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Cited by 119Research on Leishmaniasis StudiesParasitic Diseases Research and TreatmentVector-borne infectious diseases

Leishmania infantum and Dirofilaria immitis infections in Italy, 2009–2019: Changing distribution patterns

Open access
Mendoza-Roldan, Jairo, Benelli, Giovanni, Panarese, Rossella, Iatta, Roberta, Furlanello, Tommaso, Beugnet, Frederic, Zatelli, Andrea, Otranto, Domenico·2020·Parasites & Vectors
DOI 10.1186/s13071-020-04063-9PMC PMC7161282

Published version of a preprint

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Abstract

Background: For long time, canine leishmaniosis (CanL) was considered endemic in the southern, central, and insular regions of Italy, whereas heartworm disease (HW) caused by Dirofilaria immitis was considered endemic in the northern region and in the swampy Po Valley. Following the reports of new foci of both diseases, in this study we update the distribution patterns and occurrence of new foci of CanL and HW discussing the main drivers for the changes in the epidemiology of these two important zoonotic canine vector-borne diseases. Methods: Based on the statistical analyses of serological assays ( n = 90,633) on L. infantum exposure and D. immitis infection performed by two reference diagnostic centres in Italy over a ten-year period (2009–2019) irrespective of the anamnesis of dogs. The distribution patterns of both parasites are herein presented along with the occurrence of new foci. Results: Results highlighted the changing distribution patterns of L. infantum vs D. immitis infection in Italy. CanL is endemic in some areas of northern regions and HW has endemic foci in central and southern regions and islands. Significant differences in L. infantum exposure and HW infection prevalence among the study macroareas were detected. The overall results of the positive tested samples were 28.2% in southern Italy and islands, 29.6% in central Italy and 21.6% in northern Italy for L. infantum and 2.83% in northern Italy, 7.75% in central Italy and 4.97% in southern Italy and islands for HW. HW positivity significantly varied over years ( χ 2 = 108.401, df = 10, P < 0.0001), gradually increasing from 0.77% in 2009 to 8.47% in 2016–2017. Conclusions: New potential epidemiological scenarios are discussed according to a range of factors (e.g. environmental modifications, occurrence of competent insect vectors, transportation of infected animals to non-endemic areas, chemoprophylaxis or vector preventative measures), which may affect the current distribution. Overall, the results advocate for epidemiological surveillance programmes, more focussed preventative and control measures even in areas where few or no cases of both diseases have been diagnosed.

AI snapshot

Written from the paper’s full text.

TL;DR

This retrospective analysis of 90,633 canine serological tests from Italy (2009–2019) documents changing distributions of *Leishmania infantum* and *Dirofilaria immitis*, with canine leishmaniosis expanding in northern Italy and heartworm showing higher prevalence in central and southern regions/islands than in the historically endemic north. The authors argue for broader epidemiological surveillance and control measures across Italy.

Key findings

  • *L. infantum* positivity by macroarea was 28.2% in southern Italy and islands, 29.6% in central Italy, and 21.6% in northern Italy (χ² = 218.564, df = 2, P < 0.0001); *D. immitis* positivity was 2.83% in northern Italy, 7.75% in central Italy, and 4.97% in southern Italy and islands (χ² = 114.879, df = 2, P < 0.0001).
  • Heartworm positivity varied significantly over years (χ² = 108.401, df = 10, P < 0.0001), gradually increasing from 0.77% in 2009 to 8.47% in 2016–2017.
  • In northern Italy, *L. infantum* prevalence increased from 2.1% in 1999–2009 to 21.6% in 2009–2019; in Bologna province it rose from 6.6% (2007–2009) to 17.16% in this study.
  • The changing distribution patterns were not random: contingency analyses were significant for *L. infantum* (macroarea χ² = 486.62, df = 2, P < 0.0001; year χ² = 827.903, df = 10, P < 0.0001) and *D. immitis* (macroarea χ² = 104.545, df = 2, P < 0.0001; year χ² = 99.070, df = 10, P < 0.0001).

Methods

  • Retrospective analysis of two diagnostic reference centre databases totaling 90,633 serum samples from dogs in Italy: database A included 64,375 records (2009–2019), and database B included 26,258 records (2015–2019); exclusions were 78 and 70 samples with uncertain origin, plus 423 northern/central samples excluded due to transportation bias, and no anamnestic data were available.
  • Serological assays included ELISA tests (Novatec® for CanL, Dirocheck Zoetis® for HW; VetLine® Leishmania for CanL, Filarcheck 96® for HW) and an indirect semi-quantitative immunofluorescence test (MegaFLUO LEISH® for leishmaniosis).
  • Statistical analysis used weighted generalized linear models with a binomial distribution and fixed factors for macroarea/year and region/year, plus contingency analysis; distribution maps were generated with QGIS version 3.4.4-Madeira.

Limitations

  • Stated: the anamnesis of animals was not available, so travelling history from/to historically endemic areas and the effect of relocation of infected animals from southern to northern Italy could not be fully assessed.
  • Stated: *D. immitis* testing was low (10.5% of all requested serological tests), especially in southern regions; in southern Italy and islands, limited samples in 2009–2014 (n = 117) versus 2015–2019 (n = 1729) likely contributed to the non-significant year effect for *D. immitis* (χ² = 16.145, df = 10, P = 0.136).
  • Evident from the text: reliance on passive diagnostic databases may reflect clinician awareness and request behaviour rather than true prevalence, and uneven sample sizes plus missing data for several provinces limit geographic inference.

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

Integrity signals

Registry

Crossref · 10.1186/s13071-020-04063-9

Cites

32 of 32 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

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

  • Findingown data

    There was a significant difference in L. infantum prevalence between the study macroareas (χ2 = 218.564, df = 2, P < 0.0001).

    “Data showed a significant difference in L. infantum prevalence between the different study macroareas (χ2 = 218.564, df = 2, P < 0.0001)”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.
  • Findingown data

    D. immitis prevalence showed significant differences between the study macroareas (χ2 = 114.879, df = 2, P < 0.0001).

    “Dirofilaria immitis prevalence showed significant differences between the study macroareas (χ2 = 114.879, df = 2, P < 0.0001)”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.
  • Findingown data

    The distribution patterns of L. infantum and D. immitis in Italy are related to a significant relationship between positive test results, geographical provenience (macroarea), and study years (2009-2019).

    “Furthermore, our analyses showed that the distribution patterns of L. infantum and D. immitis in Italy are related to a significant relationship between L. infantum /D. immitis positive results of the tests, the geographical provenience (i.e. macroarea) and study years (2009–2019).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.
  • Findingown data

    The number of positive serum samples of L. infantum in northern Italy increased in the examined 10-year period (2009-2019) from 2.1% (1999-2009) to 21.6%.

    “Indeed, the number of positive serum samples of L. infantum in northern Italy increased in the examined 10 years’ period (2009–2019) from 2.1% (1999–2009; [1, 16]) to 21.6%.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [1] Otranto D, Capelli G, Genchi C. Changing distribution patterns of canine vector borne diseases in Italy: leishmaniosis vs. dirofilariosis. Parasit Vectors. 2009;2(Suppl. 1):S2. source

      Not checked in the free run.

    • cites [16] Maroli M, Rossi L, Baldelli R, Capelli G, Ferroglio E, Genchi C, et al. The northward spread of leishmaniasis in Italy: evidence from retrospective and ongoing studies on the canine reservoir and phlebotomine vectors. Trop Med Int Health. 2008;13:256–64. source

      Not checked in the free run.

    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.
  • Findingown data

    In the province of Bologna (Emilia Romagna), L. infantum seroprevalence increased from 6.6% (16 out of 245 animals examined in 2007-2009) to 17.16% (217 out of 1264 tests in this study).

    “For example, in the province of Bologna (Emilia Romagna) the seroprevalence increased from 6.6% (i.e. 16 out of 245 animals examined in the period 2007–2009 [17]) up to 17.16% (i.e. 217 out of 1264 tests in this study).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [17] Baldelli R, Piva S, Salvatore D, Parigi M, Melloni O, Tamba M, et al. Canine leishmaniasis surveillance in a northern Italy kennel. Vet Parasitol. 2011;179:57–61. source

      Not checked in the free run.

    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.
  • May combine two claims. 28
  • Classified as probably not a substantial claim. 5

  • May combine two claims.

    Findingown data

    In northern Italy, L. infantum prevalence showed significant differences over the study years (χ2 = 286.277, df = 10, P < 0.0001), being highest in 2012 and 2014 (33.51% and 27.27%, respectively).

    “In northern Italy, L. infantum prevalence showed significant differences over the study years (χ2 = 286.277, df = 10, P < 0.0001), being highest in 2012 and 2014 (i.e. 33.51% and 27.27%, respectively)”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    The study year significantly impacted L. infantum results in Italy (χ2 = 559.846, df = 10, P < 0.0001), with values > 30% in 2011, 2012, 2014, and 2015.

    “The impact of the study year on L. infantum results in Italy was also significant (χ2 = 559.846, df = 10, P < 0.0001), with values > 30% in 2011, 2012, 2014 and 2015.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In central Italy, D. immitis positive results were affected by study year (χ2 = 55.333, df = 10, P < 0.0001), showing values > 10% in 2016 (12.1%) and 2017 (13.32%).

    “Positive results for D. immitis were also affected by the study year (χ2 = 55.333, df = 10, P < 0.0001), showing values of > 10% in 2016 (i.e. 12.1%) and 2017 (i.e. 13.32%)”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In southern Italy and islands, L. infantum positive tests were significantly different among study years (χ2 = 201.963, df = 10, P < 0.0001), with values ranging from 24.55% (2017) to 50.66% (2011).

    “In southern Italy and islands, L. infantum positive tests were significantly different among the study years (χ2 = 201.963, df = 10, P < 0.0001), with values ranging from 24.55% (2017) to 50.66% (2011)”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In northern Italy, study year and region significantly impacted D. immitis results (χ2 = 56.954, df = 10, P < 0.0001; and χ2 = 40.555, df = 7, P < 0.0001, respectively), with the highest prevalence observed in 2016 (7.20%).

    “The study year and region significantly impacted the results of D. immitis in northern Italy (χ2 = 56.954, df = 10, P < 0.0001; and χ2 = 40.555, df = 7, P < 0.0001, respectively), with the highest prevalence observed in 2016 (7.20%)”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    D. immitis positivity significantly varied over years (χ2 = 108.401, df = 10, P < 0.0001), gradually increasing from 0.77% in 2009 to values ranging between 5.19-8.47% in 2016-2017.

    “HW positivity significantly varied over years (χ2 = 108.401, df = 10, P < 0.0001), gradually increasing from 0.77% in 2009 to 8.47% in 2016–2017.”
    • Also stated in: § Results · plain
      “On the whole Italian territory, the number of HW positive tests significantly varied over years (χ2 = 108.401, df = 10, P < 0.0001), gradually increasing from 0.77% in 2009 to values ranging between 5.19–8.47% in 2016–2017”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In northern Italy, the highest D. immitis prevalence rates were in Aosta Valley (11.36%), Trentino Alto Adige (7.41%), and Piedmont (6.29%), while the lowest was in Veneto (2.12%).

    “The highest prevalence rate of D. immitis were recorded in Aosta Valley(11.36%), Trentino Alto Adige (7.41%) and Piedmont (6.29%), while the lowest was found in Veneto (2.12%).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In southern Italy and islands, L. infantum results showed significant differences between regions (χ2 = 642.949, df = 6, P < 0.0001) with the highest values recorded in Molise (54.26%), Sicily (50.18%), and Sardinia (38.34%).

    “Leishmania infantum results in this macroarea also showed significant differences between regions (χ2 = 642.949, df = 6, P < 0.0001) with the highest values recorded in Molise (54.26%), Sicily (50.18%) and Sardinia (38.34%).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In central Italy, there were significant differences in D. immitis prevalence (χ2 = 80.975, df = 4, P < 0.0001) with the highest values recorded in Tuscany (11.48%) and Marche (7.84%).

    “Significant differences in the prevalence for D. immitis were noted in central Italy (χ2 = 80.975, df = 4, P < 0.0001, respectively) with the highest values recorded in Tuscany (11.48%) and Marche (7.84%).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    Overall L. infantum positivity in the tested samples was 28.2% in southern Italy and islands, 29.6% in central Italy, and 21.6% in northern Italy.

    “The overall results of the positive tested samples were 28.2% in southern Italy and islands, 29.6% in central Italy and 21.6% in northern Italy for L. infantum”
    • Also stated in: § Results · plain
      “with an overall positivity of 28.2% in southern Italy and islands, 29.68% in central Italy and 21.62% in northern Italy (Table 1, Fig. 2)”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In central Italy, L. infantum prevalence was more than 30% in 2012, 2014, 2015, and 2016, with the highest values in Lazio (38.52%), followed by Umbria (35.61%) and Abruzzo (34.10%).

    “It was more than 30% in 2012, 2014, 2015 and 2016 (Fig. 2), with the highest values in Lazio (38.52%), followed by Umbria (35.61%) and Abruzzo (34.10%).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In northern Italy, there were significant variations in L. infantum positive tests among regions (χ2 = 190.657, df = 7, P < 0.0001), with the highest values in Piedmont (28.93%), Trentino Alto Adige (27.59%), Aosta Valley (27.40%), and Friuli Venezia Giulia (27.17%).

    “Notably, significant variations in tests positive for L. infantum among the various northern Italy regions were recorded (χ2 = 190.657, df = 7, P < 0.0001), with the highest values in Piedmont, Trentino Alto Adige, Aosta Valley and Friuli Venezia Giulia (28.93%, 27.59%, 27.40% and 27.17%, respectively).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    Overall D. immitis positivity in the tested samples was 2.83% in northern Italy, 7.75% in central Italy, and 4.97% in southern Italy and islands.

    “2.83% in northern Italy, 7.75% in central Italy and 4.97% in southern Italy and islands for HW”
    • Also stated in: § Results · plain
      “being of 2.83% in northern Italy, 7.75% in central Italy and 4.97% in southern Italy and islands”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    In central Italy, both study year and region led to significant differences in L. infantum prevalence (χ2 = 371.252, df = 10, P < 0.0001; and χ2 = 609.769, df = 5, P < 0.0001, respectively).

    “In central Italy, both the study year and region led to significant differences in L. infantum prevalence (χ2 = 371.252, df = 10, P < 0.0001; and χ2 = 609.769, df = 5, P < 0.0001, respectively).”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    L. infantum was widely distributed throughout the Italian Peninsula, with a number of positive animals > 400 in the central (Lazio and Tuscany) and southern (Apulia and Basilicata) regions as well as in both islands (Sardinia and Sicily).

    “Leishmania infantum was widely distributed throughout the Italian Peninsula, with a number of positive animals > 400 in the central (Lazio and Tuscany) and southern (Apulia and Basilicata) regions as well as in both islands (Sardinia and Sicily).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    The highest percentage of positive D. immitis tests was registered in the central regions (Tuscany and Lazio) followed by the southern and northern regions with annual variation patterns throughout the observation period.

    “The highest percentage of positive tests of D. immitis was registered in the central regions (i.e. Tuscany and Lazio) followed by the southern and northern regions with annual variation patterns throughout the observation period (Fig. 3).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingcitation

    The cumulative prevalence of D. immitis infection greatly increased in central (7.7%) and southern Italy and islands (5%), being higher than in the North (2.8%), which was historically considered the sole endemic area.

    “On the other hand, the cumulative prevalence of D. immitis infection greatly increased in central (7.7%) and southern Italy and islands (5%), being higher than in the North (2.8%), which was historically considered the sole endemic area [1, 20].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [1] Otranto D, Capelli G, Genchi C. Changing distribution patterns of canine vector borne diseases in Italy: leishmaniosis vs. dirofilariosis. Parasit Vectors. 2009;2(Suppl. 1):S2. source

      Not checked in the free run.

    • cites [20] Genchi C, Solari Basano F, Marrone RV, Petruschke G. Canine and feline heartworm in Europe with special emphasis on Italy. In: Proceedings of the Heartworm Symposium ʼ98, 1–3 May, Tampa, Florida, USA; 1998. p. 75–82.

      Not checked in the free run.

    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    An overall lower number of samples was positive for D. immitis compared to L. infantum, with > 10 positive cases recorded in three provinces in northern Italy (Turin, Piedmont; Genova, Liguria; and Belluno, Veneto).

    “An overall lower number of samples was positive for D. immitis compared to L. infantum, with > 10 positive cases recorded in three provinces in the northern Italy (i.e. Turin, Piedmont; Genova, Liguria; and Belluno, Veneto).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Findingown data

    Clinicians' perception and awareness of the presence of CanL in non-endemic areas seem to be increased in the northern regions, with more than 21,545 tests performed, whereas the South remains the area with the largest number of tests requested.

    “In addition, clinicians’ perception and awareness of the presence of CanL in non-endemic areas seem to be increased in the northern regions, with more than 21,545 tests performed, whereas the South remains the area with the largest number of tests requested (Table 1).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.

  • May combine two claims.

    Premisecitation

    Earlier studies illustrated the islands to have a large number of diagnosed HW as they are suitable for Dirofilaria spp. to thrive.

    “Indeed, earlier studies illustrated the islands to have a large number of diagnosed HW [31] as they are suitable for Dirofilaria spp. to thrive [13].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [31] Genchi M, Rinaldi L, Venco L, Cringoli G, Vismarra A, Kramer L. Dirofilaria immitis and D. repens in dog and cat: a questionnaire study in Italy. Vet Parasitol. 2019;267:26–31. source

      Not checked in the free run.

    • cites [13] Otranto D, Brianti E, Gaglio G, Dantas-Torres F, Azzaro S, Giannetto S. Human ocular infection with Dirofilaria repens (Railliet and Henry, 1911) in an area endemic for canine dirofilariasis. Am J Trop Med Hyg. 2011;84:1002–4. source

      Not checked in the free run.

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

    Premisecitation

    Other studies reported cases of CanL and human visceral leishmaniasis diagnosed in the same area, along with their vectors, P. perniciosus and P. neglectus.

    “In addition, other studies reported cases of CanL and human visceral leishmaniasis diagnosed in the same area, along with their vectors, P. perniciosus and P. neglectus [25].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [25] Capelli G, Baldelli R, Ferroglio E, Genchi C, Gradoni L, Gramiccia M, et al. Monitoring of canine leishmaniasis in northern Italy: an update from a scientific network. Parassitologia. 2004;46:193–7.

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Based on the results, positive tests for L. infantum and D. immitis varied over the 2009-2019 period, also in comparison with data available from the prior decade (1999-2009).

    “Based on the results of this large dataset (n = 90,633) of serological assays presented herein, the positive tests for L. infantum and D. immitis varied over the last 10 years’ period (2009–2019), also in comparison with data available from the prior decade (1999–2009) [1].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [1] Otranto D, Capelli G, Genchi C. Changing distribution patterns of canine vector borne diseases in Italy: leishmaniosis vs. dirofilariosis. Parasit Vectors. 2009;2(Suppl. 1):S2. source

      Not checked in the free run.

    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based). May combine two claims.

    Interpretationreasoning

    The low prevalence of HW in Sicily and Sardinia could be explained by the small number of tests requested or no tests performed in many provinces from these islands.

    “The low prevalence of HW in Sicily and Sardinia could be explained by the small number of tests requested or no tests performed in many provinces from these islands.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.

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

    Study design and conductcitation

    A major hindrance of this study could be that the anamnesis of animals was not available (e.g., their travelling history from/to historically endemic areas for both diseases).

    “Conversely, a major hindrance of this study could be that the anamnesis of animals was not available (e.g. their travelling history from/to historically endemic areas for both diseases) [5, 22].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [5] Genchi C, Mortarino M, Rinaldi L, Cringoli G, Traldi G, Genchi M. Changing climate and changing vector-borne disease distribution: the example of Dirofilaria in Europe. Vet Parasitol. 2011;176:295–9. source

      Not checked in the free run.

    • cites [22] Brandonisio O, Carelli G, Ceci L, Consenti B, Fasanella A, Puccini V. Canine leishmaniasis in the Gargano promontory (Apulia, South Italy). Eur J Epidemiol. 1992;8:273–6. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    The number of cases positive for L. infantum has increased progressively in the past decade in the northern Italian regions, with an overall prevalence higher than that recorded in previous studies.

    “The results also indicate that the number of cases positive for L. infantum has increased progressively in the past decade in the northern Italian regions, with an overall prevalence higher than that recorded in previous studies [1, 17].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [1] Otranto D, Capelli G, Genchi C. Changing distribution patterns of canine vector borne diseases in Italy: leishmaniosis vs. dirofilariosis. Parasit Vectors. 2009;2(Suppl. 1):S2. source

      Not checked in the free run.

    • cites [17] Baldelli R, Piva S, Salvatore D, Parigi M, Melloni O, Tamba M, et al. Canine leishmaniasis surveillance in a northern Italy kennel. Vet Parasitol. 2011;179:57–61. source

      Not checked in the free run.

    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Premisecitation

    Hyperendemic D. immitis infection has been recorded in sheltered dogs from the Apulia region (southern Italy), with the highest prevalence of infection (44.2%) in Europe.

    “Hyperendemic D. immitis infection has been recorded in sheltered dogs from Apulia region (southern Italy) with the highest prevalence of infection (i.e. 44.2%) in Europe [30].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [30] Panarese R, Iatta R, Latrofa MS, Zatelli A, Ignjatović Ćupina A, Montarsi F, Pombi M, Mendoza-Roldan JA et al. Hyperendemic Dirofilaria immitis infection in sheltered dog population: an expanding threat in the Mediterranean regions. Int J Parasitol. 2020 in press. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Endemic foci of CanL in the same provinces of Veneto and Piedmont confirmed the epidemiological picture, with a competent vector of L. infantum (P. perniciosus) captured in entomological surveys performed in that area.

    “Endemic foci of CanL in the same provinces of Veneto [23] and Piedmont [24] confirmed the above mentioned epidemiological picture with a competent vector of L. infantum (i.e. P. perniciosus) captured in entomological surveys performed in that area [19].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [23] Vascellari M, Natale A, Schievenin E, Miatto A, Brino A, Frangipane Di Regalbono A, et al. Descrizione di un nuovo focolaio di leishmaniosi canina nella Regione Veneto. Veterinaria. 2005;3:25–9.

      Not checked in the free run.

    • cites [24] Biglino A, Bolla C, Concialdi E, Trisciuoglio A, Romano A, Ferroglio E. Asymptomatic Leishmania infantum infection in an area of northwestern Italy (Piedmont region) where such infections are traditionally nonendemic. J Clin Microbiol. 2010;48:131–6. source

      Not checked in the free run.

    • cites [19] Signorini M, Cassini R, Drigo M, di Regalbono A, Pietrobelli M, Montarsi F, et al. Ecological niche model of Phlebotomus perniciosus, the main vector of canine leishmaniasis in north-eastern Italy. Geospat Health. 2014;9:193–201. source

      Not checked in the free run.

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

    Premisecitation

    The southward changing pattern of HW has been detailed in previous studies.

    “The southward changing pattern of HW has been detailed in previous studies [26–29].”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [26] Di Cesare A, Castagna G, Meloni S, Milillo P, Latrofa S, Otranto D, et al. Canine and feline infections by cardiopulmonary nematodes in central and southern Italy. Parasitol Res. 2011;109:87–96. source

      Not checked in the free run.

    • cites [27] Giangaspero A, Marangi M, Latrofa MS, Martinelli D, Traversa D, Otranto D, et al. Evidences of increasing risk of dirofilarioses in southern Italy. Parasitol Res. 2013;112:1357–61. source

      Not checked in the free run.

    • cites [28] Del Prete L, Maurelli MP, Pennacchio S, Bosco A, Musella V, Ciuca L, et al. Dirofilaria immitis and Angiostrongylus vasorum: the contemporaneous detection in kennels. BMC Vet Res. 2015;11:305. source

      Not checked in the free run.

    • cites [29] Sauda F, Malandrucco L, Macrì G, Scarpulla M, De Liberato C, Terracciano G, Fichi G, et al. Leishmania infantum, Dirofilaria spp. and other endoparasite infections in kennel dogs in central Italy. Parasite. 2018;25:2. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationnone given

    The decreased prevalence of D. immitis infection in northern Italy regions could be a consequence of clinicians' awareness of the disease and thus of the continuous usage of chemoprophylactic programmes in this area.

    “The decreased prevalence of D. immitis infection in northern Italy regions could be a consequence of clinicians’ awareness of the disease and thus of the continuous usage of chemoprophylactic programmes in this area.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    L. infantum exposure has spread progressively in the past decades from the endemic southern regions towards northern regions, making the whole Italian Peninsula endemic for this infection.

    “Overall, L. infantum exposure has spread progressively in the past decades from the endemic southern regions towards northern regions, making the whole Italian Peninsula endemic for this infection.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

  • May combine two claims.

    Interpretationown data

    Given the number of tests requested, the overall clinicians' awareness in northern Italy is increasing for CanL and diminishing for HW.

    “Moreover, given the number of tests requested, the overall clinicians’ awareness in northern Italy is increasing for CanL and diminishing for HW.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.

  • May combine two claims.

    Interpretationown data

    Overall, results highlighted changing distribution patterns of CanL vs HW in Italy over a 10-year period (2009-2019) in which the number of cases of CanL has increased in the northern Italy regions, and HW has endemic foci in the central and southern Italy and in islands.

    “Overall, results highlighted the changing distribution patterns of CanL vs HW in Italy over a 10-year period (2009–2019) in which the number of cases of CanL has increased in the northern Italy regions, and HW has endemic foci in the central and southern Italy and in islands.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.
    • Rests on an assumption: The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.
    • Rests on an assumption: The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.
32 of 32

  • The paper relies on this without support.

    The serological samples submitted to the two diagnostic centres are representative of the canine population in each Italian macroarea.

    “Databases from two diagnostic reference centres (hereafter reported as database A and B) were analysed (total number of serum samples = 90,633).”

  • The paper relies on this without support.

    The geographical origin of the samples reflects the location where the dogs acquired L. infantum or D. immitis infection.

    “Conversely, a major hindrance of this study could be that the anamnesis of animals was not available (e.g. their travelling history from/to historically endemic areas for both diseases) [5, 22].”

  • The paper relies on this without support.

    The diagnostic tests used in database A accurately detect L. infantum exposure and D. immitis infection.

    “Different serological (Novatec® kit for CanL and Dirocheck Zoetis® for HW) enzyme-linked immune sorbent assay (ELISA) tests were used.”

  • The paper relies on this without support.

    The absence of anamnesis (e.g., travelling history) does not substantially bias the observed distribution patterns.

    “However, for all included samples in both datasets no anamnestic data were available.”
4 of 4

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • A study by Mendoza-Roldan et al. between 2009-2019 showed that the number of heartworm-infected dogs significantly varied over years, gradually increasing from 0.77% in 2009 to 5.19-8.47% in 2016-2017.

    “Finally, a study conducted by Mendoza-Roldan et al. [41] between 2009–2019 showed that the number of heartworm-infected dogs significantly varied over years, gradually increasing from 0.77% in 2009 to values ranging between 5.19–8.47% in 2016–2017.”

    From What has happened to heartworm disease in Europe in the last 10 years? (2022) · cites this paper as [41]

  • In Italy, prevalence in the north is decreasing while in the centre and south it is increasing.

    “Moreover, the results showed that prevalence in the north is decreasing, while in the centre and south of the country, it is increasing, which corroborated studies previously carried out by other authors.”

    From What has happened to heartworm disease in Europe in the last 10 years? (2022) · cites this paper as [41]

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.

  • Southern share of Leishmania tests is overstated

    Minor

    The table gives 32,610 southern tests out of 80,309 L. infantum tests, or about 40.6%, rather than 37.7%.

    Reported 37.7 · recomputed 40.605661

  • Central heartworm positivity does not match its counts

    Minor

    The reported 243 positive tests among 3,119 central tests give 7.79%, not the table's 7.5%. The 7.75% stated in the Results is also inconsistent with these counts.

    Reported 7.5 · recomputed 7.790959

  • Heartworm distribution is cited to the CanL figure

    Minor

    The discussion cites Fig. 4 for clustered D. immitis infection, but Fig. 4 is captioned as the CanL distribution map. The HW distribution map is labeled Fig. 5.

  • Northern share of Leishmania tests is understated

    Minor

    The table gives 21,545 northern tests out of 80,309 L. infantum tests, or about 26.8%, rather than 24.7%.

    Reported 24.7 · recomputed 26.827628

  • Central share of Leishmania tests is understated

    Minor

    The table gives 26,128 central tests out of 80,309 L. infantum tests, or about 32.5%, rather than 31%.

    Reported 31 · recomputed 32.534336

  • Leishmania distribution is cited to the heartworm figure

    Minor

    The discussion cites Fig. 3 for provinces with clustered L. infantum exposure, but Fig. 3 is captioned as a D. immitis prevalence plot. The CanL distribution map is labeled Fig. 4.

6 of 6

Cites

Flagged first, then by citations

Research works printed but not linked: 2

  1. QGIS Development Team. QGIS geographic information system. Open Source Geospatial Foundation Project, Versão. 2015;2:7.
  2. Genchi C, Solari Basano F, Marrone RV, Petruschke G. Canine and feline heartworm in Europe with special emphasis on Italy. In: Proceedings of the Heartworm Symposium ʼ98, 1–3 May, Tampa, Florida, USA; 1998. p. 75–82.

Cited by

Sorted by citations

Related

Authors
Mendoza-Roldan, J., Benelli, G., Panarese, R., Iatta, R., Furlanello, T., Beugnet, F., Zatelli, A., & Otranto, D.
Affiliations
  • University of Pisa (IT)
  • University of Bari Aldo Moro (IT)
  • Bu-Ali Sina University (IR)
Corresponding author
Otranto, Domenico
ORCID
Venue
Parasites & Vectors
Publisher
Springer Science and Business Media LLC
Published
2020-04-15
Volume
13
Issue
1
Pages
193-193
ISSN
1756-3305 (ISSN-L)
DOI
10.1186/s13071-020-04063-9
PMC
PMC7161282
OpenAlex
W3015911297
Cited by
119
References
32
Citations by year
2026: 9 · 2025: 19 · 2024: 16 · 2023: 12 · 2022: 26 · 2021: 25 · 2020: 11
FWCI
13.87
Type
journal article
Language
en
Open access
Licence
Locations
  • Parasites & Vectors (publishedVersion, cc-by)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • CINECA IRIS Institutional Research Information System (University of Bari Aldo Moro) (submittedVersion, cc-by)
  • CINECA IRIS Institutional Research Information System (University of Bari Aldo Moro) (submittedVersion)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Research on Leishmaniasis Studies
  • Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
  • Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
Keywords
canine leishmaniasis, heartworm disease, Leishmania infantum, Dirofilaria immitis, disease distribution, new foci, seroprevalence, Italy, disease surveillance, environmental change
MeSH terms
Animals, Dirofilaria immitis, Dirofilariasis, Dog Diseases, Dogs, Insect Vectors, Italy, Leishmaniasis, Psychodidae, Serologic Tests, Zoonoses, Leishmania infantum

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.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

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