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      Subcutaneous dirofilariosis ( Dirofilaria repens): an infection spreading throughout the old world

      review-article
      1 , , 2
      Parasites & Vectors
      BioMed Central
      15th American Heartworm Society Triennial Symposium
      September 11-13, 2016
      Dirofilaria repens, Subcutaneous dirofilariosis, Zoonosis

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          Abstract

          Background

          Two main Dirofilaria species infect dogs: D. immitis and D. repens. While D. immitis has a worldwide distribution, D. repens is currently found only in Europe, Asia, and Africa. Adult D. repens are located in subcutaneous tissues of natural hosts where they survive for long periods of time. First-stage larvae, microfilariae, circulate in the peripheral bloodstream, where they are taken up by the mosquito intermediate hosts. Infected mosquitoes then transmit infective third-stage (L3) larvae to new hosts through the blood meal. In dogs, most infections are asymptomatic, although cutaneous disorders such as pruritus, dermal swelling, subcutaneous nodules, and ocular conjunctivitis can be observed. Currently, two factors have increased the concerns about this parasitic infection 1) its spread throughout the European countries and to other continents and its prevalence in dog populations, where in some cases it has overcome D. immitis; and 2) its zoonotic potential, which is much greater than that of D. immitis.

          Results

          Different hypotheses can be put forward to explain these concerns. First, climate change has allowed more favorable conditions for survival of culicid vectors. Second, accidental hosts such as humans may have a less efficient immune reaction against a parasite that is located in subcutaneous tissues, and thus less exposed to the host’s immune response than, for instance, D. immitis. Furthermore, the absence of clinical signs in the majority of canine infections and the difficulty in diagnosing the infection, due to the lack of serologic tests and thus the reliance on the identification of microfilariae and differentiation from D. immitis to confirm the presence of the parasite, favor the further spread of this species. Finally, among the macrocyclic lactones currently used to prevent heartworm infection, only moxidectin has been found to be fully effective against the infective larvae transmitted by mosquitoes and partially effective (efficacy 96%) against adult D. repens in experimental studies.

          Conclusions

          Dirofilaria repens infection is much more difficult than D. immitis to diagnose and control in the reservoir population (microfilaremic dogs). In addition, lack of familiarity with D. repens infection could lead to lack of vigilance underestimation for this parasite . The number of human cases in Europe and Asia is currently a serious public health concern. Medical doctors and veterinarians must collaborate closely for better control and surveillance of D. repens infection.

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          Most cited references59

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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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            Human dirofilariasis due to Dirofilaria (Nochtiella) repens: an update of world literature from 1995 to 2000.

            Following on from their review of 1995 (Pampiglione et al.), the authors present an update of human cases of dirofilariasis due to Dirofilaria (Nochtiella) repens (Nematoda, Filarioidea, Onchocercidae) reported in the world literature. Cases of the parasitosis published from 1995 to 2000 are reported country by country. The essential data are presented in tabular form and the clinical, parasitological, histopathological, epidemiological features are analysed. 372 new cases spread over 25 countries are thus added to the list published in 1995. The countries most affected are Italy, Sri Lanka, some republics of the ex-Soviet Union. The age of the patients varied from 4 months to 100 years, the majority being in their 40s. There was virtually no difference in incidence between sexes. The parasite appeared most frequently in the upper half of the body, particularly in the head and ocular region and also in the upper limbs. Cases of visceral involvement are also reported. Of the various forms of human dirofilariasis, that due to D. (N.) repens is confirmed to be the most important as regards not only the number of subjects affected and the wide geographical distribution but also the variety of organs involved, notably the lungs, the male genitals and the female breast, invariably leading to a wrong diagnosis of malignant tumour. In man, the zoonosis may be described as emerging: whereas until the middle of the last century only a few dozen cases were reported, in the last 50 years the number has gradually increased to reach the present 782.
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              Changing climate and changing vector-borne disease distribution: the example of Dirofilaria in Europe.

              Climatic changes, together with an increase in the movement of dogs across Europe, have caused an increase in the geographical range of Dirofilaria infections. The present paper is focuses on northeastern European countries, where survey data have shown an increase of Dirofilaria repens infections both in animals and humans. A growing degree day-based forecast model has been developed to predict the occurrence. The model is based on evidence that there is a threshold of 14 °C below which Dirofilaria development will not proceed in mosquitoes, there is a requirement of 130 growing degree-days (GDDs) for larvae to reach infectivity, and there is a maximum life expectancy of 30 days for a mosquito vector. The output of this model predicted that the summer temperatures (with peaks in August) are sufficient to facilitate extrinsic incubation of Dirofilaria even at latitudes of 56 °N and longitudes of 39 °E. Despite the fact that both Dirofilaria immitis and D. repens have the same temperature requirement for extrinsic incubation in mosquitoes, empirical data has shown that D. repens is the main cause of dirofilarial infections in both humans and animals. Clinical signs are absent in most canine infections with D. repens. Furthermore, diagnosis is problematic and in-clinic serological tests, such as those for D. immitis, do not exist. Therefore, most infections go undiagnosed, allowing the infection to spread undetected. Copyright © 2011 Elsevier B.V. All rights reserved.
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                Author and article information

                Contributors
                +39 0250317101 , claudio.genchi@unimi.it
                laurahellen.kramer@unipr.it
                Conference
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                9 November 2017
                9 November 2017
                2017
                : 10
                Issue : Suppl 2 Issue sponsor : Publication of this supplement was funded by the American Heartworm Society. The articles have undergone the journal's standard peer review process for supplements. The Supplement Editor declares that they have no competing interests.
                : 517
                Affiliations
                [1 ]ISNI 0000 0004 1757 2822, GRID grid.4708.b, Dipartimento di Medicina Veterinaria, , Università degli Studi di Milano, ; 20133 Milan, Italy
                [2 ]ISNI 0000 0004 1758 0937, GRID grid.10383.39, Dipartimento di Scienze Medico Veterinarie, , Università di Parma, ; Parma, Italy
                Article
                2434
                10.1186/s13071-017-2434-8
                5688444
                29143643
                4d7f4165-303e-4bb7-9944-8ff38357bfeb
                © The Author(s). 2017

                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.

                15th American Heartworm Society Triennial Symposium
                New Orleans, LA, USA
                September 11-13, 2016
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                © The Author(s) 2017

                Parasitology
                dirofilaria repens,subcutaneous dirofilariosis,zoonosis
                Parasitology
                dirofilaria repens, subcutaneous dirofilariosis, zoonosis

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