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Cited by 19Helminth infection and controlParasitic infections in humans and animalsParasite Biology and Host Interactions

Distribution of Parasitic Helminths in the Small Intestine of the Red Fox (Vulpes vulpes)

Open access
Karamon, Jacek, Sroka, Jacek, Dąbrowska, Joanna, Bilska-Zając, Ewa, Skrzypek, Katarzyna, Różycki, Mirosław, Zdybel, Jolanta, Cencek, Tomasz·2020·Pathogens
DOI 10.3390/pathogens9060477PMC PMC7350372
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Abstract

The aim of the study was to analyze the distribution of the main groups of parasitic helminths within the small intestine of the red fox on the example of animals coming from eastern Poland. Two hundred and sixteen red foxes shot in eastern Poland were used in the investigation. Before examination, each small intestine was divided into three equal parts: anterior (A), middle (M), and posterior (P). Each part was examined separately with the sedimentation and counting technique. Six different types of intestinal parasites were detected: Alaria alata (78.7%), Mesocestoides spp. (78.2%), hookworms (72.7%), Taenia spp. (53.2%), Toxocara/Toxascaris (43.1%), and Echinococcus multilocularis (18.5%). Alaria alata was most often found in A and in the only-A variant. Taenia spp. and Toxocara/Toxascaris occurred often in A and were the second (after A. alata) parasites in terms of frequency occurring in the only-A variant. Mesocestoides spp. was most commonly located in M. Parasites with predilection sites located mainly in M and P were E. multilocularis and hookworms. In all parasite species, the variant covering the entire intestine (A + M + P) was found in samples with a higher intensity compared to variants limited to one or two fragments. Our investigation, as one of the few of its type, conducted a comprehensive analysis of the distribution of intestinal helminths in the small intestine of the red fox. It showed significant differences in the distribution of parasitic helminths in the small intestine of the red fox. Determining typical predilection sites for parasites in the intestine can be helpful in creating effective diagnostic methods.

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Written from the paper’s full text.

TL;DR

This study examined the distribution of intestinal helminths in the small intestines of 216 red foxes from eastern Poland, finding significant species-specific predilection sites along the anterior, middle, and posterior thirds. It reports high overall infection (215/216, 99.5%) and shows that heavier infections tend to occupy the entire small intestine.

Key findings

  • Six parasite groups were detected: *Alaria alata* (78.7%), *Mesocestoides* spp. (78.2%), hookworms (72.7%), *Taenia* spp. (53.2%), *Toxocara/Toxascaris* (43.1%), and *Echinococcus multilocularis* (18.5%).
  • *A. alata* was predominantly anterior: 99.4% of positive foxes had it in the anterior part, and 70.6% had the only-A distribution. *Taenia* spp. and *Toxocara/Toxascaris* also favored the anterior part, with only-A distributions of 49.6% and 47.3%, respectively.
  • *Mesocestoides* spp. was most often in the middle part (92.9%), with dominant variants A + M + P (30.2%), M + P (28.4%), and only M (21.3%). *E. multilocularis* and hookworms favored middle/posterior sites: *E. multilocularis* occurred in the posterior part in 92.5% and had an only-P variant in 20%; hookworms occurred in middle (82.8%) and posterior (73.2%) parts, most often as M + P (40.1%).
  • For all parasite species, the A + M + P variant occurred in samples with higher intensity than variants limited to one or two fragments. Positive intensity correlations were found between *Mesocestoides* and *E. multilocularis* (rs = 0.151497), *Mesocestoides* and *Taenia* (rs = 0.264254), *Mesocestoides* and hookworms (rs = 0.171528), and *A. alata* and hookworms (rs = 0.135900); no significantly negative correlations were found.

Methods

  • Two hundred and sixteen red foxes shot in Lubelskie Province, eastern Poland, from 2007 to 2008 were used; samples came from an official anti-rabies vaccination survey and had been analyzed previously only for *E. multilocularis*.
  • Each small intestine was divided into three equal parts—anterior (A), middle (M), and posterior (P)—and each part was examined separately using the sedimentation and counting technique after storage at below −70 °C for at least two weeks.
  • Statistical comparisons used chi-square tests with Bonferroni correction, Kruskal–Wallis tests with Bonferroni correction, and Spearman’s rank-order correlation; significance was set at p < 0.05.

Limitations

  • The paper does not include a dedicated limitations section. It states that the authors lacked additional data such as age, health condition, or eating behavior, and that hookworm species were not identified; *Taenia* spp. and *Toxocara/Toxascaris* were also analyzed together rather than to species.
  • Evident from the text: the study is cross-sectional and limited to one region of Poland, uses samples collected in 2007–2008, and analyzes parasite distribution only among infected animals, so it cannot establish temporal trends or causal interactions.

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

Integrity signals

Registry

Crossref · 10.3390/pathogens9060477

Cites

47 of 47 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

26 of 58 cited sources checked · 14 supported · 0 flagged · accuracy not yet measured

  • Premisecitation

    Similar correlations connected with regions were observed in different studies conducted in Poland.

    “Similar correlations connected with regions were observed in different studies conducted in Poland [21,23,33].”
    Quote in the paperNot a substantial claim2 of 3 sources checked
    • cites [21] Tylkowska, 2018, The presence of Alaria alata fluke in the red fox (Vulpes vulpes) in north-western Poland, Jpn. J. Vet. Res. source
    • cites [23] Karamon, 2016, Intestinal helminths of raccoon dogs (Nyctereutes procyonoides) and red foxes (Vulpes vulpes) from the Augustow Primeval Forest (north-eastern Poland), J. Vet. Res. source
    • cites [33] Borecka, 2007, Prevalence of Echinococcus multilocularis tapeworm in red foxes in central Poland, Med. Weter.
  • Premisecitation

    In other parts of Europe, the percentage of A. alata infected foxes differs depending on the investigation and region, from very high to moderate and low to areas where these trematodes were not detected.

    “In other parts of Europe, the percentage of A. alata infected foxes differs depending on the investigation (and region) from very high [3,34], moderate, and low [1,8,12,18,19,35] to areas where these trematodes were not detected [17,36,37].”
    Quote in the paperNot a substantial claim4 of 10 sources checked
    • cites [3] Sarkunas, 2012, Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania, Parasitology source
    • cites [34] Ozolina, 2018, The host age related occurrence of Alaria alata in wild canids in Latvia, Parasitol. Res. source
    • cites [1] Franssen, F., Nijsse, R., Mulder, J., Cremers, H., Dam, C., Takumi, K., and van der Giessen, J. (2014). Increase in number of helminth species from Dutch red foxes over a 35-year period. Parasites Vectors, 7. source
    • cites [8] Fiocchi, 2016, Helminth parasites of the red fox Vulpes vulpes (L., 1758) and the wolf Canis lupus italicus Altobello, 1921 in Emilia-Romagna, Italy, Ital. J. Zoolog. source

      Citation [34] is attached to the claim of very high A. alata infection in foxes. The indexed Abstract reports A. alata among parasites found in foxes in Emilia-Romagna, but gives no infection percentage for that species; its 91.2% figure is for parasites overall. Searches for A. alata prevalence and very high infection found no passage establishing the attributed level. (LLM, conf=0.72)

      Experimental — accuracy not yet measured
    • cites [12] Schuster, 2017, A comparative study of helminths of raccoon dogs (Nyctereutes procynoides) and red foxes (Vulpes vulpes) sharing the same territory, Asian Pac. J. Trop. Dis. source
    • cites [18] Manke, 1998, Parasitological studies of red foxes (Vulpes vulpes L.) in the northern districts of Schleswig-Holstein, Tierarztl. Umschau.

      Not checked in the free run.

    • cites [19] Halasa, 2014, Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark, Acta Parasitol.

      Not checked in the free run.

    • cites [35] Murphy, 2012, The prevalence and distribution of Alaria alata, a potential zoonotic parasite, in foxes in Ireland, Parasitol. Res. source
    • cites [17] Smith, 2003, Prevalence of zoonotic important parasites in the red fox (Vulpes vulpes) in Great Britain, Vet. Parasitol. source
    • cites [36] Jankovska, 2016, Parasites with possible zoonotic potential in the small intestines of red foxes (Vulpes vulpes) from Northwest Bohemia (CzR), Helminthologia source
  • Premisecitation

    Prevalence of A. alata strongly depends on the region and presence of water reservoirs.

    “Prevalence of A. alata strongly depends on the region and presence of water reservoirs (necessary for the development of intermediate hosts).”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [14] Karamon, 2018, Prevalence of intestinal helminths of red foxes (Vulpes vulpes) in central Europe (Poland): A significant zoonotic threat, Parasites Vectors source
  • Study design and conductown data

    The analysis of all Taenia tapeworms together without distinguishing species makes it hard to conclude definitely about regional differences.

    “It is hard to conclude definitely because we analyzed all tapeworms from Taenia genus together without distinguishing species (e.g., T. crassiceps, T. pisiformis, T. polyacantha, T. hydatigena, and T. taeniaeformis) [1,8,16] which have different lifecycles with various intermediate hosts.”
    Quote in the paperSubstantial claim2 of 3 sources checked
    • cites [1] Franssen, F., Nijsse, R., Mulder, J., Cremers, H., Dam, C., Takumi, K., and van der Giessen, J. (2014). Increase in number of helminth species from Dutch red foxes over a 35-year period. Parasites Vectors, 7. source

      The Results (Molecular characterisation of intestinal parasites) distinguish T. crassiceps from T. polyacantha, and Table 1 lists intermediate hosts for T. crassiceps. The paper does not say that pooling Taenia species makes regional differences hard to assess, nor does the cited evidence establish the differing lifecycles of all five species listed. The statement that tapeworms were pooled describes the citing authors’ own analysis, not this source’s. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites [8] Fiocchi, 2016, Helminth parasites of the red fox Vulpes vulpes (L., 1758) and the wolf Canis lupus italicus Altobello, 1921 in Emilia-Romagna, Italy, Ital. J. Zoolog. source

      The passages in our indexed copy are a repository record listing an accepted manuscript, not the manuscript’s text (repository entry, no page number). Searches for the named Taenia species, intermediate hosts, and regional differences found no passage addressing whether grouping species limits the conclusion. (LLM, conf=0.70)

      Experimental — accuracy not yet measured
    • cites [16] Posedi, 2013, Intestinal parasites of the red fox (Vulpes vulpes) in Slovenia, Acta. Vet. Hung. source
  • Interpretationcitation

    The prevalence of Taenia spp. in the study (53.2%) is similar to that observed in southern, northern, northeastern, and southeastern Poland.

    “This result is similar to the prevalence observed in southern, northern, northeastern, and southeastern Poland [14].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [14] Karamon, 2018, Prevalence of intestinal helminths of red foxes (Vulpes vulpes) in central Europe (Poland): A significant zoonotic threat, Parasites Vectors source
  • May combine two claims. 40
  • Classified as probably not a substantial claim. 9
  • The quote only partly states this claim. 2

  • May combine two claims.

    Premisecitation

    Free-living red foxes are generally infected with more than one species of intestinal helminths, most often three or four coinfecting parasites.

    “It must be stressed that free-living red foxes are generally infected with more than one species of intestinal helminths, most often three or four coinfecting parasites [1,14,23].”
    Quote in the paperSubstantial claim3 of 3 sources checked
    • cites [1] Franssen, F., Nijsse, R., Mulder, J., Cremers, H., Dam, C., Takumi, K., and van der Giessen, J. (2014). Increase in number of helminth species from Dutch red foxes over a 35-year period. Parasites Vectors, 7. source

      The Results section, “Multiple infections per fox” (page unavailable), reports frequent coinfection among the Dutch foxes studied. But three to four coinfections is the peak reported for males; younger females peak at two to three. The count also covers helminth species generally, not only intestinal helminths, so it does not establish three or four intestinal species as the usual pattern for free-living red foxes generally. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
    • cites [14] Karamon, 2018, Prevalence of intestinal helminths of red foxes (Vulpes vulpes) in central Europe (Poland): A significant zoonotic threat, Parasites Vectors source
    • cites [23] Karamon, 2016, Intestinal helminths of raccoon dogs (Nyctereutes procyonoides) and red foxes (Vulpes vulpes) from the Augustow Primeval Forest (north-eastern Poland), J. Vet. Res. source

      The Results report that only 4.6% of the red foxes studied had one parasite type and that three types were the most frequent count (43.9%). The Discussion says most animals had two, three, or four parasite types. These findings come from the Augustów Primeval Forest; they do not establish that free-living red foxes generally are most often infected with three or four. (LLM, conf=0.83)

      Experimental — accuracy not yet measured

  • May combine two claims.

    Interpretationcitation

    The prevalence of Mesocestoides spp. in the studied foxes (78.2%) is similar to the mean prevalence in Poland (84.1%) and to the prevalence in southwest Poland (77.3%).

    “The percentage of infected foxes is similarly high as in the study conducted recently in different regions of Poland [14] (mean prevalence 84.1%), and it was especially close to the prevalence in the southwest region (77.3%) [14] directly bordering the area investigated in the present study.”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [14] Karamon, 2018, Prevalence of intestinal helminths of red foxes (Vulpes vulpes) in central Europe (Poland): A significant zoonotic threat, Parasites Vectors source

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

    Premisecitation

    The authors of the cited paper concluded that this type of interaction is observed relatively often in experimental infections; however, in wild animal populations, it occurs very rarely.

    “The authors of this paper concluded that this type of interaction is observed relatively often in experimental infections; however, in wild animal populations, it occurs very rarely [24,25].”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [24] Behnke, 2005, Do the helminth parasites of wood mice interact?, J. Anim. Ecol. source

      The Discussion (page unavailable in our copy) contrasts well-established interactions in laboratory rodent infections with weak field evidence and concludes that quantitative interactions are not dominant in the studied wild wood-mouse communities. It does not conclude that interactions occur very rarely in wild animal populations generally; it explicitly notes interactions in wild rodents and an important role for them in some bird communities. (LLM, conf=0.88)

      Experimental — accuracy not yet measured
    • cites [25] Behnke, 2001, Interactions involving intestinal nematodes of rodents experimental and field studies, Parasitology source

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

    Interpretationcitation

    The vast majority of hookworms detected in the study belonged to Uncinaria stenocephala.

    “In our investigation, species of these helminths were not identified, but previous studies carried out in Poland [20,31,41,42] and Europe [1,17,18,19] may suggest that the vast majority of them belonged to Uncinaria stenocephala.”
    Quote in the paperNot a substantial claim1 of 8 sources checked
    • cites [20] Szczepaniak, 2018, Determining the occurrence of the Uncinaria stenocephala and Ancylostoma caninum nematode invasion in dogs in Poland, with special emphasis on the Lublin region, Med. Weter.

      Not checked in the free run.

    • cites [31] Borecka, 2009, Prevalence of zoonotic helminth parasites of the small intestine in red foxes from central Poland, Med. Weter.
    • cites [41] Ramisz, 2003, Fauna of gastro-intestinal parasites in red foxes in Western Poland, Med. Weter.

      Not checked in the free run.

    • cites [42] Gorski, 2006, Molecular and morphological comparison of hookworms from genus Uncinaria invading red fox (Vulpes vulpes) and dog (Canis familiaris), Wiad. Parazytol.
    • cites [1] Franssen, F., Nijsse, R., Mulder, J., Cremers, H., Dam, C., Takumi, K., and van der Giessen, J. (2014). Increase in number of helminth species from Dutch red foxes over a 35-year period. Parasites Vectors, 7. source

      The Results (Tables 1 and 2; page unavailable) identify Uncinaria stenocephala in Dutch red foxes and list no other hookworm species, supporting the citing sentence’s tentative suggestion. The paper reports prevalence among foxes, however, not the proportion of hookworms belonging to that species in the citing authors’ investigation; it cannot establish the claimed ‘vast majority’ there. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites [17] Smith, 2003, Prevalence of zoonotic important parasites in the red fox (Vulpes vulpes) in Great Britain, Vet. Parasitol. source
    • cites [18] Manke, 1998, Parasitological studies of red foxes (Vulpes vulpes L.) in the northern districts of Schleswig-Holstein, Tierarztl. Umschau.

      Not checked in the free run.

    • cites [19] Halasa, 2014, Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark, Acta Parasitol.

      Not checked in the free run.

  • May combine two claims.

    Findingown data

    The most frequent Toxocara/Toxascaris distribution variant was only A (47.3%), significantly more frequent than all other variants.

    “The most frequent variant of distribution for Toxocara/Toxascaris was only A (47.3%), and it was significantly more frequent than all other variants: : A + M + P (χ2 = 40.01, p < 0.0001), A + M (χ2 = 11.37, p = 0.0007), M + P (χ2 = 55.04, p < 0.0001), A + P (χ2 = 48.55, p < 0.0001), only M (χ2 = 19.29, p < 0.0001), and only P (χ2 = 42.71, p < 0.0001).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Statistical comparisons of A. alata intensities between distribution variants showed significant differences (H = 36.89, p < 0.0001) but only between A + M + P (mean 362.5) and only-A (mean 46.0).

    “Statistical comparisons of intensities between distribution variants showed significant differences (H = 36.89, p < 0.0001) but only between A + M + P (mean intensity 362.5) and the only-A variant (mean intensity 46.0) (p < 0.0001) (Table 4).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    For Taenia, the A + M variant was the second most frequent and was significantly higher than A + M + P, M + P, A + P, only M, and only P.

    “The presence in the anterior and middle parts together (A + M) was the second most frequent variant; it was significantly higher than A + M + P (χ2 = 11.38, p = 0.0007), M + P (χ2 = 18.26, p < 0.0001), A + P (χ2 = 14.52, p = 0.0001), only M (χ2 = 16.31, p = 0.0001), and only P (χ2 = 25.20, p < 0.0001) (Figure 1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    E. multilocularis occurred most frequently in the posterior part (P) (92.5%), significantly higher than in the anterior part (A) (57.5%).

    “Echinococcus multilocularis tapeworms occurred most frequently in the posterior part of the intestine (P) (92.5%), and this was significantly higher than in the anterior part (A) (57.5%) (χ2 = 52.38, p = 0.0008).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    For Toxocara/Toxascaris, the next most frequent variants were A + M (23.7%) and only M (17.2%), with no significant differences between them.

    “Next in frequency was the A + M (23.7%) and only M (17.2%) variants without significant differences between them.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The A + P variant was observed very rarely in each parasite (from 0.6% to 6.1%), with no statistical differences between species.

    “This combination was observed very rarely in the case of each parasite (from 0.6% to 6.1%), and no statistical differences between species were noted.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the middle part, three parasite species (E. multilocularis, Mesocestoides, and hookworms) were most often found, with no significant differences between them, and all occurred significantly more frequently than other parasites.

    “In the middle part, three parasite species (E. multilocularis, Mesocestoides, and hookworms without significant differences between them) were most often found; all of them occurred significantly more frequently in this part than other parasites.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The three dominant Mesocestoides distribution variants were A + M + P (30.2%), M + P (28.4%), and only M (21.3%), with no significant differences between them.

    “There were three dominant distribution variants of Mesocestoides, A + M + P (30,2%), M + P (28.4%), and only M (21.3%), without significant differences between them.”
    Quote in the paperNot a substantial claim

  • The quote only partly states this claim.

    Findingown data

    A. alata occurrence in the anterior part was significantly higher than in the middle (26.5%) and posterior (10.6%) parts.

    “The occurrence in the anterior (A) part was significantly higher than in the other parts: M (χ2 = 190.77, p < 0.0001) and P (χ2 = 267.38, p < 0.0001).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The most frequent Taenia distribution variant was only A (49.6%), significantly higher than all other variants.

    “The most frequent variant of distribution for Taenia spp. was only A (49.6%), and it was significantly higher than all other variants: A + M + P (χ2 = 46.94, p < 0.0001), A + M (χ2 = 13.54, p = 0.0002), M + P (χ2 = 57.43, p < 0.0001), A + P (χ2 = 51.98, p < 0.0001), only M (χ2 = 54.65, p < 0.0001), and only P (χ2 = 66.48 p < 0.0001).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Mesocestoides tapeworms were found most frequently in the middle part (92.9%), significantly higher than in the posterior (63.9%) and anterior (45.0%) parts.

    “Mesocestoides tapeworms were found most frequently in the middle part (92.9%) with a significantly higher incidence than that in the posterior (63.9%) (χ2 = 41.95, p < 0.0001) and anterior parts (45.0%) (χ2 = 90.64, p < 0.0001).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Taenia tapeworms occurred most often in the anterior part (87.0%), significantly more frequent than in the middle (43.5%) and posterior (20.0%) parts.

    “Tapeworms of the Taenia genus occurred most often in the anterior part of the intestine (87.0%) and was significantly more frequent than in the middle (43.5%) (χ2 = 47.92, p < 0.0001) and in the posterior parts (20.0%) (χ2 = 103.61, p < 0.0001).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    The only-A variant was observed most frequently in A. alata infection (70.6%), significantly more often than in all other parasites.

    “This variant was observed most frequently in A. alata infection (70.6% of A. alata positive intestines had these flukes localized only in the anterior part), significantly more often than in case of all other parasites: E. multilocularis (χ2 = 63.03, p < 0.0001), Mesocestoides (χ2 = 170.62, p < 0.0001), Taenia spp. (χ2 = 12.88, p = 0.0003), hookworms (χ2 = 154.19, p < 0.0001), and Toxocara/Toxasca”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Intensity of E. multilocularis was similar in each part, with no significant differences.

    “Intensity of E. mutlilocularis was similar in each part, and there were no significant differences (Table 3).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the middle part, E. multilocularis differed significantly from A. alata, Taenia spp., and Toxocara/Toxascaris.

    “E. multilocularis differed significantly from A. alata (χ2 = 37.68, p < 0.0001), Taenia spp. (χ2 = 14.46, p = 0.0001), and Toxocara/Toxascaris (χ2 = 11.63, p = 0.0007).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    A. alata was detected more frequently in the entire intestine (A + M + P) compared to M + P, only M, and only P.

    “Moreover, A. alata was detected more frequently in the entire intestine (A + M + P) compared to M + P (χ2 = 14.60, p = 0.0001), only M (χ2 = 10.04, p < 0.0015), and only P (χ2 = 14.60, p = 0.0001) (Figure 1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The A + M + P variant was most often observed in E. multilocularis infection (55.0%), significantly more frequently than in A. alata, Mesocestoides, Taenia spp., hookworms, and Toxocara/Toxascaris infections.

    “The variant of distribution in the entire intestine was most often observed in the case of E. multilocularis infection (55.0%). It was significantly more frequently noted in this tapeworm than in cases of A. alata (χ2 = 49.86, p < 0.0001), Mesocestoides (χ2 = 8.77, p = 0.0031), Taenia spp. (χ2 = 38.38, p < 0.0001), hookworms (χ2 = 19.33, p < 0.0001), and Toxocara/Toxascaris (χ2 = 39.56, p < 0.0001”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the only-A variant, Taenia spp. (49.6%) and Toxocara/Toxascaris (47.3%) were the next most frequent and were observed in similar percentages.

    “Next, two parasite infections observed very often in this variant of distribution (in similar percentage) were Taenia spp. (49.6%) and Toxocara/Toxascaris (47.3%).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the only-M variant, Mesocestoides spp. and hookworms occurred significantly more often than Taenia spp.

    “Moreover, Mesocestoides spp. and hookworms occurred only in the middle part significantly more often than Taenia spp. (χ2 = 12.80, p = 0.0003; χ2 = 12.24, p = 0.0005, respectively).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Hookworm intensity in the A + M + P variant was significantly higher than in the only-A, only-M, and only-P variants.

    “Intensity in the A + M + P variant was significantly higher than the only-A (p = 0.0003), only-M (p < 0.0001), and only-P (p = 0.0009) variants.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    For Mesocestoides, the A + M variant was significantly higher than A + P and only A.

    “Moreover, the A + M variant was significantly higher than A + P (χ2 = 11.26, p < 0.0001) and only A (χ2 = 14.00, p = 0.0002) (Figure 1).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In the posterior part, the proportion and significant differences between parasites were similar to those in the middle part, with the same three species dominant.

    “The proportion (and significant differences) between parasites in the posterior part was similar to that in the middle; the same three parasites species were dominant.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    A. alata was detected in the anterior part in almost all infected foxes (99.4%); only one had no A. alata in the anterior part.

    “Alaria alata were detected in the anterior part of intestine (A) in almost all foxes positive for this infection (99.4%); only one had no A. alata flukes in the anterior part.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    For E. multilocularis, there were no significant differences in occurrence between M and A and between M and P.

    “There were no significant differences between M and A and between M and P (Table 2).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Mesocestoides was the next parasite most widely distributed in the intestine (30.2%); the A + M + P variant occurred significantly more often in Mesocestoides infection than in A. alata, Taenia spp., and Toxocara/Toxascaris infections.

    “Mesocestoides was the next parasite most widely distributed in the intestine (30.2%); the A + M + P variant significantly more often occurred in Mesocestoides infection than in infections of A. alata (χ2 = 24.93, p < 0.0001), Taenia spp. (χ2 = 19.20, p < 0.0001), and Toxocara/Toxascaris (χ2 = 20.51, p < 0.0001).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The M + P variant was noted most frequently in hookworms, Mesocestoides spp., and E. multilocularis, with no statistical differences between them.

    “This range of distribution was noted most frequently in three species: hookworms, Mesocestoides spp., and E. multilocularis; there were no statistical differences between them.”
    Quote in the paperNot a substantial claim

  • The quote only partly states this claim.

    Findingown data

    Intestinal helminths were detected in 215 of 216 red foxes (99.5%) from eastern Poland.

    “Intestinal helminths were detected in 215 (99.5%) red foxes.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sample of 216 red foxes is representative of the red fox population in eastern Poland.

  • May combine two claims.

    Findingown data

    For A. alata, the A + M variant was the next most frequent and occurred significantly more often than M + P, A + P, only M, and only P.

    “Next for frequency was the A + M variant, which occurred significantly more often than M + P (χ2 = 31.94, p < 0.0001), A + P (χ2 = 21.53, p < 0.0001), only M (χ2 = 29.01, p < 0.0001), and only P (χ2 = 31.94, p < 0.0001).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Toxocara/Toxascaris nematodes occurred most often in the anterior part (78.5%), significantly more frequent than in the middle (46.2%) and posterior (11.8%) parts.

    “Toxocara/Toxascaris nematodes occurred most often in the anterior part of the intestine (78.5%) significantly more frequent than in the middle (46.2%) (χ2 = 20.62, p < 0.0001) and in the posterior parts (11.8%) (χ2 = 83.45, p < 0.0001).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Both Taenia spp. and Toxocara/Toxascaris occurred more often in the anterior part of the intestine than in the middle and posterior parts.

    “Both parasites occurred more often in the anterior part of intestine than in the middle and posterior parts.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Variant A + M + P was most frequently found in E. multilocularis infection: in more than half of E. multilocularis-positive samples, these tapeworms were found in all three parts together.

    “Variant A + M + P was most frequently found in E. multilocularis infection: in more than half of E. multilocularis-positive samples, these tapeworms were found in all three parts together.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    For Taenia spp. and Toxocara/Toxascaris, occurrence in the middle part was significantly higher than in the posterior part.

    “Additionally, occurrence in the middle part was significantly higher than in the posterior part.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    In this study, the most prevalent parasites were A. alata, Mesocestoides spp., and hookworms (similar high mean prevalence from 73% to 79%), followed by Taenia spp., Toxocara, and E. multilocularis.

    “In our study, the most prevalent parasites were A. alata, Mesocestoides spp., and hookworms (with similar high mean prevalence from 73% to 79%) followed by Taenia spp., Toxocara, and E. multilocularis.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The sample of 216 red foxes is representative of the red fox population in eastern Poland.

  • May combine two claims.

    Findingown data

    The third most highly prevalent parasites in the study were hookworms, with a prevalence of 72.2%.

    “The third most highly prevalent parasites in our study were hookworms (72.2%).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    The infection intensity of Mesocestoides in the middle part was significantly higher than in the anterior part but did not differ from the intensity in the posterior part.

    “Moreover, our study showed that the infection intensity in M was significantly higher than in A but did not differ from the intensity in the posterior part (P).”
    Quote in the paperSubstantial claim

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

    Interpretationreasoning

    The lower percentage of hookworm-infected animals in earlier Polish studies was probably caused by using less sensitive methods for examination of intestines.

    “Although, in earlier studies, in Poland [31,41], the percentage of infected animals was significantly lower, which probably was caused by using less sensitive methods for examination of intestines.”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [31] Borecka, 2009, Prevalence of zoonotic helminth parasites of the small intestine in red foxes from central Poland, Med. Weter.
    • cites [41] Ramisz, 2003, Fauna of gastro-intestinal parasites in red foxes in Western Poland, Med. Weter.

      Not checked in the free run.

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

    Study design and conductnone given

    The samples were stored for at least two weeks at a temperature lower than −70 °C before examination to inactivate dangerous tapeworm (Echinococcus) eggs.

    “The samples were stored for at least two weeks at a temperature lower than −70 °C before examination to inactivate dangerous tapeworm (Echinococcus) eggs.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationreasoning

    The relatively high prevalence (79%) of A. alata in Lubelskie Province obtained in this study was expected because some lake districts are present in this region.

    “The relatively high prevalence (79%) in Lubelskie Province obtained in our study was expected because, in this region, some lake districts are present.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The sample of 216 red foxes is representative of the red fox population in eastern Poland.

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductreasoning

    Because T. canis and T. leonina are difficult to distinguish in routine microscopic examination, they were analyzed together.

    “Because T. canis and T. leonina are difficult to distinguish in routine microscopic examination, they were analyzed together.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductown data

    The distribution of quantitative variables was tested by the Shapiro-Wilk test, and the normality hypothesis of the data was rejected.

    “The distribution of quantitative variables was tested by the Shapiro–Wilk test, and the normality hypothesis of the data was rejected.”
    Quote in the paperSubstantial claim

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

    Premisecitation

    The similar positive correlation was observed in the study conducted on rabbits where intensity of Graphidium strigosum was higher in host coinfected with another nematode (Trichostrongulus retortaeformis) than single-infected hosts.

    “The similar positive correlation was observed in the study conducted on rabbits where intensity of Graphidium strigosum was higher in host coinfected with another nematode (Trichostrongulus retortaeformis) than single-infected hosts [26].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [26] Murphy, 2013, A co-infection with two gastrointestinal nematodes alters host immune responses and only partially parasite dynamics, Parasite Immunol. source

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    In the distribution analysis of parasites within the intestine, only animals in which the parasites were found were considered.

    “In the distribution analysis of parasites within the intestine, only animals in which the parasites were found were considered.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Interpretationreasoning

    The lack of significant competition may be associated with different intestinal distributions and other predilection sites.

    “This may be associated with different intestinal distributions and other predilection sites.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    Taenia spp. and Toxocara/Toxascaris have a predilection for the anterior part of the intestine, but not as clearly visible as in the case of A. alata.

    “This indicates a predilection for the anterior part of the intestine, but not so clearly visible as in the case of A. alata.”
    Quote in the paperSubstantial claim
48 of 48

  • The paper relies on this without support.

    There is a lack of data concerning all parasitic helminths in red foxes from eastern Poland (Lubelskie Province).

    “However, there is a lack of data concerning all parasitic helminths in red foxes from the eastern part of the country (Lubelskie Province).”

  • The paper relies on this without support.

    The distribution of parasites across the three intestinal segments reflects their predilection sites.

    “Determining typical predilection sites for parasites in the intestine can be helpful in creating effective diagnostic methods.”

  • The paper relies on this without support.

    The sample of 216 red foxes is representative of the red fox population in eastern Poland.

    “Two hundred and sixteen red foxes shot in eastern Poland were used in the investigation.”

  • The authors state this as an assumption.

    Tapeworms detected in the study mostly belonged to the Mesocestoides litteratus species.

    “Genetic analysis of Mesocestoides isolated in Poland [39,40] allowed us to assume that tapeworms detected in our study mostly belonged to the Mesocestoides litteratus species.”

  • The authors state this as an assumption.

    Approximately 80% of Toxocara/Toxascaris positive samples belonged to the Toxocara canis species.

    “However, based on experience form our previous study [14], we can assume that the majority (approximately 80%) of these positive samples belonged to the Toxocara canis species.”

  • The authors state this as an assumption.

    Positive correlations regarding the intensity of Mesocestoides and other tapeworms as well as hookworms and A. alata may be the result of a higher susceptibility of individual foxes to parasitic infections in general, e.g., caused by general immunosuppression.

    “On the other hand, positive correlations regarding the intensity of Mesocestoides and other tapeworms as well as hookworms and A. alata may be the result of a higher susceptibility of individual foxes to parasitic infections in general, e.g., caused by general immunosuppression.”

  • The authors state this as an assumption.

    Another reason for a positive correlation in the intensity of coinfecting parasites, having in their life cycle intermediate hosts (Mesocestoides, Taenia, and E. multilocularis), may be the high hunting activity of individual foxes.

    “Another reason for a positive correlation in the intensity of coinfecting parasites, having in their life cycle intermediate hosts (Mesocestoides, Taenia, and E. multilocularis), may be the high hunting activity of individual foxes.”

  • The paper relies on this without support.

    The investigation presented for the first time the prevalence and intensity of intestinal helminths in red foxes in this region of Poland.

    “Moreover, our investigation presented for the first time the prevalence and intensity of intestinal helminths in red foxes in this region of Poland.”
8 of 8

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.

  • The same chi-square value has conflicting p-values

    Minor

    Both comparisons report χ2 = 11.26, but one gives p = 0.0008 and the other p < 0.0001. These cannot both be the p-value for the same one-degree-of-freedom chi-square statistic.

  • Hookworm prevalence is reported as both 72.7% and 72.2%

    Minor

    The abstract reports hookworm prevalence as 72.7%, while the discussion reports 72.2% for the same study.

2 of 2

Cites

Flagged first, then by citations

3 of the 50 references couldn’t be matched to a known paper.

Research works printed but not linked: 3

  1. Manke, 1998, Parasitological studies of red foxes (Vulpes vulpes L.) in the northern districts of Schleswig-Holstein, Tierarztl. Umschau., 53, 207
  2. Lassnig, 1998, Parasites of the red fox (Vulpes vulpes) in Styria, Wien. Tierarz. Monats., 85, 116
  3. Ramisz, 2003, Fauna of gastro-intestinal parasites in red foxes in Western Poland, Med. Weter., 59, 922

Cited by

Sorted by citations

Related

Authors
Karamon, J., Sroka, J., Dąbrowska, J., Bilska-Zając, E., Skrzypek, K., Różycki, M., Zdybel, J., & Cencek, T.
Affiliations
National Veterinary Research Institute (PL)
Corresponding author
Karamon, Jacek
ORCID
Venue
Pathogens
Publisher
MDPI AG
Published
2020-06-16
Volume
9
Issue
6
Pages
477
ISSN
2076-0817 (ISSN-L)
DOI
10.3390/pathogens9060477
PMC
PMC7350372
OpenAlex
W3035580901
Cited by
19
References
50
Citations by year
2026: 1 · 2025: 5 · 2024: 5 · 2023: 3 · 2022: 2 · 2021: 3
FWCI
1.71
Type
journal article
Language
en
Open access
Licence
Locations
  • Pathogens (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Polish Ministry of Agriculture (“Protection of animal and public health”)
  • National Veterinary Research Institute in Puławy, Poland. (the statutory funds)
Topics
  • Health Sciences › Veterinary › Small Animals › Helminth infection and control
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Parasitic infections in humans and animals
  • Physical Sciences › Environmental Science › Ecology › Parasite Biology and Host Interactions
Keywords
red fox, intestinal helminths, small intestine, parasite distribution, predilection sites, Alaria alata, Mesocestoides, hookworm, Taenia, Toxocara, Toxascaris, Echinococcus multilocularis, Eastern Poland

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 2026-10-26.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-26.

Cited sources are checked by gpt-6-sol.

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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