Tylkowska et al. Acta Vet Scand (2021) 63:19 https://doi.org/10.1186/s13028-021-00584-0 Acta Veterinaria Scandinavica RESEARCH Open Access The prevalence of intestinal nematodes among red foxes (Vulpes vulpes) in north-western Poland Agnieszka Tylkowska1* , Bogumiła Pilarczyk2, Agnieszka Tomza‑Marciniak2 and Renata Pilarczyk3 Abstract Background: The red fox (Vulpes vulpes) is widely distributed in the Northern Hemisphere and Australia. The pres‑ ence of nematode‑infected foxes in urbanized areas increases the risk of transmission of nematodes to domestic dogs and thus, to humans. The aim of this study was to determine the prevalence and species composition of intestinal nematodiasis in red foxes in Western Pomerania, a province in north‑western Poland. The intestinal contents of 620 red foxes killed during a government reduction shooting programme were examined for adult nematodes using the sedimentation and counting technique (SCT). Results: Intestinal nematodes, including Toxocara canis, Toxascaris leonina, Uncinaria stenocephala and Trichuris vulpis, were found in 77.3% (95% CI 73.8–80.4%) of the examined foxes with a mean infection burden of 20.1 nematode per animal. Male and female foxes had similar infection burdens. Conclusions: The nematodes are present in high prevalence and intensity among foxes in north‑western Poland. Furthermore, this high prevalence of nematodes in foxes may likely constitute a health risk to humans and domestic animals due to increasing fox densities in urban and periurban areas. Keywords: Ecological indicators, Helminths, Nematodes, Prevalence, Red fox Background in urbanized areas increases the risk of transmission of Te red fox (Vulpes vulpes) is widely distributed in the these nematodes to humans, either directly, or indirectly Northern Hemisphere and Australia [1]. A rapid increase through infection of domestic dogs [5–7]. Infected foxes in its number has been observed in many European can contaminate sandpits, parks and squares with their countries since the late twentieth century [2–4]. Tis faeces, thus exposing humans to the eggs of zoonotic growth may be explained by a reduction in mortality rate nematode species such as Toxocara canis, Toxascaris due to intensive rabies vaccination campaigns and the leonina and Trichuris vulpis, and nematodes from the opportunistic behaviour of the fox itself [2]. Ancylostomatidae family [8–12]. Te growth in the fox population has resulted in its Te most widespread helminth zoonosis in developed expansion to new habitats. Unfortunately, as foxes may be countries is toxocariasis, known to cause visceral and infected by zoonotic intestinal nematodes, their presence ocular larva migrans syndrome [3, 13, 14]. In humans, as paratenic hosts, the larvae of T. canis, responsible for tox- ocariasis, do not develop into an adult stage but migrate *Correspondence: [email protected] throughout the tissues and remain as L3 arrested larvae 1 Department of Animal Environment Biology, Faculty of Animal Breeding, Bioengineering and Conservation, Warsaw University of Life Sciences, for an extended period of time [15]. Ciszewskiego 8, 02‑787 Warsaw, Poland Te prevalence of T. canis seropositive cases in humans Full list of author information is available at the end of the article has been estimated at 2.4% in Denmark [16], 7% in © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://crea‑ tivecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdo‑ main/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Tylkowska et al. Acta Vet Scand (2021) 63:19 Page 2 of 7 Sweden [17] and 6.3% in Austria [18]. A signifcant pro- water. Other parasites were collected using the sedimen- portion of the human population in Poland have also tation and counting technique (SCT). Te sex of the ani- been found to harbour T. canis antibodies, with a sero- mals was identifed based on the gonads. Te recovered prevalence ranging from 18.6 to 43% depending on the nematodes were identifed according to Stefański and region [19, 20]. Similar symptoms can be observed fol- Żarnowski [33] and preserved in 70% alcohol. lowing infection with T. leonina and T. vulpis larvae [21]. Te Jaccard coexistence index (J) [34] was used to com- An additional threat is also posed to humans by hook- pare the coexistence of particular species of nematodes, worms, i.e. nematodes of the Ancylostomatidae family, where the feature is the presence of a species in the sam- such as Ancylostoma caninum and Uncinaria stenoceph- ple (environment). A value ​​of 100% indicates that two ala, with approximately 1.3 billion people being esti- analysed nematode species always co-occur, regardless of mated to be infected by a nematode from this family [22]. their numbers, and 0% indicates that the two species are Hookworm infection rarely results in mortality but leads never observed together. to anaemia and malnutrition [23], which lead to chronic c Jp1p2 = × 100 health problems such as lethargy and impaired physical a + b − c and cognitive development [24]. A number of studies, including one carried out from where: Jp1p2—coexistence index between species p1 and 1996 to 1998 in north-western Poland by Bieńko [25], p2; a—the number of occurrences of species p1; b—the indicate that the occurrence of nematodes in foxes var- number of occurrences of species p2; c—the number of ies considerably [26–30]. Terefore, the aim of the pre- common occurrences of species p1 and p2 in the habitat. sent study was to determine the prevalence of intestinal Te obtained results were analysed using Statistica nematoidiasis in red foxes (Vulpes vulpes) in north-west- 10.0. Te occurrence of individual nematode species was ern Poland and investigate other parameters associated compared between the sex of the host was determined with its presence, e.g. examine its distribution between using the Mann–Whitney U-test. Te occurrence of sexes and predilection. nematodes was compared between individual sections of the gastrointestinal tract using the Kruskal–Wallis test. Methods Te confdence interval of a proportion was calculated by Te study was conducted in Western Pomerania, a prov- the modifed Wald method, as recommended by Agresti ince of north-western Poland. Te material comprised a and Coull [35]. total of 620 red foxes (236 females and 384 males) culled during a government reduction shooting programme in Results 18 counties in the region. Te remains of the foxes were Nematodes were found in 77.3% (95% CI 73.8–80.4%) of acquired from the Departments of Veterinary Hygiene analysed foxes, while the mean infection intensity was in Szczecin and Koszalin during the hunting seasons of 20.1 nematodes per animal. T. canis, T. leonina, U. steno- 2008/2009, 2009/2010 and 2010/2011. Te minimum cephala and T. vulpis were isolated from the tested foxes. sample size was calculated according to the Cochran Of these, U. stenocephala was the most prevalent (34.0%, formula. 95% CI 30.4–37.9%), with an intermediate intensity of Parasitological analyses were carried out at the Depart- infection (20.7) (Table 1). ment of Veterinary Hygiene in Szczecin and Koszalin. T. canis was more commonly observed in male foxes Fox carcasses delivered to the department by hunters (32.0%, 95% CI 27.6–36.9%) than females (27.1%, 95% were initially frozen at − 70 °C for four days to prevent CI 21.8–33.1%), while U. stenocephala was more com- transmission of infective Echinococcus multilocularis mon in female foxes (37.7%, 95% CI 31.8–44.0%) than eggs. Te carcasses were then thawed and examined. males (31.8%, 95% CI 27.3–36.6%). Tese diferences in Te alimentary tracts of the foxes were subjected incidence were not statistically signifcant (p > 0.05). In to parasitological analysis using sectional methods both males and females, the highest mean intensity of described by Eckert et al. [31, 32] and by Stefański and infection was found for U. stenocephala, which displayed Żarnowski [33]. Briefy, the alimentary tract samples similar intensities in female (21.7) and male foxes (19.9) were isolated from the animals and divided into oral (Table 2). cavity, oesophagus, stomach, small intestine, caecum Nematodes were observed in the duodenum, jejunum, and large intestine samples. In addition, the small intes- ileum and caecum; however, none were noted in the oral tine was further divided into three sections: duodenum, cavity, the oesophagus, the stomach or the large intestine. jejunum and ileum. Te organs were opened along their Te parts of the alimentary tract where nematodes were entire length. Visible parasites were removed immedi- found were then subjected to further analysis; among ately from the mucosa and placed in Petri dishes with these, signifcantly higher numbers of nematodes were Tylkowska et al. Acta Vet Scand (2021) 63:19 Page 3 of 7 Table 1 Parameters of occurrence of nematodes in red fox In the duodenum, the most common nematodes were Parasite Number of foxes Prevalence Intensity of U.