High-resolution phylogeography of zoonotic tapeworm<i>Echinococcus granulosus</i>sensu stricto genotype G1 with an emphasis on its distribution in Turkey, Italy and Spain

Kinkar, Liina; Laurimäe, Teivi; Şimşek, Sami; Balkaya, İbrahim; Casulli, Adriano; Manfredi, Maria Teresa; Ponce-Gordo, Francisco; Varcasia, Antonio; Lavikainen, Antti; González, Luís Miguel; Rehbein, Steffen; Giessen, Joke van der; Sprong, Hein; Saarma, Urmas

doi:10.1017/s0031182016001530

Cited by 54 publications

(49 citation statements)

References 73 publications

(103 reference statements)

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“…This sequence type is the most commonly recorded G1 variant in southern Palearctic and it was previously recorded in China (Qinghai province) in sheep [33], in Russia (Altai region) in human [34], in Mongolia in human (GenBank Accession No. AB787538, unpublished), in Turkey in sheep, cattle and human [20,35], in Iran in sheep, human, camel and goat [36] and GenBank Accession No. KP751431 (unpublished), in Jordan in sheep [36], and in Tunisia in cattle, sheep and donkey [37].…”

Section: Resultsmentioning

confidence: 99%

A molecular survey of Echinococcus granulosus sensu lato in central-eastern Europe

et al. 2016

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Open Life Sci. 2016; 11: 524-532 while infections with E. granulosus s.s. which are highly infectious for humans are more commonly encountered in Romania and Hungary.Keywords: Echinococcus granulosus, genotype, DNA sequences, human, pig, central-eastern Europe IntroductionThe larval stages of the tapeworm Echinococcus granulosus sensu lato (s.l.) are the causative agents of cystic echinococcosis (CE), one of the most important cestode infections causing morbidity and mortality in humans and significant economic losses in livestock. Around one million or more people are currently suffering from CE globally and the financial burden of the disease on the livestock industry is substantial, with up to two billion dollars lost annually [1]. Recent molecular phylogenetic analyses have revealed that E. granulosus is a complex of spesies/genotypes with at least five different species: E. granulosus sensu stricto (s.s.) (genotypes G1-G3), Echinococcus equinus (G4), Echinococcus ortleppi (G5), Echinococcus canadensis (G6-G10), and Echinococcus felidis ("lion strain") [2][3][4].CE remains one of the most important helminth zoonoses in many regions of Europe, especially the Mediterranean littoral (Spain, Italy, Greece and Turkey) and southeastern countries such as Bulgaria and Romania. The disease seems to be less prevalent in the UK, Central Europe, the Baltic States and the Scandinavian countries [5,6]. Surveys that addressed the incidence of CE over the last decade from central-eastern Europe has reported a relatively greater incidence in Romania (average incidence annual rate was 0.29 per 100,000 population) and Ukraine (0.30), whereas in Hungary (0.07), Poland (0.08) and Slovakia (0.10) lower numbers of human cases were documented [7]. This also is due to the fact that E. granulosus s.s., which is responsible for the majority Abstract: Central-eastern Europe is an endemic region for cystic echinococcosis where multiple species of intermediate hosts are commonly infected with Echinococcus granulosus sensu lato tapeworms of major medical and veterinary importance. Investigations of the genetic variation of 25 Echinococcus isolates from five countries (Slovakia, Romania, Ukraine, Hungary, Poland) were undertaken using three mitochondrial DNA markers. The 18 isolates from pigs derived from Slovakia and Ukraine and the four human isolates from Slovakia, Poland and Ukraine were identified as E. canadensis G7, whereas the three human isolates from Romania and Hungary were classified as E. granulosus sensu stricto G1. This study reports the first confirmed human case of E. granulosus s.s. in Hungary. The haplotype G7A with two polymorphic sites relative to the most common regional variant of E. canadensis G7 was recorded in both pigs from Ukraine and in a single pig isolate from Slovakia. The results of this study support the circumstantial evidence that E. canadensis G7 with low infectivity for humans is highly prevalent in the northern parts of the region (Poland, Slovakia, forest-steppe zone of Ukraine),

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Section: Resultsmentioning

confidence: 99%

A molecular survey of Echinococcus granulosus sensu lato in central-eastern Europe

et al. 2016

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“…Furthermore, a large proportion of the haplotypes described in Romig et al (2015) were not homologous with any of the sequences of G1, G2 or G3 originally described in Bowles et al (1992). However, using significantly longer mtDNA sequences (Kinkar et al 2016;Laurimäe et al 2016) could provide means to differentiate G1-G3 from each other with confidence. The correct genotyping of this highly zoonotic cluster would also be of great epidemiological importance as it forms the basis for further analysis regarding the possible differences between these genotypes (e.g.…”

Section: Introductionmentioning

confidence: 98%

New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto

Kinkar

Laurimäe

Sharbatkhori

et al. 2017

Infection, Genetics and Evolution

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102

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Cystic echinococcosis, a zoonotic disease caused by Echinococcus granulosus sensu lato (s. l.), is a significant global public health concern. Echinococcus granulosus s. l. is currently divided into numerous genotypes (G1-G8 and G10) of which G1-G3 are the most frequently implicated genotypes in human infections. Although it has been suggested that G1-G3 could be regarded as a distinct species E. granulosus sensu stricto (s. s.), the evidence to support this is inconclusive. Most importantly, data from nuclear DNA that provide means to investigate the exchange of genetic material between G1-G3 is lacking as none of the published nuclear DNA studies have explicitly included G2 or G3. Moreover, the commonly used relatively short mtDNA sequences, including the complete cox1 gene, have not allowed unequivocal differentiation of genotypes G1-G3. Therefore, significantly longer mtDNA sequences are required to distinguish these genotypes with confidence. The main aim of this study was to evaluate the phylogenetic relations and taxonomy of genotypes G1-G3 using sequences of nearly complete mitogenomes (11,443bp) and three nuclear loci (2984bp). A total of 23 G1-G3 samples were analysed, originating from 5 intermediate host species in 10 countries. The mtDNA data demonstrate that genotypes G1 and G3 are distinct mitochondrial genotypes (separated by 37 mutations), whereas G2 is not a separate genotype or even a monophyletic cluster, but belongs to G3. Nuclear data revealed no genetic separation of G1 and G3, suggesting that these genotypes form a single species due to ongoing gene flow. We conclude that: (a) in the taxonomic sense, genotypes G1 and G3 can be treated as a single species E. granulosus s. s.; (b) genotypes G1 and G3 should be regarded as distinct genotypes only in the context of mitochondrial data; (c) we recommend excluding G2 from the genotype list.

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“…The presence of E. granulosus G1-G3 complex (E. granulosus s.s.) coincides with areas of high CE prevalence, whereas for E. canadensis G6/G7 a low infectivity for humans was suggested because case numbers are usually low in regions where these genotypes predominate . In a recent phylogeographical study of Kinkar et al (2016) on Mediterraenan and South European E. granulosus s.s. G1, Romanian cattle isolate was genetically most closely related to Turkish samples derived from one of central haplotypes than to geographically more close samples. This indicated a substantial role of livestock trade, which has facilitated the parasite dispersal over vast areas, in shaping phylogeographical G1 pattern.…”

Section: Discussionmentioning

confidence: 99%

Genetic survey of alveolar and cystic echinococcoses in Romania: first molecular evidence of Echinococcus multilocularis in humans in the country

et al. 2017

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SummaryCystic echinococcosis (CE) and alveolar echinococcosis (AE) are considered as one of the most important zoonotic diseases in Romania, where they are subject to mandatory reporting. To obtain more knowledge about the genetic diversity of Echinococcus causative agents of these diseases, 11 isolates from humans and ungulate intermediate hosts from the two regions of Romania were genotyped using mitochondrial markers. In clinical samples of fi ve patients from north-eastern Romania (Iasi, Botosani, Vaslui counties), Echinococcus multilocularis was identifi ed as causal agent by cox1 sequence analysis. To the best of our knowledge this fi nding presents the fi rst molecular evidence of E. multilocularis in humans from Romania. Only two cases of AE in patients were previously documented in the country by serological methods. In our four patients the most widespread European variant E5 of E. multilocularis was recorded, whereas in isolate from Vaslui county three nucleotide substitutions were detected as compared to the most related E5 haplotype. One of these mutations (411T/G) matched N1 and N2 haplotypes described previously from North America. In six CE samples retrieved from western Romania (Caras-Severin and Timis counties), two human isolates were diagnosed as Echinococcus canadensis G7, one as E. granulosus s.s. G1 and one as E. granulosus s.s. G3 using atp6 and rrnS sequencing. In ungulates, the cattle isolate was allocated to E. granulosus s.s. G1 and pig isolate to E. canadensis G7. The two G7 fi ndings in humans reinforced the recent view that G7 was underestimated as compared to the E. granulosus s.s. regarding human CE threat that can be further employed for identifying sources of infections and establishing suitable preventive measures.

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High-resolution phylogeography of zoonotic tapewormEchinococcus granulosussensu stricto genotype G1 with an emphasis on its distribution in Turkey, Italy and Spain

Cited by 54 publications

References 73 publications

A molecular survey of Echinococcus granulosus sensu lato in central-eastern Europe

A molecular survey of Echinococcus granulosus sensu lato in central-eastern Europe

New mitogenome and nuclear evidence on the phylogeny and taxonomy of the highly zoonotic tapeworm Echinococcus granulosus sensu stricto

Genetic survey of alveolar and cystic echinococcoses in Romania: first molecular evidence of Echinococcus multilocularis in humans in the country

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