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      Leishmania infantum and Dirofilaria immitis infections in Italy, 2009–2019: changing distribution patterns

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          Abstract

          Background

          For long time, canine leishmaniosis (CanL) was considered endemic in the southern, central, and insular regions of Italy, whereas heartworm disease (HW) caused by Dirofilaria immitis was considered endemic in the northern region and in the swampy Po Valley. Following the reports of new foci of both diseases, in this study we update the distribution patterns and occurrence of new foci of CanL and HW discussing the main drivers for the changes in the epidemiology of these two important zoonotic canine vector-borne diseases.

          Methods

          Based on the statistical analyses of serological assays ( n = 90,633) on L. infantum exposure and D. immitis infection performed by two reference diagnostic centres in Italy over a ten-year period (2009–2019) irrespective of the anamnesis of dogs. The distribution patterns of both parasites are herein presented along with the occurrence of new foci.

          Results

          Results highlighted the changing distribution patterns of L. infantum vs D. immitis infection in Italy. CanL is endemic in some areas of northern regions and HW has endemic foci in central and southern regions and islands. Significant differences in L. infantum exposure and HW infection prevalence among the study macroareas were detected. The overall results of the positive tested samples were 28.2% in southern Italy and islands, 29.6% in central Italy and 21.6% in northern Italy for L. infantum and 2.83% in northern Italy, 7.75% in central Italy and 4.97% in southern Italy and islands for HW. HW positivity significantly varied over years ( χ 2 = 108.401, df = 10, P < 0.0001), gradually increasing from 0.77% in 2009 to 8.47% in 2016–2017.

          Conclusions

          New potential epidemiological scenarios are discussed according to a range of factors (e.g. environmental modifications, occurrence of competent insect vectors, transportation of infected animals to non-endemic areas, chemoprophylaxis or vector preventative measures), which may affect the current distribution. Overall, the results advocate for epidemiological surveillance programmes, more focussed preventative and control measures even in areas where few or no cases of both diseases have been diagnosed.

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          Most cited references29

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          Phlebotomine vectors of the leishmaniases: a review

          An account is given of work published during the past 10 years incriminating species of phlebotomine sandflies as vectors of Leishmania species which infect man. An assessment is made of the degrees of certainty of the vectorial roles of eighty-one species and subspecies of sandflies (thirty-seven Old World and forty-four New World) in the transmission of twenty-nine leishmanial parasites of mammals. At least one species of sandfly is considered to be a proven vector of each of ten parasites. Of the eighty-one sandfly taxa, evidence is judged to be sufficient to incriminate nineteen as proven vectors (eleven Phlebotomus species and eight Lutzomyia species or subspecies) and evidence for a further fourteen (nine Phlebotomus species and five Lutzomyia species or subspecies) is considered to be strong. The suggested criteria for incrimination of a vector are anthropophily and common infection with the same leishmanial parasite as that found in man in the same place. More weight should be given to natural infections persisting after the digestion of a bloodmeal than those in the presence of blood. Supporting evidence is a concordance in the distribution of the fly and the disease in man, proof that the fly feeds regularly on the reservoir host, a flourishing development of the parasite in infected flies and the experimental transmission of the parasite by the bite of the fly.
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            Canine and feline vector-borne diseases in Italy: current situation and perspectives

            In Italy, dogs and cats are at risk of becoming infected by different vector-borne pathogens, including protozoa, bacteria, and helminths. Ticks, fleas, phlebotomine sand flies, and mosquitoes are recognized vectors of pathogens affecting cats and dogs, some of which (e.g., Anaplasma phagocytophilum, Borrelia burgdorferi, Dipylidium caninum, Leishmania infantum, Dirofilaria immitis, and Dirofilaria repens) are of zoonotic concern. Recent studies have highlighted the potential of fleas as vectors of pathogens of zoonotic relevance (e.g., Rickettsia felis) in this country. While some arthropod vectors (e.g., ticks and fleas) are present in certain Italian regions throughout the year, others (e.g., phlebotomine sand flies) are most active during the summer season. Accordingly, control strategies, such as those relying on the systematic use of acaricides and insecticides, should be planned on the basis of the ecology of both vectors and pathogens in different geographical areas in order to improve their effectiveness in reducing the risk of infection by vector-borne pathogens. This article reviews the current situation and perspectives of canine and feline vector-borne diseases in Italy.
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              The northward spread of leishmaniasis in Italy: evidence from retrospective and ongoing studies on the canine reservoir and phlebotomine vectors.

              Visceral leishmaniasis (VL) incidence has been increased in Italy in humans and dogs since the 1990s, with new foci being detected within traditional boundaries of endemic transmission but also in northern regions previously regarded as non-endemic. To monitor the putative VL spreading, surveillance was implemented in northern continental Italy comprising: analysis of human cases recorded from 1990 through 2005; retrospective literature analysis of canine leishmaniasis (CanL) and phlebotomine sandfly records through 2002; prospective investigations in dogs from 2003 through 2005 and surveys on sandflies in 2003 and 2004. Two-hundred-thirty human cases (11% of Italian cases) were recorded. Their stratification by age and HIV status disclosed a sharp decrease of HIV/VL co-infections paralleled by concomitant increase of paediatric and HIV-negative adult patients during the study period. Four patients had no travel history. Seven leishmaniasis foci were retrospectively identified since 1990, whereas prospective investigations in dogs disclosed 47 autochthonous clinical cases and 106 autochthonous seropositives among 5442 dogs (2.1%) from 16 foci of six regions. Parasites were typed as Leishmania infantum MON-1. Four vector species were identified among 1696 Phlebotomus (Larroussius) collected specimens. Comparisons with historical data showed that P. perniciosus and P. neglectus have increased in density and expanded their geographic range in the study area. Northern continental Italy is now focally endemic for VL and a moderate risk for human disease does exist, although the intensity of transmission seems to be lower than in traditional settings of Mediterranean VL.
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                Author and article information

                Contributors
                jairo.mendozaroldan@uniba.it
                giovanni.benelli@unipi.it
                rossella.panarese@uniba.it
                roberta.iatta@uniba.it
                tf@sanmarcovet.it
                frederic.beugnet@boehringer-ingelheim.com
                andrea.zatelli@uniba.it
                domenico.otranto@uniba.it
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                15 April 2020
                15 April 2020
                2020
                : 13
                : 193
                Affiliations
                [1 ]GRID grid.7644.1, ISNI 0000 0001 0120 3326, Dipartimento di Medicina Veterinaria, , Università degli Studi di Bari, ; Bari, Italy
                [2 ]GRID grid.5395.a, ISNI 0000 0004 1757 3729, Department of Agriculture, Food and Environment, , University of Pisa, ; Pisa, Italy
                [3 ]San Marco Veterinary Clinic and Laboratory, Veggiano, Padova Italy
                [4 ]GRID grid.484445.d, ISNI 0000 0004 0544 6220, Boehringer Ingelheim Animal Health, ; Lyon, France
                [5 ]GRID grid.411807.b, ISNI 0000 0000 9828 9578, Faculty of Veterinary Sciences, , Bu-Ali Sina University, ; Hamedan, Iran
                Article
                4063
                10.1186/s13071-020-04063-9
                7161282
                32293524
                fca006ca-6d07-4988-8a43-a7c0adafcac7
                © 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
                : 21 February 2020
                : 6 April 2020
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Parasitology
                aedes mosquitoes,canine vector-borne diseases,dirofilaria immitis,leishmania infantum,sandflies

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