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Acta Tropica 169 (2017) 69–83
Contents lists available at ScienceDirect
Acta Tropica
jo ur nal home p age: www.elsev ier .com/ locate /ac ta t ropica
ntestinal parasitic infections in Iranian preschool and schoolhildren: A systematic review and meta-analysis
hmad Daryania,d, Saeed Hosseini-Teshnizib, Seyed-Abdollah Hosseinia,e,hsan Ahmadpourc, Shahabeddin Sarvia,d, Afsaneh Amoueia, Azadeh Mizania,ara Gholamid, Mehdi Sharif a,d,∗
Toxoplasmosis Research Center, Mazandaran University of Medical Sciences, Sari, IranParamedical School, Hormozgan University of Medical Science, Bandar Abbas, IranInfectious and Tropical Diseases Research Center, Tabriz University of Medical Sciences, Tabriz, IranDepartment of Parasitology and Mycology, Sari Medical School, Mazandaran University of Medical Sciences, Sari, IranStudent Research Committee, Mazandaran University of Medical Sciences, Sari, Iran
r t i c l e i n f o
rticle history:eceived 31 December 2015eceived in revised form0 December 2016ccepted 19 January 2017vailable online 24 January 2017
eywords:ntestinal parasitesreschoolchoolhildren
ranystematic revieweta-analysis
a b s t r a c t
Parasitic infections are a serious public health problem because they cause anemia, growth retardation,aggression, weight loss, and other physical and mental health problems, especially in children. Numerousstudies have been performed on intestinal parasitic infections in Iranian preschool and school children.However, no study has gathered and analyzed this information systematically. The aim of this study wasto provide summary estimates for the available data on intestinal parasitic infections in Iranian children.We searched 9 English and Persian databases, unpublished data, abstracts of scientific congresses during1996–2015 using the terms intestinal parasite, Giardia, Cryptosporidium, Enterobiusvermicularis, oxyure,school, children, preschool, and Iran. We conducted meta-analysis using STATA, and for all statistical tests,p-value less than 0.05was considered significant. Among the 68,532 publications searched as a result, 103were eligible for inclusion in the study. The prevalence rate of intestinal parasitic infections was 38% (95%CI- 33%, 43%). Prevalence of protozoa, helminthic intestinal infections, and non-pathogenic parasites was16.9%, 9.48%, and 18.5%, respectively, which affected 14.27% males and 15.3% females. The rate of infec-tion in preschool and school children was 38.19% and 43.37% respectively. Giardia, Enterobiusvermicularis
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 intestinalparasitic 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.
ontents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 702. Material and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
2.1. Search strategy and data extraction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 702.2. Statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .704. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
∗ Corresponding author at: Parasitology and Mycology Dept, Toxoplasmosis Research Coad, Sari, Mazandaran Province, Iran.
E-mail address: [email protected] (M. Sharif).
ttp://dx.doi.org/10.1016/j.actatropica.2017.01.019001-706X/© 2017 Published by Elsevier B.V.
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80
enter (TRC), Mazandaran University of Medical Sciences, 18th Km of Khazar Abad
7 Tropica 169 (2017) 69–83
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Intestinal Parasitic Infections Cryptosporidium E. vermicularis Giardia
Proceed ing s of Ir anian medical congresses were searched
manually.
68532 pap ers fro m 9 da tabase s (PubMed, Scopus, Science Direct, Google Scholar Magiran, Iran Medex, IranDoc and SID) were identified.
68438 studies that did not deal with prevalence of intestinal
parasite in preschool and school children were excluded along
with duplicate papers.
9 scientific congress articles were included.
94 studies were selected bas ed on to pics.
Finally 103 studies that met the eligibility criteria were approved in the
current review .
0 A. Daryani et al. / Acta
. Introduction
Intestinal parasitic infections (IPIs) are a health problem inost countries, especially so in developing countries. The infec-
ions cause iron deficiency anemia, growth retardation in children,eight loss, abdominal pain, dyspepsia, and other physical andental health problems (Norhayati et al., 2003; WHO, 2008;
chmunis and López Antunano, 2010).According to a WHO report, 3.5 billion people are affected,
nd 450 million are sick because of parasitic infections, ofhich the majority is children. Of the total annual mortalities ineveloping countries, parasitic diseases accounts for 16 millioneaths. Approximately 39 million disability-adjusted life years arettributed to IPIs and these infections represent a substantial eco-omic burden. Preschool and school children are easily identifiablearget groups. IPIs are transmitted directly among children throughecal contamination of soil and water, or indirectly through pooranitation (WHO, 2007; Fan et al., 2012; Stephenson et al., 2000).
Epidemiological studies around the world have shown that theocio-economic status of the people is the main cause of prevalencef IPIs. Moreover, poor hygiene and environmental conditions arenown to be related to the propagation of these infective diseasesGamboa et al., 1998; Tellez et al., 1997).
Investigation of parasitic infections can consider sanitation asn important indicator of disease prevalenceat the community levelPhiri et al., 2000). Geographically, Iran is situated in the Middle Eastnd borders the Caspian Sea, Persian Gulf, and Oman Sea. Iran hasavorable conditions for the activity of various parasites becausef the geographical location, climate, and biological and culturalharacteristics.
Numerous studies have been performed on IPIs in preschool andchool children from Iran. However, there is no study to gather andystematically analyze this information. The aim of this study waso provide summary estimates for the available data on intesti-al parasitic infections in Iranian children. This study has beenarried out to evaluate the prevalence of parasitic infections andemographic data (age and sex).
. Material and methods
.1. Search strategy and data extraction
We searched MEDLINE via PubMed, Scopus, Science Direct, Webf Science (ISI), Google Scholar (as English databases); Magiran, Iranedex, Iran Doc, and SID (as Persian databases) during 1996 to April
015 using the terms: intestinal parasites, Giardia, Cryptosporidium,nterobiusvermicularis (oxyure), school, children, preschool, day care,indergarten, Iran.
Owing to the high number and the importance of studies oniardia, Cryptosporidium, and Enterobiusvermicularis (oxyure) in
ranian children, these terms also were searched with intestinalarasites.
To collect precise information, a comprehensive search was car-ied out on all published and unpublished articles including fullexts, abstracts, and parasitology congress summaries. Data wereollected from articles in the English and Persian language. A pro-ocol for data extraction was defined and assessed independentlyy two authors. Disagreements were resolved by discussion.
Extracted data from the studies included year of the study, firstuthor, province of the study, total sample size, the age of samples
preschool or school children), and the number of male and femaleubjects.Entamoeba coli, Iodamoebabütschlii, Entamoebahartmanni,ndolimax nana, Dientamoebafragilis, Trichomonashominis and
Fig. 1. Flow diagram describing the study design process.
Chilomastixmesnili were considered non-pathogenic protozoa, inour study.
The quality of selected studies was assessed using the STROBEscale (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).
2.2. Statistical analysis
In this study, forest plots were used to estimate pool effectsize and effect of each study with their confidence interval (CI) toprovide a visual summary of the data. To evaluate heterogeneityamong studies, common approaches including the Cochran’s Q testand I-square indices were used. A significance threshold of p = 0.05was applied to the heterogeneity �2. I-squared values less than25% were defined as low heterogeneity, 25–50% as moderate, andgreater than 50% as high heterogeneity. At present heterogeneity,random effects model (DerSimonian Laird model) and the other-wise applied fixed effect model (Mantel Haenszel) were used tocompute overall effect. Begg’s Funnel plot (Qualitative method)and Egger’s regression test (Quantitative method) were used forevaluating the possibility of publication bias. We conducted meta-analysis using STATA software (Intercooled, version 11, STATA Corp,College Station, TX), and for all statistical tests, p < 0.05 was consid-ered significant.
3. Results
Of the 68,532 publications that were gathered for this systematicreview, 103 were eligible for inclusion under intestinal parasiticinfections (Fig. 1 and Table 1).
A. Daryani et al. / Acta Tropica 169 (2017) 69–83 71
Table 1Baseline 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)
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The mean score obtained for STROBE scale was 18.41, whichndicated that the quality of studies was moderate to high (Vonlm et al., 2008).
In this study, the pooled prevalence of IPIs among Iranianreschool and school children was 38.3% (95% CI: 33.2%, 43.4%).mong 54 studies, Ahvaz (Ghafari et al., 2012) and Hamadan
Saeidi-jam and Sajadi, 2001) provinces had the lowest (5%) andighest (86%) prevalence rates of IPIs, respectively (Fig. 2 andable 1).
The pooled estimation of the prevalence of Giardia was 16% (95%I: 14%, 18%).
The results of random-effects meta-analysis showed that preva-ence of Cryptosporidium spp. was 3% (95% CI: 0.03%, 7%). However,n a study on cancer patients, the prevalence of this parasite was2% (Fig. 3, Fig. 4 and Table 2).
The pooled estimation of the prevalence of E. vermicularis was8% (95% CI: 15%, 20%) (Fig. 5 and Table 2).
In this study, the prevalence of protozoa, helminths, and non-athogenic parasites was 16.9% (95% CI- 14%, 20%), 9.48% (95%I- 6.82%, 12.54%), and 18.5% (95% CI- 14.3%, 23.2%), respectively.he highest prevalence rate of IPIs was reported from Hamadanrovince (83.86%), and the lowest was reported from Tehranrovince (12.91%) (Fig. 6 and Table 3).
Giardia was the most common parasite among the proto-oan infections (16%). The highest prevalence was from the Southhorasan province (30.14%), and the lowest was from the West-
rn Azerbaijan province (4.72%). Prevalence of Cryptosporidiumpp., Blastocystishominis, and Entamoebahistolytica was 3%, 7%, and.47%, respectively. The highest prevalence of Cryptosporidium wasn Razavi Khorasan province (7.76%) and the lowest in Tehran
able 2he prevalence rate of intestinal parasitic infections, Giardia, Cryptosporidium and E. verm
Key words of search strategy No. studies No. Studies of IPIs that properly reCryptosporidium and E.vermicula
IPIs 54 –
Giardia 9 54
Cryptosporidium 26 0
E. vermicularis 14 17
um Ziehl-Neelsen 547 27 (4.93) Graham test 95 14 (14.73)
Formalin-ether 811 180 (22.19)
province (0.1%) (Tables 3 and 4). Among the helminthic infec-tions, E. vermicularis was the most common parasite (18%),withthe highest prevalence in Lorestan province (33.77%) and the low-est in Zanjan province (1.35%). Prevalence of Hymenolepis spp. andAscaris was 1.5% (95% CI- 1.07%, 2.2%) and 0.75% (95% CI- 0.4%, 1.2%),respectively. The highest and lowest prevalence of Hymenolepis spp.was reported from Sistan and Balochestan (9.55%) and Ilam (0%)provinces, respectively (Tables 3 and 5).
Heterogeneity was observed among the studies related to IPIs,Giardia, Cryptosporidium, and E.vermicularis. The results of subgroupanalysis showed that except for Cryptosporidium, sex and age werethe two main causes of heterogeneity in this meta-analysis. Theresults of Egger’s test showed that there was a strong publica-tion bias for studies on IPIs caused by Cryptosporidium and Giardia(p < 0.001), but not for those caused by E. vermicularis (p = 0.18)(Table 6).
According to the subgroup analysis of 50 studies that had sexdata, there was a significant relationship between sex and preva-lence of IPIs (p < 0.001). The prevalence of IPIs in females (30.9%)was significantly higher than in males (16.5%).
Moreover, according to subgroup analysis on 31 studies that hadage data, the prevalence of IPIs in preschool children (43.7%) wassignificantly higher than that in school children (18.8%) (p < 0.001)(Table 7).
In our study, there was no significant relationship betweenprevalence of Giardia and the sex of the children (in 50 studies
that had analyzed sex data); however, there was a significant rela-tionship between the prevalence of Giardia and age (12 studiescomprising age data were analyzed). In addition, the prevalenceicularis in Iranian children during 1996–2015.
ported Giardia,ris
Total studies for analysis Prevalence (95% CI)
54 38% 33.2–43.463 16% 14–1826 3% 0.3–731 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.E dencet ond ret
rp
roa
tsal(
w
ach square represents the effect size (ES) for each individual study. Their 95% confio the weight assigned (%Weight) to each study within the meta-analysis. The diamhe vertical solid line represents value of null hypothesis.
ate of Giardia in school children (14.2%) was higher than that inreschool children (8%) (Table 7).
Data analysis in our study showed that there was no significantelationship between the prevalence of Cryptosporidium and the sexf the children (8 studies comprising sex data were analyzed) andge groups (12 studies comprising age data were analyzed).
Our analysis of 30 studies that included age data showed thathe prevalence of E. vermicularis in preschool children (10.0%) wasignificantly higher than that in school children (6.4%). Moreover,nalysis of 13 studies comprising sex data showed that the preva-
ence in males (14.4%) was significantly higher than that in females8.9%) (p = 0.003) (Table 7).In the present study, the overall prevalence of A. lumbricoidesas 0.75%, T. trichiura 0.12%, and Hymenolepis spp. 1.5%.
interval (95% CI) for prevalence is reflected by the size of each square proportionalpresents the overall pooled. The vertical dash line represents overall estimate and
Trichostrongylus spp. and Strongyloides stercoralis were rarelyfound in Iranian school children. However, in Mazandaran province,prevalence rate of these parasites was 1.7% and 1.2%, respectively.
Data analysis indicates that prevalence of IPI decreased in Ira-nian preschool and school children during January 1996–April 2015(Fig. 7).
4. Discussion
This systematic review and meta-analysis will be beneficial for
understanding the situation of IPIs in Iranian children. This studyestimated the prevalence rate of IPIs in this group, using the docu-mented data from the literature reviews, which have been gatheredfrom 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 proportionalto the weight assigned (%Weight) to each study within the meta-analysis. The diamond represents the overall pooled. The vertical dash line represents overall estimate andthe vertical solid line represents value of null hypothesis.
Table 3The 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)
1007622
435
asI
l
Tehran 148642
Yazd 3580
Zanjan 2148
After searching through 9 databases, unpublished data, andbstracts of scientific congresses, 103 articles were included in the
tudy. According to our results, the prevalence rate of IPIs amongranian children was 38% during January 1996–April 2015.Epidemiologic studies in different countries showed a corre-ation between the prevalence rate of IPIs and personal, social,
1 (6.7) 8460 (5.6) 2068 (1.3)(17.3) 867 (24.2) 263 (7.3)(20.2) 275 (12.8) 91(4.2)
and cultural habits, as well as the region’s historical and geo-graphical characteristics. In meta-analysis has been carried out, the
prevalence of IPIs differs in various provinces. Hamadan provincereported the highest (83.86%) prevalence rate of IPIs. Studies car-ried out in Hamadan province a couple of decades ago indicatedthat the level of sanitation was low, both at the individual, as well
A. Daryani et al. / Acta Tropica 169 (2017) 69–83 75
Table 4The 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(7.5)
ND ND 904 0(0)
Hajialiani et al. (2014)
Ardabil 1883 266 (14.1) 371 15(4.1)
1070 0(0)
Daryani and Ettehad (2005); Etehad (2008);Mohammadi ghalehbin et al. (2006)
Chaharmahal and Bakhtiari ND ND 789 20(2.5)
ND ND Khalili et al. (2006); Khalili et al. (2007)
Eastern Azarbayjan 900 79 (8.7) 50 3 (6)(7.6)
900 0(0)
Kosha et al. (2011); Davodi et al. (2010)
Fars 1275 211(16.5)
ND ND 1275 51(4)
Davami et al. (2008); Forotani and Rezaiyan(2001)
Ghazvin 1851 217 (11.7) 1469 15(0.1)
1068 0(0)
Akhlaghi et al. (2013); Keshavarz-riazi et al.(2010); Ghoreishimakri et al. (2008); Mahyarand Hadiloo, (2000); Mahyar et al. (2000)
Golestan 1171 153 (13.1) 547 27(4.9)
1171 8(0.6)
Fani et al. (2001); Kohsar et al. (2004);Mesgarian et al. (2014); Rostami et al. (2012);Tohidi and Qorbani (2009)
Hamedan 1097 226 (20.6) 974 32(3.2)
1097 4(0.3)
Asadi et al. (2014); Fallah and Haghighi (1996);Saeidi-jam and Sajadi (2001); Taherkhani(2001)
Hormozgan 654 40(6.1)
ND ND 654 0(0)
Khademi and Arman (2010); Sobati andMobedi (2004)
Ilam 230 27 (13.7) 979 29(2.9)
230 7(3.1)
Abdi et al. (2013); Naserifar and Khosravi(2001)
Isfahan 2640 417 (15.7) 1488 67(4.5)
2640 19(0.7)
Aazami and Dorostkar-Moghadam (2008);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(0)
Ahmadrajabi et al. (2003);Mohseni-moghadam et al. (2007); Molazadeand Rahimi (2005)
Kermanshah ND ND 1100 28(2.5)
ND ND Hamzavi (2000); Hamzavi et al. (2014)
Khozestan 863 138 (15.9) ND ND 863 5(0.5)
Ghafari et al. (2012); Samie et al. (2003)
Kohgiluyeh and Boyer-Ahmad 912 252 (27.6) ND ND 912 0(0)
Moghimi and Sharifi (2002); Moshfea andSharifi (2000)
Lorestan 500 97 (19.4) 400 19(4.7)
ND ND Fallahi et al. (2007); Malaki et al. (2005)
Markazi 1428 115 (8.1) 405 31(7.6)
1043 25(2.4)
Alavi-naiini and Davari (1999); Davami et al.(2002); Mosayebi and Eslami-Rad, (2001)
Mazandaran 6482 1191(18.3)
ND ND 5211 9(0.1)
Daryani et al. (2012); Ghahramanloo et al.(2001); Kalantari and Mobadi (2000);Sedighian et al. (2000); Soud-Bakhsh et al.(2002)
Razavi Khorasan ND ND 335 26(7.7)
ND ND Berenji et al. (2007); Mohajeri et al. (2003)
Semnan 2395 281(11.7)
153 5(3.2)
2395 12(0.5)
Akbari-eidgahi et al. (2004); Atashnafs et al.(2006); Ghorbani et al. (1999); Heidari andRokni (2003); Rahimi et al. (2015)
Sistan and Balochestan 1800 330 (18.3) 528 24(4.5)
1800 58(3.2)
Dabirzade et al. (2003); Davodi et al. (2004);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(0.1)
148642 357(0.2)
Amiri-moghadam and Khansari (2000);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); Salehiet al. (2013); Taghipour et al. (2011)
Western Azarbayjan 2116 199(9.4)
102 3(2.9)
ND ND Hazrati-tappe et al. (2011); Hazrati-tappe et al.(2005b); Hazrati-tappe et al. (2014); Manafiet al. (2013)
Yazd 3580 503 (14.1) ND ND 2080 65(3.1)
Anvari-Tafti et al. (2014);; Ebadi et al. (2007);Fatahi-bafghi (1997); Mozafar-iKhaosravi andDehgani (1997)
Zanjan 2148 433 (20.1) ND ND 2148 2(0.9)
Ataiyan et al. (1996)
76 A. Daryani et al. / Acta Tropi
NOTE: Weights are from random effects analysis
Overall (I-s quared = 98.9%, p = 0.00 0)
Giardia
0.16 (0. 14, 0.18)
ES (95% CI)
100.00
Weigh t
%
0-.177 0 .17 7
Fig. 4. Estimate of prevalence of Giardia based on 63 studies in different years andareas in Iran. The pooled random effect size (ES) and 95% confidence interval (95%Cpl
aattum
(
FCo
I) represents by diamond. Overall heterogeneity was showed by I-squared (98%, = 0.000). The vertical dash line represents overall estimate and the vertical solid
ine represents value of null hypothesis.
s at the societal level. In addition, people were using human fecess agriculture fertilizer (manure), which was responsible for theransmission of parasites (cysts and eggs of parasites) through con-aminated vegetables. Moreover, in rural areas, animal feces were
sed as a fuel in the winter, which was responsible for the trans-ission of zoonotic parasites.The lowest prevalence was observed in Tehran province12.91%). The low rate of IPIs in Tehran province (the capital of
ig. 5. Forest plot of prevalence of E. vermicularis in Iranian Children. Each square represeI) for prevalence is reflected by the size of each square proportional to the weight assignverall pooled. The vertical dash line represents overall estimate and the vertical solid lin
ca 169 (2017) 69–83
Iran) seems to be because of advances in public health measuresthan in other provinces, especially those in drinking water purifi-cation, as well as measures for control and treatment programsagainst parasitic diseases.
The prevalence of IPIs is different in neighboring and other coun-tries. For example, prevalence is 47.6% in Afghanistan (Gabrielliet 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-economicstatus, poor hygiene and sanitary facilities, weather, climate andenvironmental factors, as well as inappropriate drinking water.
Data analysis in our study showed that the prevalence of IPIsin females (30.9%) was significantly higher than in males (16.5%)(p < 0.001), which is in sharp contrast to a study carried out byGelaw et al. (2013). This is likely due to different behavioral patternsas well as gender-based differences in females and males. Femalesusually favor eating raw salads. They also cook vegetables that maybe contaminated with parasitic cysts and eggs.
In the present study, the prevalence of IPIs in preschool childrenwas (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 otherstudies (Jayarani et al., 2014; Workneh et al., 2014). The reasoncould be increased person-to-person contact in preschool childrenas well as lack of personal hygiene.
According to information obtained from the study, the overall
prevalence rate of parasitic protozoan infections was 16.9%, withGiardia lamblia (16%) having the highest prevalence. Other stud-ies that investigated intestinal infections in developing countriesreported similar findings (Okyay et al., 2004; El-Soud et al., 2009).nts the effect size (ES) for each individual study. Their 95% confidence interval (95%ed (%Weight) to each study within the meta-analysis. The diamond represents thee 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.
1996-2000 2001-2005 2006-2010 2011-2015IPIs 46.4 27. 5 25.8 11.7Giardi a 19.2 15.03 11.5 5.6Cryptosporidium 4.5 3. 6 3. 1 1.6E. vermicular is 9.02 8. 4 23.7 11.54
0
5
10
15
20
25
30
35
40
45
50
Infe
c�on
rat (
%)
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 5The prevalence rates of major helminthes in Iranian children by province.
Province Enterobius Ascaric Hymenolepis Reference
No. Pos.(%)
No. Pos. (%) No. Pos.(%)
Alborz 904 21(2.3)
904 0(0)
904 0(0)
Hajialiani et al. (2014)
Ardabil 400 73(18.2)
1070 5(0.1)
1070 5(0.4)
Daryani et al. (2004); Daryani and Ettehad(2005)
Eastern Azarbayjan ND ND ND ND ND NDFars ND ND 1275 12 (0.9) 1275 99
(7.7)Davami et al. (2008)
Ghazvin ND ND 1068 0(0)
1068 0(0)
Akhlaghi et al. (2013); Mahyar et al. (2000)
Golestan 328 52(15.8)
1171 4(0.3)
1171 36(3.1)
Fani et al. (2001); Kohsar et al. (2004); Rostamiet al. (2012); Tohidi and Qorbani (2009)
Hamedan 776 155 (19.9) 1097 434(39.5)
1097 65(5.9)
Saeidi-jam and Sajadi (2001); Taherkhani andSardarian (2005); Taherkhani (2001)
Hormozgan ND ND 654 0(0)
654 8(1.2)
Khademi and Arman (2010); Sobati andMobedi (2004)
Ilam ND ND 230 9 (3.9) 230 0(0)
Abdi et al. (2013)
Isfahan 1126 155 (17.1) 2640 151 (5.7) 2640 31(1.1)
Abedi et al. (2004); Baghaii et al. (2001);Bahadoran et al. (1996); Momenharavi et al.(2012)
Kerman 370 60(16.2)
1290 7(0.5)
1290 30(2.3)
Ahmadrajabi et al. (2003); Molazade andRahimi (2005)
Kermanshah 95 14 (14.7) ND ND ND ND Shah-mohammadi et al. (2014)Khozestan ND ND 863 0
(0)863 30
(3.4)Ghafari et al. (2012); Samie et al. (2003)
Kohgiluyeh and Boyer-Ahmad 912 102 (11.1) 912 1(0.1)
912 15(1.6)
Moghimi and Sharifi (2002); Moshfea andSharifi (2000)
Lorestan 598 202 (33.7) ND ND ND ND Badparva et al. (2009)Markazi ND ND 1043 9
(0.8)1043 3
(0.2)Alavi-naiini and Davari (1999)
Mazandaran 1365 243(17.8)
5211 4 (0.07) 5211 34(0.6)
Sharif and Ziaie-hezar-garibi (2000); Daryaniet 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(0.9)
Atashnafs et al. (2006); Atashnafs et al. (2007);Ghorbani et al. (1999); Heidari and Rokni(2003); Rahimi et al. (2015)
Sistan and Balochestan 2144 603 (28.1) 1800 2(0.1)
1800 172(9.5)
Fazaeili et al. (1997); Sharifi-mod et al. (2000);Ebrahimzade et al. (2014)
Southern Khorasan 734 138(18.8)
2568 15 (0.5) 2568 160(6.2)
Farajzade and Foroughi-Ameri (2003); Rafieiet al. (2000); Taheri et al. (2011); Taheri andSaadatjoo (2003)
Tehran 20115 1039 (5.1) 148642 211 (0.1) 148642 507(0.3)
Aminzade and Hosseinzadeh (2008);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(22.8)
676 0(0)
676 2(0.2)
Hazrati-tappe et al. (2005a); Hazrati-tappeet al. (2011); Hazrati-tappe et al. (2002);Hazrati-tappe et al. (2006)
Yazd ND ND 2080 114 (5.48) 2080 102(4.9)
Anvari-Tafti et al. (2014); Ebadi et al. (2007);Fatahi-bafghi, 1997; Mozafar-iKhaosravi andDehgani (1997)
Zanjan 2148 29(1.3)
2148 4(0.1)
2148 56(2.6)
Ataiyan et al. (1996)
Table 6The 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 <0.0001.01
.048
0.01
AJi
Cryptosporidium 26 0Giardia 63 0E. vermicularis 31 0
mong the other countries, the prevalence rate of Giardia is 36% inordan (Nimri, 1993), 22–24% in Syria (Almerie et al., 2008), 16.5%n Turkey (C eliksöz et al., 2005), 10.9% Saudi Arabia (Omar et al.,
0.001 6.65 <0.00010.004 10.49 <0.00010.03 1.36 0.18
1991), 10.5% in Oman (Nimri, 1994), and 8% in Gaza Strip (Astal,2004).
A. Daryani et al. / Acta Tropica 169 (2017) 69–83 79
Table 7Subgroup 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 < 0.001School 10 18.8 17.1 40.6 99.1%
Sex Male 25 16.5 14.6 18.5 98.4% P < 0.001Female 25 30.9 26.8 34.9 98.7%
Giardia Age Pre-school 14 8.0 7.4 8.6 90.1% P < 0.001School 36 14.2 13.7 14.6 98%
Sex Male 6 9.4 8.3 10.6 94.5 0.819Female 6 9.3 8.1 10.4 95.3
Cryptosporidium Age Pre-school 9 1.0 0.7 1.3 92.3 0.937School 3 1 0 2.1 56.8
Sex Male 4 3.9 2.6 5.2 85.2 0.921Female 4 4 2.5 5.4 62.1
E.vermicularis Age Pre-school 18 10 9.4 10.6 98.6 P < 0.0016.4
14.4
8.9
alraLbeG(lodad
iiKscro3EiPi(S
scaieec
p2i2wp
School 12
Sex Male 6
Female 7
G. lamblia has a negative impact on school children’s growthnd development because giardiasis causes diarrhea, malnutrition,oss of appetite etc. This problem mostly occurs in deprived andural areas, where the drinking water supply and sewage networksre less developed than in advanced and urban areas(Muhsen andevine, 2012). In our study, there was no significant relationshipetween prevalence of Giardia and the sex of the children; how-ver, there was a significant relationship between prevalence ofiardia and age. The prevalence rate of Giardia in school children
14.2%) was higher than in preschool children (8%), which is simi-ar to the study done by Jayarani et al. (2014). The reason for thisbservation may include poor environmental sanitation, low stan-ards of hygiene in schools, low family income, and greater outdoorctivities in school children compared with those in preschool chil-ren.
In the present study, the overall prevalence of Cryptosporid-um spp. was 3%. The prevalence rate of Cryptosporidium spp.n patients with lymphohematopoietic malignancies in Razavihorasan province was 22% (Berenji et al., 2007). These resultshow that HIV positive and cancer patients are mainly at risk ofryptosporidiosis. In the current study, there was no significantelationship between prevalence of Cryptosporidium and the sexr age groups. The prevalence rates of Cryptosporidium spp. are–10.2% in Asia, Australia, Africa, and 1–2% in Central and Southurope (Frost et al., 2000). The major risk factor for cryptosporid-um infection is drinking water that is contaminated with oocysts.eople at higher risk include animal handlers, people in close prox-mity to infected persons, as well as preschool and school childrenCheckley et al., 2015; Kotloff et al., 2013; Huang et al., 2004;teinberg et al., 2004).
Amebiasis is a serious health problem in many tropical andubtropical regions of the world, and especially so in developingountries such as Iran. According to our studies, the prevalence ofmebiasis is 0.34% in Iran. The prevalence rate of this protozoons 5.3% in Turkey (Peruzzi et al., 2006), 9.2% in Saudi Arabia (Omart al., 1995), 10.6% in Jordan (Battikhi, 2004), and 11% in India (Kaurt al., 2002). This difference may be due to varying socio-economiconditions in these countries.
Recently, Blastocystishominis has been considered as a potentialrotozoan pathogen (Stenzel and Boreham, 1996; Andiran et al.,006; Carrascosa et al., 1996). Young age groups are at higher risk of
nfection, causing clinical manifestations of disease (Graczyk et al.,005). In the present study, the overall prevalence rate of B. hominisas 3.6%, which is lesser than in other Asian countries. For exam-le, 40.7% in Philippines (Eleonor et al., 2004), 36.9% in Thailand
5.9 7 99.310.7 12.5 98.5 0.0037.4 10.4 97.9
(Leelayoova et al., 2004), 32% in Pakistan (Yakoob et al., 2004), 29%Turkey (Dogruman-Al et al., 2010), and 25% in Jordan (Nimri, 1993).
The overall prevalence rate of non-pathogenic protozoa in ourstudy group was 18.5%. Entamoeba coli showed the highest preva-lence (7.1%). Iodamoebabütschlii was the second most commonnon-pathogenic parasite in Iranian children (0.09%). E. hartmanni,E. nana, D. fragilis, T. hominis, and C. mesnili are non-pathogenic pro-tozoa that were reported in our study. However, their prevalencerates were very low. The study carried out by Walana et al. (2014) inGhana showed that the prevalence of E. coli, E. nana, and I. bütschliiwas 10.3%, 7%, and 1.5%, respectively.
The overall prevalence of helminthic infections amongpreschool and school children in our study was 9.48%. Amonghelminthic infections, E. vermicularis had the highest prevalence(18%). Studies in other countries show that the prevalence of entero-biasisis 38.82% in Thailand (Nithikathkul et al., 2001), 17% in Turkey(Celiksoz et al., 2010), 10.5% in Korea (Lee et al., 2011), 6.8% in China(Wu et al., 2012), and 0.62% in Japan (Fukushima et al., 2010). Thehelminths that are common in preschool children worldwide arecosmopolitan in distribution (Akkus and Cıngıl, 2004; Beaver et al.,1984; C ulha and Duran, 2006; Gündüz et al., 2005; Song et al.,2003). Our analysis shows that the prevalence rate of E. vermicularisin preschool children (10.0%) was significant compared to that inschool children (6.4%), which is similar to that from another study(Hong-yong, 2010). The difference observed between preschooland school children might be because of close contact between stu-dents as well as unhygienic conditions. Moreover, this prevalencein males (14.4%) was significantly higher than in females (8.9%)(p = 0.003). This finding is similar to that from studies by Lee et al.(2011). The reason may be inadequate personal hygiene, playingon the floor, nail-biting, and a failure to wash hands before mealsin males compared to females.
Soil-transmitted helminthias is (STH) is commonly caused byAscarislumbricoides, hookworms and Trichuristrichiura. STH is apublic health problem, especially in the developing countries. Overone billion individuals in the world are affected by STH. School-going children (5–15 years) are particularly at risk (Bethony et al.,2006; Debalke et al., 2013). The prevalence rate of STH variesworldwide. For example, the prevalence rate is 15.6% in Thailand(Anantaphruti et al., 2004), 43.5% in Ethiopia (Belyhun et al.,2010), 53% in Guinea (Glickman et al., 1999), and 88.4% in Turkey
(Ulukanligil et al., 2001). In the present study, the overall preva-lence rate of A. lumbricoides was 0.75% and that of T. trichiura was0.12%. Hookworms were reported in 2 of 54 articles in our study.Ghahramanloo et al. (2001) from Mazandaran province (north of
8 Tropi
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A
tbv
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A
A
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A
0 A. Daryani et al. / Acta
ran), analyzed 3429 samples of which 2 were positive. Further-ore, Rostami et al. (2012) from Golestan province (north of Iran)
ound that 3 cases were positive in 800 samples.In our study, the prevalence rate of Hymenolepisspp. was 1.5%.
ll species were Hymenolepisnana, except for three positive cases ofymenolepisdiminuta, which were reported by Haghi-ashtiani et al.
2011) in Tehran.There were several limitations to the present systematic review
nd meta-analysis: (i) In most studies included in this review,tool samples were prepared once, whereas for standard diagno-is, at least 3 samplings are necessary. (ii) The number of parasitess important in Blastocystis pathogenesis; however, the studiesncluded in this review did not refer to the number of parasites.iii) Gram staining is the gold standard for detection of enterobiasis.owever, many studies have been conducted only using the directethod (wet smear). We have discarded these studies to determine
. vermicularis prevalence. (iv) Modified acid-fast staining of a fecalmear is the gold standard and commonly used method for detect-ng Cryptosporidium oocysts in stool. This method was used in mostf the studies included in our review (18 cases from 22 papers). Theolymerase chain reaction (PCR) and serological methods were alsosed for detecting Cryptosporidium. However, many studies per-ormed only the direct method. We have discarded these studies tobtain accurate ratesof Cryptosporidium spp. (v) There were manytudies that presented data and analysis of demographic informa-ion and risk-factors such as sex, age, the literacy level of parents,tc. that were not mentioned in their articles.
It is recommended that researchers conduct proper diagnos-ic methods for each parasite (Graham test for E. vermicularisnd Ziehl-Neelsenstaining for Cryptosporidium) and analyze demo-raphic and risk factor information mentioned in the respectiverticles.
. Conclusions
This is the first systematic review and meta-analysis that pro-ides a comprehensive overview of the epidemiology of IPIs inranian preschool and school children. Our results showed that therevalence of IPI is declining in Iranian preschool and school chil-ren. Improved sanitation, personal hygiene, increased awareness,nd health education can be effective in reducing parasitic infec-ions in different communities. Moreover, the establishment ofppropriate sanitation facilities and education in hygiene in kinder-artens and schools will help make a healthy society.
cknowledgments
We thank Mr. Mohammad-Taghi Rahimi for critical review ofhe manuscript and technical assistance. This work was supportedy grant (No. 2044) from the deputy of research, Mazandaran Uni-ersity of Medical Sciences, Sari, Iran.
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