Spirometra

Scholz, Tomáš, Kuchta, Roman & Brabec, Jan, 2019, Broad tapeworms (Diphyllobothriidae), parasites of wildlife and humans: Recent progress and future challenges, International Journal for Parasitology: Parasites and Wildlife 9, pp. 359-369 : 364-366

7. Spirometra & sparganosis: current problems and prospects

Species of the genus Spirometra have been recognised as intestinal parasites of carnivores for a long time, but still remain unsatisfactorily known ( Daly, 1981; Kuchta and Scholz, 2017). Despite numerous attempts to clarify their taxonomy, host specificity and geographical distribution ( Faust et al., 1929; Wardle et al., 1974), the genus remains one of the most complicated groups of tapeworms. Iwata (1934, 1972), Mueller (1974) and Odening (1985) concluded that it is almost impossible to distinguish some of nearly 50 nominal species of Spirometra based on morphological characteristics only ( Table 2). In the last revision of the family, Kamo (1999) recognised only four species as valid; Kuchta and Scholz (2017) accepted this taxonomic view. Our preliminary molecular data (LSU and cox 1) comparisons of isolates of Spirometra from several biogeographical regions indicate that the actual species diversity of the genus is higher and different than assumed by previous authors including Kamo (1999) and Kuchta and Scholz (2017). Taxonomy of this genus should thus be regarded as in its infancy thanks to the numerous problems with species circumscription and distinguishing remain to be resolved using methods of integrative taxonomy applied to newly collected and properly processed material ( Kuchta and Scholz, 2017).

Unfortunately, general uniformity of most species, their high intraspecific variability and lack of agreement among investigators as to species circumscription has led to confusion about the classification of Spirometra ( Mueller, 1974; Daly, 1981; Kuchta and Scholz, 2017). Moreover, most of the available material was obtained from host examined long time post mortem or even from decomposed carcasses, which may have caused significant morphological changes (Hernández-Orts et al., 2015). Live tapeworms obtained from experimentally infected hosts were usually fixed under pressure or following their relaxation in saline or tap water, which may have also led to unnatural changes in worms’ morphology and anatomy. As a result, morphological and biometrical data in some species descriptions may be misleading or even erroneous, which seriously impedes reliable species identification of individual taxa.

Similarly, most clinical samples of larval stages (plerocercoids called ‘sparganum’; plural ‘spargana’) were not characterised molecularly and were described under four different names ( Table 2). In many cases, no voucher material has been preserved for many records to confirm identification. Poorly resolved taxonomy and classification of the genus have also led to apparently erroneous reports, such as repeated identification of isolates from southeastern Asia as the South American species S. decipiens and the European S. ranarum in Myanmar ( Jeon et al., 2015, 2018). Cosmopolitan distribution of the type species, S. erinaceieuropaei , is also questionable and should be confirmed by a critical study of isolates from throughout the world, mainly from Europe. This species was described from Europe and its occurrence may be limited.

Another serious limitation that has considerably contributed to the existing deplorable situation in the taxonomy of Spirometra is very poor morphological description of the type species, S. erinaceieuropaei , originally based on larvae (plerocercoids) from a European hedgehog ( Erinaceus europaeus ) from an unknown locality in Europe. It is desirable to obtain presumably conspecific adults and larvae from Europe for a detailed morphological and molecular characterisation of the type species and its differentiation from other congeneric species ( Odening and Bockhardt, 1982; Qiu and Qiu, 2009; Kuchta and Scholz, 2017). However, adults of Spirometra are reported from Europe very rarely and prevalence of infection of carnivorans with adults is apparently very low and restricted to a few localities such as Białowieża National Park in Poland, Belarus, Lithuania, Ukraine or Bulgaria ( Odening, 1985; Kornyushin et al., 2011; Kołodziej-Sobocińska and Miniuk, 2018).

Molecular data on Spirometra have been collected intensively, but nearly exclusively for isolates from China and Korea, including complete characterisation of a total number of eight mitochondrial genomes ( Zhang et al., 2017). While the available mitochondrial sequence-based comparisons document only very low levels of genetic differentiation within the Asian isolates ( Eom et al., 2015; Jeon et al., 2015; Zhang et al., 2015, 2016, 2017), the relatively sporadic (and mostly highly fragmentary) sequence data on Spirometra from remaining regions suggest there is far greater diversification among geographically distant (and presumably individual species-level) taxa (Almeida et al., 2016; Eberhard et al., 2015; Petrigh et al., 2015; Waeschenbach et al., 2017). Based on this simple observation, one could expect that any sequence data of isolates from under-sampled geographical localities (Europe, Africa, the Americas) will allow to obtain far greater insights into the taxonomical richness of the genus.

The life cycle is known only partially for a few species of Spirometra ( Daly, 1981; Kuchta and Scholz, 2017). Planktonic crustaceans (copepods) serve as the first and a wide range of tetrapods as the second intermediate or paratenic hosts. Identification of spargana from these hosts to the species level using morphological tools is impossible. The larvae are most commonly found in frogs and reptiles that serve as source of infections of mammals ( Magnino et al., 2009; Oda et al., 2016). They may also occur in a spectrum of wild mammals such as badgers, baboons, feral swines, macaques, monotremes, raccoons, but also in cats and dogs and other domestic animals ( Keeling et al., 1993; Nobrega-Lee et al., 2007; Stief and Enge, 2011; Woldemeskel, 2014). As many as 128 spargana have been found in a single badger ( Meles meles ) in the Białowieża Primeval Forest in Poland ( Kołodziej-Sobocińska et al., 2014). It is of special interest that some of the above-listed mammals may serve as both intermediate/paratenic and definitive hosts – raccoons, foxes, hyenas, etc. ( Daly, 1981; Buergelt et al., 1984; Bengtson and Rogers, 2001; Bauchet et al., 2013).

Species of Spirometra are distributed around the globe, throughout much of the tropics and subtropics, but also in part of Europe and Americas ( Daly, 1981; Kuchta et al., 2015); Fig. 3 ). The prevalence of infection in the definitive as well as intermediate hosts seems to be usually very low (around 1.5% in South America – Oda et al., 2016). Exceptions include some endemic areas in Asia (e.g., in China prevalence up to 40% – Hong et al., 2016) or few studies from Serbia reporting prevalence in pigs up to 57% and from Russia in grass snake ( Natrix natrix ) up o 100% ( Dubinina, 1951; Rukavina et al., 1957; Ryzhenko, 1969).

Whereas adults of Spirometra hardly cause any pathology, the penetration and migration of plerocercoids through tissues of intermediate and incidental hosts typically result in clinical manifestations ( Daly, 1981). Adults of Spirometra are capable of maturing in the human intestine, causing rather rare disease spirometrosis, usually lacking any clinical symptoms ( Lee et al., 1984; Wang et al., 2012; Le et al., 2017). In contrast, spargana often cause serious disease in humans and other vertebrates (mammals) called sparganosis ( Daly, 1981; Bauchet et al., 2013). More than 1,600 human cases have been reported globally so far, with the number of patients recently increasing in endemic areas, especially in China and South East Asia ( Liu et al., 2015). Larvae are usually located in the subcutaneous tissue and muscles of the host or alternatively invade other internal organs ( Liu et al., 2015; Kuchta et al., 2015). In rare cases, sparganosis may result in fatalities, manifesting mostly as a so-called proliferative sparganosis caused by closely uncharacterised taxonomic entity called Sparganum proliferum ( Moulinier et al., 1982; Kuchta et al., 2015). Fatal proliferative sparganosis was also reported from domestic cats in North America ( Buergelt et al., 1984; Woldemeskel, 2014) and dog in Europe ( Stief and Enge, 2011).

Spargana may cause rapid growth in hypophysectomised or thyroidectomised rats, and exert an ameliorative effect in the diabetic rat ( Mueller, 1974; Odening, 1985). The growth response is due to a protein that is synthesised and released by plerocercoids in the host called ‘sparganum growth factor’ (SGF) or ‘plerocercoid growth factor’ (PGF). It is transported by the blood and interacts with growth hormone receptors ( Phares, 1996). This activity is not yet well understood, but it illustrates the clear impact of larvae of Spirometra on the second intermediate, paratenic or accidental host.

Figures

Fig. 3. Distribution of two genera of diphyllobothriid tapeworms from wildlife and man. A – Dibothriocephalus spp., B – Spirometra spp. Based on available literature data by countries except for some large countries where occurrence was estimated based on data available (Russia, China, etc.).