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The present situation of echinococcoses in Mongolia

Published online by Cambridge University Press:  03 August 2015

A. Ito  and
C.M. Budke
A. Ito*
Affiliation:
Department of Parasitology and NTD Research Laboratory, Asahikawa Medical University, Midorigaoka Higashi 2-1-1-1, Asahikawa078-8510, Japan
C.M. Budke
Affiliation:
Department of Veterinary Integrative Biosciences, College of Veterinary Medicine & Biomedical Sciences, Texas A & M University, College Station, TX77843-4458, USA
*
*E-mail: [email protected]
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Abstract

This review presents the historical and current situation of echinococcoses in Mongolia. Since the collapse of the Soviet Union in 1991, Mongolia's health surveillance infrastructure has been very poor, especially as it pertains to chronic diseases, including neglected zoonotic diseases (NZDs). Although there is anecdotal evidence of people dying from hepatic disease due to infection with the larval stage of Echinococcus spp., there are very few published reports. All confirmed cases of echinococcoses in Mongolia are from hospitals located in the capital city of Ulaanbaatar. Cases of cystic echinococcosis (CE), caused by either Echinococcus granulosus sensu stricto or Echinococcus canadensis are believed to be relatively common throughout Mongolia. In contrast, cases of alveolar echinococcosis (AE), caused by Echinococcus multilocularis, are believed to be rare. Recent wild-animal surveys have revealed that wolves (Canis lupus) are the major definitive hosts of E. canadensis, whereas both wolves and red foxes (Vulpes vulpes) are the primary definitive hosts of E. multilocularis. Although wild-animal surveys have begun to elucidate the transmission of Echinococcus spp. in Mongolia, there have yet to be large-scale studies conducted in domestic dogs and livestock. Therefore, further epidemiological studies, in addition to education-based control campaigns, are needed to help combat this NZD.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 6 , November 2015 , pp. 680 - 688
Copyright
Copyright © Cambridge University Press 2015 

Introduction

Echinococcoses, including cystic echinococcosis (CE) and alveolar echinococcosis (AE), are considered important yet neglected zoonotic diseases (NZDs) (Craig et al., Reference Craig, Deshan, Macpherson, Dazhong, Reynolds, Barnish, Gottstein and Zhirong1992, Reference Craig, Giraudoux, Shi, Bartholomot, Barnish, Delattre, Quere, Harraga, Bao, Wang, Lu, Ito and Vuitton2000, Reference Craig, McManus, Lightowlers, Chabalgoity, Garcia, Gavidia, Gilman, Gonzalez, Lorca, Naquira, Nieto and Schantz2007; McManus et al., Reference McManus, Zhang, Li and Bartley2003; Schantz et al., Reference Schantz, Wang, Qiu, Liu, Saito, Emshoff, Ito, Roberts and Delker2003; Eckert & Deplazes, Reference Eckert and Deplazes2004; Ito et al., Reference Ito, Craig and Schantz2006, Reference Ito, Zhou, Craig and Giraudoux2013a; Budke et al., Reference Budke, Deplazes and Torgerson2006; Brunetti et al., Reference Brunetti, Kern and Vuitton2010, Reference Brunetti, Garcia and Junghanss2011; Torgerson et al., Reference Torgerson, Keller, Magnotta and Ragland2010; Hotez & Alibek, Reference Hotez and Alibek2011; Carmena & Cardona, Reference Carmena and Cardona2013; Torgerson, Reference Torgerson2013). The prevalence of these conditions is underestimated, due to a lack of reporting, in almost all developing endemic countries, including Mongolia. In addition to under-reporting, many endemic countries do not have access to appropriate diagnostic tools with which to confirm a diagnosis of CE or AE, with many cases likely misdiagnosed as liver cancer.

Due to their differing life cycles, distinct risk factors have been identified for the acquisition of CE and AE. Infection with CE has been associated with a pastoral life style, since the life cycle of Echinococcus granulosus sensu stricto is typically maintained between dogs and livestock. As the Mongolian people are largely nomadic, it is not unexpected that CE would be prevalent in this country (Ebright et al., Reference Ebright, Altantsetseg and Oyungerel2003). In contrast, AE is expected to be less common, since the Echinococcus multilocularis life cycle is typically maintained between wild canids (e.g. foxes and wolves) and small mammals. However, under-diagnosis may also contribute to the small number of reported AE cases (Ito et al., Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014).

While earlier works indicated the presence of echinococcoses in the former Soviet Union and Mongolia (Rausch, Reference Rausch1952, Reference Rausch, Thompson and Lymbery1995, Reference Rausch2003; Abuladze, Reference Abuladze and Skrjabin1964; Bessonov, Reference Bessonov1998, Reference Bessonov, Craig and Pawlowski2003), there are few actual case reports from this region (Bessonov, Reference Bessonov1998, Reference Bessonov, Craig and Pawlowski2003; Wang et al., Reference Wang, He, Wen, Li, Waili, Zhang, Zhou, Zhang, Wen, Davaadorj, Gambolt, Mukhar, Rogan and Craig2005; Lukmanova et al., Reference Lukmanova, Gumenov, Nartaĭlakov, Bilalov and Baĭmiev2007; Ito et al., Reference Ito, Agvaandaram, Bat-Ochir, Chuluunbaatar, Conchigsenghe, Yanagida, Sako, Myyadagsuren, Dorjsuren, Nakaya, Nakao, Ishikawa, Davaajav and Dulmaa2010, Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014; Jabbar et al., Reference Jabbar, Narankhajid, Nolan, Jex, Campbell and Gasser2011; Konyaev et al., Reference Konyaev, Yanagida, Ingovatova, Shoilhet, Nakao, Sako, Bondarev and Ito2012a, Reference Konyaev, Yanagida, Ivanov, Ruppel, Sako, Nakao and Itob, Reference Konyaev, Yanagida, Nakao, Ingovatova, Shoykhet, Bondarev, Odnokurtsev, Loskutova, Lukmanova, Dokuchaev, Spidonov, Alshinecky, Sivkova, Andreyanov, Abramov, Krivopalov, Karpenko, Lopatina, Dupal, Sako and Ito2013; Nakao et al., Reference Nakao, Lavikainen, Yanagida and Ito2013a, Reference Nakao, Yanagida, Konyaev, Lavikainen, Odnokurtsev, Zaikov and Itob). In fact, the number of AE and CE cases is likely underestimated for all of Central Asia (Torgerson & Budke, Reference Torgerson and Budke2003; Hotez & Alibek, Reference Hotez and Alibek2011; Torgerson, Reference Torgerson2013; Zhang et al., Reference Zhang, Zhang, Wu, Shi, Li, Zhou, Wen and McManus2015). For example, while there are only approximately 200 AE cases confirmed in Kyrgyzstan, more recent reports indicate that this number should be closer to 700 (Sato, Japanese Embassy, Bishkek, pers. comm.). Similar situations are expected from other Central Asian countries, including Tajikistan, Turkmenistan, Uzbekistan and Mongolia (Torgerson et al., Reference Torgerson, Keller, Magnotta and Ragland2010; Torgerson, Reference Torgerson2013; Zhang et al., Reference Zhang, Zhang, Wu, Shi, Li, Zhou, Wen and McManus2015).

Furthermore, recent molecular studies have revealed that E. granulosus sensu lato is not a single species, but rather a complex of five independent species: E. granulosus sensu stricto (G1–3), Echinococcus equinus (G4), Echinococcus ortleppi (G5), Echinococcus canadensis (G6–10) and Echinococcus felidis (Nakao et al., Reference Nakao, McManus, Schantz, Craig and Ito2007, Reference Nakao, Lavikainen, Yanagida and Ito2013a, Reference Nakao, Yanagida, Konyaev, Lavikainen, Odnokurtsev, Zaikov and Itob; Alvarez Rojas et al., Reference Alvarez Rojas, Romig and Lightowlers2014), with CE not only caused by E. granulosus sensu stricto (G1–3) but also by E. canadensis (mainly G6/7) (Lavikainen et al., Reference Lavikainen, Lehtinen, Laaksonen, Ågren, Oksanen and Meri2006; Hüttner et al., Reference Hüttner, Siefert, Mackenstedt and Romig2009; Saarma et al., Reference Saarma, Jõgisalu, Moks, Varcasia, Lavikainen, Oksanen, Simsek, Andresluk, Denegri, González, Ferrer, Gárate, Rinaldi and Maravilla2009; Šnábel et al., Reference Šnábel, Altintas, D'Amelio, Nakao, Romig, Yolasigmaz, Gunes, Turk, Busi, Hüttner, Sevcova, Ito, Altintas and Dubinský2009; Nakao et al., Reference Nakao, Li, Han, Ma, Xiao, Qiu, Wang, Yanagida, Mamuti, Wen, Moro, Giraudoux, Craig and Ito2010, Reference Nakao, Lavikainen, Yanagida and Ito2013a, Reference Nakao, Yanagida, Konyaev, Lavikainen, Odnokurtsev, Zaikov and Itob; Omer et al., Reference Omer, Dinkel, Romig, Mackenstedt, Elnahas, Aradaib, Ahmed, Elmalik and Adam2010; Jabbar et al., Reference Jabbar, Narankhajid, Nolan, Jex, Campbell and Gasser2011; Hailemariam et al., Reference Hailemariam, Nakao, Menkir, Lavikainen, Yanagida, Okamoto and Ito2012; Ito et al., Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013b, Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014; Konyaev et al., Reference Konyaev, Yanagida, Nakao, Ingovatova, Shoykhet, Bondarev, Odnokurtsev, Loskutova, Lukmanova, Dokuchaev, Spidonov, Alshinecky, Sivkova, Andreyanov, Abramov, Krivopalov, Karpenko, Lopatina, Dupal, Sako and Ito2013; Mbaya et al., Reference Mbaya, Magambo, Njenga, Zeyhle, Mbae, Mulinge, Wassermann, Kern and Romig2014; Monteiro et al., Reference Monteiro, Botton, Tonin, Azevedo, Graichen, Noal and de la Rue2014; Rodriguez-Prado et al., Reference Rodriguez-Prado, Jimenez-Gonzalez, Avila, Gonzalez, Martinez-Flores, de la Peña, Hernandoz-Castro, Romero-Valdovinos, Flisser, Martinez-Herandez, Maravilla and Martinez-Maya2014; Schurer et al., Reference Schurer, Gesy, Elkin and Jenkins2014) and E. ortleppi (Bowles et al., Reference Bowles, van Knappen and McManus1992; de la Rue et al., Reference de la Rue, Takano, Brochado, Costa, Soares, Yamano, Yagi, Katoh and Takahashi2011; Grenouillet et al., Reference Grenouillet, Umhang, Arbez-Gindre, Mantion, Delabrousse, Millon and Boue2014).

CE due to E. canadensis is rather common in Europe (Dybicz et al., Reference Dybicz, Gierczak, Dąbrowska, Rdzanek and Michałowicz2013), Central Asia (Ziadinov et al., Reference Ziadinov, Mathis, Trachsel, Rysmukhambetova, Abdyjaparov, Kuttubaev, Deplazes and Torgerson2008; Van Kesteren et al., 2013; Zhang et al., Reference Zhang, Zhang, Wu, Shi, Li, Zhou, Wen and McManus2015), China (Bart et al., Reference Bart, Abdukader, Zhang, Lin, Wang, Nakao, Ito, Craig, Piarroux, Vuitton and Wen2006; Zhang et al., Reference Zhang, Yang, Zeng, Zhao, Liu, Piao, Jiang, Cao, Shen, Liu and Zhang2014; Ma et al., Reference Ma, Wang, Lin, Zhao, Li, Zhang, Ma, Zhang, Hou, Cai, Liu and Wang2015; Yang et al., Reference Yang, Zhang, Zeng, Zhao, Zhang and Liu2015) and Mongolia (Jabbar et al., Reference Jabbar, Narankhajid, Nolan, Jex, Campbell and Gasser2011; Ito et al., Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014). Although CE cases are known to be caused by multiple species, E. granulosus s.s. is believed to result in the majority of human cases. However, since the species have different life cycles and means of transmission to humans, molecular identification of the causative species for human CE cases is essential. Molecular identification will allow for improved understanding of the disease's pathogenesis and better-targeted control measures, since imaging and serology, or even histopathology, cannot provide a definitive diagnosis of the causative species.

Review

In Mongolia, there are very few hospital-based reports of human echinococcoses (Ebright et al., Reference Ebright, Altantsetseg and Oyungerel2003; Abmed et al., Reference Abmed, Ganbold and Otgontsetseg2005; Gurbadam et al., Reference Gurbadam, Nyamkhuu, Nyamkhuu, Tsendjav, Sergelen, Narantuya, Batsukh, Battsetseg, Oyun-Erdene, Uranchimeg, Otgonbaatar, Temuulen, Bayarmaa, Abmed, Tsogtsaikhan, Usukhbayar, Smirmaul, Gereltuya and Ito2010; Ito et al., Reference Ito, Agvaandaram, Bat-Ochir, Chuluunbaatar, Conchigsenghe, Yanagida, Sako, Myyadagsuren, Dorjsuren, Nakaya, Nakao, Ishikawa, Davaajav and Dulmaa2010, Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014; Jabbar et al., Reference Jabbar, Narankhajid, Nolan, Jex, Campbell and Gasser2011) and only a few community-based screening studies (Watson-Jones et al., Reference Watson-Jones, Craig, Badamochir, Rogan, Wen and Hind1997; Lee et al., Reference Lee, Chung, Lee, Nam and Kim1999; Wang et al., Reference Wang, He, Wen, Li, Waili, Zhang, Zhou, Zhang, Wen, Davaadorj, Gambolt, Mukhar, Rogan and Craig2005; Huh et al., Reference Huh, Yu, Kim, Gotov, Janchiv and Seo2006).

Human echinococcoses

Hospital reports of human echinococcoses

The vast majority of clinical cases of echinococcoses in Mongolia are managed by surgeons. In 1950, 7.8% of all surgical patients in Mongolia were diagnosed with CE, whereas this value had decreased to 1.9% by 1990 (Cross, Reference Cross1995; Davaatseren et al., Reference Davaatseren, Otogondalai, Nyamkhuu and Susher1995; Abmed et al., Reference Abmed, Ganbold and Otgontsetseg2005). However, CE was diagnosed in 18% of surgical cases treated at the First Hospital of Ulaanbaatar in 1993 (Cross, Reference Cross1995). While this value is very high, it most likely reflects the fact that this is a referral hospital and is much more likely to see CE cases compared to smaller, more rural hospitals. To date, all surgical echinococcosis cases have been confirmed to be due to CE except for five cases of AE (Davaatseren et al., Reference Davaatseren, Otogondalai, Nyamkhuu and Susher1995; Ebright et al., Reference Ebright, Altantsetseg and Oyungerel2003; Gurbadam et al., Reference Gurbadam, Nyamkhuu, Nyamkhuu, Tsendjav, Sergelen, Narantuya, Batsukh, Battsetseg, Oyun-Erdene, Uranchimeg, Otgonbaatar, Temuulen, Bayarmaa, Abmed, Tsogtsaikhan, Usukhbayar, Smirmaul, Gereltuya and Ito2010; Ito et al., Reference Ito, Agvaandaram, Bat-Ochir, Chuluunbaatar, Conchigsenghe, Yanagida, Sako, Myyadagsuren, Dorjsuren, Nakaya, Nakao, Ishikawa, Davaajav and Dulmaa2010, Reference Ito, Okamoto, Li, Wandra, Dharmawan, Swastika, Dekumyoy, Kusolsuk, Davajav, Davaasuren, Dorjsuren, Mekonnen, Negashi, Yanagida, Sako, Nakao, Nakaya, Lavikainen, Nkouawa and Mohammadzadeh2011). The first case of AE was reported in 1982. However, very little demographic information is available about this case. The other four cases were confirmed in 2002, 2006, 2007 and 2009, with the patients born in the provinces of Orkhon-Uul, Uvs, Khovd and Bayan-Ulgii, respectively (fig. 1) (Ito et al., Reference Ito, Agvaandaram, Bat-Ochir, Chuluunbaatar, Conchigsenghe, Yanagida, Sako, Myyadagsuren, Dorjsuren, Nakaya, Nakao, Ishikawa, Davaajav and Dulmaa2010).

Fig. 1 Distribution of Echinococcus spp. from red fox (Vulpus vulpus) and wolves (Canis lupus) (Ito et al., Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013b). *One lacustrine vole (Microtus limnophilus) confirmed to be infected with E. multilocularis (Gardner et al., 2013). # Provinces where four AE patients were identified (Ito et al., Reference Ito, Agvaandaram, Bat-Ochir, Chuluunbaatar, Conchigsenghe, Yanagida, Sako, Myyadagsuren, Dorjsuren, Nakaya, Nakao, Ishikawa, Davaajav and Dulmaa2010).

Molecular studies

There was no molecular identification of the causative species of echinococcoses in Mongolia until 2010. Molecular studies conducted on histopathological specimens from three AE patients (Ito et al., Reference Ito, Agvaandaram, Bat-Ochir, Chuluunbaatar, Conchigsenghe, Yanagida, Sako, Myyadagsuren, Dorjsuren, Nakaya, Nakao, Ishikawa, Davaajav and Dulmaa2010) revealed that the cases were caused by two distinct E. multilocularis genotypes, the Asian and Mongolian genotypes (Nakao et al., Reference Nakao, Xiao, Okamoto, Yanagida, Sako and Ito2009). In addition, molecular differentiation of CE cases caused by E. granulosus s.s. and E. canadensis G6/7 and G10 have been published (Jabbar et al., Reference Jabbar, Narankhajid, Nolan, Jex, Campbell and Gasser2011; Ito et al., Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014) (fig. 2). These reports confirmed the presence of CE cases caused by both E. granulosus s.s. and E. canadensis from numerous provinces in western Mongolia. Specifically, CE cases due to E. canadensis (G10) have been confirmed from the provinces of Tuv (Ito et al., Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013b) and Uvurkhangai (Jabbar et al., Reference Jabbar, Narankhajid, Nolan, Jex, Campbell and Gasser2011). In addition, CE cases caused by E. canadensis (G6/7) have been confirmed from 13 provinces, including Uvurkhangai. While human CE cases caused by E. canadensis (G10) have yet to be identified in Zavkhan, this species has been found in local wolves (Canis lupus) (Ito et al., Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013b) (fig. 1). Therefore, human CE cases caused by E. canadensis (G10) are also likely to occur in this province.

Serological studies

Serology using recombinant antigen B (rAgB8/1) (Mamuti et al., Reference Mamuti, Yamasaki, Sako, Nakao, Xiao, Nakaya, Sato, Vuitton, Piarroux, Lightowlers, Craig and Ito2004) has been applied to CE cases in Mongolia. An enzyme-linked immunosorbent assay (ELISA) using rAgB8/1 positively identified 9 of 10 (90%) and 13 of 20 (65%) CE cases caused by E. granulosus s.s. and E. canadensis (G6/7), respectively (Ito et al., Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014). Most of the evaluated CE cases were from Ulaanbaatar, where more than 50% of the population of Mongolia lives. All 18 CE cases in children were due to E. canadensis. Additional information is needed to evaluate differences in serological response, age and pathology of CE cases caused by E. granulosus s.s. and E. canadensis. Introduction of a rapid diagnostic kit (Ito & Budke, Reference Ito and Budke2014) or routine ELISA and immunoblot using recombinant antigens would help improve diagnostics and case identification in Mongolia (Mamuti et al., Reference Mamuti, Yamasaki, Sako, Nakao, Xiao, Nakaya, Sato, Vuitton, Piarroux, Lightowlers, Craig and Ito2004, Reference Mamuti, Sako, Nakao, Xiao, Nakaya, Ishikawa, Yamasaki, Lightowlers and Ito2006, Reference Mamuti, Sako, Bart, Nakao, Ma, Wen and Ito2007; Tamarozzi et al., Reference Tamarozzi, Sako, Ito, Piccoli, Grisolia, Itoh, Gatti, Meroni, Genco, Filice and Brunetti2013).

Community surveys

There are a few older reports using the Casoni skin test to screen for echinococcoses in Mongolia (Jezek et al., Reference Jezek, Rusinko, Mingir and Cerenshimide1971, Reference Jezek, Rachkovsky, Mingir and Galbadrakh1973). More recently, there have been several studies that have used an ELISA to evaluate Mongolian populations. One study identified 5.2% (17/334) of semi-nomadic pastoralists in Bayan-Ulgii as strongly seropositive against E. granulosus native Antigen B using an ELISA (Watson-Jones et al., Reference Watson-Jones, Craig, Badamochir, Rogan, Wen and Hind1997). Another study found that 8.5% (12/141) of the inhabitants of rural areas near Ulaanbaatar (Lee et al., Reference Lee, Chung, Lee, Nam and Kim1999), 2.1% (4/187) of the inhabitants of Dornod in eastern Mongolia, and 11.7% (58/496) of the inhabitants of Selenge in north-central Mongolia were positive against crude hydatid cyst fluid by ELISA (Huh et al., Reference Huh, Yu, Kim, Gotov, Janchiv and Seo2006). However, the reliability of serology is based on the quality of the diagnostic antigens and the type of control population used to evaluate the test and its findings (Mamuti et al., Reference Mamuti, Yamasaki, Sako, Nakaya, Nakao, Lightowlers and Ito2002; Ito, 2013, Reference Ito2015). It is, therefore, important to confirm cases with ultrasound and histopathology whenever possible.

Animal echinococcoses in Mongolia

There is one review article focusing on the animal hosts of Echinococcus spp. in Mongolia (Abmed et al., Reference Abmed, Ganbold and Otgontsetseg2005). In addition, there are two reports of dog surveys for Echinococcus spp. in the country (Zoljargal et al., Reference Zoljargal, Ganzorig, Nonaka, Oku and Kamiya2001; Wang et al., Reference Wang, He, Wen, Li, Waili, Zhang, Zhou, Zhang, Wen, Davaadorj, Gambolt, Mukhar, Rogan and Craig2005). Zoljargal et al. (Reference Zoljargal, Ganzorig, Nonaka, Oku and Kamiya2001) used a copro-antigen test to evaluate 67 dogs and two red foxes in the town of Altai, with 17 dogs and one fox found positive. Since the monoclonal antibody used for this copro-antigen test was not species or genus specific, it was not possible to evaluate the degree to which false positives and false negatives were reported without additional molecular and/or necropsy evidence. In the second study, Wang et al. (Reference Wang, He, Wen, Li, Waili, Zhang, Zhou, Zhang, Wen, Davaadorj, Gambolt, Mukhar, Rogan and Craig2005) reported that 35.7% (5/14) of necropsied dogs were infected with E. granulosus s.s. (G1) in Bulgan Province.

Very little direct evidence exists of Echinococcus species infection in livestock. There is only a single study that reported the findings from sheep (n= 590), goats (n= 338) and cattle (n= 779) screened serologically using recombinant Antigen B (8/1) (rAgB8/1) (Chinchuluun et al., Reference Chinchuluun, Sako, Khatanbaatar, Bayamaa, Lkhagvatseren, Battsetseg, Yanagida, Itoh, Temuulen, Budke, Ito and Batsukh2014). All serum samples were collected from the serum bank at the Institute of Veterinary Medicine in Ulaanbaatar, with samples available from 19 of the 22 Mongolian provinces. Seropositive cattle were identified from 13 provinces, with 18.0% (9/50) of cattle samples from Ulaanbaatar seropositive. Since molecular studies have not been conducted in Mongolian cattle, it is not known if any of these infections were due to other species, such as E. ortleppi (G5).

While camels are an important livestock species in some regions of Mongolia, serological studies have not been conducted for camels since, at present, there is no good secondary antibody to detect antibody responses. However, camels have been found to be infected with E. granulosus s.l. in Mongolia (Chinchuluun, unpublished) and other endemic regions of the world. Therefore, molecular identification of Echinococcus spp. infection in all locally important livestock species is needed to better understand the life cycles of the circulating Echinococcus species.

Recent surveys of wild animals have revealed that both wolves (C. lupus) and red foxes (Vulpes vulpes) are definitive hosts of E. multilocularis in Mongolia, whereas thus far only wolves have been identified as definitive hosts of E. canadensis (G6/7 and G10) (Ito et al., Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013b). The Mongolian E. multilocularis genotype has been found in wild canids throughout Mongolia (fig. 1). In contrast, E. canadensis has only been identified in a few provinces in western Mongolia. In 2012, Gardner et al. (Reference Gardner, Dursahinhan, Racz, Batsaikhan, Ganzorig, Tinnin, Damdinbazar, Wood, Peterson, Alandia, Molericona and Salazar-Bravo2013) found one lacustrine vole (Microtus limnophilus) infected with E. multilocularis from Khovd Province (fig. 1). To the authors’ knowledge, this is the only Mongolian small mammal confirmed to be infected with E. multilocularis (GenBank #AB271235) (Gardner et al., Reference Gardner, Dursahinhan, Racz, Batsaikhan, Ganzorig, Tinnin, Damdinbazar, Wood, Peterson, Alandia, Molericona and Salazar-Bravo2013). Brandt’ vole (Microtus brandtii) is a known intermediate host of the Mongolian genotype in Inner Mongolia, China (Tang et al., Reference Tang, Chen, Tang, Cui, Qian, Kang and Lu2001, Reference Tang, Quian, Kang, Cui, Lu, Shu, Wang and Tang2004, Reference Tang, Wang, Peng, Tang and Chen2006, Reference Tang, Cui, Qian, Kang, Wang, Peng, Lu and Chen2007). However, to date, this small mammal species has not been identified as an intermediate host in Mongolia.

Echinococcoses in neighbouring countries

A number of studies evaluating the prevalence of AE and CE have been conducted in the neighbouring country of China (Craig et al., Reference Craig, Deshan, Macpherson, Dazhong, Reynolds, Barnish, Gottstein and Zhirong1992, Reference Craig, Giraudoux, Shi, Bartholomot, Barnish, Delattre, Quere, Harraga, Bao, Wang, Lu, Ito and Vuitton2000, Reference Craig2006, Reference Craig, Li, Qiu, Zhen, Wang, Giraudoux, Ito, Heath, Warnock, Schantz and Yang2008; Andersen et al., Reference Andersen, Chai and Liu1993; Schantz et al., Reference Schantz, Wang, Qiu, Liu, Saito, Emshoff, Ito, Roberts and Delker2003; Tiaoying et al., Reference Tiaoying, Jiamin, Wen, Craig, Xingwang, Ning, Ito, Giraudoux, Wulamu, Wen and Schantz2005; T. Li et al., Reference Li, Ito, Nakaya, Qiu, Nakao, Zhen, Xiao, Chen, Giraudoux and Craig2008, Reference Li, Ito, Pengcuo, Sako, Chen, Qiu, Xiao and Craig2011; Zhang et al., Reference Zhang, Yang, Zeng, Zhao, Liu, Piao, Jiang, Cao, Shen, Liu and Zhang2014; D. Li et al., Reference Li, Gao, Liu, Feng, Ning, Eong, Tao, Li, Tian, Gu and Xin2015). However, only a few of these studies have identified the causative species of CE (Y.R. Yang et al., Reference Yang, Rorenzvit, Zhang, Zhang and McManus2005; Bart et al., Reference Bart, Abdukader, Zhang, Lin, Wang, Nakao, Ito, Craig, Piarroux, Vuitton and Wen2006; Li et al., Reference Li, Ito, Nakaya, Qiu, Nakao, Zhen, Xiao, Chen, Giraudoux and Craig2008; Nakao et al., Reference Nakao, Li, Han, Ma, Xiao, Qiu, Wang, Yanagida, Mamuti, Wen, Moro, Giraudoux, Craig and Ito2010; Zhang et al., Reference Zhang, Yang, Zeng, Zhao, Liu, Piao, Jiang, Cao, Shen, Liu and Zhang2014; Ma et al. Reference Ma, Wang, Lin, Zhao, Li, Zhang, Ma, Zhang, Hou, Cai, Liu and Wang2015; D. Yang et al., Reference Yang, Zhang, Zeng, Zhao, Zhang and Liu2015). As both CE and AE are highly endemic in the Chinese provinces of Xinjiang, Gansu and Inner Mongolia, which share a border with Mongolia, it is suspected that there are additional unreported cases occurring in the border areas of Mongolia.

Limited comparative studies are available on the frequency of Echinococcus spp. infection in ethnically Mongolian communities located in Mongolia and across the border in China. Wang et al. (Reference Wang, He, Wen, Li, Waili, Zhang, Zhou, Zhang, Wen, Davaadorj, Gambolt, Mukhar, Rogan and Craig2005) evaluated the ultrasound-based prevalence of human CE in the communities of Hobukesar, in Xinjiang Province, China and Bulgan, in western Mongolia, and found a significantly higher prevalence in the community located in China (2.7% (49/1844)) compared to the community in Mongolia (0.2% (4/1609)). This same study also evaluated necropsy-based infection prevalence in dogs located in these two communities, but did not find a significant difference in the frequency of infection. The authors attributed the lower prevalence of CE in residents of Bulgan to Soviet Union administered dog deworming programmes that were common in Mongolia until the mid-1980s. There are relatively few reports, in the English language literature, on CE and AE in bordering regions of Russia (Rausch, Reference Rausch1952, Reference Rausch, Thompson and Lymbery1995, Reference Rausch2003; Abuladze, Reference Abuladze and Skrjabin1964; Bessonov, Reference Bessonov1998, Reference Bessonov, Craig and Pawlowski2003; Konyaev et al., Reference Konyaev, Yanagida, Ingovatova, Shoilhet, Nakao, Sako, Bondarev and Ito2012a, Reference Konyaev, Yanagida, Ivanov, Ruppel, Sako, Nakao and Itob, Reference Konyaev, Yanagida, Nakao, Ingovatova, Shoykhet, Bondarev, Odnokurtsev, Loskutova, Lukmanova, Dokuchaev, Spidonov, Alshinecky, Sivkova, Andreyanov, Abramov, Krivopalov, Karpenko, Lopatina, Dupal, Sako and Ito2013). However, recent molecular studies have confirmed the presence of all four E. multilocularis genotypes in Russia, as well as the presence of E. granulosus s.s. and E. canadensis (G6/7 and G10) (Nakao et al., Reference Nakao, Yanagida, Konyaev, Lavikainen, Odnokurtsev, Zaikov and Ito2013b).

General discussion

There is now evidence that both E. granulosus s.s. and E. canadensis G6/7 and G10 are distributed in Mongolia (Jabbar et al., Reference Jabbar, Narankhajid, Nolan, Jex, Campbell and Gasser2011; Ito et al., Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013b, Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014). However, additional species such as E. ortleppi may yet be detected. Due to the presence of these zoonotic parasites, there is an urgent need to establish a centralized repository for data on Mongolian echinococcoses cases. As part of this initiative, all histopathology specimens should be further identified using molecular tools. Questions remain on whether or not cases of CE caused by E. canadensis are more benign compared to cases caused by E. granulosus s.s. Evidence from Alaska and Canada also suggests that lung cysts caused by E. canadensis are typically smaller than those caused by E. granulosus s.s. (Wilson et al., Reference Wilson, Diddams and Rausch1968; Pinch & Wilson, Reference Pinch and Wilson1973; Finlay & Speert, Reference Finlay and Speert1992; Lamy et al., Reference Lamy, Cameron, LeBlanc, Culham, Blair and Taylor1993; Rausch, Reference Rausch2003). Thus far, there has been no differentiation between CE cases caused by E. granulosus s.s. and E. canadensis when it comes to standardization and assessment of pathology, imaging, treatment and evaluation of serology (Ito, Reference Ito2015). Therefore, Mongolia may be an ideal location to investigate these differences between the circulating Echinococcus species.

Further systematic studies are essential to better elaborate the epidemiology of, and to guide control measures for, echinococcoses in Mongolia. Although CE caused by both E. canadensis and E. granulosus s.s. is found in residents of Ulaanbaatar, the age distribution of cases appears to differ between the two species (Ito et al., Reference Ito, Dorjsuren, Davaasuren, Yanagida, Sako, Nakaya, Nakao, Bat-Ochir, Ayushkhuu, Bazarragchaa, Gonchigsengee, Li, Agvaandaram, Davaajav, Boldbaatar and Chuluunbaatar2014). Thus far, there have been no studies to try to identify risk factors associated with Echinococcus spp. infection in and around Ulaanbaatar. Evaluation of stray dogs and wild canids for intestinal infection, and molecular differentiation of the infecting species, would also aid in identifying how human infection may be occurring locally.

Human AE cases from Mongolia have been confirmed to be caused by both the Mongolian and Asian genotypes (Ito et al., Reference Ito, Agvaandaram, Bat-Ochir, Chuluunbaatar, Conchigsenghe, Yanagida, Sako, Myyadagsuren, Dorjsuren, Nakaya, Nakao, Ishikawa, Davaajav and Dulmaa2010). Bretagne et al. (Reference Bretagne, Assouline, Vidaud, Houin and Vidaud1996) was the first to report the existence of three different E. multilocularis genotypes (North American, Asian and European). The Mongolian genotype was first reported from Inner Mongolia, China as the Inner Mongolian genotype (Nakao et al., Reference Nakao, Xiao, Okamoto, Yanagida, Sako and Ito2009). Prior to molecular characterization, the parasite had been described as the new species Echinococcus sibiricensis or Echinococcus russicensis (Tang et al., Reference Tang, Chen, Tang, Cui, Qian, Kang and Lu2001, Reference Tang, Quian, Kang, Cui, Lu, Shu, Wang and Tang2004, Reference Tang, Wang, Peng, Tang and Chen2006, Reference Tang, Cui, Qian, Kang, Wang, Peng, Lu and Chen2007). However, molecular studies revealed that it was, in fact, an intra-species variant of E. multilocularis (Nakao et al., Reference Nakao, McManus, Schantz, Craig and Ito2007, Reference Nakao, Xiao, Okamoto, Yanagida, Sako and Ito2009).

Thus far, all E. multilocularis adult worms from red foxes in Mongolia have been the Mongolian genotype (Ito et al., Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013b), with 7.9% (15/191) of red foxes, but no corsac foxes (0/111), found to be infected with E. multilocularis. However, since there has been a confirmed case of human AE in Mongolia caused by the Asian genotype (Ito et al., Reference Ito, Agvaandaram, Bat-Ochir, Chuluunbaatar, Conchigsenghe, Yanagida, Sako, Myyadagsuren, Dorjsuren, Nakaya, Nakao, Ishikawa, Davaajav and Dulmaa2010), Mongolian wild canids are expected to be infected with this genotype as well. The Mongolian and Asian genotypes have been identified from corsac foxes in Inner Mongolia, China (Tang et al., Reference Tang, Quian, Kang, Cui, Lu, Shu, Wang and Tang2004).

The main definitive host of the Mongolian E. multilocularis genotype has been hypothesized to be the red fox. However, additional molecular testing of adult worms from both red and corsac foxes is needed to confirm or reject this hypothesis. This is especially true since worm abundance may be smaller in corsac foxes as compared to red foxes, and currently available tools (Matoba et al., Reference Matoba, Yamada, Asano, Oku, Kitamura, Yagi, Tenora and Asakawa2006) may not be sensitive enough to detect very small worm burdens (Ito et al., Reference Ito, Chuluunbaatar, Yanagida, Davaasuren, Sumiya, Asakawa, Ki, Nakaya, Davaajav, Dorjsuren, Nakao and Sako2013b). Additional wild canid studies need to be conducted to determine which animals are currently acting as definitive hosts for E. multilocularis in Mongolia.

Human echinococcoses may be substantially under-diagnosed in Mongolia, due to the chronic nature of the disease and the inability of patients to seek care in the large referral hospitals in Ulaanbaatar. Therefore, community-based studies using serology and diagnostic imaging are needed to better elaborate the frequency of infection in the population. Stray dogs were routinely killed when Mongolia was strongly influenced by the former Soviet Union (Wang et al., Reference Wang, He, Wen, Li, Waili, Zhang, Zhou, Zhang, Wen, Davaadorj, Gambolt, Mukhar, Rogan and Craig2005). While this practice might seem cruel to some, it did help control a number of dog-associated zoonotic diseases, including echinococcoses. In an effort to decrease disease spread among dogs and to people, the city council of Ulaanbaatar re-introduced the culling of stray dogs in 2013. However, no parasitological studies have been associated with the culling programme.

Hegglin et al. (Reference Hegglin, Bontadina and Deplazes2015) and Liccioli et al. (Reference Liccioli, Giraudoux, Deplazes and Massolo2015) have discussed that the urban red fox population is increasing in many European cities, as is the risk of AE to those who live in these cities. As Mongolia industrializes, the influx of foxes and other wildlife into the cities will also become more of a problem. It is, therefore, essential that the population is educated about the disease risks that foxes and other wildlife present. Along those same lines, the importance of wolves and free-roaming dogs as definitive hosts should be recognized.

Perspectives

Mongolia currently lacks the resources to assess and address NZDs, including echinococcoses, adequately. Thus far, three expert meetings on echinococcoses have been conducted in Ulaanbaatar, in June 2009, 2012 and 2014 (Gurbadam et al., Reference Gurbadam, Nyamkhuu, Nyamkhuu, Tsendjav, Sergelen, Narantuya, Batsukh, Battsetseg, Oyun-Erdene, Uranchimeg, Otgonbaatar, Temuulen, Bayarmaa, Abmed, Tsogtsaikhan, Usukhbayar, Smirmaul, Gereltuya and Ito2010). In addition, the World Health Organization (WHO) held a one-day meeting on NZDs in September 2012. To date, most human AE and CE data are from the major referral hospitals (State Central First Hospital and National Centre of Maternal and Child Health, etc.) and the National Centre of Pathology in Ulaanbaatar. The National Centre of Pathology has been strongly encouraged to conduct molecular identification of all Echinococcus spp. specimens that it receives. In the spirit of One Health, all personnel involved in the evaluation and control of echinococcoses in Mongolia (National Centre of Communicable Diseases, Mongolian National University of Medical Sciences, National Centre of Zoonotic Diseases, National Institute of Veterinary Medicine, etc.) should work together for the common good. A WHO-supported project aimed at the control of echinococcoses in Mongolia, which would provide education to the general population and train local researchers towards the goal of controlling these diseases, would be very beneficial.

Acknowledgements

The authors sincerely thank numerous collaborators in Mongolia and Japan.

Financial support

The studies carried out by Mongolian and Japanese collaborators were supported by Grant-in-Aid for scientific research (21256003 and 24256002), Asia–Africa Scientific Platform Funds (2006–2008, 2009–2011) from the Japan Society for the Promotion of Science, the Hokkaido Translational Research Fund (2007–2011) and the Special Coordination Fund for Promoting Science and Technology (2003–2005, 2010–2012) from the Ministry of Education, Culture, Sports, Science and Technology in Japan to A.I.

Conflict of interest

None.

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Figure 0

Fig. 1 Distribution of Echinococcus spp. from red fox (Vulpus vulpus) and wolves (Canis lupus) (Ito et al., 2013b). *One lacustrine vole (Microtus limnophilus) confirmed to be infected with E. multilocularis (Gardner et al., 2013). # Provinces where four AE patients were identified (Ito et al., 2010).

Figure 1

Fig. 2 Distribution of human CE cases in Mongolia differentiated into E. granulosus s.s., E. canadensis (G6/7) and E. canadensis (G10) (Jabbar et al., 2011; Ito et al., 2014). Black symbols represent samples from Ito et al. (2014) whereas red symbols represent samples from Jabbar et al. (2011).