Taenia Asiatica Research Articles

Epidemiology of Taenia solium in Nepal: is it influenced by the social characteristics of the population and the presence of Taenia asiatica?

The transmission of the zoonotic pork tapeworms Taenia solium and T. asiatica depends on a combination of specific risk factors, such as open defecation, backyard pig raising and the consumption of raw or undercooked pork and viscera. A community-based survey was conducted among 289 households in south-eastern Nepal to study the heterogeneity of these risk factor frequencies as a function of the social composition of the population. The frequency of open defecation, backyard pig raising and pork consumption differed significantly (P < 0.005) among the different coexisting caste and ethnic groups. In the same survey, the taeniosis prevalence was examined among the different groups. Tapeworm carriers were identified at a high prevalence among the Dum, one of the most disadvantaged communities of Nepal. A PCR-RFLP assay revealed that all collected tapeworm specimens were T. asiatica, a species thus far not known to occur in South Asia. These results can help to understand the epidemiology of T. solium in Nepal, which appears to be more complex than thought so far.

Evidence of hybridization between Taenia saginata and Taenia asiatica

There has long been a debate as to the specific status of the cestode Taenia asiatica, with some people regarding it as a distinct species and some preferring to recognize it as a strain of Taenia saginata. The balance of current opinion seems to be that T. asiatica is a distinct species. In this study we performed an allelic analysis to explore the possibility of gene exchange between these closely related taxa. In total, 38 taeniid tapeworms were collected from humans living in many localities including Kanchanaburi Province, Thailand where the two species are sympatric. A mitochondrial DNA (mtDNA)-based multiplex PCR tentatively identified those parasites as T. asiatica ( n = 20) and T. saginata ( n = 18). Phylogenetic analyses of a mitochondrial cytochrome c oxidase subunit 1 ( cox1) gene and two nuclear loci, for elongation factor-1 alpha ( ef1) and ezrin-radixin-moesin (ERM)-like protein ( elp), assigned all except two individual parasites to the species indicated by multiplex PCR. The two exceptional individuals, from Kanchanaburi Province, showed a discrepancy between the mtDNA and nuclear DNA phylogenies. In spite of their possession of sequences typical of the T. saginata cox1 gene, both were homozygous at the elp locus for one of the alleles found in T. asiatica. At the ef1 locus, one individual was homozygous for the allele found at high frequency in T. asiatica while the other was homozygous for the major allele in T. saginata. These findings are evidence of occasional hybridization between the two species, although the possibility of retention of ancestral polymorphism cannot be excluded.

Taenia in the Gastrointestinal Tract

To the Editor: Liao and Bair (Sept. 6 issue)1 describe a tapeworm in a 60-year-old woman from a community where pork and pork liver are eaten, especially at festivals, and suggest infection with Taenia solium (the pork tapeworm) rather than T. saginata (the beef tapeworm). It is possible that the infection was caused instead by Asian taenia (T. asiatica, T. saginata asiatica), which has been reported in aborigines in Taiwan,2 with subsequent reports from other Asian countries: Korea, Indonesia, the Philippines, Vietnam, and China.3,4 T. asiatica is believed to be transmissible only through ingestion of pig viscera . . .

Taeniasis/cysticercosis in a Tibetan population in Sichuan Province, China

The results of a preliminary survey of taeniasis/cysticercosis in Yajiang County, Ganze Tibetan Prefecture in southwest Sichuan Province, China, indicated a very high prevalence of taeniasis (22.5%), with Taenia saginata as the dominant species. There was also a significant occurrence of late-onset epilepsy (8.5% prevalence and 16.4% seropositive for Taenia solium antibodies) attributable in large part to probable neurocysticercosis caused by T. solium. The poor sanitation and hygiene in this Tibetan community likely contributed to a high risk of human cysticercosis despite a low level of T. solium taeniasis (actually no T. solium carriers were detected amongst the 21 proven Taenia carriers). In addition, three taeniasis cases were confirmed by DNA genotyping as Taenia asiatica, which is the first report of this tapeworm in Tibetans, the first report for Sichuan Province and only the third report for mainland China.

Molecular Discrimination of Taeniid Cestodes

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What is Asian Taenia?

Asian Taenia is a human tapeworm which was first recognized in Taiwan aborigines and subsequently from Asian countries: Korea, Indonesia, Vietnam, and China. It was originally described as T. asiatica Eom and Rim, 1993 based on the morphology in its adult and larval stage. A taxonomic disagreement on whether it is species or subspecies level is mainly due to the morphological similarity of this tapeworm with T. saginata, but a sympatric distribution of these two tapeworms is also known in China. The life cycle is quite distinct from T. saginata in using the pig as intermediate host and parasitizing visceral organs such as liver, lung and omentum. A long unresolved question in Asian countries concerns the inconsistency between worm ratio and the food preferences was clarified with this viscerotropic tapeworm. Molecular biological differentiation is possible with DNA techniques and a complete genome of mtDNA was sequenced recently which may provide a resource for comparative mitochondrial genomics and systematic studies of parasitic cestodes. This is a young parasite discovered most recently with many research questions yet to be clarified.

Molecular discrimination of taeniid cestodes

DNA approaches are now being used routinely for accurate identification of Echinococcus and Taenia species, subspecies and strains, and in molecular epidemiological surveys of echinococcosis/taeniasis in different geographical settings and host assemblages. The publication of the complete sequences of the mitochondrial (mt) genomes of E. granulosus, E. multilocularis, T. solium and Asian Taenia, and the availability of mtDNA sequences for a number of other taeniid genotypes, has provided additional genetic information that can be used for more in depth phylogenetic and taxonomic studies of these parasites. This very rich sequence information has provided a solid molecular basis, along with a range of different biological, epidemiological, biochemical and other molecular-genetic criteria, for revising the taxonomy of the genus Echinococcus and for estimating the evolutionary time of divergence of the various taxa. Furthermore, the accumulating genetic data has allowed the development of PCR-based tests for unambiguous identification of Echinococcus eggs in the faeces of definitive hosts and in the environment. Molecular phylogenies derived from mtDNA sequence comparisons of geographically distributed samples of T. solium provide molecular evidence for two genotypes, one being restricted to Asia, with the other occurring in Africa and America. Whether the two genetic forms of T. solium differ in important phenotypic characteristics remains to be determined. As well, minor DNA sequence differences have been reported between isolates of T. saginata and Asian Taenia. There has been considerable discussion over a number of years regarding the taxonomic position of Asian Taenia and whether it should be regarded as a genotype, strain, subspecies or sister species of T. saginata. The available molecular genetic data do not support independent species status for Asian Taenia and T. saginata. What is in agreement is that both taxa are closely related to each other but distantly related to T. solium. This is important in public health terms as it predicts that cysticercosis in humans attributable to Asian Taenia does not occur, because cysticercosis is unknown in T. saginata.

ACUTE PANCREATITIS CAUSED BY TAPEWORM IN THE BILIARY TRACT

Taeniasis is a helminthic infection endemic in southeast Asia, including Taiwan. Recent studies suggest that Asian Taenia is a new subspecies of Taenia saginata and has been renamed as Taenia saginata asiatica. It is usually asymptomatic or associated with only mild gastrointestinal symptoms. We report the case of a 52-year-old woman with acute epigastric pain and vomiting. Her levels of amylase and lipase were significantly elevated on admission. Gastrointestinal endoscopy showed proglottids of a tapeworm in the papilla of the duodenum. The epigastric pain subsided and the amylase and lipase levels decreased after removal of the tapeworm by endoscopy and anthelminthic treatment. Although parasites are not an uncommon cause of pancreatitis, especially in disease-endemic areas, it is rare for Taenia to cause acute pancreatitis.

Human Taeniasis and cysticercosis in Asia.

Human Taeniasis caused by the pork, Taenia solium, or beef, T saginata, tapeworm arises after eating pork or beef contaminated with metacestodes, the larval stage of these parasites. Taeniasis with T solium can lead to neurocysticercosis and threaten others by accidental ingestion of eggs released from asymptomatic Taeniasis patients. The 2003 World Health Assembly declared that T solium is of worldwide public-health importance, and that it is an eradicable parasitic disease worldwide. Adult taeniid tapeworms expelled from people in almost all Asian countries appeared to be T saginata (the so-called Asian Taenia), even though they ate pork. The organism is now named T asiatica, and has been found in Taiwan, Korea, China, Vietnam, and Indonesia. But it has been difficult to differentiate T saginata from beef and Asian Taenia from pork. Marshall Lightowlers and colleagues (Int J Parasitol 2003; 33: 1207-17) recently demonstrated that recombinant oncosphere vaccines against several taeniid cestodes, including T ovis, T saginata, T solium, and Echinococcus granulosus, are highly effective. Protection was almost 100%, in the laboratory and in the field. These researchers found several common features, including a predicted secretory signal sequence, and one or two copies of a fibronectin type III domain, each encoded by separate exons within the associated gene. WHERE NEXT? Molecular and immunological techniques, including vaccine research and development of animal models for differentiation of taeniid species in humans, have greatly advanced over the past decade. The clinical importance of infections by these taeniids, including T asiatica, in humans, and the potential for cysticercosis attributable to T asiatica in humans, needs further study.

The Asian Taenia and the possibility of cysticercosis.

In certain Asian countries, a third form of human Taenia, also known as the Asian Taenia, has been discovered. This Asian Taenia seems to be an intermediate between Taenia solium and T. saginata since in morphological terms it is similar to T. saginata, yet biologically, as it uses the same intermediate host (pigs), it is more akin to T. solium. Taenia solium causes human cysticercosis, while T. saginata does not. It is not known whether the Asian taeniid is able to develop to the larval stage in humans or not. The arguments proposed by those authors who consider it unlikely that the Asian Taenia causes human cysticercosis are: (a) its molecular similarities with T. saginata; (b) the absence of cases of human cysticercosis in populations where the Asian adult is highly prevalent; and (c) the unsupporting results derived from an experimental infestation study. These three arguments are debated, although bearing in mind that at present there is still no clear scientific data to support that human cysticercosis can be caused by the Asian Taenia.

NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequences compared for members of the genus Taenia (Cestoda)

Nine members of the genus Taenia ( Taenia taeniaeformis, Taenia hydatigena, Taenia pisiformis, Taenia ovis, Taenia multiceps, Taenia serialis, Taenia saginata, Taenia solium and the Asian Taenia) were characterised by their mitochondrial NADH dehydrogenase subunit 1 gene sequences and their genetic relationships were compared with those derived from the cytochrome c oxidase subunit I sequence data. The extent of inter-taxon sequence difference in NADH dehydrogenase subunit 1 (∼5.9–30.8%) was usually greater than in cytochrome c oxidase subunit I (∼2.5–18%). Although topology of the phenograms derived from NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequence data differed, there was concordance in that T. multiceps, T. serialis (of canids), T. saginata and the Asian Taenia (of humans) were genetically most similar, and those four members were genetically more similar to T. ovis and T. solium than they were to T. hydatigena and T. pisiformis (of canids) or T. taeniaeformis (of cats). The NADH dehydrogenase subunit 1 sequence data may prove useful in studies of the systematics and population genetic structure of the Taeniidae.

Basic and applied immunology in cestode infections: from hymenolepis to Taenia and Echinococcus

In larval cestode infections, it is well established that the intermediate mammalian host infected with egg-derived metacestodes in the tissue becomes completely immune to reinfection with eggs, whereas autoinfection has been conceived to occur in Hymenolepis nana/mouse (and human) and Taenia solium/human systems when these hosts are initially infected with metacestode-derived adult tapeworms in the lumen. In this review paper, the first topic is immunobiology of H. nana/mouse system on the reinfection immunity in order to get critical information as to how the initially ingested parasite (eggs or metacestodes) can develop into adult worms and how autoinfection does or does not occur in immunocompetent mice, since H. nana can complete its whole life cycle in the mouse intestinal tissue and lumen. When mice are infected with eggs (=oncospheres) of H. nana, they become immune to challenge infections with eggs within a few days (early response) and with cysticercoids within two weeks (late response). The initially established adult worms are expelled later (worm expulsion response). When mice are infected with cysticercoids, either derived from beetles or mice, they become immune to challenge infection with cysticercoids but not with eggs. Therefore, autoinfection occurs in the intestinal tissue for the establishment of cysticercoids in the tissue but never occurs in the intestinal lumen for the establishment of adult worms in immunocompetent mice. The second topic is vaccination trial against challenge infection with eggs of Asian Taenia in pigs. Pigs vaccinated with frozen oncospheres of Asian Taenia from Taiwan or Korea or T. saginata showed very strong resistance, whereas pigs vaccinated with those of T. solium showed partial resistance only. It is suggested that Asian Taenia is much closer to T. saginata than T. solium from the immunobiological viewpoint. The third topic is immunodiagnosis of echinococcosis and cysticercosis. Immunoblot analysis has revealed that Em18 (18kDa component of crude antigens of Echinococcus multilocularis protoscolex) and glycoproteins of T. solium cysticerci are highly specific or unique to alveolar echinococcosis and cysticercosis, respectively. The fourth topic is discussion on miscellaneous prospects including laboratory animal models for echinococcosis and cysticercosis.

In vitro hatched oncospheres of Asian Taenia from Korea and Taiwan develop into cysticerci in the peritoneal cavity of female scid (severe combined immunodeficiency) mice

In vitro hatched (but not activated) oncospheres of Asian Taenia obtained in Korea and Taiwan, prepared by the sodium hypochlorite method, rinsed with sterile PBS several times and adjusted to 5 × 10 4/0.5 ml PBS, were injected intraperitoneally or subcutaneously into male or female scid mice of 3 different strains. When these scid mice were sacrificed 4 months later, the females harboured fully developed cysticerci either in the peritoneal cavity or under the back skin, whereas males did not. All cysticerci from the peritoneal cavity were easily recovered by rinsing the abdomen with PBS. Although most cysticerci recovered from pig liver usually become calcified within 1–2 months, in female scid mice they all increased in size and were viable. Intrapertioneal (i.p.) injection of in vitro hatched oncospheres is recommended for easier recovery of Asian Taenia metacestodes in laboratory animals.

Human Taenia eggs develop into cysticerci in scid mice.

The intermediate hosts for Taenia saginata and T. solium are cattle and pigs (and humans for the latter), respectively. In vitro-hatched (but not activated) oncospheres of both Asian Taenia (T. saginata asiatica, a new subspecies of T. saginata or T. asiatica, a new species) and T. solium injected subcutaneously into the backs of mice with severe combined immunodeficiency (scid) developed into fully matured cysticerci. Five-month-old metacestodes of Asian Taenia had no hooklets and were bigger in size than those previously reported and similar to those of T. saginata. Their morphology suggested that the cysticerci were more advanced than those in the intermediate host animals. It is suggested that scid mice are valuable experimental animal models for studying human taeniid cestode infections.

Comparison of single and trickle infections of pigs with eggs of the Asian Taenia

Two groups of seven Belgian Landrace piglets each were either infected with a single dose of 3000 or with five consecutive doses of 600 Asian Taenia eggs at weekly intervals. Nine weeks after the first infection all pigs were autopsied and the number of metacestodes was obtained by slicing the liver. There were no significant differences between the mean number of viable or dead cysts present in both groups of animals. Only very low numbers of living metacestodes were foundd: 0.4% (3/779) of the total number of cysts present in the single infection group and 1.8% (13/707) in the trickle infection group. Circulating antigens could be detected in only four out of 13 animals and no differences in antibody kinetics were present between the two groups of pigs. The presence of high numbers of degenerated cysts in experimental as well as in field conditions seems to indicate that the biotic potential of the Asian Taenia is rather low.

Taenia crassiceps: Cloning and Mapping of Mitochondrial DNA and Its Application to the Phenetic Analysis of a New Species of Taenia from Southeast Asia

Asian Taenia is a human-infecting Taenia tapeworm known as Taenia asiatica following morphological examination of adult and larval stages of the tapeworm by Eom and Rim (1993). The life cycle of T. asiatica differs from that of T. saginata in its intermediate host (pigs versus cattle) as well as in the infected organs (liver versus muscle). T. asiatica can be differentiated from T. solium and T. saginata by examination of morphological characteristics such as the scolex, mature and gravid proglottids in the adult stage, and the scolex and bladder surface in the larval stage. T. asiatica has been identified in Korea, Taiwan, the Philippines, China, Thailand, Indonesia, Vietnam, Japan, Lao PDR, Nepal and India. The molecular tools employed for T. asiatica identification have been developed to differentiate T. asiatica from other human-infecting Taenia tapeworms based on genetic information such as nucleotide sequence of mitochondrial genes, nuclear ribosomal genes and nuclear genes that lead to development of the subsequent molecular techniques, such as PCR-RFLP, PCR-RAPD, BESST-base, LAMP and qPCR. Investigation of the phylogenetic relationships among human Taenia species revealed that T. asiatica is a sister species with T. saginata, which is genetically more similar than other Taenia species in terms of the nucleotide sequences of cox1, nad1 and 28S rDNA. The mitochondrial genomes of human Taenia tapeworms comprise 13,703 bp (T. asiatica), 13,670 bp (T. saginata) and 13,709 bp (T. solium), and contain 36 genes including 12 protein-coding genes, 2 ribosomal RNAs (rRNAs, a small and a large subunit), and 22 transfer RNAs (tRNAs). Sequence differences in the full genome of T. asiatica and T. saginata mitochondria is 4.6%, while T. solium differs by 11%. Hox gene orthology in T. asiatica was established by comparative analysis with Platyhelminthes Hox genes. T. asiatica Hox revealed six Hox orthologs including two lab/Hox1, two Hox3, one Dfd/Hox4 and one Lox/Lox4. Hybridization between T. asiatica and T. saginata was definitely observed in these species which are sympatrically endemic in the regions of Korea, Thailand, China and Lao PDR. Comparative analyses of T. asiatica, T. saginata and T. solium genomes were also reported with genome features. Taenia asiaticus nomen novum was proposed for T. asiatica Eom and Rim, 1993 which is a homonym of T. asiatica Linstow, 1901 (Davaineidae).

Failure of experimental infection of baboons (Papio hamadryas) with the eggs of Asian Taenia

The infectivity of the eggs of Asian Taenia sp. for humans is not known. Using baboons (Papio hamadryas) as a model to extrapolate the findings, three animals were exposed per os with 1000, 10,000 and 50,000 infective eggs of the Asian Taenia sp. The serological, biochemical, haematological and parasitological (based on necropsy) results show that baboons are refractory to the infection. It is concluded that the Asian taeniid eggs may fail to develop in man.

Cross protection against Taenia taeniaeformis in rats vaccinated with non-viable oncospheres of Asian Taenia or T. saginata

It was determined to examine whether rats injected with non-viable oncospheres of Asian Taenia or Taenia saginata became resistant to challenge infection with eggs of Taenia taeniaeformis, since (a) metacestodes of Asian Taenia and T. taeniaeformis develop in the liver of pigs and rats, respectively, and (b) Asian Taenia and T. saginata have human origins. Rats injected intravenously or subcutaneously with complete Freund's adjuvant with non-viable oncospheres of Asian Taenia showed statistically significant resistance to challenge infection with eggs of T. taeniaeformis, whereas those injected with non-viable oncospheres of T. saginata did not show any resistance.

Genetic Characterization of the Asian Taenia, a Newly Described Taeniid Cestode of Humans

Recent studies on the epidemiologic pattern of taeniasis in Southeast Asia have indicated the existence of a third form of human Taenia, distinguishable from Taenia saginata and T. solium. Originally termed Taiwan Taenia, and first described in Taiwanese aboriginals, this newly recognized taeniid is now generally referred to as Asian Taenia since it has since been recorded in a number of other Asian countries. Here we have used a genetic yardstick approach to determine whether the Asian Taenia should most appropriately be considered as a new, distinct species or as a subspecies, strain, or variant of T. saginata, which previous studies have shown it closely resembles. Sequence variation in the 28S rRNA and mitochondrial cytochrome c oxidase I (COI) genes of a range of taeniid cestodes and the COI and rDNA internal transcribed spacer I polymerase chain reaction (PCR) restriction fragment length polymorphism (RFLP) pattern differences in the Asian Taenia, T. saginata, and T. solium were used as markers of genetic identity. The PCR-RFLP approaches proved useful for rapid and unambiguous discrimination of Asian Taenia from the other two human species, whereas the mitochondrial and nuclear sequence comparisons indicate that the Asian Taenia is much more closely related to T. saginata than recognized taeniid species are to each other. The results support earlier conclusions that the Asian Taenia is a genetically distinct entity but is closely related to T. saginata, and suggest that its taxonomic classification as a subspecies or strain of T. saginata is more appropriate than formal designation as a new species. The very close relationship between Asian Taenia and T. saginata has public health implications in that the Asian form is unlikely to be an important cause of human cysticercosis because T. saginata cysticercosis, if it occurs at all in humans, is an extremely rare phenomenon.

Asian (Taiwan) Taenia: species or strain?

Recent studies on the epidemoiological pattern of taenisis in Southeast Asia have indicated the existence of a third form of human Taenia which is distinguishable from Taenia saginata and T. solium. Don McManus and Josephine Bowles here review how new genetic evidence supports earlier conclusions that the Asian Taenia is a distinct entity but is closely related T. saginata, and suggests its taxonomic classification as a subspecies or strain of T. saginata is more appropriate than formal designation as a new species.