{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T22:03:53Z","timestamp":1791410633799,"version":"4.3.3"},"reference-count":82,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2025,7,2]],"date-time":"2025-07-02T00:00:00Z","timestamp":1751414400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2025,7,2]],"date-time":"2025-07-02T00:00:00Z","timestamp":1751414400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","award":["01Kl2022"],"award-info":[{"award-number":["01Kl2022"]}],"id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Bernhard-Nocht-Institut f\u00fcr Tropenmedizin"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Infect Dis Poverty"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>\n                      <jats:italic>Dirofilaria immitis<\/jats:italic>\n                      and\n                      <jats:italic>D. repens<\/jats:italic>\n                      are mosquito-borne nematodes with dogs as primary hosts, but other mammalian species including humans can be also infected. In the last century, circulation of both pathogens was predominantly restricted to Southern Europe. However, different studies indicated a potential establishment in Central, Eastern and Western parts of Europe as an increasing threat to animal and human health. Therefore, we conducted a systematic literature review of\n                      <jats:italic>Dirofilaria<\/jats:italic>\n                      data in Europe to give a comprehensive overview of potential mosquito vectors and vertebrate hosts, including the collection of different metadata (e.g. sampling year and site), allowing to analyse the spread pattern of the parasites in Europe.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      On 24 January 2022, we conducted a systematic literature review of all available publications in the PubMed database reporting\n                      <jats:italic>D. immitis<\/jats:italic>\n                      and\n                      <jats:italic>D. repens<\/jats:italic>\n                      screening in mosquitoes and mammalian vertebrates in Europe. We only included acute infection of\n                      <jats:italic>Dirofilaria<\/jats:italic>\n                      spp., i.e. excluding studies only screening antibodies, and in addition noted the travel history and the accuracy of the sampling locations. These data were used to analyse the range of potential vectors and hosts and for a comparison of the spatial distribution between the twentieth and twenty-first century.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Both nematodes appear to have a high overlap of\n                      <jats:italic>Aedes<\/jats:italic>\n                      ,\n                      <jats:italic>Anopheles<\/jats:italic>\n                      and\n                      <jats:italic>Culex as<\/jats:italic>\n                      potential vector species, which are abundant in Europe. Most published\n                      <jats:italic>D. immitis<\/jats:italic>\n                      infections were reported in dogs, while\n                      <jats:italic>D. repens<\/jats:italic>\n                      predominantly were reported in humans.\n                      <jats:italic>Dirofilaria immitis<\/jats:italic>\n                      infections were detected in a wider range of wild and zoo animals. Compared to the last century, many more countries especially in Central Europe were affected by\n                      <jats:italic>Dirofilaria<\/jats:italic>\n                      spp. circulation, illustrating a significant spread over the last 20\u00a0years.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>\n                      Our findings suggest that\n                      <jats:italic>D. immitis<\/jats:italic>\n                      and\n                      <jats:italic>D. repens<\/jats:italic>\n                      are a growing health concern for animals and humans in Europe. Continuous globalisation and climate warming will probably lead to a further spread and increased circulation in the future. All data are made available open access, which will enable further analysis.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Graphical Abstract<\/jats:title>\n                  <\/jats:sec>","DOI":"10.1186\/s40249-025-01328-2","type":"journal-article","created":{"date-parts":[[2025,7,2]],"date-time":"2025-07-02T02:31:10Z","timestamp":1751423470000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Vectors, host range, and spatial distribution of Dirofilaria immitis and D. repens in Europe: a systematic review"],"prefix":"10.1186","volume":"14","author":[{"given":"Carolin","family":"Hattendorf","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1984-839X","authenticated-orcid":false,"given":"Renke","family":"L\u00fchken","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,7,2]]},"reference":[{"key":"1328_CR1","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/S0065-308X(08)00204-2","volume":"66","author":"JW McCall","year":"2008","unstructured":"McCall JW, Genchi C, Kramer LH, Guerrero J, Venco L. Heartworm disease in animals and humans. Adv Parasitol. 2008;66:193\u2013285. https:\/\/doi.org\/10.1016\/S0065-308X(08)00204-2.","journal-title":"Adv Parasitol"},{"key":"1328_CR2","doi-asserted-by":"publisher","first-page":"482","DOI":"10.1186\/s13071-020-04353-2","volume":"13","author":"B Moroni","year":"2020","unstructured":"Moroni B, Rossi L, Meneguz PG, Orusa R, Zoppi S, Robetto S. Dirofilaria immitis in wolves recolonizing northern Italy: are wolves competent hosts? Parasit Vectors. 2020;13:482. https:\/\/doi.org\/10.1186\/s13071-020-04353-2.","journal-title":"Parasit Vectors"},{"key":"1328_CR3","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1079\/JOH200152","volume":"75","author":"JM Egovia","year":"2001","unstructured":"Egovia JM, Torres J, Miquel J, Llaneza L, Feliu C. Helminths in the wolf, Canis lupus, from north-western Spain. J Helminthol. 2001;75:183\u201392.","journal-title":"J Helminthol"},{"key":"1328_CR4","doi-asserted-by":"publisher","first-page":"837","DOI":"10.7589\/2019-09-234","volume":"56","author":"H Medkour","year":"2020","unstructured":"Medkour H, Laidoudi Y, Mari\u00e9 J-L, Fenollar F, Davoust B, Mediannikov O. Molecular investigation of vector-borne pathogens in red foxes (Vulpes vulpes) from southern France. J Wildl Dis. 2020;56:837\u201350. https:\/\/doi.org\/10.7589\/2019-09-234.","journal-title":"J Wildl Dis"},{"key":"1328_CR5","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.vetpar.2016.05.012","volume":"224","author":"JM Liesner","year":"2016","unstructured":"Liesner JM, Kr\u00fccken J, Schaper R, Pachnicke S, Kohn B, M\u00fcller E, et al. Vector-borne pathogens in dogs and red foxes from the federal state of Brandenburg. Germany Vet Parasitol. 2016;224:44\u201351. https:\/\/doi.org\/10.1016\/j.vetpar.2016.05.012.","journal-title":"Germany Vet Parasitol"},{"key":"1328_CR6","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1128\/CMR.00012-12","volume":"25","author":"F Sim\u00f3n","year":"2012","unstructured":"Sim\u00f3n F, Siles-Lucas M, Morch\u00f3n R, Gonz\u00e1lez-Miguel J, Mellado I, Carret\u00f3n E, et al. Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clin Microbiol Rev. 2012;25:507\u201344.","journal-title":"Clin Microbiol Rev"},{"key":"1328_CR7","doi-asserted-by":"publisher","first-page":"1127","DOI":"10.1016\/j.cvsm.2009.06.003","volume":"39","author":"DD Bowman","year":"2009","unstructured":"Bowman DD, Atkins CE. Heartworm biology, treatment, and control. Vet Clin North Am Small Anim Pract. 2009;39:1127\u201358. https:\/\/doi.org\/10.1016\/j.cvsm.2009.06.003.","journal-title":"Vet Clin North Am Small Anim Pract"},{"key":"1328_CR8","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1177\/1098612X18823348","volume":"21","author":"S Garrity","year":"2019","unstructured":"Garrity S, Lee-Fowler T, Reinero C. Feline asthma and heartworm disease: clinical features, diagnostics and therapeutics. J Feline Med Surg. 2019;21:825\u201334. https:\/\/doi.org\/10.1177\/1098612X18823348.","journal-title":"J Feline Med Surg"},{"key":"1328_CR9","doi-asserted-by":"publisher","first-page":"109131","DOI":"10.1016\/j.vetpar.2020.109131","volume":"283","author":"MK Ames","year":"2020","unstructured":"Ames MK, Atkins CE. Treatment of dogs with severe heartworm disease. Vet Parasitol. 2020;283:109131. https:\/\/doi.org\/10.1016\/j.vetpar.2020.109131.","journal-title":"Vet Parasitol"},{"key":"1328_CR10","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.amjms.2021.07.017","volume":"363","author":"BK Saha","year":"2022","unstructured":"Saha BK, Bonnier A, Chong WH, Chieng H, Austin A, Hu K, et al. Human pulmonary dirofilariasis: a review for the clinicians. Am J Med Sci. 2022;363:11\u20137. https:\/\/doi.org\/10.1016\/j.amjms.2021.07.017.","journal-title":"Am J Med Sci"},{"key":"1328_CR11","doi-asserted-by":"publisher","first-page":"1307","DOI":"10.1089\/vbz.2010.0247","volume":"11","author":"C Genchi","year":"2011","unstructured":"Genchi C, Kramer LH, Rivasi F. Dirofilarial infections in Europe. Vector Borne Zoonotic Dis. 2011;11:1307\u201317. https:\/\/doi.org\/10.1089\/vbz.2010.0247.","journal-title":"Vector Borne Zoonotic Dis"},{"key":"1328_CR12","first-page":"35","volume":"112","author":"TI Avdiukhina","year":"1996","unstructured":"Avdiukhina TI, Lysenko AI, Supriaga VG, Postnova VF. Dirofilariasis of the vision organ: registry and analysis of 50 cases in the Russian Federation and in countries of the United Independent States. Vestn Oftalmol. 1996;112:35\u20139.","journal-title":"Vestn Oftalmol"},{"key":"1328_CR13","doi-asserted-by":"publisher","first-page":"567","DOI":"10.1159\/000325796","volume":"51","author":"S Negahban","year":"2007","unstructured":"Negahban S, Daneshbod Y, Atefi S, Daneshbod K, Sadjjadi SM, Hosseini SV, et al. Dirofilaria repens diagnosed by the presence of microfilariae in fine needle aspirates: a case report. Acta Cytol. 2007;51:567\u201370. https:\/\/doi.org\/10.1159\/000325796.","journal-title":"Acta Cytol"},{"key":"1328_CR14","doi-asserted-by":"publisher","first-page":"1761","DOI":"10.3201\/eid2409.180462","volume":"24","author":"I Potters","year":"2018","unstructured":"Potters I, Vanfraechem G, Bottieau E. Dirofilaria repens nematode infection with microfilaremia in traveler returning to Belgium from Senegal. Emerg Infect Dis. 2018;24:1761\u20133. https:\/\/doi.org\/10.3201\/eid2409.180462.","journal-title":"Emerg Infect Dis"},{"key":"1328_CR15","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1111\/j.1699-0463.1998.tb01352.x","volume":"106","author":"V Petrocheilou","year":"1998","unstructured":"Petrocheilou V, Theodorakis M, Williams J, Prifti H, Georgilis K, Apostolopoulou I, et al. Microfilaremia from a Dirofilaria-like parasite in Greece. Case report. APMIS. 1998;106:315\u20138.","journal-title":"APMIS"},{"key":"1328_CR16","first-page":"183","volume":"87","author":"JP Nozais","year":"1994","unstructured":"Nozais JP, Bain O, Gentilini M. A case of subcutaneous Dirofilaria (Nochtiella) repens with microfilaremia originating in Corsica. Bull Soc Pathol Exot. 1994;87:183\u20135.","journal-title":"Bull Soc Pathol Exot"},{"key":"1328_CR17","doi-asserted-by":"publisher","first-page":"100306","DOI":"10.1016\/j.onehlt.2021.100306","volume":"13","author":"A Pupi\u0107-Bakra\u010d","year":"2021","unstructured":"Pupi\u0107-Bakra\u010d A, Pupi\u0107-Bakra\u010d J, Beck A, Jurkovi\u0107 D, Polkinghorne A, Beck R. Dirofilaria repens microfilaremia in humans: case description and literature review. One Health. 2021;13:100306. https:\/\/doi.org\/10.1016\/j.onehlt.2021.100306.","journal-title":"One Health"},{"key":"1328_CR18","doi-asserted-by":"publisher","DOI":"10.1186\/s13071-017-2434-8","author":"C Genchi","year":"2017","unstructured":"Genchi C, Kramer L. Subcutaneous dirofilariosis (Dirofilaria repens): an infection spreading throughout the old world. Parasit Vectors. 2017. https:\/\/doi.org\/10.1186\/s13071-017-2434-8.","journal-title":"Parasit Vectors"},{"key":"1328_CR19","doi-asserted-by":"publisher","first-page":"663","DOI":"10.1186\/s13071-018-3205-x","volume":"11","author":"G Capelli","year":"2018","unstructured":"Capelli G, Genchi C, Baneth G, Bourdeau P, Brianti E, Cardoso L, et al. Recent advances on Dirofilaria repens in dogs and humans in Europe. Parasit Vectors. 2018;11:663. https:\/\/doi.org\/10.1186\/s13071-018-3205-x.","journal-title":"Parasit Vectors"},{"key":"1328_CR20","unstructured":"Lusitano A. Curationum Medicinalium Centuria Septima. Venetiis: apud Vincentium Valgresium, curatio 63. 1566. p. 106."},{"key":"1328_CR21","first-page":"77","volume-title":"Trattato cinegetico, ovvero della caccia","author":"F Birago","year":"1626","unstructured":"Birago F. Trattato cinegetico, ovvero della caccia. Milan: Sfondrato V; 1626. p. 77."},{"key":"1328_CR22","doi-asserted-by":"publisher","first-page":"108995","DOI":"10.1016\/j.vetpar.2019.108995","volume":"280","author":"C Genchi","year":"2020","unstructured":"Genchi C, Kramer LH. The prevalence of Dirofilaria immitis and D. repens in the Old World. Vet Parasitol. 2020;280:108995. https:\/\/doi.org\/10.1016\/j.vetpar.2019.108995.","journal-title":"Vet Parasitol"},{"key":"1328_CR23","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1186\/1756-3305-6-38","volume":"6","author":"A Masny","year":"2013","unstructured":"Masny A, Go\u0142\u0105b E, Cielecka D, Sa\u0142amatin R. Vector-borne helminths of dogs and humans - focus on central and eastern parts of Europe. Parasit Vectors. 2013;6:38. https:\/\/doi.org\/10.1186\/1756-3305-6-38.","journal-title":"Parasit Vectors"},{"key":"1328_CR24","doi-asserted-by":"publisher","first-page":"109067","DOI":"10.1016\/j.vetpar.2020.109067","volume":"280","author":"Z Sz\u00e9ll","year":"2020","unstructured":"Sz\u00e9ll Z, Bacsadi \u00c1, Szeredi L, Nemes C, F\u00e9zer B, Bakcsa E, et al. Rapid spread and emergence of heartworm resulting from climate and climate-driven ecological changes in Hungary. Vet Parasitol. 2020;280:109067. https:\/\/doi.org\/10.1016\/j.vetpar.2020.109067.","journal-title":"Vet Parasitol"},{"key":"1328_CR25","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.vetpar.2005.04.009","volume":"133","author":"C Genchi","year":"2005","unstructured":"Genchi C, Rinaldi L, Cascone C, Mortarino M, Cringoli G. Is heartworm disease really spreading in Europe? Vet Parasitol. 2005;133:137\u201348. https:\/\/doi.org\/10.1016\/j.vetpar.2005.04.009.","journal-title":"Vet Parasitol"},{"key":"1328_CR26","doi-asserted-by":"publisher","first-page":"286","DOI":"10.1016\/j.vetpar.2009.03.026","volume":"163","author":"C Genchi","year":"2009","unstructured":"Genchi C, Rinaldi L, Mortarino M, Genchi M, Cringoli G. Climate and Dirofilaria infection in Europe. Vet Parasitol. 2009;163:286\u201392. https:\/\/doi.org\/10.1016\/j.vetpar.2009.03.026.","journal-title":"Vet Parasitol"},{"key":"1328_CR27","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1136\/vr.152.4.97","volume":"152","author":"LA Trotz-Williams","year":"2003","unstructured":"Trotz-Williams LA, Trees AJ. Systematic review of the distribution of the major vector-borne parasitic infections in dogs and cats in Europe. Vet Rec. 2003;152:97\u2013105. https:\/\/doi.org\/10.1136\/vr.152.4.97.","journal-title":"Vet Rec"},{"key":"1328_CR28","unstructured":"PubMed. National Library of Medicine. 2025. https:\/\/pubmed.ncbi.nlm.nih.gov\/. Accessed 29 Mar 2025."},{"key":"1328_CR29","unstructured":"Eurostat. NUTS - Nomenclature of territorial units for statistic. 2025. https:\/\/ec.europa.eu\/eurostat\/web\/nuts\/background. Accessed 29 Mar 2025."},{"key":"1328_CR30","unstructured":"The R Project for Statistical Computing. 2025. https:\/\/www.R-project.org. Accessed 29 Mar 2025."},{"key":"1328_CR31","unstructured":"Hijmans RJ. Terra: Spatial Data Analysis. 2024. 2025. https:\/\/CRAN.R-project.org\/package=terra. Accessed 29 Mar 2025."},{"key":"1328_CR32","doi-asserted-by":"publisher","unstructured":"Hernang\u00f3mez D. Using the tidyverse with terra objects: the tidyterra package. J Open Source Softw. 2023;8:5751. https:\/\/doi.org\/10.21105\/joss.05751","DOI":"10.21105\/joss.05751"},{"key":"1328_CR33","unstructured":"Hijmans RJ, Barbosa M, Ghosh A, Mandel A. geodata: Download Geographic Data. 2024. 2025. https:\/\/CRAN.R-project.org\/package=geodata. Accessed 29 Mar 2025."},{"key":"1328_CR34","unstructured":"Wickham H, Bryan J. readxl: Read Excel Files. 2023. 2025. https:\/\/CRAN.R-project.org\/package=readxl. Accessed 29 Mar 2025."},{"key":"1328_CR35","unstructured":"Kassambara A. ggpubr: \u201cggplot2\u201d Based Publication Ready Plots. 2023. https:\/\/CRAN.R-project.org\/package=ggpubr. Accessed 29 Mar 2025."},{"key":"1328_CR36","doi-asserted-by":"publisher","DOI":"10.18637\/jss.v040.i01","author":"H Wickham","year":"2011","unstructured":"Wickham H. The split-apply-combine strategy for data analysis. J Stat Softw. 2011. https:\/\/doi.org\/10.18637\/jss.v040.i01.","journal-title":"J Stat Softw"},{"key":"1328_CR37","unstructured":"Wickham H, Fran\u00e7ois R, Henry L, M\u00fcller K, Vaughan D. dplyr: A Grammar of Data Manipulation. 2023. 2025. https:\/\/CRAN.R-project.org\/package=dplyr. Accessed 29 Mar 2025."},{"key":"1328_CR38","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-319-24277-4","volume-title":"ggplot2","author":"H Wickham","year":"2016","unstructured":"Wickham H. ggplot2. Cham: Springer International Publishing; 2016. https:\/\/doi.org\/10.1007\/978-3-319-24277-4."},{"key":"1328_CR39","doi-asserted-by":"publisher","first-page":"206","DOI":"10.1186\/1756-3305-7-206","volume":"7","author":"C Genchi","year":"2014","unstructured":"Genchi C, Bowman D, Drake J. Canine heartworm disease (Dirofilaria immitis) in Western Europe: survey of veterinary awareness and perceptions. Parasit Vectors. 2014;7:206. https:\/\/doi.org\/10.1186\/1756-3305-7-206.","journal-title":"Parasit Vectors"},{"key":"1328_CR40","doi-asserted-by":"publisher","first-page":"1042","DOI":"10.3390\/pathogens11091042","volume":"11","author":"R Morch\u00f3n","year":"2022","unstructured":"Morch\u00f3n R, Montoya-Alonso JA, Rodr\u00edguez-Escolar I, Carret\u00f3n E. What has happened to heartworm disease in Europe in the last 10 years? Pathogens. 2022;11:1042. https:\/\/doi.org\/10.3390\/pathogens11091042.","journal-title":"Pathogens"},{"key":"1328_CR41","doi-asserted-by":"publisher","first-page":"196","DOI":"10.3389\/fphys.2012.00196","volume":"3","author":"R Morch\u00f3n","year":"2012","unstructured":"Morch\u00f3n R, Carret\u00f3n E, Gonz\u00e1lez-Miguel J, Mellado-Hern\u00e1ndez I. Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends. Front Physiol. 2012;3:196. https:\/\/doi.org\/10.3389\/fphys.2012.00196.","journal-title":"Front Physiol"},{"key":"1328_CR42","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1186\/s13071-024-06439-7","volume":"17","author":"ML Wehmeyer","year":"2024","unstructured":"Wehmeyer ML, Jaworski L, J\u00f6st H, \u0218ule\u0219co T, Rauh\u00f6ft L, Afonso SMM, et al. Host attraction and host feeding patterns indicate generalist feeding of Culex pipiens s.s. and Cx. torrentium. Parasit Vectors. 2024;17:369. https:\/\/doi.org\/10.1186\/s13071-024-06439-7.","journal-title":"Parasit Vectors"},{"key":"1328_CR43","unstructured":"European Centre for Disease Prevention and Control. Mosquito maps. 2023. 2025. https:\/\/www.ecdc.europa.eu\/en\/disease-vectors\/surveillance-and-disease-data\/mosquito-maps. Accessed 29 Mar 2025."},{"key":"1328_CR44","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1186\/s13071-016-1597-z","volume":"9","author":"J B\u00f6rstler","year":"2016","unstructured":"B\u00f6rstler J, J\u00f6st H, Garms R, Kr\u00fcger A, Tannich E, Becker N, et al. Host-feeding patterns of mosquito species in Germany. Parasit Vectors. 2016;9:318. https:\/\/doi.org\/10.1186\/s13071-016-1597-z.","journal-title":"Parasit Vectors"},{"key":"1328_CR45","doi-asserted-by":"publisher","first-page":"1268","DOI":"10.3390\/pathogens10101268","volume":"10","author":"H-P Fuehrer","year":"2021","unstructured":"Fuehrer H-P, Morelli S, Unterk\u00f6fler MS, Bajer A, Bakran-Lebl K, Dwu\u017cnik-Szarek D, et al. Dirofilaria spp. and Angiostrongylus vasorum: current risk of spreading in Central and Northern Europe. Pathogens. 2021;10:1268. https:\/\/doi.org\/10.3390\/pathogens10101268.","journal-title":"Pathogens"},{"key":"1328_CR46","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1053\/j.tcam.2010.09.003","volume":"25","author":"ACY Lee","year":"2010","unstructured":"Lee ACY, Atkins CE. Understanding feline heartworm infection: disease, diagnosis, and treatment. Top Companion Anim Med. 2010;25:224\u201330. https:\/\/doi.org\/10.1053\/j.tcam.2010.09.003.","journal-title":"Top Companion Anim Med"},{"key":"1328_CR47","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1186\/1756-3305-3-25","volume":"3","author":"S Mazzariol","year":"2010","unstructured":"Mazzariol S, Cassini R, Voltan L, Aresu L, Di Regalbono F, Heartworm A. Dirofilaria immitis infection in a leopard (Panthera pardus pardus) housed in a zoological park in north-eastern Italy. Parasit Vectors. 2010;3:25. https:\/\/doi.org\/10.1186\/1756-3305-3-25.","journal-title":"Parasit Vectors"},{"key":"1328_CR48","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1186\/s13071-017-2073-0","volume":"10","author":"AM Alho","year":"2017","unstructured":"Alho AM, Marcelino I, Colella V, Flanagan C, Silva N, Correia JJ, et al. Dirofilaria immitis in pinnipeds and a new host record. Parasit Vectors. 2017;10:142. https:\/\/doi.org\/10.1186\/s13071-017-2073-0.","journal-title":"Parasit Vectors"},{"key":"1328_CR49","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1111\/j.1748-5827.2010.00950.x","volume":"51","author":"V Moln\u00e1r","year":"2010","unstructured":"Moln\u00e1r V, Paz\u00e1r P, Rig\u00f3 D, M\u00e1th\u00e9 D, Fok E, Gl\u00e1vits R, et al. Autochthonous Dirofilaria immitis infection in a ferret with aberrant larval migration in Europe. J Small Anim Pract. 2010;51:393\u20136. https:\/\/doi.org\/10.1111\/j.1748-5827.2010.00950.x.","journal-title":"J Small Anim Pract"},{"key":"1328_CR50","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1136\/vr.158.7.240","volume":"158","author":"MR Ruiz de Yb\u00e1\u00f1ez","year":"2006","unstructured":"Ruiz de Yb\u00e1\u00f1ez MR, Mart\u00ednez-Carrasco C, Mart\u00ednez JJ, Ortiz JM, Attout T, Bain O. Dirofilaria immitis in an African lion (Panthera leo). Vet Rec. 2006;158:240\u20132. https:\/\/doi.org\/10.1136\/vr.158.7.240.","journal-title":"Vet Rec"},{"key":"1328_CR51","doi-asserted-by":"publisher","first-page":"332","DOI":"10.1186\/s13071-017-2269-3","volume":"10","author":"AM Ionic\u0103","year":"2017","unstructured":"Ionic\u0103 AM, Matei IA, D\u2019Amico G, Ababii J, Daskalaki AA, S\u00e1ndor AD, et al. Filarioid infections in wild carnivores: a multispecies survey in Romania. Parasit Vectors. 2017;10:332. https:\/\/doi.org\/10.1186\/s13071-017-2269-3.","journal-title":"Parasit Vectors"},{"key":"1328_CR52","doi-asserted-by":"publisher","first-page":"3281","DOI":"10.1007\/s00436-014-3991-9","volume":"113","author":"A Penezi\u0107","year":"2014","unstructured":"Penezi\u0107 A, Selakovi\u0107 S, Pavlovi\u0107 I, \u0106irovi\u0107 D. First findings and prevalence of adult heartworms (Dirofilaria immitis) in wild carnivores from Serbia. Parasitol Res. 2014;113:3281\u20135. https:\/\/doi.org\/10.1007\/s00436-014-3991-9.","journal-title":"Parasitol Res"},{"key":"1328_CR53","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1016\/j.vetpar.2014.04.004","volume":"203","author":"Z Tolnai","year":"2014","unstructured":"Tolnai Z, Sz\u00e9ll Z, Sproch \u00c1, Szeredi L, Sr\u00e9ter T. Dirofilaria immitis: an emerging parasite in dogs, red foxes and golden jackals in Hungary. Vet Parasitol. 2014;203:339\u201342. https:\/\/doi.org\/10.1016\/j.vetpar.2014.04.004.","journal-title":"Vet Parasitol"},{"key":"1328_CR54","doi-asserted-by":"publisher","first-page":"101409","DOI":"10.1016\/j.cimid.2019.101409","volume":"68","author":"A Potkonjak","year":"2020","unstructured":"Potkonjak A, Rojas A, Guti\u00e9rrez R, Nachum-Biala Y, Kleinerman G, Savi\u0107 S, et al. Molecular survey of Dirofilaria species in stray dogs, red foxes and golden jackals from Vojvodina, Serbia. Comp Immunol Microbiol Infect Dis. 2020;68:101409. https:\/\/doi.org\/10.1016\/j.cimid.2019.101409.","journal-title":"Comp Immunol Microbiol Infect Dis"},{"key":"1328_CR55","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1556\/AVet.2014.021","volume":"62","author":"D Cirovi\u0107","year":"2014","unstructured":"Cirovi\u0107 D, Penezi\u0107 A, Pavlovi\u0107 I, Kuli\u0161i\u0107 Z, Cosi\u0107 N, Burazerovi\u0107 J, et al. First records of Dirofilaria repens in wild canids from the region of Central Balkan. Acta Vet Hung. 2014;62:481\u20138. https:\/\/doi.org\/10.1556\/AVet.2014.021.","journal-title":"Acta Vet Hung"},{"key":"1328_CR56","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1007\/bf00366537","volume":"20","author":"A Marconcini","year":"1996","unstructured":"Marconcini A, Magi M, Macchioni G, Sassetti M. Filariosis in foxes in Italy. Vet Res Commun. 1996;20:316\u20139. https:\/\/doi.org\/10.1007\/bf00366537.","journal-title":"Vet Res Commun"},{"key":"1328_CR57","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1089\/vbz.2007.0207","volume":"8","author":"M Magi","year":"2008","unstructured":"Magi M, Calderini P, Gabrielli S, Dell\u2019Omodarme M, Macchioni F, Prati MC, et al. Vulpes vulpes: a possible wild reservoir for zoonotic filariae. Vector Borne Zoonotic Dis. 2008;8:249\u201352. https:\/\/doi.org\/10.1089\/vbz.2007.0207.","journal-title":"Vector Borne Zoonotic Dis"},{"key":"1328_CR58","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1556\/004.2019.007","volume":"67","author":"P Gavrilovi\u0107","year":"2019","unstructured":"Gavrilovi\u0107 P, Dobrosavljevi\u0107 I, Vaskovi\u0107 N, Todorovi\u0107 I, \u017divulj A, Kurelju\u0161i\u0107 B, et al. Cardiopulmonary parasitic nematodes of the red fox (Vulpes vulpes) in Serbia. Acta Vet Hung. 2019;67:60\u20139. https:\/\/doi.org\/10.1556\/004.2019.007.","journal-title":"Acta Vet Hung"},{"key":"1328_CR59","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/s0304-4017(98)00192-7","volume":"80","author":"C Gort\u00e1zar","year":"1998","unstructured":"Gort\u00e1zar C, Villafuerte R, Lucientes J, Fern\u00e1ndez-de-Luco D. Habitat related differences in helminth parasites of red foxes in the Ebro valley. Vet Parasitol. 1998;80:75\u201381. https:\/\/doi.org\/10.1016\/s0304-4017(98)00192-7.","journal-title":"Vet Parasitol"},{"key":"1328_CR60","doi-asserted-by":"publisher","first-page":"545","DOI":"10.7589\/0090-3558-30.4.545","volume":"30","author":"C Gortazar","year":"1994","unstructured":"Gortazar C, Castillo JA, Lucientes J, Blanco JC, Arriolabengoa A, Calvete C. Factors affecting Dirofilaria immitis prevalence in red foxes in northeastern Spain. J Wildl Dis. 1994;30:545\u20137. https:\/\/doi.org\/10.7589\/0090-3558-30.4.545.","journal-title":"J Wildl Dis"},{"key":"1328_CR61","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/j.vetpar.2016.04.016","volume":"223","author":"A Hod\u017ei\u0107","year":"2016","unstructured":"Hod\u017ei\u0107 A, Ali\u0107 A, Klebi\u0107 I, Kadri\u0107 M, Brianti E, Duscher GG. Red fox (Vulpes vulpes) as a potential reservoir host of cardiorespiratory parasites in Bosnia and Herzegovina. Vet Parasitol. 2016;223:63\u201370. https:\/\/doi.org\/10.1016\/j.vetpar.2016.04.016.","journal-title":"Vet Parasitol"},{"key":"1328_CR62","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1016\/j.vetpar.2008.02.030","volume":"154","author":"ER Morgan","year":"2008","unstructured":"Morgan ER, Tomlinson A, Hunter S, Nichols T, Roberts E, Fox MT, et al. Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Vet Parasitol. 2008;154:48\u201357. https:\/\/doi.org\/10.1016\/j.vetpar.2008.02.030.","journal-title":"Vet Parasitol"},{"key":"1328_CR63","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1186\/s13071-016-1524-3","volume":"9","author":"AM Ionic\u0103\u01ce","year":"2016","unstructured":"Ionic\u0103\u01ce AM, Matei IA, Amico D, Daskalaki G, Jur\u00e1nkov\u00e1 AA, Ionescu J. Role of golden jackals (Canis aureus) as natural reservoirs of Dirofilaria spp. Romania. Parasit Vectors. 2016;9:240. https:\/\/doi.org\/10.1186\/s13071-016-1524-3.","journal-title":"Parasit Vectors"},{"key":"1328_CR64","doi-asserted-by":"publisher","DOI":"10.1515\/ap-2017-0107","author":"P Gavrilovi\u0107","year":"2017","unstructured":"Gavrilovi\u0107 P, Marinkovi\u0107 D, Todorovi\u0107 I, Gavrilovi\u0107 A. First report of pneumonia caused by Angiostrongylus vasorum in a golden jackal. Acta Parasitol. 2017. https:\/\/doi.org\/10.1515\/ap-2017-0107.","journal-title":"Acta Parasitol"},{"key":"1328_CR65","first-page":"175","volume":"60","author":"P Gavrilovi\u0107","year":"2015","unstructured":"Gavrilovi\u0107 P, Blitva-Robertson G, \u00d6zvegy J, Kisk\u00e1roly F, Becskei Z. Case report of dirofilariasis in gray wolf in Serbia. Acta Parasitol. 2015;60:175\u20138.","journal-title":"Acta Parasitol"},{"key":"1328_CR66","doi-asserted-by":"publisher","first-page":"544","DOI":"10.1016\/j.vetpar.2013.02.028","volume":"196","author":"M Miterp\u00e1kov\u00e1","year":"2013","unstructured":"Miterp\u00e1kov\u00e1 M, Hurn\u00edkov\u00e1 Z, Zale\u015bny G, Chovancov\u00e1 B. Molecular evidence for the presence of Dirofilaria repens in beech marten (Martes foina) from Slovakia. Vet Parasitol. 2013;196:544\u20136. https:\/\/doi.org\/10.1016\/j.vetpar.2013.02.028.","journal-title":"Vet Parasitol"},{"key":"1328_CR67","first-page":"149","volume":"37","author":"S Pampiglione","year":"1995","unstructured":"Pampiglione S, Canestri Trotti G, Rivasi F. Human dirofilariasis due to Dirofilaria (Nochtiella) repens: a review of world literature. Parassitologia. 1995;37:149\u201393.","journal-title":"Parassitologia"},{"key":"1328_CR68","first-page":"231","volume":"42","author":"S Pampiglione","year":"2000","unstructured":"Pampiglione S, Rivasi F. Human dirofilariasis due to Dirofilaria (Nochtiella) repens: an update of world literature from 1995 to 2000. Parassitologia. 2000;42:231\u201354.","journal-title":"Parassitologia"},{"key":"1328_CR69","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1016\/j.pt.2010.01.003","volume":"26","author":"ACY Lee","year":"2010","unstructured":"Lee ACY, Montgomery SP, Theis JH, Blagburn BL, Eberhard ML. Public health issues concerning the widespread distribution of canine heartworm disease. Trends Parasitol. 2010;26:168\u201373. https:\/\/doi.org\/10.1016\/j.pt.2010.01.003.","journal-title":"Trends Parasitol"},{"key":"1328_CR70","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1016\/j.vetpar.2008.10.053","volume":"160","author":"H Huang","year":"2009","unstructured":"Huang H, Wang T, Yang G, Zhang Z, Wang C, Yang Z, et al. Molecular characterization and phylogenetic analysis of Dirofilaria immitis of China based on COI and 12S rDNA genes. Vet Parasitol. 2009;160:175\u20139. https:\/\/doi.org\/10.1016\/j.vetpar.2008.10.053.","journal-title":"Vet Parasitol"},{"key":"1328_CR71","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1007\/s002840010100","volume":"41","author":"C Bazzocchi","year":"2000","unstructured":"Bazzocchi C, Jamnongluk W, O\u2019Neill SL, Anderson TJ, Genchi C, Bandi C. wsp gene sequences from the Wolbachia of filarial nematodes. Curr Microbiol. 2000;41:96\u2013100. https:\/\/doi.org\/10.1007\/s002840010100.","journal-title":"Curr Microbiol"},{"key":"1328_CR72","first-page":"65","volume-title":"Factors influencing the spread of heartworms in Italy Interaction between Dirofilaria immitis and Dirofilaria repens","author":"C Genchi","year":"1995","unstructured":"Genchi C, Basano S, Bandi F, Sacco D, Venco B, Vezzoni L. Factors influencing the spread of heartworms in Italy Interaction between Dirofilaria immitis and Dirofilaria repens. Baravia: American Heartworm Society; 1995. p. 65\u201371."},{"key":"1328_CR73","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1016\/j.vetpar.2011.01.012","volume":"176","author":"C Genchi","year":"2011","unstructured":"Genchi C, Mortarino M, Rinaldi L, Cringoli G, Traldi G, Genchi M. Changing climate and changing vector-borne disease distribution: the example of Dirofilaria in Europe. Vet Parasitol. 2011;176:295\u20139. https:\/\/doi.org\/10.1016\/j.vetpar.2011.01.012.","journal-title":"Vet Parasitol"},{"key":"1328_CR74","doi-asserted-by":"publisher","first-page":"1537","DOI":"10.1007\/s00436-011-2659-y","volume":"110","author":"D Hamel","year":"2012","unstructured":"Hamel D, Silaghi C, Lescai D, Pfister K. Epidemiological aspects on vector-borne infections in stray and pet dogs from Romania and Hungary with focus on Babesia spp. Parasitol Res. 2012;110:1537\u201345. https:\/\/doi.org\/10.1007\/s00436-011-2659-y.","journal-title":"Parasitol Res"},{"key":"1328_CR75","doi-asserted-by":"publisher","first-page":"499","DOI":"10.4081\/gh.2016.499","volume":"11","author":"L Ciuc\u0103","year":"2016","unstructured":"Ciuc\u0103 L, Musella V, Miron LD, Maurelli MP, Cringoli G, Bosco A, et al. Geographic distribution of canine heartworm (Dirofilaria immitis) infection in stray dogs of eastern Romania. Geospat Health. 2016;11:499. https:\/\/doi.org\/10.4081\/gh.2016.499.","journal-title":"Geospat Health"},{"key":"1328_CR76","doi-asserted-by":"publisher","first-page":"329","DOI":"10.2478\/helm-2019-0033","volume":"56","author":"H Stoyanova","year":"2019","unstructured":"Stoyanova H, Carret\u00f3n E, Montoya-Alonso JA. Stray dogs of Sofia (Bulgaria) could be an important reservoir of heartworm (Dirofilaria immitis). Helminthologia. 2019;56:329\u201333.","journal-title":"Helminthologia"},{"key":"1328_CR77","first-page":"625","volume":"41","author":"JF Fortin","year":"1981","unstructured":"Fortin JF, Slocombe J. Temperature requirements for the development of Dirofilaria immitis in Aedes triseriatus and Ae. vexans. Mosq News. 1981;41:625\u201333.","journal-title":"Mosq News"},{"key":"1328_CR78","first-page":"141","volume":"37","author":"G Cancrini","year":"1995","unstructured":"Cancrini G, Pietrobelli M, Frangipane di Regalbono AF, Tampieri MP, della Torre A. Development of Dirofilaria and Setaria nematodes in Aedes albopictus. Parassitologia. 1995;37:141\u20135.","journal-title":"Parassitologia"},{"key":"1328_CR79","doi-asserted-by":"publisher","DOI":"10.46471\/gigabyte.57","author":"M\u00c1 Miranda","year":"2022","unstructured":"Miranda M\u00c1, Barcel\u00f3 C, Arnoldi D, Augsten X, Bakran-Lebl K, Balatsos G, et al. AIMSurv: first pan-European harmonized surveillance of Aedes invasive mosquito species of relevance for human vector-borne diseases. GigaByte. 2022. https:\/\/doi.org\/10.46471\/gigabyte.57.","journal-title":"GigaByte"},{"key":"1328_CR80","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1089\/vbz.2006.0562","volume":"7","author":"MQ Benedict","year":"2007","unstructured":"Benedict MQ, Levine RS, Hawley WA, Lounibos LP. Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector Borne Zoonotic Dis. 2007;7:76\u201385. https:\/\/doi.org\/10.1089\/vbz.2006.0562.","journal-title":"Vector Borne Zoonotic Dis"},{"key":"1328_CR81","doi-asserted-by":"publisher","first-page":"9916","DOI":"10.1038\/s41598-021-89096-5","volume":"11","author":"S Oliveira","year":"2021","unstructured":"Oliveira S, Rocha J, Sousa CA, Capinha C. Wide and increasing suitability for Aedes albopictus in Europe is congruent across distribution models. Sci Rep. 2021;11:9916. https:\/\/doi.org\/10.1038\/s41598-021-89096-5.","journal-title":"Sci Rep"},{"key":"1328_CR82","unstructured":"Companion Animal Parasite Council. Heartworm. 2016. 2025. https:\/\/capcvet.org\/guidelines\/heartworm\/. Accessed 29 Mar 2025."}],"container-title":["Infectious Diseases of Poverty"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40249-025-01328-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s40249-025-01328-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40249-025-01328-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,7,2]],"date-time":"2025-07-02T02:31:16Z","timestamp":1751423476000},"score":1,"resource":{"primary":{"URL":"https:\/\/idpjournal.biomedcentral.com\/articles\/10.1186\/s40249-025-01328-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,2]]},"references-count":82,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,12]]}},"alternative-id":["1328"],"URL":"https:\/\/doi.org\/10.1186\/s40249-025-01328-2","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2025.02.17.638693","asserted-by":"object"}]},"ISSN":["2049-9957"],"issn-type":[{"value":"2049-9957","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,7,2]]},"assertion":[{"value":"18 February 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"5 June 2025","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"2 July 2025","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"58"}}