Species and genotypes belonging to <i>Echinococcus granulosus</i> <i>sensu lato</i> complex causing human cystic echinococcosis in Europe (2000–2021): a systematic review

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Abstract

Background

This study aimed to fill a gap of knowledge by providing a quantitative measure of molecularly identified species and genotypes belonging to Echinococcus granulosus sensu lato ( s.l.) causing human cystic echinococcosis (CE) in Europe during the period 2000–2021. As these species and genotypes are characterized by genetic, animal host and geographical differences, studying the E. granulosus s.l. complex is epidemiologically relevant.

Methods

A systematic review (SR) was conducted on the basis of both scientific and grey literature considering primary studies between 2000 and 2021 in four databases. From a total of 1643 scientific papers, 51 records were included in the SR. The main inclusion criterion for this study was the molecular confirmation of E. granulosus s.l. at the genotype/species level as a causative agent of human CE cases in selected European countries.

Results

Relevant data were obtained from 29 out of 39 eligible European countries. This SR identified 599 human molecularly confirmed echinococcal cysts: 460 (76.8%) identified as E. granulosus sensu stricto ( s.s.), 130 (21.7%) as E. canadensis cluster (G6/7 and G10), 7 (1.2%) as E. ortleppi (G5), and 2 as E. vogeli (0.3%). Three geographical hotspots of human CE caused by different species of the E. granulosus s.l. complex were identified: (1) E. granulosus s.s. in Southern and South-eastern Europe (European-Mediterranean and Balkan countries); (2) E. canadensis (G6/7) in Central and Eastern Europe; (3) E. ortleppi in Central and Western Europe. This SR also identified data gaps that prevented a better definition of the geographical distribution of the Echinococcus granulosus s.l. species complex in Europe: western Balkan countries, part of Central Europe, and Baltic countries.

Conclusions

These results mandate longitudinal, multi-centre, intersectoral and transdisciplinary studies which consider both molecular and clinical epidemiology in animals and humans. Such studies would be valuable for a better understanding of the transmission of the E. granulosus s.l. species complex and their potential clinical impact on humans.

Graphical Abstract

Supplementary Information

The online version contains supplementary material available at 10.1186/s13071-022-05197-8.

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Most cited references 75

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Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing.

J. Bowles, D. Blair, D. McManus (1992)

The pattern of species and strain variation within the genus Echinococcus is complex and controversial. In an attempt to characterise objectively the various species and strains, the sequence of a region of the mitochondrial cytochrome c oxidase subunit I (CO1) gene was determined for 56 Echinococcus isolates. Eleven different genotypes were detected, including 7 within Echinococcus granulosus, and these were used to categorise the isolates. The 4 generally accepted Echinococcus species were clearly distinguishable using this approach. In addition, the consensus view of the strain pattern within E. granulosus, based on a variety of criteria of differentiation, was broadly upheld. Very little variation was detected within Echinococcus multilocularis. Remarkable intra-strain homogeneity was found at the DNA sequence level. This region of the rapidly evolving mitochondrial genome is useful as a marker of species and strain identity and as a preliminary indication of evolutionary divergence within the genus Echinococcus.

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Biology and Systematics of Echinococcus.

R Thompson (2017)

The biology of Echinococcus, the causative agent of echinococcosis (hydatid disease) is reviewed with emphasis on the developmental biology of the adult and metacestode stages of the parasite. Major advances include determining the origin, structure and functional activities of the laminated layer and its relationship with the germinal layer; and the isolation, in vitro establishment and characterization of the multipotential germinal cells. Future challenges are to identify the mechanisms that provide Echinococcus with its unique developmental plasticity and the nature of activities at the parasite-host interface, particularly in the definitive host. The revised taxonomy of Echinococcus is presented and the solid nomenclature it provides will be essential in understanding the epidemiology of echinococcosis.

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Is Open Access

International consensus on terminology to be used in the field of echinococcoses

Dominique A. Vuitton, Donald McManus, Michael T Rogan … (2020)

Echinococcoses require the involvement of specialists from nearly all disciplines; standardization of the terminology used in the field is thus crucial. To harmonize echinococcosis terminology on sound scientific and linguistic grounds, the World Association of Echinococcosis launched a Formal Consensus process. Under the coordination of a Steering and Writing Group (SWG), a Consultation and Rating Group (CRG) had the main missions of (1) providing input on the list of terms drafted by the SWG, taking into account the available literature and the participants’ experience; and (2) providing independent rating on all debated terms submitted to vote. The mission of the Reading and Review Group (RRG) was to give an opinion about the recommendation paper in terms of readability, acceptability and applicability. The main achievements of this process were: (1) an update of the current nomenclature of Echinococcus spp.; (2) an agreement on three names of diseases due to Echinococcus spp.: Cystic Echinococcosis (CE), Alveolar Echinococcosis (AE) and Neotropical Echinococcosis (NE), and the exclusion of all other names; (3) an agreement on the restricted use of the adjective “hydatid” to refer to the cyst and fluid due to E. granulosus sensu lato; and (4) an agreement on a standardized description of the surgical operations for CE, according to the “Approach, cyst Opening, Resection, and Completeness” (AORC) framework. In addition, 95 “approved” and 60 “rejected” terms were listed. The recommendations provided in this paper will be applicable to scientific publications in English and communication with professionals. They will be used for translation into other languages spoken in endemic countries.

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Author and article information

Contributors

Adriano Casulli:

ORCID: http://orcid.org/0000-0001-9183-7591

adriano.casulli@iss.it

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 28 March 2022

Publication date PMC-release: 28 March 2022

Publication date Collection: 2022

Volume: 15

Electronic Location Identifier: 109

Affiliations

[1 ]GRID grid.416651.1, ISNI 0000 0000 9120 6856, WHO Collaborating Centre for the Epidemiology, Detection and Control of Cystic and Alveolar Echinococcosis, Department of Infectious Diseases, , Istituto Superiore Di Sanità, ; Rome, Italy

[2 ]GRID grid.416651.1, ISNI 0000 0000 9120 6856, European Reference Laboratory for Parasites, Department of Infectious Diseases, , Istituto Superiore Di Sanità, ; Rome, Italy

[3 ]GRID grid.5395.a, ISNI 0000 0004 1757 3729, Department of Biology, , Ethology Unit, University of Pisa, ; Pisa, Italy

[4 ]GRID grid.22072.35, ISNI 0000 0004 1936 7697, Department of Ecosystem and Public Health, Faculty of Veterinary Medicine, , University of Calgary, ; Calgary, AB Canada

[5 ]GRID grid.493090.7, ISNI 0000 0004 4910 6615, UMR CNRS 6249 Chrono-Environnement, , Université Bourgogne Franche-Comté, ; Besancon, France

[6 ]GRID grid.10939.32, ISNI 0000 0001 0943 7661, Department of Zoology, Institute of Ecology and Earth Sciences, , University of Tartu, ; Tartu, Estonia

[7 ]Anses LRFSN, National Reference Laboratory for Echinococcus Spp, Malzéville, France

Author information

Adriano Casulli http://orcid.org/0000-0001-9183-7591

Article

Publisher ID: 5197

DOI: 10.1186/s13071-022-05197-8

PMC ID: 8962544

PubMed ID: 35346335

SO-VID: 5297af56-245d-4012-8cf6-29dba075125d

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 21 December 2021

Date accepted : 12 February 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100010661, Horizon 2020 Framework Programme;

Award ID: 773830

Award Recipient : Adriano Casulli

Funded by: Estonian Ministry of Education and Research

Award ID: PRG1209

Award Recipient : Urmas Saarma

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: echinococcus granulosussensu lato,echinococcus granulosussensu stricto,echinococcus canadensis,echinococcus ortleppi,genotypes,human cystic echinococcosis,europe

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: echinococcus granulosussensu lato, echinococcus granulosussensu stricto, echinococcus canadensis, echinococcus ortleppi, genotypes, human cystic echinococcosis, europe

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Species and genotypes belonging to Echinococcus granulosus sensu lato complex causing human cystic echinococcosis in Europe (2000–2021): a systematic review

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Abstract

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Graphical Abstract

Supplementary Information

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Malaria vaccine development

Most cited references 75

Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing.

Biology and Systematics of Echinococcus.

International consensus on terminology to be used in the field of echinococcoses

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Cited by 27

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