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

Dirofilaria infections in dogs in different areas of Greece

Open access
Diakou, Anastasia, Kapantaidakis, Emmanouil, Tamvakis, Androniki, Giannakis, Vassilios, Strus, Nina·2016·Parasites & Vectors

Abstract

BACKGROUND: The nematodes Dirofilaria immitis and D. repens are enzootic in Greece. In the light of evidence of dirofilariosis spreading to new areas around the world, the aim of the present study was to update and enrich the current knowledge on the prevalence of Dirofilaria infections in dogs in Greece, to assess the risk factors of heartworm infection, and to initiate the drawing of the epizootiological map of canine dirofilariosis, investigating Dirofilaria infections in five locations along the north-south axis of the country, i.e. municipalities of Thessaloniki, Larissa, Achaia, Attica and Heraklion, associated with the five largest urban centres of Greece. METHODS: Blood samples collected from 750 dogs in total, were examined by the modified Knott's method and by serology. A questionnaire including information about each examined dog was filled in and statistical analysis of the results was performed using the Chi-square test and a Binary Multiple Univariate Generalized Linear Model. RESULTS: In total, 31 (4.1 %) out of 750 examined animals were found positive for D. immitis by any of the tests applied (Knott's method and serological examination). Moreover, microfilariae of D. repens and Acanthocheilonema reconditum were detected by the Knott's method in 17 (2.3 %) and 10 (1.3 %) of the animals, respectively. At the municipality level, the prevalence of infection was 14, 7, 5.3, 0.7 and 0 % for D. immitis, 1, 2, 8.7, 0.3 and 0 % for D. repens, and 0, 3, 2.7, 0.7 and 1 % for A. reconditum in Thessaloniki, Larissa, Achaia, Attica and Heraklion, respectively. In addition, in three dogs (one each in Thessaloniki, Achaia and Attica) mixed D. immitis - D. repens infections were detected by the Knott's method. The area of the country, dog's usage and age were determined as risk factors for heartworm infection. CONCLUSIONS: Northern areas of Greece have higher Dirofilaria prevalence and the prevalence in a western province (Achaia) is recorded for the first time. The mosquito population dynamics recorded in the past is likely to play an important role in the distribution of Dirofilaria infections in Greece, and needs further investigation. Similarly, the role of wild reservoirs of filarial parasites in different areas needs to be clarified. Promotion by veterinarians of preventive treatment and compliance by pet owners is essential in all parts of Greece, regardless of the recorded prevalence of infection.

AI snapshot

Written from the paper’s full text.

TL;DR

A cross-sectional survey of 750 owned dogs in five Greek municipalities found canine Dirofilaria infections to be more prevalent in northern and western areas than in southern areas. Area of residence, dog usage, and age were identified as risk factors for D. immitis infection.

Key findings

  • Overall, 31/750 dogs (4.1%) were positive for D. immitis by at least one method; municipality prevalence was 14% in Thessaloniki, 7% in Larissa, 5.3% in Achaia, 0.7% in Attica, and 0% in Heraklion.
  • Modified Knott’s method detected D. immitis microfilariae in 19/750 (2.5%), D. repens in 17/750 (2.3%), and Acanthocheilonema reconditum in 10/750 (1.3%); mixed D. immitis–D. repens infections were found in 3 dogs.
  • Serology detected D. immitis antigen in 28/750 (3.7%); 9 antigen-positive dogs had no microfilariae by Knott’s, and 3 Knott’s-positive dogs were seronegative.
  • Risk factors for D. immitis were municipality (χ² = 40.22, df = 4, P < 0.001), usage (χ² = 27.51, df = 7, P < 0.001), and age (χ² = 6.09, df = 2, P = 0.048); in the GLM, odds ratios were 26.8 for Thessaloniki vs Attica, 11.9 for Larissa vs Attica, 6.0 for Achaia vs Attica, 8.2 for guard vs pet, 5.3 for hunter vs pet, 6.4 for age 2–7 vs ≤2 years, and 9.5 for age >7 vs ≤2 years.

Methods

  • Cross-sectional study of 750 owned dogs older than 18 months, not receiving preventive treatment for dirofilariosis or macrocyclic lactones, sampled in Thessaloniki (n = 100), Larissa (n = 100), Achaia (n = 150), Attica (n = 300), and Heraklion (n = 100); a questionnaire recorded dog and environmental characteristics.
  • Blood samples were examined by the modified Knott’s method for microfilariae and by the commercial Pet Check® (IDEXX) serological kit for adult D. immitis antigen; microfilariae were identified morphologically.
  • Statistical analysis used the Chi-square test and a binary multiple univariate Generalized Linear Model in R 3.2.2, with factors significant at P < 0.2 in Chi-square testing entered into the GLM.

Limitations

  • The paper states that the recorded north–south distribution is contradictory to temperature- and DDU-based models and requires further attempts to explain; it also states that the role of mosquito population dynamics and wild reservoirs needs further investigation.
  • Evident from the text: the study examined owned dogs only, used a questionnaire, and relied on two diagnostic methods with known discordance (occult infections and false-negative serology); the authors note that cross-reactions with Angiostrongylus vasorum were considered minimal but possible.
  • The paper does not include a dedicated limitations section.

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

Integrity signals

Registry

Crossref · 10.1186/s13071-016-1797-6

Cites

41 of 41 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

    Mixed D. immitis and D. repens infections were detected by the Knott's method in 3 dogs overall (one each in Thessaloniki, Achaia and Attica).

    “In addition, mixed D. immitis and D. repens infections were revealed by the Knott’s method overall in 3 cases, i.e. in 1 (1 %), 1 (0.7 %), and 1 (0.3 %) of the dogs from Thessaloniki, Achaia and Attica, respectively.”
    Quote in the paperNot a substantial claim
  • Findingown data

    In the multiple GLM, dogs aged 2-7 years were 6.4 times more likely to be infected with D. immitis than dogs aged ≤2 years.

    “| 2–7 vs ≤ 2 | 6.4 | 1.6–43.0 | 0.019* |”
    Quote in the paperSubstantial claim
  • Findingown data

    The area of the country (municipality) was a risk factor for D. immitis infection in dogs.

    “the municipality where the dog lived, its usage and its age were the most important risk factors”
    Quote in the paperSubstantial claim
  • Findingown data

    In the multiple GLM, a dog living in Larissa was 11.9 times more likely to be infected with D. immitis than a dog living in Attica.

    “| Larisa vs Attica | 11.9 | 2.6–85.5 | 0.003** |”
    Quote in the paperSubstantial claim
  • Findingown data

    Dog's usage was a risk factor for D. immitis infection.

    “the municipality where the dog lived, its usage and its age were the most important risk factors”
    Quote in the paperSubstantial claim
  • May combine two claims. 12
  • The quote only partly states this claim. 1
  • Classified as probably not a substantial claim. 2
  • May combine two claims.

    Findingown data

    The prevalence of A. reconditum infection in dogs was 0% in Thessaloniki, 3% in Larissa, 2.7% in Achaia, 0.7% in Attica, and 1% in Heraklion.

    “At the municipality level, the prevalence of infection was 14, 7, 5.3, 0.7 and 0 % for D. immitis, 1, 2, 8.7, 0.3 and 0 % for D. repens, and 0, 3, 2.7, 0.7 and 1 % for A. reconditum in Thessaloniki, Larissa, Achaia, Attica and Heraklion, respectively.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    The prevalence of D. immitis infection (by any test) in dogs was 14% in Thessaloniki, 7% in Larissa, 5.3% in Achaia, 0.7% in Attica, and 0% in Heraklion.

    “At the municipality level, the prevalence of infection was 14, 7, 5.3, 0.7 and 0 % for D. immitis, 1, 2, 8.7, 0.3 and 0 % for D. repens, and 0, 3, 2.7, 0.7 and 1 % for A. reconditum in Thessaloniki, Larissa, Achaia, Attica and Heraklion, respectively.”
    Quote in the paperSubstantial claim
  • The quote only partly states this claim.

    Findingown data

    Microfilariae of Acanthocheilonema reconditum were detected by the modified Knott's method in 10 (1.3 %) of the 750 dogs.

    “Moreover, Acanthocheilonama reconditum microfilariae were found in 10 (1.3 %) of the dogs in total”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    The prevalence of D. repens infection in dogs was 1% in Thessaloniki, 2% in Larissa, 8.7% in Achaia, 0.3% in Attica, and 0% in Heraklion.

    “At the municipality level, the prevalence of infection was 14, 7, 5.3, 0.7 and 0 % for D. immitis, 1, 2, 8.7, 0.3 and 0 % for D. repens, and 0, 3, 2.7, 0.7 and 1 % for A. reconditum in Thessaloniki, Larissa, Achaia, Attica and Heraklion, respectively.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Gender, breed, hair length, body size, living together with other animals, water collections and type of vegetation in the area were not associated with higher risk of D. immitis infection.

    “On the other hand, factors gender, breed, hair length, body size, living together with other animals, water collections and type of vegetation in the area were not associated with higher risk of infection.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning

    Age was an important risk factor for D. immitis infection, most likely related to the accumulation of transmission periods and opportunities for infection in hosts not under preventive treatment.

    “Age was also identified as an important risk factor, most likely related to the accumulation of transmission periods and, subsequently, opportunities for an infection to occur in hosts that are not under preventive treatment.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Various factors can lead to a false negative serological test, one of them being the antigen-antibody complex formation.

    “Various factors can lead to a false negative serological test [29, 33], one of them being the antigen-antibody complex formation, that in some cases occurs to such an extent that it does not leave enough antigen circulating to be detected by the serological tests [34].”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [29] Brianti E, Gaglio G, Napoli E, Giannetto S, Dantas-Torres F, Bain O, Otranto D. New insights into the ecology and biology of Acanthocheilonema reconditum (Grassi, 1889) causing canine subcutaneous filariosis. Parasitology. 2012;139:530–6. source

      Not checked in the free run.

    • cites [33] Drake J, Gruntmeir J, Merritt H, Allen L, Little SE. False negative antigen tests in dogs infected with heartworm and placed on macrocyclic lactone preventives. Parasit Vectors. 2015;8:68. source

      Not checked in the free run.

    • cites [34] Little SE, Raymond MR, Thomas JE, Gruntmeir J, Hostetler JA, Meinkoth JH, Blagburn BL. Heat treatment prior to testing allows detection of antigen of Dirofilaria immitis in feline serum. Parasit Vectors. 2014;7:1–4. source

      Not checked in the free run.

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

    Premisecitation

    In some similar studies, no risk factors for filarial infection could be identified.

    “However, in some similar studies, no risk factors for filarial infection could be identified [26, 37].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [26] Traversa D, Aste G, Milillo P, Capelli G, Pampurini F, Tunesi C, et al. Autochthonous foci of canine and feline infections by Dirofilaria immitis and Dirofilaria repens in central Italy. Vet Parasitol. 2010;169:128–32. source

      Not checked in the free run.

    • cites [37] Tasic A, Tasic-Otasevic S, Gabrielli S, Miladinovic-Tasic N, Ignjatovic A, Dordevic J, et al. Canine Dirofilaria infections in two uninvestigated areas of Serbia: epidemiological and genetic aspects. Vector Borne Zoonotic Dis. 2012;12:1031–5. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The distribution of A. reconditum infections reflects different epizootiological characteristics, as its prevalence did not follow the respective for Dirofilaria sp. and remained in relatively low levels in all areas (0-3 %).

    “The distribution of A. reconditum infections as found in the present study reflects the different epizootiological characteristics of this parasite, as its prevalence did not follow the respective for Dirofilaria sp. and remained in relatively low levels in all areas (0–3 %).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation

    Populations of Culex spp. in the region of Central Macedonia were 20 times higher than in the Peloponnese region and 31 times higher than in Attica region.

    “In particular, populations of Culex spp. in the region of Central Macedonia were found to be 20 times higher than in the Peloponnese region and even 31 times higher than in Attica region.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [40] Diakou A, Gewehr S, Kapantaidakis E, Mourelatos S. Can mosquito population dynamics predict Dirofilaria hyperendemic foci? E-SOVE 2014 the 19th Conference. 2014; Thessaloniki. p. 76.

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The situation of heartworm disease in Greece has remained quite similar in recent decades, with D. immitis and D. repens infections being more prevalent in the north compared to the rest of the country, while in western areas like Achaia there is an important prevalence of filarial infections.

    “The results of the present study suggest that the situation of heartworm disease in the country has remained quite similar in recent decades, with D. immitis and D. repens infections being more prevalent in the north compared to the rest of the country, while there is evidence, that in western areas like Achaia, there is an important prevalence of filarial infections.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The five selected municipalities (Thessaloniki, Larissa, Achaia, Attica, and Heraklion) are representative of the respective areas of Greece for the prevalence of Dirofilaria infections in dogs.
  • May combine two claims.

    Premisecitation

    Populations of jackals and wolves are widely distributed in the central and northern part of the country (jackals are also present in Peloponnese), but absent elsewhere.

    “As populations of jackals and wolves are widely distributed in the central and northern part of the country (jackals are also present in Peloponnese), but absent elsewhere [44, 45] the role of these species in the prevalence configuration of heartworm infections in Greece is worth investigating.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [44] Papageorgiou N, Vlachos C, Sfougaris A, Tsachaldis E. Status and diet of wolves in Greece. Act Theriol. 1994;39:411–6. source

      Not checked in the free run.

    • cites [45] Chapron G, Kaczensky P, Linnell JD, von Arx M, Huber D, Andrén H, López-Bao JV, Adamec M, Álvares F, Anders O. Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science. 2014;346:1517–9. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    D. repens infection was found in higher prevalence in northern and western areas of Greece, while in southern areas the occurrence of the infection was very low or non-existent.

    “Similarly, D. repens infection was also found in higher prevalence in northern and western areas of the country, while in southern areas the occurrence of the infection was very low or even non-existent.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The five selected municipalities (Thessaloniki, Larissa, Achaia, Attica, and Heraklion) are representative of the respective areas of Greece for the prevalence of Dirofilaria infections in dogs.
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Rice field abundance was acknowledged as one of the possible elements contributing to the higher Dirofilaria infection rates in certain areas of Portugal.

    “Rice field abundance was acknowledged as one of the possible elements contributing to the higher Dirofilaria infection rates in certain areas of Portugal [24].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [24] Alho AM, Landum M, Ferreira C, Meireles J, Goncalves L, de Carvalho LM, Belo S. Prevalence and seasonal variations of canine dirofilariosis in Portugal. Vet Parasitol. 2014;206:99–105. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Guard and hunting dogs were at higher risk of D. immitis infection, probably as a consequence of the outdoor lifestyle and higher exposure to mosquito bites.

    “The usage of the animal was also very important, thus, guard and hunting dogs were at higher risk of infection, probably as a consequence of the outdoor lifestyle and higher exposure to mosquito bites.”
    Quote in the paperSubstantial claim
15 of 15
  • The paper relies on this without support.

    The five selected municipalities (Thessaloniki, Larissa, Achaia, Attica, and Heraklion) are representative of the respective areas of Greece for the prevalence of Dirofilaria infections in dogs.

    “In order to form a basic and representative picture of the prevalence of filarial infection in different areas of Greece, five locations, distributed along the north-south axis of the country, associated with the five biggest urban centres were selected.”
  • The paper relies on this without support.

    Filarial infections had never been investigated in Achaia before this study.

    “The prevalence found in Achaia is a new record, in the sense that, to date, filarial infections have never been investigated in this area of Greece (western Greece).”
2 of 2

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 Greece, there has been an increase in the number of areas analysed in recent years, with reported canine heartworm prevalences in urban cities of Thessaloniki, Larissa, Achaia, Attica, and Heraklion of 14, 7, 5.3, 0.7, and 0%, respectively, and 0.5% on the islands of Skiathos, Tinos, Ios, and Santorini.

    “In Greece, there has been an increase in the number of areas analysed in the recent years [4]. The reported prevalence in the urban cities of Thessaloniki, Larissa, Achaia, Attica, and Heraklion were 14, 7, 5.3, 0.7, and 0%, respectively. On the islands of Skiathos, Tinos, Ios, and Santorini, the reported prevalence was 0.5%.”
  • In Greece, the first feline study was carried out in the north of the country, reporting a prevalence of 3%.

    “In Greece, the first feline study was carried out in the north of the country, reporting a prevalence of 3% [93].”
  • The majority of previous studies on CVBDs in Greece focused on single species of pathogens and examined the situation in a restricted area and number of animals.

    “However, the majority of the fore-mentioned studies have been focused on single species of pathogens and examined the situation in a restricted area and number of animals.”
  • Many CVBDs have been reported in canine populations and in human populations in Greece.

    “According to relevant studies, many CVBDs have been reported in canine populations [18, 19], as well as in human populations in Greece [20–22].”
  • In Greece, the prevalence of D. immitis was 4.1% out of 750 dogs examined in 2016 and the highest prevalence could be found in northern Greece.

    “In Greece, the prevalence of D. immitis was 4.1% out of 750 dogs examined in 2016 and the highest prevalence could be found in northern Greece, where most of the dogs in the present study with a travel history to Greece had travelled (Diakou et al. 2016).”

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.

  • Attica heartworm prevalence differs between discussion and results

    Minor

    The discussion gives Attica's D. immitis prevalence as 0.6%, whereas Table 2 gives 0.7% for 2 positive dogs among 300 examined.

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 5

  1. Diakou A. Epidemiological study of dog parasitosis diagnosed by blood and serological examinations. Anima. 2000;8:9–17 (In Greek).
  2. Plevraki A, Savvas I, Papadopoulos B, Diakou A, Haralabidis S. Parasites of the dogs in an animal shelter in Ahlada (Heraklion) (In Greek). Stock Farm Develop. 1996;21:24–6.
  3. Diakou A. Angiostrongylus vasorum and angiostrongylosis in Greece. J Hell Vet Med Soc. 1995;46:51–6 (In Greek).
  4. Diakou A, Gewehr S, Kapantaidakis E, Mourelatos S. Can mosquito population dynamics predict Dirofilaria hyperendemic foci? E-SOVE 2014 the 19th Conference. 2014; Thessaloniki. p. 76.
  5. Tsochatzis DE. Development of analytical methods for the determination of residues of pesticides used in rice cultures: application for the assessment of their environmental implications, PhD Thesis, School of Chemical Engineering, Department of Chemistry. Thessaloniki: Aristotle University of Thessaloniki; 2012. p. 201.

Cited by

Sorted by citations

Authors
Diakou, A., Kapantaidakis, E., Tamvakis, A., Giannakis, V., & Strus, N.
Affiliations
Aristotle University of Thessaloniki (GR)
Venue
Parasites & Vectors
Published
2016-09-20
Volume
9
Issue
1
Pages
508-508
ISSN
1756-3305 (ISSN-L)
OpenAlex
W2523506607
Cited by
56
References
41
Citations by year
2026: 2 · 2025: 6 · 2024: 9 · 2023: 1 · 2022: 13 · 2021: 8 · 2020: 8 · 2019: 4 · 2018: 4 · 2017: 1
FWCI
2.77
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Parasites & Vectors (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Elanco Animal Health
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, Acanthocheilonema reconditum, heartworm infection, prevalence, risk factors, Greece, urban dogs, serology, Achaia, Thessaloniki
MeSH terms
Animals, Dirofilaria immitis, Dirofilariasis, Disease Reservoirs, Dog Diseases, Dogs, Female, Greece, Male, Culicidae, Risk Factors, Prevalence, Coinfection, Dirofilaria repens, Acanthocheilonema

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