Monitoring of Animal Dirofilariosis Incidence in Kharkiv Region of Ukraine
Abstract
A total of 38 species of mosquitoes of the Culicidae family of two subfamilies Anophelinae and Culicinae belonging to 6 genera, were identified on the territory of Kharkiv Region from 2009 to 2019. Dirofilaria larvae were found in 932 insects, which was 4.46 % of the surveyed mosquitoes. The prevalence of the infection of female mosquitoes by dirofilaria was 4.46 ± 0.24 %, while the mean intensity of dirofilariae was 5.4 ± 2.1. Infection of mosquitoes with dirofilariae is currently detected in 11 districts of Kharkiv Region and the city of Kharkiv. The infection rate of mosquitoes of the genus Aedes was 3.83 ± 0.63 %, of the genus Culex — 0.75 ± 0.34 %, of the genus Anopheles — 0.12 ± 0.39 %, whereas females of the genera Culiseta, Coquillettidia, and Uranotaenia were uninfected. It was found that in Kharkiv Region there were 2 types of canine dirofilariae — Dirofilaria immitis (Leidy, 1856) and Dirofilaria repens (Railliet & Henry, 1911), with a predominance of Dirofilaria repens. For the period from 2009 to 2019, we examined 378 blood samples from dogs (190 males and 188 females) aged from 8 months to 13 years with suspected dirofilariasis. According to the results of the studies, 140 samples were positive, the prevalence of infection by the larvae of Dirofilaria spp. in blood samples from dogs with suspected dirofilariasis was 37.03 ± 0.12 %, while infection with Dirofilaria immitis was 2.86 ± 0.45 %, and Dirofilaria repens — 97.35 ± 0.24 %. The number of positive samples from mongrel dogs was 42 (30 %). It was found that cats are more often amicrofilariaemic than dogs.
References
Anvari, D., Saadati, D., Siyadatpanah, A., Gholami, S. 2019. Prevalence of dirofilariasis in shepherd and stray dogs in Iranshahr, southeast of Iran. Journal of Parasitic Diseases, 43, 319-323.
https://doi.org/10.1007/s12639-019-01096-5
Bocková, E., Iglodyova, A., Kočišová, A. 2015. Potential mosquito (Diptera:Culicidae) vector of Dirofilaria repens and Dirofilaria immitis in urban areas of Eastern Slovakia. Parasitology Research, 114 (12).
https://doi.org/10.1007/s00436-015-4692-8
Bodnia, K. I., Potapova, L. M. 2016. Vliyaniye global'nogo izmeneniya klimata na vidovoy sostav i chislennost' krovososushchikh dvukrylykh i kleshchey kak perenoschikov zooantroponoznykh zabolevaniy [The impact of global climate change on the species composition and abundance of bloodsucking diptera and mites as vectors zooanthroponoses]. International Medical Journal, 22 (4), 91-93 [In Russian]. http://nbuv.gov.ua/UJRN/Mmzh_2016_22_4_20
Bogach, M., Paliy, A., Liulin, P., Perots'ka, L., Bohach, O., Pyvovarova, I., Palii, A. 2021. Parasites of domestic and wild pigeons in the south of Ukraine. Biosystems Diversity, 29 (2), 135-139.
https://doi.org/10.15421/012118
Bogach, M. V., Paliy, A. P., Perotsʼka, L. V., Pyvovarova, І. V., Stoyanova, V. Y., Palii, A. P. 2020. The influence of hydro-meteorological conditions on the spread of chicken cestodiasis. Regulatory Mechanisms in Biosystems, 11 (3), 414-418.
https://doi.org/10.15421/022063
Boyko, O. O., Kabar, A. M., Brygadyrenko, V. V. 2020. Nematicidal activity of aqueous tinctures of medicinal plants against larvae of the nematodes Strongyloides papillosus and Haemonchus contortus. Biosystems Diversity, 28 (1), 119-123.
https://doi.org/10.15421/012016
Chagas, C. R. F., Binkienė, R., Ilgūnas, M., Iezhova, T., Valkiūnas, G. 2020. The buffy coat method: a tool for detection of blood parasites without staining procedures. Parasites & Vectors, 13 (1), 104.
https://doi.org/10.1186/s13071-020-3984-8
Chungpivat, S., Taweethavonsawat, P. 2008. The differentiation of microfilariae in dogs and cats using Giemsa's staining and the detection of acid phosphatase activity. J Thai Vet Pract., 20, 47-55.
Cielecka, D., Żarnowska-Prymek, H., Masny, A., Salamatin, R., Wesołowska, M., Gołąb, E. 2012. Human dirofilariosis in Poland: the first cases of autochthonous infections with Dirofilaria repens. Annals of Agricultural and Environmental Medicine, 19 (3), 445-450.
Dantas-Torres, F., Otranto, D. 2013. Dirofilariosis in the Americas: a more virulent Dirofilaria immitis? Parasites & Vectors, 6 (1), 288.
https://doi.org/10.1186/1756-3305-6-288
Demiaszkiewicz, A. W., Polańczyk, G., Osińska, B., Pyziel, A. M., Kuligowska, I., Lachowicz, J., Sikorski, A. 2014. The prevalence and distribution of Dirofilaria repens in dogs in the Mazovian Province of central-eastern Poland. Annals of agricultural and environmental medicine, 21 (4), 701-704.
https://doi.org/10.5604/12321966.1129918
Diaz, J. H. 2015. Increasing Risks of Human Dirofilariasis in Travelers. Journal of Travel Medicine, 22(2), 116-123.
https://doi.org/10.1111/jtm.12174
Filipcova, O. V., Gazzavi-Rogozina, L. V., Bodnia, I. P., Naboka, O. I. 2016. Dyrofilyarioz u Kharkivsʹkiy oblasti vzhe ne ekzotyka [Heartworm disease in the Kharkiv region is no longer exotic]. Modern pharmacy, 4, 76-77 [in Ukrainian].
Fuehrer, H. P., Auer, H., Leschnik, M., Silbermayr, K., Duscher, G., Joachim, A. 2016. Dirofilaria in Humans, Dogs, and Vectors in Austria (1978-2014) From Imported Pathogens to the Endemicity of Dirofilaria repens. PLoS neglected tropical diseases, 10 (5), e0004547.
https://doi.org/10.1371/journal.pntd.0004547
Furtado, A. P., Do Carmo, E. S., Giese, E. G., Vallinoto, A. C., Lanfredi, R. M., Santos, J. N. 2009. Detection of dog filariasis in Marajo Island, Brazil by classical and molecular methods. Parasitology research, 105 (6), 1509-1515.
https://doi.org/10.1007/s00436-009-1584-9
Furtado, A. P., Melo, F. T. V., Giese, E. G., dos Santos, J. N. 2010. Morphological Redescription of Dirofilaria immitis. The Journal of Parasitology, 96 (3), 499-504.
https://doi.org/10.1645/GE-2178.1
Gazzawi-Rogozina, L. V. 2015. Vidovoy sostav malyariynykh komarov Khar'kovskoy oblasti. prirodnyye faktory rasprostraneniya malyarii [Species composition of malarial mosquitoes Kharkiv region. natural factors of malaria transmission]. Annals of Mechnikov Institute, 2, 105-107 [in Russian]. http://nbuv.gov.ua/UJRN/ami_2015_2_18
Genchi, C., Kramer, L. H., Rivasi, F. 2011. Dirofilarial infections in Europe. Vector borne and zoonotic diseases, 11(10), 1307-1317.
https://doi.org/10.1089/vbz.2010.0247
Genchi, C., Kramer, L. 2017. Subcutaneous dirofilariosis (Dirofilaria repens): an infection spreading throughout the old world. Parasites & Vectors, 10 (Suppl 2), 517.
https://doi.org/10.1186/s13071-017-2434-8
Hou, H., Shen, G., Wu, W., Gong, P., Liu, Q., You, J., Cai, Y., Li, J., Zhang, X. 2011. Prevalence of Dirofilaria immitis infection in dogs from Dandong, China. Veterinary parasitology, 183 (1-2), 189-193.
https://doi.org/10.1016/j.vetpar.2011.06.016
Ionică, A. M., Matei, I. A., Mircean, V., Dumitrache, M. O., D'Amico, G., Győrke, A., Pantchev, N., Annoscia, G., Albrechtová, K., Otranto, D., Modrý, D., Mihalca, A. D. 2014. Current surveys on the prevalence and distribution of Dirofilaria spp. and Acanthocheilonema reconditum infections in dogs in Romania. Parasitology Research, 114 (3), 975-982.
https://doi.org/10.1007/s00436-014-4263-4
Jokelainen, P., Mõtsküla, P. F., Heikkinen, P., Ülevaino, E., Oksanen, A., Lassen, B. 2016. Dirofilaria repens Microfilaremia in Three Dogs in Estonia. Vector borne and zoonotic diseases, 16 (2), 136-138.
https://doi.org/10.1089/vbz.2015.1833
Khedri, J., Radfar, M. H., Borji, H., Azizzadeh, M., Akhtardanesh, B. 2014. Canine Heartworm in Southeastern of Iran with Review of disease distribution. Iranian journal of parasitology, 9 (4), 560-567. PMID: 25759738
Landum, M., Ferreira, C. C., Calado, M., Alho, A. M., Maurício, I. L., Meireles, J. S., de Carvalho, L. M., Cunha, C., Belo, S. 2014. Detection of Wolbachia in Dirofilaria infected dogs in Portugal. Veterinary parasitology, 204 (3-4), 407-410.
https://doi.org/10.1016/j.vetpar.2014.05.027
Magnis, J., Lorentz, S., Guardone, L., Grimm, F., Magi, M., Naucke, T. J., Deplazes, P. 2013. Morphometric analyses of canine blood microfilariae isolated by the Knott's test enables Dirofilaria immitis and D. repens species-specific and Acanthocheilonema (syn. Dipetalonema) genus-specific diagnosis. Parasites & Vectors, 6, 48.
https://doi.org/10.1186/1756-3305-6-48
Manrique‐Saide, P., Escobedo‐Ortegón, J., Bolio‐González, M., Sauri‐Arceo, C., Dzib‐Florez, S., Guillermo‐May, G., Ceh‐Pavía, E., Lenhart, A. 2010. Incrimination of the mosquito, Aedes taeniorhynchus, as the primary vector of heartworm, Dirofilaria immitis, in coastal Yucatan, Mexico. Medical and Veterinary Entomology, 24 (4), 456-460.
https://doi.org/10.1111/j.1365-2915.2010.00884.x
Maurizio, A., Frangipane di Regalbono, A., Cassini, R. 2021. Quantitative monitoring of selected groups of parasites in domestic ruminants: a comparative review. Pathogens (Basel, Switzerland), 10 (9), 1173.
https://doi.org/10.3390/pathogens10091173
Miterpáková, M., Antolová, D., Hurníková, Z., Dubinský, P., Pavlačka, A., Németh, J. 2010. Dirofilaria infections in working dogs in Slovakia. Journal of Helminthology, 84 (2), 173-176.
https://doi.org/10.1017/S0022149X09990496
Orr, B., Ma, G., Koh, W. L., Malik, R., Norris, J. M., Westman, M. E., Wigney, D., Brown, G., Ward, M. P., Šlapeta, J. 2020. Pig-hunting dogs are an at-risk population for canine heartworm (Dirofilaria immitis) infection in eastern Australia. Parasites & Vectors, 13, 69.
https://doi.org/10.1186/s13071-020-3943-4
Paliy, A. P., Mashkey, A. M., Sumakova, N. V., Paliy, A. P. 2018 a. Distribution of poultry ectoparasites in industrial farms, farms, and private plots with different rearing technologies. Biosystems Diversity, 26 (2), 153-159.
https://doi.org/10.15421/011824
Paliy, A. P., Mashkey, A. N., Faly, L. I., Kysterna, O. S., Rebenko, H. I., Palii, A. P. 2021. Ecology of zoophilic flies in livestock biocenoses of Ukraine. Biosystems Diversity, 29 (3), 258-263.
https://doi.org/10.15421/012132
Paliy, A. P., Sumakova, N. V., Mashkey, A. M., Petrov, R. V., Paliy, A. P., Ishchenko, K. V. 2018 b. Contamination of animal-keeping premises with eggs of parasitic worms. Biosystems Diversity, 26 (4), 327-333.
https://doi.org/10.15421/011848
Paliy, A., Sumakova, N., Petrov, R., Shkromada, O., Ulko, L., Palii, A. 2019. Contamination of urbanized territories with eggs of helmiths of animals. Biosystems Diversity, 27 (2), 118-124.
https://doi.org/10.15421/011916
Pietikäinen, R., Nordling, S., Jokiranta, S., Saari, S., Heikkinen, P., Gardiner, C., Kerttula, A. M., Kantanen, T., Nikanorova, A., Laaksonen, S., Lavikainen, A., Oksanen, A. 2017. Dirofilaria repens transmission in southeastern Finland. Parasites & Vectors, 10 (1), 561.
https://doi.org/10.1186/s13071-017-2499-4
Pisarski, K. 2019. The global burden of disease of zoonotic parasitic diseases: top 5 contenders for priority consideration. Tropical Medicine and Infectious Disease, 4 (1), 44.
https://doi.org/10.3390/tropicalmed4010044
Reinert, J. F. 2009. List of abbreviations for currently valid generic-level taxa in family Culicidae (Diptera). European Mosquito Bulletin, 27, 68-76.
Rudolf, I., Šebesta, O., Mendel, J., Betášová, L., Bocková, E., Jedličková, P., Venclíková, K., Blažejová, H., Šikutová, S., Hubálek, Z. 2014. Zoonotic Dirofilaria repens (Nematoda: Filarioidea) in Aedes vexans mosquitoes, Czech Republic. Parasitology research, 113 (12), 4663-4667.
https://doi.org/10.1007/s00436-014-4191-3
Rzayev, F. H. 2021. A systematic review of flukes (Trematoda) of domestic goose (Anser anser dom.). Biosystems Diversity, 29 (3), 294-302.
https://doi.org/10.15421/012137
Sabūnas, V., Radzijevskaja, J., Sakalauskas, P., Petkevičius, S., Karvelienė, B., Žiliukienė, J., Lipatova, I., Paulauskas, A. 2019. Dirofilaria repens in dogs and humans in Lithuania. Parasites & Vectors, 12, 177.
https://doi.org/10.1186/s13071-019-3406-y
Saichenko, I. V., Antipov, A. A., Bakhur, T. I., Bezditko, L. V., Shmayun, S. S. 2021. Co-infection of Trichuris vulpis and Toxocara canis in different aged dogs: Influence on the haematological indices. Biosystems Diversity, 29 (2), 129-134.
https://doi.org/10.15421/012117
Sałamatin, R. V., Pavlikovska, T. M., Sagach, O. S., Nikolayenko, S. M., Kornyushin, V. V., Kharchenko, V. O., Masny, A., Cielecka, D., Konieczna-Sałamatin, J., Conn, D. B., Golab, E. 2013. Human dirofilariasis due to Dirofilaria repens in Ukraine, an emergent zoonosis: epidemiological report of 1465 cases. Acta parasitologica, 58 (4), 592-598.
https://doi.org/10.2478/s11686-013-0187-x
Shekhar, K. C., Pathmanathan, R., Krishnan, R. 1996. Human infection with Dirofilaria repens in Malaysia. Journal of Helminthology, 70 (3), 249-252.
https://doi.org/10.1017/S0022149X00015480
Shkromada, O., Skliar, O., Paliy, A., Ulko, L., Gerun, I., Naumenko, О., Ishchenko, K., Kysterna, O., Musiienko, O., Paliy A. 2019. Development of measures to improve milk quality and safety during production. Eastern-European Journal of enterprise technologies, 3/11 (99), 30-39.
https://doi.org/10.15587/1729-4061.2019.168762
Silaghi, C., Beck, R., Capelli, G., Montarsi, F., Mathis, A. 2017. Development of Dirofilaria immitis and Dirofilaria repens in Aedes japonicas and Aedes geniculatus. Parasites & Vectors, 10, 94.
https://doi.org/10.1186/s13071-017-2015-x
Simón, F., Siles-Lucas, M., Morchón, R., González-Miguel, J., Mellado, I., Carretón, E., Montoya-Alonso, J. A. 2012. Human and animal dirofilariasis: the emergence of a zoonotic mosaic. Clinical microbiology reviews, 25 (3), 507-544.
https://doi.org/10.1128/CMR.00012-12
Simsek, S., Ozkanlar, Y., Balkaya, I., Aktas, M. S. 2011. Microscopic, serologic and molecular surveys on Dirofilaria immitis in stray dogs, Turkey. Veterinary Parasitology, 183 (1-2), 109-113.
https://doi.org/10.1016/j.vetpar.2011.06.012
Șuleșco, T., Volkova, T., Yashkova, S., Tomazatos, A., von Thien, H., Lühken, R., Tannich, E. 2016. Detection of Dirofilaria repens and Dirofilaria immitis DNA in mosquitoes from Belarus. Parasitology research, 115 (9), 3535-3541.
https://doi.org/10.1007/s00436-016-5118-y
Tarello, W. 2008. Autochthonous Dirofilaria (Nochtiella) repens infection in dogs in Kuwait. Zoonoses and public health, 55 (6), 328-330.
https://doi.org/10.1111/j.1863-2378.2008.01140.x
Tasić, A., Rossi, L., Tasić, S., Miladinović-Tasić, N., Ilić, T., Dimitrijević, S. 2008. Dimitrijević S Survey of canine dirofilariasis in Vojvodina, Serbia. Parasitology Research, 103 (6), 1297-1302.
https://doi.org/10.1007/s00436-008-1132-z
Todorovic, S., McKay, T. 2020. Potential mosquito (Diptera: Culicidae) vectors of Dirofilaria immitis from residential entryways in Northeast Arkansas. Veterinary Parasitology, 282, 109105.
https://doi.org/10.1016/j.vetpar.2020.109105
Trancoso, T. A. L., Lima, N. C., Barbosa, A. S., Leles, D., Fonseca, A. B. M., Labarthe, N. V., Bastos, O. M. P., Uchôa, C. M. A. 2020. Detection of Dirofilaria immitis using microscopic, serological and molecular techniques among dogs in Cabo Frio, RJ, Brazil. Revista Brasileira de Parasitologia Veterinária, 29 (1), e017219.
https://doi.org/10.1590/s1984-29612020009
Trari, B., Dakki, M., Harbach, R. E. 2017. An updated checklist of the Culicidae (Diptera) of Morocco, with notes on species of historical and current medical importance. Journal of Vector Ecology, 42 (1), 94-104.
https://doi.org/10.1111/jvec.12243
Weil, G. J., Ramzy, R. M. 2007. Diagnostic tools for filariasis elimination programs. Trends in parasitology, 23 (2), 78-82.
https://doi.org/10.1016/j.pt.2006.12.001
Wilkerson, R. C., Linton, Y-M., Fonseca, D. M., Schultz, T. R., Price, D. C., Strickman, D. A. 2015. Making Mosquito Taxonomy Useful: A Stable Classification of Tribe Aedini that Balances Utility with Current Knowledge of Evolutionary Relationships. PLoS ONE, 10 (7), e0133602.
https://doi.org/10.1371/journal.pone.0133602
Wu, C. C., Fan, P. C. 2003. Prevalence of canine dirofilariasis in Taiwan. Journal of Helminthology, 77 (1), 83-88.