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      Pathological findings in the red fox ( Vulpes vulpes), stone marten ( Martes foina) and raccoon dog ( Nyctereutes procyonoides), with special emphasis on infectious and zoonotic agents in Northern Germany

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          Abstract

          Anthropogenic landscape changes contributed to the reduction of availability of habitats to wild animals. Hence, the presence of wild terrestrial carnivores in urban and peri-urban sites has increased considerably over the years implying an increased risk of interspecies spillover of infectious diseases and the transmission of zoonoses. The present study provides a detailed characterisation of the health status of the red fox ( Vulpes vulpes), stone marten ( Martes foina) and raccoon dog ( Nyctereutes procyonoides) in their natural rural and peri-urban habitats in Schleswig-Holstein, Germany between November 2013 and January 2016 with focus on zoonoses and infectious diseases that are potentially threatening to other wildlife or domestic animal species. 79 red foxes, 17 stone martens and 10 raccoon dogs were collected from traps or hunts. In order to detect morphological changes and potential infectious diseases, necropsy and pathohistological work-up was performed. Additionally, in selected animals immunohistochemistry (influenza A virus, parvovirus, feline leukemia virus, Borna disease virus, tick-borne encephalitis, canine adenovirus, Neospora caninum, Toxoplasma gondii and Listeria monocytogenes), next-generation sequencing, polymerase chain reaction (fox circovirus) and serum-neutralisation analysis (canine distemper virus) were performed. Furthermore, all animals were screened for fox rabies virus (immunofluorescence), canine distemper virus (immunohistochemistry) and Aujeszky’s disease (virus cultivation). The most important findings included encephalitis (n = 16) and pneumonia (n = 20). None of the investigations revealed a specific cause for the observed morphological alterations except for one animal with an elevated serum titer of 1:160 for canine distemper. Animals displayed macroscopically and/or histopathologically detectable infections with parasites, including Taenia sp., Toxocara sp. and Alaria alata. In summary, wildlife predators carry zoonotic parasitic disease and suffer from inflammatory diseases of yet unknown etiology, possibly bearing infectious potential for other animal species and humans. This study highlights the value of monitoring terrestrial wildlife following the “One Health” notion, to estimate the incidence and the possible spread of zoonotic pathogens and to avoid animal to animal spillover as well as transmission to humans.

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          Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern.

          Echinococcosis in humans is a zoonotic infection caused by larval stages (metacestodes) of cestode species of the genus Echinococcus. Cystic echinococcosis (CE) is caused by Echinococcus granulosus, alveolar echinococcosis (AE) is caused by E. multilocularis, and polycystic forms are caused by either E. vogeli or E. oligarthrus. In untreated cases, AE has a high mortality rate. Although control is essentially feasible, CE remains a considerable health problem in many regions of the northern and southern hemispheres. AE is restricted to the northern hemisphere regions of North America and Eurasia. Recent studies have shown that E. multilocularis, the causative agent of AE, is more widely distributed than previously thought. There are also some hints of an increasing significance of polycystic forms of the disease, which are restricted to Central and South America. Various aspects of human echinococcosis are discussed in this review, including data on the infectivity of genetic variants of E. granulosus to humans, the increasing invasion of cities in Europe and Japan by red foxes, the main definitive hosts of E. multilocularis, and the first demonstration of urban cycles of the parasite. Examples of emergence or reemergence of CE are presented, and the question of potential spreading of E. multilocularis is critically assessed. Furthermore, information is presented on new and improved tools for diagnosing the infection in final hosts (dogs, foxes, and cats) by coproantigen or DNA detection and the application of molecular techniques to epidemiological studies. In the clinical field, the available methods for diagnosing human CE and AE are described and the treatment options are summarized. The development of new chemotherapeutic options for all forms of human echinococcosis remains an urgent requirement. A new option for the control of E. granulosus in the intermediate host population (mainly sheep and cattle) is vaccination. Attempts are made to reduce the prevalence of E. multilocualaris in fox populations by regular baiting with an anthelmintic (praziquantel). Recent data have shown that this control option may be used in restricted areas, for example in cities, with the aim of reducing the infection risk for humans.
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            Urbanization and the ecology of wildlife diseases

            Urbanization is intensifying worldwide, with two-thirds of the human population expected to reside in cities within 30 years. The role of cities in human infectious disease is well established, but less is known about how urban landscapes influence wildlife–pathogen interactions. Here, we draw on recent advances in wildlife epidemiology to consider how environmental changes linked with urbanization can alter the biology of hosts, pathogens and vectors. Although urbanization reduces the abundance of many wildlife parasites, transmission can, in some cases, increase among urban-adapted hosts, with effects on rarer wildlife or those living beyond city limits. Continued rapid urbanization, together with risks posed by multi-host pathogens for humans and vulnerable wildlife populations, emphasize the need for future research on wildlife diseases in urban landscapes.
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              Human anelloviruses: an update of molecular, epidemiological and clinical aspects.

              Human torque teno viruses (TTVs) are new, emerging infectious agents, recently assigned to the family Anelloviridae. The first representative of the genus, torque teno virus (TTV), was discovered in 1997, followed by torque teno mini virus (TTMV) in 2000, and torque teno midi virus (TTMDV) in 2007. These viruses are characterized by an extremely high prevalence, with relatively uniform distribution worldwide and a high level of genomic heterogeneity, as well as an apparent pan-tropism at the host level. Although these viruses have a very high prevalence in the general population across the globe, neither their interaction with their hosts nor their direct involvement in the etiology of specific diseases are fully understood. Since their discovery, human anelloviruses, and especially TTV, have been suggested to be associated with various diseases, such as hepatitis, respiratory diseases, cancer, hematological and autoimmune disorders, with few arguments for their direct involvement. Recent studies have started to reveal interactions between TTVs and the host's immune system, leading to new hypotheses for potential pathological mechanisms of these viruses. In this review article, we discuss the most important aspects and current status of human TTVs in order to guide future studies.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                11 April 2017
                2017
                : 12
                : 4
                : e0175469
                Affiliations
                [1 ]Department of Pathology, University of Veterinary Medicine Hannover, Hannover, Lower Saxony, Germany
                [2 ]Center for Systems Neuroscience, Hannover, Germany
                [3 ]Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Büsum, Schleswig-Holstein, Germany
                [4 ]Department of Viroscience, The Erasmus University Medical Center, Rotterdam, the Netherlands
                [5 ]Institute of Parasitology, Justus Liebig University Giessen, Giessen, Germany
                [6 ]Research Center for Emerging Infections and Zoonoses, University of Veterinary Medicine Hannover, Hannover, Lower Saxony, Germany
                University of Pretoria, SOUTH AFRICA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: US WB AO.

                • Data curation: CL NJ AvN AR AU VMP RB AO WB CB MLG US.

                • Formal analysis: CL NJ.

                • Funding acquisition: US WB AO.

                • Investigation: CL NJ AvN AR AU VMP RB AO WB CB MLG US.

                • Methodology: US CL WB AvN.

                • Project administration: US WB.

                • Resources: RB AO WB US.

                • Supervision: WB US AO.

                • Validation: US WB CB RB AO CL NJ VMP MLG AvN AR AU.

                • Visualization: CL NJ.

                • Writing – original draft: CL NJ RB VMP MG.

                • Writing – review & editing: US WB CB RB AO CL NJ VMP MLG AvN AR AU.

                [¤]

                Current address: Department of Farm Animal Health, Faculty of Veterinary Medicine, Utrecht University, Utrecht, the Netherlands

                ‡ These authors also contributed equally to this work.

                Author information
                http://orcid.org/0000-0002-3534-1257
                Article
                PONE-D-16-47753
                10.1371/journal.pone.0175469
                5388480
                28399176
                319aa136-fccd-4a87-b8e6-1eef7e881a47
                © 2017 Lempp et al

                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
                : 2 December 2016
                : 27 March 2017
                Page count
                Figures: 4, Tables: 2, Pages: 20
                Funding
                Funded by: Ministry of Energy, Agriculture, the Environment and Rural Affairs of Schleswig Holstein
                Funded by: German Hunting Union
                Funded by: Niedersachsen-Research Network on Neuroinfectiology
                Funded by: European Union Horizon 2020
                Award ID: COMPARE, grant No.: 643476
                The investigation was funded by the Ministry of Energy, Agriculture, the Environment and Rural Affairs of Schleswig-Holstein and the German Hunting Union and partly supported by the Niedersachsen-Research Network on Neuroinfectiology (N-RENNT) of the Ministry of Science and Culture of Lower Saxony, Germany, and by the COMPARE project and received funding from the European Union’s Horizon 2020 research and innovation program COMPARE (grant agreement no. 643476). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Foxes
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Raccoons
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                People and Places
                Geographical Locations
                Europe
                Germany
                Medicine and Health Sciences
                Infectious Diseases
                Infectious Diseases of the Nervous System
                Encephalitis
                Medicine and Health Sciences
                Neurology
                Infectious Diseases of the Nervous System
                Encephalitis
                Medicine and Health Sciences
                Infectious Diseases
                Zoonoses
                Biology and Life Sciences
                Organisms
                Animals
                Animal Types
                Wildlife
                Biology and Life Sciences
                Zoology
                Animal Types
                Wildlife
                Biology and Life Sciences
                Veterinary Science
                Veterinary Diseases
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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