Skip to main content Accessibility help
×
Home

Information:

  • Access
  • Cited by 11

Actions:

      • Send article to Kindle

        To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

        Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

        Find out more about the Kindle Personal Document Service.

        Echinococcus granulosus genotypes in Iran: a systematic review
        Available formats
        ×

        Send article to Dropbox

        To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

        Echinococcus granulosus genotypes in Iran: a systematic review
        Available formats
        ×

        Send article to Google Drive

        To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

        Echinococcus granulosus genotypes in Iran: a systematic review
        Available formats
        ×
Export citation

Abstract

Cystic echinococcosis (CE) caused by Echinococcus granulosus sensu lato (s.l.) is a significant zoonosis, especially in developing countries of the Middle East, with many studies focusing on CE genotypes in Iran. We performed a systematic review to determine the exact status of E. granulosus genotypes in the country. We explored English (Pubmed, Scopus, ISI Web of Science and Science Direct) and Persian (Magiran, Iran Medex and Scientific Information Database) databases along with Google Scholar. Our review included 73 studies published prior to the end of 2015. In total, 2952 animal (intermediate and definitive) hosts were examined, and the prevalent genotypes comprised G1 (92.75%) and G6 (4.53%) in sheep, cattle, camels, goats and buffaloes; G3 (2.43%) in five herbivore hosts and dogs; G7 (0.2%) in sheep and goats; and G2 (0.06%) in dogs. G1 was mostly dominant in West Azerbaijan, whereas G3 and G6 were identified most frequently in the provinces of Isfahan and Fars, respectively. Regarding human CE infection, 340 cases were reported from Iran, with the identified genotypes G1 (n = 320), G6 (n = 13) and G3 (n = 7). Most CE-infected humans originated from Isfahan province (168 cases), whereas the lowest number of infected persons was noted in Kerman province (two cases). The information obtained from this systematic review is central to better understanding the biological and epidemiological characteristics of E. granulosus s.l. genotypes in Iran, leading to more comprehensive control strategies.

Footnotes

*

Current address: Department of Parasitology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran. P.O. Box: 111-14115

Introduction

Despite global community efforts to minimize parasitic helminthiases in humans and animals in recent decades, numerous cases of such devastating diseases are still reported worldwide (Carmena & Cardona, Reference Carmena and Cardona2014; Bartsch et al., Reference Bartsch, Hotez, Asti, Zapf, Bottazzi, Diemert and Lee2016; Cucher et al., Reference Cucher, Macchiaroli and Baldi2016; Khademvatan et al., Reference Khademvatan, Salmanzadeh, Foroutan-Rad and Ghomeshi2016; Saki et al., Reference Saki, Khademvatan, Foroutan-Rad and Gharibzadeh2017; Weatherhead et al., Reference Weatherhead, Hotez and Mejia2017). Echinococcus granulosus sensu lato (s.l.), a cestode helminth belonging to the Taeniidae family, is the causative agent of a prevalent zoonotic disease, cystic echinococcosis (CE) (Rojas et al., Reference Rojas, Romig and Lightowlers2014). This tapeworm uses canids and herbivores/omnivores as definitive and intermediate hosts, respectively, and human infection occurs accidentally by ingestion of the eggs (Rokni, Reference Rokni2009). The disease in humans entails the development of a fluid-filled hydatid cyst, which localizes in the liver and lungs and, to a lesser extent, in the abdominal cavity, muscle, heart, bone and nervous system (Craig et al., Reference Craig, McManus and Lightowlers2007). The disease causes impotency, disability and decreased work productivity in endemic territories, including Australia, New Zealand, China, Russia, South America, North Africa and the Middle East (Battelli, Reference Battelli2009; Shariatzadeh et al., Reference Shariatzadeh, Spotin, Gholami, Fallah, Hazratian, Mahami-Oskouei, Montazeri, Moslemzadeh and Shahbazi2015). As a consequence of CE, 1–3.6 million disability-adjusted life years (DALYs) are missed globally; most of these cases occur in low-income countries (Budke et al., Reference Budke, Deplazes and Torgerson2006; Torgerson et al., Reference Torgerson, Devleesschauwer and Praet2015). Given the numerous traditional animal husbandries and access of dogs to waste materials of abattoirs there, Iran has been considered a hyperendemic region (Dalimi et al., Reference Dalimi, Motamedi, Hosseini, Mohammadian, Malaki, Ghamari and Ghaffarifar2002; Pour et al., Reference Pour, Hosseini and Shayan2011; Khademvatan et al., Reference Khademvatan, Yousefi, Rafiei, Rahdar and Saki2013). More recently, the weighted prevalence of hydatidosis in human and animal intermediate hosts in Iran reached 4.2% (95% confidence interval (CI) = 3.0–5.5%) and 15.6% (95% CI = 14.2–17.1%), respectively. The pooled prevalence of E. granulosus infection in definitive hosts totalled 23.6% (95% CI = 17.6–30.1%) (Khalkhali et al., Reference Khalkhali, Foroutan, Khademvatan, Majidiani, Aryamand, Khezri and Aminpour2017). Human infection in Iran was mostly concentrated in the south, whereas the lowest prevalence rate was observed in central parts of the country (Khalkhali et al., Reference Khalkhali, Foroutan, Khademvatan, Majidiani, Aryamand, Khezri and Aminpour2017). The annual monetary burden of CE in the country was estimated to be c. USD 232.3 million (Mobedi & Dalimi, Reference Mobedi and Dalimi1994; Harandi et al., Reference Harandi, Budke and Rostami2012a).

Extensive intraspecies genetic diversity of CE has been recorded over a long period of time, and this condition may influence characteristics such as morphology, epidemiology, host specificity, infectivity and drug resistance (Carmena & Cardona, Reference Carmena and Cardona2014). Four molecular approaches – single-gene analysis using mitochondrial DNA, microsatellite markers for polymorphic DNA loci, full-genome exploration, and comparison of discrepancies among mitochondrial and nuclear DNA for species hybridization – have been used to categorize Echinococcus species into several genotypes (Ito & Budke, Reference Ito and Budke2017). Most of our understanding in this area originates from the investigation of Bowles and colleagues into cox1 and nad1 mitochondrial genes (Bowles et al., Reference Bowles, Blair and McManus1992). Accordingly, ten deduced strains of CE have been characterized and encompassed in a number of clades, including E. granulosus sensu stricto (s.s.) (G1–3), E. equinus (G4), E. ortleppi (G5) and E. canadensis (G6–10), and E. felidis (the lion strain) (Amer et al., Reference Amer, Helal, Kamau, Feng and Xiao2015). G1 and G2 are sheep strains, whereas G3 and G5 are buffalo and cattle strains, respectively. G4 is found in horses, G6 in camels, G7 in pigs and G8–10 in cervids (Rojas et al., Reference Rojas, Romig and Lightowlers2014). G1 genotype is the most commonly reported in human CE cases globally. Additionally, studies have reported that the subsequent strains are infective to humans (Grosso et al., Reference Grosso, Gruttadauria, Biondi, Marventano and Mistretta2012). Host–parasite immunological interplay and cross transmission templates can justify the emergence of Echinococcus strains and their related genetic diversity (Bowles et al., Reference Bowles, Blair and McManus1992; Thompson, Reference Thompson2013; Thompson & Jenkins, Reference Thompson and Jenkins2014). Detecting these genetic variations in E. granulosus s.l. populations is significant for better understanding of various life cycles of CE in endemic regions of Iran and shedding light on more efficient prevention strategies, as well as diagnosis and treatment of CE (Shariatzadeh et al., Reference Shariatzadeh, Spotin, Gholami, Fallah, Hazratian, Mahami-Oskouei, Montazeri, Moslemzadeh and Shahbazi2015).

Thus far, numerous papers have investigated CE genotypes in animal hosts and human cases in Iran. However, there is a lack of collective and processed data for systematic review. Accordingly, we performed a qualitative evaluation to clarify the status of CE genotypes in the country.

Methods

Search strategy

To unravel the genetic distribution of hydatid genotypes in Iran, a systematic review was designed on the basis of literature in English and Persian available online. Four English (PubMed, Scopus, Science Direct and ISI Web of Science) and three Persian (Scientific Information Database, Iran Medex and Magiran) databases were explored for published papers from inception to 31 December 2015, as was Google Scholar as a common, multilingual engine for both English and Persian terms. The current review was conducted using the following Medical Subject Headings (MeSH) terms: ‘Echinococcus granulosus’, ‘Echinococcus’, ‘Echinococcosis’, ‘Hydatid’, ‘Hydatic’, ‘Iran’, ‘Prevalence’, ‘Epidemiology’ and ‘Genotype’, alone or combined together with ‘OR’ or/and ‘AND’ operators.

Study selection and data extraction

Eligibility of studies and inclusion criteria were checked carefully by two independent reviewers (S. Khademvatan and S. Aryamand). Contradiction among studies was obviated by discussion and consensus (Foroutan-Rad et al., Reference Foroutan-Rad, Khademvatan, Majidiani, Aryamand, Rahim and Malehi2016a, Reference Foroutan-Rad, Majidiani, Dalvand, Daryani, Kooti, Saki, Hedayati-Rad and Ahmadpourb; Majidiani et al., Reference Majidiani, Dalvand, Daryani, de la Luz Galvan-Ramirez and Foroutan-Rad2016; Foroutan et al., Reference Foroutan, Dalvand, Daryani, Ahmadpour, Majidiani, Khademvatan and Abbasi2017a, Reference Foroutan, Dalvand, Khademvatan, Majidiani, Khalkhali, Masoumifard and Shamsaddinb, Reference Foroutan, Khademvatan, Majidiani, Khalkhali, Hedayati-Rad, Khashaveh and Mohammadzadehc; Khademvatan et al., Reference Khademvatan, Foroutan, Hazrati-Tappeh, Dalvand, Khalkhali, Masoumifard and Hedayati-Rad2017; Khalkhali et al., Reference Khalkhali, Foroutan, Khademvatan, Majidiani, Aryamand, Khezri and Aminpour2017; Maleki et al., Reference Maleki, Khorshidi, Gorgipour, Mirzapour, Majidiani and Foroutan2017). The inclusion criteria were as follows: (1) peer-reviewed original research papers; (2) cross-sectional studies based on various polymerase chain reaction techniques and investigating the genotypes of E. granulosus in Iran; (3) published in English or Persian; (4) published online from inception to 31 December 2015; (5) full-text articles were available. Papers that failed to meet these criteria were excluded. The required data were collected accurately using a data extraction form, on the basis of the first author, province, geographical region (north, south, east, west, centre), infected organ, genotypes (G1, G2, G3, G4, G5, G6, G7, G8, G9, G10), intermediate and definitive hosts, human cases, type of diagnostic method and the DNA/RNA fragment used in detection. The review was conducted in accordance with PRISMA (preferred reporting items for systematic reviews and meta-analyses) guidelines (Moher et al., Reference Moher, Liberati, Tetzlaff and Altman2010). ArcGIS (http://www.esri.com) was used for mapping the geographical distribution of various genotypes of E. granulosus in Iran.

Results

In total, 73 of 4793 studies met the inclusion criteria and were included in the systematic review (fig. 1). Literature search results and study properties (species, genotypes, animal intermediate host, definitive host, number of animal and human cases) are presented in table 1. Table 2 and supplementary fig. S1 show the geographical diversification of genotypes detected in different provinces in Iran. The number of each genotype in each of the various hosts is shown in table 3.

Fig. 1. PRISMA 2009 flow diagram.

Table 1. Genotypes of Echinococcus granulosus identified in domestic natural hosts (intermediate and definitive) and humans in Iran.

Table 2. Numbers of E. granulosus s.l. genotypes identified in various regions of Iran.

Table 3. Numbers of E. granulosus s.l. genotypes identified in animal and human hosts in Iran.

Intermediate and definitive animal hosts

In total, 2952 animal (intermediate and definitive) hosts were examined for cystic echinococcosis. Five E. granulosus s.l. genotypes exist in Iran (G1, G2, G3, G6, G7), and five livestock species (sheep, goats, cattle, buffaloes, camels) were affected by CE (table 1). With the exception of G7, which is localized in Khorasan province, eastern Iran, other genotypes were detected mostly in central and western parts of the country (supplementary fig. S1). Molecular studies revealed that E. granulosus s.s. clade (G1–3) was involved in most cases of infection, among which the G1 genotype was the most diverse and prevalent, with 2738 of 3058 (92%) cases in animal hosts, and dominant in 17 provinces, particularly in West Azerbaijan (table 2). The geographical distribution and involvement of various intermediate hosts demonstrates why G1 is the most abundant in the country. Results also revealed that the dog–sheep cycle of CE is widespread in most parts of Iran, indicating that G1 is viable for transmission. Most G3 and G6 cases were reported from Isfahan and Fars provinces, respectively (table 2). Animal host involvements of each recognized genotype in Iran are as follows: G1 (92.75%) and G6 (4.53%) in sheep, cattle, camels, goats and buffaloes; G3 (2.43%) in five herbivore hosts and dogs; G2 (0.06%) in dogs; and G7 (0.2%) in sheep and goats (table 3). In one study, genotype co-infection with G1, G3 and G6 was discerned. With respect to G2 and G7 genotypes, more sequencing data from various animal hosts (intermediate and definitive), particularly from provinces with fewer studies, are required to reach a rational consensus on the host range and geographical distribution of these genotypes. The findings suggest that special attention be paid to water buffaloes in subsequent works, as they may play a role in lifecycle maintenance of G1, G3 and G6 strains in Iran. Some characteristics of the G6 genotype are significant for CE diagnosis and control strategies (Kamenetzky et al., Reference Kamenetzky, Muzulin, Gutierrez, Angel, Zaha, Guarnera and Rosenzvit2005; Chow et al., Reference Chow, Gauci, Vural, Jenkins, Heath, Rosenzvit, Harandi and Lightowlers2008; Muzulin et al., Reference Muzulin, Kamenetzky, Gutierrez, Guarnera and Rosenzvit2008). No sequencing information exists for the G4 genotype in Iran, necessitating molecular studies in horses. No molecular evidence from G8–10 genotypes has been reported from the country.

In general, in the case of neighbouring countries there was a low diversity in the animal hosts examined and subsequently in CE genotypes isolated, with most studies focused on E. granulosus s.s. (Utuk et al., Reference Utuk, Simsek, Koroglu and McManus2008; Latif et al., Reference Latif, Tanveer, Maqbool, Siddiqi, Kyaw-Tanner and Traub2010; Simsek et al., Reference Simsek, Balkaya, Ciftci and Utuk2011; Eryıldız & Şakru, Reference Eryıldız and Şakru2012; Hama et al., Reference Hama, Mero and Jubrael2012; Hama & Shareef, Reference Hama and Shareef2016; Hasan et al., Reference Hasan, Fadhil and Fadhil2016; Gökpınar et al., Reference Gökpınar, Değİrmencİ and Yıldız2017; Hassan et al., Reference Hassan, Mero, Casulli, Interisano and Boufana2017). With some exceptions (Al-Qaoud et al., Reference Al-Qaoud, Abdel-Hafez and Craig2003; Trachsel et al., Reference Trachsel, Deplazes and Mathis2007; Ziadinov et al., Reference Ziadinov, Mathis, Trachsel, Rysmukhambetova, Abdyjaparov, Kuttubaev, Deplazes and Torgerson2008), the strains identified in definitive hosts in Iran are partly identical to detected genotypes in adjacent countries.

Human cases

In total, 340 cases of CE in humans have been reported, with sequencing data, from Iran. Major E. granulosus genotypes in infected individuals include G1 (n = 320) and G3 (n = 7) as E. granulosus s.s., and G6 (n = 13) as E. canadensis (tables 1 and 3). Alongside the exclusive G1 genotype, which is dominant globally, G6 is the most prevalent clade in human infections in Iran, similar to recent data from South American countries (Cucher et al., Reference Cucher, Macchiaroli and Baldi2016). Based on the study of Sadjjadi et al. (Reference Sadjjadi, Mikaeili, Karamian, Maraghi, Sadjjadi, Shariat-Torbaghan and Kia2013) in Iran, E. canadensis is responsible for brain infections, suggesting an alternative predilection site to the liver. Consequently, nationwide research is required to clarify the exact epidemiological status and biological behaviour of this clade in Iran. Based on our results, the highest and lowest incidences of human CE infections were in Isfahan (168 cases) and Kerman (two cases) provinces, respectively. Considering the capability of cattle and camels to harbour multiple genotypes (table 1), these animals probably play a central role in preserving the CE life cycle and the risk of human transmission, particularly camels in central arid parts of Iran, where they are possibly involved in G6 environmental maintenance. The absence of G7 (pig strain) in human cases may be partially attributed to the lack of pig breeding in Islamic culture. Human cases in Afghanistan and Pakistan have been discerned as the G1 strain, whereas more diverse CE genotypes have been isolated from human subjects in Iraq and Turkey than in Iran (Rojas et al., Reference Rojas, Romig and Lightowlers2014).

Discussion

Cystic echinococcosis is an important neglected parasitic disease worldwide. In a review of the current situation of echinococcosis in Asia, Ito & Budke (Reference Ito and Budke2017) discussed various aspects of CE throughout the continent but provided no data for Iran. The current work and a previously published meta-analysis (Khalkhali et al., Reference Khalkhali, Foroutan, Khademvatan, Majidiani, Aryamand, Khezri and Aminpour2017) appropriately report up-to-date information regarding the epidemiology of CE in Iran. Several strains of CE with specific epidemiological and biological emphases have been categorized in various clades, including the following: E. granulosus s.s. (G1–3), E. equinus (G4), E. ortleppi (G5) and E. canadensis (G6–10), and E. felidis (the lion strain). More studies using sophisticated molecular tools are a requisite to revealing more genotype diversity and their respective hosts in Iran. This paper reviewed works featuring sequencing discrimination of CE genotypes in natural hosts and human cases in Iran. Reportedly, G6 was the second most abundant genotype in all hosts, after G1. Regarding antigenic variations in EG95-related proteins of G1 and G6, studies should focus on the diagnosis, chemotherapy and pathogenicity of the G6 strain (Alvarez Rojas et al., Reference Alvarez Rojas, Gauci and Lightowlers2013). The lack of human cases of the G4 genotype may be attributable to the requirement of additional host samples and sequencing information and/or the non-infectious condition of the G4 genotype for human hosts. A wide range of animals were proven to be involved in the ecological maintenance of pastoral and sylvatic life cycles of CE. Our review was confined to published literature, and therefore our findings may not provide a full representation of CE genotypes throughout Iran. In conclusion, the data obtained from this systematic review could benefit local and nationwide CE control initiatives, such as effective CE vaccines for dogs and livestock, improved diagnostic methods for humans and definitive hosts, efficient treatment options and development of well-structured mathematical models for better evaluation of cost-effective interventions.

Supplementary material

To view supplementary material for this article, please visit https://doi.org/10.1017/S0022149X18000275

Acknowledgements

The authors would like to thank all staff of the Department of Medical Parasitology of Urmia University of Medical Sciences and Tarbiat Modares University, Iran.

Financial support

This study received financial support from the Student Research Committee of Urmia University of Medical Sciences, Urmia, Iran (grant no. 1395-01-42-2621).

Conflict of interest

None.

Ethical standards

This study was approved by the Ethical Committee of Urmia University of Medical Sciences, Urmia, Iran (IR.UMSU.REC.1395.511).

Author contributions

S. Khademvatan and M. Foroutan conceived the study; S. Khademvatan and S. Aryamand designed the study protocol; M. Foroutan and S. Khademvatan searched the literatures; S. Aryamand extracted the data; H. Khalkhali analysed and interpreted the data; H. Majidiani wrote the manuscript; S. Khademvatan, H. Majidiani, M. Foroutan and K. Hazrati Tappeh critically revised the manuscript. All authors read and approved the final manuscript.

References

Al-Qaoud, KM, Abdel-Hafez, SK and Craig, PS (2003) Canine echinococcosis in northern Jordan: increased prevalence and dominance of sheep/dog strain. Parasitology Research 90, 187191.
Alvarez Rojas, CA, Gauci, CG and Lightowlers, MW (2013) Antigenic differences between the EG95-related proteins from Echinococcus granulosus G1 and G6 genotypes: implications for vaccination. Parasite Immunology 35, 99102.
Amer, S, Helal, IB, Kamau, E, Feng, Y and Xiao, L (2015) Molecular characterization of Echinococcus granulosus sensu lato from farm animals in Egypt. PLoS ONE 10(3), e0118509.
Babazadeh, M, Sharifiyazdi, H, Moazeni, M, Gorjipour, S and Heidari, M (2015) Molecular characterization of a new microvariant of the G3 genotype for Echinococcus granulosus in water buffalo in Iran. Veterinary Research Forum 6, 8387.
Bartsch, SM, Hotez, PJ, Asti, L, Zapf, KM, Bottazzi, ME, Diemert, DJ and Lee, BY (2016) The global economic and health burden of human hookworm infection. PLoS Neglected Tropical Diseases 10(9), e0004922.
Battelli, G (2009) Echinococcosis: costs, losses and social consequences of a neglected zoonosis. Veterinary Research Communications 33, 4752.
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165173.
Budke, CM, Deplazes, P and Torgerson, PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerging Infectious Diseases 12, 296303.
Carmena, D and Cardona, GA (2014) Echinococcosis in wild carnivorous species: epidemiology, genotypic diversity, and implications for veterinary public health. Veterinary Parasitology 202, 6994.
Chow, C, Gauci, CG, Vural, G, Jenkins, DJ, Heath, DD, Rosenzvit, MC, Harandi, MF and Lightowlers, MW (2008) Echinococcus granulosus: variability of the host-protective EG95 vaccine antigen in G6 and G7 genotypic variants. Experimental Parasitology 119, 499505.
Craig, PS, McManus, DP, Lightowlers, MW et al. (2007) Prevention and control of cystic echinococcosis. The Lancet Infectious Diseases 7, 385394.
Cucher, MA, Macchiaroli, N, Baldi, G et al. (2016) Cystic echinococcosis in South America: systematic review of species and genotypes of Echinococcus granulosus sensu lato in humans and natural domestic hosts. Tropical Medicine and International Health 21, 166175.
Dalimi, A, Motamedi, G, Hosseini, M, Mohammadian, B, Malaki, H, Ghamari, Z and Ghaffarifar, F (2002) Echinococcosis/hydatidosis in western Iran. Veterinary Parasitology 105, 161171.
Dousti, M, Abdi, J, Bakhtiyari, S, Mohebali, M, Mirhendi, S and Rokni, M (2013) Genotyping of hydatid cyst isolated from human and domestic animals in Ilam Province, Western Iran using PCR-RFLP. Iranian Journal of Parasitology 8, 4752.
Eryıldız, C and Şakru, N (2012) Molecular characterization of human and animal isolates of Echinococcus granulosus in the Thrace Region, Turkey. Balkan Medical Journal 29, 261267.
Eslami, A, Shayan, P and Bokaei, S (2014) Morphological and genetic characteristics of the liver hydatid cyst of a donkey with Iran origin. Iranian Journal of Parasitology 9, 302310.
Fadakar, B, Tabatabaei, N, Borji, H and Naghibi, A (2015) Genotyping of Echinococcus granulosus from goats and sheep indicating G7 genotype in goats in the northeast of Iran. Veterinary Parasitology 214, 204207.
Farhadi, M, Fazaeli, A and Haniloo, A (2015) Genetic characterization of livestock and human hydatid cyst isolates from northwest Iran, using the mitochondrial cox1 gene sequence. Parasitology Research 114, 43634370.
Foroutan-Rad, M, Khademvatan, S, Majidiani, H, Aryamand, S, Rahim, F and Malehi, AS (2016a) Seroprevalence of Toxoplasma gondii in the Iranian pregnant women: a systematic review and meta-analysis. Acta Tropica 158, 160169.
Foroutan-Rad, M, Majidiani, H, Dalvand, S, Daryani, A, Kooti, W, Saki, J, Hedayati-Rad, F and Ahmadpour, E (2016b) Toxoplasmosis in blood donors: a systematic review and meta-analysis. Transfusion Medicine Reviews 30, 116122.
Foroutan, M, Dalvand, S, Daryani, A, Ahmadpour, E, Majidiani, H, Khademvatan, S and Abbasi, E (2017a) Rolling up the pieces of a puzzle: systematic review and meta-analysis of the prevalence of toxoplasmosis in Iran. Alexandria Journal of Medicine (in press).
Foroutan, M, Dalvand, S, Khademvatan, S, Majidiani, H, Khalkhali, H, Masoumifard, S and Shamsaddin, G (2017b) A systematic review and meta-analysis of the prevalence of Leishmania infection in blood donors. Transfusion and Apheresis Science 56, 544551.
Foroutan, M, Khademvatan, S, Majidiani, H, Khalkhali, H, Hedayati-Rad, F, Khashaveh, S and Mohammadzadeh, H (2017c) Prevalence of Leishmania species in rodents: a systematic review and meta-analysis in Iran. Acta Tropica 172, 164172.
Gholami, S, Sosarai, M, Fakhar, M, Sharif, M and Daryani, A (2011) Genotype identification of Echinococcus granulosus from paraffin-embedded tissues of hydatid cysts isolated from human by PCR-RFLP. Journal of Mazandaran University of Medical Sciences 21, 1019.
Gökpınar, S, Değİrmencİ, R and Yıldız, K (2017) Genotyping of Echinococcus granulosus obtained from cattle slaughtered in Kırıkkale Province. Ankara Üniversitesi Veteriner Fakültesi Dergisi 64, 5154.
Grosso, G, Gruttadauria, S, Biondi, A, Marventano, S and Mistretta, A (2012) Worldwide epidemiology of liver hydatidosis including the Mediterranean area. World Journal of Gastroenterology 18, 14251437.
Hajialilo, E, Harandi, MF, Sharbatkhori, M, Mirhendi, H and Rostami, S (2012) Genetic characterization of Echinococcus granulosus in camels, cattle and sheep from the south-east of Iran indicates the presence of the G3 genotype. Journal of Helminthology 86, 263270.
Hama, AA and Shareef, OH (2016) Morphological and morphometric study of Echinococcus granulosus (metacestode) in Sulaimani Province/Kurdistan Region, Iraq. Kurdistan Journal of Applied Research 1, 7176.
Hama, AA, Mero, WM and Jubrael, JM (2012) Molecular characterization of E. granulosus, first report of sheep strain in Kurdistan–Iraq. In 2nd International Conference on Ecological, Environmental and Biological Sciences (EEBS 2012), 13th–14th October.
Hanifian, H, Diba, K, Hazrati Tappeh, K, Mohammadzadeh, H and Mahmoudlou, R (2013) Identification of Echinococcus granulosus strains in isolated hydatid cyst specimens from animals by PCR-RFLP method in West Azerbaijan–Iran. Iranian Journal of Parasitology 8, 376381.
Haniloo, A, Farhadi, M, Fazaeli, A and Nourian, N (2013) Genotype characterization of hydatid cysts isolated from Zanjan using PCR-RFLP technique. Journal of Zanjan Univeristy of Medical Sciences and Health Services 21, 5765.
Harandi, MF, Budke, CM and Rostami, S (2012a) The monetary burden of cystic echinococcosis in Iran. PLoS Neglected Tropical Diseases 6(11), e1915.
Harandi, MF, Hajialilo, E and Shokouhi, M (2012b) Larval hook length measurement for differentiating G1 and G6 genotypes of Echinococcus granulosus sensu lato. Türkiye Parazitolojii Dergisi 36, 215218.
Harandi, MF, Hobbs, RP, Adams, PJ, Mobedi, I, Morgan-Ryan, UM and Thompson, RCA (2002) Molecular and morphological characterization of Echinococcus granulosus of human and animal origin in Iran. Parasitology 125, 367373.
Hasan, HF, Fadhil, MH and Fadhil, ZH (2016) Molecular characterization of Echinococcus granulosus isolated from human and domestic animals in Kirkuk, Iraq. Animal Research International 13.
Hassan, ZI, Mero, WM, Casulli, A, Interisano, M and Boufana, B (2017) Epidemiological study of cystic echinococcosis in sheep, cattle and goats in Erbil Province. Science Journal of University of Zakho 4, 4355.
Hosseini, SH, Pour, AA and Shayan, P (2012) Morphological characteristics of Echinococcus granulosus derived from buffalo in Iran. Parasitology 139, 103109.
Hosseinzadeh, S, Fazeli, M, Hosseini, A and Shekarforoush, SS (2012) Molecular characterization of Echinococcus granulosus in south of Iran. Open Journal of Veterinary Medicine 2, 201206.
Ito, A and Budke, CM (2017) The echinococcoses in Asia: the present situation. Acta Tropica 176, 1121.
Kamenetzky, L, Muzulin, PM, Gutierrez, AM, Angel, SO, Zaha, A, Guarnera, EA and Rosenzvit, MC (2005) High polymorphism in genes encoding antigen B from human infecting strains of Echinococcus granulosus. Parasitology 131, 805815.
Karimi, A and Dianatpour, R (2008) Genotypic and phenotypic characterization of Echinococcus granulosus of Iran. Biotechnology 7, 757762.
Khademvatan, S, Foroutan, M, Hazrati-Tappeh, K, Dalvand, S, Khalkhali, H, Masoumifard, S and Hedayati-Rad, F (2017) Toxoplasmosis in rodents: a systematic review and meta-analysis in Iran. Journal of Infection and Public Health 10, 487493.
Khademvatan, S, Salmanzadeh, S, Foroutan-Rad, M and Ghomeshi, M (2016) Elimination of urogenital schistosomiasis in Iran: past history and the current situation. Parasitology 143, 13901396.
Khademvatan, S, Yousefi, E, Rafiei, A, Rahdar, M and Saki, J (2013) Molecular characterization of livestock and human isolates of Echinococcus granulosus from south-west Iran. Journal of Helminthology 87, 240244.
Khalkhali, H, Foroutan, M, Khademvatan, S, Majidiani, H, Aryamand, S, Khezri, P and Aminpour, A (2017) Prevalence of cystic echinococcosis in Iran: a systematic review and meta-analysis. Journal of Helminthology (in press).
Kia, EB, Rahimi, H, Sharbatkhori, M, Talebi, A, Harandi, MF and Mirhendi, H (2010) Genotype identification of human cystic echinococcosis in Isfahan, central Iran. Parasitology Research 107, 757760.
Latif, AA, Tanveer, A, Maqbool, A, Siddiqi, N, Kyaw-Tanner, M and Traub, RJ (2010) Morphological and molecular characterisation of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Veterinary Parasitology 170, 4449.
Majidiani, H, Dalvand, S, Daryani, A, de la Luz Galvan-Ramirez, M and Foroutan-Rad, M (2016) Is chronic toxoplasmosis a risk factor for diabetes mellitus? A systematic review and meta-analysis of case–control studies. The Brazilian Journal of Infectious Diseases 20, 605609.
Maldonado, LL, Assis, J, Araújo, FMG et al. (2017) The Echinococcus canadensis (G7) genome: a key knowledge of parasitic platyhelminth human diseases. BMC Genomics 18, 204.
Maleki, B, Khorshidi, A, Gorgipour, M, Mirzapour, A, Majidiani, H and Foroutan, M (2017) Prevalence of Toxocara spp. eggs in soil of public areas in Iran: a systematic review and meta-analysis. Alexandria Journal of Medicine (in press).
Moazeni, M, Taghipoor, S, Abolhasani, M, Hashemzadeh, M, Zarean, E and Darani, HY (2013) Molecular characterization of the human and sheep hydatid cyst strains in Chaharmahal va Bakhtiari province of Iran using restriction fragment length polymorphism (PCR RFLP). Applied Cell Biology 2, 7883.
Mobedi, I and Dalimi, A (1994) Epidemiology of hydatid cyst in Iran and world. Tehran: Moghaddam Publication, 132147.
Mobedi, I, Zare-Bidaki, M, Siavashi, M, Naddaf, S, Kia, E and Mahmoudi, M (2013) Differential detection of Echinococcus spp. copro-DNA by nested-PCR in domestic and wild definitive hosts in Moghan Plain, Iran. Iranian Journal of Parasitology 8, 107113.
Moher, D, Liberati, A, Tetzlaff, J, Altman, DG and the PRISMA Group (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. International Journal of Surgery 8, 336341.
Muzulin, PM, Kamenetzky, L, Gutierrez, AM, Guarnera, EA and Rosenzvit, MC (2008) Echinococcus granulosus antigen B gene family: further studies of strain polymorphism at the genomic and transcriptional levels. Experimental Parasitology 118, 156164.
Nejad, MR, Taghipour, N, Nochi, Z, Mojarad, EN, Mohebbi, SR, Harandi, MF and Zali, MR (2012) Molecular identification of animal isolates of Echinococcus granulosus from Iran using four mitochondrial genes. Journal of Helminthology 86, 485492.
Nikmanesh, B, Mirhendi, H, Ghalavand, Z, Alebouyeh, M, Sharbatkhori, M, Kia, E, Mohebali, M, Eghbali, M and Rokni, MB (2014) Genotyping of Echinococcus granulosus isolates from human clinical samples based on sequencing of mitochondrial genes in Iran, Tehran. Iranian Journal of Parasitology 9, 2027.
Oskouei, MM, Mehrabani, NG, Miahipour, A and Fallah, E (2016) Molecular characterization and sequence analysis of Echinococcus granulosus from sheep isolates in East Azerbaijan province, northwest of Iran. Journal of Parasitic Diseases 40, 785790.
Parsa, F, Haghpanah, B, Pestechian, N and Salehi, M (2011) Molecular epidemiology of Echinococcus granulosus strains in domestic herbivores of Lorestan, Iran. Jundishapur Journal of Microbiology 4, 123130.
Parsa, F, Harandi, MF, Rostami, S and Sharbatkhori, M (2012) Genotyping Echinococcus granulosus from dogs from Western Iran. Experimental Parasitology 132, 308312.
Pestechian, N, Safa, AH, Tajedini, M, Rostami-Nejad, M, Mousavi, M, Yousofi, H and Javanmard, SH (2014) Genetic diversity of Echinococcus granulosus in center of Iran. The Korean Journal of Parasitology 52, 413418.
Pezeshki, A, Akhlaghi, L, Sharbatkhori, M, Razmjou, E, Oormazdi, H, Mohebali, M and Meamar, AR (2013) Genotyping of Echinococcus granulosus from domestic animals and humans from Ardabil Province, northwest Iran. Journal of Helminthology 87, 387391.
Pour, AA, Hosseini, SH and Shayan, P (2011) Comparative genotyping of Echinococcus granulosus infecting buffalo in Iran using cox1 gene. Parasitology Research 108, 12291234.
Rahimi, HR, Kia, EB, Mirhendi, SH, Talebi, A, Harandi, MF, Jalali-Zand, N and Rokni, MB (2007) A new primer pair in ITS1 region for molecular studies on Echinococcus granulosus. Iranian Journal of Public Health 36, 4549.
Rajabloo, M, Hosseini, SH and Jalousian, F (2012) Morphological and molecular characterisation of Echinococcus granulosus from goat isolates in Iran. Acta Tropica 123, 6771.
Rojas, CAA, Romig, T and Lightowlers, MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. International Journal for Parasitology 44, 918.
Rokni, M (2009) Echinococcosis/hydatidosis in Iran. Iranian Journal of Parasitology 4, 116.
Rostami Nejad, M, Nazemalhosseini Mojarad, E, Taghipour, N, Nochi, Z, Cheraghipour, K, Dabiri, H, Mohebbi, SR, Noorinayer, B and Zali, MR (2011) Molecular determination of Echinococcus granulosus isolated from hydatid cyst using mitoconderial atp6 gene. Journal of Gorgan University of Medical Sciences 13, 6167.
Rostami, S, Torbaghan, SS, Dabiri, S, Babaei, Z, Mohammadi, MA, Sharbatkhori, M and Harandi, MF (2015) Genetic characterization of Echinococcus granulosus from a large number of formalin-fixed, paraffin-embedded tissue samples of human isolates in Iran. The American Journal of Tropical Medicine and Hygiene 92, 588594.
Sadjjadi, SM, Mikaeili, F, Karamian, M, Maraghi, S, Sadjjadi, FS, Shariat-Torbaghan, S and Kia, EB (2013) Evidence that the Echinococcus granulosus G6 genotype has an affinity for the brain in humans. International Journal for Parasitology 43, 875877.
Sadri, A, Moshfe, A, Doosti, A, Ansari, H, Abidi, H and Ghorbani Dalini, S (2012) Characterization of isolated hydatid cyst from slaughtered livestock in Yasuj industrial slaughterhouse by PCR-RFLP. Armaghane Danesh 17, 243252.
Saki, J, Khademvatan, S, Foroutan-Rad, M and Gharibzadeh, M (2017) Prevalence of intestinal parasitic infections in Haftkel County, southwest of Iran. International Journal of Infection 4, e15593. doi: 10.5812/iji.15593.
Shahnazi, M, Hejazi, H, Salehi, M and Andalib, AR (2011) Molecular characterization of human and animal Echinococcus granulosus isolates in Isfahan, Iran. Acta Tropica 117, 4750.
Sharafi, SM, Rostami-Nejad, M, Moazeni, M, Yousefi, M, Saneie, B, Hosseini-Safa, A and Yousofi-Darani, H (2014) Echinococcus granulosus genotypes in Iran. Gastroenterology and Hepatology from Bed to Bench 7, 8288.
Sharbatkhori, M, Harandi, MF, Mirhendi, H, Hajialilo, E and Kia, EB (2011) Sequence analysis of cox1 and nad1 genes in Echinococcus granulosus G3 genotype in camels (Camelus dromedarius) from central Iran. Parasitology Research 108, 521527.
Sharbatkhori, M, Mirhendi, H, Harandi, MF, Rezaeian, M, Mohebali, M, Eshraghian, M, Rahimi, H and Kia, EB (2010) Echinococcus granulosus genotypes in livestock of Iran indicating high frequency of G1 genotype in camels. Experimental Parasitology 124, 373379.
Sharbatkhori, M, Mirhendi, H, Jex, AR, Pangasa, A, Campbell, BE, Kia, EB, Eshraghian, MR, Harandi, MF and Gasser, RB (2009) Genetic categorization of Echinococcus granulosus from humans and herbivorous hosts in Iran using an integrated mutation scanning-phylogenetic approach. Electrophoresis 30, 26482655.
Shariatzadeh, SA, Spotin, A, Gholami, S, Fallah, E, Hazratian, T, Mahami-Oskouei, M, Montazeri, F, Moslemzadeh, HR and Shahbazi, A (2015) The first morphometric and phylogenetic perspective on molecular epidemiology of Echinococcus granulosus sensu lato in stray dogs in a hyperendemic Middle East focus, northwestern Iran. Parasites & Vectors 8, 409.
Sharifiyazdi, H, Oryan, A, Ahmadnia, S and Valinezhad, A (2011) Genotypic characterization of Iranian camel (Camelus dromedarius) isolates of Echinoccocus granulosus. Journal of Parasitology 97, 251255.
Simsek, S, Balkaya, I, Ciftci, AT and Utuk, AE (2011) Molecular discrimination of sheep and cattle isolates of Echinococcus granulosus by SSCP and conventional PCR in Turkey. Veterinary Parasitology 178, 367369.
Spotin, A, Gholami, S, Nasab, AN, Fallah, E, Oskouei, MM, Semnani, V, Shariatzadeh, SA and Shahbazi, A (2015) Designing and conducting in silico analysis for identifying of Echinococcus spp. with discrimination of novel haplotypes: an approach to better understanding of parasite taxonomic. Parasitology Research 114, 15031509.
Thompson, RCA and Jenkins, DJ (2014) Echinococcus as a model system: biology and epidemiology. International Journal for Parasitology 44, 865877.
Thompson, RCA (2013) Parasite zoonoses and wildlife: one health, spillover and human activity. International Journal for Parasitology 43, 10791088.
Torgerson, PR, Devleesschauwer, B, Praet, N et al. (2015) World Health Organization estimates of the global and regional disease burden of 11 foodborne parasitic diseases, 2010: a data synthesis. PLoS Medicine 12, e1001920. doi: 10.1371/journal.pmed.1001920.
Trachsel, D, Deplazes, P and Mathis, A (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911920.
Utuk, AE, Simsek, S, Koroglu, E and McManus, DP (2008) Molecular genetic characterization of different isolates of Echinococcus granulosus in east and southeast regions of Turkey. Acta Tropica 107, 192194.
Vahedi, A, Mahdavi, M, Ghazanchaei, A and Shokouhi, B (2014) Genotypic characteristics of hydatid cysts isolated from humans in East Azerbaijan Province (2011–2013). Journal of Analytical Research in Clinical Medicine 2, 152157.
Weatherhead, JE, Hotez, PJ and Mejia, R (2017) The global state of helminth control and elimination in children. Pediatric Clinics of North America 64, 867877.
Yakhchali, M and Mardani, K (2011) Study on Echinococcus granulosus genotype diversity in domestic cycle using nucleotide sequence of nda-1 gene. Iran Veterinary Journal 7, 6369.
Yakhchali, M and Mardani, K (2013) A study on Echinococcus granulosus strains using nucleotide sequence of CO-1 gene by PCR-RFLP technique in West Azarbaijan Province, Iran. Urmia Medical Journal 23, 792798.
Yousofi Darani, H, Hashemzadeh, CM, Aliyari, Z, Zebardast, N and Farokhi, E (2007) Molecular characterization of the strains cause sheep-hydatid cyst, in Chaharmahal va Bakhtiary Province using restriction fragment length polymorphism. Journal of Shahrekord University of Medical Sciences 9.
Youssefi, MR, Tabaripour, R, Omrani, VF, Spotin, A and Esfandiari, B (2013) Genotypic characterization of Echinococcus granulosus in Iranian goats. Asian Pacific Journal of Tropical Disease 3, 362366.
Ziadinov, I, Mathis, A, Trachsel, D, Rysmukhambetova, A, Abdyjaparov, TA, Kuttubaev, OT, Deplazes, P and Torgerson, PR (2008) Canine echinococcosis in Kyrgyzstan: using prevalence data adjusted for measurement error to develop transmission dynamics models. International Journal for Parasitology 38, 11791190.