Cystic Echinococcoses in Mongolia: Molecular Identification, Serology and Risk Factors

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Abstract

Background

Cystic echinococcosis (CE) is a globally distributed cestode zoonosis that causes hepatic cysts. Although Echinococcus granulosus sensu stricto (s.s.) is the major causative agent of CE worldwide, recent molecular epidemiological studies have revealed that E. canadensis is common in countries where camels are present. One such country is Mongolia.

Methodology/Principal Findings

Forty-three human hepatic CE cases that were confirmed histopathologically at the National Center of Pathology (NCP) in Ulaanbaatar (UB) were identified by analysis of mitochondrial cox 1 gene as being caused by either E. canadensis (n = 31, 72.1%) or E. granulosus s.s. (n = 12, 27.9%). The majority of the E. canadensis cases were strain G6/7 (29/31, 93.5%). Twenty three haplotypes were identified. Sixteen of 39 CE cases with data on age, sex and province of residence were citizens of UB (41.0%), with 13 of the 16 cases from UB caused by E. canadensis (G6/7) (81.3%). Among these 13 cases, nine were children (69.2%). All pediatric cases (n = 18) were due to E. canadensis with 17 of the 18 cases (94.4%) due to strain G6/7. Serum samples were available for 31 of the 43 CE cases, with 22 (71.0%) samples positive by ELISA to recombinant Antigen B8/1 (rAgB). Nine of 10 CE cases caused by E. granulosus s.s. (90.0%) and 13 of 20 CE cases by E. canadensis (G6/7) (65.0%) were seropositive. The one CE case caused by E. canadensis (G10) was seronegative. CE cases caused by E. granulosus s.s. showed higher absorbance values (median value 1.131) than those caused by E. canadensis (G6/7) (median value 0.106) ( p = 0.0137).

Conclusion/Significance

The main species/strains in the study population were E. canadenis and E. granulossus s.s. with E. canadensis the predominant species identified in children. The reason why E. canadensis appears to be so common in children is unknown.

Author Summary

Cystic echinococcosis (CE) is a parasitic zoonosis with a cosmopolitan distribution. Molecular analysis was carried out on 43 hepatic CE cysts from 43 cases confirmed histopathologically at the NCP, Mongolia. Molecular analysis revealed two species, Echinococcus canadensis and Echinococcus granulosus s.s. Twenty three haplotypes of the cox1 gene were identified. All pediatric cases (n = 18) were by E. canadensis. Sixteen of 39 CE cases with data on age, sex and province of residence were from UB (41.0%), and 13 of these 16 cases were caused by E. canadensis (81.3%). Among the 13 cases from UB, nine were children (69.2%). A total of 31 serum samples from these 43 cases were analyzed for antibody response to rAgB with 22 (71.0%) samples positive by ELISA to rAgB. Thirteen of 20 E. canadensis (G6/7) (65%) and nine of 10 E. granulosus s.s. (90%) were seropositive. CE cases by E. granulosus s.s. showed a higher absorbance value than cases by E. canadensis ( p = 0.0137). This is the first study to evaluate age distribution of and antibody responses to rAgB in CE cases caused by the two species in Mongolia. It remains unknown why E. canadensis appears to be more common in pediatric cases.

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Most cited references 53

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Echinococcus granulosus sensu lato genotypes infecting humans--review of current knowledge.

Julio Rojas, Thomas Romig, Marshall Lightowlers (2013)

Genetic variability in the species group Echinococcus granulosus sensu lato is well recognised as affecting intermediate host susceptibility and other biological features of the parasites. Molecular methods have allowed discrimination of different genotypes (G1-10 and the 'lion strain'), some of which are now considered separate species. An accumulation of genotypic analyses undertaken on parasite isolates from human cases of cystic echinococcosis provides the basis upon which an assessment is made here of the relative contribution of the different genotypes to human disease. The allocation of samples to G-numbers becomes increasingly difficult, because much more variability than previously recognised exists in the genotypic clusters G1-3 (=E. granulosus sensu stricto) and G6-10 (Echinococcus canadensis). To accommodate the heterogeneous criteria used for genotyping in the literature, we restrict ourselves to differentiate between E. granulosus sensu stricto (G1-3), Echinococcus equinus (G4), Echinococcus ortleppi (G5) and E. canadensis (G6-7, G8, G10). The genotype G1 is responsible for the great majority of human cystic echinococcosis worldwide (88.44%), has the most cosmopolitan distribution and is often associated with transmission via sheep as intermediate hosts. The closely related genotypes G6 and G7 cause a significant number of human infections (11.07%). The genotype G6 was found to be responsible for 7.34% of infections worldwide. This strain is known from Africa and Asia, where it is transmitted mainly by camels (and goats), and South America, where it appears to be mainly transmitted by goats. The G7 genotype has been responsible for 3.73% of human cases of cystic echinococcosis in eastern European countries, where the parasite is transmitted by pigs. Some of the samples (11) could not be identified with a single specific genotype belonging to E. canadensis (G6/10). Rare cases of human cystic echinococcosis have been identified as having been caused by the G5, G8 and G10 genotypes. No cases of human infection with G4 have been described. Biological differences between the species and genotypes have potential to affect the transmission dynamics of the parasite, requiring modification of methods used in disease control initiatives. Recent investigations have revealed that the protective vaccine antigen (EG95), developed for the G1 genotype, is immunologically different in the G6 genotype. Further research will be required to determine whether the current EG95 vaccine would be effective against the G6 or G7 genotypes, or whether it will be necessary, and possible, to develop genotype-specific vaccines. Copyright © 2013 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.

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A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes.

P. I. Craig, Stimson P Schantz, Akira Ito … (2007)

Taxonomic revision by molecular phylogeny is needed to categorize members of the genus Echinococcus (Cestoda: Taeniidae). We have reconstructed the phylogenetic relationships of E. oligarthrus, E. vogeli, E. multilocularis, E. shiquicus, E. equinus, E. ortleppi, E. granulosus sensu stricto and 3 genotypes of E. granulosus sensu lato (G6, G7 and G8) from their complete mitochondrial genomes. Maximum likelihood and partitioned Bayesian analyses using concatenated data sets of nucleotide and amino acid sequences depicted phylogenetic trees with the same topology. The 3 E. granulosus genotypes corresponding to the camel, pig, and cervid strains were monophyletic, and their high level of genetic similarity supported taxonomic species unification of these genotypes into E. canadensis. Sister species relationships were confirmed between E. ortleppi and E. canadensis, and between E. multilocularis and E. shiquicus, regardless of the analytical approach employed. The basal positions of the phylogenetic tree were occupied by the neotropical endemic species, E. oligarthrus and E. vogeli, whose definitive hosts are derived from carnivores that immigrated from North America after the formation of the Panamanian land bridge. Host-parasite co-evolution comparisons suggest that the ancestral homeland of Echinococcus was North America or Asia, depending on whether the ancestral definitive hosts were canids or felids.

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Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion.

Anke Dinkel, Akira Ito, Thomas Romig … (2008)

Echinococcus felidis had been described in 1937 from African lions, but was later included in Echinococcus granulosus as a subspecies or a strain. In the absence of any genetic characterization, most previous records of this taxon from a variety of large African mammals remained unconfirmed due to the lack of diagnostic criteria and the possible confusion with the sympatric E. granulosus sensu stricto, Echinococcus ortleppi and Echinococcus canadensis. In this study, we obtained taeniid eggs from lion feces in Uganda and amplified DNA from individual eggs. Mitochondrial and nuclear DNA sequences showed similarities with those of other Echinococcus spp., but high values of percentage divergence of mitochondrial genes indicated the presence of a distinct species. In a second step, we compared this material with the preserved specimens of adult E. granulosus felidis, which had been identified morphologically approximately 40 years ago in South Africa. All DNA fragments (<200 bp) that could be amplified from the adults showed 100% similarity with the Ugandan material. In the phylogenetic tree of Echinococcus which was constructed from the mitochondrial genes, E. felidis is positioned as a sister taxon of E. granulosus sensu stricto. The data obtained will facilitate the development of diagnostic tools necessary to study the epidemiology of this enigmatic parasite.

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Author and article information

Contributors

Malcolm K. Jones: Role: Editor

Journal

Journal ID (nlm-ta): PLoS Negl Trop Dis

Journal ID (iso-abbrev): PLoS Negl Trop Dis

Journal ID (publisher-id): plos

Journal ID (pmc): plosntds

Title: PLoS Neglected Tropical Diseases

Publisher: Public Library of Science (San Francisco, USA )

ISSN (Print): 1935-2727

ISSN (Electronic): 1935-2735

Publication date Collection: June 2014

Publication date (Electronic): 19 June 2014

Volume: 8

Issue: 6

Electronic Location Identifier: e2937

Affiliations

[1 ]Department of Parasitology, Asahikawa Medical University, Asahikawa, Japan

[2 ]Department of Medical Biology and Histology, School of Biomedicine, Health Sciences University of Mongolia, Ulaanbaatar, Mongolia

[3 ]National Center for Communicable Diseases, Ulaanbaatar, Mongolia

[4 ]National Center of Pathology, Ulaanbaatar, Mongolia

[5 ]National Center for Maternal and Child Health, Ulaanbaatar, Mongolia

[6 ]Department of Surgery, State Central First Hospital, Ulaanbaatar, Mongolia

[7 ]Institute of Parasitic Diseases, Sichuan Centers for Disease Control and Prevention, Chengdu, China

[8 ]Institute of Veterinary Medicine, Ulaanbaatar, Mongolia

[9 ]Mongolian Academy of Science, Ulaanbaatar, Mongolia

University of Queensland, Australia

Author notes

* E-mail: akiraito@ 123456asahikawa-med.ac.jp

The authors have declared that no competing interests exist.

Conceived and designed the experiments: AI TD. Performed the experiments: TD ADavaas CB GC TY YS KN. Analyzed the data: TD ADavaas TY YS MN TL AI. Contributed reagents/materials/analysis tools: OEBO TA NB NG GA ADavaaj. Wrote the paper: AI TD ADavaas GC YS TY.

† Deceased

Article

Publisher ID: PNTD-D-14-00153

DOI: 10.1371/journal.pntd.0002937

PMC ID: 4063745

PubMed ID: 24945801

SO-VID: ac72ed62-1027-4666-ad89-f1b6e1c60b3e

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 29 January 2014

Date accepted : 27 April 2014

Page count

Pages: 8

Funding

The studies 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 (2010-2012) from the Ministry of Education, Culture, Sports, Science & Technology in Japan (MEXT) to AI. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Cystic Echinococcoses in Mongolia: Molecular Identification, Serology and Risk Factors

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Abstract

Background

Methodology/Principal Findings

Conclusion/Significance

Author Summary

Related collections

China CDC Weekly: COVID19

Most cited references 53

Echinococcus granulosus sensu lato genotypes infecting humans--review of current knowledge.

A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes.

Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion.

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