Cited by 56Parasitic Diseases Research and TreatmentHelminth infection and controlResearch on Leishmaniasis Studies

The current situation of canine dirofilariosis in Hungary

Open access
Farkas, Róbert, Mag, Viktória, Gyurkovszky, Mónika, Takács, Nóra, Vörös, Károly, Solymosi, Norbert·2020·Parasitology Research

Abstract

Between April and September 2017, blood samples were collected from 344 randomly selected dogs older than 1 year in 180 settlements of 19 counties in Hungary. The dogs lived exclusively outdoors, had never travelled and had neither been examined for Dirofilaria infection nor treated against mosquitoes with insecticides or/and filarioid worms with macrocyclic lactones. Dirofilaria infection was examined with a modified Knott’s test for microfilariae, DiroCHEK®, for the presence of D. immitis antigen, as well as by multiplex and conventional PCR. Altogether, 77 (22.4%) dogs living in 58 settlements of 17 counties were found to be infected with one or both Dirofilaria species based on the PCR techniques. Twenty-eight (8.1%) and 38 (11.1%) dogs were infected with D. immitis and D. repens , respectively. Coinfections were recorded in 11 samples (3.2%) collected in 11 locations of 8 counties. The results confirmed that both dirofilarioses are endemic in dogs and the eastern areas of the country are hyperendemic for heartworm disease. Temperature showed a significant association with the prevalence of D. immitis (OR 2.41, 95% CI 1.24–4.86, p = 0.012) but not with that of D. repens (OR 1.37, 95% CI 0.78–2.47, p = 0.286). The prevalence of neither D. immitis (OR 0.99, 95% CI 0.98–1.00, p = 0.213) nor D. repens (OR 1.01, 95% CI 0.99–1.01, p = 0.094) showed a significant correlation with precipitation. The number of yearly growing degree days (GDD) based on the lifecycle of Dirofilaria in mosquitoes ranged between 3.73 and 7.57 for the Hungarian districts. The GDD showed a significant positive association with the prevalence of D. immitis (OR 2.38, 95% CI 1.43–4.15, p = 0.001) and a non-significant positive relationship with that of D. repens (OR 1.25, 95% CI 0.83–1.95, p = 0.291).

AI snapshot

Written from the paper’s full text.

TL;DR

In a 2017 survey of 344 outdoor, non-travelled, untreated dogs across Hungary, 22.4% were infected with Dirofilaria spp., with D. repens at 14.2% and D. immitis at 11.3%. Both infections were endemic, heartworm disease was hyperendemic in eastern Hungary, and temperature/GDD were significantly associated with D. immitis prevalence.

Key findings

  • Overall Dirofilaria prevalence was 22.4% (77/344) by serology and PCR; PCR-based single infections were 28 (8.1%) for D. immitis and 38 (11.1%) for D. repens, with coinfections in 11 (3.2%). Total animals with heartworms were 39 (11.3%), and total D. repens prevalence was 49/344 (14.2%).
  • Infected dogs lived in 58 settlements of 17 counties; D. immitis-infected dogs were in 34 settlements of 12 counties and D. repens-infected dogs in 35 settlements of 16 counties. Significant spatial clusters were found for D. immitis (p < 0.001) and D. repens (p = 0.044), with eastern Hungary hyperendemic for heartworm disease.
  • Temperature was significantly associated with D. immitis prevalence (OR 2.41, 95% CI 1.24–4.86, p = 0.012) but not D. repens (OR 1.37, 95% CI 0.78–2.47, p = 0.286). GDD-based yearly Dirofilaria lifecycles ranged from 3.73 to 7.57 and were significantly associated with D. immitis (OR 2.38, 95% CI 1.43–4.15, p = 0.001) but not D. repens (OR 1.25, 95% CI 0.83–1.95, p = 0.291). Precipitation was not significantly associated with either species.

Methods

  • Cross-sectional survey between April and September 2017: blood samples from 344 randomly selected dogs older than 1 year in 180 settlements of 19 Hungarian counties, excluding Budapest. Dogs lived exclusively outdoors, had never travelled out of their county, and had not been examined or treated for Dirofilaria or treated against mosquitoes with insecticides and filarioid worms with macrocyclic lactones.
  • Diagnostic testing used a modified Knott’s test for microfilariae, DiroCHEK® for D. immitis antigen, and multiplex and conventional PCR targeting 12S rDNA of both Dirofilaria spp. and 16S rRNA of D. immitis; PCR was performed on blood samples containing microfilariae.
  • Spatial clustering was tested with the Kulldorff scan method, and environmental associations were analysed by logistic regression using NUTS 4 climate data from ECMWF ERA-Interim for 2008–2017, including temperature, precipitation, and growing degree days (GDD).

Limitations

  • The authors state that other factors—such as vector and host population density, potential mosquito-breeding habitats, and veterinarians’ awareness—also play critical roles but were not analysed; they call for further systematic monitoring to understand environmental risk factors and identify competent mosquito vectors. They also note it is not known why D. repens has higher prevalence than D. immitis and that further research is needed on temperature effects on D. repens.
  • Evident from the text: PCR was performed only on samples containing microfilariae, so molecular detection was conditional on microfilaraemia, and no specific serological test for D. repens was available.
  • Evident from the text: the study population was restricted to dogs older than 1 year that lived exclusively outdoors, had never travelled, and had not received prior Dirofilaria examination or preventive treatment, so prevalence estimates may not represent all Hungarian dogs.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1007/s00436-019-06478-5

Cites

46 of 46 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 12 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    No significant spatial aggregation was found for the pooled data of both species (p = 0.07).

    “However, non-significant (p = 0.07) spatial aggregation was found for the pooled data of both species.”
    Quote in the paperNot a substantial claim
  • Findingown data

    Precipitation did not show a significant correlation with the prevalence of D. immitis (OR 0.99, 95% CI 0.98-1.00, p = 0.213).

    “The prevalence of neither D. immitis (OR 0.99, 95% CI 0.98–1.00, p = 0.213) nor D. repens (OR 1.01, 95% CI 0.99–1.01, p = 0.094) showed a significant correlation with precipitation.”
    • Also stated in: § Results · plain
      “The prevalence of neither D. immitis (OR 0.99, 95% CI 0.98–1.00, p = 0.213) nor D. repens (OR 1.01, 95% CI 0.99–1.01, p = 0.094) showed a significant correlation with precipitation.”
    Quote in the paperNot a substantial claim
  • Findingown data

    GDD showed a non-significant positive relationship with the prevalence of D. repens (OR 1.25, 95% CI 0.83-1.95, p = 0.291).

    “The GDD showed a significant positive association with the prevalence of D. immitis (OR 2.38, 95% CI 1.43–4.15, p = 0.001) and a non-significant positive relationship with that of D. repens (OR 1.25, 95% CI 0.83–1.95, p = 0.291).”
    • Also stated in: § Results · plain
      “It showed a significant positive association with the prevalence of D. immitis (OR 2.38, 95% CI 1.43–4.15, p = 0.001) and a non-significant positive relationship with that of D. repens (OR 1.25, 95% CI 0.83–1.95, p = 0.291).”
    Quote in the paperNot a substantial claim
  • Findingown data

    GDD showed a significant positive association with the prevalence of D. immitis (OR 2.38, 95% CI 1.43-4.15, p = 0.001).

    “The GDD showed a significant positive association with the prevalence of D. immitis (OR 2.38, 95% CI 1.43–4.15, p = 0.001) and a non-significant positive relationship with that of D. repens (OR 1.25, 95% CI 0.83–1.95, p = 0.291).”
    • Also stated in: § Results · plain
      “It showed a significant positive association with the prevalence of D. immitis (OR 2.38, 95% CI 1.43–4.15, p = 0.001) and a non-significant positive relationship with that of D. repens (OR 1.25, 95% CI 0.83–1.95, p = 0.291).”
    Quote in the paperSubstantial claim
  • Findingown data

    Precipitation did not show a significant correlation with the prevalence of D. repens (OR 1.01, 95% CI 0.99-1.01, p = 0.094).

    “The prevalence of neither D. immitis (OR 0.99, 95% CI 0.98–1.00, p = 0.213) nor D. repens (OR 1.01, 95% CI 0.99–1.01, p = 0.094) showed a significant correlation with precipitation.”
    • Also stated in: § Results · plain
      “The prevalence of neither D. immitis (OR 0.99, 95% CI 0.98–1.00, p = 0.213) nor D. repens (OR 1.01, 95% CI 0.99–1.01, p = 0.094) showed a significant correlation with precipitation.”
    Quote in the paperNot a substantial claim
  • May combine two claims. 4
  • Classified as probably not a substantial claim. 1
  • May combine two claims.

    Findingown data

    The prevalence of D. repens was 49/344 (14.2%), with infected dogs in 35 settlements of 16 counties.

    “The prevalence of D. repens was slightly higher (49/344, 14.2%); the infected dogs lived in 35 settlements of 16 counties (Fig. 1).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    The total number of dogs with heartworms was 39 (11.3%), living in 34 settlements of 12 counties.

    “The total number of animals with heartworms was 39 (11.3%): these dogs lived in 34 settlements of 12 counties.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    Both dirofilarioses are endemic in dogs in Hungary.

    “The results confirmed that both dirofilarioses are endemic in dogs and the eastern areas of the country are hyperendemic for heartworm disease.”
    • Also stated in: § Conclusions · plain
      “Both dirofilarioses are endemic in Hungary, and heartworm disease is more prevalent in the eastern areas of the country.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationreasoning

    The risk period for Dirofilaria transmission is seasonal in Hungary, with peaks in the summer.

    “The risk period for Dirofilaria transmission is seasonal in Hungary, with peaks in the summer, when the temperature is especially sufficient to facilitate the extrinsic incubation of Dirofilaria in vectors.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    In each PCR reaction set, a positive control (DNA from adult nematodes) and a no-DNA sample were included.

    “In each reaction set, a positive control (DNA extracted from adult nematodes) and a sample with no DNA were included.”
    Quote in the paperNot a substantial claim
5 of 5
  • The authors state this as an assumption.

    More D. immitis-infected local dogs facilitated the spreading of this nematode species in eastern Hungary than in other parts of the country.

    “We assume that more D. immitis-infected local dogs facilitated the spreading of this nematode species there than in the other part of the country.”
1 of 1

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • In Hungary, the first autochthonous case was detected in 2009, and studies showed low-moderate prevalence between 0.36 and 8.1%, co-infections with D. repens (3.2%), and high prevalence (51%) in Szeged.

    “In Hungary, where the first autochthonous case was detected in 2009 [109], the number of epidemiological studies has increased considerably. There are studies that showed low-moderate prevalence between 0.36 and 8.1% [110,111,112,113] and co-infections with D. repens (3.2%) [111], while a high prevalence (51%) was reported in Szeged, a city close to Serbia and Romania [114].”
  • In Hungary, prevalence of 3.7% in red foxes and 7.4% in golden jackals was reported.

    “In Hungary, a prevalence of 3.7% in red foxes and 7.4% in golden jackals was reported [112].”
  • No apparent correlation with FeLV and FIV infection was noted in a study of 2011.

    “Contrary to this study, no apparent correlation with FeLV and FIV infection was noted in a study of 2011 [8,20,34].”
  • In the last decade, epidemiological and seroepidemiological studies and clinical reporting have shown that dirofilariasis has been introduced into the countries of the Balkans peninsula.

    “In addition, in the last decade, different epidemiological and seroepidemiological studies, alongside clinical reporting, have shown that dirofilariasis has been introduced into the countries of the Balkans peninsula (1, 3, 4, 11, 19).”
  • Dirofilariasis is on the rise in the European population of dogs and humans.

    “Dirofilariasis is on the rise in the European population of dogs and humans (1, 3, 11, 12).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Range is described as both growing degree days and lifecycles

    Minor

    The abstract identifies 3.73-7.57 as the number of yearly growing degree days, whereas the Results identify the same range as the number of GDD-based parasite lifecycles. Growing degree days and lifecycles are different quantities.

1 of 1

Cites

Flagged first, then by citations

3 of the 49 references couldn’t be matched to a known paper.

Research works printed but not linked: 5

  1. Fok É, Kiss G, Majoros G, Jacsó O, Farkas R, Gyurkovszky M (2007) Preliminary results of an epidemiological survey on dirofilariosis of dogs and cats in Hungary. In: Genchi C, Rinaldi L, Cringoli G (eds) Dirofilaria immitis and D. repens in dog and cat and human infections. Roland Editore, Napoli, pp 194–196
  2. Fok É, Szabó Z, Farkas R (1998) The first autochthonous case of a dog infected with Dirofilaria repens in Hungary. Kisállatorvoslás 4:218–219 (in Hungarian)
  3. Jacsó O (2014) Distribution of Dirofilaria spp. in Hungary and their veterinary importance, the experience of the treatment. Dissertation. University of Veterinary Medicine, Budapest (in Hungarian)
  4. Kotlán A (1951) On a new case of human filarioidosis in Hungary. Acta Vet Acad Sci Hung 1:69–79
  5. Vörös K, Kiss G, Baska F, Bagdi N, Széll Z (2000) Heartworm disease in dogs. Review article and case report. Magy Allatorv Lapja 122:106–108 (in Hungarian)

Cited by

Sorted by citations

Authors
Farkas, R., Mag, V., Gyurkovszky, M., Takács, N., Vörös, K., & Solymosi, N.
Affiliations
University of Veterinary Medicine (HU)
Corresponding author
Farkas, Róbert
Venue
Parasitology Research
Published
2019-11-21
Volume
119
Issue
1
Pages
129-135
ISSN
  • 0044-3255 (ISSN-L)
  • 0932-0113
  • 1432-1955
OpenAlex
W2989794391
Cited by
55
References
49
Citations by year
2026: 9 · 2025: 4 · 2024: 4 · 2023: 6 · 2022: 13 · 2021: 13 · 2020: 5 · 2018: 1
FWCI
5.94
Type
journal article
Language
en
Open access
Locations
  • Parasitology Research (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
  • Health Sciences › Veterinary › Small Animals › Helminth infection and control
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Research on Leishmaniasis Studies
Keywords
canine dirofilariasis, Dirofilaria immitis, Dirofilaria repens, heartworm disease, prevalence, growing degree days, temperature, precipitation, co-infection, Hungary, endemicity, mosquito-borne transmission, climate and disease transmission
MeSH terms
Animals, Dirofilaria immitis, Dirofilariasis, Dog Diseases, Dogs, Hungary, Culicidae, Prevalence, Polymerase Chain Reaction, Coinfection, Dirofilaria repens

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