Multispecies reservoir of Spirometra erinaceieuropaei (Cestoda: Diphyllobothridae) in carnivore communities in north-eastern Poland

Abstract

Background: Spirometra erinaceieuropaei is a diphylobothriid tapeworm with a complex life-cycle including definitive, intermediate and paratenic (transport) hosts. Multiple routes of parasite transmission often make it impossible to determine what type of host a specific infected animal is considered to be. Spargana larvae cause sparganosis, a severe food- and water-borne disease mainly found in Asia. In Poland, Spirometra sp. was reported in large carnivores in Białowieża Primeval Forest for the first time in the 1940s and was recently confirmed as S. erinaceieuropaei in several mammals and snakes using molecular methods.

Methods: In total, 583 carcasses of 9 carnivore species were necropsied between 2013 and 2019 in north-eastern (NE) Poland. The larvae of S. erinaceieuropaei (spargana) were isolated from subcutaneous tissue, counted, and preserved for genetic analyses. We calculated the prevalence and intensity of infection. To assess spatial variation in S. erinaceieuropaei infection probability in NE Poland, we applied a generalized additive model (GAM) with binomial error distribution. To confirm the species affiliation of isolated larvae, we amplified a partial fragment of the 18S rRNA gene (240 bp in length).

Results: Spirometra larvae were found in the subcutaneous tissue of 172 animals of 7 species and confirmed genetically as S. erinaceieuropaei. The overall prevalence in all studied hosts was 29.5% with a mean infection intensity of 14.1 ± 33.8 larvae per individual. Native European badgers and invasive raccoon dogs were characterized by the highest prevalence. An analysis of parasite spread showed a spatially diversified probability of infection with the highest values occurring in the biodiversity hot spot, Białowieża Primeval Forest.

Conclusions: Our study revealed that various mammal species (both native and non-native) can serve as S. erinaceieuropaei reservoirs. The frequency and level of infection may differ between selected hosts and likely depend on host diversity and habitat structure in a given area. Further studies are needed to assess the distribution of the parasite throughout Europe and the environmental and biological factors influencing infection severity in wild mammals.

Keywords: European badger; Paratenic hosts; Plerocercoid larvae; Raccoon dog; Sparganosis; Zoonosis.

Fig. 1

The distribution of study sites and samples in the study area. Black dots indicate carnivore individuals infected with Spirometra erinaceieuropaei, white dots indicate non-infected individuals

Fig. 2

Cysts containing Spirometra erinaceieuropaei plerocercoids in subcutaneous tissue of American mink (Neovison vison) from Białowieża Primeval Forest. Visible skin from the inside in the abdominal part of the body

Fig. 3

The predicted probability of Spirometra erinaceieuropaei infection in carnivore hosts in NE Poland. Results of the generalized additive model (GAM). Black dots indicate infected animals, white dots indicate non-infected animals. Abbreviations: AF, Augustów Forest; BPF, Białowieża Primeval Forest; KF, Knyszyn Forest; BV, Biebrza Valley