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      Wildlife-transmitted Taenia and Versteria cysticercosis and coenurosis in humans and other primates

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          Abstract

          Wild mustelids and canids are definitive hosts of Taenia and Versteria spp. while rodents act as natural intermediate hosts. Rarely, larval stages of these parasites can cause serious zoonoses. In Europe, four cases of Taenia martis cysticercosis have been diagnosed in immunocompetent women, and two cases in zoo primates since 2013. In North America, a zoonotic genotype related but distinct from Versteria mustelae has been identified in 2014, which had caused a fatal infection in an orangutan and liver- and disseminated cysticercoses in two severely immune deficient human patients in 2018, respectively. Additionally, we could attribute a historic human case from the USA to this Versteria sp. by reanalysing a published nucleotide sequence. In the last decades, sporadic zoonotic infections by cysticerci of the canid tapeworm Taenia crassiceps have been described (4 in North America, 8 in Europe). Besides, 3 ocular cases from North America and one neural infection from Europe, all in immunocompetent patients, 6 cutaneous infections were described in severely immunocompromised European patients. Correspondingly, besides oral infections with taeniid eggs, accidental subcutaneous oncosphere establishment after egg-contamination of open wounds was suggested, especially in cases with a history of cutaneous injuries at the infection site. Taenia multiceps is mainly transmitted in a domestic cycle. Only five human coenurosis cases are published since 2000. In contrast, T. serialis coenurosis (1 human case since 2000) is primarily transmitted by wild canids. The etiological diagnosis of exotic cysticercoses is challenging. Usually, clinical material does not allow for a morphological identification, and serological tests are not available. These limitations have partly been overcome by molecular tools. Without claiming any dramatic emergence of cysticercoses and coenuroses transmitted by wild carnivores, further sporadic cases of such ‘exotic’ infections have to be expected.

          Graphical abstract

          Taenia crassiceps cysticerci from the abdomen of an infected rodent.

          Highlights

          • Wild canids and mustelids transmit rare but potentially fatal cysticercoses and coenuroses.

          • Martens and weasels can rarely transmit dangerous parasitic infections.

          • Tapeworm eggs may contaminate wounds and develop locally.

          • In North America, the mustelid tapeworm Versteria causes severe human infections.

          • Molecular analyses from minute clinical material allows for a specific diagnosis.

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          Most cited references 203

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

          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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            Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA.

            A multiplex polymerase chain reaction (PCR) was evaluated for the identification of morphologically indistinguishable eggs of the taeniid tapeworms from carnivores using primers targeting mitochondrial genes. The primers for Echinococcus multilocularis (amplicon size 395 bp) were species-specific as assessed by in silico analysis and in the PCR using well-defined control samples. The design of primers that specifically amplify DNA from E. granulosus or Taenia spp. was not possible. The primers designed for E. granulosus also amplified DNA (117 bp) from E. vogeli, and those designed for Taenia spp. amplified products (267 bp) from species of Mesocestoides, Dipylidium and Diphyllobothrium. Nevertheless, as our diagnostic approach includes the concentration of taeniid eggs by sequential sieving and flotation, followed by their morphological detection, this non-specificity has limited practical importance. Sequence analysis of the corresponding amplicon can identify most of the described E. granulosus genotypes. Taenia spp. can be identified by direct sequencing of the 267 bp amplicon, or, for most species, by restriction fragment length polymorphism (RFLP) analysis. The multiplex PCR was readily able to detect 1 egg (estimated to contain 7000 targets, as determined by quantitative PCR). Having been validated using a panel of well-defined samples from carnivores with known infection status, this approach proved to be useful for the identification of taeniid eggs from both individual animals and for epidemiological studies.
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              Ecology and Life Cycle Patterns of Echinococcus Species.

              The genus Echinococcus is composed of eight generally recognized species and one genotypic cluster (Echinococcus canadensis cluster) that may in future be resolved into one to three species. For each species, we review existing information on transmission routes and life cycles in different geographical contexts and - where available - include basic biological information of parasites and hosts (e.g., susceptibility of host species). While some Echinococcus spp. are transmitted in life cycles that involve predominantly domestic animals (e.g., dog - livestock cycles), others are wildlife parasites that do or do not interact with domestic transmission. In many cases, life cycle patterns of the same parasite species differ according to geography. Simple life cycles contrast with transmission patterns that are highly complex, involving multihost systems that may include both domestic and wild mammals. Wildlife transmission may be primary or secondary, i.e., resulting from spillovers from domestic animals. For most of the species and regions, existing information does not yet permit a conclusive description of transmission systems. Such data, however, would be highly relevant, e.g., for anticipation of geographical changes of the presence and frequency of these parasites in a warming world, or for initiating evidence-based control strategies.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol Parasites Wildl
                Int J Parasitol Parasites Wildl
                International Journal for Parasitology: Parasites and Wildlife
                Elsevier
                2213-2244
                11 April 2019
                August 2019
                11 April 2019
                : 9
                : 342-358
                Affiliations
                Institute of Parasitology, University of Zürich, 8057, Zürich, Switzerland
                Author notes
                []Corresponding author. Institute of Parasitology, University of Zurich, Winterthurerstr. 266a, 8057 Zurich, Switzerland. deplazesp@ 123456access.uzh.ch
                Article
                S2213-2244(19)30022-7
                10.1016/j.ijppaw.2019.03.013
                6626850
                © 2019 Published by Elsevier Ltd on behalf of Australian Society for Parasitology.

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                Categories
                Special section: Emerging Zoonoses and Wildlife

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