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.

Unique genetic structure of the human tapeworm Dibothriocephalus latus from the Alpine lakes region – a successful adaptation?

“…Dibothriocephalus latus , however, was not found during our ichthyoparasitological examinations of perch and pike from Pomeranian Bay and Białowieża Primeval forest (Radačovská et al , 2019 c ). The eggs detected in otter, lynx and wolf (Górski et al , 2006, 2010; Szczęsna et al , 2008) likely belonged to the recently intensively studied S. erinaceieuropaei in northeastern Poland (Kondzior et al , 2020). Finally, the examination of 700 European perch from the Slovak part of the Danube river also did not reveal any D. latus (Radačovská et al , 2019 b ).…”

Genetic interrelationships of Spirometra erinaceieuropaei (Cestoda: Diphyllobothriidea), the causative agent of sparganosis in Europe

“…The definitive hosts are wild and domesticated carnivores. Humans become infected either by drinking water containing infected copepods or by consuming plerocercoids in raw or inadequately cooked meat of the second intermediate or paratenic host [ 9 , 14 ].…”

“…In the past two decades, the occurrence of S. erinaceieuropaei in wild carnivores, mustelids, wild boars, and snakes has been reported in several northern and eastern European countries, mainly in the vicinity of the Białowieża National Park in eastern Poland [ 4 – 9 , 14 ] and in western Belarus [ 22 , 24 , 25 ], but also in Serbia [ 17 ], Estonia [ 10 ], Latvia [ 1 ], Ukraine, and Finland [ 11 , 14 , 15 ]. The genetic structure of S. erinaceieuropaei based on the mitochondrial cox 1 gene is so far available only for the populations from Poland and Latvia [ 1 , 7 ] and only single sequences were published for tapeworms from Finland and Ukraine [ 14 , 15 ].…”

Digestive tract nematode infections in non-native invasive American mink with the first molecular identification of Molineus patens

“…American mink is an important invasive mammal species serving in its introduced range as both, intermediate and definitive host for many endoparasite species belonging to various taxonomic groups: trematodes, cestodes, nematodes ( Shimalov and Shimalov, 2001a ; Torres et al, 2003 , 2008 ); among them such zoonotic parasites as: Trichinella spp., Alaria spp, Spirometra erionaceieuropaei , Echinococcus spp., Toxocara spp. ( Hurníková et al, 2016 ; Kołodziej-Sobocińska et al, 2020 ; Kondzior et al, 2020 ; Shimalov and Shimalov, 2001a ). Our previous study showed that the increased abundance of nematodes inhabiting digestive tract was observed with time since the American mink populations were established and, as a result, it caused a decline in mink body condition ( Kołodziej-Sobocińska et al, 2018 ).…”