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. 2021 Apr 14;1:100023. doi: 10.1016/j.crpvbd.2021.100023

Perspectives on intestinal tapeworm infections: An evaluation of direct and indirect life-cycles with a special emphasis on species of Hymenolepis

Akira Ito a, Christine M Budke b,∗
PMCID: PMC8906094  PMID: 35284891

Abstract

Numerous experimental studies have been conducted on the rodent tapeworm, Hymenolepis microstoma. In contrast, less is known about the life-cycle and immunobiology of the zoonotic dwarf tapeworm, Hymenolepis nana. However, H. nana appears to be unique in that; (i) it can complete its entire life-cycle within a single mammalian host, and (ii) cysticercoids that develop in beetle intermediate hosts are tailed, while those that develop in the intestinal tissue of mammals are tailless. This is in contrast to all other Hymenolepis spp., which only appear to develop tailed cysticercoids in beetles or experimentally infected immunodeficient rodents. Even though H. microstoma and H. nana are phylogenetically much closer to each other than to Hymenolepis diminuta, when mice with severe combined immunodeficiency (SCID) were inoculated with H. microstoma eggs, hatched oncospheres invaded the intestinal tissue and developed into infective tailed cysticercoids in approximately 11 days. Therefore, H. nana appears to be truly unique in its ability to develop tailed cysticercoids in beetles and tailless cysticercoids in mammals. These unique evolutionary characteristics are discussed in relation to other cyclophyllidean cestodes, including Taenia solium and Echinococcus spp.

Keywords: Hymenolepis nana, Hymenolepis microstoma, Tailed cysticercoid, Tailless cysticercoid, Evolution from indirect to direct life-cycle

Graphical abstract

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Highlights

  • •

    Hymenolepis nana is unique in that it can complete its entire life-cycle within a single mammalian host.

  • •

    The ability to develop tailless cysticercoids in mammals may be an evolutionary adaption for H. nana.

  • •

    Adult cestode lifespan may be a good indicator as to whether or not a particular species can have a direct life-cycle.

1. Introduction

Cestodes belonging to the genus Hymenolepis use arthropods, most commonly beetles belonging to the species Tribolium or Tenebrio, as intermediate hosts. These beetles harbor cysticercoid larvae. Rodents and other small mammals act as definitive hosts, which harbor adult tapeworms in the intestine or bile duct, as is the case for Hymenolepis microstoma (the mouse bile duct tapeworm). Hymenolepis nana (the mouse tapeworm) and Hymenolepis diminuta (the rat tapeworm) are well known zoonotic tapeworms (Arai, 1980). Among the three species, H. diminuta is phylogenetically distant from H. nana and H. microstoma (Okamoto et al., 1997; Jarošová et al., 2020). Adult worms of most species in this genus live for one to two years, which typically corresponds to the lifespan of the host rodent (Arai, 1980; Andreassen, 2010). The exceptions include H. nana, which survives less than one month and possibly H. microstoma, which survives in the bile duct for at least six months but likely less than a year. Therefore, the H. nana lifespan appears to be shortest followed by H. microstoma (Ito & Smyth, 1987; Cunningham & Olson, 2010).

The difference in lifespan is possibly related to H. nana evolutionarily establishing a direct life-cycle (i.e. via ingestion of parasite eggs) versus only the indirect life-cycle (i.e. via ingestion of cysticercoids) found in all other species of Hymenolepis, including H. microstoma. Due to this difference, H. microstoma does not appear to be a good model to study H. nana and other taeniids that have alternative direct life-cycles consisting of intestinal tapeworm infection followed by larval stage development in parenteral tissue after egg ingestion. In many ways, H. nana has more similarities with the zoonotic taeniids, Taenia solium and Echinococcus spp. than with other members of the genus Hymenolepis. For example, while T. solium completes its entire life-cycle between pigs (intermediate hosts) and humans (definitive host), humans can also be infected with eggs through autoinfection or from other tapeworm carriers. Among the three human-infecting Taenia, which include T. solium, Taenia saginata, and the ‘Asian Taenia’ (T. saginata asiatica) (Fan et al., 1995; Okamoto et al., 2010; Yamane et al., 2012; Ito & Budke, 2021), T. solium, exclusively causes cysticercosis in humans. Although less common, Echinococcus infection in the definitive host may result in infection with the larval stage of the parasite, causing cystic or alveolar echinococcosis (Ishino, 1941; Weiss & Köhler, 2010; Konyaev et al., 2012; Gottstein et al., 2014; Conraths & Deplazes, 2015; Frey et al., 2017; Antolová et al., 2018; Zajac et al., 2020). This paper focuses on the establishment of indirect and direct life-cycles for cyclophyllidean cestodes and builds upon previous reviews of these parasites (Ito, 2015, 2016; Ito & Budke, 2021).

2. Hymenolepis nana

Definitive hosts for the H. nana tapeworm include rodents and other small mammals and humans. These hosts are infected through ingestion of eggs (direct cycle) or metacestodes (cysticercoids) located in beetles and other intermediate hosts (indirect cycle). All developmental stages, including oncospheres, cysticercoids, and adult tapeworms appear to be immunogenic, resulting in stage-specific immunity to reinfection (Ito, 1984; Ito & Onitake, 1986; Ito & Smyth, 1987). When a definitive host becomes infected via the direct cycle, oncospheres invade the intestinal tissue and the host becomes immune to reinfection within a few days (Hunninen, 1935; Heyneman, 1962; Weinmann, 1966; Okamoto, 1970; Okamoto & Koizumi, 1972; Asano et al., 1986; Asano & Okamoto, 1992; Asano & Muramatsu, 1997). A host may become immune after only a single oncosphere invades the intestinal wall ( Ito & Yamamoto, 1976). When a definitive host is infected with H. nana eggs, the resulting mature tapeworms produce eggs. However, there is no autoinfection due to acquired immunity to the parasite eggs, which occurs within 4 days after primary infection with eggs. Oncospheres from reinfection may invade the intestinal tissue, but do not develop into cysticercoids ( Ito & Smyth, 1987).

Similar to the direct infection cycle, definitive hosts infected via ingestion of H. nana cysticercoids, found in beetle intermediate hosts, produce adult worms that release eggs. However, when a definitive host is experimentally infected with cysticercoids, either from beetles or other rodents, autoinfection resulting in large second-generation stunted worms can occur in some strains of mice (Ito & Kamiyama, 1984; Ito, 1985; Ito et al., 1988) (see figure 1 in Ito, 2015). Adult tapeworm longevity and autoinfection are affected by the host immune response to the lumen phase of H. nana cysticercoids and adult tapeworms, but the timing of this response is highly variable among mouse strains. Usually, within one month of infection, the adult tapeworms become stunted and disappear ( Ito & Smyth, 1987). However, adult worm longevity is variable among hosts. The mechanism by which this stunting occurs remains unknown.

There are several H. nana strains that do not appear to cause autoinfection (Ito, 1982; Ito et al., 1988). This may be explained by the rapid onset of immunity to the parasite’s lumen phase before eggs are released from cysticercoid-derived adult tapeworms. However, other unknown factors may be involved. The indirect cycle can be established in small mammal definitive hosts by feeding them cysticercoids. Some strains of H. nana do not mature in rats, including congenitally athymic nude rats (Ito, 1983; Ito & Kamiyama, 1984; Ito, 1985), but instead the rats develop cysticercoids. There does not appear to be a difference in antigenicity of H. nana cysticercoids developed in beetles compared to those developed in small mammals (Ito & Onitake, 1987). An interesting phenomenon is that H. nana cysticercoids that develop in mammals (e.g. mice, rats, hamsters) have no tails and have been named ‘tailless cysticercoids’, while those in beetles have tails and are called ‘tailed cysticercoids’. The tailless variety of cysticercoids does not appear to be present in any other hymenolepidid species.

Infective H. nana cysticercoids develop in mouse intestinal tissue within 4 days and escape into the intestinal lumen to develop into adult tapeworms. However, in immunodeficient mice, some oncospheres migrate to the liver similar to certain taeniid species and some cysticercoids become established in deeper intestinal tissues and the liver where they remain as balloon-like cysticercoids (Ito & Kamiyama, 1984; Ito, 1985; Ito, 2015) (see figure 1 in Ito, 2016). The presence of cysticercoids in the mouse liver suggests a possible alternative cycle by cannibalism if the parasite can complete its life-cycle outside of the mouse intestine.

All species belonging to the genus Hymenolepis mature into adult tapeworms in small mammals and primarily use beetles as intermediate hosts. Hymenolepis nana is more common in mice than in rats (Ogura, 1936; Soh et al., 1961). For example, an isolate first maintained in mice located in a laboratory in Tokyo, Japan, more than 50 years ago does not mature in rats (Okamoto, 1970; Ito & Kamiyama, 1984; Ito, 1985). Molecular studies will be informative to further evaluate any differences in mouse-adapted versus rat-adapted H. nana isolates. All H. nana isolates are also known to be infective to humans (Weinmann, 1966). A recent study conducted in Mexico where both H. nana and H. microstoma are known to occur revealed that all hymenolepidid eggs identified in children were H. nana (see Panti-Maya et al., 2020). Thus far, H. nana and H. diminuta are the only known truly zoonotic species in the genus Hymenolepis. However, other species may occasionally infect humans as evidenced by the recovery of an Hymenolepis hibernia adult worm from a 52-year-old Tibetan woman (Nkouawa et al., 2015).

3. Hymenolepis microstoma

In contrast to H. nana, more is known about H. microstoma and the parasite’s full genome has been analyzed (Cunningham & Olson, 2010; Tsai et al., 2013). Hymenolepis microstoma adults, whose scolices attach to the bile duct, can survive approximately six months without reinfection (Jarošová et al., 2020). In this species, fully mature tailed cysticercoids develop approximately 11 days after egg inoculation in mice with severe combined immunodeficiency (SCID) (Andreassen et al., 2004). When mice infected with H. microstoma were housed in the same cage with uninfected mice, the uninfected mice eventually showed antibody responses to H. microstoma oncospheres (Ito et al., 1989). This suggests that even though H. microstoma has not been shown to have a direct life-cycle, oncospheres may still hatch and invade intestinal tissue (Onitake et al., 1990).

Gene expression, in H. microstoma, allows it to hatch in the intestines of mammalian hosts, developing into tailed cysticercoids in immunodeficient mice (Andreassen et al., 2004). Experimental infection of congenitally athymic nude mice with H. microstoma eggs resulted in few cysticercoids in the intestinal tissue. When these SCID mice were then infected with cysticercoids, they produced first generation tapeworms in addition to a large number of tailed cysticercoids derived from autoinfection (second generation). In comparison, when congenitally athymic NMRI-nu mice infected with cysticercoids, which later became adult H. microstoma, were allowed to eat their own feces containing tapeworm eggs, the oncospheres penetrated the intestinal tissue and developed into cysticercoids. After excysting, the parasites grew into adult worms in the lumen of the small intestine and bile duct. The same outcome occurred when NMRI-nu mice, non-obese diabetic SCID (NOD/Shi-scid) mice, and NOD/Shi-scid, IL-2 Rynull (NOG) mice were orally inoculated with H. microstoma eggs (Andreassen et al., 2004).

In summary, differences between H. microstoma and H. nana cysticercoid development in mouse intestinal tissues include: (i) the time course for development of infective cysticercoids was approximately 11 days for H. microstoma, but only 4 days for H. nana; and (ii) H. microstoma cysticercoids that developed in mice had tails, while those of H. nana had no tails. Therefore, H. nana appears to be unique among Hymenolepis tapeworms in its ability to adapt to direct infection, with resulting unique morphologic characteristics (i.e. the production of tailless cysticercoids).

4. Comparison of the Hymenolepididae and Taeniidae

Experimental studies in rodents have shown that host immunity can occur after a single egg has invaded the intestinal wall for both H. nana (see Ito & Yamamoto, 1976) and Taenia taeniaeformis (see Ito & Hashimoto, 1993). In addition, the speed at which differentiation from oncosphere to metacestode occurs may contribute to the variability in immune response between taeniid species (Okamoto et al., 2005). Unlike taeniid eggs that require mammalian bile salts to hatch, hymenolepidid oncospheres are easily hatched and activated in vivo and in vitro without the use of a stimulative solution (Laws, 1968). Physiological or mechanical stimulation is sufficient to activate and hatch the oncospheres. This difference may be related to the short lifespan of Hymenolepis spp. compared to some taeniids (Yoshino, 1934; Garcia et al., 2003; Lightowlers, 2010; Li et al., 2019; Zein et al., 2019; Ito et al., 2020; Ito & Budke, 2021).

Among the taeniids, T. solium is exceptional in that human infection regularly occurs through ingestion of parasite eggs (resulting in cysticercosis) or cysticerci (resulting in taeniasis). Infection with Echinococcus spp. eggs has been reported in carnivorous and omnivorous definitive hosts, resulting in echinococcosis (Ishino, 1941; Konyaev et al., 2012; Corsini et al., 2015; Ito, 2016; Fley et al., 2017; Antolová et al., 2018). However, at this time, there is no indication that other human-infecting Taenia spp. (T. saginata and ‘Asian Taenia’) can result in human cysticercosis. While there has been some conjecture regarding human cysticercosis caused by ‘Asian Taenia’, no evidence is currently available to support this hypothesis (McManus, 1996, 2006; Ito & Budke, 2021). Based on molecular findings, some researchers believe ‘Asian Taenia’ to be an intraspecies variant of T. saginata and T. saginata asiatica (Zarlenga et al., 1991; Bowles & McManus, 1994; McManus & Bowles, 1994; Fan et al., 1995; Gasser et al., 1999; Okamoto et al., 2007, 2010; Yamane et al., 2012, 2013), while others believe it to be a unique species, Taenia asiatica (see Eom & Rim, 1993). Regardless, serological screening in populations located in Sichuan, China, where T. solium, T. saginata, and ‘Asian Taenia’ are sympatrically distributed, appears to further support the idea that cysticercosis is exclusively caused by T. solium (see Li et al., 2019).

Overall, adult parasite lifespan may be a good indicator as to whether or not the species may have a direct life-cycle. For example, H. nana is known to have a short life-span, while there is some evidence that the T. solium lifespan is also short, with a hypothesized lifespan less than five years (Yoshino, 1934; Garcia et al., 2003; Lightowlers, 2010;Li et al., 2019; Zein et al., 2019; Ito et al., 2020; Ito & Budke, 2021). In contrast, the other human taeniids, T. saginata and ‘Asian Taenia’, are known to live as long as 50 years (Li et al., 2019; Zein et al., 2019).

5. Perspectives

The question arises of what are the next steps in trying to better understand infection by Hymenolepis spp. and other cyclophyllidean cestodes. First, it would be beneficial to experimentally infect mice or rats with H. diminuta eggs and see if pathogen-free rodents kept in the same cage develop an antibody response (Ito et al., 1989), similar to what was seen with H. microstoma. If uninfected rodents show antibody responses to oncosphere antigens, the next step would be to duplicate the experiment using congenitally athymic nude rats or SCID rats. This type of study can also be applied to Taenia spp. and Echinococcus spp. (Nakaya et al., 2006; Nakao et al., 2007, 2013a, b). Secondly, if other cyclophyllidean cestode species besides H. nana, T. solium, and Echinococcus spp. are found to have relatively short lifespans in the definitive hosts, studies will need to be conducted to evaluate if definitive hosts can also become infected via the ingestion of parasite eggs. These types of studies may help clarify why the larval stage of T. solium is able to develop in the definitive host (Hoberg et al., 2001; Nakao et al., 2002), while this is not possible for T. saginata and ‘Asian Taenia’ (Ito et al., 2003; Li et al., 2019; Ito & Budke, 2021). A final research theme to evaluate in greater detail is the mechanism for the rapid onset (within a few days) of reinfection with eggs from H. nana (see Okamoto, 1970; Okamoto & Koizumi, 1972; Asano et al., 1986; Asano & Okamoto, 1992; Asano & Muramatsu, 1997) and other species in the family Taeniidae. This rapid onset appears to be independent from antibody responses and requires additional research beyond what has been conducted for vaccine development (Rickard & Williams, 1982; Johnson et al., 1989; Ito et al., 1991; Lightowlers et al., 1993).

Funding

There was no funding associated with this work.

CRediT author statement

AI prepared the initial draft. CMB and AI edited the manuscript for content and language.

Declaration of competing interests

The authors declare that they have no competing interests.

References

  1. Andreassen J. In: Topley & Wilson’s Microbiology & Microbial Infections: Parasitology. 10th ed. Cox F.E.G., Wakelin D., Gillespie S., Despommier D.D., editors. John Wiley & Sons; New York: 2010. Intestinal tapeworms; pp. 658–676. [Google Scholar]
  2. Andreassen J., Ito A., Ito M., Nakao M., Nakaya K. Hymenolepis microstoma: direct life cycle in immunodeficient mice. J. Helminthol. 2004;78:1–5. doi: 10.1079/joh2003207. [DOI] [PubMed] [Google Scholar]
  3. Antolová D., Vichová B., Jarošová J., Gál V., Bajužík B. Alveolar echinococcosis in a dog; analysis of clinical and historical findings and molecular identification of Echinococcus multilocularis. Acta Parasitol. 2018;63:486–494. doi: 10.1515/ap-2018-0058. [DOI] [PubMed] [Google Scholar]
  4. Arai H. Academic Press; New York: 1980. Biology of the tapeworm Hymenolepis diminuta. [Google Scholar]
  5. Asano K., Muramatsu K. Importance of interferon-gamma in protective immunity against Hymenolepis nana cysticercoids derived from challenge infection with eggs in BALB/c mice. Int. J. Parasitol. 1997;27:1437–1443. doi: 10.1016/s0020-7519(97)00106-9. [DOI] [PubMed] [Google Scholar]
  6. Asano K., Okamoto K. Transfer of T-cell mediated immunity to Hymenolepis nana from mother mice to their neonates. Experientia. 1992;48:67–71. doi: 10.1007/BF01923611. [DOI] [PubMed] [Google Scholar]
  7. Asano K., Shinoda M., Nakamura F., Okamoto K. Hymenolepis nana: passive transfer of mouse immunity by T-cell subset of phenotype Lyt-1. Exp. Parasitol. 1986;61:373–378. doi: 10.1016/0014-4894(86)90193-1. [DOI] [PubMed] [Google Scholar]
  8. Bowles J., McManus D.P. Genetic characterization of the Asian Taenia, a newly described taeniid cestode of humans. Am. J. Trop. Med. Hyg. 1994;50:33–44. [PubMed] [Google Scholar]
  9. Conraths F.J., Deplazes P. Echinococcus multilocularis: epidemiology, surveillance and state-of-art diagnostics from a veterinary public health perspective. Vet. Parasitol. 2015;213:149–161. doi: 10.1016/j.vetpar.2015.07.027. [DOI] [PubMed] [Google Scholar]
  10. Corsini M., Geissbuhler U., Howard J., Gottstein B., Speng U., Fery C.F. Clinical presentation, diagnosis, therapy and outcome of alveolar echinococcosis in dogs. Vet. Rec. 2015;177:69. doi: 10.1136/vr.103470. [DOI] [PubMed] [Google Scholar]
  11. Cunningham L.J., Olson P.D. Description of Hymenolepis microstoma (Nottingham strain): a classical tapeworm model for research in the genomic era. Parasit. Vectors. 2010;3:123. doi: 10.1186/1756-3305-3-123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Eom K.S., Rim H.J. Morphologic description of Taenia asiatica sp. n. Kor. J. Parasitol. 1993;31:1–6. doi: 10.3347/kjp.1993.31.1.1. [DOI] [PubMed] [Google Scholar]
  13. Fan P.C., Lin C.Y., Chen C.C., Chung W.C. Morphological description of Taenia saginata asiatica (Cyclophyllidea: Taeniidae) from man in Asia. J. Helminthol. 1995;69:299–303. doi: 10.1017/s0022149x00014863. [DOI] [PubMed] [Google Scholar]
  14. Fley C.F., Marreros N., Renneler S., Schmidt L., Sager H., Hendrich B., et al. Dogs as victim of their own worms: serodiagnosis of canine alveolar echinococcosis. Parasit. Vectors. 2017;10:422. doi: 10.1186/s13071-017-2369-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Garcia H.H., Gilman R.H., Gonzalez A.E., Verastegui M., Rodriguez S., Gavidia C., et al. Hyperendemic human and porcine Taenia solium infection in Peru. Am J Trop Med Hyg. 2003;68:268–275. [PubMed] [Google Scholar]
  16. Gasser R.B., Zhu X., McManus D.P. NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequences compared for members of the genus Taenia (Cestoda) Int. J. Parasitol. 1999;29:1965–1970. doi: 10.1016/s0020-7519(99)00153-8. [DOI] [PubMed] [Google Scholar]
  17. Gottstein B., Frey C.F., Campbell-Palmer R., Pizzi R., Barlow A., Hentrich B., et al. Immunoblotting for the serodiagnosis of alveolar echinococcosis in alive and dead Eurasian beavers (Castor fiber) Vet. Parasitol. 2014;205:113–118. doi: 10.1016/j.vetpar.2014.06.017. [DOI] [PubMed] [Google Scholar]
  18. Heyneman D. Studies on helminth immunity. IV. Rapid onset of reinfection by the white mouse against a challenging infection with eggs of Hymenolepis nana (Cestoda: Hymenolepididae) J. Immunol. 1962;88:210–220. [PubMed] [Google Scholar]
  19. Hoberg E.P., Alkire N.L., de Queiroz A., Jones A. Out of Africa: origin of Taenia worms in humans. Proc. Biol. Sci. 2001;268:781–787. doi: 10.1098/rspb.2000.1579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hunninen A.V. Studies on the life history and host-parasite relations of Hymenolepis fraterna (H. nana var. fraterna styles) in the white mice. Am J Epidemiol. 1935;22:414–443. [Google Scholar]
  21. Ishino H. Alveolar echinococcosis in an Arctic fox in Simushir Is., Kurile Islands. Kachiku Eisei Kyoukaihou. 1941;9:115. (in Japanese) [Google Scholar]
  22. Ito A. Hymenolepis nana: immunogenicity of a lumen phase of the direct cycle and failure of autoinfection in BALB/c mice. Exp. Parasitol. 1982;54:113–120. doi: 10.1016/0014-4894(82)90117-5. [DOI] [PubMed] [Google Scholar]
  23. Ito A. Hymenolepis nana: maturation in an immunosuppressed unnatural rat host. Exp. Parasitol. 1983;56:318–326. doi: 10.1016/0014-4894(83)90077-2. [DOI] [PubMed] [Google Scholar]
  24. Ito A. Stage-specific immunogens of Hymenolepis nana in mice. J. Helminthol. 1984;58:235–238. doi: 10.1017/s0022149x00027036. [DOI] [PubMed] [Google Scholar]
  25. Ito A. Thymus dependency of induced immune responses against Hymenolepis nana (cestode) using congenitally athymic nude mice. Clin. Exp. Immunol. 1985;60:87–94. [PMC free article] [PubMed] [Google Scholar]
  26. Ito A. Basic and applied problems in developmental biology and immunobiology of cestode infections: Hymenolepis, Taenia and Echinococcus. Parasite Immunol. 2015;37:53–69. doi: 10.1111/pim.12167. [DOI] [PubMed] [Google Scholar]
  27. Ito, A., 2016. Immunobiology in cestode infections. In: Ratcliffe, M.J.M. (Editor in Chief). Encyclopedia of immunobiology, Vol. 4. Academic Press, New York, pp. 159–165.
  28. Ito A., Bøgh H., Lightowlers M.S., Mitchell G.F., Takami T., Kamiya M., et al. Vaccination against Taenia taeniaeformis in rats using recombinant protein and preliminary analysis of the induced responses. Mol. Biochem. Parasitol. 1991;44:43–49. doi: 10.1016/0166-6851(91)90219-v. [DOI] [PubMed] [Google Scholar]
  29. Ito A., Budke C.M. Genetic diversity of Taenia solium and its relation to clinical presentation of cysticercosis. Yale J. Biol. Med. 2021 [PMC free article] [PubMed] [Google Scholar]
  30. Ito A., Hashimoto A. Vaccination with hatched but non-activated, non-viable oncospheres of Taenia taeniaeformis in rats. J. Helminthol. 1993;67:165–168. doi: 10.1017/s0022149x00013079. [DOI] [PubMed] [Google Scholar]
  31. Ito A., Itoh M., Andreassen J., Onitake K. Stage-specific antigens of Hymenolepis microstoma recognized by BALB/c mice. Parasite Immunol. 1989;11:453–462. doi: 10.1111/j.1365-3024.1989.tb00681.x. [DOI] [PubMed] [Google Scholar]
  32. Ito A., Kamiyama T. Hymenolepis nana: worm recovery from congenitally athymic nude and phenotypically normal rats and mice. Exp. Parasitol. 1984;58:132–137. doi: 10.1016/0014-4894(84)90028-6. [DOI] [PubMed] [Google Scholar]
  33. Ito A., Lightowlers M.W., Rickard M.D., Mitchell G.F. Failure of auto-infection with Hymenolepis nana in seven inbred strains of mice initially given beetle-derived cysticercoids. Int. J. Parasitol. 1988;18:321–324. doi: 10.1016/0020-7519(88)90140-3. [DOI] [PubMed] [Google Scholar]
  34. Ito A., Nakao M., Wandra T. Rapid review: human taeniasis and cysticercosis in Asia. Lancet. 2003;362:1918–1920. doi: 10.1016/S0140-6736(03)14965-3. [DOI] [PubMed] [Google Scholar]
  35. Ito A., Onitake K. Complete resistance to challenges with Hymenolepis nana cysticercoids from mouse, rat and beetle in mice. Int. J. Parasitol. 1986;16:623–628. doi: 10.1016/0020-7519(86)90030-5. [DOI] [PubMed] [Google Scholar]
  36. Ito A., Onitake K. Changes in surface antigens of Hymenolepis nana during differentiation and maturation in mice. J. Helminthol. 1987;61:129–136. doi: 10.1017/s0022149x00009871. [DOI] [PubMed] [Google Scholar]
  37. Ito A., Saito M., Donadeu M., Lightowlers M.W. Kozen Yoshino’s experimental infections with Tania solium tapeworms: an experiment never to be repeated. Acta Trop. 2020;205:105378. doi: 10.1016/j.actatropica.2020.105378. [DOI] [PubMed] [Google Scholar]
  38. Ito A., Smyth D.J. In: Immune Responses in Parasitic Infections: Immunology, Immunopathology and Immunoprophylaxis. Vol. 2: Soulsby E.J.L., editor. CRC Press; Boca Raton: 1987. Adult cestodes – immunology of the lumen-dwelling cestode infections; pp. 115–163. (Trematodes and Cestodes,). [Google Scholar]
  39. Ito A., Yamamoto M. The mode of active protection against Hymenolepis nana reinfection in mice inoculated with different doses of shell-free eggs. Jpn. J. Parasitol. 1976;25:247–253. [Google Scholar]
  40. Jarošová J., Šnábel V., Cavallero S., Chovanocová G., Hurníková Z., Antolová D. The mouse bile duct tapeworm, Hymenolepis microstoma in free-living small mammals in Slovakia: occurrence and genetic analysis. Helminthologia. 2020;57:120–128. doi: 10.2478/helm-2020-0022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Johnson K.S., Harrison G.B., Lightowlers M.W., O’Hoy K.L., Cougle W.G., Dempster R.P., et al. Vaccination against ovine cysticercosis using a defined recombinant antigen. Nature. 1989;338(6216):585–587. doi: 10.1038/338585a0. [DOI] [PubMed] [Google Scholar]
  42. Konyaev S.V., Yanagida T., Ivanov M.V., Ruppel V.V., Sako Y., Nakao M., et al. The first report on cystic echinococcosis in a cat caused by Echinococcus granulosus sensu stricto (G1) J. Helminthol. 2012;86:391–394. doi: 10.1017/S0022149X1100054X. [DOI] [PubMed] [Google Scholar]
  43. Laws G.F. The hatching of taeniid eggs. Exp. Parasitol. 1968;23:1–10. doi: 10.1016/0014-4894(68)90038-6. [DOI] [PubMed] [Google Scholar]
  44. Li T.Y., Chen X.W., Wang H., Openshaw J., Zhong B., Felt S.A., et al. High prevalence of taeniasis and Taenia solium cysticercosis in children in western Sichuan, China. Acta Trop. 2019;199:105133. doi: 10.1016/j.actatropica.2019.105133. [DOI] [PubMed] [Google Scholar]
  45. Lightowlers M.W. Eradication of Taenia solium cysticercosis: a role for vaccination of pigs. Int. J. Parasitol. 2010;40:1183–1192. doi: 10.1016/j.ijpara.2010.05.001. [DOI] [PubMed] [Google Scholar]
  46. Lightowlers M.W., Mitchell G.F., Rickard M.D. In: Immunology and Molecular Biology of Parasitic Infections. 3rd ed. Warren K.S. (Ed.), editor. Blackwell Scientific Publication; Boston: 1993. Cestodes; pp. 438–472. [Google Scholar]
  47. McManus D.P. Reply. Parasitol. Today. 1996;12:123. [Google Scholar]
  48. McManus D.P. Molecular discrimination of taeniid cestodes. Parasitol. Int. 2006;55:S31–S37. doi: 10.1016/j.parint.2005.11.004. [DOI] [PubMed] [Google Scholar]
  49. McManus D.P., Bowles J. Asian (Taiwan) Taenia: species or strain? Parasitol. Today. 1994;10:273–275. doi: 10.1016/0169-4758(94)90145-7. [DOI] [PubMed] [Google Scholar]
  50. Nakao M., Lavikainen A., Yanagida T., Ito A. Phylogenetic systematics taxonomy of the genus Echinococcus (Cestoda: Taeniidae) Int. J. Parasitol. 2013;43:1017–1029. doi: 10.1016/j.ijpara.2013.06.002. [DOI] [PubMed] [Google Scholar]
  51. Nakao M., McManus D.P., Schantz P.M., Craig P.S., Ito A. The molecular phylogeny of Echinococcus tapeworms based on complete mitochondrial genomic sequences. Parasitology. 2007;134:713–722. doi: 10.1017/S0031182006001934. [DOI] [PubMed] [Google Scholar]
  52. Nakao M., Okamoto M., Sako Y., Yamasaki H., Nakaya K., Ito A. A phylogenetic hypothesis for the distribution of two genotypes of the pig tapeworm Taenia solium worldwide. Parasitology. 2002;124:657–662. doi: 10.1017/s0031182002001725. [DOI] [PubMed] [Google Scholar]
  53. Nakao M., Yanagida T., Konyaev S., Lavikainen A., Odnokurtsev V.A., Zaikov V.A., et al. Mitochondrial phylogeny of the genus Echinococcus (Cestoda: Taeniidae) with emphasis on relationships among Echinococcus canadensis genotypes. Parasitology. 2013;140:1625–1636. doi: 10.1017/S0031182013000565. [DOI] [PubMed] [Google Scholar]
  54. Nakaya K., Mamuti W., Xiao N., Sato M.O., Wandra T., Nakao M., et al. Usefulness of severe combined immunodeficiency (scid) and inbred mice for studies of cysticercosis and echinococcosis. Parasitol. Int. 2006;55:S91–S97. doi: 10.1016/j.parint.2005.11.014. [DOI] [PubMed] [Google Scholar]
  55. Nkouawa A., Haukisalmi V., Li T., Nakao M., Lavikainen A., Chen X., et al. Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitol. Int. 2015;65:83–86. doi: 10.1016/j.parint.2015.10.009. [DOI] [PubMed] [Google Scholar]
  56. Ogura K. Studies on the Hymenolepis nana in Korea. Chosen Igakkukai Zasshi. 1936;26:649–668. (English summary 35–35) [Google Scholar]
  57. Okamoto K. Hymenolepis nana: depression and restoration of acquired immunity in neonatally thymectomized mice. Exp. Parasitol. 1970;27:28–32. doi: 10.1016/s0014-4894(70)80006-6. [DOI] [PubMed] [Google Scholar]
  58. Okamoto M., Agatsuma T., Kurosawa T., Ito A. Phylogenetic relationships of three hymenolepidid species inferred from nuclear ribosomal and mitochondrial DNA sequences. Parasitology. 1997;115:661–666. doi: 10.1017/s0031182097001741. [DOI] [PubMed] [Google Scholar]
  59. Okamoto K., Koizumi M. Hymenolepis nana: effect of antithymocyte serum on acquired immunity in mice. Exp. Parasitol. 1972;32:56–61. doi: 10.1016/0014-4894(72)90009-4. [DOI] [PubMed] [Google Scholar]
  60. Okamoto M., Matsumoto K., Shibui A., Shibahara T., Ito A. Fundamental study of expression-library immunization against Taenia taeniaeformis in rats. Southeast Asian J. Trop. Med. Public Health. 2005;36(Suppl. 4):135–138. [PubMed] [Google Scholar]
  61. Okamoto M., Nakao M., Blair D., Anantaphruti M.T., Waikagul J., Ito A. Evidence of hybridization between Taenia saginata and Taenia asiatica. Parasitol. Int. 2010;59:70–74. doi: 10.1016/j.parint.2009.10.007. [DOI] [PubMed] [Google Scholar]
  62. Okamoto M., Nakao M., Tachi E., Sako Y., Sato M.O., Yamasaki H., et al. Asian Taenia: species or subspecies? Southeast Asian J. Trop. Med. Public Health. 2007;38(Suppl. 1):125–130. [Google Scholar]
  63. Onitake K., Sasaki J., Andreassen J., Ito A. Hymenolepis microstoma: oncospheres invade the intestinal tissue of the definitive host. J. Helminthol. 1990;64:168–170. doi: 10.1017/s0022149x00012086. [DOI] [PubMed] [Google Scholar]
  64. Panti-Maya J.A., Servían A., Ferrari W., Zonta L., Hernández-Mena D.L., Hernández-Betancourt S.F., et al. Morphological and molecular identification of hymenolepidid cestodes in children and synanthropic rodents from rural Mexico. Parasitol. Int. 2020;75:102042. doi: 10.1016/j.parint.2019.102042. [DOI] [PubMed] [Google Scholar]
  65. Rickard M.D., Williams J.F. Hydatidosis/cysticercosis: immune mechanisms and immunization against infection. Adv. Parasitol. 1982;21:229–296. doi: 10.1016/s0065-308x(08)60277-8. [DOI] [PubMed] [Google Scholar]
  66. Soh C.T., Lee K.T., Shin E.W., Kang T.C. Incidence of parasites in Seoul area based on an examination of the Severance hospital out-patients. Yonsei Med. J. 1961;2:31–42. [Google Scholar]
  67. Tsai I.J., Zarowiecki M., Holroyd N., Garciarrubio A., Sánches-Flores A., Brooks K.L., et al. The genomes of four tapeworm species reveal adaptation to parasitism. Nature. 2013;496(7443):57–63. doi: 10.1038/nature12031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Weinmann C.J. In: Biology of Parasites. Soulsby E.J.L., editor. Academic Press; New York: 1966. Immunity mechanisms in cestode infection; pp. 301–320. [Google Scholar]
  69. Weiss A., Th A., Bauer C., Köhler K. Canine alveolar echinococcosis: morphology and inflammatory response. J. Comp. Parasitol. 2010;143:233–238. doi: 10.1016/j.jcpa.2010.03.004. [DOI] [PubMed] [Google Scholar]
  70. Yamane K., Suzuki Y., Tachi E., Li T.-Y., Chen X.-W., Nakao M., et al. Recent hybridization between Taenia asiatica and Taenia saginata. Parasitol. Int. 2012;61:351–355. doi: 10.1016/j.parint.2012.01.005. [DOI] [PubMed] [Google Scholar]
  71. Yamane K., Yanagida T., Li T., Chen X., Dekmuyoy P., Waikagul J., et al. Genotypic relationships between Taenia saginata and Taenia asiatica and their hybrids. Parasitology. 2013;140:1595–1601. doi: 10.1017/S0031182013001273. [DOI] [PubMed] [Google Scholar]
  72. Yoshino K. On the subjective symptoms caused by the parasitism of Taenia solium and its development in man. J. Med. Assoc. Formosa. 1934;33:183–194. (in Japanese) [Google Scholar]
  73. Zajac A., Fairman D., McGee E., Wells B., Jenkins P.E., LeRoith T., et al. Alveolar echinococcosis in a dog in the eastern United States. J. Vet. Diagn. Investig. 2020 doi: 10.1177/1040638720943842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Zarlenga D.S., McManus D.P., Fan P.C., Cross J.H. Characterization and detection of a newly described Asian taeniid using cloned ribosomal DNA fragments and sequence amplification by polymerase chain reaction. Exp Parasitol. 1991;72:174–183. doi: 10.1016/0014-4894(91)90135-j. [DOI] [PubMed] [Google Scholar]
  75. Zein U., Siregar S., Janis I., Pane A., Purba J., Sardjono T.W., et al. Identification of a previously unidentified endemic region for taeniasis in North Sumatra, Indonesia. Acta Trop. 2019;189:114–116. doi: 10.1016/j.actatropica.2018.10.004. [DOI] [PubMed] [Google Scholar]

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