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      Recent advances on Dirofilaria repens in dogs and humans in Europe

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          Abstract

          Dirofilaria repens is a nematode affecting domestic and wild canids, transmitted by several species of mosquitoes. It usually causes a non-pathogenic subcutaneous infection in dogs and is the principal agent of human dirofilariosis in the Old World. In the last decades, D. repens has increased in prevalence in areas where it has already been reported and its distribution range has expanded into new areas of Europe, representing a paradigmatic example of an emergent pathogen. Despite its emergence and zoonotic impact, D. repens has received less attention by scientists compared to Dirofilaria immitis. In this review we report the recent advances of D. repens infection in dogs and humans, and transmission by vectors, and discuss possible factors that influence the spread and increase of this zoonotic parasite in Europe. There is evidence that D. repens has spread faster than D. immitis from the endemic areas of southern Europe to northern Europe. Climate change affecting mosquito vectors and the facilitation of pet travel seem to have contributed to this expansion; however, in the authors’ opinion, the major factor is likely the rate of undiagnosed dogs continuing to perpetuate the life-cycle of D. repens. Many infected dogs remain undetected due to the subclinical nature of the disease, the lack of rapid and reliable diagnostic tools and the poor knowledge and still low awareness of D. repens in non-endemic areas. Improved diagnostic tools are warranted to bring D. repens diagnosis to the state of D. immitis diagnosis, as well as improved screening of imported dogs and promotion of preventative measures among veterinarians and dog owners. For vector-borne diseases involving pets, veterinarians play a significant role in prevention and should be more aware of their responsibility in reducing the impact of the zoonotic agents. In addition, they should enhance multisectorial collaboration with medical entomologists and the public health experts, under the concept and the actions of One Health-One Medicine.

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          The online version of this article (10.1186/s13071-018-3205-x) contains supplementary material, which is available to authorized users.

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          Human and animal dirofilariasis: the emergence of a zoonotic mosaic.

          Dirofilariasis represents a zoonotic mosaic, which includes two main filarial species (Dirofilaria immitis and D. repens) that have adapted to canine, feline, and human hosts with distinct biological and clinical implications. At the same time, both D. immitis and D. repens are themselves hosts to symbiotic bacteria of the genus Wolbachia, the study of which has resulted in a profound shift in the understanding of filarial biology, the mechanisms of the pathologies that they produce in their hosts, and issues related to dirofilariasis treatment. Moreover, because dirofilariasis is a vector-borne transmitted disease, their distribution and infection rates have undergone significant modifications influenced by global climate change. Despite advances in our knowledge of D. immitis and D. repens and the pathologies that they inflict on different hosts, there are still many unknown aspects of dirofilariasis. This review is focused on human and animal dirofilariasis, including the basic morphology, biology, protein composition, and metabolism of Dirofilaria species; the climate and human behavioral factors that influence distribution dynamics; the disease pathology; the host-parasite relationship; the mechanisms involved in parasite survival; the immune response and pathogenesis; and the clinical management of human and animal infections.
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            Heartworm disease in animals and humans.

            Heartworm disease due to Dirofilaria immitis continues to cause severe disease and even death in dogs and other animals in many parts of the world, even though safe, highly effective and convenient preventatives have been available for the past two decades. Moreover, the parasite and vector mosquitoes continue to spread into areas where they have not been reported previously. Heartworm societies have been established in the USA and Japan and the First European Dirofilaria Days (FEDD) Conference was held in Zagreb, Croatia, in February of 2007. These organizations promote awareness, encourage research and provide updated guidelines for the diagnosis, treatment and prevention of heartworm disease. The chapter begins with a review of the biology and life cycle of the parasite. It continues with the prevalence and distribution of the disease in domestic and wild animals, with emphasis on more recent data on the spreading of the disease and the use of molecular biology techniques in vector studies. The section on pathogenesis and immunology also includes a discussion of the current knowledge of the potential role of the Wolbachia endosymbiont in inflammatory and immune responses to D. immitis infection, diagnostic use of specific immune responses to the bacteria, immunomodulatory activity and antibiotic treatment of infected animals. Canine, feline and ferret heartworm disease are updated with regard to the clinical presentation, diagnosis, prevention, therapy and management of the disease, with special emphasis on the recently described Heartworm Associated Respiratory Disease (HARD) Syndrome in cats. The section devoted to heartworm infection in humans also includes notes on other epizootic filariae, particularly D. repens in humans in Europe. The chapter concludes with a discussion on emerging strategies in heartworm treatment and control, highlighting the potential role of tetracycline antibiotics in adulticidal therapy.
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              Melanization immune responses in mosquito vectors.

              The production and deposition of melanin pigments on invading pathogens and parasites represents a unique, innate immune response in the phylum Arthropoda. This immune response has started to receive considerable attention because of the potential to exploit this mechanism to control mosquito-borne diseases. In this article, we summarize knowledge about this complex biochemistry, the use of melanin biosynthesis in diverse physiological processes and the gaps in knowledge that must be addressed if this immune process is to be manipulated in genetic-based control strategies.
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                Author and article information

                Contributors
                gcapelli@izsvenezie.it
                claudio.genchi@unimi.it
                gad.baneth@mail.huji.ac.il
                patrick.bourdeau@oniris-nantes.fr
                ebrianti@unime.it
                lcardoso@utad.pt
                pdanesi@izsvenezie.it
                Hans-Peter.Fuehrer@vetmeduni.ac.at
                alessio.giannelli@uniba.it
                ionica.angela@usamvcluj.ro
                carlamaia@ihmt.unl.pt
                modryd@vfu.cz
                fmontarsi@izsvenezie.it
                Juergen.Kruecken@fu-berlin.de
                eliaspap@vet.auth.gr
                dusanp@polj.uns.ac.rs
                pfeffer@vetmed.uni-leipzig.de
                sara@niv.ns.ac.rs
                domenico.otranto@uniba.it
                sven@poppert.eu
                Cornelia.Silaghi@fli.de
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                19 December 2018
                19 December 2018
                2018
                : 11
                : 663
                Affiliations
                [1 ]ISNI 0000 0004 1805 1826, GRID grid.419593.3, Laboratory of Parasitology, National reference centre/OIE collaborating centre for diseases at the animal-human interface, Istituto Zooprofilattico Sperimentale delle Venezie, ; Legnaro, Italy
                [2 ]ISNI 0000 0004 1757 2822, GRID grid.4708.b, Department of Veterinary Medicine, , Università degli Studi di Milano, ; Milan, Italy
                [3 ]ISNI 0000 0004 1937 0538, GRID grid.9619.7, Koret School of Veterinary Medicine, , The Hebrew University, ; Rehovot, Israel
                [4 ]GRID grid.4817.a, Veterinary School of Nantes ONIRIS, , University of Nantes, LUNAM, ; Nantes, France
                [5 ]ISNI 0000 0001 2178 8421, GRID grid.10438.3e, Department of Veterinary Science, , Università degli Studi di Messina, ; Messina, Italy
                [6 ]ISNI 0000000121821287, GRID grid.12341.35, Department of Veterinary Sciences, , School of Agrarian and Veterinary Sciences, University of Trás-os-Montes e Alto Douro, ; Vila Real, Portugal
                [7 ]ISNI 0000 0000 9686 6466, GRID grid.6583.8, Institute of Parasitology, University of Veterinary Medicine, ; Vienna, Austria
                [8 ]ISNI 0000 0001 0120 3326, GRID grid.7644.1, Department of Veterinary Medicine, , University of Bari, ; Valenzano, Italy
                [9 ]ISNI 0000 0001 1012 5390, GRID grid.413013.4, Department of Parasitology and Parasitic Diseases, , University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, ; Cluj-Napoca, Romania
                [10 ]ISNI 0000000121511713, GRID grid.10772.33, Global Health and Tropical Medicine (GHTM), Instituto de Higiene e Medicina Tropical (IHMT), Universidade Nova de Lisboa (UNL), ; Lisboa, Portugal
                [11 ]ISNI 0000 0001 1009 2154, GRID grid.412968.0, Department of Pathology and Parasitology, , University of Veterinary and Pharmaceutical Sciences, ; Brno, Czech Republic
                [12 ]Biology Centre, Institute of Parasitology, Czech Academy of Sciences, České Budějovice, Czech Republic
                [13 ]ISNI 0000 0000 9116 4836, GRID grid.14095.39, Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, ; Berlin, Germany
                [14 ]ISNI 0000000109457005, GRID grid.4793.9, Laboratory of Parasitology and Parasitic Diseases, Faculty of Veterinary Sciences, , Aristotle University of Thessaloniki, ; Thessaloniki, Greece
                [15 ]ISNI 0000 0001 2149 743X, GRID grid.10822.39, Laboratory for medical and veterinary entomology, Faculty of Agriculture, , University of Novi Sad, ; Novi Sad, Serbia
                [16 ]ISNI 0000 0001 2230 9752, GRID grid.9647.c, Institute of Animal Hygiene and Veterinary Public Health, Veterinary Faculty, University of Leipzig, ; Leipzig, Germany
                [17 ]ISNI 0000 0004 0475 5996, GRID grid.483502.8, Scientific Veterinary Institute “Novi Sad”, ; Novi Sad, Serbia
                [18 ]ISNI 0000 0004 0587 0574, GRID grid.416786.a, Swiss Tropical and Public Health Institute, ; Basel, Switzerland
                [19 ]ISNI 0000 0004 1937 0642, GRID grid.6612.3, University Basel, ; Basel, Switzerland
                [20 ]ISNI 0000 0004 1937 0650, GRID grid.7400.3, National Centre of Vector Entomology, , University of Zurich, ; Zurich, Switzerland
                [21 ]GRID grid.417834.d, Institute of Infectology, Friedrich-Loeffler-Institute, ; Isle of Riems, Greifswald, Germany
                Article
                3205
                10.1186/s13071-018-3205-x
                6299983
                30567586
                6887edd4-8bdd-49b0-a105-79c7dc793c41
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

                History
                : 19 July 2018
                : 19 November 2018
                Categories
                Review
                Custom metadata
                © The Author(s) 2018

                Parasitology
                dirofilaria repens,vector-borne infections,mosquitoes,zoonosis,emergent parasite,one health

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