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Cited by 16Parasitic Diseases Research and TreatmentHelminth infection and controlResearch on Leishmaniasis Studies

Stray dogs of Sofia (Bulgaria) could be an important reservoir of heartworm ( Dirofilaria immitis )

Open access
Stoyanova, H., Carretón, E., Montoya-Alonso, J. A.·2019·Helminthologia
DOI 10.2478/helm-2019-0033PMC PMC6818634
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Abstract

Summary: Dirofilaria immitis (heartworm) is a zoonotic and an emerging disease, expanding in Europe. In Bulgaria, the presence of the parasite has been described in many regions. However, canine heartworm has hardly been evaluated in the capital of the country and, therefore, the aim of this study was to evaluate the prevalence and distribution of canine heartworm in Sofia. Eighty stray dogs from the city of Sofia and the metropolitan area were analysed for circulating D. immitis antigens. The prevalence was 31.25 %, being 34.7 % in the metropolitan area and 25.8 % in the city of Sofia. The current results are among the highest reported in the country. This could be due to the lack of prophylactic measures against infection in these dogs, but also to the spread of D. immitis into non-endemic countries. Stray dogs may act as an important reservoir of heartworm being a risk for client-owned animals and for the development of pulmonary dirofilariosis in inhabitants. The results show the need to establish further epidemiological studies and prophylactic campaigns for stray and client-owned animals, as well as to create awareness campaigns about the severity and importance of this disease for both animals and humans.

AI snapshot

Written from the paper’s full text.

TL;DR

In 80 stray dogs from Sofia and its metropolitan area, circulating Dirofilaria immitis antigen prevalence was 31.25%, with higher prevalence in older dogs and in the metropolitan area. The authors conclude stray dogs may be an important heartworm reservoir and call for broader epidemiological studies and prophylactic/awareness campaigns.

Key findings

  • Overall D. immitis antigen prevalence was 31.25%; it was 34.7% in the metropolitan area versus 25.8% in the city of Sofia, a non-significant difference.
  • Prevalence increased with age: 42.3% in dogs aged 10–19 years, 37.9% in dogs aged 5–9 years, and 12% in dogs aged 1–4 years (p<0.05). Positive dogs ranged from 3 to 19 years, with a mean age of 8.7 years.
  • Male dogs had 36.4% prevalence versus 25% in females, and mixed-breed dogs had 33.3% versus 25% in purebred dogs; neither difference was statistically significant.
  • The authors state that stray dogs may act as an important reservoir for heartworm, increasing risk to client-owned animals and humans, and that control/prophylactic measures are lacking in Sofia.

Methods

  • The study included 80 stray dogs from Sofia and its metropolitan area, captured between December 2017 and February 2018 during routine neutering campaigns; inclusion criteria were dogs over 7 months of age that had not been treated with macrocyclic lactones.
  • Blood samples were collected from the cephalic vein and tested for circulating D. immitis antigens using a commercial immunochromatographic test kit (Uranotest Dirofilaria®, Urano Vet SL, Barcelona, Spain).
  • Data were analyzed with SPSS Base 25.0; descriptive proportions were calculated and chi-square tests were used to compare proportions, with significance set at p<0.05.

Limitations

  • The paper states the sample size was small and the results cannot be considered definitive, though they are indicative of widespread parasite presence; it also notes that microfilariae were not evaluated in the studied dogs.
  • Evident from the text: sampling was limited to stray dogs captured for neutering between December 2017 and February 2018, so findings may not generalize to client-owned dogs or to other seasons.

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

Integrity signals

Registry

Crossref · 10.2478/helm-2019-0033

Cites

16 of 16 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 26 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The prevalence of D. immitis in stray dogs from the city of Sofia was 25.8%.

    “The prevalence was 31.25 %, being 34.7 % in the metropolitan area and 25.8 % in the city of Sofia.”
    • Also stated in: § Results · plain
      “The prevalence was higher in the metropolitan area of Sofia (34.7 %) than in the city of Sofia (25.8 %), although the differences were not statistically significant.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The commercial immunochromatographic test kit used accurately detects circulating D. immitis antigens in dogs.
    • Rests on an assumption: The 80 stray dogs sampled are representative of the stray dog population in Sofia and its metropolitan area.
  • Findingown data

    The prevalence of D. immitis in stray dogs from the metropolitan area of Sofia was 34.7%.

    “The prevalence was 31.25 %, being 34.7 % in the metropolitan area and 25.8 % in the city of Sofia.”
    • Also stated in: § Results · plain
      “The prevalence was higher in the metropolitan area of Sofia (34.7 %) than in the city of Sofia (25.8 %), although the differences were not statistically significant.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The commercial immunochromatographic test kit used accurately detects circulating D. immitis antigens in dogs.
    • Rests on an assumption: The 80 stray dogs sampled are representative of the stray dog population in Sofia and its metropolitan area.
  • Findingown data

    The prevalence of D. immitis in the studied stray dog population from Sofia and its metropolitan area was 31.25%.

    “The prevalence of D. immitis in the canine population in the studied area was 31.25 %.”
    • Also stated in: § Abstract · plain
      “The prevalence was 31.25 %, being 34.7 % in the metropolitan area and 25.8 % in the city of Sofia.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The commercial immunochromatographic test kit used accurately detects circulating D. immitis antigens in dogs.
    • Rests on an assumption: The 80 stray dogs sampled are representative of the stray dog population in Sofia and its metropolitan area.
  • Interpretationown data

    The current results are among the highest reported in Bulgaria.

    “The current results are among the highest reported in the country.”
    • Also stated in: § Discussion · plain
      “the current results reported an increase in the prevalence of heartworm infections in the country.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Georgieva et al., 2001

      Not checked in the free run.

    • cites Kirkova et al., 2007

      Not checked in the free run.

    • cites Radev et al., 2016

      Not checked in the free run.

  • Interpretationreasoning

    The current results indicate an increase in the prevalence of heartworm infections in Bulgaria compared to previous studies.

    “According to previous research, which reported prevalences from 7.4 % to 9.2 % in client-owned dogs in different regions of Bulgaria (Georgieva et al., 2001; Kirkova et al., 2007) and from 10 % to 15 % in stray dogs (Georgieva et al., 1992; 2001; Radev et al., 2016), the current results reported an increase in the prevalence of heartworm infections in the country.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Georgieva et al., 2001

      Not checked in the free run.

    • cites Kirkova et al., 2007

      Not checked in the free run.

    • cites Radev et al., 2016

      Not checked in the free run.

  • May combine two claims. 11
  • Classified as probably not a substantial claim. 7

  • May combine two claims.

    Findingown data

    The prevalence of D. immitis was higher in the metropolitan area (34.7%) than in the city of Sofia (25.8%), but the difference was not statistically significant.

    “The prevalence was higher in the metropolitan area of Sofia (34.7 %) than in the city of Sofia (25.8 %), although the differences were not statistically significant.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The commercial immunochromatographic test kit used accurately detects circulating D. immitis antigens in dogs.
    • Rests on an assumption: The 80 stray dogs sampled are representative of the stray dog population in Sofia and its metropolitan area.

  • May combine two claims.

    Findingown data

    Seroprevalence was highest in the oldest age group (42.3% in dogs 10-19 years) and lowest in the youngest (12% in dogs 1-4 years), with a statistically significant difference (p<0.05).

    “When age ranges were considered, the highest seroprevalences were found in the oldest part of the population, with 42.3 % of positives in dogs from 10 to 19 years old, followed by 37.9 % in dogs between 5 and 9 years. The lowest number of positive cases (12 %) was represented by dogs from 1 to 4 years (p<0.05).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The commercial immunochromatographic test kit used accurately detects circulating D. immitis antigens in dogs.
    • Rests on an assumption: The 80 stray dogs sampled are representative of the stray dog population in Sofia and its metropolitan area.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Dirofilaria immitis is a zoonotic parasite that causes pulmonary dirofilariosis in infected humans.

    “Furthermore, D. immitis is a zoonotic parasite that causes pulmonary dirofilariosis in infected humans (McCall et al., 2008; Simón et al., 2012).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites McCall et al., 2008

      Not checked in the free run.

    • cites Simón et al., 2012

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In Bulgaria, the presence of D. immitis has been described in many regions.

    “In Bulgaria, the presence of the parasite has been described in many regions.”
    • Also stated in: § Introduction · plain
      “Previous publications have shown presence of heartworm in Bulgaria.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Pantchev et al., 2015

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Several factors have been reported as possible causes of the spread of D. immitis, such as climate change, human activity, movement of microfilaremic dogs, introduction of new mosquito species, and infected wild animals as reservoirs.

    “Several factors have been reported as possible causes of this spread, such as climate change, the development of human activity for agricultural or urban uses in new areas, the growing movement of microfilaremic dogs throughout Europe or the introduction of new species of mosquitoes able to act as vectors. Also, infected wild animals can be reservoirs of the disease (Morchón et al., 2012; Simón et”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Morchón et al., 2012

      Not checked in the free run.

    • cites Simón et al., 2012

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Sofia, the average annual temperature of the urban area is 0.5°C higher than that of the peripheral area; in winter, the temperature in the center is 1°-1.5° higher than that of rural regions.

    “In Sofia, the average annual temperature of the urban area is 0.5°C higher than that of the peripheral area; moreover, in winter the temperature in the center of the capital is 1° – 1.5° higher than that of the rural regions (Kovachev, 2005).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Kovachev, 2005

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Previous studies in Bulgaria reported prevalences from 7.4% to 9.2% in client-owned dogs and from 10% to 15% in stray dogs.

    “According to previous research, which reported prevalences from 7.4 % to 9.2 % in client-owned dogs in different regions of Bulgaria (Georgieva et al., 2001; Kirkova et al., 2007) and from 10 % to 15 % in stray dogs (Georgieva et al., 1992; 2001; Radev et al., 2016)”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites Georgieva et al., 2001

      Not checked in the free run.

    • cites Kirkova et al., 2007

      Not checked in the free run.

    • cites Radev et al., 2016

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationcitation

    These results are consistent with studies reporting an increasing prevalence of D. immitis in Europe.

    “These results are consistent with studies that reported an increasing prevalence of D. immitis in Europe (Genchi et al., 2009; Morchón et al., 2012).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites Genchi et al., 2009

      Not checked in the free run.

    • cites Morchón et al., 2012

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Stray dogs in Sofia may act as an important reservoir for heartworm, increasing the risk of infection of client-owned animals and humans living in the city.

    “Stray dogs may act as an important reservoir of heartworm being a risk for client-owned animals and for the development of pulmonary dirofilariosis in inhabitants.”
    • Also stated in: § Discussion · hedged
      “so these stray dogs may act as an important reservoir for heartworm, increasing the risk of infection of client-owned animals and humans living in the city.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The 80 stray dogs sampled are representative of the stray dog population in Sofia and its metropolitan area.

  • May combine two claims.

    Interpretationreasoning

    Heartworm infection was higher in older animals probably because they were constantly exposed to mosquitoes and not receiving prophylactic treatment.

    “Probably, for the same reason heartworm infection was higher in the group of older animals.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Stray dogs in Sofia were constantly exposed to mosquitoes.
    • Rests on an assumption: There are no established control and prophylactic measures aiming to prevent heartworm in Sofia.

  • Classified as probably not a substantial claim.

    Study design and conductown data

    The small sample size means the results cannot be determined as definitive.

    “Although the results of this work cannot be determined as definitive, given the small size of the sample studied”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationcitation

    Urban Heat Islands in Sofia retain heat and increase temperature inside the city, which indirectly influences the development of D. immitis larvae in mosquito vectors during colder months and enlarges the transmission season.

    “in the city of Sofia high levels of urbanization can cause the phenomenon called Urban Heat Islands (Gago et al., 2013; Yang et al., 2016) which retains heat and increase the temperature inside the city. This indirectly influences the development of D. immitis larvae in mosquito vectors during the colder months and thus enlarges the transmission season (Arnfield, 2003).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Gago et al., 2013

      Not checked in the free run.

    • cites Yang et al., 2016

      Not checked in the free run.

    • cites Arnfield, 2003

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The disease has also been observed and studied in wild carnivores, with high prevalences in foxes and jackals.

    “The disease has also been observed and studied in wild carnivores, being described high prevalences in foxes and jackals (Kirkova et al., 2007; Mirchev et al., 2013; Panayotova-Pencheva et al., 2016).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites Kirkova et al., 2007

      Not checked in the free run.

    • cites Mirchev et al., 2013

      Not checked in the free run.

    • cites Panayotova-Pencheva et al., 2016

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    The abundant vegetation and water reservoirs in Sofia and its metropolitan area may offer a perfect environment for reproduction and proliferation of mosquito vectors, which could favor the spread of D. immitis infection.

    “The abundant vegetation and water reservoirs (green parks, artificial lakes and water ponds) present in the city of Sofia and in the metropolitan area may offer a perfect environment for reproduction and proliferation of the mosquito vectors which could favor the spread of the infection”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Premisenone given

    There is a lack of studies on heartworm in client-owned pets in Sofia.

    “there is a lack of studies on heartworm in client-owned pets in Sofia”
    Quote in the paperNot a substantial claim
15 of 15

  • The paper relies on this without support.

    Stray dogs in Sofia were constantly exposed to mosquitoes.

    “all dogs were constantly exposed to mosquitoes and not receiving any prophylactic treatment.”

  • The paper relies on this without support.

    There are no established control and prophylactic measures aiming to prevent heartworm in Sofia.

    “there are no established control and prophylactic measures aiming to prevent the presence of different diseases, including heartworm.”

  • The paper relies on this without support.

    The commercial immunochromatographic test kit used accurately detects circulating D. immitis antigens in dogs.

    “all the dogs were tested for circulating D. immitis antigens using a commercial immunochromatographic test kit (Uranotest Dirofilaria®, Urano Vet SL, Barcelona, Spain). The tests were performed according to the manufacturer’s instructions.”

  • The paper relies on this without support.

    The 80 stray dogs sampled are representative of the stray dog population in Sofia and its metropolitan area.

    “The present study included 80 stray dogs from different parts of the city of Sofia and its metropolitan area.”
4 of 4

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?

  • Several studies have shown prevalence of D. immitis antigens between 3-44.4% in red foxes and 4.4-58.7% in golden jackals, with isolated cases detected by necropsy.

    “In addition, several studies have shown a prevalence of D. immitis antigens between 3–44.4% in red foxes, and 4.4–58.7% in golden jackals; furthermore, isolated cases of infected red foxes and golden jackals were detected by necropsy [83,89,144].”

    From What has happened to heartworm disease in Europe in the last 10 years? (2022) · cites this paper as [89]

  • High numbers of stray dogs in some countries act as reservoirs for Dirofilaria parasites.

    “Another reason is the continuously high number of stray dogs in some countries, which are not subject to regular treatment and act as reservoirs for the parasites, e.g. countries with many stray dogs, such as Romania or Bulgaria continue to regularly report Dirofilaria spp. cases [74–76].”

    From Vectors, host range, and spatial distribution of Dirofilaria immitis and D. repens in Europe: a systematic review (2025) · cites this paper as [76]

Cites

Flagged first, then by citations

Research works printed but not linked: 4

  1. Georgieva, D., Kirkova, Z., Ivanov, A. (2001): A study on the incidence and diagnostics of dirofilariosis (heartworm disease) in carnivores. Bulg. J. Vet. Med., 4(4): 231–236
  2. Kirkova, Z., Ivanov, A., Georgieva, D. (2007): Dirofilariosis In Dogs And Wild Carnivores In Bulgaria. In: Genchi, C., Rinaldi, L., Cringoli, G. (Eds) Dirofilaria immitis and D. repens in dog and cat and human infections. Naples, Italy: Rolando Editore, pp. 204
  3. Kostadinov, M. (2007): Dirofilariosis among dogs in a small animal practice in the Plovdiv region, Bulgaria. In: Genchi, C., Rinaldi, L., Cringoli, G. (Eds) Dirofilaria immitis and D. repens in dog and cat and human infections. Naples, Italy: Rolando Editore, pp. 205
  4. Mirchev, R., Trifonova, A., Panayotova-Pencheva, M.S. (2013): Dirofilaria immitis in foxes (Vulpes Vulpes, LINNAEUS, 1758) in different areas from Bulgaria. Science & Technologies, 3(5): 38 – 42 (In Bulgarian, English summary)

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Authors
Stoyanova, H., Carretón, E., & Montoya-Alonso, J. A.
Affiliations
  • Ashleigh Veterinary Centre, M16 0DE- Manchester , Manchester , United Kingdom
  • Universidad de Las Palmas de Gran Canaria (ES)
Corresponding author
Carretón, E.
ORCID
Venue
Helminthologia
Publisher
Walter de Gruyter GmbH
Published
2019-11-05
Volume
56
Issue
4
Pages
329-333
ISSN
  • 0440-6605 (ISSN-L)
  • 1336-9083
DOI
10.2478/helm-2019-0033
PMC
PMC6818634
OpenAlex
W2986284690
Cited by
16
References
16
Citations by year
2026: 1 · 2025: 2 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 3 · 2020: 4 · 2019: 1 · 2018: 1
FWCI
1.73
Type
journal article
Language
en
Open access
Licence
Locations
  • Helminthologia (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Acceda (Universidad de Las Palmas de Gran Canaria) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
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
Dirofilaria immitis, canine heartworm disease, stray dogs, reservoir hosts, prevalence, circulating antigens, zoonoses, Sofia, Bulgaria, prophylaxis

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