2.1. Literature search and Search strategy
In this meta-analysis, 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 identify all the
published studies from 2000 to 31st April, 2019.
Duplicates, studies out of Iran were excluded. All original descriptive
studies (designated as cross-sectional) about intestinal parasites in
food handlers were concerned. The process is shown in Figure 1. The
search was performed using terms: “intestinal parasites”,“parasitic
infection”, “parasitic diseases”, “parasite”, “food handlers”,”
prevalence”, alone or in combination, both in Persian and
Englishlanguages.
Data collection
In the initial search of collected bibliographic references, 433 studies
were founded. After removing duplicated, irrelevant studies and studies
out of Iran, finally, 25 papers with epidemiological parameters of
interest were 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 were including:
first author, the year of publication, prevalence rate, demographic
information (age, gender), geographical region of study, diagnostic
test, sample size (number of examined people) and the number of infected
cases (Table 1).
- Quality of studyTo assess the quality of observational studies included in this
meta-analysis using a check list as in Table1. It contains 12 items
with scores “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
used to explore the effect of each study on pooled effect size.
Heterogeneity among studies assessed using both Q-test which suggestion
by the Cochrane Handbook (P<0.1 as substantial heterogeneity)
and I-square index (\(I^{2}<50\%\ \), as substantial heterogeneity).
If found that a substantial heterogeneity, sub group meta-analysis
(fixed or random effect model) performed to compute the pooled
prevalence of infection based on characteristic such as sex, country,
education, pathogen and parasite species. In addition to meta-regression
examined to find source of heterogeneity. To detect sources of
heterogeneity 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 detected a
substantially publication bias, the trim and fill method applied to
estimate and adjust for the number of missing studies (due to
publication bias) in a meta-analysis (Ebrahim ,2006). All statistical
analysis performed using Stata/MP (version 14.0, College Station, TX,
USA).
RESULTS AND DISCUSSION:
Among all eight databases searched and unpublished data from 2000 to
2019 (19 years), 25 articles were eligible to include in this systematic
review and meta-analysis. The literature searches and selection process
are shown in Figure 1. Totally
140447 cases were examined and 1163 cases were infected with intestinal
parasites. Of all examined cases,
although all studies did not define male and female genders, in studies
which defined the gender of
participants, a number of 19516
cases were male and 5901 cases were
femalewith1163 and 652 infected
cases respectively (Table 1). There was no significant difference
between infection among males 13%(10%-15%) and females 8%(5%-11%)
(P = 0.39) and in age of participants (P=0.65) (Table 2).
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 figure2. All effect sizes of
25 studies were located in 95%confidence interval (95%CI). Therefore,
none of studies substantially had effect on pooled prevalence of
intestinal infection and we can include all studies in meta-analysis
(Figure2).
The results of Egger’ test showed that there no evidence of publication
bias among studies on spices of parasite (p>0.1). Also,
there was not enough studies for assessing publication bias forDientamoeba fragilis and Trichuris trichura (Table 3).
The overall prevalence of intestinal parasitic infections in food
handlers in Iran was evaluated 14% [95%CI: 11-17%]. According to
the results of subgroup analysis, Giardia lamblia , with
prevalence of 41.0% [95%CI: 25.0%-59.0%], Blastosystis
hominis , with 28% [95%CI: 15.0%-44.0%] and Entamoaba
coli with 22.0% [95%CI: 16.0%-29.0%], had the highest
prevalence, respectively. Also, other species had the prevalence between
1.0% (Trichuris trichiura ) to 9.0% (Entamoaba histolytica
/dispar ) (Figure 3).
The subgroup analysis for intestinal protozoan parasites revealed the
prevalence of 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 3.0% [95%CI:1.0%-7.0%].
The results for intestinal helminthic infections showed thatAscaris lumbricoides with prevalence of 7.0% [95%CI:
0.0%-29.0%] had the highest prevalence and then Enterobiu
svermicularis with infection rate of 3.0% [95%CI: 1.0%-5.0%],Hymenolepis nana with 2.0%
[95%CI:1.0%-3.0%],Taenia spp with 2.0% [95%CI: 0.0%-7.0%] andTrichuris trichiura 1.0% [95%CI: 0.0%-1.0%] were the most
prevalent intestinal helminthic infections (Figure 3).The highest rate
of infection was found in owners of school cafeteria with 27.7%
followed with 11.50% in butchers and 10.17% among bakeries.The lowest
infection rate was 1.70% in confectioners (Table 4,5). The results of
our analysis indicated that frequency of intestinal parasitic infections
was in contrast with educational levels and increase of educational
level, the intestinal parasitic infection was showed a decrease process.
The prevalence of intestinal parasitic infection in individuals with
education level lower than high school, was estimated 20%
[95%CI:9.0-34.0%] (Figure 4). The prevalence of intestinal
parasitic infection in individuals with education level between high
school to bachelor of science level, was 16.0%
[95%CI:7.0%-28.0%] and in people with education higher than
bachelorof science level was reduced to 12.0% [95%CI:2.0%-28.0%]
with no statistical significant difference between them (Z=0.41, P=0.82)
(Figure4). According to the results of random effect model, infection
among male (13.0%) was more than female (8%) with statistically
significant difference between them (p=0.00) (Figure 5). The results of
meta-regression showed that the prevalence of intestinal parasitic
infectionin food handlers have significantly decreased in recent years
(p=0.01). Also, our analysis revealed that sample size had no effect on
the prevalence of intestinal parasitic infection
in food handlers (p=0.68). To
evaluate the effect of each study on the pooled prevalence, by
meta-analysis, the sensitivity of studies was shown in Figure 2. At the
first level a fixed effect meta-analysis was performed on 25 included
studies and results revealed a considerable heterogeneity
(I ^2 =99.40%, p<0.001). In
subgroup analysis, a random effect model was performed on parasite
species (Figure 3). All effect sizes of 25 studies were located with95%
interval confidence. Therefore, studies had no effect on pooled
prevalence of intestinal infections in food handlers and we can include
all studies in meta-analysis (Figure2).
Food-borne parasitic diseases are one of main public health concerns all
around the world whichmay lead to morbidity and mortality in developing
countries (Simsek et al.2009). The importance of hygienic food
preparation and delivery, revealthe importance of personal sanitation
and education. This systematic review and meta-analysis aimed to
evaluate the prevalence of intestinal parasitic infections in food
handlers in Iran during 19 years (from 2000 to 2019). The results of
meta-analysis revealed the overall prevalence of intestinal parasitic
infections was 14% [95%CI: 11-17%] in food handlers in Iran.The
results indicated thepoor healthand inadequate personal hygiene in food
handlers who are involve in food producing and food serving process in
Iran. The highest rate (72%) of infection was reported in a study
carried out in East Azarbaijan by
Garedaghi et al in 2014, and
Dargahi et al. in 2016 who
reported the rate of 59.4% in Tehran province (Garedaghi et al., 2014;
Dargahi et al., 2016). The lowest prevalence of infection (1%) was
reported from Mazandaran province by Khazan et al in 2014 (Table 1). The
sub-group analysis revealed that G. lamblia , with the prevalence
of 41.0% [95%CI: 25.0%-59.0%], B. hominis , with 28%
[95%CI: 15.0%-44.0%] and E.coli with 22.0% [95%CI:
16.0%-29.0%], had the highest prevalence among all intestinal
parasites in food handlers in Iran.The highest rate of infection
(27.7%) was achieved in owners of
school snack bars, where children
took cooked food and snacks. The results may have a bias for small
sample size, but the important point in this regard is that5 of 18
different school cafeteria owners were infected with intestinal
parasites whichis considerable. This may be resulted from weak health
controlling programs in schools. In a study carried out by Costa- Cruz
et al in Brazil, the researchers studied 20 school for the evaluation of
intestinal parasitic infections in school food handlers. They found
that, 49 of 104 (47.1%) of school food handlers were infected (Khazan
et al., 2013). Comparing their findings with ours indicates the higher
rate of infection in their studied subjects. The meta-analysis revealed
the high prevalence of intestinal parasitic infection in butchers
(11.5%) and backers (10.17%). Theses two groups play an important role
in public food health. Interestingly, the lowest prevalence of
intestinal parasitic infection rate was observed among confectioners
(1.70%). Although the sample size comprised 978 cases and relatively
big, the results indicate anappropriate personal hygiene in this group
whichis regularly monitored by health care system.
In our meta -analysis, the infection rate of 13% in men achieved while
the rate of infection among women was 8% with statistically significant
difference (p˂ 0.0001). Considering the higher rate of infection in men,
the difference may be resulted from smaller sample size in women which
is resulted from the fewer women involved in food handling than men in
Iran. In some countries the ratio of men to women wasdifferent from
ours. In a study in Thailand in 2011, Kusolsuk et al, studied 219 women
and 47 men. This is resulted from the great role of women in food
preparing and handling in Thailand. The result of their study revealed
that infection rate in 273 food handlers was 10.3% which is higher than
our results when compared with infection rate of 14% in 140447 subjects
in our study. In contrast with our results, the most infecting cases
were found with hookworms (70%) while our most prevalent helminthic
infection was with H. nana worms (Kusolsuk et al., 2013). Their
results revealed the insufficient hygiene in food preparation and our
results indicates inappropriate personalhygiene. Our meta-analysis
showed that the highest intestinal infection in food handlers were
caused by protozoan parasites and the most frequent parasite (41%) wasG. lamblia (Fig 3). These protozoa are considered one of the most
pathogenic parasites (Arora et al., 2007) which can cause acute or
chronic diarrhea with or without clinical signs. The parasite can be
transmitted directly from infected persons to the healthy individuals,
on the other hand eradication and controlling the parasite is very
difficult.It is estimated that 200 million people in Asia, Latin America
and Africa suffering from giardiasis (AL-Khayat et al., 2017).In a study
carried out by Simsek et al in 2009 in Turkey, intestinal parasitic
infection evaluated in 299 foodhandlers from Sanliurfa,Southeastern
Anatolia. The results showed that 52.2% of food handlers were infected
with intestinal parasites and most of them (26.8%) were infected withG. lamblia , fallowed withA. lumbricoides (10.7%) and T. saginata (10%). Also
13.3% of them were infected with both Staphylococcus aureus and
intestinal parasites. Unlike to our results, the infection rate withG. lamblia in their study was higher.
The meta-analysis elucidated that prevalence of intestinal parasitic
infection in individuals with education level lower than high school, to
be 20% while in individuals with education level between high school to
bachelor of science level, was 16.0% and in cases with education higher
than bachelor of science level was reduced to 12.0% but there found no
statistical significant difference (Z=0.41, P=0.82) (Figure 4). Although
the results indicated no association between intestinal parasitic
infection and educational levels, but it seems that infection rate in
individuals with lower level is higher than those with higher
educational levels. It seems that food hygiene knowledge, attitudes and
practices in food handlers play an important role in prevention of food
contamination with intestinal parasites. In a study designed by Acikel
et al in 2008, a total of 83 food handlers in kitchen were evaluated
with questionnaires for their information and behaviors before and after
training. The results indicated the significant difference in behavioral
practices and, the researchers concluded that education has an important
impact on decreasing the infection rate in food handlers. Although the
researchers studied the decreased bacterial density, it can be extended
in parasitic infections too as the way of transmission is almost same
(Acikel et al.,2008). In a study by Kheirandish et al, in 2011, out of
816 bakery workers with health certificate, 630 individuals had
knowledge about intestinal parasitic infections and the ways of
transmission but, 78(12.3%) of them were infected with intestinal
parasites. Also, 186(22.8%) of this population had no knowledge in this
regard and 19 (10.2%) individuals were infected among them. These
researchers declared that 85% of intestinal parasitic infections
observed in people who did not attend in hygiene training programs. This
shows that training in order to upgrade personal information in parasite
transmission is necessary for all food handlers. Also training hygiene
can affect the improvement of society health (Kheirandish et al., 2011).