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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.

Background

It is supposed that all organisms on Earth are involved in host-parasite interactions [1]. The trophic chain of hosts plays an important role for parasites in enabling them to come into contact with a variety of hosts and colonize new environments [2]. Parasite transmission is common among members of foraging guilds [3]. For most of helminth parasites, host specificity appears less defined at the intermediate host stage than at the definitive host stage, with non-adult intermediate (larval) stages able to infect different organs and tissues of diverse intermediate hosts. The range of specificity of the parasite is a crucial determinant of its invasive capacity and the likelihood of new host-parasite combinations occurring [4]. In addition, several parasites use paratenic (transport) hosts, where parasite larvae show no development [5]. The role of paratenic hosts is important; they facilitate contact between parasite larvae and the definitive host, contributing to an increase of prevalence in a specific host population [6].

Spirometra Faust, Campbell & Kellogg, 1929 is a genus of diphylobothriid cestodes that reproduce mainly in the small intestines of felids and canids [7, 8] and require two intermediate hosts. The unembryonated eggs released with animal faeces produce a ciliated stage (coracidium). The first intermediate host is a copepod (planktonic freshwater crustacean), in which coracidia develop into procercoid larvae (the first larval stage). When the infected copepod is swallowed by a second intermediate host, such as an amphibian or reptile [9,10,11,12], the procercoid larvae penetrate the intestinal tract and transform to plerocercoids (spargana), which then migrate and settle in other organs and tissues, such as subcutaneous connective tissue, the brain, lungs, spinal cord, urinary bladder or eye [13,14,15,16,17,18,19,20].

The life-cycle of Spirometra spp. may also include paratenic hosts. Second intermediate hosts infected with plerocercoid larvae can be preyed upon and thus reach a wide variety of tetrapods such as birds or mammals (including humans) that may serve as paratenic hosts for this parasite [21, 22]. Multiple routes of parasite transmission often make it impossible to determine what type of host a specific infected animal is considered to be. After passing through the intestinal wall, spargana settle in host tissues and cause sparganosis [23, 24]. Paratenic hosts, however, are unnecessary for the completion of life-cycle, thus the larval Spirometra can infect and subsist in numerous species of paratenic hosts until finally consumed by felids or canids, serving as definitive hosts [25], though they are also reservoirs of spargana for other carnivores. It has also been found that some canids, such as the red fox (Vulpes vulpes Linnaeus, 1758) and the raccoon dog (Nyctereutes procyonoides Gray, 1834), may serve as both definitive and paratenic hosts [7, 26, 27].

Spargana in intermediate and/or paratenic hosts cause sparganosis, a severe food- and water-borne disease [18, 23, 28]. Most of the research on sparganosis has been conducted in Asia, where sparganosis is a serious public health problem [11, 13,14,15,16,17, 19, 22, 23]. However, there are also reports from other continents, including South and North America, Africa, Australia, and Europe [29,30,31]. European records of sparganosis in wildlife are mainly based on incidental reports of the presence of the parasite in vertebrates, including canids [26, 27], mustelids [32,33,34], rodents [35], insectivores [7], snakes [9, 36, 37] and frogs [36,37,38]. In Poland, the first report of adult Spirometra was described as S. janickii in wolves (Canis lupus Linnaeus, 1758) and Eurasian lynxes (Lynx lynx Linnaeus, 1758) from Białowieża Primeval Forest (BPF) in the 1940s [7]. Nonetheless, this finding is controversial. This species has not been reported since its original description, likely because most authors synonymised S. janickii with S. erinaceieuropaei. European genotypes of S. erinaceieuropaei in Polish wildlife were reported for several species of mammals, including the American mink (Neovison vison Schreber, 1777) [39], Eurasian lynx [8], European badger (Meles meles Linnaeus, 1758) [32], European polecat (Mustela putorius Linnaeus, 1758) [39], raccoon dog [39] and wild boar (Sus scrofa Linnaeus, 1758) [40], and for one species of reptile, the grass snake (Natrix natrix Linnaeus, 1758) [9]. Recently, the first case of human sparganosis in Poland was confirmed in an individual in the surroundings of BPF [28]; the source of infection likely being consumption of wild boar meat containing spargana [40]. It can be supposed that the consumption of venison may cause an increase in the number of cases of human sparganosis.

The role of wild carnivores as transmission vectors for zoonotic diseases has been widely described [41,42,43,44] and includes both native as well as non-native invasive species. Invasive species are important for spreading and transmitting of diseases because they can carry their own parasites and acquire new ones during the colonization of new territories [45, 46]. Nothing is known about the role of invasive species in the spread of sparganosis, and very little about the contribution of native carnivores to the maintenance of this disease in European wildlife.

The main goal of this paper was to investigate the spread of S. erinaceieuropaei in well-preserved communities of wild carnivores in north-eastern (NE) Poland. We aimed to: (i) investigate which carnivore species (native and/or non-native invasive) may serve as S. erinaceieuropaei hosts in wildlife and whether the parasite’s presence is only local or perhaps more widespread; (ii) calculate the infection parameters, prevalence and intensity; (iii) assess spatial patterns of infection probability in the study area; and (iv) reveal whether wild canids and felids, the typical definitive hosts, may also serve as paratenic hosts carrying spargana.

Methods

Study area

Our study was performed in Podlasie and the eastern part of the Masurian Lakes region, north-eastern (NE) Poland. Both regions are characterized by well-preserved forest ecosystems (with four national parks and a large area covered by Natura 2000, a network of nature protection areas in the territory of the European Union) and greater forest cover (32%) in comparison to the rest of Poland [47]. Our main sampling sites were large forested areas: Augustów Forest (AF); Białowieża Primeval Forest (BPF); Biebrza Valley (BV); Knyszyn Forest (KF); and the Masurian Lake District (MLD). AF, KF and MLD are dominated by coniferous forests [48]. In BPF over 60% of the area is covered by deciduous and mixed forests with high species richness [49]. Wet habitats cover over 40% of the area [48], and BV is the largest marshland in central Europe with concentrated patches of woodlands [50]. Moreover, the northern part of the study area in MLD and AF is interspersed by numerous lakes.

The region is characterized by a low degree of urbanization and the lowest human densities in Poland (59 individuals/km2) [47]. NE Poland is located within a zone of temperate transitional climate with marked continental influences. The study area is inhabited by well-preserved animal communities with as many as 12 local species of carnivores [51].

Carcass collection

A total of 583 carcasses of 9 mammal species were collected in BPF and AF between 2013 and 2019, in BV, KF and MLD between 2016 and 2019, and in the surroundings of studied forests between 2015 and 2019 (Fig. 1, Table 1). Mammal carcasses originated from road kills or legal culling from predator control for gallinaceous bird, i.e. the black grouse (Lyrurus tetrix Linnaeus, 1758) and the western cappercaillie (Tetrao urogallus Linnaeus, 1758), conservation projects. No animals were killed specifically for this study.

Fig. 1
figure1

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

Table 1 Prevalence and infection intensity of Spirometra erinaceieuropaei in carnivores in NE Poland

Necropsies and genetic identification of larvae

The collected carcasses were kept frozen at − 80 °C for a minimum of one week to minimize the risk of Echinococcus multilocularis (Leuckart, 1863) infection [52]. During necropsies the animals were weighed, measured and sexed. Spargana were isolated from subcutaneous tissue, counted, and preserved in 99% ethanol for molecular identification as described below. Prevalence (the proportion of infected individuals in %) was calculated as the ratio of infected individuals to all collected study animals. The mean intensity of infection in each host species was calculated as the average number of spargana per one infected individual of a particular species. We also calculated a standard deviation of the mean intensity of infection as the square root of its variance.

To confirm larval species affiliation, we molecularly confirmed 25 larvae isolated from different carnivore species (see details in Additional file 1: Table S1, Additional file 2: Figure S1, Additional file 3: Figure S2). We used primers and procedures described by Liu et al. [53] to achieve a sequence of an evolutionarily conserved nuclear 18S rRNA gene of over 240 bp in length. The sequences were aligned with previously analysed ones from wild boars, European badgers, and grass snakes from BPF [9, 32, 40] (Additional file 1: Table S1), as well as with sequences available on GenBank subsequently trimmed to 222 bp in length and analysed using the ClustalW multiple alignment test (BioEdit sequence alignment editor [54]) and Basic Local Alignment Search Tool (BLAST) [55]. A Tamura-Neil model (TrN) was selected for maximum likelihood analysis using MEGA v6 [56]. The following reference sequences for other Diphyllobothriidae were retrieved from GenBank: Spirometra erinacei (D64072.1); S. erinaceieuropaei (KX528090 and KX552801); and Dibothriocephalus latus (Linnaeus, 1758) (KF218247, KF218246.1 and DQ925309). Taenia pisiformis (Bloch, 1780) (JX317675.1) and Taenia krabbei (Moniez, 1879) (MH843684.1) were used as the outgroup in analyses (Additional file 2: Figure S1 and Additional file 3: Figure S2). A list of all newly generated sequences of 18S rRNA is presented in Additional file 1: Table S1.

Statistical analysis

To assess the spatial variation of S. erinaceieuropaei infection probability in NE Poland, we applied a generalized additive model (GAM) with binomial error distribution in the mgcv package implemented in R [57]. We added the presence/absence of larvae in the sampled individuals as a binomial dependent variable, while the interaction of longitude and latitude of sample locations (explanatory variables) was fitted as a non-parametric spline. We limited analyses to samples collected in BPF, KF, AF and BV due to larger numbers of carcasses collected during the study period.

Results

Plerocercoid larvae of Spirometra were found in 172 of 583 mammals belonging to 7 out of 9 studied species (Table 1, Fig. 2). The overall prevalence of spargana infection in carnivore hosts was 29.5%. The highest overall prevalence was estimated for European badgers (36.4%) and raccoon dogs (30.9%). Twenty-seven stone martens (Martes foina Erxleben, 1777) and 3 Eurasian lynxes were uninfected. The overall mean infection intensity was 14.1 ± 33.8 with the highest values up to 276 found in European badgers (38.2 ± 56.0) (Table 1).

Fig. 2
figure2

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

All 25 newly generated 18S rRNA sequences of larvae isolated from autopsied animals of 7 different species showed 99% identity with the 3 sequences for S. erinaceieuropaei deposited on GenBank (Additional file 2: Figure S1, Additional file 3: Figure S2). Comparisons with previously published 18S rRNA sequences from isolates in European badgers, wild boars, and grass snakes, revealed that the new sequences all showed 99.4–100% similarity (BLAST). The only variation was observed in the DNA of 2 out of 4 analysed larvae originating from European polecats and was, in both cases, an insertion of a T nucleotide at position 207 of sequences (see Additional file 2: Figure S1). The occurrence of S. erinaceieuropaei was confirmed for the first time using molecular methods in the pine marten (Martes martes Linnaeus, 1758), red fox, and river otter (Lutra lutra Linnaeus, 1758) (Additional file 1: Table S1; Additional file 2: Figure S1, Additional file 3: Figure S2).

The GAM showed a significant spatial pattern in the probability of S. erinaceieuropaei infection in the study area (χ2 = 47.8, P < 0.001). The highest probability of infection was observed in BPF and was observed to decrease northward (Fig. 3).

Fig. 3
figure3

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

Discussion

Most European cases of sparganosis in wildlife represent exclusively single findings. Thus far, the only comprehensive research has been carried out in Belarusian Polesie, which is closely related to BPF where the parasite has been found in amphibians, reptiles and mammals (including 7 species of carnivores) [26, 27, 33, 37, 58,59,60,61]. Our study focused on S. erinaceieuropaei spread in well-preserved carnivore communities of NE Poland. We revealed high species richness of intermediate/paratenic mammalian hosts for S. erinaceieuropaei, including seven out of nine studied species, both native (European badger, European polecat, river otter, pine marten and red fox) and invasive (American mink and raccoon dog). Previously, the parasite was also confirmed in Poland in the wild boar (larvae) as well as in the Eurasian lynx and wolf (adult parasites) [7, 8, 32, 39, 40]. We molecularly confirmed pine marten and river otter as hosts of S. erinaceieuropaei for the first time and provided the first comprehensive epidemiological data for seven mammal species in NE Poland. Previous research from Europe has also shown six other mammal species as hosts of S. erinaceieuropaei, including the brown rat (Mus decumanus Berkenhout, 1769), European hedgehog (Erinaceus europeaus Linnaeus, 1758), European mink (Mustela lutreola Linnaeus, 1761), European mole (Talpa europaea Linnaeus, 1758), stoat (Mustela erminea Linnaeus, 1758) and weasel (Mustela nivalis Linnaeus, 1766) [34, 35, 60,61,62]. The species richness of infected carnivores indicates a wider than previously expected spread and complex circulation of the parasite in wildlife. The lack of other comprehensive data about S. erinaceieuropaei occurrence in Europe has previously not given us a reason to suppose that the parasite is so widespread and prevalent in European wildlife.

The highest infection rates were revealed in the invasive raccoon dog and the native European badger. Therefore, the role of invasive species may be particularly significant in disease spreading; by settling into new areas, they can either bring alien parasite species into colonized areas [44, 63], or become new hosts for native parasites and facilitate their spread [44]. High infection rates in both species may result from consuming prey (primarily amphibians and reptiles) in addition to carrion (wild boar and other mesocarnivores) for the raccoon dog that serve as the source of Spirometra infection [51]. Moreover, European badgers and raccoon dogs are preyed upon and consumed by large predators (wolf and Eurasian lynx) [51, 64]; predation by wolves and dogs is one of the main sources of raccoon dog mortality [64]. This allows Spirometra to complete its life-cycle and continue spreading. The parasite can be effectively spread over large areas by its medium-sized and large carnivores hosts (European badger: maximal daily movement distance 17.5 km; Eurasian lynx: 24.8 km; wolf: 64 km) [65,66,67], or even to human settlements through dogs. Further studies are needed to reveal how diet composition influences infection severity in Spirometra-infected hosts.

We did not find S. erinaceieuropaei plerocercoids in stone marten and Eurasian lynx specimens. This could be due to stone marten habitat selection as well as the diet of both species. The stone martens’ diet does not consist of amphibians and reptiles; they mainly prey on small mammals and birds [68], which can be a potential source of infection. In NE Europe, stone martens usually occur in urban and rural areas and avoid large, continuous forest complexes [69], which limit their potential to come into contact with possible wild hosts of S. erinaceieuropaei. So far, stone martens have been considered a host for Spirometra sp. accidentally in Italy [70]. However, the Eurasian lynx is a known definitive host of S. erinaceieuropaei [7, 8, 71]. Its diet only sporadically consists of amphibians, and it mostly preys on ungulates, which do not serve as hosts for Spirometra [51]. Moreover, carnivores like the red fox, raccoon dog and raccoon (Procyon lotor Linnaeus, 1758) may serve as both intermediate/paratenic and definitive host of Spirometra sp. [26, 27, 72]. We did not find any spargana in the three Eurasian lynx carcasses, but the number of studied animals was very low. Raccoons have not yet been reported as either intermediate/paratenic or definitive host for Spirometra in European wildlife; they have only been confirmed experimentally [72]. However, our study has confirmed that the red fox and raccoon dog, the typical definitive hosts, can also act as intermediate/paratenic hosts for S. erinaceieuropaei. This may be important for sparganosis spread in wildlife, since it highlights the diversity of the disease transmission routes, which range from parasite eggs present in the faeces of definitive hosts, to intermediate/paratenic hosts infected with spargana and preyed upon by large predators [46, 64].

We focused on intermediate/paratenic hosts for S. erinaceieuropaei in which larvae may be found in subcutaneous tissue and other organs. Morphological identification of spargana to the species level is impossible and such analyses are justified only in the case of adult tapeworms that complete their life-cycle in a definitive host [24]. Thus, it is highly recommended to use molecular methods for reliable identification of larval Spirometra. So far, notwithstanding our studies in NE Poland over the last few years [8, 9, 32, 39, 40], no genetic analyses of Spirometra larvae in Europe have been carried out; therefore, it is not clear which species have caused previously reported infections. Additionally, the adult tapeworms of S. janickii described by Furmaga in the 1950s [7], have not yet been found again, and thus cannot be analysed in more detail. Our study revealed only minor genetic divergence in the studied 18S rRNA gene sequences, which can be interpreted as inter-individual differences. All studied parasite specimens isolated from different hosts and locations undoubtedly belong to the same species, S. erinaceieuropaei. This may be explained by the fact that the sites are separated by no more than 200 km and hosts such as the Eurasian lynx, wolf, red fox, raccoon dog, and European badger can move over significant distances, dispersing parasites between sites [73,74,75,76]. Our study showed that the probability of S. erinaceieuropaei infection varies spatially. The highest probability of infection and prevalence (54.8%) occurred in BPF, indicating beneficial conditions for the parasite, likely because this site had the highest species richness of mammal species among all studied sites [49, 51, 77]. Additionally, S. erinaceieuropaei was found in grass snakes from BPF [9], which may promote the transmission of sparganosis in wildlife in this area. It was found that a decrease in the number of intermediate/paratenic hosts results in a lower prevalence in definitive hosts [78]; thus, host diversity may be an important factor responsible for the spread of sparganosis. Mammalian species richness was lower in other locations [48, 51], although we observed that the probability of infection was highest inside forest complexes and decreased as the distance from the forest complex increased. BPF was also characterized by various forest and non-forest habitats, including wetlands [48], which are crucial to the life-cycle of Spirometra [10, 24]. Wet habitats in BPF are the optimal environment for the development of freshwater copepods, which are the first intermediate hosts for the parasite. In S. erinaceieuropaei hosts inhabiting AF and BV, the probability of infection was lower than in BPF, but higher than in KF. This may be due to lower habitat heterogeneity, but with a relatively high percentage of wetland habitats [48]. KF, characterized by the lowest probability of infection and prevalence (13.7%), is generally less diversified in terms of species and habitat structure, with a lower proportion of wetlands [48, 49].

Conclusions

Our study revealed that the spectrum of S. erinaceieuropaei intermediate/paratenic hosts in Europe is broad, and therefore, that the trophic dependencies that enable S. erinaceieuropaei to spread in the environment are complex. Sparganosis is likely more widespread in European wildlife than expected and may be transmitted by both native and not-native mammals. Presumably, infection rates vary spatially and depend on numerous factors, including habitat structure, species richness, and density of potential hosts. Further research is required to confirm which environmental and biological factors have the most significant impact on shaping the level of S. erinaceieuropaei infection in European wild mammalian hosts.

Availability of data and materials

The sequences analysed during the presented study are deposited in the GenBank database under the accession numbers MT127121-MT127125, MT131358-MT131361, MT136495-MT136508, MT140351 and MT140352.

Abbreviations

AF:

Augustów Forest

BLAST:

Basic Local Alignment Search Tool

BV:

Biebrza Valley

BPF:

Białowieża Primeval Forest

GAM:

generalized additive model

KF:

Knyszyn Forest

MLD:

Masurian Lake District

NE:

North-eastern

References

  1. 1.

    Sorci G, Garnier S. Evolutionary ecology: evolution of parasitism. In: Fath BD, editor. Encyclopedia of ecology. 2nd ed. Amsterdam: Elsevier; 2019. p. 304–9.

    Google Scholar 

  2. 2.

    Wells K, Gibson DI, Clark NJ. Global patterns in helminth host specificity: phylogenetic and functional diversity of regional host species pools matter. Ecography. 2019;42:416–27.

    Article  Google Scholar 

  3. 3.

    Hoberg EP, Brooks DR. A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. J Biogeogr. 2008;35:1533–50.

    Article  Google Scholar 

  4. 4.

    Agosta SJ, Janz N, Brooks DR. How specialists can be generalists: resolving the ‘parasite paradox’ and implications for emerging infectious disease. Zoologia. 2010;27:151–62.

    Article  Google Scholar 

  5. 5.

    Bush AO, Fernandez JC, Esch GW, Seed JR. Parasitism. The diversity and ecology of animal parasites. 1st ed. Cambridge: Cambridge University Press; 2001.

    Google Scholar 

  6. 6.

    Médoc V, Rigaud T, Motreuil S, Perrot-Minnot MJ, Bollache L. Paratenic hosts as regular transmission route in the acanthocephalan Pomphorhynchus laevis: potential implications for food webs. Naturwissenschaften. 2011;98:825–35.

    PubMed  Article  CAS  Google Scholar 

  7. 7.

    Furmaga S. Spirometra janickii sp.n. (Diphyllobothriidae). Acta Parasitol Polon. 1953;1:29–59.

    Google Scholar 

  8. 8.

    Kołodziej-Sobocińska M, Yakovlev Y, Schmidt K, Hurníková Z, Ruczyńska I, Bednarski M, et al. Update of the helminth fauna in Eurasian lynx (Lynx lynx) in Poland. Parasitol Res. 2018;117:2613–21.

    PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Kondzior E, Tokarska M, Kowalczyk R, Ruczyńska I, Sobociński W, Kołodziej-Sobocińska M. The first case of genetically confirmed sparganosis (Spirometra erinaceieuropaei) in European reptiles. Parasitol Res. 2018;117:3659–62.

    PubMed  Article  Google Scholar 

  10. 10.

    Oda FH, Borteiro C, da Graça RJ, Tavares LER, Crampet A, Guerra V, et al. Parasitism by larval tapeworms genus Spirometra in South American amphibians and reptiles: new records from Brazil and Uruguay, and a review of current knowledge in the region. Acta Trop. 2016;164:150–64.

    PubMed  Article  Google Scholar 

  11. 11.

    Li MW, Song HQ, Li C, Lin HY, Xie WT, Lin RQ, et al. Sparganosis in mainland China. Int J Inf Dis. 2011;15:e154–6.

    Article  Google Scholar 

  12. 12.

    Zhang X, Hong X, Liu SN, Jiang P, Zhao SC, Sun CX, et al. Large-scale survey of a neglected agent of sparganosis Spirometra erinaceieuropaei (Cestoda: Diphyllobothriidae) in wild frogs in China. PLoS Negl Trop Dis. 2020;14:e0008019.

    PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Sen DK, Muller R, Gupta VP, Chilana JS. Cestode larva (sparganum) in the anterior chamber of the eye. Trop Geogr Med. 1989;41:270–3.

    CAS  PubMed  Google Scholar 

  14. 14.

    Cho YD, Huh JD, Hwang YS, Kim HK. Sparganosis in the spinal canal with partial block: an uncommon infection. Neuroradiology. 1992;34:241–4.

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Chang KH, Chi JG, Cho SY, Han MH, Han DH, Han MC. Cerebral sparganosis: analysis of 34 cases with emphasis on CT features. Neuroradiology. 1992;34:1–8.

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Oh SJ, Chi Je G, Lee Sang E. Eosinophilic cystitis caused by vesical sparganosis: a case report. J Urology. 1993;149:581–3.

    CAS  Article  Google Scholar 

  17. 17.

    Jeong SC, Bae JC, Hwang SH, Kim HC, Lee BC. Cerebral sparganosis with intracerebral hemorrhage. Neurology. 1998;50:503–6.

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Pampiglione S, Fioravanti ML, Rivasi F. Human sparganosis in Italy. APMIS. 2003;111:349–54.

    PubMed  Article  Google Scholar 

  19. 19.

    Li N, Xiang Y, Feng Y, Li M, Li Gao B, Yun Li Q. Clinical features of pulmonary sparganosis. Am J Med Sci. 2015;350:436–41.

    PubMed  Article  Google Scholar 

  20. 20.

    Lo Presti A, Aguirre DT, De Andrés P, Daoud L, Fortes J, Muñiz J. Cerebral sparganosis: case report and review of the European cases. Acta Neurochir. 2015;157:1339–43.

    PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    Scholz T, Kuchta R, Brabec J. Broad tapeworms (Diphyllobothriidae), parasites of wildlife and humans: recent progress and future challenges. Int J Parasitol Parasites Wildl. 2019;9:359–69.

    PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Hong Q, Feng J, Liu H, Li X, Gong L, Yang Z, et al. Prevalence of Spirometra mansoni in dogs, cats, and frogs and its medical relevance in Guangzhou,China. Int J Infect Dis. 2016;53:41–5.

    PubMed  Article  Google Scholar 

  23. 23.

    Liu Q, Li MW, Wang ZD, Zhao GH, Zhu XQ. Human sparganosis, a neglected food borne zoonosis. Lancet Infect Dis. 2015;15:1226–35.

    PubMed  Article  PubMed Central  Google Scholar 

  24. 24.

    Kuchta R, Scholz T, Brabec J, Narduzzi-Wicht B. Diphyllobothrium, Diplogonoporus, and Spirometra. In: Xiao L, Ryan U, Feng Y, editors. Biology of foodborne parasites. 1st ed. Boca Raton: CRC Press; 2015. p. 299–326.

    Google Scholar 

  25. 25.

    Mueller JF. The biology of Spirometra. J Parasitol. 1974;60:3–14.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Shimalov VV, Shimalov VT. Helminth fauna of the racoon dog (Nyctereutes procyonoides Gray, 1834) in Belorussian Polesie. Parasitol Res. 2002;88:944–5.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

    Shimalov V, Shimalov V. Helminth fauna of the red fox (Vulpes vulpes Linnaeus, 1758) in southern Belarus. Parasitol Res. 2002;89:77–8.

    PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Czyżewska J, Namiot A, Koziołkiewicz K, Matowicka-Karna J, Dzięcioł J, Kemona H. The first case of human sparganosis in Poland and a review of the cases in Europe. Parasitol Int. 2019;70:89.

    PubMed  Article  PubMed Central  Google Scholar 

  29. 29.

    Waeschenbach A, Brabec J, Scholz T, Littlewood DTJ, Kuchta R. The catholic taste of broad tapeworms - multiple routes to human infection. Int J Parasitol. 2017;47:831–43.

    CAS  PubMed  Article  Google Scholar 

  30. 30.

    Eberhard ML, Thiele EA, Yembo GE, Yibi MS, Cama VA, Ruiz-Tiben E. Thirty-seven human cases of sparganosis from Ethiopia and South Sudan caused by Spirometra Spp. Am J Trop Med Hyg. 2015;93:350–5.

    PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Zhu XQ, Beveridge I, Berger L, Barton D, Gasser RB. Single-strand conformation polymorphism-based analysis reveals genetic variation within Spirometra erinacei (Cestoda: Pseudophyllidea) from Australia. Mol Cell Probe. 2002;16:159–65.

    CAS  Article  Google Scholar 

  32. 32.

    Kołodziej-Sobocińska M, Tokarska M, Kowalczyk R. The first report of sparganosis (Spirometra sp.) in Eurasian badger (Meles meles). Parasitol Int. 2014;63:397–9.

    PubMed  Article  Google Scholar 

  33. 33.

    Shimalov VV, Shimalov VT. Helminth fauna of the American mink (Mustela vison Schreber, 1777) in Belorussian Polesie. Parasitol Res. 2001;87:886–7.

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Anisimova EI. Study on the European mink Mustela lutreola helminthocenoses in connection with American mink M. vison expansion in Belarus: story of the study and review of the results. Helminthologia. 2004;41:193–6.

    Google Scholar 

  35. 35.

    Panzera O. Due casi di sparganosi nel ratto. Natura Riv Sci Nat. 1931;22:65–8.

    Google Scholar 

  36. 36.

    Joyeux B, Baer JG. Sur quelques larves de Bothriocephales. B Soc Pathol Exot. 1927;20:921–36.

    Google Scholar 

  37. 37.

    Shimalov VV. Spirometrosis and sparganosis and other diphyllobothriases in the Republic of Belarus and their medical significance. Med Parazitol (Mosk). 2009;3:48–52.

    Google Scholar 

  38. 38.

    Gastaldi B. Degli elminti in genere e di alcuni nuovi in specie. In: Cenni sopra alcuni nuovi elminti della Rana esculenta: con nuove osservazioni sul Codonocephalus mutabilis (Diesing). Turin: Tip. G. Favale e Compagnia; 1854.

  39. 39.

    Kołodziej-Sobocińska M, Stojak J, Kondzior E, Ruczyńska I, Wójcik JM. Genetic diversity of two mitochondrial DNA genes in Spirometra erinaceieuropaei (Cestoda: Diphyllobothridae) from Poland. J Zool Syst Evol Res. 2019;57:764–77.

    Article  Google Scholar 

  40. 40.

    Kołodziej-Sobocińska M, Miniuk M, Ruczyńska I, Tokarska M. Sparganosis in wild boar (Sus scrofa) - implications for veterinarians, hunters, and consumers. Vet Parasitol. 2016;227:115–7.

    PubMed  Article  Google Scholar 

  41. 41.

    Kołodziej-Sobocińska M. Factors affecting the spread of parasites in populations of wild European terrestrial mammals. Mammal Res. 2019;64:301–18.

    Article  Google Scholar 

  42. 42.

    Bagrade G, Deksne G, Ozoliņa Z, Howlett SJ, Interisano M, Casulli A, Pozio E. Echinococcus multilocularis in foxes and raccoon dogs: an increasing concern for Baltic countries. Parasit Vectors. 2016;9:615.

    PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Laurimaa L, Süld K, Davison J, Moks E, Valdmann H, Saarma U. Alien species and their zoonotic parasites in native and introduced ranges: the raccoon dog example. Vet Parasitol. 2016;219:24–33.

    PubMed  Article  Google Scholar 

  44. 44.

    Duscher T, Hodžić A, Glawischnig W, Duscher GG. The raccoon dog (Nyctereutes procyonoides) and the raccoon (Procyon lotor) - their role and impact of maintaining and transmitting zoonotic diseases in Austria, central Europe. Parasitol Res. 2017;116:1411–6.

    PubMed  PubMed Central  Article  Google Scholar 

  45. 45.

    Stricker KB, Harmon PF, Goss EM, Clay K, Flory SL. Emergence and accumulation of novel pathogens suppress an invasive species. Ecol Lett. 2016;19:469–77.

    PubMed  Article  Google Scholar 

  46. 46.

    Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM. Parasite spillback: a neglected concept in invasion ecology? Ecology. 2009;90:2047–56.

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Statistic Poland. https://stat.gov.pl/. Accessed 20 Apr 2020.

  48. 48.

    Sokołowski AW. Lasy północno-wschodniej Polski. Warszawa: Centrum Informacyjne Lasów Państwowych; 2006.

    Google Scholar 

  49. 49.

    Angelstam P, Dönz-Breuss M. Measuring forest biodiversity at the stand scale: an evaluation of indicators in European forest history gradients. Ecol Bull. 2004;51:305–32.

    Google Scholar 

  50. 50.

    State Forests Information Center. https://www.cilp.lasy.gov.pl/. Accessed 20 Apr 2020.

  51. 51.

    Jędrzejewska B, Jędrzejewski W. Predation in vertebrate communities: the Bialowieza Primeval Forest as a case study. Berlin: Springer; 2013.

    Google Scholar 

  52. 52.

    Hildreth MB, Blunt DS, Oaks JA. Lethal effects of freezing Echinococcus multilocularis eggs at ultralow temperatures. J Parasitol. 2004;90:841–4.

    CAS  PubMed  Article  Google Scholar 

  53. 53.

    Liu DW, Kato H, Sugane K. The nucleotide sequence and predicted secondary structure of small subunit (18S) ribosomal RNA from Spirometra erinaceieuropaei. Gene. 1997;184:221–7.

    CAS  PubMed  Article  Google Scholar 

  54. 54.

    BioEdit. www. bioedit.software.informer.com.

  55. 55.

    Basic Local Alignment Search Tool. www.blast.ncbi.nlm.gov/Blast.cgi.

  56. 56.

    Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993;10:512–26.

    CAS  PubMed  Google Scholar 

  57. 57.

    Wood SN. Just another Gibbs additive modeler: interfacing JAGS and mgcv. J Stat Soft. 2016;75:1–15.

    Article  Google Scholar 

  58. 58.

    Shimalov VV, Shimalov VT, Shimalov AV. Helminth fauna of otter (Lutra lutra Linnaeus, 1758) in Belorussian Polesie. Parasitol Res. 2000;86:528.

    CAS  PubMed  Article  Google Scholar 

  59. 59.

    Shimalov VV, Shimalov VT. Helminth fauna of the wolf (Canis lupus Linnaeus, 1758) in Belorussian Polesie. Parasitol Res. 2000;86:163–4.

    CAS  PubMed  Article  Google Scholar 

  60. 60.

    Shimalov VV, Shimalov VT. Helminth fauna of the European mole (Talpa europaea Linnaeus, 1758) in Belorussian Polesie. Parasitol Res. 2001;87:790–1.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  61. 61.

    Shimalov VV, Shimalov VT. Helminth fauna of the stoat (Mustela erminea Linnaeus, 1758) and the weasel (M. nivalis Linnaeus, 1758) in Belorussian Polesie. Parasitol Res. 2001;87:680–1.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  62. 62.

    Rudolphi KA. Entozoorum synopsis cui accedunt mantissa duplex et indices locupletissimi. Berlin: Sumtibus A. Rücker; 1819.

    Google Scholar 

  63. 63.

    Popiołek M, Szczęsna-Staśkiewicz J, Bartoszewicz M, Okarma H, Smalec B, Zalewski A. Helminth parasites of an introduced invasive carnivore species, the raccoon (Procyon lotor L.), from the Warta Mouth National Park (Poland). J Parasitol. 2011;97:357–60.

    PubMed  Article  PubMed Central  Google Scholar 

  64. 64.

    Kowalczyk R, Zalewski A, Jędrzejewska B, Ansorge H, Bunevich AN. Reproduction and mortality of invasive raccoon dogs (Nyctereutes procyonoides) in the Białowieża Primeval Forest (eastern Poland). Ann Zool Fenn. 2009;46:291–301.

    Article  Google Scholar 

  65. 65.

    Jedrzejewski W, Schmidt K, Theuerkauf J, Jedrzejewska B, Okarma H. Daily movements and territory use by radio-collared wolves (Canis lupus) in Bialowieza Primeval Forest in Poland. Can J Zool. 2001;79:1993–2004.

    Article  Google Scholar 

  66. 66.

    Kowalczyk R, Zalewski A, Jędrzejewska B. Daily movement and territory use by badgers Meles meles in Białowieża Primeval Forest, Poland. Wildlife Biol. 2006;12:385–91.

    Article  Google Scholar 

  67. 67.

    Jędrzejewski W, Schmidt K, Okarma H, Kowalczyk R. Movement pattern and home range use by the Eurasian lynx in Białowieża Primeval Forest (Poland). Ann Zool Fenn. 2002;39:29–41.

    Google Scholar 

  68. 68.

    Czernik M, Kowalczyk R, Zalewski A. Spatio-temporal variation of predator diet in a rural habitat: stone martens in the villages of Białowieża forest. Mammal Res. 2016;61:187–96.

    Article  Google Scholar 

  69. 69.

    Wereszczuk A, Leblois R, Zalewski A. Genetic diversity and structure related to expansion history and habitat isolation: stone marten populating rural-urban habitats. BMC Ecol. 2017;17:46.

    PubMed  PubMed Central  Article  Google Scholar 

  70. 70.

    Molin R. Prospectus helminthum, quae in prodromo faunae helminthologicae Venetiae continentur. Sitz-Ber K Akad Wiss, Math-Naturwiss Cl. 1858;30:127–58.

    Google Scholar 

  71. 71.

    Szczęsna J, Popiołek M, Schmidt K, Kowalczyk R. Coprological study on helminth fauna in Eurasian Lynx (Lynx lynx) from the Białowieża Primeval Forest in eastern Poland. Parasitology. 2008;94:981–4.

    Article  Google Scholar 

  72. 72.

    Odening K, Bockhardt I. Zwei europaische Spirometra-Formen (Cestoidea: Diphyllobothriidae) mit unterschiedlichem Sparganum Growth Factor. Angew Parasitol. 1982;23:15–27.

    CAS  PubMed  Google Scholar 

  73. 73.

    Huck M, Jędrzejewski W, Borowik T, Miłosz-Cielma M, Schmidt K, Jędrzejewska B, et al. Habitat suitability, corridors and dispersal barriers for large carnivores in Poland. Acta Theriol. 2010;55:177–92.

    Article  Google Scholar 

  74. 74.

    Kauhala K, Kowalczyk R. Invasion of the raccoon dog Nyctereutes procyonoides in Europe: history of colonization, features behind its success, and threats to native fauna. Curr Zool. 2011;57:584–98.

    PubMed  PubMed Central  Article  Google Scholar 

  75. 75.

    Mullins J, McDevitt AD, Kowalczyk R, Ruczyńska I, Górny M, Wójcik JM. The influence of habitat structure on genetic differentiation in red fox populations in north-eastern Poland. Acta Theriol. 2014;59:367–76.

    PubMed Central  Article  PubMed  Google Scholar 

  76. 76.

    Schmidt K. Maternal behaviour and juvenile dispersal in the Eurasian lynx. Acta Theriol. 1998;43:391–408.

    Article  Google Scholar 

  77. 77.

    Niedziałkowska M, Kończak J, Czarnomska S, Jędrzejewska B. Species diversity and abundance of small mammals in relation to forest productivity in northeast Poland. Ecoscience. 2010;17:109–19.

    Article  Google Scholar 

  78. 78.

    Reperant LA, Hegglin D, Fischer C, Kohler L, Weber JM, Deplazes P. Influence of urbanization on the epidemiology of intestinal helminths of the red fox (Vulpes vulpes) in Geneva. Switzerland. Parasitol Res. 2007;101:605–11.

    PubMed  Article  Google Scholar 

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Acknowledgements

We would like to thank the Associate Editor Jesus Servando Hernandez-Orts and two anonymous reviewers for the comprehensive and accurate comments which allowed us to improve the manuscript. We also thank hunters who collected carnivore carcasses during predator control for the projects: “Active protection of lowland populations of capercaillie in the Bory Dolnośląskie Forest and Augustowska Primeval Forest” (LIFE11 NAT/PU428) and “Active protection of the black grouse the land managed by State Forests in Poland” as well as many volunteers who collected carcasses in BPF. We also would like to thank Ewelina Hapunik, Dariusz Chilecki, Iwona Ruczyńska and Eugeniusz Bujko-workers from the Mammal Research Institute Polish Academy of Sciences for their technical assistance and Anita Michalak for English corrections.

Funding

This study was supported by the National Science Centre, Poland (Grant Number 2016/21/B/NZ8/02429).

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Contributions

EK carried out material collection, data analysis, drafting of the manuscript and the literature review. RK designed the research concept and performed manuscript editing. MT carried out genetic analyses and interpretation of results. TB performed statistical analyses. AZ carried out material collection and manuscript editing. MKS completed the research concept and design, funding acquisition, material and data collection, literature review, manuscript editing and supervised the study. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Eliza Kondzior.

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Not applicable. According to National Ethics Committee for Animal Experiments resolution no. 22/2006, no separate permission from the Local Ethics Committee for Animal Experimentation was needed to collect biological material from dead animals.

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The authors declare that they have no competing interests.

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Supplementary information

Additional file 1: Table S1.

Spirometra erinaceieuropaei larvae isolated from different mammalian host species which were analysed genetically with accession numbers of obtained sequences. Abbreviations: BPF, Białowieża Primeval Forest; KF, Knyszyn Forest.

Additional file 2: Figure S1.

18S rRNA gene fragment (222 bp) alignment of Spirometra erinacei (GenBank: D64072.1, KX528090 and KY552801) and DNA of Spirometra individuals extracted from 9 different mammal species combined with 3 related plathyhelminth species, Diphyllobothrium latum, Taenia krabbei and Taenia pisiformis. The newly generated sequences are indicated in bold; the sequences of Spirometra from the European badger, wild boar, and grass snake have been published in 2014, 2016 and 2018 [9, 32, 40]. Dots indicate nucleotide identity with the reference sequence (Polecat 50L_4). The alignment shows almost complete genetic homogeneity in most cases of Spirometra erinaceieuropaei from various mammalian species from north-eastern Poland.

Additional file 3: Figure S2.

Maximum likelihood phylogenetic tree of 225 bp sequences of the 18S RNA gene fragment based on 38 sequences of Spirometra sp. individuals extracted from mammal and reptile species and reference sequences retrieved from GenBank: Spirometra erinacei (D64072.1); Taenia krabbei (MH843684.1); and Taenia pisiformis (JX317675.1). The sequences generated in the present study are indicated in bold. Spirometra DNA sequences from the European badger, wild boar, and grass snake had been published by Kołodziej-Sobocińska et al. [32, 40] and Kondzior et al. [9]. The tree is drawn to scale, the scale-bar indicates the number of substitutions per site.

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Kondzior, E., Kowalczyk, R., Tokarska, M. et al. Multispecies reservoir of Spirometra erinaceieuropaei (Cestoda: Diphyllobothridae) in carnivore communities in north-eastern Poland. Parasites Vectors 13, 560 (2020). https://doi.org/10.1186/s13071-020-04431-5

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Keywords

  • Sparganosis
  • Plerocercoid larvae
  • Paratenic hosts
  • European badger
  • Raccoon dog
  • Zoonosis