the intestinal
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protozoans, in Iran (Abbaszadeh Afshar et al., 2020; Ghadirian et al., 1973; Ghadirian et al.,
12 1972; Rokni, 2008). The high prevalence of protozoan parasites is possibly due to their high
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13 proliferation rate and also the simple route of infection via contaminated food and water
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14 (Abera et al., 2010).

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15 G. lamblia, E. coli, and Blastocystis spp. were the most protozoan species reported during the
16 period under review. Although the overall prevalence of Giardia has been declining during the
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17 past decade in Iran, it still seems relatively high depending on the target population
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18 (Abbaszadeh Afshar et al., 2020). The reported range of Blastocystis infections in Iran varies
19 from 7.5 to 28.4% (Hemmati et al., 2017; Mowlavi et al., 2008). Several studies have
20 demonstrated controversial associations between this parasite infection and clinical
21 manifestations (Matiut and Hritcu, 2015; Tan et al., 2010). The majority of individuals infected
22 with G. lamblia and Blastocystis spp. are asymptomatic and excrete numerous cysts that remain
23 viable for a long time in the environment, contaminating water and food sources. Although E.
24 coli manifests no symptoms, their presence indicates fecal-oral transmissions of infective
25 agents by food handlers. This is a good indicator of the general hygiene assessment in the
26 region. High transmission potential through food and water, and on the other hand, zoonotic
27 aspects of G. lamblia and Blastocystis spp. may explain the high prevalence of these species
28 compared with other protozoa.

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1 A. lumbricoides, E. vermicularis, and H. nana were the most predominant helminths records in
2 food handlers in Iran. The considerable prevalence of A. lumbricoides in the present study may
3 be associated with low levels of personal hygiene, environmental sanitation and resistance of
4 Ascaris eggs under extreme environmental conditions (O'lorcain and Holland, 2000). Moreover,
5 enormous numbers of eggs produced by adult female worms and the thick and sticky shells of
6 Ascaris eggs may facilitate attachment of Ascaris on human hands, fruits, and vegetables
7 (Quilès et al., 2006). Although the prevalence of human helminthic diseases has plunged in
8 recent decades throughout Iran, some of them, particularly those with direct fecal-oral

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9 transmissions, such as Enterobius and Hymenolepis, remain common (Rokni, 2008). These
parasites can easily be spread in restaurants and hotels, resulting in serious health issues.

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11 Although no significant correlations were found between the prevalence of IPs and food
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12 handler’s educational levels, results indicate that food handlers with low education levels were
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13 nearly 20% more exposed to IPs compared to those with high education levels. Educated food
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14 handlers are more aware of IPs transmissions and may use necessary measures to avoid
15 infections.
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16 The findings of the present study will be an alarm for health policymakers in Iran and could be
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17 used as a guide to design and employed a strategic and cost-effective program by targeting
18 food handlers as a super spreader population to reduce the burden of IPs in Iran. To bringing
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19 down the magnitude of IPs infections, further direct interventions are suggested as follows: a)
20 free training for food handlers to increase standards of personal hygiene during the handling,
21 preparation, and cooking food as well as informing them about how IPs are transmitted to
22 society, b) periodic check-ups of food handlers for IPs should be monitoring by the health
23 authorities, strictly, c) improving the level of public health by providing appropriate training and
24 instructions through the media, d) allocate sufficient funds by health policymakers to prevent
25 and control of IPs. We also suggest large-scale studies using standard diagnostic methods
26 among food handlers, particularly in regions such as Khorasan and Sistan and Baluchistan,
27 where information on the prevalence of IPs among food handlers are limited.

28 Limitations

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1 Despite the valuable data provided by this study, several limitations affected its findings,
2 including a) lack of literature in several regions of the country such as east and north-east
3 regions, b) uneven distribution of the studies across the regions and study period, and c) high
4 heterogeneity among the included studies, which might have resulted from variations in study
5 designs, employed diagnostic methods, and sample populations. Indeed, with these in hand, a
6 more precise picture of the current situation of IPs in food handlers in Iran could be achieved.

7 5. Conclusion
8 IPs infections are highly prevalent among food handlers in Iran, especially in the central and

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9 north-west regions. Besides taking into account the presented epidemiological information,

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10 health authorities should adopt a holistic approach, including raising public awareness about
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12 and treatment of infected food handlers.
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foodborne diseases, intensive training/retraining, health education of food service employees,
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13 Abbreviations
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14 IPs: Intestinal parasites; CI: Confidence Interval; WHO: World Health Organization; JBI: Joanna
Briggs Institute; OR: Odds ratio; PRISMA: Preferred Reporting Items for Systematic Reviews and
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16 Meta-Analyses
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17 Acknowledgments
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18 The authors acknowledge the financial support of Shiraz University of Medical sciences.
19 Declarations of interest: none.

20 Funding
21 This work is funded by Shiraz University of Medical Sciences (Grant No: 99-01-106-23117; Ethics
22 No: IR.SUMS.REC.1399.588). The funders had no role in study design, data collection and
23 analysis, decision to publish, or preparation of the manuscript.

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 Tables

Table 1 List and characteristics of the 32 eligible studies

Sample No. of Prevalence Diagnostic Risk of bias
Reference Year of study Province Region
size positive (%) method assessment
(Rouhani et al., 2000) 1994/1995 Mazandaran North 411 124 30.17 D, C Low risk
(Kheirandish et al., 2003) 2001 Lorestan West 933 123 13.18 D, C Low risk
(Fallah et al., 2004) 2003 Hamedan Center 938 713 76.01 D, C Moderate risk
(Davami et al., 2006) 2002 Markazi Center 460 201 43.70 D, C Low risk
(Neghab et al., 2006) 2002 Fars South 39 23 58.97 D, C High risk
(Garedaghi and Mashaei, 2011) 2009 East-Azerbaijan North-west 300 78 26.00 D, C Moderate risk
(Kheirandish et al., 2011) 2010 Lorestan West 816 96 11.76 D, C, S(t) Low risk
(Koohsar et al., 2012) 2010 Golestan North 500 30 6.00 D, C Low risk

f
(Saki et al., 2012) 2000-2009 Khuzestan South 62007 20580 33.19 D, C, S(t) Low risk

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(Abedi et al., 2013) 2012 Sistan and Baluchestan South-east 210 53 25.24 D, C Low risk
(Amiri et al., 2013) 2011 Semnan Center 801 143 17.85 D, C Low risk
(Niazi et al., 2013) 2012 Bushehr South 203 18 8.87 D, C Low risk

r
(Salary and Safizadeh, 2013) 2010 Kerman South-east 7748 96 1.24 D Low risk
(Kheirandish et al., 2014)
(Balarak et al., 2014)
2011
2014
Lorestan
Qom
-pWest
Center
210
2925
19
112
9.05
3.83
D,C, S(t)
D
Low risk
Low risk
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(Garedaghi and Firouzivand, 2014) 2013 East-Azerbaijan North-west 100 72 72.00 D, C, S(t) Moderate risk
(Halakou, 2014) 2013 Golestan North 100 1 1.00 D, C, S(r) Low risk
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(Zarezadeh and Malakotian, 2014) 2011/2012 Kerman South-east 450 66 14.67 D, C Low risk
(Sharif et al., 2015) 2011/2012 Mazandaran North 1041 161 15.47 D, C, S(z&t) Low risk
(Motazedian et al., 2015) 2016 Fars South 1021 106 10.38 D, C Low risk
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(Balarak et al., 2016) 2014 East-Azerbaijan North-west 4612 172 3.73 D Low risk
(Safi et al., 2016) 2012/2013 Khuzestan South 27058 2325 8.59 D, C Low risk
(Dargahi et al., 2016) 2015 Tehran Center 109 69 63.30 D, C Low risk
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(Beiromvand et al., 2017b) 2015 Khuzestan South 480 12 2.50 D, C Low risk
(Hooshyar et al., 2017) 2015 Isfahan Center 3653 47 1.29 D, C Low risk
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(Heydari-Hengami et al., 2018) 2015 Hormozgan South 800 279 34.88 D, C, S(z&t) Low risk
(Babaei and Razmjou, 2018) 2014 Ardabil North-west 1000 31 3.10 D, C Low risk
(Hatami and Azarbarzin, 2018) 2016 Tehran Center 4072 271 6.66 D Low risk
(Khodabakhsh Arbat et al., 2018) 2017/2018 Isfahan Center 1018 104 10.22 D, C Low risk
(Mohammadzadeh et al., 2018) 2016 East-Azerbaijan North-west 87 16 18.39 D, C, S(t) Moderate risk
(Shahnazi, Sadeghi, et al., 2019) 2016 Qazvin Center 1530 82 5.36 D, C, S(t) Low risk
(Shahnazi, Abdollahpour, et al., 2019) 2016 Kurdistan West 1530 92 6.01 D, C, S(t) Low risk
D: Direct wet-mount, C: Concentration, S: Staining (t: Trichrome, z: Ziehl-Neelsen, and r: Rapid Safranin)

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Table 2 Pooled prevalence estimates for IPs infection in Iranian food handlers stratified according to sub-groups
Variables No. of Pooled prevalence estimates Heterogeneity
2
studies Sample size Positives Prevalence (95% CI) I (%) Q-p
Region
Center 9 15506 1742 24.6 (17.3 to 31.8) 99.7 < 0.001
North 4 2052 316 13.0 (3.4 to 22.6) 98.4 < 0.001
North-west 5 6069 369 22.1 (15.1 to 29.1) 98.7 < 0.001
South 7 91608 23343 21.5 (9.0 to 34.5) 99.9 < 0.001
South-east 3 8408 215 13.5 (0.1 to 26.8) - -
West 4 3489 330 10.0 (6.0 to 14.0) 93.0 < 0.001
Study period
1994-2000 1 411 124 - - -
2001-2005 5 64377 21640 44.6 (26.0 to 63.3) 99.6 < 0.001
2006-2010 4 9364 300 10.9 (3.5 to 18.3) 98.4 < 0.001
2011-2015 17 44773 3686 14.5 (11.9 to 17.1) 99.1 < 0.001
2016-2020 5 8237 565 7.4 (5.7 to 9.1) 85.7 < 0.001

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Sample size

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30-500 14 3659 782 26.1 (18.4 to 33.9) 98.6 < 0.001
501-1000 6 5288 1385 26.1 (6.6 to 45.6) 99.8 < 0.001
1001-1500 3 3080 371 12.0 (8.8 to 15.2) - -

r
1501-2000
>2000
Diagnostic method
2
7
3060
112075
174
23603
-p 5.7 (4.8 to 6.5)
8.4 (0.9 to 17.6)
-
99.9
-
< 0.001
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D 4 19357 651 3.8 (1.5 to 6.2) 98.7 < 0.001
D and C 18 39584 4266 22.0 (17.4 to 26.5) 99.6 < 0.001
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D, C, and S 10 68221 21398 20.4 (9.3 to 31.5) 99.8 < 0.001

Risk of bias
Low 27 125703 26003 16.5 (11.8 to 21.3) 99.8 < 0.001
na

Medium 4 1420 289 32.1 (12.4 to 51.8) 98.2 < 0.001

High 1 39 23 - - -
Overall 32 127162 26315 19.3 (14.9 to 23.7) 99.8 < 0.001
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2
D: Direct wet-mount, C: Concentration, S: Staining, CI: Confidence interval, I : Inverse variance index, Q-p: Cochran’s p-value
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14
Table 3 Species-specific pooled prevalence estimates for IPs in Iranian food handlers
Parasite No. of Pooled prevalence estimates Heterogeneity
studies Sample size Positives Prevalence (95% CI) I2 (%) Q-p
Protozoa 32 127062 9445 20 (13.7 to 26.3) 99.9 < 0.001
Giardia lamblia 30 126975 6013 5.2 (4.3 to 6.1) 98.2 < 0.001
Entamoeba coli 24 52562 1230 5.0 (4.2 to 5.9) 98.0 < 0.001
Entamoeba histolytica/dispar 16 107218 1190 1.0 (0.6 to 1.4) 98.0 < 0.001
Blastocystis spp. 15 11346 508 4.4 (3.1 to 5.8) 96.7 < 0.001

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Iodamoeba bucheli 11 9403 165 1.5 (0.9 to 2.1) 92.4 < 0.001

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Endolimax nana 9 7575 101 1.1 (0.6 to 1.6) 90.4 < 0.001
Chilomastix mesnili 6 3904 55 1.3 (0.4 to 2.2) 88.9 < 0.001
Dientamoeba fragilis 3 2756 72 2.7 (0.0 to 5.6) 96.3 < 0.001

r
Entamoeba hartmanni
Cryptosporidium spp.
2
1
1739
1041
-p106
5
2.9 (2.1 to 3.6)
-
-
-
< 0.001
-
re
Helminths 26 113819 1922 1.6 (1.1 to 2.0) 98.3 < 0.001
Hymenolepis nana 23 108907 988 0.5 (0.3 to 0.7) 95.6 < 0.001
Ascaris lumbricoides 12 77273 771 1.4 (0.8 to 1.9) 98.2 < 0.001
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Taenia spp. 9 8854 24 0.2 (0.1 to 0.3) 0.00 0.878

Enterobius vermicularis 4 29207 92 0.9 (0.3 to 1.5) 92.5 < 0.001
na

Trichostrongylus spp. 3 1849 14 0.1 (0.0 to 1.9) 81.0 0.005

Hookworms 3 1512 8 0.4 (0.0 to 0.8) 43.7 0.169
Strongyloides stercoralis 2 1349 11 0.2 (0.1 to 0.4) - 0.151
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Trichuris trichiura 1 938 8 - - -

2
CI: Confidence interval, I : Inverse variance index, Q-p: Cochran’s p-value
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Table 4 Univariate meta-regression of factors related to the heterogeneity of IPs in Iranian food handlers
Variables Coefficient p-value
Year of publication -.0196238 0.010
Sample size 2.73e-07 0.935

15
Figures

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Fig. 1 PRISMA flowchart diagram for the selection process of eligible studies

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Fig. 2 Forest plot showing the pooled prevalence of IPs in Iranian food handlers

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Fig. 3 Funnel plot displaying the prevalence estimate of IPs in Iranian food handlers

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Fig. 4 Sensitivity analysis of included studies to determine the pooled prevalence estimate
of IPs in Iranian food handlers
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Fig. 5 Forest plot for pooled odds ratio (log scale) of correlation between educational level
and IPs infection in Iranian food handlers. OR: Odds Ratio

20
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Highlights
• We estimate the pooled prevalence of intestinal parasites (IPs) in food handlers of
foodservice establishments in Iran.

• Our analysis revealed 19.3% (95% CI = 14.9 to 23.7%) of IPs infection in food handlers
across the country.

• Giardia lamblia, Entamoeba coli, and Blastocystis spp., were the most commonly
reported protozoan species.

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• Ascaris lumbricoides, Enterobius vermicularis, and Hymenolepis nana were the most

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commonly reported helminthic species.

• -p
IPs infections are highly prevalent among food handlers in Iran, especially in the central
regions.
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YFMIC 103703

Conflicts of Interest Statement

Journal: Food microbiology

Manuscript title: Intestinal parasites among food handlers in Iran: A systematic review and
meta-analysis

The authors whose names are listed immediately below certify that they have NO affiliations
with or involvement in any organization or entity with any financial interest (such as honoraria;
educational grants; participation in speakers’ bureaus; membership, employment, consultancies,
stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements),

of
or non-financial interest (such as personal or professional relationships, affiliations, knowledge

ro
or beliefs) in the subject matter or materials discussed in this manuscript.

Authors name:
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1. Aref Teimouri
2. Hossein Keshavarz
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3. Sina Mohtasebi
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4. Fatemeh Goudarzi
5. Fattaneh Mikaeili
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6. Alireza Borjian
7. Mahya Allahmoradi
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8. Yonas Yimam
9. Mohammad Javad Abbaszadeh Afshar (Corresponding author)