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Cited by 59Vector-borne infectious diseasesResearch on Leishmaniasis StudiesParasitic Diseases Research and Treatment

Current Distribution of Selected Vector-Borne Diseases in Dogs in Spain

Open access
Montoya-Alonso, José Alberto, Morchón, Rodrigo, Costa-Rodríguez, Noelia, Matos, Jorge Isidoro, Falcón-Cordón, Yaiza, Carretón, Elena·2020·Frontiers in Veterinary Science
DOI 10.3389/fvets.2020.564429PMC PMC7643126
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Abstract

Currently, climate change, modifications of landscapes and habitats due to human activities, as well as an increase in the movement of reservoirs and new species of competent vectors, have contributed to the spread of canine vector-borne diseases. These are mostly emerging and neglected diseases, some of them with zoonotic potential. Therefore, the objective of this study was to assess the prevalence and distribution of four major canine vector-borne diseases (Dirofilaria immitis, Leishmania infantum, Anaplasma spp. and Ehrlichia canis) in Spain. Between September 2018 and February 2020, blood was sampled from 4643 client-owned dogs from 111 veterinary clinics from the 17 autonomous communities of Spain. All samples were tested for the detection of D. immitis antigens, and for antibodies against L. infantum, Anaplasma spp. and E. canis. Of the studied dogs, 22.14% were positive for one or several diseases while the prevalence was 6.25% (CI: 5.59-6.98) for D. immitis, and the seroprevalences were 10.36% (CI: 9.52-11.27) for L. infantum, 5.06% (CI: 4.47-5.73) for Anaplasma spp., and 4.26% (CI: 3.72-4.88) for E. canis. Co-infections by two and three vector-borne diseases were reported in 13% and 2% of the infected dogs, respectively. The studied vector-borne diseases are widely distributed throughout the Spanish geography, being observed and expanding northward in the case of D. immitis and L. infantum. The results point to an insufficiency of preventive measures to avoid the infection, and the need of the implementation of awareness campaigns among veterinarians and owners. Furthermore, a close collaboration between veterinarians, physicians and health authorities would be necessary for such zoonotic vector-borne diseases

AI snapshot

Written from the paper’s full text.

TL;DR

This cross-sectional study estimated the prevalence and distribution of four major canine vector-borne diseases in Spain using 4,643 client-owned dogs sampled from 111 veterinary clinics across all 17 autonomous communities between September 2018 and February 2020. It found widespread distribution, with 22.14% of dogs positive for one or more diseases and evidence of northward expansion for *Dirofilaria immitis* and *Leishmania infantum*.

Key findings

  • Overall, 22.14% (1,028/4,643) of dogs were positive for one or several diseases. Prevalence was 6.25% (290/4,643; 95% CI 5.59–6.98) for *D. immitis*, and seroprevalences were 10.36% (481/4,643; 95% CI 9.52–11.27) for *L. infantum*, 5.06% (235/4,643; 95% CI 4.47–5.73) for *Anaplasma* spp., and 4.26% (198/4,643; 95% CI 3.72–4.88) for *Ehrlichia canis*. Estimated true prevalences were 6.65%, 10.78%, 5.32%, and 4.69%, respectively.
  • Co-infections occurred in 15% of infected dogs: 13% with two vector-borne infections and 2% with three. The most frequent two-pathogen combinations included *L. infantum* + *E. canis* (n=41), *L. infantum* + *Anaplasma* spp. (n=32), *L. infantum* + *D. immitis* (n=19), and *D. immitis* + *Anaplasma* spp. (n=19).
  • The diseases were widely distributed across Spain. *D. immitis* and *L. infantum* were observed expanding northward; highest *D. immitis* prevalence was in the Canary Islands (9.97%), while highest *L. infantum* seroprevalence was in Murcia (24.66%), the Balearic Islands (21.11%), Andalusia (18.03%), and the Valencian Community (17.11%). *Anaplasma* spp. and *E. canis* were fairly homogeneous geographically.
  • Risk-factor analyses found female dogs were 43% more likely to be positive for *D. immitis*; outdoor or indoor/outdoor habitat was significantly associated with *D. immitis* and *L. infantum*; and co-infections significantly increased the risk of other infections, e.g., *Anaplasma* spp. increased *D. immitis* risk by 64%, and *Anaplasma* spp. and *E. canis* increased *L. infantum* risk by 79% and 56%, respectively.

Methods

  • Cross-sectional study of 4,643 blood samples from client-owned dogs presented for routine health examination at 111 voluntary veterinary clinics/hospitals in the 17 autonomous communities of Spain, September 2018–February 2020. Inclusion criteria were no previous history of the studied vector-borne diseases, no regular chemoprophylaxis for them, and owner consent.
  • Serum samples were tested by immunochromatography using Uranotest Quattro for *D. immitis* antigens and antibodies against *L. infantum*, *Anaplasma* spp., and *E. canis*. Reported test sensitivity was 97% for *L. infantum*, 95% for *Ehrlichia*, 94% for *D. immitis*, and 96% for *Anaplasma*; specificity was 99%, 94.6%, 100%, and 99%, respectively.
  • Descriptive analysis and univariate/multivariate logistic regression models were performed in SPSS Base 20.0 to assess associations with gender, age, co-infection, climate, habitat, and region.

Limitations

  • The paper states that although clinicians were asked to choose samples randomly, they may have inadvertently selected samples based on personal preference, and the sample was not representative of each autonomous community, especially larger ones, despite efforts to recruit many clinics across the geography.
  • The paper states that results for filaria and anaplasma should be interpreted cautiously because the goodness of fit of the model was not sufficiently good, as indicated by the Hosmer and Lemeshow test with p < 0.05.
  • Evident from the text: antibody detection for *L. infantum*, *Anaplasma* spp., and *E. canis* indicates exposure rather than necessarily current infection, and the cross-sectional design cannot establish temporal trends or causality; voluntary clinic participation and non-probability sampling may further limit generalizability.

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

Integrity signals

Registry

Crossref · 10.3389/fvets.2020.564429

Cites

71 of 71 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 105 cited sources checked · 0 supported · 0 flagged

  • Findingreasoning

    Taking into account the sensitivity and specificity of the tests used, the true prevalence of E. canis was estimated as 4.69%.

    “Taking into account the sensitivity and specificity of the tests used, true prevalence could be estimated as 6.65% (D. immitis), 10.78% (L. infantum), 5.32% (Anaplasma spp.), and 4.69% (E. canis).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The diagnostic tests used have the stated sensitivity and specificity values.
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.
  • Findingown data

    Higher prevalences of D. immitis were observed in the Canary Islands.

    “higher prevalences were observed in the Canary Islands (D. immitis)”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.
  • Findingown data

    The Cfb climate compared to the Bsk climate reduced the presence of dirofilariosis by 66%.

    “the Cfb climate compared to the Bsk climate reduced the presence of dirofilariosis by 66%.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.
  • Findingown data

    Females were 43% more likely than males to present dirofilariosis.

    “being females 43% more likely to present dirofilariosis”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.
  • Findingown data

    Cfb, Csb, and subtropical climates reduced the presence of L. infantum compared to the Bsk climate, by 73%, 75%, and 92%, respectively.

    “Regarding climate, it was observed that the Cfb, Csb, and subtropical climates reduced the presence of L. infantum when compared to the Bsk climate, being a reduction of 73, 75, and 92%, respectively.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.
  • May combine two claims. 29
  • Classified as probably not a substantial claim. 19
  • The quote only partly states this claim. 1

  • May combine two claims.

    Findingown data

    Indoor/outdoor habitat presented 2.43 times more risk of L. infantum infection, and outdoor habitat presented 3.76 times more risk.

    “The indoor/outdoor habitat presented 2.43 times more risk of being infected, while the outdoor habitat presented 3.76 times more risk of infection.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Findingown data

    Age was significantly associated with the presence of Leishmania; as age increased, the risk of leishmaniasis increased, except in dogs >15 years, in which the association was no longer significant.

    “Regarding age, a significant association was observed with the presence of Leishmania; as age increased, the risk of leishmaniasis increased, except in dogs >15 years, in which the association was no longer significant.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Findingown data

    Presence of co-infections significantly increased the risk of anaplasmosis; D. immitis increased this risk by 57% and L. infantum by 82%.

    “The presence of co-infections significantly increased the risk of anaplasmosis; infection by D. immitis increased this risk by 57% and L. infantum by 82%.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Findingown data

    Dogs infected by E. canis between 5 and 10 years had 3.37 times more risk, and those between 10 and 15 years had 3.86 times more risk, compared to dogs <1 year.

    “When dogs infected by E. canis were analyzed, those between 5 and 10 years showed 3.37 times more risk of presenting the infection, and those between 10 and 15 years showed 3.86 times more risk of infection, when compared to dogs <1 years, both associations being significant.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Findingown data

    Co-infections with Anaplasma spp. and E. canis significantly increased the risk of L. infantum by 79% and 56%, respectively.

    “Co-infections with Anaplasma spp. and E. canis significantly increased the risk of L. leishmaniasis by 79 and 56%, respectively.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Findingown data

    Animals in the central zone showed an increase of 91% in presenting Anaplasma spp. compared to the northern zone; those in the southern zone had 3.32 times more risk than those in the northern zone.

    “Animals in the central zone showed an increase of 91% in presenting the disease compared to those that lived in the northern zone. Those in the southern zone had 3.32 times more risk of infection than those who lived in the northern zone.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Findingown data

    Anaplasma spp. and E. canis were quite homogeneously distributed in the country.

    “Anaplasma spp. and E. canis were quite homogeneously distributed in the country.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Findingown data

    L. infantum presence is confirmed throughout northern Spain, which is dominated by Cfb climate, and this region has the lowest seroprevalences in the country.

    “The presence of L. infantum is confirmed throughout the north of the country, dominated by the Cfb climate, with the lowest seroprevalences in the entire country.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

  • May combine two claims.

    Findingown data

    The results of this research confirm the presence of leishmaniasis in northern Spain and its wide expansion throughout all autonomous communities traditionally considered free of the disease.

    “The results of this research confirm not only the presence of leishmaniasis in the north, but its wide expansion throughout all the autonomous communities traditionally considered free of the disease”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

  • May combine two claims.

    Findingown data

    This study has completed and updated the epidemiological map of these autonomous communities and provided prevalences in communities that had never been epidemiologically evaluated.

    “The results of this research have made it possible to complete and update the epidemiological map of these autonomous communities, as well as to provide prevalences in those communities that had never been epidemiologically evaluated.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

  • May combine two claims.

    Findingcitation

    This study completes the epidemiological map of L. infantum in Spain, which had only been studied in some provinces of certain autonomous communities (Andalusia, Extremadura, Castile and Leon, Castilla la Mancha, Valencian Community, Catalonia, or Aragon).

    “In this study, the epidemiological map of the disease is completed, only studied in some provinces of the autonomous communities (i.e., Andalusia, Extremadura, Castile and Leon, Castilla la Mancha, Valencian Community, Catalonia, or Aragon) (9, 15, 17, 50–53).”
    Quote in the paperSubstantial claim0 of 7 sources checked
    • cites [9] Miró, 2013, Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study, Parasit Vectors. source

      Not checked in the free run.

    • cites [15] Ballart, 2012, Is leishmaniasis widespread in Spain? First data on canine leishmaniasis in the province of Lleida, Catalonia, northeast Spain, Trans R Soc Trop Med Hyg. source

      Not checked in the free run.

    • cites [17] Ballart, 2013, First survey on canine leishmaniasis in a non-classical area of the disease in Spain (Lleida, Catalonia) based on a veterinary questionnaire and a cross-sectional study, Prev Vet Med. source

      Not checked in the free run.

    • cites [50] Encinas Grandes, 1988, Leishmaniasis in the province of Salamanca, Spain. Prevalence in dogs, and seasonal dynamics of vectors, Ann Parasitol Hum Comp. source

      Not checked in the free run.

    • cites [51] Fisa, 1999, Epidemiology of canine leishmaniosis in Catalonia (Spain) the example of the Priorat focus, Vet Parasitol. source

      Not checked in the free run.

    • cites [52] Martinez Cruz, 1990, Epidemiología de la leishmaniosis canina en Córdoba, Rev Ibér Parasitol.

      Not checked in the free run.

    • cites [53] Velez, 2019, Seroprevalence of canine Leishmania infantum infection in the Mediterranean region and identification of risk factors: the example of North-Eastern and Pyrenean areas of Spain, Prev Vet Med. source

      Not checked in the free run.

    • Rests on an assumption: The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

  • May combine two claims.

    Findingcitation

    Prevalences of Anaplasma spp. and E. canis from previous studies in Galicia, Castilla, and Leon or Madrid were lower than the results obtained in this study, except for E. canis in Castilla and Leon (19.2%).

    “The prevalences obtained from studies previously carried out in Galicia, Castilla, and Leon or Madrid on both bacteria (9, 65–68) were lower than the results obtained in this study, except in the case of Castilla and Leon (19.2% for E. canis) (66).”
    Quote in the paperNot a substantial claim0 of 5 sources checked
    • cites [9] Miró, 2013, Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study, Parasit Vectors. source

      Not checked in the free run.

    • cites [65] Couto, 2010, Serological study of certain vector-borne diseases in refuge dogs in central Spain, Vector by Zoonotic Dis. source

      Not checked in the free run.

    • cites [66] Sainz, 1998, Canine ehrlichiosis in the community of Madrid in central Spain, Ann NY Acad Sci. source

      Not checked in the free run.

    • cites [67] Sainz, 1996, Seroprevalence of canine ehrlichiosis in Castilla-León (northwest of Spain), Prev Med Vet. source

      Not checked in the free run.

    • cites [68] Sainz, 1995, Seroprevalence of Ehrlichia canis infections in police dogs in Spain, Prev Vet Med. source

      Not checked in the free run.

    • Rests on an assumption: The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

  • May combine two claims.

    Findingreasoning

    The presence of Anaplasma spp. and E. canis is quite homogeneous and does not appear to be influenced by the type of climate prevailing in the autonomous communities.

    “The presence of Anaplasma spp. and E. canis is quite homogeneous, without appearing to be influenced by the type of climate prevailing in the autonomous communities.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

  • May combine two claims.

    Findingreasoning

    Anaplasma spp. and E. canis are distributed throughout Spain in a fairly homogeneous way.

    “Both Anaplasma spp. and E. canis are distributed throughout the geography in a fairly homogeneous way.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

  • May combine two claims.

    Findingown data

    Higher seropositivities were found in adult dogs between 1 and 10 years, with a slight decrease in dogs >15 years.

    “Regarding age, higher seropositivities were found in adult dogs between 1 and 10 years, observing a slight decrease in dogs >15 years.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

  • May combine two claims.

    Interpretationown data

    The results show the inexorable expansion of D. immitis throughout the Spanish geography, as suspected and as already reported at the European level.

    “this shows the inexorable expansion of D. immitis throughout the Spanish geography as suspected, and as has already been reported at the European level (1).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [1] Morchón, 2012, Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends, Front Physiol. source

      Not checked in the free run.

    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Premisecitation

    Prior to this study, except in Galicia, studies in northern Spain had been carried out in specific areas such as towns or small areas of Cantabria, Asturias and the Basque Country, and in some cases demonstrated that leishmaniasis was already present.

    “Previously, except in the case of Galicia (9, 14) studies had been carried out in specific areas, such as towns or small areas of Cantabria, Asturias and the Basque Country, which in some cases demonstrated that leishmaniasis was already present (16)”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [9] Miró, 2013, Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study, Parasit Vectors. source

      Not checked in the free run.

    • cites [14] Amusátegui, 2004, Seroprevalence of Leishmania infantum in northwestern Spain, an area traditionally considered free of leishmaniasis, Ann N Y Acad Sci. source

      Not checked in the free run.

    • cites [16] Miró, 2012, Current status of Leishmania infantum infection in shelter dogs in northern Spain, Parasit Vectors. source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data

    The goodness of fit of the model is not sufficiently good, as indicated by the Hosmer and Lemeshow test with p < 0.05, so results must be interpreted cautiously.

    “we must be cautious in interpreting the results because the goodness of fit of the model is not sufficient good as indicated by the Hosmer and Lemeshow test with a p < 0.05.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationreasoning

    D. immitis prevalences rise in La Rioja and Aragón, possibly because they present important irrigated areas crossed by the Ebro River.

    “These prevalences rise in La Rioja and Aragón, possibly because, despite the weather, they present important irrigated areas crossed by one of the main rivers of the Iberian Peninsula, the Ebro River.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationown data

    The results point to an insufficiency of preventive measures to avoid infection by the studied vector-borne diseases.

    “The results point to an insufficiency of preventive measures to avoid the infection”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims. The quote only partly states this claim.

    Interpretationreasoning

    In general, the lowest prevalences of D. immitis and L. infantum corresponded to autonomous communities dominated by the Cfb climate, probably due to the low temperatures present much of the year.

    “In general, the lowest prevalences corresponded to those autonomous communities dominated by the Cfb climate, probably due to the low temperatures that are present much of the year.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

  • May combine two claims.

    Premisecitation

    The four studied canine vector-borne diseases are among the most clinically relevant and most prevalent in the Spanish geography.

    “This research focuses on four canine vector-borne diseases that are among the most clinically relevant and most prevalent in the Spanish geography (1, 3, 4).”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [1] Morchón, 2012, Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends, Front Physiol. source

      Not checked in the free run.

    • cites [3] Sainz, 2015, Guideline for veterinary practitioners on canine ehrlichiosis and anaplasmosis in Europe, Parasit Vectors. source

      Not checked in the free run.

    • cites [4] Miró, 2008, Canine Leishmaniosis: new concepts and ideas about an expanding zoonosis: part two, Parasitol Trends. source

      Not checked in the free run.

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

    Interpretationnone given

    Differences in techniques and sampling between studies could confound comparisons of L. infantum prevalence variations across years.

    “the different techniques and sampling carried out could be a confounding factor when comparing the variations in the prevalences obtained in the studies obtained in different years.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    The studied vector-borne diseases are widely distributed throughout the Spanish geography, being observed and expanding northward in the case of D. immitis and L. infantum.

    “The studied vector-borne diseases are widely distributed throughout the Spanish geography, being observed and expanding northward in the case of D. immitis and L. infantum.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sampled dogs are representative of the canine population in Spain and in each autonomous community.

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

    Premisecitation

    Climatic factors such as temperature and humidity influence the distribution of animal diseases, including vector-borne diseases, causing dynamic changes in their geographical distribution, epidemiology, pathogenicity, and control.

    “It is described that climatic factors (i.e., temperature and humidity) influence the distribution of animal diseases, such as vector-borne diseases, causing dynamic changes in their geographical distribution, epidemiology, pathogenicity, and control.”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [1] Morchón, 2012, Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends, Front Physiol. source

      Not checked in the free run.

    • cites [2] Dantas-Torres, 2015, Climate change, biodiversity, ticks and tick-borne diseases: the butterfly effect, Int J Parasitol Parasites Wildl. source

      Not checked in the free run.

    • cites [3] Sainz, 2015, Guideline for veterinary practitioners on canine ehrlichiosis and anaplasmosis in Europe, Parasit Vectors. source

      Not checked in the free run.

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

    Interpretationreasoning

    A possible explanation for the high L. infantum prevalences is that prophylactic measures are still insufficient.

    “a possible explanation being that the prophylactic measures are still insufficient.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Anthropogenic factors such as globalization, transport of infected animals from endemic areas, environmental changes related to human activities, and climatic change favor the spread of vector-borne diseases.

    “anthropogenic factors such as globalization with the increasing circulation of people and goods, the transport of infected animals from endemic areas, environmental changes related to human activities and climatic change, favor the spread of vector-borne diseases (1–3).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [1] Morchón, 2012, Heartworm disease (Dirofilaria immitis) and their vectors in Europe - new distribution trends, Front Physiol. source

      Not checked in the free run.

    • cites [2] Dantas-Torres, 2015, Climate change, biodiversity, ticks and tick-borne diseases: the butterfly effect, Int J Parasitol Parasites Wildl. source

      Not checked in the free run.

    • cites [3] Sainz, 2015, Guideline for veterinary practitioners on canine ehrlichiosis and anaplasmosis in Europe, Parasit Vectors. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    In Spain, canine leishmaniasis is currently considered endemic in most of the Iberian Peninsula and the Balearic Islands, with prevalences between 3.7% and 46.6%, being higher in southern and eastern areas.

    “In Spain, canine leishmaniasis was considered to be limited to the Mediterranean region (13, 14) but currently is considered endemic in most of the Iberian Peninsula and the Balearic Islands with prevalences between 3.7 and 46.6%, being higher in southern and eastern areas of the country (4, 14–18).”
    Quote in the paperNot a substantial claim0 of 6 sources checked
    • cites [4] Miró, 2008, Canine Leishmaniosis: new concepts and ideas about an expanding zoonosis: part two, Parasitol Trends. source

      Not checked in the free run.

    • cites [14] Amusátegui, 2004, Seroprevalence of Leishmania infantum in northwestern Spain, an area traditionally considered free of leishmaniasis, Ann N Y Acad Sci. source

      Not checked in the free run.

    • cites [15] Ballart, 2012, Is leishmaniasis widespread in Spain? First data on canine leishmaniasis in the province of Lleida, Catalonia, northeast Spain, Trans R Soc Trop Med Hyg. source

      Not checked in the free run.

    • cites [16] Miró, 2012, Current status of Leishmania infantum infection in shelter dogs in northern Spain, Parasit Vectors. source

      Not checked in the free run.

    • cites [17] Ballart, 2013, First survey on canine leishmaniasis in a non-classical area of the disease in Spain (Lleida, Catalonia) based on a veterinary questionnaire and a cross-sectional study, Prev Vet Med. source

      Not checked in the free run.

    • cites [18] Mattin, 2014, The frequency and distribution of canine leishmaniosis diagnosed by veterinary practitioners in Europe, Vet J. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Other epidemiological studies found no significant gender differences in Dirofilaria infections, while others did.

    “although other epidemiological studies found no significant differences (9, 14, 34), these differences were also observed in others (7, 8, 70).”
    Quote in the paperNot a substantial claim0 of 6 sources checked
    • cites [9] Miró, 2013, Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study, Parasit Vectors. source

      Not checked in the free run.

    • cites [14] Amusátegui, 2004, Seroprevalence of Leishmania infantum in northwestern Spain, an area traditionally considered free of leishmaniasis, Ann N Y Acad Sci. source

      Not checked in the free run.

    • cites [34] Montoya-Alonso, 2017, Prevalence of heartworm in dogs and cats of Madrid, Spain, Parasit Vectors. source

      Not checked in the free run.

    • cites [7] Montoya-Alonso, 2015, Prevalence of Dirofilaria immitis in dogs from Barcelona: validation of a geospatial prediction model, Vet Parasitol. source

      Not checked in the free run.

    • cites [8] Montoya-Alonso, 2016, The impact of the climate on the epidemiology of Dirofilaria immitis in the pet population of the Canary Islands, Vet Parasitol. source

      Not checked in the free run.

    • cites [70] Montoya-Alonso, 2011, Current prevalence of Dirofilaria immitis in dogs, cats and humans from the island of Gran Canaria, Spain, Vet Parasitol. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    R. sanguineus is the most common tick found in dogs in Spain and has been detected across the country.

    “Regarding R. sanguineus, this tick is the most common tick found in dogs in Spain (61–63) and it has been detected across the country”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [61] Estrada-Peña, 2017, Species of ticks and carried pathogens in owned dogs in Spain: results of a one-year national survey, Ticks Tick Borne Dis. source

      Not checked in the free run.

    • cites [62] Chitimia-Dobler, 2019, Genetic analysis of Rhipicephalus sanguineus sensu lato ticks, parasites of dogs in the Canary Islands, Cyprus, and Croatia, based on mitochondrial 16S rRNA gene sequences, Parasitol Res. source

      Not checked in the free run.

    • cites [63] Vila, 2019, Endosymbionts carried by ticks feeding on dogs in Spain, Ticks Tick Borne Dis. source

      Not checked in the free run.

    • cites [64] 2019

      Not checked in the free run.

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

    Premisecitation

    A. phagocytophilum has been isolated from other hosts, including humans.

    “this agent has also been isolated from other hosts, including humans (58–60).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [58] Gray, 2009, Effects of climate change on ticks and tick-borne diseases in Europe, Interdiscip Perspect Infect Dis. source

      Not checked in the free run.

    • cites [59] Medlock, 2013, Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe, Parasit Vect. source

      Not checked in the free run.

    • cites [60] Oteo, 2000, First report of human granulocytic ehrlichiosis from southern Europe (Spain), Emerg Infect Dis. source

      Not checked in the free run.

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

    Interpretationcitation

    The lower prevalences in that recent study could be due to different sampling procedures and number of samples.

    “which could be due to the different sampling procedures—being the samples from the northernmost area of the studied autonomous communities—and number of samples (44).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [44] Díaz-Regañón, 2020, Serological evaluation of selected vector-borne pathogens in owned dogs from northern Spain based on a multicenter study using a commercial test, Parasit Vect. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    The Canary Islands were considered free of L. infantum, although personal communications and a publication of a clinical case raised suspicion of indigenous cases.

    “These islands were considered free of the disease, although personal communications and a publication of a clinical case (54) raised suspicion of the presence of indigenous cases.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [54] Dandrieux, 2018, Canine Leishmania infantum infection: an imported case in UK after staying in the Canary Islands, Parasitol Res. source

      Not checked in the free run.

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

    Interpretationnone given

    The presence of Anaplasma spp. may refer to A. platys or A. phagocytophilum.

    “The presence of Anaplasma spp. may refer to A. platys or A. phagocytophilum.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Indoor animals are more protected against the presence of vectors.

    “This result is understandable since indoor animals are more protected against the presence of vectors.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    Presence of antibodies denotes that the animal is exposed to the disease and at risk of infection, whether or not it is a current infection.

    “the presence of antibodies denotes that, whether or not it is a current infection, the animal is exposed to the disease and, therefore, at risk of infection”
    Quote in the paperSubstantial claim

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

    Premisecitation

    Co-infections of vector-borne diseases are common, and up to half of patients with positive test results may have evidence of co-infection or co-exposure.

    “it has been previously reported that co-infections of vector-borne diseases are common, and studies have reported that up to half of all patients with positive test results for vector-borne diseases may have evidence of co-infection or co-exposure (71–74).”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [71] Tabar, 2013, Wolbachia, filariae and Leishmania coinfection in dogs from a Mediterranean area, J Small Anim Pract. source

      Not checked in the free run.

    • cites [72] Maggi, 2014, Comparison of serological and molecular panels for the diagnosis of vector-borne diseases in dogs, Parasit Vect. source

      Not checked in the free run.

    • cites [73] Attipa, 2018, Association between canine leishmaniosis and Ehrlichia canis co-infection: a prospective case-control study, Parasit Vectors. source

      Not checked in the free run.

    • cites [74] Baxarias, 2018, Does co-infection with vector-borne pathogens play a role in clinical canine leishmaniosis?, Parasit Vectors. source

      Not checked in the free run.

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

    Premisecitation

    This finding agrees with previous studies on vector-borne diseases.

    “This agrees with previous studies carried out in vector-borne diseases (9, 23, 34).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [9] Miró, 2013, Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study, Parasit Vectors. source

      Not checked in the free run.

    • cites [23] Solano-Gallego, 2006, A serological study of exposure to arthropod-borne pathogens in dogs from northeastern Spain, Vet Res. source

      Not checked in the free run.

    • cites [34] Montoya-Alonso, 2017, Prevalence of heartworm in dogs and cats of Madrid, Spain, Parasit Vectors. source

      Not checked in the free run.

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

    Study design and conductnone given

    Written informed consent was obtained from the owners for the participation of their animals in this study.

    “Written informed consent was obtained from the owners for the participation of their animals in this study.”
    Quote in the paperNot a substantial claim

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

    Study design and conductnone given

    This animal study was reviewed and approved by the ethical committee of Veterinary Medicine Service of the University of Las Palmas de Gran Canaria.

    “This animal study was reviewed and approved by ethical committee of Veterinary Medicine Service of the University of Las Palmas de Gran Canaria.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    This highlights a lack of preventive measures to avoid interaction with vectors.

    “This highlights a lack of preventive measures to avoid the interaction with the vectors”
    Quote in the paperNot a substantial claim

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

    Study design and conductnone given

    The samples were chosen randomly by veterinary clinicians, but there is a possibility that they inadvertently selected samples out of personal preference.

    “even though the samples were chosen randomly by veterinary clinicians, there is a possibility that they have inadvertently selected the samples out of some sort of personal preference.”
    Quote in the paperNot a substantial claim

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

    Interpretationreasoning

    The different results across studies by age could be due to different methodology, sampling, and sensitivity/specificity of tests.

    “This could be due to the different methodology used in the studies, both in sampling and in the sensitivity/specificity of the different tests used.”
    Quote in the paperNot a substantial claim

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

    Interpretationreasoning

    The lower prevalences in dogs <1 year may be due to less exposure to pathogens and, for D. immitis, because antigens are not detected until 6 months post-infection.

    “possibly due to less exposure to the pathogens and, in the case of D. immitis, due to the fact that antigens are not detected until 6 months post-infection.”
    Quote in the paperNot a substantial claim

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

    Premisecitation

    Previous epidemiological studies have obtained different results when dogs were assessed by age, with statistical significance between age groups in some studies but not in others.

    “Previous epidemiological studies have obtained different results when the dogs were assessed by age, finding statistical significance between age groups in some epidemiological studies of vector-borne diseases but not in others (8, 9, 46).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [8] Montoya-Alonso, 2016, The impact of the climate on the epidemiology of Dirofilaria immitis in the pet population of the Canary Islands, Vet Parasitol. source

      Not checked in the free run.

    • cites [9] Miró, 2013, Seropositivity rates for agents of canine vector-borne diseases in Spain: a multicentre study, Parasit Vectors. source

      Not checked in the free run.

    • cites [46] Martín-Sánchez, 2009, Canine leishmaniasis in southeastern Spain, Emerg Infect Dis. source

      Not checked in the free run.

45 of 45

  • The paper relies on this without support.

    The distribution of the studied vector-borne diseases in Spain is incomplete because epidemiological studies have not been carried out in some provinces and autonomous communities, and some existing studies were done more than 20 years ago.

    “In Spain, the distribution of these vector borne-diseases is incomplete because epidemiological studies have not been carried out in some provinces and autonomous communities. Moreover, some of these studies were done more than 20 years ago”

  • The paper relies on this without support.

    The diagnostic tests used have the stated sensitivity and specificity values.

    “The sensitivity of the tests was: 97% for L. infantum (vs. IFI), 95% for Ehrlichia (vs. IFI), 94% for D. immitis (vs. necropsy) and 96% for Anaplasma (vs. IFI). The specificity was: 99% for L. infantum (vs. IFI), 94.6% for Ehrlichia (vs. IFI), 100% for D. immitis (vs. necropsy), and 99% for Anaplasma (vs. IFI).”

  • The paper relies on this without support.

    The sampled dogs are representative of the canine population in Spain and in each autonomous community.

    “The study included a total of 4,643 blood samples from domestic dogs, collected between September 2018 and February 2020. Samples were collected from dogs presented for routine health examination to 111 veterinary clinics and hospitals located in the 17 autonomous communities present in Spain”

  • The paper relies on this without support.

    The diagnostic tests used in this study accurately classify infection/exposure status for the vector-borne pathogens studied.

    “In the case of D. immitis, the detection of parasitic antigens allows to determine current infections.”

  • The paper relies on this without support.

    The owners' reports of whether dogs live indoors or outdoors accurately reflect the dogs' actual habitat.

    “By habitat, prevalences were significantly lower in dogs living indoors.”
5 of 5

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?

  • Dogs living indoors showed significantly lower prevalences because they are less exposed to vector mosquitoes.

    “Regarding habitat, dogs living indoors showed significantly lower prevalences, as shown in other similar studies [8,9,11,12,13,19]. As has been pointed out in previous studies, animals that live indoors are less exposed to the presence of vector mosquitoes and, thus, prevalences are lower.”

    From Expansion of canine heartworm in Spain (2022) · cites this paper as [9]

  • In the last 15 years, a slight increase in heartworm can be confirmed in most autonomous communities, with decreasing prevalences or similar values only in Aragon, Catalonia, Valencian Community, Madrid and Castilla y León.

    “in the last 15 years a slight increase in heartworm can be confirmed in most of the autonomous communities, with decreasing prevalences or with similar values only in Aragon, Catalonia, Valencian Community, Madrid and Castilla y León.”

    From Expansion of canine heartworm in Spain (2022) · cites this paper as [9]

  • Previous prevalences in Spain showed a high risk of infection throughout the Spanish territory, with the exception of some central and northern autonomous communities.

    “The prevalences previously reported showed a high risk of infection throughout the Spanish territory, with the exception of some central and northern autonomous communities [9].”

    From Expansion of canine heartworm in Spain (2022) · cites this paper as [9]

  • The lower prevalence in dogs <1 year is likely due to a minor exposure to vectors.

    “The prevalence was lower in dogs <1 year, likely due to a minor exposure to vectors, as stated in previous research [8,9,19,22].”

    From Expansion of canine heartworm in Spain (2022) · cites this paper as [9]

  • In the Canary Islands, prevalences have remained similar or with slight oscillations during the last 20 years, although the presence of the parasite is reported for the first time in Lanzarote.

    “the prevalences have remained similar or with slight oscillations during the last 20 years [9,12,27,28,29], although the presence of the parasite is reported for the first time in Lanzarote.”

    From Expansion of canine heartworm in Spain (2022) · cites this paper as [9]

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.

  • Crude E. canis outdoor odds ratio conflicts with Table 2

    Major

    Table 3 reports an outdoor-versus-indoor crude odds ratio of 1.19. Table 2 shows 92 positives among 1,726 outdoor dogs versus 10 among 1,393 indoor dogs, corresponding to a substantially larger crude odds ratio of about 7.8.

  • Crude E. canis indoor/outdoor odds ratio reverses the observed association

    Major

    Table 3 gives an indoor/outdoor-versus-indoor crude odds ratio of 0.12. Table 2 reports E. canis positivity of 6.30% for indoor/outdoor dogs versus 0.72% for indoor dogs, which requires a crude odds ratio greater than 1.

  • Co-infection percentage changes denominator

    Minor

    The discussion says co-infections occurred in 15% of the dogs, whereas the results specify 15% of the infected dogs. These are different denominators: the study reports 1,028 infected dogs out of 4,643 studied dogs.

  • Five age groups are described as four

    Minor

    The sentence says dogs were divided into four age groups but lists five: under 1, 1-5, 5-10, 10-15 and over 15 years.

  • Crude Leishmania gender odds ratio has the wrong direction

    Minor

    With males as the reference category, Table 3 reports a crude odds ratio of 1.43 for females. Table 2 instead shows lower Leishmania seroprevalence in females (9.90%) than males (10.75%), so the crude female-to-male odds ratio must be below 1.

  • Significant D. immitis association is asserted for all dogs over one year

    Minor

    The statement includes dogs older than 15, but Table 3 gives that age group an adjusted confidence interval of 0.57-8.57 and does not mark its association significant.

  • Murcia is called Csa despite its Bsk classification

    Minor

    The discussion includes Murcia among communities said to be dominated by the Csa climate, while Table 1 classifies Murcia as Bsk.

  • Figure labels an Anaplasma spp. result as A. platys

    Minor

    The figure caption identifies panel C specifically as A. platys, but the paper says its Anaplasma spp. positives may represent either A. platys or A. phagocytophilum.

8 of 8

Cites

Flagged first, then by citations

Research works printed but not linked: 5

  1. Guerrero, 1989, Estudio de la incidencia de la enfermedad del gusano del corazón en la población canina española, Med Vet., 6, 217
  2. Guerrero, 1995, The extension of the prevalence of Dirofilaria immitis in Cataluña, Spain. In: MD Soll, DH Knigh, editors, 73
  3. Rojo-Vázquez, 1990, Prevalencia de la dirofilariosis canina en cuatro áreas geográficas de España, Med Vet., 7, 297
  4. Simón, 2009, Dirofilariosis canina en La Coruña, Argos., 106, 10
  5. Martinez Cruz, 1990, Epidemiología de la leishmaniosis canina en Córdoba, Rev Ibér Parasitol., 50, 1

Cited by

Sorted by citations

Related

Authors
Montoya-Alonso, J. A., Morchón, R., Costa-Rodríguez, N., Matos, J. I., Falcón-Cordón, Y., & Carretón, E.
Affiliations
  • Universidad de Las Palmas de Gran Canaria (ES)
  • Universidad de Salamanca (ES)
Corresponding author
Carretón, Elena
ORCID
Venue
Frontiers in Veterinary Science
Publisher
Frontiers Media SA
Published
2020-10-22
Volume
7
Pages
564429-564429
ISSN
2297-1769 (ISSN-L)
DOI
10.3389/fvets.2020.564429
PMC
PMC7643126
OpenAlex
W3093854988
Semantic Scholar
c2b3e17c3ad631df464fafb273ac06e325a71fa7
Cited by
59
References
71
Citations by year
2026: 8 · 2025: 7 · 2024: 12 · 2023: 8 · 2022: 13 · 2021: 11
FWCI
6.00
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Veterinary Science (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Acceda (Universidad de Las Palmas de Gran Canaria) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Agencia Canaria de Investigación, Innovación y Sociedad de la Información (ProID2017010111)
  • Ministerio de Ciencia, Innovación y Universidades (GOB-ESP2019-12)
  • Boehringer Ingelheim
Topics
  • Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Research on Leishmaniasis Studies
  • Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
Keywords
canine vector-borne diseases, Dirofilaria immitis, Leishmania infantum, Anaplasma, Ehrlichia canis, seroprevalence, co-infection, zoonoses, emerging infectious diseases, spatial distribution, climate change, Spain

About these checks

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.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-09.

Statistics and arithmetic are recomputed, not judged.

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