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      A first report of Thelazia callipaeda infection in Phortica okadai and wildlife in national nature reserves in China

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          Abstract

          Background

          Thelazia callipaeda is a zoonotic parasitic nematode of the family Thelaziidae, with Phortica okadai as its intermediate host and only confirmed vector in China. China has the largest number of human cases of thelaziosis in the world. It is generally believed that infected domestic animals (dogs and cats) are the most important reservoir hosts of T. callipaeda, and thus pose a direct threat to humans. At present, there is little research or attention focused on the role of wildlife in the transmission cycle of thelaziosis in nature reserves.

          Methods

          We selected locations in four national nature reserves across China to monitor P. okadai and wildlife. We used a fly-trap method to monitor P. okadai density. Morphological analysis of the parasites collected from the conjunctival sac of the infected wildlife was undertaken as the first step in species identification, and polymerase chain reaction (PCR) was used for species confirmation.

          Results

          In 2019, the density of P. okadai in Foping National Nature Reserve in China increased sharply, and infected P. okadai were newly found in the reserve. Giant panda, wild boar, leopard cat, and black bear were found to be newly infected with T. callipaeda (one individual of each species). A total of four worms were collected, one from each species of wildlife. The four worms were identified as T. callipaeda by their morphological characteristics; species identification was confirmed by PCR amplification.

          Conclusions

          To the best of our knowledge, this is the first report of T. callipaeda infection in P. okadai as well as in a variety of wildlife, including giant panda, in nature reserves in China. These results indicate that there is a transmission cycle of T. callipaeda among wildlife in these nature reserves. The increasing number of case reports of thelaziosis in wildlife suggest a likely risk of T. callipaeda infection for the inhabitants of villages situated around nature reserves.

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          Most cited references24

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          A review of the interactions between free-roaming domestic dogs and wildlife

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            Current status and epidemiological observation of Thelazia callipaeda (Spirurida, Thelaziidae) in dogs, cats and foxes in Italy: a "coincidence" or a parasitic disease of the Old Continent?

            Thelazia callipaeda is a spirurid nematode which causes ocular infections in dogs and man and, occasionally, in cats, foxes and rabbits. The intermediate host and vector of T. callipaeda is unknown. For a long time T. callipaeda incidence was reported only from the Russian Federation and the Far East, but recently it has also been found in Italy. In order to investigate the spread of T. callipaeda in Italy, a survey was carried out in two sites, site A in the Piedmont region (North West Italy), and site B in the Basilicata region (Southern Italy). Dogs, cats and foxes in site A and dogs in site B were examined for eyeworms, using different procedures and timing. From January 1995 to August 2002, 91 dogs, 4 cats and 903 fox carcasses were examined in site A, and from October 1999 to January 2003, 443 dogs were examined in site B, and the eyeworms collected were identified using morphological keys. Twenty-one (23.07%) and 185 (41.76%) of the dogs from sites A and B, respectively, were found to be infected by eyeworms; furthermore, all the cats examined and 46 fox carcasses (5.1%) were positive for eyeworms. All the nematodes collected were identified as T. callipaeda. These results indicate that T. callipaeda is not confined to Eastern Europe and Asia, but that it has spread to the Old Continent, and to both Northern and Southern Italy. Considering the high prevalence of infected dogs reported in some municipalities (e.g. 60.14% of 138 dogs examined in a municipality from site B), it is assumed that one or more vectors are significantly present in the areas under investigation. Furthermore, there is good reason to believe that T. callipaeda is also present in other European countries. Speculation as to the origins of this parasitic infestation in Europe and the biology of T. callipaeda and its vector/s is also discussed.
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              Analysis of genetic variability within Thelazia callipaeda (Nematoda: Thelazioidea) from Europe and Asia by sequencing and mutation scanning of the mitochondrial cytochrome c oxidase subunit 1 gene.

              This study investigated genetic variability within the 'eyeworm'Thelazia callipaeda (Nematoda: Thelazioidea) from Europe and Asia by polymerase chain reaction (PCR)-coupled sequencing and mutation scanning of the mitochondrial cytochrome c oxidase subunit 1 gene (cox 1). Eight different sequence variants of cox 1 (haplotypes) were determined for the 50 individual adult specimens of T. callipaeda (from dogs, foxes or cats from Italy, Germany and the Netherlands and from dogs from China and Korea). Nucleotide variation (0.3--2%) was detected at 23 of 649 positions in the cox 1. Six of these positions were invariable among all 37 individuals from Europe and among the 13 individuals from Asia (irrespective of host origin) but differed (five G A and one C T changes) between Europe and Asia. PCR-based single-strand conformation polymorphism (SSCP) analysis of the most variable portion (v-cox 1) of the cox 1 was validated (for a subset of samples) as a tool to rapidly screen for genetic (haplotypic) variability. The results for the SSCP analysis and sequencing were concordant, indicating that the mutation scanning approach provides a useful tool for investigating the population genetics and molecular ecology of T. callipaeda.
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                Author and article information

                Contributors
                yipengjin@vip.sina.com
                lzc94@126.com
                1580895259@qq.com
                245215913@qq.com
                1055829743@qq.com
                784873396@qq.com
                csama@sina.com
                jiahao_lin@cau.edu.cn
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                6 January 2021
                6 January 2021
                2021
                : 14
                : 13
                Affiliations
                [1 ]GRID grid.22935.3f, ISNI 0000 0004 0530 8290, College of Veterinary Medicine, , People’s Republic of China Agricultural University, ; No. 2 Yuanmingyuan West Road, Haidian District, Beijing, 100193 People’s Republic of China
                [2 ]Foping National Nature Reserve, Shaanxi, 723400 People’s Republic of China
                Author information
                http://orcid.org/0000-0003-0807-9801
                Article
                4509
                10.1186/s13071-020-04509-0
                7789172
                33407836
                4f578992-f150-406b-8586-94e0206805f4
                © The Author(s) 2020

                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
                : 26 July 2020
                : 1 December 2020
                Categories
                Short Report
                Custom metadata
                © The Author(s) 2021

                Parasitology
                thelazia callipaeda,phortica okadai,wildlife,vector-borne zoonosis,nature reserves,china
                Parasitology
                thelazia callipaeda, phortica okadai, wildlife, vector-borne zoonosis, nature reserves, china

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