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In Europe, the zoonotic parasite Dirofilaria repens continues to spread northward. We describe three likely autochthonous canine microfilaremic D. repens infections from Estonia, an European Union country located in the Baltic region of northern Europe. The parasite species was confirmed with sequencing. These are new northernmost D. repens findings in Europe and show that the zoonotic parasite has spread farther north. Infection with D. repens should be included in the list of differential diagnoses for human and animal hosts also in northern Europe.
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... The northern border of distribution of Dirofilaria spp. is practically not limited by the availability of vectors but rather by environmental factors allowing microfilariae to mature into infective larvae in the vectors (Genchi et al. 2011b, Sassnau and Genchi 2013, Pietikäinen et al. 2017. The northernmost European locations, where D. repens life cycle has been confirmed, are Tartumaa county in Estonia ( Jokelainen et al. 2016) and the Novgorod Region in Russia (Ermakova et al. 2014). ...
... The last searches were performed on December 27, 2019. Jokelainen et al. 2016, Sab unas et al. 2019. The parasite has since then established itself in all three countries. ...
... In Estonia, the first reported D. repens finding was from a dog, detected apparently in 2012 ( Järvis 2012) and the first finding that was confirmed by molecular methods to be D. repens was made from a dog the following year 2013 ( Jokelainen et al. 2016). The confirmed finding was part of a case series that reported microfilaremia in three dogs, all without history of travel or import. ...
Article
The zoonotic parasite Dirofilaria repens has spread toward north in Europe, and cases of autochthonous dirofilariosis caused by D. repens have emerged in the Baltic countries Estonia, Latvia, and Lithuania. We conducted a review on the emergence of dirofilariosis in humans and domestic dogs in these three countries in northeastern Europe. Based on the available literature and reports, the first finding in the Baltic countries was made in Latvia in 2008, followed by the first in Lithuania in 2010, and the first in Estonia in 2012. In all three countries, further findings were reported soon after the first reports. By the end of 2019, autochthonous human D. repens infections had been described from Latvia and Lithuania, and autochthonous canine D. repens infections had been described from all three Baltic countries. While no epidemiological studies estimating prevalence or incidence of the human infections have been published from the three countries, a substantial proportion of investigated dogs have tested positive for microfilariae in studies performed in Latvia and Lithuania. Dirofilariosis is an emerging zoonosis in northern Europe, and the summarized data confirm that D. repens has become established and endemic in the Baltic countries. The available data do not provide a good overview of the situation, and further epidemiological studies are needed. Awareness about the recently emerged zoonotic parasite should be increased among medical doctors, veterinarians, and the general public. Managing this zoonotic infection is a public health challenge that needs to be addressed using a One Health approach. Investigating the spread of D. repens in the Baltic countries could be useful for better preparedness for the anticipated further spread to the Nordic countries.
... There is a clear, recent expansion of D. repens into more northern and particularly north-eastern European countries. While transmission in southern Russia in close vicinity to the Black Sea (Ermakova, Nagorny, Krivorotova, Pshenichnaya, & Matina, 2014;Ermakova, Nagorny, Pshenichnaya, Ambalov, & Boltachiev, 2017) is not very surprising considering subtropical conditions in the summer season in these areas, potential but not always proven autochthonous transmission has been described from northern Germany (Czajka et al., 2014;Sassnau et al., 2013;Tappe et al., 2014), Lithuania (Jokelainen et al., 2016) and even as far north as Finland (Jokelainen et al., 2016). Reports of human, canine and feline infections with D. repens from Asia (e.g., Al-Abd et al., 2015;Ashrafi, Golchai, & Geranmayeh, 2010;Dissanaike, Abeyewickreme, Wijesundera, Weerasooriya, & Ismail, 1997;Lee, Kim, Chong, Klein, & Lee, 2007;Rohela et al., 2009;Wongkamchai et al., 2014) and Africa (e.g., Moodley et al., 2015;Mukendi, Kimbita, Mbanzulu, Maindo, & Misinzo, 2016;Noden & Soni, 2015) are quite rare, presumably because of considerable under diagnosis in resource-poor communities. ...
... There is a clear, recent expansion of D. repens into more northern and particularly north-eastern European countries. While transmission in southern Russia in close vicinity to the Black Sea (Ermakova, Nagorny, Krivorotova, Pshenichnaya, & Matina, 2014;Ermakova, Nagorny, Pshenichnaya, Ambalov, & Boltachiev, 2017) is not very surprising considering subtropical conditions in the summer season in these areas, potential but not always proven autochthonous transmission has been described from northern Germany (Czajka et al., 2014;Sassnau et al., 2013;Tappe et al., 2014), Lithuania (Jokelainen et al., 2016) and even as far north as Finland (Jokelainen et al., 2016). Reports of human, canine and feline infections with D. repens from Asia (e.g., Al-Abd et al., 2015;Ashrafi, Golchai, & Geranmayeh, 2010;Dissanaike, Abeyewickreme, Wijesundera, Weerasooriya, & Ismail, 1997;Lee, Kim, Chong, Klein, & Lee, 2007;Rohela et al., 2009;Wongkamchai et al., 2014) and Africa (e.g., Moodley et al., 2015;Mukendi, Kimbita, Mbanzulu, Maindo, & Misinzo, 2016;Noden & Soni, 2015) are quite rare, presumably because of considerable under diagnosis in resource-poor communities. ...
Article
Dirofilaria repens is a zoonotic, mosquito-borne filaria infecting carnivores, particularly dogs. It is expanding its range in Europe but epidemiological information is sparse for other Eurasian regions. In Hong Kong and India, the closely related species Candidatus Dirofilaria hongkongensis was proposed. Previous analysis of 2.5 kb partial mitochondrial genome sequences containing the particularly variable non-coding control region revealed low diversity in European D. repens while Asian nematodes showed high diversity. Sequences derived from feline blood samples from Narathiwat (Thailand) led to the proposal of a third potential species, Dirofilaria sp. "Thailand II". To avoid bias from rapidly evolving non-coding regions, this study aimed to compare Dirofilaria sp. "Thailand II" with D. repens and C. D. hongkongensis based on complete mitochondrial genomes. Using PCRs and Sanger sequencing, three complete mitochondrial genomes (13,651 bp) were assembled from DNA obtained from different feline blood samples. Mitochondrial genome organisation was identical to other onchocercids with eleven protein-coding, two rRNA and 22 tRNA genes and no atp-8 gene. All genes were on the same strand showing an extremely high thymidine content (56.7%). Maximum-likelihood phylogenetic analysis using protein and rRNA sequences confirmed closer relationship of Dirofilaria sp. "Thailand II" to C. D. hongkongensis than to D. repens. All distances between these three putative species were considerably larger than the distance between the valid sibling species Onchocerca volvulus and Onchocerca ochengi. Sequencing of a 2.5 kb fragment containing the control region from microfilarial DNA from additional feline blood samples from Narathiwat 3-4 years later revealed that these also fell into the C. D. hongkongensis clade but were remarkably different from C. D. hongkongensis and Dirofilaria sp. "Thailand II". Since D. repens-like filaria are absent from dogs in Narathiwat, further field studies are required to confirm if these genotypes represent locally circulating cat-specific Dirofilaria genotypes or species. This article is protected by copyright. All rights reserved.
... The precise transmission dynamics were not determined, but since her recent travel history precluded infection outside Finland, it is speculated that a mosquito within Finland was responsible for this infection. Further uncertainty remains concerning the origin of such an infected mosquito, since D. repens is not otherwise known from Finland, but has been recorded in southeastern Russia and Estonia (Ermakova et al., 2014;Jokelainen et al., 2016;Pietikainen et al., 2017). ...
Thesis
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http://urn.fi/URN:ISBN:978-951-51-8537-2 Mosquitoes (Diptera, Culicidae) are amongst the most socioeconomically important animals in the world, with many species being vectors of disease-causing pathogens, including bacteria, helminths, protozoa and viruses. While not subjected to the same mosquito-borne disease burden as the tropics, Finland nonetheless has three known mosquito-borne viruses which cause disease in humans. Sindbis virus (Togaviridae: Alphavirus), which causes Pogosta disease, as well as Inkoo Virus and Möhkö strains of Chatanga virus (Peribunyaviridae: Orthobunyavirus). Three insect-specific flaviviruses have also been isolated from mosquitoes in Finland, Hanko, Ilomantsi and Lammi viruses (Flaviviridae: Flavivirus) as well as one Negevirus, Mekrijärvi negevirus. Knowledge of the mosquitoes, however, had become outdated, with no significant records of mosquitoes published since 1979 when distribution maps for each of the 38 recorded species were created using historical and contemporary collections. Additionally, the viruses which have been isolated from mosquitoes in Finland have been found in pools of unidentified specimens, which means that no vector or invertebrate host species have been confirmed for five of the seven aforementioned viruses. The aims were therefore to increase the knowledge of the composition and distribution of the Finnish mosquito fauna and the viruses associated with them. Adult and immature mosquito collections were made around the country in all 19 regions (corresponding to the European NUTS-3 divisions) between 2012–2018. The main collection efforts were made in 2014–2017 along transects in Lapland, southern Finland and the mainland of the Åland Archipelago (Ahvennanmaa). All specimens were morphologically identified, where possible, and stored in one of a variety of ways suitable for either virus cell culture experiments, virus PCR experiments, DNA studies or morphological studies. Study I was the first to focus on the mosquitoes of the Åland Archipelago, which is situated between Finland and Sweden in the Baltic Sea. From the collections made on mainland (Fasta) Åland in late 2015 and across 2016, 12 new species records were observed. This included the first country record for Aedes geminus Peus and reconfirmation of Anopheles maculipennis s.s. Meigen and Ochlerotatus sticticus (Meigen) following their recent removal from the fauna of Finland. It also recorded what later became the only confirmed record of Dahliana geniculata (Olivier) in Finland. The Finnish mosquito fauna increased from 38 to 41 species. Study II used DNA sequences extracted from specimens of the Anopheles maculipennis complex to identify which species are present in Finland. This resulted in the discovery of a new country record for Anopheles daciae Linton, Nicolescu & Harbach, a sibling species of An. messeae Falleroni. The Finnish mosquito fauna increased from 41 to 42 species. Study III utilised records for all 52,466 specimens from 1,031 collections to create distribution maps for 40 of the 43 recorded species that were collected for this thesis. Specimens of Aedes rossicus Dolbeškin, Gorickaja & Mitrofanova, Culiseta subochrea (Edwards) and Ochlerotatus cyprius (Ludlow) were not collected, nor mapped, but have been recorded previously. These new collection data significantly extended the recorded distributions for several species, while other common species were still found across the country. Questions were raised about the presence of Ochlerotatus riparius, since only adult specimens were identified, which are easily confused with closely related species. This study provides a solid foundation for future studies to build upon. Study IV explored the RNA viromes of nine man-biting Ochlerotatus species collected in Finland using next generation sequencing. In total, 514 viral polymerases were sequenced, which grouped into 159 species belonging to 25 families or equivalent taxonomic groups as follows: Aliusviridae (1), Aspiviridae (1), Botybirnavirus (8), Chrysoviridae (5), Chuviridae (14), Endornaviridae (2), Flaviviridae (9), Iflaviridae (17), Negevirus (41), Partitiviridae (55), Permutotetraviridae (6), Phasmaviridae (13), Phenuiviridae (58), Picornaviridae (5), Qinviridae (7), Quenyavirus (2), Rhabdoviridae (21), Sedoreoviridae (10), Solemoviridae (15), Spinareoviridae (1), Togaviridae (1), Totiviridae (205), Virgaviridae (7), Xinmoviridae (9) and Yueviridae (1). Twelve of these species have previously been described, while 147 were novel viruses. The host-vector associations of these viruses are yet to be established. Overall, studies I–IV contribute a wealth of contemporary knowledge about the mosquitoes of Finland. More research is required to complete our understanding of mosquito distributions in the country and mosquito-virus associations and interactions, but this thesis provides a solid foundation upon which future research can now be built.
... pipiens (Lundström et al. 2011;Dryselius et al. 2019). Furthermore, the filarial nematode Dirofilaria repens Railliet & Henry appears to also have become established in Estonia, since it has been found in local dogs several times since 2008 (Jokelainen et al. 2016). The mosquito-borne Dirofilaria repens normally parasitizes subcutaneous tissues of carnivores and is often asymptomatic in dogs, but can also infect humans, resulting in skin nodules, ocular dirofilariasis or other complications (Capelli et al. 2018;Ciuca et al. 2020;Pupić-Bakrač et al. 2021). ...
Article
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Female mosquitoes (Diptera: Culicidae) affect their hosts in numerous negative ways and are crucial to the spread of vector-borne pathogens. It is, therefore, important to have a detailed overview of regional mosquitoes, to be able to detect changes in species diversity and identify possible health threats. The aim of this study was to update the checklist of the mosquito fauna of Estonia for the first time since 1957. For this purpose, 24,344 adult mosquitoes (94% females) were collected in Estonia from 2008 to 2020 using various trapping methods. Specimens were primarily identified by morphological characteristics, but DNA barcoding based on the partial cytochrome c oxidase subunit 1 gene (COI) was also used. Species were included in the checklist based on historical records as well as new collections, while also considering reports from neighboring countries. Species records are supplemented with voucher specimens, distribution maps and DNA evidence. The updated checklist includes 34 species, 27 of which were confirmed with recently collected material. All in all, Aedes communis (de Geer, 1776) proved to be the most common mosquito in Estonia, accounting for 30.1% of the specimens collected. This is noteworthy, as this species has been implicated in the transmission of multiple disease agents present in the area. New evidence revealed the presence of Ae. hexodontus Dyar, 1916, Ae. sticticus (Meigen, 1838), Anopheles messeae Falleroni, 1926 and Culiseta bergrothi (Edwards, 1921) in Estonia.
... The situation was very different to that in the nearby Baltic countries, in particular regarding D. repens: almost a fourth of veterinarians practicing in Baltic countries reported having seen dog(s) with D. repens infection, and none of these had a history of travel or import [56]. Dirofilaria repens emerged in the Baltic countries in 2008-2012 and became endemic [11,13,189,190]. ...
Article
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In the past few decades, the relevance of Dirofilaria immitis and Dirofilaria repens, causing cardiopulmonary and subcutaneous dirofilariosis in dogs and cats, and of Angiostrongylus vasorum, causing canine angiostrongylosis, has steadily increased in Central and Northern Europe. In this review, a summary of published articles and additional reports dealing with imported or autoch-thonous cases of these parasites is provided) and Northern (Denmark, Finland, Iceland, Norway, and Sweden) Europe. Research efforts focusing on Dirofilaria spp. and A. vasorum have Citation: Fuehrer, H.-P.; Morelli, S.; Unterköfler, M.S.; Bajer, A.; Bakran-Lebl, K.; Dwużnik, D.; Farkas, R.; Grandi, G.; Heddergott, M.; Jokelainen, P.; et al. Dirofilaria spp. and Angiostrongylus vasorum:
... In contrast to the reduction of prevalence in those areas, increased transmission in Central and Northern Europe has been observed and may be attributed to climate changes (Simón et al., 2012;Capelli et al., 2018;Széll et al., 2020). Even in areas as far north as Finland, Estonia and Siberia, autochthonous cases have been reported (Jokelainen et al., 2016;Pietikäinen et al., 2017;Genchi and Kramer, 2019). An additional factor contributing to the spread of dirofilariosis is the movement of positive dogs from endemic countries to formerly heartworm-free countries like Germany (Genchi et al., 2014). ...
Article
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Dirofilaria immitis, also known as heartworm, is a major parasitic threat for dogs and cats around the world. Because of its impact on the health and welfare of companion animals, heartworm disease is of huge veterinary and economic importance especially in North America, Europe, Asia and Australia. Within the animal health market many different heartworm preventive products are available, all of which contain active components of the same drug class, the macrocyclic lactones. In addition to compliance issues, such as under-dosing or irregular treatment intervals, the occurrence of drug-resistant heartworms within the populations in the Mississippi River areas adds to the failure of preventive treatments. The objective of this review is to provide an overview of the disease, summarize the current disease control measures and highlight potential new avenues and best practices for treatment and prevention.
... There are reports of D. immitis infection also in other Mediterranean countries (Rjeibi et al., 2016;Khatat et al., 2017;Tahir et al., 2017) and Balkans (Rapti and Rehbein, 2010;Ionicǎ et al., 2015;Pantchev et al., 2015;Mrljak et al., 2017), while the parasite progressively spreads over Europe , establishing new enzootic areas in formerly heartworm-free regions (Traversa et al., 2010). Simultaneously, D. repens shows a more aggressive spreading pattern with the northernmost areas reporting autochthonous cases being Northern Russia, Finland and Estonia (Jokelainen et al., 2016;Pietikäinen et al., 2017). ...
Article
The current study investigated for the first time the occurrence of filarial infections in dogs in Cyprus. Blood samples of dogs from five districts of Cyprus (Lefkosia, Lemessos, Larnaka, Pafos and Ammochostos) were examined by the modified Knott's method and by serology, and the morphological classification of microfilariae was confirmed by molecular methods. A total of 200 dogs, 153 living in shelters and 47 owned dogs, were included in the study. Acanthocheilonema reconditum microfilariae were found in 9 (4.5%) samples and one (0.5%) sample was seropositive for D. immitis. No statistical significance was observed between microfilaraemic samples and the evaluated variables apart from the district (p = .005). The present study showed that dogs in Cyprus can be infected with blood circulating microfilariae and for the first time A. reconditum was reported as autochthonous infection in dogs in the country. No microfilariae of Dirofilaria spp. were detected. However, veterinarians should remain vigilant regarding Dirofilaria infections and should consider preventive protection to the animals, at least in case of travel in enzootic areas.
... infections have been seen in Finland and other Nordic countries (e.g., EVIRA 2014, Saevik et al. 2014, Klintebjerg et al. 2015, Vatne 2015, Saari et al. 2016, Pietikäinen et al. 2017, Tiškina et al. 2017. Recently, autochthonous infections have also been reported in the region, for example, canine infections in Estonia ( Jokelainen et al. 2016), and a human case in Finland (Pietikäinen et al. 2017). The lifecycle of D. repens is well established in Russia, where the incidence of autochthonous human infections has increased (Ermakova et al. 2014, Moskvina and Ermolenko 2018. ...
Article
Zoonotic vector-borne parasites Dirofilaria immitis and Dirofilaria repens have been spreading northwards in Europe. Awareness across sectors is a key factor for preparedness to zoonotic emerging diseases. In this study, an online questionnaire was used to survey the knowledge of medical doctors and veterinarians in Finland on whether D. immitis and D. repens can infect humans and dogs, and whether these infections have been detected in Finland. Participants were recruited via two social media discussion groups, and participation was voluntary. The questionnaire was completed by 198 medical doctors and 61 veterinarians in January 2019. Knowing that D. immitis can infect both humans and dogs was indicated by the answers of 7.1% of the medical doctors and 42.6% of the veterinarians—7.6% of the medical doctors and 42.6% of the veterinarians knew D. immitis can infect humans, 9.6% of the medical doctors and 98.4% of the veterinarians knew it can infect dogs. Knowing that D. repens can infect both humans and dogs was indicated by the answers of 3.0% of the medical doctors and 60.7% of the veterinarians—3.0% of the medical doctors and 60.7% of the veterinarians knew D. repens can infect humans; 8.1% of the medical doctors and 88.5% of the veterinarians knew it can infect dogs. Overall, 4.5% of the medical doctors and 59.0% of the veterinarians selected five or more correct “yes” answers. While the results of this survey should be interpreted with caution due to limited number of participants and participation bias, they not only suggest room for improvement but also show presence of cross-sectoral knowledge. Answering “I do not know” was common. Increasing awareness about these emerging zoonotic vector-borne parasites is needed across the sectors.
... Autochthonous D. repens cases have also been recorded in the Netherlands [46], Austria [47,48], Belarus [49] and Ukraine [50]. New D. repens infections in northernmost Europe, which are likely to be autochthonous, have been reported in Estonia [51] and Finland [52]. Climatic changes, global warming and the movement of dogs across Europe are the main factors influencing the continuing spread of Dirofilaria in European countries [11,53]. ...
Article
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Background In Lithuania, the first case of canine subcutaneous dirofilariosis was recorded in 2010. Since then, an increasing number of cases of canine dirofilariosis have been documented in different veterinary clinics throughout the country. Human dirofilariosis was diagnosed in Lithuania for the first time in September 2011. However, to the authors’ knowledge, there are no published data on the presence and prevalence of autochthonous dirofilariosis in dogs and humans in the country. The present study provides information about the predominant species and prevalence of Dirofilaria in dogs and describes the cases of human dirofilariosis in Lithuania. It also outlines PCR detection of the bacterial endosymbiont Wolbachia that contributes to the inflammatory features of filarioid infection. Results A total of 2280 blood samples and six adult worms from pet and shelter dogs were collected in the central and eastern regions of Lithuania in 2013–2015. Based on their morphological appearance, morphometric measurements and molecular analysis, all the adult nematodes were identified as Dirofilaria repens. The diagnosis of microfilariae in blood samples was based on blood smear analysis and Knott’s test. The PCR and sequence analysis of the ribosomal DNA ITS2 region and cox1 gene confirmed the presence of D. repens. Overall, 61 (2.7%) of the 2280 blood samples were found to be positive for the presence of D. repens. The infection rate of D. repens was significantly higher in shelter dogs (19.0%; 19/100) than in pet dogs (1.9%; 42/2180) (χ² = 100.039, df = 1, P < 0.0001). Forty-nine DNA samples of D. repens-infected dogs were tested for the presence of the bacterial endosymbiont Wolbachia and, of these, 40 samples (81.6%) were found to be positive. Three ocular and six subcutaneous cases of human dirofilariosis were diagnosed in Lithuania in the period 2011–2018. Conclusions To the authors’ knowledge, this is the first report of autochthonous D. repens infection in dogs and humans in Lithuania. The present data demonstrate that D. repens is the main etiological agent of dirofilariosis in Lithuania. The DNA of the filarioid endosymbiotic bacterium Wolbachia was detected in the vast majority of dogs infected with D. repens.
... Thus far, the northernmost European site where the parasite life-cycle has been confirmed is Estonia (Tartu 58°23'N, 26°43'E) where D. repens microfilariae were reported in three dogs in 2013-2014 [154], while no human cases have been suspected or confirmed. ...
Article
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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. Electronic supplementary material The online version of this article (10.1186/s13071-018-3205-x) contains supplementary material, which is available to authorized users.
... It has also been found in Lithuania in dogs [20], and in Latvia, in both dogs and humans [21,22]. Thus far, the northernmost European site where the parasite life-cycle has been confirmed to take place is Estonia, where D. repens microfilaraemia was seen in three dogs in 2013-2014 [23]. In European Russia, the reported northern limit of D. repens is in the Novgorod Region [24]. ...
Article
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Background The spread of vector-borne diseases to new regions has become a global threat due to climate change, increasing traffic, and movement of people and animals. Dirofilaria repens, the canine subcutaneous filarioid nematode, has expanded its distribution range northward during the last decades. The northernmost European locations, where the parasite life-cycle has been confirmed, are Estonia and the Novgorod Region in Russia. ResultsHerein, we describe an autochthonous D. repens infection in a Finnish woman. We also present two cases of D. repens infection in imported dogs indicating the life-cycle in the Russian Vyborg and St Petersburg areas, close to the Finnish border. Conclusions The most obvious limiting factor of the northern distribution of D. repens is the summer temperature, due to the temperature-dependent development of larvae in vectors. With continuing climate change, further spread of D. repens in Fennoscandia can be expected.
Chapter
Dirofilaria immitis , also known as heartworm, is a major parasitic threat for dogs and cats around the world. Because of its impact on the health and welfare of companion animals, heartworm disease is of huge veterinary and economic importance especially in North America, Europe, Asia, and Australia. Within the animal health market, many different heartworm preventive products are available, all of which contain active components of the same drug class, the macrocyclic lactones. In addition to compliance issues, such as under‐dosing or irregular treatment intervals, the occurrence of drug‐resistant heartworms within populations in the Mississippi River (United States) delta areas adds to the failure of preventive treatments. Here, we show possibilities for interventions within the parasite life cycle and provide an overview on the prevalence of Dirofilaria spp., on current disease control measures, and available drugs and products.
Article
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.
Article
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Dirofilariasis in humans is a rarely diagnosed vector-borne zoonotic helminthic invasion. It is caused from filarial nematodes genus Dirofilaria & Railliet Henry, 1911 (Onchocercidae, Nematoda). Usually, the life cycle of the parasite takes place between mosquitoes (Culicidae) and carnivores. The human is an accidental host for the dirofilaria wherefore microfilariae in his blood circulation are almost always absent. The pathology of dirofilariasis results from the accidental localization of immature worms in the human body. Dirofilaria immitis caused heart and pulmonary dirofilariasis, but Dirofilaria repens, D. tenuis, and others can are found in different parts of the human body. The spread and Dirofilaria-invasive rates аrе undergone significant modifications affected by global climate change. Surgical extraction of the parasite in humans usually has a therapeutic effect, after which an etiological diagnosis is possible. The aim of the study is to review the current situation of human dirofilariasis in clinical and epidemiological aspects and possibilities for diagnosis.
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The report analyses potential new pathogens and vector species in Finland due to a warming climat and human mobility. In Finnish.
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The Poprad Landscape Park is an area of extraordinary natural, historicaland landscape values, and at the same time is the largest Landscape Park inMałopolska voivodeship. The Dunajec and Poprad valleys as well as the forested mountain ranges of Radziejowa and Jaworzyna Krynicka are the greatest assets ofthis area. The aim of the study was to check the occurrence of Ixodes ricinus at selected four sites located on the nature trail "Rogasiowy Szlak" in the Roztoka Valley located west of the center of Rytro (Małopolska Voivodeship). It is a recreational place, often visited by tourists and walkers, and mainly by children, due to the educational nature of the trail. The ticks were collected by flagging method. A total of 70 individuals of Ixodes ricinus ticks were collected: 7 females (10%), 6 males (9%), 57nymphs (81%), no larval stages were found. The tests confirm the presence of ticks inselected research areas. The results signal a high risk of exposure to ticks on the"Rogasiowy Szlak" nature trail. Research indicates the need to spread knowledge about the occurrence and activity of ticks in unexplored areas of the Poprad Landscape Park.
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Dogs are the primary host for Dirofilaria repens, therefore it is mandatory to accurately diagnose the canine infection and to expand our current knowledge on parasite biology and the immune response of the infected host for a better prevention.Thus, the aim of the present study was to provide new insights from experimental infections of dogs with D. repens, focusing on the evaluation of: 1) the pre-patent period and 2) the antibody response against D. repens somatic antigens and against the Wolbachia endosymbiont. Briefly, on Day 0, twenty purpose-bred Beagle dogs were experimentally infected with 50 infective larvae (L3) of D. repens. Starting from Day 58 until the last day of the study (Day 281), blood samples were collected on a monthly basis for detection of antibodies against D. repens (Dr) and recombinant Wolbachia surface protein (rWSP) by non-commercial IgG-ELISAs. Additional samples were collected on Days 220, 245 and 281 for the detection of microfilariae (mff) using the modified Knott’s test and biomolecular analysis, following two PCR protocols: Gioia et al. (2010; protocol A) and Rishniw et al. (2006- protocol B). The results were analysed by univariate statistical analyses using 2 × 2 contingency tables and K Cohen was calculated to assess the agreement among all the diagnostic techniques. Overall, the outcome of the study revealed that out of the 20 dogs experimentally infected with D. repens, 16 (80%) were microfilaraemic, 17 (85%) were positive at DNA detection in the blood, 18 (90%) had D. repens antibodies and 16 (80%) had Wolbachia antibodies on the last day of the study. The overall k agreement between Knott’s and PCR protocol B was 0.442 (P = 0.0001) and increased throughout the study, reaching 0.828 (P = 0.0001) on Day 281. To the authors knowledge, this is only the second study reporting antibody response to D. repens somatic antigen in experimentally infected dogs. ELISA results showed that an antibody response develops before the onset of patency, and steadily increases with time. Results would suggest that the development of an immunological response to infection could lead to application in epidemiological studies, risk assessment and as an aid in the diagnostic approach in dogs, in particular for early infections without mff.
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The world is changing, and parasites adapt. The Nordic-Baltic region in northern Europe – including the Nordic countries Denmark, Finland, Iceland, Norway and Sweden, and the Baltic States Estonia, Latvia and Lithuania – is facing new parasitological challenges due to changes in populations of parasites and their hosts and the spread of new parasites to the region due to climate change. Some changes can also be ascribed to increased awareness and detection. In this paper, we review and discuss a convenience selection of ten timely examples of recent observations that exemplify trends and challenges from different fields of parasitology, with particular focus on climate change and potential changes in epidemiology of pathogens in northern Europe. The examples illustrate how addressing parasitological challenges often requires both intersectoral and international collaboration, and how using both historical baseline data and modern methodologies are needed.
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Dirofilaria immitis and D. repens are endemic throughout Europe and southern eastern regions of Asia and reported with increasing frequency in Africa. Nevertheless, the increased awareness of veterinary practitioners, even in countries where the prevalence is low, has led to a decrease D. immitis prevalence in dogs, especially in previously endemic/hyper-endemic areas. Prevalence has significantly increased, however, in areas where heartworm has apparently spread more recently, such as Central and North Eastern Europe. Furthermore, autochthonous cases have been observed in Siberia. Low seroprevalence has been reported in Croatia, while in Romania it has reached 14%. In Greece, the prevalence ranges between 0.7% and 25% whilst in Turkey is 0-18%. Data for canine dirofilariosis in Africa is scarce, and most are case reports. Overall, the dominant species is Achanthocheilonema dracunculoides, although both D. immitis and D. repens have been reported from some countries. In the Far East, the prevalence ranges from 2% to 15% in northeastern of China. In Hong Kong a novel species has been found in dogs and humans (Candidatus Dirofilaria hongkongensis). In India, the prevalence ranges from 4.7%-29.5% in Northeastern states. The main factors that have influenced the spreading of Dirofilaria infections are the climate changes and the introduction of new, invasive, competent mosquito species such as Aedes albopictus and Ae. koreicus. Other factors include relocation and insufficient prevention in dogs, manly in the new areas of colonization. Feline heartworm infection has been diagnosed in every European country when diagnosed either by the Knott test or by serology for circulating antibodies and antigens of the parasite. However, prevalence is much lower than in dogs. In spite of the continuing spreading of heartworm infection, D. repens is the main concern in Europe, mostly for physicians, while the infection is nearly always asymptomatic in dogs. The infection is spreading from Portugal to the Southeastern regions of Finland and Siberia, and in some areas its prevalence overlaps that of D. immitis. Many reasons make more difficult the control of D. repens than D. immitis: the frequent lack of clinical symptoms of suspicion, the specific diagnosis being possible only by blood examination and the inefficacy of some macrocyclic lactones.
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Canine vector-borne diseases have been spreading northwards in Europe, and canine babesiosis and infections with Dirofilaria immitis (heartworm) and Dirofilaria repens have been diagnosed also in the Baltic and the Nordic countries. We used an online questionnaire to survey how large a proportion of veterinarians in the Baltic (Estonia, Latvia, and Lithuania) and the Nordic countries (Denmark, Finland, Iceland, Norway, and Sweden) saw canine babesiosis cases and dogs infected with D. immitis and D. repens in 2016. In addition, questions regarding transmission, zoonotic potential, clinical signs, and treatment of the infections were asked. The questionnaire was completed by 122 veterinarians. In 2016, 23% of them had seen at least one case of canine babesiosis, 15% at least one dog with D. immitis infection, and 9% at least one dog with D. repens infection. A veterinarian working in the Baltic countries had 12.2 times higher odds to have seen a canine babesiosis case and 9.3 times higher odds to have seen a dog with D. repens infection than a veterinarian working in the Nordic countries did. While 48% of the veterinarians knew that canine babesiosis is not considered a zoonosis, 26% knew that D. immitis is zoonotic and 34% knew that D. repens is zoonotic. The results suggested that autochthonous cases of the three vector-borne parasitic infections were seen by veterinarians in the Baltic countries, whereas most cases seen by veterinarians in the Nordic countries appeared to be imported. A substantial proportion of the veterinarians did not know whether the parasites are zoonotic.
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We analyze through a climatic model the influence of regional warming on the geographical spreading and potential risk of infection of human dirofilariosis in Russia, Ukraine, and other post-Soviet states from 1981 to 2011 and estimate the situation by 2030. The model correctly predicts the spatiotemporal location of 97.10% of 2154 clinical cases reported in the area during the studied period, identified by a retrospective review of the literature. There exists also a significant correlation between annual predicted Dirofilaria generations and calculated morbidity. The model states the progressive increase of 14.8% in the potential transmission area, up to latitude 64°N, and 14.7% in population exposure. By 2030 an increase of 18.5% in transmission area and 10.8% in population exposure is expected. These findings strongly suggest the influence of global warming in both geographical spreading and increase in the number of Dirofilaria generations. The results should alert about the epidemiological behavior of dirofilariosis and other mosquito-borne diseases in these and other countries with similar climatic characteristics.
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Dirofilaria repens infection was diagnosed in a dog that had been imported to Norway from Hungary three years previously. The dog was a four-year-old castrated male mixed-breed dog and presented for examination of two masses on the right thoracic wall. Fine needle sampling from the subcutaneous nodules and subsequent cytological examination revealed a high number of microfilariae and a pyogranulomatous inflammation. At re-examination approximately 3 weeks later, both masses had apparently disappeared spontaneously, based on both inspection and palpation. However, examination of peripheral blood by a modified Knott's test revealed a high number of unsheathed microfilariae with mean length of 360 mum and mean width of 6-7 mum, often with the classic umbrella handle appearance of D. repens. Polymerase chain reaction and sequencing confirmed the D. repens diagnosis. Subcutaneous dirofilariosis caused by D. repens is probably the most common cause of human zoonotic dirofilariosis in Europe, but currently is rarely encountered in northern countries such as Norway. However, travelling, import and relocation of dogs have increased, and thus the geographical range of these parasites is likely to increase from traditionally endemic southern regions. Increasing numbers of autochthonous cases of D. repens infections in dogs have been reported in eastern and central Europe. Although infection with D. repens often induces only mild signs or subclinical infections in dogs, they nevertheless represent a reservoir for zoonotic transmission and thus a public health concern, and, in addition, due to the long prepatent period and the high frequency of subclinical infections or infections with unspecific clinical signs, could easily be missed. Lack of experience and expectation of these parasites may mean that infection is underdiagnosed in veterinary clinics in northern countries. Also, predicted climate changes suggest that conditions in some countries where this infection is currently not endemic are likely to become more suitable for development in the intermediate host, and thus the establishment of the infection in new areas.
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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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Climatic changes, together with an increase in the movement of cats and dogs across Europe, have caused an increase in the geographical range of several vector borne parasites like Dirofilaria, and in the risk of infection for animals and humans. The present paper reviews the effects of climate and other global drivers on Dirofilaria immitis and Dirofilaria repens infections in Europe and the possible implications on the transmission and control of these mosquito-borne nematodes. In the last several years, growing degree day (GDD)-based forecast models, which use wide or local scale temperature data, have been developed to predict the occurrence and seasonality of Dirofilaria in different parts of the world. All these models are based on the fact that: there is a threshold of 14 degrees C below which Dirofilaria development will not proceed; and there is a requirement of 130 GDD for larvae to reach infectivity and a maximum life expectancy of 30 days for a vector mosquito. The output of these models predicts that the summer temperatures (with peaks in July) are sufficient to facilitate extrinsic incubation of Dirofilaria even at high latitudes. The global warming projected by the Intergovernmental Panel on Climate Change suggests that warm summers suitable for Dirofilaria transmission in Europe will be the rule in the future decades and if the actual trend of temperature increase continues, filarial infection should spread into previously infection-free areas. These factors not only favour incubation of Dirofilaria, but also impact on mosquito species. Recent findings have also demonstrated that Aedes albopictus is now considered to be an important, competent vector of Dirofilaria infections. This mosquito species could spread from southern to northern European countries in the near future, changing the epidemiological patterns of dirofilariosis both in humans and animals.
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Infection with the endosymbiotic bacteria Wolbachia is widespread in filarial nematodes. Previous studies have suggested concordance between the phylogeny of Wolbachia with that of their nematode hosts. However, there is only one published molecular phylogenetic study of filarial species, based on the 5S rRNA gene spacer. The phylogeny proposed by this study is partially incongruent with previous classifications of filarial nematodes, based on morphological characters. Furthermore, both traditional classifications and molecular phylogenies are, in part, inconsistent with the phylogeny of Wolbachia. Here we report mitochondrial cytochrome oxidase I (COI) gene sequences for 11 species of filaria and for another spirurid nematode which was included as an outgroup. In addition, 16S rRNA, wsp and ftsZ gene sequences were generated for the Wolbachia of several filarial species, in order to complete the available data sets and further resolve the phylogeny of Wolbachia in nematodes. We used these data to evaluate whether nematode and Wolbachia phylogenies are concordant. Some of the possible phylogenetic reconstructions based on COI gene were congruent with the phylogeny of Wolbachia and supported the grouping of the rodent filaria Litomosoides sigmodontis with the lymphatic filariae (i.e. Brugia spp. and Wuchereria spp.) and the sister group relationship of Dirofilaria spp. and Onchocerca spp. However, the placement of the Wolbachia-free filaria Acanthocheilonema viteae is ambiguous and dependent on the phylogenetic methods used.
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Wolbachia pipientis is a bacterial endosymbiont associated with arthropods and filarial nematodes. In filarial nematodes, W. pipientis has been shown to play an important role in the biology of the host and in the immuno-pathology of filariasis. Several species of filariae, including the most important parasites of humans and animals (e.g. Onchocerca volvulus, Wuchereria bancrofti and Dirofilaria immitis) have been shown to harbour these bacteria. Other filarial species, including an important rodent species (Acanthocheilonema viteae), which has been used as a model for the study of filariasis, do not appear to harbour these symbionts. There are still several open questions about the distribution of W. pipientis in filarial nematodes. Firstly the number of species examined is still limited. Secondly, it is not clear whether the absence of W. pipientis in negative species could represent an ancestral characteristic or the result of a secondary loss. Thirdly, several aspects of the phylogeny of filarial nematodes are still unclear and it is thus difficult to overlay the presence/absence of W. pipientis on a tree representing filarial evolution. Here we present the results of a PCR screening for W. pipientis in 16 species of filariae and related nematodes, representing different families/subfamilies. Evidence for the presence of W. pipientis is reported for five species examined for the first time (representing the genera Litomosoides, Litomosa and Dipetalonema); original results on the absence of this bacterium are reported for nine species; for the remaining two species, we have confirmed the absence of W. pipientis recently reported by other authors. In the positive species, the infecting W. pipientis bacteria have been identified through 16S rDNA gene sequence analysis. In addition to the screening for W. pipientis in 16 species, we have generated phylogenetic reconstructions based on mitochondrial gene sequences (12S rDNA; COI), including a total of 28 filarial species and related spirurid nematodes. The mapping of the presence/absence of W. pipientis on the trees generated indicates that these bacteria have possibly been lost during evolution along some lineages of filarial nematodes.
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Microfilariae of Brugia malayi is transmitted to man and other susceptible hosts via mosquito. The transmission of B. malayi from cat to man by Ma. uniformis bite has never been reported. The Ma. uniformis mosquito is the normal vector for Wuchereria bancrofti but has never been reported as a vector for B. malayi, or a susceptible host for the growth and development of the microfilariae of B. malayi. The purpose of this study was to examine the development of B. malayi in Mansonia uniformis after feeding on the blood of an infected cat in the laboratory. The B. malayi infected cat was identified using PCR with the primers Bm-1/Bm-2 on DNA (at 10 ng/50 microl) extracted from the WBC of the cat. W. bancrofti was employed as a negative control. The sensitivity of the B. malayi DNA detection by PCR was 0.0001 ng. Adult Ma. uniformis mosquitos at the ages of 5, 10, and 15 days, 100 mosquitos in each group, were fed on the infected cat blood. Recovery of third stage microfilariae was found to be the highest in the 5-day old mosquito group (48%), followed by the 10- and 15-day old mosquito groups (32% and 18%, respectively). The mean number of B. malayi microfilariae found in thorax, head, and abdomen of the mosquitos were composed. The 5-day old (40.3%) and 10-day old (41.9%) mosquitos were significantly more susceptible to microfilariae than the 15-day old mosquitos (17.8%) (p-values using the Scheffe method: 0.027 and 0.039, respectively). There was no significant difference in the mean number of microfilariae in the thorax (p = 0.482) by age, but the mean numbers of microfilariae in the heads, and abdomens were significantly different by age between the 5- and10-, and the 15-day old mosquitos (p < 0.001 and p = 0.004, respectively).
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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.
Article
Subcutaneous dirofilariosis caused by Dirofilaria repens is common in dogs and it is an emerging helminthozoonosis in Europe, Asia, Africa and also in Hungary. Macrocyclic lactones are used for preventing the infection; however, their activity against the microfilariae and mature stages of this species is questionable. Selamectin is widely used for the prophylaxis of heartworm (D. immitis) infection. The objective of the present study was to test the microfilaricidal efficacy of the topical formulation of selamectin in dogs naturally infected with D. repens . A total of 78 Beagle dogs were examined for the presence of circulating microfilariae by Knott's test. Twenty-three of the microfilaraemic dogs were divided into four groups and included in the trial. The dogs received monthly or biweekly selamectin treatment and were subjected to monthly blood testing for a period of 252 or 336 days. At the end of the study, 65% of the dogs were not microfilaraemic and the rest had low number of microfilariae in their blood. These results indicate that chronic spot-on selamectin treatment may be a useful tool also in the control of canine subcutaneous dirofilariosis.
Uusi loistartunta Suomeen tuodussa koirassa. [In Finnish.] (New parasitic infection in a dog imported to Finland). 2014. Available at www .evira.fi/portal
  • Finnish Evira
  • Food Safety
  • Authority
Evira, Finnish Food Safety Authority. Uusi loistartunta Suomeen tuodussa koirassa. [In Finnish.] (New parasitic infection in a dog imported to Finland). 2014. Available at www .evira.fi/portal/fi/elaimet/elainten+terveys+ja+elaintaudit/ elaintaudit/lemmikkielaimet/koirat/koirien+maahantuontiin+ voi+liittya+riskeja/dirofilaria+repens/
Helminth from the scrotum of a dog)
  • T Järvis
Järvis T. Nugiuss koera munandikotist. [In Estonian.] (Helminth from the scrotum of a dog). Eesti Loomaarstlik Ringvaade 2012; 3:4-6.
Human dirofilariasis (Dirofilaria repens ): Is Latvia a new territory? In: Abstract book of the 1st Conference on Neglected Vectors and Vector-Borne Diseases
  • M Kirjušina
  • A Kr Umin Xa
Kirjušina M, Kr umin xa A. Human dirofilariasis (Dirofilaria repens ): Is Latvia a new territory? In: Abstract book of the 1st Conference on Neglected Vectors and Vector-Borne Diseases. EurNegVec, Cluj-Napoca, Romania, April 8–11, 2014, p. 19. Available at eurnegvec.org/1ac_abstractbook.pdf/
Dirofilaria repens infection in a dog imported to Norway Address correspondence to: Pikka Jokelainen Institute of Veterinary Medicine and Animal Sciences Estonian University of
  • Bk Saevik
  • E Jörundsson
  • T Stachurska-Hagen
  • K Tysnes
Saevik BK, Jörundsson E, Stachurska-Hagen T, Tysnes K, et al. Dirofilaria repens infection in a dog imported to Norway. Acta Vet Scand 2014; 56:6. Address correspondence to: Pikka Jokelainen Institute of Veterinary Medicine and Animal Sciences Estonian University of Life Sciences Kreutzwaldi 62 51014 Tartu Estonia
New parasitic infection in a dog imported to Finland)
  • Evira
Evira, Finnish Food Safety Authority. Uusi loistartunta Suomeen tuodussa koirassa. [In Finnish.] (New parasitic infection in a dog imported to Finland). 2014. Available at www .evira.fi/portal/fi/elaimet/elainten+terveys+ja+elaintaudit/ elaintaudit/lemmikkielaimet/koirat/koirien+maahantuontiin+ voi+liittya+riskeja/dirofilaria+repens/
Available at eurnegvec.org/1ac_abstractbook
  • M Kirjušina
Kirjušina M, Kr umin xa A. Human dirofilariasis (Dirofilaria repens): Is Latvia a new territory? In: Abstract book of the 1st Conference on Neglected Vectors and Vector-Borne Diseases. EurNegVec, Cluj-Napoca, Romania, April 8-11, 2014, p. 19. Available at eurnegvec.org/1ac_abstractbook.pdf/ D. REPENS IN THREE DOGS IN ESTONIA 137