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Cited by 31Parasitic Diseases Research and TreatmentHelminth infection and controlResearch on Leishmaniasis Studies

Survey of Dirofilaria immitis antigen and antibodies to Leishmania infantum and Toxoplasma gondii in cats from Madeira Island, Portugal

Open access
Neves, Michelle, Lopes, Ana Patrícia, Martins, Carolina, Fino, Raquel, Paixão, Cláudia, Damil, Liliana, Lima, Clara, Alho, Ana Margarida +3 more·2020·Parasites & Vectors
DOI 10.1186/s13071-020-3988-4PMC PMC7171917
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Abstract

Background: Dirofilaria immitis,Leishmania infantum and Toxoplasma gondii are zoonotic parasites which can affect domestic cats. Considering the lack of published data from the local feline population, this study aimed to assess infection with or exposure to these pathogens in cats from Madeira Island, Portugal. Methods: One hundred and forty-one domestic cats (77 males and 64 females; median age: 2 years) were sampled at a veterinary medical centre in Funchal, from September 2018 to January 2019. Serum samples were tested for D. immitis antigen, with an enzyme-linked immunosorbent assay kit, and for antibodies to Leishmania spp. or to T. gondii, with the direct agglutination test and the modified agglutination test, respectively. Results: Five cats (3.5%; 95% confidence interval, CI: 1.2–8.1) were positive to D. immitis; no cats were seropositive to Leishmania spp. (0%; 95% CI: 0–2.6%); and 43 cats (30.5%; 95% CI: 23.0–38.8%) were seropositive to T. gondii. Prevalence of the D. immitis antigen was significantly different between cats that received ectoparasiticides and those which did not (0 vs 12.2%;P = 0.009). Prevalence of antibodies to T. gondii was significantly different between juvenile and adult cats (12.8 vs 38.0%;P = 0.007). There were two cats concurrently positive to D. immitis and T. gondii, but no statistical association between these two dependent variables was found (P = 0.641). Conclusions: To our knowledge, this is the first report of the presence of parasites D. immitis and T. gondii in the feline population of Madeira Island. Knowledge on the epidemiological situation of these and other zoonotic pathogens should raise awareness, both at the veterinary medical and public health levels, and contribute to promoting prevention and control.

AI snapshot

Written from the paper’s full text.

TL;DR

In a cross-sectional survey of 141 domestic cats on Madeira Island, 3.5% were positive for *Dirofilaria immitis* antigen, 30.5% were seropositive for *Toxoplasma gondii*, and none were seropositive for *Leishmania* spp. This is reported as the first evidence of *D. immitis* and *T. gondii* in the feline population of Madeira.

Key findings

  • *D. immitis* antigen was detected in 5/141 cats (3.5%; 95% CI 1.2–8.1); prevalence was 0% in cats receiving ectoparasiticides versus 12.2% in those not receiving them (P = 0.009).
  • No cats were seropositive to *Leishmania* spp. (0%; 95% CI 0–2.6).
  • *T. gondii* antibodies were found in 43/141 cats (30.5%; 95% CI 23.0–38.8); 31/43 seropositive cats (72.1%) had a high titre (≥640), and prevalence was higher in adults than juveniles (38.0% vs 12.8%; P = 0.007).
  • Two cats were concurrently positive to *D. immitis* and *T. gondii*, with no statistical association between the two (P = 0.641); no significant differences were found for municipality, sex, breed, fur length, housing, clinical status, or macrocyclic lactones for either pathogen.

Methods

  • Cross-sectional convenience sample of 141 domestic cats (77 males, 64 females; median age 2 years; range 5 months–21 years) sampled at a veterinary medical centre in Funchal, Madeira, from September 2018 to January 2019; all cats were born on Madeira and had no travel history.
  • Serum was tested for *D. immitis* antigen with a commercial ELISA kit (PetChek Canine Heartworm Antigen Test), with positives retested; *Leishmania* spp. IgG antibodies were tested by direct agglutination test (cut-off titre 100), and *T. gondii* IgG antibodies by modified agglutination test (cut-off titre 20).
  • Exact binomial 95% CIs were calculated; chi-square and Fisher’s exact tests compared proportions, with P ≤ 0.05 considered significant; the sample corresponded to an absolute error of 8.25% assuming 50% prevalence and 95% confidence.

Limitations

  • Stated in the paper: *D. immitis* antigen tests detect antigen from live adult female or dying male/female heartworms, so a negative result does not rule out infection with only male, pre-adult, or very old adult worms; antibody tests may indicate exposure rather than active or persistent infection. The paper also notes that comparison of *T. gondii* prevalence with Lisbon data may be affected by different cut-offs (titre 20 vs 40).
  • Evident from the text: the study used convenience sampling at a single veterinary centre in Funchal and was cross-sectional, with no longitudinal follow-up.
  • Evident from the text: no cats were *Leishmania*-seropositive, so risk-factor analysis for that pathogen was not possible; treatment history for ectoparasiticides and macrocyclic lactones was recorded but not described as independently verified.

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

Integrity signals

Registry

Crossref · 10.1186/s13071-020-3988-4

Cites

Statistics

Nothing to recompute.

Claims the paper makes

0 of 25 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    All D. immitis antigen-positive cats (n = 5) did not receive ectoparasiticides.

    “All the D. immitis antigen-positive cats (n = 5) did not receive ectoparasiticides.”
    Quote in the paperNot a substantial claim
  • Findingown data

    The 30.5% T. gondii prevalence in cats from Madeira differs significantly from the 20.5% in cats from the Lisbon metropolitan area using the same serological test (χ2 = 2.154, df = 1, P = 0.031).

    “The 30.5% prevalence of antibodies to T. gondii found in the present study differs significantly (χ2 = 2.154, df = 1, P = 0.031) from the 20.5% found in domestic cats from the Lisbon metropolitan area, in mainland Portugal, using the same serological test [45].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [45] Esteves F, Aguiar D, Rosado J, Costa ML, de Sousa B, Antunes F, et al. Toxoplasma gondii prevalence in cats from Lisbon and in pigs from centre and south of Portugal. Vet Parasitol. 2014;200:8–12. source

      Not checked in the free run.

  • Findingown data

    Prevalence of D. immitis antigen was significantly different between cats that received ectoparasiticides and those which did not (0 vs 12.2%; P = 0.009).

    “Prevalence of the D. immitis antigen was significantly different between cats that received ectoparasiticides and those which did not (0 vs 12.2%; P = 0.009).”
    • Also stated in: § Results · plain
      “Prevalence of D. immitis antigen was significantly different between cats that received ectoparasiticides and those which did not (0 vs 12.2%, respectively; P = 0.009; Table 1).”
    Quote in the paperNot a substantial claim
  • Findingown data

    Prevalence of antibodies to T. gondii was significantly different between juvenile and adult cats (12.8 vs 38.0%; P = 0.007).

    “Prevalence of antibodies to T. gondii was significantly different between juvenile and adult cats (12.8 vs 38.0%; P = 0.007).”
    • Also stated in: § Results · plain
      “Prevalence of antibodies to T. gondii was significantly different between juvenile (5–11 months-old) and adult cats (1–21 years-old; 12.8 vs 38.0%, respectively; P = 0.007; Table 1).”
    Quote in the paperNot a substantial claim
  • Findingown data

    No statistically significant differences were found between categories of municipality, sex, breed, fur length, housing, clinical status and macrocyclic lactones for D. immitis and T. gondii.

    “Moreover, no statistically significant differences were found between the categories of the independent variables municipality, sex, breed, fur length, housing, clinical status and macrocyclic lactones, both for D. immitis and T. gondii (Table 1).”
    Quote in the paperNot a substantial claim
  • May combine two claims. 12
  • Classified as probably not a substantial claim. 5

  • May combine two claims.

    Findingcitation

    Zero prevalence of Leishmania antibodies in cats from Madeira is in line with the 0% found in 10 dogs from Madeira.

    “The zero prevalence of antibodies to Leishmania spp. in cats from Madeira Island is in line with the value (0%) found in 10 apparently healthy dogs also from Madeira assessed, from October 2010 to April 2011, for L. infantum antibodies with a rapid test [31].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [31] Cardoso L, Mendão C, Madeira de Carvalho L. Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal—a national serological study. Parasit Vectors. 2012;5:62. source

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    None of the D. immitis-positive cats received macrocyclic lactones, but comparison with treated animals was non-significant (P = 0.079).

    “In addition, none of the D. immitis-positive cats received macrocyclic lactones, but comparison with animals treated with them revealed a statistically non-significant difference, yet close to significance (P = 0.079; Table 1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    Cats on Madeira Island are at risk of becoming infected with D. immitis and T. gondii.

    “The present study provides evidence that cats on Madeira Island are at risk of becoming infected with D. immitis and T. gondii.”
    Quote in the paperSubstantial claim

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

    Premisecitation

    Prevention of heartworm infection is attainable in cats by routine administration of macrocyclic lactones, including eprinomectin and milbemycin oxime.

    “Anyway, prevention of heartworm infection is attainable in cats by the routine administration of macrocyclic lactones, including eprinomectin and milbemycin oxime [37, 38].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [37] Baker CF, Tielemans E, Pollmeier MG, McCall JW, McCall SD, Irwin J, et al. Efficacy of a single dose of a novel topical combination product containing eprinomectin to prevent heartworm infection in cats. Vet Parasitol. 2014;202:49–53. source

      Not checked in the free run.

    • cites [38] Little SE, Hostetler JA, Thomas JE, Bailey KL, Barrett AW, Gruntmeir K, et al. Moxidectin steady state prior to inoculation protects cats from subsequent, repeated infection with Dirofilaria immitis. Parasit Vectors. 2015;8:107. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    D. immitis antigen tests of the current generation identify most infections consisting of at least one mature female heartworm and are nearly 100% specific.

    “Nevertheless, D. immitis antigen tests of the current generation identify most infections consisting of at least one mature female heartworm and are nearly 100% specific [3].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] American Heartworm Society. Current feline guidelines for the prevention, diagnosis, and management of heartworm (Dirofilaria immitis) infection in cats. Wilmington: Am Heartw Soc; 2014.

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Cats are susceptible hosts but appear more resistant than dogs to infection with adult D. immitis.

    “Cats are susceptible hosts, but they seem to be more resistant than dogs to infection with adult D. immitis [3].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] American Heartworm Society. Current feline guidelines for the prevention, diagnosis, and management of heartworm (Dirofilaria immitis) infection in cats. Wilmington: Am Heartw Soc; 2014.

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    This is the first report of D. immitis and T. gondii in the feline population of Madeira Island.

    “To our knowledge, this is the first report of the presence of parasites D. immitis and T. gondii in the feline population of Madeira Island.”
    • Also stated in: § Discussion · hedged
      “To the best of our knowledge, this is the first study describing the prevalence of infection with or exposure to vector-borne and zoonotic pathogens in the feline population from Madeira Island.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: No published information is available from the feline population on the Madeira archipelago.

  • May combine two claims.

    Premisecitation

    Seropositive cats are likely to have already excreted T. gondii oocysts, so serological surveys can help determine potential risk of infection.

    “Seropositive cats are likely to have already excreted T. gondii oocysts, whereby serological surveys for the detection of antibodies can help to determine the potential risk of infection in defined geographical areas [46, 47].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [46] Lucas SR, Hagiwara MK, Loureiro VS, Ikesaki JY, Birgel EH. Toxoplasma gondii infection in Brazilian domestic outpatient cats. Rev Inst Med Trop Sao Paulo. 1999;41:221–4. source

      Not checked in the free run.

    • cites [47] Miró G, Montoya A, Jiménez S, Frisuelos C, Mateo M, Fuentes I. Prevalence of antibodies to Toxoplasma gondii and intestinal parasites in stray: farm and household cats in Spain. Vet Parasitol. 2004;126:249–55. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Madeira is the region of Portugal with the highest prevalence of heartworm infection in dogs, where cardiopulmonary dirofilariosis is the major endemic vector-borne disease.

    “Madeira is the region of Portugal with the highest prevalence of heartworm infection in dogs, in which cardiopulmonary dirofilariosis is the major endemic vector-borne disease [8, 31].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [8] Araujo AM. Canine and human Dirofilaria immitis infections in Portugal. A review. Parassitologia. 1996;38(Suppl. 1–2):366.

      Not checked in the free run.

    • cites [31] Cardoso L, Mendão C, Madeira de Carvalho L. Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal—a national serological study. Parasit Vectors. 2012;5:62. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    D. immitis and T. gondii are uniformly distributed among the surveyed feline population of Madeira.

    “No significant differences were found for the municipality, sex, breed, fur length, housing, clinical status and macrocyclic lactones (Table 1), suggesting that both D. immitis and T. gondii are uniformly distributed among the surveyed feline population of Madeira.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    The sample of 141 cats is representative of the feline population of Madeira Island, allowing extrapolation of results to the regional feline population.

    “The number of cats together with the incorporation of different animals may be considered a representative sample of Madeira Island, thus allowing an extrapolation of results to the regional feline population.”
    Quote in the paperSubstantial claim

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

    Premisecitation

    Monthly chemoprophylaxis is a safe and effective option for cats living in geographical areas where D. immitis infection is endemic and exposure to infectious mosquitoes is likely.

    “Monthly chemoprophylaxis is a safe and effective option for cats living in geographical areas where D. immitis infection is considered endemic and exposure to infectious mosquitoes is likely [3].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] American Heartworm Society. Current feline guidelines for the prevention, diagnosis, and management of heartworm (Dirofilaria immitis) infection in cats. Wilmington: Am Heartw Soc; 2014.

      Not checked in the free run.

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

    Premisecitation

    D. immitis, L. infantum and T. gondii are endemic in animal and human populations from many parts of the world, including southern Europe.

    “Dirofilaria immitis, L. infantum and T. gondii are pathogens endemic in animal and human populations from many parts of the world, including southern Europe [1].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [1] Baneth G, Thamsborg SM, Otranto D, Guillot J, Blaga R, Deplazes P, et al. Major Parasitic zoonoses associated with dogs and cats in Europe. J Comp Pathol. 2016;155(Suppl. 1):S54–74. source

      Not checked in the free run.

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

    Premisecitation

    D. immitis, L. infantum and T. gondii are zoonotic parasites that can affect domestic cats.

    “The nematode Dirofilaria immitis and protozoans Leishmania infantum and Toxoplasma gondii are zoonotic parasites which can affect domestic cats [1].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [1] Baneth G, Thamsborg SM, Otranto D, Guillot J, Blaga R, Deplazes P, et al. Major Parasitic zoonoses associated with dogs and cats in Europe. J Comp Pathol. 2016;155(Suppl. 1):S54–74. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning

    Six 5-month-old cats were not expected to be antigen-positive, increasing the D. immitis antigen prevalence estimate from 3.5% (5/141) to 3.7% (5/136).

    “Thus, six 5-month-old cats (data not shown) were not expected to be antigen-positive, a circumstance which increases the estimate of D. immitis antigen prevalence from 3.5% (5/141) to 3.7% (5/136).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] American Heartworm Society. Current feline guidelines for the prevention, diagnosis, and management of heartworm (Dirofilaria immitis) infection in cats. Wilmington: Am Heartw Soc; 2014.

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductcitation

    The DAT cut-off titre of 100 was chosen for Leishmania seropositivity.

    “Feline sera were diluted two-fold from 1:25 to 1:3200 in saline solution (0.9% NaCl) containing 0.1 M β-mercapto-ethanol, with a cut-off titre of 100 chosen for seropositivity [26].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [26] Cardoso L, Lopes AP, Sherry K, Schallig H, Solano-Gallego L. Low seroprevalence of Leishmania infantum infection in cats from northern Portugal based on DAT and ELISA. Vet Parasitol. 2010;174:37–42. source

      Not checked in the free run.

16 of 16

  • The paper relies on this without support.

    No published information is available from the feline population on the Madeira archipelago.

    “However, no published information is available from the feline population on the Madeira archipelago, the southernmost territorial part of Portugal.”

  • The paper relies on this without support.

    The ectoparasiticides listed in Table 1 do not have a repellent or anti-feeding effect protecting against infective mosquito bites, but are insecticides that reduce the total number or abundance of insects.

    “The products listed in Table 1 do not have a repellent or anti-feeding effect protecting against infective mosquito bites, but they are insecticides that contribute to reduce the total number or abundance of insects.”

  • The authors state this as an assumption.

    The prevalence of D. immitis infection in cats is 9–18% of the infection prevalence in dogs.

    “According to another recent report [5], a theoretical prevalence of 9–18% of the infection prevalence in dogs is expected to be observed in cats.”
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?

  • In Italy, feline heartworm studies are still scarce, and in the last decade studies showed a prevalence of 17.6% in Linosa.

    “In Italy, studies are still scarce. If previously, prevalence in cats was heterogeneous being 6.06–27% in the north and centre of the country, in addition to reports of isolated cases [4,9,123,124], in the last decade, studies in cats showed a prevalence of 17.6% in Linosa (an island halfway between the island of Sicily and the African coast of Tunisia) [40].”

    From What has happened to heartworm disease in Europe in the last 10 years? (2022) · cites this paper as [123]

  • No statistically significant differences in antibody seroprevalence were found based on sex.

    “No statistically significant differences were found based on sex, as has been published in previous studies (12, 13, 27).”

    From Seroprevalence of Feline Heartworm in Spain: Completing the Epidemiological Puzzle of a Neglected Disease in the Cat (2022) · cites this paper as [27]

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.

  • Reported toxoplasmosis chi-square statistic does not support significance

    Major

    For one degree of freedom, χ2 = 2.154 gives P ≈ 0.142, not P = 0.031. The reported statistic therefore does not support the stated significant difference.

  • Macrocyclic-lactone P value differs from Table 1

    Minor

    The discussion reports P = 0.079 for the D. immitis comparison involving macrocyclic lactones, whereas Table 1 reports P = 0.076 for that comparison.

  • Reported heartworm chi-square statistic conflicts with its P value

    Minor

    For one degree of freedom, χ2 = 4.705 gives P ≈ 0.030, not P < 0.0001. The comparison remains significant at the paper's 0.05 threshold.

3 of 3

The citation lists haven’t been fetched yet

References 46 · Cited by 31

Research works printed but not linked: 4

  1. American Heartworm Society. Current feline guidelines for the prevention, diagnosis, and management of heartworm (Dirofilaria immitis) infection in cats. Wilmington: Am Heartw Soc; 2014.
  2. Araujo AM. Canine and human Dirofilaria immitis infections in Portugal. A review. Parassitologia. 1996;38(Suppl. 1–2):366.
  3. Alves-Pires C, Capela RA. Phlébotomes du Portugal. VIII. Premiére mention de Phlebotomus (Paraphlebotomus) sergenti Parrot, 1917 à l’île de Madère. Parasite. 1917;1996(3):94.
  4. Alves-Pires C, Capela RA, Pena I. Os Flebótomos de Portugal. IX. Presença de Sergentomyia minuta (Rond., 1843) na Selvagem Grande (Madeira). Bol Soc Port Entomol. 1843;1997(178):389–95.

Authors
Neves, M., Lopes, A. P., Martins, C., Fino, R., Paixão, C., Damil, L., Lima, C., Alho, A. M., Schallig, H. D. F. H., Dubey, J. P., & Cardoso, L.
Affiliations
  • University of Trás-os-Montes and Alto Douro (PT)
  • Universidade do Porto (PT)
  • University of Lisbon (PT)
  • Amsterdam UMC Location University of Amsterdam (NL)
  • Agricultural Research Service (US)
ORCID
Venue
Parasites & Vectors
Publisher
Springer Science and Business Media LLC
Published
2020-04-21
Volume
13
Issue
1
Pages
117-117
ISSN
1756-3305 (ISSN-L)
DOI
10.1186/s13071-020-3988-4
PMC
PMC7171917
OpenAlex
W3016818313
Semantic Scholar
e592ce83897ac396a3c418f368feeb431599d9f5
Cited by
31
References
46
Citations by year
2026: 1 · 2025: 3 · 2024: 3 · 2023: 2 · 2022: 16 · 2021: 5 · 2020: 1
FWCI
0.79
Type
journal article
Language
en
Open access
Licence
Locations
  • Parasites & Vectors (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Pure Amsterdam UMC (publishedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
Fundação para a Ciência e a Tecnologia (Project UIDB/CVT/00772/2020)
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, Leishmania infantum, Toxoplasma gondii, feline parasitic infection, cats, seroprevalence, zoonotic parasites, ectoparasiticides, co-infection, Madeira
MeSH terms
Animals, Antibodies, Protozoan, Antigens, Helminth, Cat Diseases, Cats, Dirofilaria immitis, Dirofilariasis, Female, Male, Portugal, Toxoplasma, Toxoplasmosis, Animal, Prevalence, Seroepidemiologic Studies, Leishmania infantum, Pets

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

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