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Cited by 22Parasitic Diseases Research and TreatmentResearch on Leishmaniasis StudiesHelminth infection and control

Seroepidemiological Study of Canine and Human Dirofilariasis in the Endemic Region of Northern Serbia

Open access
Savić, Sara, Stosic, Marina Zekic, Marcic, Doroteja, Hernández, Isabel, Potkonjak, Aleksandar, Otasevic, Suzana, Ruzic, Maja, Morchón, Rodrigo·2020·Frontiers in Veterinary Science
DOI 10.3389/fvets.2020.00571PMC PMC7550424
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Abstract

Dirofilariosis is a vector borne zoonotic diseases caused mainly by Dirofilaria immitis and Dirofilaria repens that affect dogs and humans all over the world. Serbia is considered as an endemic country to both forms of dirofilariosis although the majority of the population is concentrated in the north of the country. The aims of this study was to show the prevalence of D. immitis and D. repens in dogs and the seroprevalence in humans compared to last studies in the Northern Serbia. We analyzed a 346 dog sera samples and 265 human samples. On the one hand, dogs blood samples were analyzed by modified Knott to check whether there were Dirofilaria spp. microfilariae and serum samples were checked by a commercial D. immitis antigen test. On the other hand, human serum samples were analyzed using a non-commercial ELISA to detect the specific anti-D. immitis, anti-D. repens and anti-Wolbachia IgG antibodies, and confirmed by Western blot. The overall prevalence for Diroflilaria spp. in dogs was 29,19%. The overall prevalence for D. immitis was 26.30%. The percentage of D. immitis and D. repens microfilaremic dogs was 25.72%, and 1.45% recpectively, and for D. immitis/D. repens microfilaremic co-infections was 1.45%. The orevall seroprevalence for Diroflilaria spp. in humans was 3.77%. The overall seroprevalence for D. immitis was 1.51%, for D. repens 1.13%, and D. immitis/D. repens co-infections was 1.13%. The results indicate that D. immitis and D. repens are present in dogs and humans in the province of Vojvodina, in the Northern part of Serbia. It is most probably associated with the presence of many rivers, climate, presence of mosquitoes, so there's a real Public Health risk.

AI snapshot

Written from the paper’s full text.

TL;DR

In Northern Serbia (Vojvodina), this seroepidemiological study found Dirofilaria spp. in 29.19% of dogs and human seroprevalence of 3.77%, indicating exposure to both D. immitis and D. repens. The authors conclude that D. immitis and D. repens are present in dogs and humans in Vojvodina and that there is a real public health risk.

Key findings

  • In 346 dog sera, overall Dirofilaria spp. prevalence was 29.19%; D. immitis prevalence was 26.30%, D. immitis microfilaremia was 25.72%, D. repens microfilaremia was 1.45%, and D. immitis/D. repens co-infection microfilaremia was 1.45%.
  • In 265 human samples, overall Dirofilaria spp. seroprevalence was 3.77%; D. immitis seroprevalence was 1.51%, D. repens was 1.13%, and D. immitis/D. repens co-infection was 1.13%.
  • The paper reports significant sex differences in dogs for D. immitis (higher in males) and D. repens (higher in females) (p < 0.05), and significant age differences in humans for D. immitis, D. repens, and co-infections (p < 0.05).
  • Positive dog and human samples were geolocated near rivers, forest parks, green areas, and urban areas in northern Serbia.

Methods

  • Cross-sectional seroepidemiological study in Vojvodina, Northern Serbia, using 346 dog sera and 265 human sera collected during 2018–2019.
  • Dogs were tested by modified Knott’s method for Dirofilaria spp. microfilariae and by a commercial D. immitis antigen test; humans were tested by non-commercial ELISA for anti-D. immitis, anti-D. repens, and anti-Wolbachia IgG antibodies, with positive results confirmed by western blotting.
  • Analyses used descriptive proportions, Chi-square tests in SPSS Base 18.0 with significance at p < 0.05, and ArcGIS Pro for georeferencing positive samples.

Limitations

  • The paper does not explicitly state a limitations section.
  • Evident from the text: human samples came from patients with different symptoms rather than a general population sample, and the human sample was heavily skewed toward males (208/265, 78.49%) and those over 40 years (215/265, 81.13%).
  • Evident from the text: dog samples were obtained from veterinary clinics, and there is no commercial laboratory test for D. repens in dogs, so canine D. repens detection relied on Knott’s microfilaremia.

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

Integrity signals

Registry

Crossref · 10.3389/fvets.2020.00571

Cites

39 of 39 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 40 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The percentage of D. immitis/D. repens microfilaremia co-infections in dogs was 1.45%.

    “while D. immitis./D. repens microfilaremia co-infections were also 1.45%.”
    • Also stated in: § Results · plain
      “and 1.45% for D. immitis/D. repens microfilaremia co-infections (in all cases with a positive D. immitis antigen test).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The dog sera samples analyzed are representative of the dog population in Northern Serbia.
  • Findingown data

    The overall prevalence of D. immitis in dogs was 26.30%.

    “The overall prevalence for D. immitis was 26.30%.”
    • Also stated in: § Results · plain
      “The overall prevalence for D. immitis was 26.30%.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The dog sera samples analyzed are representative of the dog population in Northern Serbia.
  • Findingown data

    The percentage of D. immitis microfilaremia in dogs was 25.72%.

    “The percentages of D. immitis and D. repens microfilaremia in dogs were 25.72 and 1.45%, respectively”
    • Also stated in: § Results · plain
      “The percentage of D. immitis microfilaremia in dogs was 25.72% (in all cases with a positive D. immitis antigen test)”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The dog sera samples analyzed are representative of the dog population in Northern Serbia.
  • Findingown data

    The overall seroprevalence of Dirofilaria spp. in humans was 3.77%.

    “The overall seroprevalence for Dirofilaria spp. in humans was 3.77%.”
    • Also stated in: § Results · plain
      “The overall seroprevalence for Dirofilaria spp. in humans was 3.77%.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The human sera samples analyzed are representative of the human population in Northern Serbia.
  • Findingown data

    The percentage of D. repens microfilaremia in dogs was 1.45%.

    “The percentages of D. immitis and D. repens microfilaremia in dogs were 25.72 and 1.45%, respectively”
    • Also stated in: § Results · plain
      “1.45% for D. repens microfilaremia”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The dog sera samples analyzed are representative of the dog population in Northern Serbia.
  • May combine two claims. 9
  • Classified as probably not a substantial claim. 9

  • May combine two claims.

    Interpretationown data

    Both animals and infected people were geolocated in the immediate vicinity or in a relatively close environment of potential mosquito breeding areas, which poses a risk to those areas.

    “Both animals and infected people were geolocated in the immediate vicinity or in a relatively close environment of potential mosquito breeding areas, which poses a risk to those areas.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The GPS point of capture of infected dog and human samples reflects the location where infection was acquired.

  • May combine two claims.

    Interpretationcitation

    Several studies point to an increase in D. immitis infections and a decrease in D. repens infections in recent years, which is corroborated by results in this study.

    “Several studies point to an increase in D. immitis infections and a decrease of an infection with D. repens in recent years (21–23) which is corroborated by results in this study.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [21] Tasić, 2008, Survey of canine dirofilariasis in Vojvodina, Serbia, Parasitol Res. source

      Not checked in the free run.

    • cites [22] Spasojević-Kosić, 2012, Prevalence of dirofilariasis in pet dogs in Novi Sad, Contemp Agric

      Not checked in the free run.

    • cites [23] Spasojević-Kosić, 2016, Dirofilariasis and Angiostrongilosis in pet and hunting dogs in Novi Sad, Vojvodina, Serbia, Arhiv Vet Med. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In two regions of Vojvodina (Pancevo and Veliko Gradiste), previously reported seroprevalence was 22.9% for D. immitis and presence of D. repens microfilariae was 39.34%.

    “In two regions of Vojvodina (Pancevo and Veliko Gradiste), the previously reported seroprevalence was 22.9% for D. immitis and the presence of D. repens microfilariae was 39.34% (38).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [38] Tasić, 2012, Canine Dirofilaria infections in two uninvestigated areas of Serbia: epidemiological and genetic aspects, Vector Borne Zoonot Dis. source

      Not checked in the free run.

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

    Premisecitation

    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).”
    Quote in the paperNot a substantial claim0 of 5 sources checked
    • cites [1] Simón, 2012, Human and animal dirofilariasis: the emergence of a zoonotic mosaic, Clin Microbiol Rev. source

      Not checked in the free run.

    • cites [3] Capelli, 2018, Recent advances on Dirofilaria repens in dogs and humans in Europe, Parasit Vectors. source

      Not checked in the free run.

    • cites [4] Morchón, 2012, Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends, Front Physiol. source

      Not checked in the free run.

    • cites [11] Farkas, 2020, The current situation of canine dirofilariasis in Hungary, Parasitol Res. source

      Not checked in the free run.

    • cites [19] Ionică, 2017, Filarioid infections in wild carnivores: a multispecies survey in Romania, Parasit Vectors source

      Not checked in the free run.

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

    Premisecitation

    D. repens was found to circulate mostly in golden jackal and red fox populations.

    “Meanwhile, D. repens was found to circulate mostly in golden jackal and red fox populations (27).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [27] Potkonjak, 2020, Molecular survey of Dirofilaria species in stray dogs, red foxes and golden jackals from Vojvodina, Serbia, Comp Immunol Microbiol Infect Dis. source

      Not checked in the free run.

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

    Interpretationreasoning

    There could be a risk of D. immitis infection between the dog population and the wild canid population.

    “which could mean there is a risk of D. immitis infection between the dog population and the wild canid population.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Dirofilaria infections are prevalent in wild canids.

    “In addition, infections have also been found to be prevalent in wild canids (39)”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [39] Cirović, 2014, First records of Dirofilaria repens in wild canids from the region of central Balkan, Acta Vet Hung. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation

    The spatial distribution of positive cases has a clear association with different geo-environmental factors, humidity and temperature, the existence of irrigated areas, areas with abundant water, rivers in valleys protected from winds, and proximity to the coast, which are considered risk factors for the transmission of dirofilariasis.

    “The spatial distribution of positive cases has a clear association with different geo-environmental factors, humidity and temperature, the existence of irrigated areas, areas with abundant water, rivers in valleys protected from winds, and proximity to the coast, which are considered risk factors for the transmission of dirofilariasis (43).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [43] Simón, 2014, Geo-environmental model for the prediction of potential transmission risk of Dirofilaria in an area with dry climate and extensive irrigated crops. The case of Spain, Vet Parasitol. source

      Not checked in the free run.

    • Rests on an assumption: The GPS point of capture of infected dog and human samples reflects the location where infection was acquired.

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

    Premisecitation

    In Bulgaria and Croatia, studies report prevalence of D. immitis and D. repens in dogs of 8.1% and 11.1%, respectively, and co-infections of 3.2%.

    “In Bulgaria and Croatia, two neighboring countries, there are studies about the prevalence of D. immitis and D. repens in dogs (8.1 and 11.1%, respectively) and co-infections (3.2%) (11).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [11] Farkas, 2020, The current situation of canine dirofilariasis in Hungary, Parasitol Res. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    D. immitis and D. repens are present in dogs and humans in the province of Vojvodina, in the northern part of Serbia.

    “The results indicate that D. immitis and D. repens are present in dogs and humans in the province of Vojvodina, in the northern part of Serbia.”
    • Also stated in: § Discussion · hedged
      “In conclusion, the results indicate that D. immitis and D. repens are present in dogs and humans in the province of Vojvodina, in the northern part of Serbia.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The dog sera samples analyzed are representative of the dog population in Northern Serbia.
    • Rests on an assumption: The human sera samples analyzed are representative of the human population in Northern Serbia.

  • May combine two claims.

    Premisecitation

    Few human cases in Serbia have been reported to be caused by D. repens or have had specific antibodies found.

    “Few human cases have been reported to be caused by D. repens or have had specific antibodies found (25, 26).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [25] DŽamić, 2009, Human Dirofilaria repens infection in Serbia, J Helminthol. source

      Not checked in the free run.

    • cites [26] Tasić-Otašević, 2014, Seroreactivity to Dirofilaria antigens in people from different areas of Serbia, BMC Infect Dis. source

      Not checked in the free run.

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

    Premisecitation

    Other studies have reported seroprevalences of 9.7% against D. repens and 8.1% against D. immitis polyproteins specific antibodies, and 2.3% in individuals with specific antibodies to both species.

    “In addition, other studies have reported seroprevalences of 9.7% and 8.1% against D. repens and D. immitis polyproteins specific antibodies, respectively, and 2.3% in individuals with specific antibodies to both species (26).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Tasić-Otašević, 2014, Seroreactivity to Dirofilaria antigens in people from different areas of Serbia, BMC Infect Dis. source

      Not checked in the free run.

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

    Premisecitation

    In Croatia there have been human D. repens cases reported.

    “In addition, in Croatia there have been human D. repens cases reported (3).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] Capelli, 2018, Recent advances on Dirofilaria repens in dogs and humans in Europe, Parasit Vectors. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    All human samples positive by ELISA were also analyzed by western blot to confirm recognition of specific bands for D. immitis (17-22 kDa) and D. repens (43-70 kDa).

    “All samples that were positive with these kits were also analyzed by western blot to determine if they recognized the specific bands for D. immitis (17–22 kDa) and for D. repens (43–70 kDa).”
    Quote in the paperSubstantial claim

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

    Premisecitation

    Similar studies in Romania and Moldova have reported seroprevalences of 10.7% for D. immitis, 0.2% for D. repens, and 0.9% for both parasites.

    “Similar studies in neighboring countries such as Romania and Moldova have reported seroprevalences of 10.7% for D. immitis, 0.2% for D. repens, and 0.9% for both parasites (16).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [16] Ciuca, 2018, Seroepidemiological survey of human exposure to Dirofilaria spp. in Romania and Moldova, Acta Trop. source

      Not checked in the free run.

15 of 15

  • The paper relies on this without support.

    The dog sera samples analyzed are representative of the dog population in Northern Serbia.

    “346 dog sera samples (173 male and 173 female) were obtained from dogs analyzed by several veterinary clinics (Table 1)”

  • The paper relies on this without support.

    The human sera samples analyzed are representative of the human population in Northern Serbia.

    “265 human samples (208 male and 57 female) were provided to the research laboratory from different departments of clinical centers in Northern Serbia (Table 2).”

  • The paper relies on this without support.

    The GPS point of capture of infected dog and human samples reflects the location where infection was acquired.

    “All dog and human samples infected with D. immitis, D. repens, and co-infections were manually georeferenced by GPS at the point of capture.”
3 of 3

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?

  • Epidemiological studies from Serbia have shown increased canine heartworm prevalence, with ranges between 12.7 and 33.3% in the north, together with presence of some microfilaremic dogs.

    “However, epidemiological studies from Serbia have shown increased prevalence, with ranges between 12.7 and 33.3% in the north of the country, together with the presence of some microfilaremic dogs [7,68,69,70,71].”

    From What has happened to heartworm disease in Europe in the last 10 years? (2022) · cites this paper as [7]

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.

  • A female positive case contradicts the all-male statement

    Minor

    The results state that all positive human cases were male, but Table 2 records one positive female with a co-infection.

  • Male co-infection percentage is overstated

    Minor

    Table 2 reports 2 co-infections among 208 males as 1.44%, but 2/208 is 0.96%.

    Reported 1.44 · recomputed 0.961538

2 of 2

Cites

Flagged first, then by citations

Research works printed but not linked: 5

  1. Savić-Jevdenić, 2004, Brza dijagnostika dirofilarioze pasa u regionu Novog Sada, Vet Glasnik., 58, 693
  2. Spasojević-Kosić, 2012, Prevalence of dirofilariasis in pet dogs in Novi Sad, Contemp Agric, 61, 247
  3. Genchi, 2007, Guideline for the laboratory diagnosis of canine and feline Dirofilaria infections. In: Genchi C, Rinaldi L, Cringoli G, editors, 137
  4. Perera, 1994, Evaluation of a 22kDa Dirofilaria immitis antigen for the immunodiagnosis of human pulmonary dirofilariasis, Trop Med Parasitol., 45, 249
  5. Carretón, 2012, Chapter 1. Dirofilariasis cardiopulmonar canina, 1

Cited by

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Related

Authors
Savić, S., Stosic, M. Z., Marcic, D., Hernández, I., Potkonjak, A., Otasevic, S., Ruzic, M., & Morchón, R.
Affiliations
  • Scientific Veterinary Institute "Novi Sad" (RS)
  • Universidad de Salamanca (ES)
  • University of Novi Sad (RS)
Corresponding author
  • Savić, Sara
  • Morchón, Rodrigo
ORCID
Venue
Frontiers in Veterinary Science
Publisher
Frontiers Media SA
Published
2020-09-29
Volume
7
Pages
571-571
ISSN
2297-1769 (ISSN-L)
DOI
10.3389/fvets.2020.00571
PMC
PMC7550424
OpenAlex
W3090976071
Semantic Scholar
4f6c3a8dc953f691a8a6fa1b9a4958dc21d27958
Cited by
22
References
39
Citations by year
2026: 1 · 2025: 5 · 2024: 4 · 2023: 1 · 2022: 6 · 2021: 4 · 2020: 1
FWCI
0.39
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Veterinary Science (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Agencia de Desarrollo Económico
Topics
  • Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Research on Leishmaniasis Studies
  • Health Sciences › Veterinary › Small Animals › Helminth infection and control
Keywords
canine dirofilariasis, Dirofilaria immitis, Dirofilaria repens, seroprevalence, zoonoses, co-infection, microfilariae, Vojvodina, public health risk

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