Acta Tropica 169 (2017) 69–83

Contents lists available at ScienceDirect

Acta Tropica

jo urnal homepage: www.elsevier.com/locate/actatropica

Intestinal parasitic infections in Iranian preschool and school

children: A systematic review and meta-analysis

a,d b a,e

Ahmad Daryani , Saeed Hosseini-Teshnizi , Seyed-Abdollah Hosseini ,

c a,d a a

Ehsan Ahmadpour , Shahabeddin Sarvi , Afsaneh Amouei , Azadeh Mizani ,

d a,d,∗

Sara Gholami , Mehdi Sharif

a

Toxoplasmosis Research Center, Mazandaran University of Medical Sciences, Sari, Iran

b

Paramedical School, Hormozgan University of Medical Science, Bandar Abbas, Iran

c

Infectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

d

Department of Parasitology and Mycology, Sari Medical School, Mazandaran University of Medical Sciences, Sari, Iran

e

Student Research Committee, Mazandaran University of Medical Sciences, Sari, Iran

a r t i c l e i n f o a b s t r a c t

Article history: Parasitic infections are a serious public health problem because they cause anemia, growth retardation,

Received 31 December 2015

aggression, weight loss, and other physical and mental health problems, especially in children. Numerous

Received in revised form

studies have been performed on intestinal parasitic infections in Iranian preschool and school children.

10 December 2016

However, no study has gathered and analyzed this information systematically. The aim of this study was

Accepted 19 January 2017

to provide summary estimates for the available data on intestinal parasitic infections in Iranian children.

Available online 24 January 2017

We searched 9 English and Persian databases, unpublished data, abstracts of scientific congresses during

1996–2015 using the terms intestinal parasite, Giardia, Cryptosporidium, Enterobiusvermicularis, oxyure,

Keywords:

school, children, preschool, and Iran. We conducted meta-analysis using STATA, and for all statistical tests,

Intestinal parasites

Preschool p-value less than 0.05was considered significant. Among the 68,532 publications searched as a result, 103

School were eligible for inclusion in the study. The prevalence rate of intestinal parasitic infections was 38% (95%

Children CI- 33%, 43%). Prevalence of protozoa, helminthic intestinal infections, and non-pathogenic parasites was

Iran 16.9%, 9.48%, and 18.5%, respectively, which affected 14.27% males and 15.3% females. The rate of infec-

Systematic review

tion in preschool and school children was 38.19% and 43.37% respectively. Giardia, Enterobiusvermicularis

Meta-analysis

and Entamoeba coli were the most common among protozoa, helminthic, and non-pathogenic infec-

tions (15.1%, 16.5%, and 7.1%, respectively). The data analyses indicated that the prevalence of intestinal

parasitic infection is decreasing in Iranian preschool and school children. Improvement of sanitation, per-

sonal hygiene, increased awareness of people, seasonal variations, and health education can be effective

in reducing parasitic infections in different communities.

© 2017 Published by Elsevier B.V.

Contents

1. Introduction ...... 70

2. Material and methods ...... 70

2.1. Search strategy and data extraction ...... 70

2.2. Statistical analysis ...... 70

3. Results...... 70

4. Discussion ...... 73

5. Conclusions ...... 80

Acknowledgments ...... 80

References ...... 80

∗

Corresponding author at: Parasitology and Mycology Dept, Toxoplasmosis Research Center (TRC), Mazandaran University of Medical Sciences, 18th Km of Khazar Abad

Road, Sari, Mazandaran Province, Iran.

E-mail address: [email protected] (M. Sharif).

http://dx.doi.org/10.1016/j.actatropica.2017.01.019

0001-706X/© 2017 Published by Elsevier B.V.

70 A. Daryani et al. / Acta Tropica 169 (2017) 69–83

1. Introduction

68532 papers from 9 databases P roceedings of Iranian medical (PubMed, Scopus, Science Direct, congresses were searched

Google Scholar Magiran, Iran Medex,

Intestinal parasitic infections (IPIs) are a health problem in manually.

IranDoc and SID) were identified.

most countries, especially so in developing countries. The infec-

tions cause iron deficiency anemia, growth retardation in children,

weight loss, abdominal pain, dyspepsia, and other physical and 68438 studies that did not deal

with prevalence of intestinal

mental health problems (Norhayati et al., 2003; WHO, 2008;

parasite in preschool and school

9 scientific congress articles were Schmunis and López Antunano,˜ 2010). children were excluded along

included.

According to a WHO report, 3.5 billion people are affected, with duplicate papers.

and 450 million are sick because of parasitic infections, of

which the majority is children. Of the total annual mortalities in

developing countries, parasitic diseases accounts for 16 million

deaths. Approximately 39 million disability-adjusted life years are

attributed to IPIs and these infections represent a substantial eco- 94 studies were selected

nomic burden. Preschool and school children are easily identifiable based on topics.

target groups. IPIs are transmitted directly among children through

fecal contamination of soil and water, or indirectly through poor

sanitation (WHO, 2007; Fan et al., 2012; Stephenson et al., 2000).

Epidemiological studies around the world have shown that the

socio-economic status of the people is the main cause of prevalence

of IPIs. Moreover, poor hygiene and environmental conditions are

known to be related to the propagation of these infective diseases

Finally 103 studies that met the

(Gamboa et al., 1998; Tellez et al., 1997). eligibility criteria were approved in the

Investigation of parasitic infections can consider sanitation as current review.

an important indicator of disease prevalenceat the community level

(Phiri et al., 2000). Geographically, Iran is situated in the Middle East

and borders the Caspian Sea, Persian Gulf, and Oman Sea. Iran has

54 26 14 9

favorable conditions for the activity of various parasites because

Articles Articles articles articles

of the geographical location, climate, and biological and cultural Cryptosporidium E. vermicularis Giardia

characteristics. Intestinal Parasitic Infections

Numerous studies have been performed on IPIs in preschool and

school children from Iran. However, there is no study to gather and

Fig. 1. Flow diagram describing the study design process.

systematically analyze this information. The aim of this study was

to provide summary estimates for the available data on intesti-

nal parasitic infections in Iranian children. This study has been

Chilomastixmesnili were considered non-pathogenic protozoa, in

carried out to evaluate the prevalence of parasitic infections and

our study.

demographic data (age and sex).

The quality of selected studies was assessed using the STROBE

scale (score under 7.75 was considered as low quality; 7.76–15.5,

moderate; 15.6–23.5, moderate to high; and above 23.6, high qual-

ity).

2. Material and methods

2.2. Statistical analysis

2.1. Search strategy and data extraction

In this study, forest plots were used to estimate pool effect

We searched MEDLINE via PubMed, Scopus, Science Direct, Web

size and effect of each study with their confidence interval (CI) to

of Science (ISI), Google Scholar (as English databases); Magiran, Iran

provide a visual summary of the data. To evaluate heterogeneity

Medex, Iran Doc, and SID (as Persian databases) during 1996 to April

among studies, common approaches including the Cochran’s Q test

2015 using the terms: intestinal parasites, Giardia, Cryptosporidium,

and I-square indices were used. A significance threshold of p = 0.05

Enterobiusvermicularis (oxyure), school, children, preschool, day care,

was applied to the heterogeneity ␹2. I-squared values less than

kindergarten, Iran.

25% were defined as low heterogeneity, 25–50% as moderate, and

Owing to the high number and the importance of studies on

greater than 50% as high heterogeneity. At present heterogeneity,

Giardia, Cryptosporidium, and Enterobiusvermicularis (oxyure) in

random effects model (DerSimonian Laird model) and the other-

Iranian children, these terms also were searched with intestinal

parasites. wise applied fixed effect model (Mantel Haenszel) were used to

compute overall effect. Begg’s Funnel plot (Qualitative method)

To collect precise information, a comprehensive search was car-

and Egger’s regression test (Quantitative method) were used for

ried out on all published and unpublished articles including full

evaluating the possibility of publication bias. We conducted meta-

texts, abstracts, and parasitology congress summaries. Data were

analysis using STATA software (Intercooled, version 11, STATA Corp,

collected from articles in the English and Persian language. A pro-

College Station, TX), and for all statistical tests, p < 0.05 was consid-

tocol for data extraction was defined and assessed independently

ered significant.

by two authors. Disagreements were resolved by discussion.

Extracted data from the studies included year of the study, first

author, province of the study, total sample size, the age of samples 3. Results

(preschool or school children), and the number of male and female

subjects. Of the 68,532 publications that were gathered for this systematic

Entamoeba coli, Iodamoebabütschlii, Entamoebahartmanni, review, 103 were eligible for inclusion under intestinal parasitic

Endolimax nana, Dientamoebafragilis, Trichomonashominis and infections (Fig. 1 and Table 1).

A. Daryani et al. / Acta Tropica 169 (2017) 69–83 71

Table 1

Baseline characteristics of included studies.

Author Year Province Type of parasite Methods No. samples No. positive (%)

Ataiyan. A 1996 Zanjan IPIs Formalin-ether + Graham 2148 699 (32.54)

Bahadoran. M 1996 Isfahan IPIs Formalin-ether 1560 950 (60.89)

Fallah. M 1996 Hamedan Cryptosporidium Ziehl-Neelsen 554 30 (5.41)

Fatahi-bafghi. A 1997 Yazd IPIs Formalin-ether 900 523 (58.11)

Fazaeili. A 1997 Sistan and Balochestan IPIs Formalin-ether + Graham 947 587 (61.98)

Mozafar-ikhosravi. H 1997 Yazd IPIs Formalin-ether 1000 710 (71)

Alavi-naiini. S,M 1999 Markazi IPIs Formalin-ether 1043 637 (61.07)

Ghorbani. R 1999 Semnan IPIs Formalin-ether 359 51 (14.20)

Amiri-moghadam. Z,M 2000 Tehran IPIs Formalin-ether 180 110 (61.11)

Hamzavi. Y 2000 Kermanshah Cryptosporidium Ziehl-Neelsen 400 13 (3.25)

Kalantari. N 2000 Mazandaran IPIs Formalin-ether+ Graham 348 153(43.96)

Mahyar. A 2000 Ghazvin IPIs Formalin-ether 258 146 (56.58)

Mahyar. A 2000 Ghazvin Giardia Flotation 783 106 (13.53)

Moshfea. A 2000 Kohgiluyeh and Boyer-Ahmad IPIs Formalin-ether+ Graham 612 361(58.98)

Rafeii. M 2000 Tehran IPIs Formalin-ether 1155 179 (15.49)

Sedighian. F 2000 Mazandaran IPIs Formalin-ether 334 90 (26.94)

Shahabi. S 2000 Tehran IPIs Formalin-ether 1902 1256 (66.03)

Sharifi-mod. B 2000 Sistan and Balochestan E. vermiculars Graham test 384 122 (31.77)

Sharif. M 2000 Mazandaran E. vermiculars Graham test 217 64 (29.49)

Shirbazoo. Sh 2000 Tehran Giardia Formalin-ether 325 84 (25.84)

Baghaii. M 2001 Isfahan IPIs Formalin-ether+ Graham 650 337 (51.84)

Fani. M,J 2001 Golestan E. vermiculars Graham test 328 52 (15.85)

Forotani. M,R 2001 Fars IPIs Formalin-ether 865 395 (45.66)

Ghahramanlo. M 2001 Mazandaran IPIs Formalin-ether 3429 959 (27.96)

Mosayebi. M 2001 Markazi Cryptosporidium Ziehl-Neelsen 405 31 (7.65)

Naserifar. R 2001 Ilam Cryptosporidium Ziehl-Neelsen 979 29 (2.96)

Saeidi-jam. M 2001 hamedan IPIs Formalin-ether 906 779 (85.98)

Taherkhani. H 2001 Hamedan IPIs Formalin-ether 191 141(73.82)

Davami. M,H 2002 Markazi Giardia Formalin-ether 385 163 (42.33)

Hazrati-tappe. Kh 2002 West Azarbayjan E. vermiculars Graham test 830 294 (35.42)

Moghimi. M 2002 Kohgiluyeh and Boyer-Ahmad IPIs Formalin-ether+ Graham 300 109 (36.33)

Soud-Bakhsh. A 2002 Mazandaran Giardia Formalin-ether 1271 247 (19.43)

Talari. S,A 2002 Isfahan Cryptosporidium Ziehl-Neelsen 240 9 (3.75)

Ahmadrajabi. R 2003 Kerman IPIs Formalin-ether+ Graham 370 174 (47.02)

Dabirzade. M 2003 Sistan and Balochestan Cryptosporidium Ziehl-Neelsen 528 24 (4.54)

Farajzade. Z 2003 South Khorasan E. vermiculars Graham test 335 50 (14.92)

Gharavi. M,J 2003 Tehran IPIs Formalin-ether 211 77 (36.49)

Heidari. A 2003 Semnan IPIs Formalin-ether + Graham 461 314 (68.11)

Malaki. F 2003 Tehran Cryptosporidium Ziehl-Neelsen 500 5 (1)

Mohajeri. M 2003 RazaviKhorasan Cryptosporidium Ziehl-Neelsen 235 4 (1.7)

Samie. M 2003 Khozestan IPIs Formalin-ether 563 442 (78.5)

Taheri. F 2003 South Khorasan IPIs Formalin-ether + Graham 399 228 (57.14)

Abedi. S 2004 Isfahan E. vermiculars Graham test 252 6 (2.38)

Akbari-eidgahi. M,R 2004 Semnan Cryptosporidium Ziehl-Neelsen 153 5 (3.26)

Daryani. A 2004 Ardabil E. vermiculars Graham test 400 73 (18.25)

Davodi. S,M 2004 Sistan and Balochestan IPIs Formalin-ether + Graham 853 263 (30.83)

Kohsar. F 2004 Golestan IPIs Formalin-ether 252 104 (41.26)

Nematian, J 2004 Tehran IPIs Formalin-ether + Graham 19209 3534 (18.39)

Sobati. H 2004 Hormozgan IPIs Formalin-ether 120 33 (27.5)

Daryani. A 2005 Ardabil IPIs Formalin-ether + Graham 1070 338 (31.58)

Hazrati-tappe. Kh 2005 East Azarbayjan IPIs Formalin-ether + Graham 271 80 (29.52)

Hazrati-tappe. Kh 2005 West Azarbayjan Cryptosporidium Ziehl-Neelsen 102 3 (2.94)

Malaki. Sh 2005 Lorestan Cryptosporidium Ziehl-Neelsen 400 19 (4.75)

Molazade. P 2005 Kerman IPIs Formalin-ether 920 232 (25.21)

Taherkhani. H 2005 Hamedan E. vermiculars Graham test 776 155 (19.97)

Atashnafs. E 2006 Semnan IPIs Formalin-ether 764 104 (13.61)

Hazrati-tappe. Kh 2006 West Azarbayjan E. vermiculars Graham test 393 18 (4.58)

Khalili. B 2006 Chaharmahal and Bakhtiari Cryptosporidium Ziehl-Neelsen 618 12 (1.94)

Mohamadi-ghalehbin. B 2006 Ardabil Cryptosporidium Ziehl-Neelsen 371 15 (4.04)

Mosaviani. Z 2006 Tehran IPIs Formalin-ether 351 216 (61.53)

Atashnafs. E 2007 Semnan E. vermiculars Graham test 688 86 (12.5)

Berenji. F 2007 RazaviKhorasan Cryptosporidium Ziehl-Neelsen 100 22 (22)

Ebadi. M 2007 Yazd IPIs Formalin-ether 1500 128 (8.5)

Fallahi. Sh 2007 Lorestan Giardia Flotation 500 97 (19.4)

Khalili. B 2007 Chaharmahal and Bakhtiari Cryptosporidium Ziehl-Neelsen 171 8 (4.67)

Mohseni-moghadam. F 2007 Karman Giardia Formalin-ether 252 44 (17.46)

Nikmanesh. B 2007 Tehran IPIs Formalin-ether 420 31 (7.38)

Aazami. M 2008 Isfahan Cryptosporidium Ziehl-Neelsen 642 30 (4.67)

Aminzade, A 2008 Tehran IPIs Formalin-ether 293 139 (47.44)

Davami. M,H 2008 Fars IPIs Formalin-ether 410 63 (15.36)

Etehad. GH 2008 Ardabil Giardia Flotation 813 114 (14.02)

Ghoreishimakri. S, Gh 2008 Ghazvin Cryptosporidium Ziehl-Neelsen 1000 3 (0.3)

Soheiliazad. A,A 2008 Tehran IPIs Formalin-ether+ Graham 555 243 (44.18)

Badparva.E 2009 Lorestan E. vermiculars Graham test 598 202 (33.77)

Keshavarz-riazi. A 2009 Tehran &Ghazvin Cryptosporidium Ziehl-Neelsen 1263 31 (2.45)

Tohidi. F 2009 Golestan IPIs Formalin-ether 119 40 (33.61)

72 A. Daryani et al. / Acta Tropica 169 (2017) 69–83

Table 1 (Continued)

Author Year Province Type of parasite Methods No. samples No. positive (%)

Davodi. J 2010 East Azarbaijan Cryptosporidium Ziehl-Neelsen 50 3 (6)

Khademi. S,Z 2010 Hormozgan IPIs Formalin-ether 534 55 (10.29)

Saneiyan. H 2010 Isfahan Cryptosporidium Ziehl-Neelsen 606 28 (4.62)

Haghi-ashtiani. M,T 2011 Tehran IPIs Formalin-ether 124366 13408 (10.78)

Hazrati-tappe. Kh 2011 East Azarbayjan IPIs Formalin-ether + Graham 405 172 (42.46)

Kosha. A 2011 East Azarbayjan IPIs Formalin-ether 900 396 (44)

Taghipour. N 2011 Tehran Cryptosporidium Ziehl-Neelsen 794 19 (2.39)

Taheri. F 2011 South Khorasan IPIs Formalin-ether 2169 1034 (47.08)

Daryani. A 2012 Mazandaran IPIs Formalin-ether 1100 367 (33.36)

Ghafari. R 2012 Khozestan IPIs Formalin-ether 300 15 (5)

Momenharavi. M 2012 Isfahan IPIs Formalin-ether+ Graham 430 146 (33.95)

Rostami. M 2012 Golestan IPIs Formalin-ether 800 230 (28.75)

Abdi. J 2013 Ilam IPIs Formalin-ether 230 32 (13.91)

Aghamalaei. S 2013 Tehran Cryptosporidium Ziehl-Neelsen 2500 30 (1.2)

Akhlaghi. L 2013 Ghazvin IPIs Formalin-ether 810 141 (17.4)

Manafi. GH 2013 West Azarbayjan Giardia Flotation – PCR 720 34 (8.09)

Motevali-haghi. S,M 2013 Mazandaran E. vermiculars Graham test 800 59 (7.37)

Salehi. N 2013 Tehran Cryptosporidium Ziehl-Neelsen 2500 30 (1.2)

Anvari-tafti. M.H 2014 Yazd IPIs Formalin-ether 180 18 (10)

Asadi. M 2014 Hamedan Cryptosporidium Ziehl-Neelsen 420 2 (0.4)

Ebrahimzade. A 2014 Sistan and Balochestan E. vermiculars Graham test 907 218 (24.03)

Hajialiani. F 2014 Alborz IPIs Formalin-ether 904 172 (19.02)

Hazrati-tappe. Kh 2014 West Azarbayjan Giardia PCR 720 34 (4.7)

Hamzavi Y 2014 Kermanshah Cryptosporidium Ziehl-Neelsen 700 15 (2.14)

Mesgarian. F 2014 Golestan Cryptosporidium Ziehl-Neelsen 547 27 (4.93)

Shah-mohammadi. Z 2014 Kermanshah E. vermiculars Graham test 95 14 (14.73)

Rahimi. H 2015 Semnan IPIs Formalin-ether 811 180 (22.19)

The mean score obtained for STROBE scale was 18.41, which province (0.1%) (Tables 3 and 4). Among the helminthic infec-

indicated that the quality of studies was moderate to high (Von tions, E. vermicularis was the most common parasite (18%),with

Elm et al., 2008). the highest prevalence in Lorestan province (33.77%) and the low-

In this study, the pooled prevalence of IPIs among Iranian est in Zanjan province (1.35%). Prevalence of Hymenolepis spp. and

preschool and school children was 38.3% (95% CI: 33.2%, 43.4%). Ascaris was 1.5% (95% CI- 1.07%, 2.2%) and 0.75% (95% CI- 0.4%, 1.2%),

Among 54 studies, Ahvaz (Ghafari et al., 2012) and Hamadan respectively. The highest and lowest prevalence of Hymenolepis spp.

(Saeidi-jam and Sajadi, 2001) provinces had the lowest (5%) and was reported from Sistan and Balochestan (9.55%) and Ilam (0%)

highest (86%) prevalence rates of IPIs, respectively (Fig. 2 and provinces, respectively (Tables 3 and 5).

Table 1). Heterogeneity was observed among the studies related to IPIs,

The pooled estimation of the prevalence of Giardia was 16% (95% Giardia, Cryptosporidium, and E.vermicularis. The results of subgroup

CI: 14%, 18%). analysis showed that except for Cryptosporidium, sex and age were

The results of random-effects meta-analysis showed that preva- the two main causes of heterogeneity in this meta-analysis. The

lence of Cryptosporidium spp. was 3% (95% CI: 0.03%, 7%). However, results of Egger’s test showed that there was a strong publica-

in a study on cancer patients, the prevalence of this parasite was tion bias for studies on IPIs caused by Cryptosporidium and Giardia

22% (Fig. 3, Fig. 4 and Table 2). (p < 0.001), but not for those caused by E. vermicularis (p = 0.18)

The pooled estimation of the prevalence of E. vermicularis was (Table 6).

18% (95% CI: 15%, 20%) (Fig. 5 and Table 2). According to the subgroup analysis of 50 studies that had sex

In this study, the prevalence of protozoa, helminths, and non- data, there was a significant relationship between sex and preva-

pathogenic parasites was 16.9% (95% CI- 14%, 20%), 9.48% (95% lence of IPIs (p < 0.001). The prevalence of IPIs in females (30.9%)

CI- 6.82%, 12.54%), and 18.5% (95% CI- 14.3%, 23.2%), respectively. was significantly higher than in males (16.5%).

The highest prevalence rate of IPIs was reported from Hamadan Moreover, according to subgroup analysis on 31 studies that had

province (83.86%), and the lowest was reported from Tehran age data, the prevalence of IPIs in preschool children (43.7%) was

province (12.91%) (Fig. 6 and Table 3). significantly higher than that in school children (18.8%) (p < 0.001)

Giardia was the most common parasite among the proto- (Table 7).

zoan infections (16%). The highest prevalence was from the South In our study, there was no significant relationship between

Khorasan province (30.14%), and the lowest was from the West- prevalence of Giardia and the sex of the children (in 50 studies

ern Azerbaijan province (4.72%). Prevalence of Cryptosporidium that had analyzed sex data); however, there was a significant rela-

spp., Blastocystishominis, and Entamoebahistolytica was 3%, 7%, and tionship between the prevalence of Giardia and age (12 studies

0.47%, respectively. The highest prevalence of Cryptosporidium was comprising age data were analyzed). In addition, the prevalence

in Razavi Khorasan province (7.76%) and the lowest in Tehran

Table 2

The prevalence rate of intestinal parasitic infections, Giardia, Cryptosporidium and E. vermicularis in Iranian children during 1996–2015.

Key words of search strategy No. studies No. Studies of IPIs that properly reported Giardia, Total studies for analysis Prevalence (95% CI)

Cryptosporidium and E.vermicularis

IPIs 54 – 54 38% 33.2–43.4

Giardia 9 54 63 16% 14–18

Cryptosporidium 26 0 26 3% 0.3–7

E. vermicularis 14 17 31 18% 15–20

A. Daryani et al. / Acta Tropica 169 (2017) 69–83 73

Fig. 2. Forest plot of prevalence of Intestinal parasitic infections in Iranian Children.

Each square represents the effect size (ES) for each individual study. Their 95% confidence interval (95% CI) for prevalence is reflected by the size of each square proportional

to the weight assigned (%Weight) to each study within the meta-analysis. The diamond represents the overall pooled. The vertical dash line represents overall estimate and

the vertical solid line represents value of null hypothesis.

rate of Giardia in school children (14.2%) was higher than that in Trichostrongylus spp. and Strongyloides stercoralis were rarely

preschool children (8%) (Table 7). found in Iranian school children. However, in Mazandaran province,

Data analysis in our study showed that there was no significant prevalence rate of these parasites was 1.7% and 1.2%, respectively.

relationship between the prevalence of Cryptosporidium and the sex Data analysis indicates that prevalence of IPI decreased in Ira-

of the children (8 studies comprising sex data were analyzed) and nian preschool and school children during January 1996–April 2015

age groups (12 studies comprising age data were analyzed). (Fig. 7).

Our analysis of 30 studies that included age data showed that

the prevalence of E. vermicularis in preschool children (10.0%) was

4. Discussion

significantly higher than that in school children (6.4%). Moreover,

analysis of 13 studies comprising sex data showed that the preva-

This systematic review and meta-analysis will be beneficial for

lence in males (14.4%) was significantly higher than that in females

understanding the situation of IPIs in Iranian children. This study

(8.9%) (p = 0.003) (Table 7).

estimated the prevalence rate of IPIs in this group, using the docu-

In the present study, the overall prevalence of A. lumbricoides

mented data from the literature reviews, which have been gathered

was 0.75%, T. trichiura 0.12%, and Hymenolepis spp. 1.5%.

from different provinces of Iran.

74 A. Daryani et al. / Acta Tropica 169 (2017) 69–83

Fig. 3. Forest plot of prevalence of cryptosporidium in Iranian Children.

Each square represents the effect size (ES) for each individual study. Their 95% confidence interval (95% CI) for prevalence is reflected by the size of each square proportional

to the weight assigned (%Weight) to each study within the meta-analysis. The diamond represents the overall pooled. The vertical dash line represents overall estimate and

the vertical solid line represents value of null hypothesis.

Table 3

The prevalence rates of protozoa (pathogen and non-pathogen) and helminthes in Iranian children by province.

Province No. Samples Intestinal Parasites

Protozoa Helminthes

Pathogen (%) Non-pathogens (%) Pathogen (%)

Alborz 904 68 (7.5) 97 (10.7) 21 (2.3)

Ardabil 1070 152 (14.2) 170 (15.8) 16 (1.4)

Eastern Azarbayjan 1576 279 (17.7) 286 (18.1) 123 (7.8)

Fars 1275 333 (26.1) 521(40.8) 122 (9.5)

Ghazvin 1068 112 (10.4) 372 (34.8) 17 (1.5)

Golestan 1171 161 (13.7) 260 (22.2) 57 (4.8)

Hamadan 1097 233 (21.2) 1026 (93.5) 578 (52.6)

Hormozgan 654 42 (6.4) 42 (6.4) 13 (1.9)

Isfahan 2640 443 (16.7) 571 (21.6) 340 (12.8)

Kerman 370 66 (17.8) 102 (27.5) 87 (23.5)

Khozestan 863 143 (16.5) 159 (18.4) 31 (3.5)

Kohgiluyeh and Boyer-Ahmad 912 252 (27.6) 343 (37.6) 119 (13)

Mazandaran 4877 898 (18.4) 367 (7.5) 282 (5.7)

Semnan 2395 294 (12.2) 222 (9.2) 222 (9.2)

Sistan and Balochestan 1800 430 (23.8) 1041 (57.8) 448 (24.8)

Southern Khorasan 2568 774 (30.1) 411 (16) 274 (10.6)

Tehran 148642 10071 (6.7) 8460 (5.6) 2068 (1.3)

Yazd 3580 622 (17.3) 867 (24.2) 263 (7.3)

Zanjan 2148 435 (20.2) 275 (12.8) 91(4.2)

After searching through 9 databases, unpublished data, and and cultural habits, as well as the region’s historical and geo-

abstracts of scientific congresses, 103 articles were included in the graphical characteristics. In meta-analysis has been carried out, the

study. According to our results, the prevalence rate of IPIs among prevalence of IPIs differs in various provinces. Hamadan province

Iranian children was 38% during January 1996–April 2015. reported the highest (83.86%) prevalence rate of IPIs. Studies car-

Epidemiologic studies in different countries showed a corre- ried out in Hamadan province a couple of decades ago indicated

lation between the prevalence rate of IPIs and personal, social, that the level of sanitation was low, both at the individual, as well

A. Daryani et al. / Acta Tropica 169 (2017) 69–83 75

Table 4

The prevalence rates of major protozoa in Iranian children by province.

Province Giardia Cryptosporidium Entamoeba(histolytica/dispar)Reference

No. Pos. (%) No. Pos. No. Pos.

(%) (%)

Alborz 904 68 ND ND 904 0 Hajialiani et al. (2014)

(7.5) (0)

Ardabil 1883 266 (14.1) 371 15 1070 0 Daryani and Ettehad (2005); Etehad (2008);

(4.1) (0) Mohammadi ghalehbin et al. (2006)

Chaharmahal and Bakhtiari ND ND 789 20 ND ND Khalili et al. (2006); Khalili et al. (2007)

(2.5)

Eastern Azarbayjan 900 79 (8.7) 50 3 (6) 900 0 Kosha et al. (2011); Davodi et al. (2010)

(7.6) (0)

Fars 1275 211 ND ND 1275 51 Davami et al. (2008); Forotani and Rezaiyan

(16.5) (4) (2001)

Ghazvin 1851 217 (11.7) 1469 15 1068 0 Akhlaghi et al. (2013); Keshavarz-riazi et al.

(0.1) (0) (2010); Ghoreishimakri et al. (2008); Mahyar

and Hadiloo, (2000); Mahyar et al. (2000)

Golestan 1171 153 (13.1) 547 27 1171 8 Fani et al. (2001); Kohsar et al. (2004);

(4.9) (0.6) Mesgarian et al. (2014); Rostami et al. (2012);

Tohidi and Qorbani (2009)

Hamedan 1097 226 (20.6) 974 32 1097 4 Asadi et al. (2014); Fallah and Haghighi (1996);

(3.2) (0.3) Saeidi-jam and Sajadi (2001); Taherkhani

(2001)

Hormozgan 654 40 ND ND 654 0 Khademi and Arman (2010); Sobati and

(6.1) (0) Mobedi (2004)

Ilam 230 27 (13.7) 979 29 230 7 Abdi et al. (2013); Naserifar and Khosravi

(2.9) (3.1) (2001)

Isfahan 2640 417 (15.7) 1488 67 2640 19 Aazami and Dorostkar-Moghadam (2008);

(4.5) (0.7) Baghaii et al. (2001); Bahadoran et al. (1996);

Momenharavi et al. (2012); Saneiyan et al.

(2010); Talari et al. (2002)

Kerman 1542 246 (15.9) ND ND 1290 0 Ahmadrajabi et al. (2003);

(0) Mohseni-moghadam et al. (2007); Molazade

and Rahimi (2005)

Kermanshah ND ND 1100 28 ND ND Hamzavi (2000); Hamzavi et al. (2014)

(2.5)

Khozestan 863 138 (15.9) ND ND 863 5 Ghafari et al. (2012); Samie et al. (2003)

(0.5)

Kohgiluyeh and Boyer-Ahmad 912 252 (27.6) ND ND 912 0 Moghimi and Sharifi (2002); Moshfea and

(0) Sharifi (2000)

Lorestan 500 97 (19.4) 400 19 ND ND Fallahi et al. (2007); Malaki et al. (2005)

(4.7)

Markazi 1428 115 (8.1) 405 31 1043 25 Alavi-naiini and Davari (1999); Davami et al.

(7.6) (2.4) (2002); Mosayebi and Eslami-Rad, (2001)

Mazandaran 6482 1191 ND ND 5211 9 Daryani et al. (2012); Ghahramanloo et al.

(18.3) (0.1) (2001); Kalantari and Mobadi (2000);

Sedighian et al. (2000); Soud-Bakhsh et al.

(2002)

Razavi Khorasan ND ND 335 26 ND ND Berenji et al. (2007); Mohajeri et al. (2003)

(7.7)

Semnan 2395 281 153 5 2395 12 Akbari-eidgahi et al. (2004); Atashnafs et al.

(11.7) (3.2) (0.5) (2006); Ghorbani et al. (1999); Heidari and

Rokni (2003); Rahimi et al. (2015)

Sistan and Balochestan 1800 330 (18.3) 528 24 1800 58 Dabirzade et al. (2003); Davodi et al. (2004);

(4.5) (3.2) Fazaeili et al. (1997)

Southern Khorasan 2568 774 (30.1) ND ND ND ND Taheri et al. (2011); Taheri and Saadatjoo

(2003)

Tehran 148967 9665 (6.4) 131874 142 148642 357 Amiri-moghadam and Khansari (2000);

(0.1) (0.2) Gharavi et al. (2003); Malaki and Hasani

(2003); Aminzade and Hosseinzadeh (2008);

Haghi-ashtiani et al. (2011); Mosaviani (2006);

Nematian et al. (2004); Keshavarz-riazi et al.

(2010); Aghamalaei et al. (2013); Rafiei et al.

(2000); Shahabi (2000); Soheiliazad et al.

(2008); Shirbazoo and Aghamiri (2000); Salehi

et al. (2013); Taghipour et al. (2011)

Western Azarbayjan 2116 199 102 3 ND ND Hazrati-tappe et al. (2011); Hazrati-tappe et al.

(9.4) (2.9) (2005b); Hazrati-tappe et al. (2014); Manafi

et al. (2013)

Yazd 3580 503 (14.1) ND ND 2080 65 Anvari-Tafti et al. (2014);; Ebadi et al. (2007);

(3.1) Fatahi-bafghi (1997); Mozafar-iKhaosravi and

Dehgani (1997)

Zanjan 2148 433 (20.1) ND ND 2148 2 Ataiyan et al. (1996) (0.9)

76 A. Daryani et al. / Acta Tropica 169 (2017) 69–83

Iran) seems to be because of advances in public health measures

than in other provinces, especially those in drinking water purifi-

cation, as well as measures for control and treatment programs

%

against parasitic diseases.

The prevalence of IPIs is different in neighboring and other coun-

Giardia ES ( 95% CI) Weight

tries. For example, prevalence is 47.6% in Afghanistan (Gabrielli

et al., 2005), 42.5% in Syria (Al-kafri and Harba, 2009), 31.8–37.2%

in Turkey (Okyay et al., 2004), and 27% in Egypt (El-Soud et al.,

2009). The reasons for these differences could be socio-economic

Overall (I-squared = 98.9%, p = 0.000) 0.16 (0.14, 0.18) 100.00

status, poor hygiene and sanitary facilities, weather, climate and

environmental factors, as well as inappropriate drinking water.

Data analysis in our study showed that the prevalence of IPIs

NOTE: Weights are from random effects analysis

in females (30.9%) was significantly higher than in males (16.5%)

-.177 0 .177 (p < 0.001), which is in sharp contrast to a study carried out by

Gelaw et al. (2013). This is likely due to different behavioral patterns

as well as gender-based differences in females and males. Females

Fig. 4. Estimate of prevalence of Giardia based on 63 studies in different years and

usually favor eating raw salads. They also cook vegetables that may

areas in Iran. The pooled random effect size (ES) and 95% confidence interval (95%

be contaminated with parasitic cysts and eggs.

CI) represents by diamond. Overall heterogeneity was showed by I-squared (98%,

p = 0.000). The vertical dash line represents overall estimate and the vertical solid In the present study, the prevalence of IPIs in preschool children

line represents value of null hypothesis. was (43.7%), which was significantly higher than that in school chil-

dren (18.8%) (p < 0.001). This result is in contrast to that from other

studies (Jayarani et al., 2014; Workneh et al., 2014). The reason

as at the societal level. In addition, people were using human feces

could be increased person-to-person contact in preschool children

as agriculture fertilizer (manure), which was responsible for the

as well as lack of personal hygiene.

transmission of parasites (cysts and eggs of parasites) through con-

According to information obtained from the study, the overall

taminated vegetables. Moreover, in rural areas, animal feces were

prevalence rate of parasitic protozoan infections was 16.9%, with

used as a fuel in the winter, which was responsible for the trans-

Giardia lamblia (16%) having the highest prevalence. Other stud-

mission of zoonotic parasites.

ies that investigated intestinal infections in developing countries

The lowest prevalence was observed in Tehran province

reported similar findings (Okyay et al., 2004; El-Soud et al., 2009).

(12.91%). The low rate of IPIs in Tehran province (the capital of

Fig. 5. Forest plot of prevalence of E. vermicularis in Iranian Children. Each square represents the effect size (ES) for each individual study. Their 95% confidence interval (95%

CI) for prevalence is reflected by the size of each square proportional to the weight assigned (%Weight) to each study within the meta-analysis. The diamond represents the

overall pooled. The vertical dash line represents overall estimate and the vertical solid line represents value of null hypothesis.

A. Daryani et al. / Acta Tropica 169 (2017) 69–83 77

Fig. 6. prevalence rate of IPIs in different provinces of Iran.

50 45 40 35 30 25 20 15 Infecon rat (%) 10 5

0

1996-2000 2001-2005 2006-2010 2011-2015

IPIs 46.4 27.5 25.8 11.7

Giardia 19.2 15.03 11.5 5.6

Cryptosporidium 4.5 3.63.11.6

E. vermicularis 9.02 8.4 23.7 11.54

Fig. 7. Intestinal Parasitic Infections (IPIs), Giardia, Cryptosporidium and E. vermicularis prevalence rates among Iranian preschool and school children by year.

78 A. Daryani et al. / Acta Tropica 169 (2017) 69–83

Table 5

The prevalence rates of major helminthes in Iranian children by province.

Province Enterobius Ascaric Hymenolepis Reference

No. Pos. No. Pos. (%) No. Pos.

(%) (%)

Alborz 904 21 904 0 904 0 Hajialiani et al. (2014)

(2.3) (0) (0)

Ardabil 400 73 1070 5 1070 5 Daryani et al. (2004); Daryani and Ettehad

(18.2) (0.1) (0.4) (2005)

Eastern Azarbayjan ND ND ND ND ND ND

Fars ND ND 1275 12 (0.9) 1275 99 Davami et al. (2008)

(7.7)

Ghazvin ND ND 1068 0 1068 0 Akhlaghi et al. (2013); Mahyar et al. (2000)

(0) (0)

Golestan 328 52 1171 4 1171 36 Fani et al. (2001); Kohsar et al. (2004); Rostami

(15.8) (0.3) (3.1) et al. (2012); Tohidi and Qorbani (2009)

Hamedan 776 155 (19.9) 1097 434 1097 65 Saeidi-jam and Sajadi (2001); Taherkhani and

(39.5) (5.9) Sardarian (2005); Taherkhani (2001)

Hormozgan ND ND 654 0 654 8 Khademi and Arman (2010); Sobati and

(0) (1.2) Mobedi (2004)

Ilam ND ND 230 9 (3.9) 230 0 Abdi et al. (2013)

(0)

Isfahan 1126 155 (17.1) 2640 151 (5.7) 2640 31 Abedi et al. (2004); Baghaii et al. (2001);

(1.1) Bahadoran et al. (1996); Momenharavi et al.

(2012)

Kerman 370 60 1290 7 1290 30 Ahmadrajabi et al. (2003); Molazade and

(16.2) (0.5) (2.3) Rahimi (2005)

Kermanshah 95 14 (14.7) ND ND ND ND Shah-mohammadi et al. (2014)

Khozestan ND ND 863 0 863 30 Ghafari et al. (2012); Samie et al. (2003)

(0) (3.4)

Kohgiluyeh and Boyer-Ahmad 912 102 (11.1) 912 1 912 15 Moghimi and Sharifi (2002); Moshfea and

(0.1) (1.6) Sharifi (2000)

Lorestan 598 202 (33.7) ND ND ND ND Badparva et al. (2009)

Markazi ND ND 1043 9 1043 3 Alavi-naiini and Davari (1999)

(0.8) (0.2)

Mazandaran 1365 243 5211 4 (0.07) 5211 34 Sharif and Ziaie-hezar-garibi (2000); Daryani

(17.8) (0.6) et al. (2012); Ghahramanloo et al. (2001);

Kalantari and Mobadi (2000); Sedighian et al.

(2000); Motevali-haghi et al. (2013)

Semnan 1149 242 (21.1) 2395 14 (0.5) 2395 22 Atashnafs et al. (2006); Atashnafs et al. (2007);

(0.9) Ghorbani et al. (1999); Heidari and Rokni

(2003); Rahimi et al. (2015)

Sistan and Balochestan 2144 603 (28.1) 1800 2 1800 172 Fazaeili et al. (1997); Sharifi-mod et al. (2000);

(0.1) (9.5) Ebrahimzade et al. (2014)

Southern Khorasan 734 138 2568 15 (0.5) 2568 160 Farajzade and Foroughi-Ameri (2003); Rafiei

(18.8) (6.2) et al. (2000); Taheri et al. (2011); Taheri and

Saadatjoo (2003)

Tehran 20115 1039 (5.1) 148642 211 (0.1) 148642 507 Aminzade and Hosseinzadeh (2008);

(0.3) Amiri-moghadam and Khansari (2000);

Gharavi et al. (2003); Haghi-ashtiani et al.

(2011); Mosaviani (2006); Nematian et al.

(2004); Nikmanesh et al. (2007); Rafiei et al.

(2000); Shahabi (2000); Soheiliazad et al.

(2008)

Western Azarbayjan 1899 433 676 0 676 2 Hazrati-tappe et al. (2005a); Hazrati-tappe

(22.8) (0) (0.2) et al. (2011); Hazrati-tappe et al. (2002);

Hazrati-tappe et al. (2006)

Yazd ND ND 2080 114 (5.48) 2080 102 Anvari-Tafti et al. (2014); Ebadi et al. (2007);

(4.9) Fatahi-bafghi, 1997; Mozafar-iKhaosravi and

Dehgani (1997)

Zanjan 2148 29 2148 4 2148 56 Ataiyan et al. (1996) (1.3) (0.1) (2.6)

Table 6

The result of Egger’s test to evaluation publication bias.

Parasites No. studies Co. ef Std. Err T P

Intestinal Parasitic Infections 54 0.10 0.013 7.73 <0.0001

Cryptosporidium 26 0.01 0.001 6.65 <0.0001

Giardia 63 0.048 0.004 10.49 <0.0001

E. vermicularis 31 0 0.01 0.03 1.36 0.18

Among the other countries, the prevalence rate of Giardia is 36% in 1991), 10.5% in Oman (Nimri, 1994), and 8% in Gaza Strip (Astal,

Jordan (Nimri, 1993), 22–24% in Syria (Almerie et al., 2008), 16.5% 2004).

in Turkey (C¸ eliksöz et al., 2005), 10.9% Saudi Arabia (Omar et al.,

A. Daryani et al. / Acta Tropica 169 (2017) 69–83 79

Table 7

Subgroup meta-analysis of the prevalence rates of Intestinal Parasitic Infections (IPIs), Cryptosporidium,Giardia and E. vermicularis for Sex and Age.

Parasites variable No.studies Prevalence(%) 95% CI I-squared P

Lower Upper

IPIs Age Pre-school 21 43.7 36 51.3 99% P < 0.001

School 10 18.8 17.1 40.6 99.1%

Sex Male 25 16.5 14.6 18.5 98.4% P < 0.001

Female 25 30.9 26.8 34.9 98.7%

Giardia Age Pre-school 14 8.0 7.4 8.6 90.1% P < 0.001

School 36 14.2 13.7 14.6 98%

Sex Male 6 9.4 8.3 10.6 94.5 0.819

Female 6 9.3 8.1 10.4 95.3

Cryptosporidium Age Pre-school 9 1.0 0.7 1.3 92.3 0.937

School 3 1 0 2.1 56.8

Sex Male 4 3.9 2.6 5.2 85.2 0.921

Female 4 4 2.5 5.4 62.1

E.vermicularis Age Pre-school 18 10 9.4 10.6 98.6 P < 0.001

School 12 6.4 5.9 7 99.3

Sex Male 6 14.4 10.7 12.5 98.5 0.003

Female 7 8.9 7.4 10.4 97.9

G. lamblia has a negative impact on school children’s growth (Leelayoova et al., 2004), 32% in Pakistan (Yakoob et al., 2004), 29%

and development because giardiasis causes diarrhea, malnutrition, Turkey (Dogruman-Al et al., 2010), and 25% in Jordan (Nimri, 1993).

loss of appetite etc. This problem mostly occurs in deprived and The overall prevalence rate of non-pathogenic protozoa in our

rural areas, where the drinking water supply and sewage networks study group was 18.5%. Entamoeba coli showed the highest preva-

are less developed than in advanced and urban areas(Muhsen and lence (7.1%). Iodamoebabütschlii was the second most common

Levine, 2012). In our study, there was no significant relationship non-pathogenic parasite in Iranian children (0.09%). E. hartmanni,

between prevalence of Giardia and the sex of the children; how- E. nana, D. fragilis, T. hominis, and C. mesnili are non-pathogenic pro-

ever, there was a significant relationship between prevalence of tozoa that were reported in our study. However, their prevalence

Giardia and age. The prevalence rate of Giardia in school children rates were very low. The study carried out by Walana et al. (2014) in

(14.2%) was higher than in preschool children (8%), which is simi- Ghana showed that the prevalence of E. coli, E. nana, and I. bütschlii

lar to the study done by Jayarani et al. (2014). The reason for this was 10.3%, 7%, and 1.5%, respectively.

observation may include poor environmental sanitation, low stan- The overall prevalence of helminthic infections among

dards of hygiene in schools, low family income, and greater outdoor preschool and school children in our study was 9.48%. Among

activities in school children compared with those in preschool chil- helminthic infections, E. vermicularis had the highest prevalence

dren. (18%). Studies in other countries show that the prevalence of entero-

In the present study, the overall prevalence of Cryptosporid- biasisis 38.82% in Thailand (Nithikathkul et al., 2001), 17% in Turkey

ium spp. was 3%. The prevalence rate of Cryptosporidium spp. (Celiksoz et al., 2010), 10.5% in Korea (Lee et al., 2011), 6.8% in China

in patients with lymphohematopoietic malignancies in Razavi (Wu et al., 2012), and 0.62% in Japan (Fukushima et al., 2010). The

Khorasan province was 22% (Berenji et al., 2007). These results helminths that are common in preschool children worldwide are

show that HIV positive and cancer patients are mainly at risk of cosmopolitan in distribution (Akkus¸ and Cıngıl, 2004; Beaver et al.,

cryptosporidiosis. In the current study, there was no significant 1984; C¸ ulha and Duran, 2006; Gündüz et al., 2005; Song et al.,

relationship between prevalence of Cryptosporidium and the sex 2003). Our analysis shows that the prevalence rate of E. vermicularis

or age groups. The prevalence rates of Cryptosporidium spp. are in preschool children (10.0%) was significant compared to that in

3–10.2% in Asia, Australia, Africa, and 1–2% in Central and South school children (6.4%), which is similar to that from another study

Europe (Frost et al., 2000). The major risk factor for cryptosporid- (Hong-yong, 2010). The difference observed between preschool

ium infection is drinking water that is contaminated with oocysts. and school children might be because of close contact between stu-

People at higher risk include animal handlers, people in close prox- dents as well as unhygienic conditions. Moreover, this prevalence

imity to infected persons, as well as preschool and school children in males (14.4%) was significantly higher than in females (8.9%)

(Checkley et al., 2015; Kotloff et al., 2013; Huang et al., 2004; (p = 0.003). This finding is similar to that from studies by Lee et al.

Steinberg et al., 2004). (2011). The reason may be inadequate personal hygiene, playing

Amebiasis is a serious health problem in many tropical and on the floor, nail-biting, and a failure to wash hands before meals

subtropical regions of the world, and especially so in developing in males compared to females.

countries such as Iran. According to our studies, the prevalence of Soil-transmitted helminthias is (STH) is commonly caused by

amebiasis is 0.34% in Iran. The prevalence rate of this protozoon Ascarislumbricoides, hookworms and Trichuristrichiura. STH is a

is 5.3% in Turkey (Peruzzi et al., 2006), 9.2% in Saudi Arabia (Omar public health problem, especially in the developing countries. Over

et al., 1995), 10.6% in Jordan (Battikhi, 2004), and 11% in India (Kaur one billion individuals in the world are affected by STH. School-

et al., 2002). This difference may be due to varying socio-economic going children (5–15 years) are particularly at risk (Bethony et al.,

conditions in these countries. 2006; Debalke et al., 2013). The prevalence rate of STH varies

Recently, Blastocystishominis has been considered as a potential worldwide. For example, the prevalence rate is 15.6% in Thailand

protozoan pathogen (Stenzel and Boreham, 1996; Andiran et al., (Anantaphruti et al., 2004), 43.5% in Ethiopia (Belyhun et al.,

2006; Carrascosa et al., 1996). Young age groups are at higher risk of 2010), 53% in Guinea (Glickman et al., 1999), and 88.4% in Turkey

infection, causing clinical manifestations of disease (Graczyk et al., (Ulukanligil et al., 2001). In the present study, the overall preva-

2005). In the present study, the overall prevalence rate of B. hominis lence rate of A. lumbricoides was 0.75% and that of T. trichiura was

was 3.6%, which is lesser than in other Asian countries. For exam- 0.12%. Hookworms were reported in 2 of 54 articles in our study.

ple, 40.7% in Philippines (Eleonor et al., 2004), 36.9% in Thailand Ghahramanloo et al. (2001) from Mazandaran province (north of

80 A. Daryani et al. / Acta Tropica 169 (2017) 69–83

Iran), analyzed 3429 samples of which 2 were positive. Further- Aminzade, Z., Hosseinzadeh, B., 2008. Prevalence of intestinal parasites and related

factors in primary schools children, Varamin city, Iran. In: 13th International

more, Rostami et al. (2012) from Golestan province (north of Iran)

Congress on Infectious Diseases Abstracts, Kuala Lumpur, Malaysia, pp.

found that 3 cases were positive in 800 samples. 373–374.

In our study, the prevalence rate of Hymenolepisspp. was 1.5%. Amiri-moghadam, Z., Khansari, M., 2000. Survey of intestinal parasitic infections

among primary school children Absard-area in 1996. J. Res. Med. 24, 177–190

All species were Hymenolepisnana, except for three positive cases of

(Persian).

Hymenolepisdiminuta, which were reported by Haghi-ashtiani et al.

Aazami, M., Dorostkar-Moghadam, D., 2008. Prevalence of cryptosporidium in

(2011) in Tehran. children under 5 years of age, immunocompromised patients and high risk

persons in Isfahan province. Iran. J. South Med. 11, 47–54 (Persian).

There were several limitations to the present systematic review

Abdi, J., Farhadi, M., Aghaii, S., Avazpour, M., 2013. Survey of intestinal parasitic

and meta-analysis: (i) In most studies included in this review,

infections among children referred to day cares center in Ilam, Iran. In: 16th

stool samples were prepared once, whereas for standard diagno- Environmental Health Congress in Iran, Tabriz University of Medical Sciences,

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Abedi, S., Ezadi, S., Davari, B., 2004. Prevalence of oxyuriasis in kindergartens of

is important in Blastocystis pathogenesis; however, the studies

Isfahan, Iran. J. Hormozgan Med. 8, 63–66 (Persian).

included in this review did not refer to the number of parasites.

Aghamalaei, S., Salehi, N., Kazemi, B., Abadi, A., Tahvildar-Biderouni, F., 2013.

(iii) Gram staining is the gold standard for detection of enterobiasis. Determination of sensitivity and specificity of direct fluorescent antibody

assay for the diagnosis of cryptosporidiosis in children with diarrhea. Med. Sci.

However, many studies have been conducted only using the direct

J. Islamic Azad Univ. 23, 43–48 (Persian).

method (wet smear). We have discarded these studies to determine

Ahmadrajabi, R., Varzandeh, F., Arab, M., Abbaszadeh, A., 2003. Prevalence of

E. vermicularis prevalence. (iv) Modified acid-fast staining of a fecal intestinal parasite infections in the day care centers of bam. J. Rafsanjan Univ.

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smear is the gold standard and commonly used method for detect-

Akbari-eidgahi, M., Abooei-Mehrizi, M., Amin-Beidokhti, M., Shaebani, A., 2004.

ing Cryptosporidium oocysts in stool. This method was used in most

Evaluation of cryptosporidiosis in diarrheic children referred to Amir al

of the studies included in our review (18 cases from 22 papers). The Moemenin hospital, Semnan. J. Koomesh 5, 99–104 (Persian).

Akhlaghi, L., Mafi, M., Oormazdi, H., Meamar, A., Shirbazou, S., Tabatabaie, F., 2013.

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schoolchildren and community members in a west-central border area of

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Atashnafs, E., Ghorbani, R., Peyvandi, S., Imani, S., 2007. Prevalence of oxyuriasis

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