Increase in number of helminth species from Dutch red foxes over a 35-year period
Open accessAbstract
BACKGROUND: The red fox (Vulpes vulpes) is host to a community of zoonotic and other helminth species. Tracking their community structure and dynamics over decades is one way to monitor the long term risk of parasitic infectious diseases relevant to public and veterinary health. METHODS: We identified 17 helminth species from 136 foxes by mucosal scraping, centrifugal sedimentation/flotation and the washing and sieving technique. We applied rarefaction analysis to our samples and compared the resulting curve to the helminth community reported in literature 35 years ago. RESULTS: Fox helminth species significantly increased in number in the last 35 years (p-value <0.025). Toxascaris leonina, Mesocestoides litteratus, Trichuris vulpis and Angiostrongylus vasorum are four new veterinary-relevant species. The zoonotic fox tapeworm (E. multilocularis) was found outside the previously described endemic regions in the Netherlands. CONCLUSIONS: Helminth fauna in Dutch red foxes increased in biodiversity over the last three decades.
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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].”
From Distribution of Parasitic Helminths in the Small Intestine of the Red Fox (Vulpes vulpes) (2020) · cites this paper as [1]
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 measuredThe 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.”
From Distribution of Parasitic Helminths in the Small Intestine of the Red Fox (Vulpes vulpes) (2020) · cites this paper as [1]
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 measuredThe 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.”
From Distribution of Parasitic Helminths in the Small Intestine of the Red Fox (Vulpes vulpes) (2020) · cites this paper as [1]
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 measuredThe prevalence of Toxocara/Toxascaris nematodes in the study was similar to results obtained in other Polish regions and Europe.
“In the present study, the prevalence of these nematodes was similar to results obtained in other Polish regions [14,31,38,41] and Europe [1,2,3,8,10,13,16,19,37].”
From Distribution of Parasitic Helminths in the Small Intestine of the Red Fox (Vulpes vulpes) (2020) · cites this paper as [1]
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].”
From Distribution of Parasitic Helminths in the Small Intestine of the Red Fox (Vulpes vulpes) (2020) · cites this paper as [1]
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Omeragić, J., Kapo, N., Softić, A., Škapur, V., Goletić, Š., Alić, A., & Goletić, T. (2024) · Macedonian Veterinary Review · doi:10.2478/macvetrev-2024-0017 · Cited by 6 · see citing works
Bełcik, A., Cencek, T., Korpysa-Dzirba, W., Samorek-Pieróg, M., Karamon, J., Sroka, J., Zdybel, J. M., Skubida, M., & Bilska-Zając, E. (2025) · Pathogens · doi:10.3390/pathogens14070625 · Cited by 3 · see citing works
Heydarian, P., Kia, E. B., Heidari, Z., Sharifdini, M., Zarei, Z., & Zahabiun, F. (2023) · Acta Parasitologica · doi:10.1007/s11686-022-00657-8 · Cited by 3 · see citing works
Ендопаразитози лисиці рудої (Vulреs vulреs) півночі Харківського району
Mazannyі, O. V., Liulin, P., & Нікіфорова, О. В. (2023) · Scientific Progress & Innovations · doi:10.31210/spi2023.26.03.18 · Cited by 3 · see citing works
Liu, G., Ji, N., Hornok, S., Zhang, Y., Zhao, S., Chen, X., Hazihan, W., Gu, X., & Wang, Y. (2021) · International Journal for Parasitology Parasites and Wildlife · doi:10.1016/j.ijppaw.2021.11.003 · Cited by 2 · see citing works
Gomez-Puerta, L. A., Rossin, M. A., Pacheco, J. I., Angulo-Tisoc, J. M., & Gonzalez, A. E. (2025) · Parasitology International · doi:10.1016/j.parint.2025.103079 · Cited by 1 · see citing works
Morphological and Genetic Diversity of Angiostrongylus vasorum
Stevanović, O., Despotović, D., Prošić, I., Radalj, A., Nedic, D. N., Vasić, A., & Ilić, T. (2025) · Macedonian Veterinary Review · doi:10.2478/macvetrev-2025-0029 · Cited by 1 · see citing works
Pilarczyk, B., Tomza–Marciniak, A., Pilarczyk, R., Bąkowska, M., Rząd, I., Stapf, A., Felska‐Błaszczyk, L., Tylkowska, A., & Seremak, B. (2024) · Pathogens · doi:10.3390/pathogens13060490 · Cited by 1 · see citing works
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- Authors
- Franssen, F., Nijsse, R., Mulder, J., Cremers, H., Dam, C., Takumi, K., & van der Giessen, J.
- Affiliations
- National Institute for Public Health and the Environment (NL)
- Utrecht University (NL)
- Corresponding author
- Franssen, Frits
- ORCID
- Takumi, Katsuhisa
- Venue
- Parasites & Vectors
- Published
- 2014
- Volume
- 7
- Issue
- 1
- Pages
- 166
- ISSN
- 1756-3305 (ISSN-L)
- PMC
- PMC3978201
- OpenAlex
- W2095696144
- Cited by
- 48
- References
- 45
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 2 · 2023: 3 · 2021: 7 · 2020: 5 · 2019: 2 · 2018: 3 · 2017: 3 · 2016: 6 · 2015: 7 · 2014: 3
- FWCI
- 9.28
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Parasites & Vectors (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Rivm (National Institute for Public Health and the Environment) (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion)
- 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, helminth communities, zoonotic parasites, Echinococcus multilocularis, Angiostrongylus vasorum, Trichuris vulpis, Toxascaris leonina, Netherlands
- MeSH terms
- Animals, Foxes, Gastrointestinal Contents, Helminthiasis, Animal, Helminths, Netherlands, Species Specificity, Time Factors
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