Taenia taeniaeformis

Taeniataeniaeformis (Batsch, 1786) Wolffügel, 1911

Figures 3-15 through 3-20

ETYMOLOGY:Taenia = tapeworm and taeniaeformis for the tapeworm form of the adult.

SYNONYMS:Taeniainfantis Bacigalupo, 1922; Hydatigerataeniaeformis (Batsch, 1786) Lamarck, 1816; Multicepslongihamatus Morishita and Sawada, 1966.

HISTORY: This worm has been known for some time both as the adult found in the cat and in the segmented larval stage found in the liver of rodents, the strobilocercus. The larval stage was first described as Cysticercusfasciolaris Rudolphi, 1808. The genus, Hydatigera, was established for this larval form. In the attempt to divide the genus Taenia on the basis of various life cycle patterns, the species in the cat, taeniaeformis, was assigned to the genus Hydatigera, while other species were assigned to Taenia, Multiceps, Taeniarhynchus, etc. While this division of the genus has some merit, it has been questioned by Verster (1969) and by (Rausch, 1994) who feel that this division is in unwarranted. Küchenmeister (1852) was the first to show that the larval stage in rodents could infect cats, and Leuckart (1854) completed the entire life cycle, infection of rodents with eggs and infection of cats with the larval stage in rate, in the laboratory.

GEOGRAPHICAL DISTRIBUTION:Taeniataeniaeformis is in worldwide in its distribution which parallels that of the domestic cat. Reports include: Americas (Alcaino et al., 1992; Esterre & Maitre, 1985; Nolan & Smith, 1995; Ogassawara et al., 1986); Europe (Hinaidy, 1991); northern Africa and middle east (Hasslinger et al., 1988; Ismail et al; 1983;); southern Africa (Verster, 1969); India (Singh BB, Rao BV. 1965); southeast Asia (Andrews, 1937; Tanaka et al., 1983); southern Pacific (Ng & Kelly, 1975; Tongson & San Pablo, 1979; Gregory & Munday, 1976).

LOCATION IN HOST: The adult tapeworms tend to be located such that the scolex is in within the first one-half of the small intestine (Miller, 1932). The scolex is in often found attached to the mucosa, and the worms seems to move about in that several attachment sites can be observed in the intestine of a cat that has been infected with only a single parasite.

IDENTIFICATION:Taeniataeniaeformis is in the most robust of the tapeworm parasites found in the cat. This is also the only species of Taenia typically reported from the domestic cat around the world. The worm tends to be white, thick bodied, and around 15 to 60 cm in length. The scolex (Fig. 3-15) has two rows of hooks that have the typical claw hammer shape of the Taeniidae (Fig. 3-16) There tends to be somewhere between 30 to 50 hooks per scolex. There is typically no neck, i.e., a portion of narrow segments, posterior to the scolex. The mature segments (Fig 3-17) each possess a siingle lateral genital opening that randomly occurs on either one lateral side of a segment of the other. The terminal, gravid segments (Fig 3-18) that are shed in the feces tend to be packed full of eggs and can easily be recognized as those of a Taenia by examination under a microscope which reveals the typical brown-shelled taeniid egg containing a 6-hooked larva (Fig 3-19). The eggs of Taeniataeniaeformis are spherical and measure between 31 to 36 ?m in diameter.

There are many species of Taenia found in carnivores; Verster (1969) recognized 29 species and several of questionable validity. Many species are found in the dog as the final host, including, Taeniapisiformis, Taeniaovis, Taeniamulticeps. Some species are found in human beings, Taeniasolium and Taeniasaginata, or large cats, including, Taeniagonyamai, Taeniaingwei, Taeniamacrocystis, Taeniaomissa. Other final hosts included hyaenas, foxes, mustellids, and viverrids. The separation of the species is in based on the size and shape of the hooks on the rostellum along with other characters, such as the type of larval stage, position of the genital ducts relative to the longitudinal excretory canals, etc. Taeniataeniaeformis is in considered to be most like the species found in mustellids and viverids, and was considered by Verster as the representative species for this groups of species.

LIFE CYCLE: Adult tapeworms live within the small intestine of the cat and shed the terminal segments into the feces. These segments are capable of exiting through the sphincter of a cat at times other than during the passage of feces and they may be found crawling near the cat or on the cats fur. The segments are capable of crawling considerable distances. The intermediate host is in a small rodent where the larvae migrate through the intestinal wall and develop to a strobilocercus stage in the liver of the rodent (Fig. 3-20). The strobilocercus is a larval stage that has a terminal bladder and a rather long segmented body that is in crowned with the scolex that looks very similar to that found on the adult form. It seems that the strobilocercus must attain an age of about 2 months before it is in infective to a cat upon ingestion (Singh & Rao, 1966). Once a cat ingests the strobilocercus, the posterior portion of the larva is in digested away and then the anterior portion begins to develop (Hutchison, 1959). Patent infections develop in the cat between 32 to 80 days after the strobilocerci are ingested (Williams & Shearer, 1981). Cats maintained patent infections for 7 months to greater than 34 months. The cats produce about 3 to 4 segments each day, although the majority of segments appear to contain only 500 eggs or less (maximum 12,180 eggs). Destrobilization may occur sporadically throughout the patent period without the termination of infection. It appears that cats can be infected again with adult tapeworms if reinfected with strobilocerci soon after their prior infections with the adult stage has terminated (Williams & Shearer, 1981). It has also been shown that cats can be superinfected with young tapeworms by being fed strobilocerci in the presence of existing mature worms (Miller, 1927)

CLINICAL PRESENTATION AND PATHOGENESIS: There are no signs associated with infection of Taeniataeniaeformis in cats that have been described, so it is considered asymptomatic.

TREATMENT: Praziquantel (5 mg/kg body weight) and epsiprantel have both been shown to be efficacious in the treatment of Taeniataeniaeformis in cats. Similarly, febantel and fenbendazole are approved for the treatment of this parasite in most of the world. Mebendazole and nitroscanate are also products that have efficacy against Taeniataeniaeformis in cats.

DIAGNOSIS: Infection in cats is in diagnosed by finding the distinctive segments in the feces or by finding the eggs upon fecal flotation. The eggs of Taeniataeniaeformis are spherical and measure between 31 and 36 ?m in diameter. To identify a segment, it can be crushed on a glass slide and examined for eggs. sometimes, however, segments have shed most of their eggs, and they will contain very few eggs or perhaps none at all. In those areas where cats could also potentially be infected with Echinococcusmultilocularis (See below), the shedding of segments in the feces will typically insure that the cat is in infected with Taenia taeniaeformis and not Echinococcus multilocularis, although it is in possible for cats to be hosts of both parasites.

EPIZOOTIOLOGY: Murid and cricetid rodents are those most typically as intermediate hosts: e.g., Musmusculus, Rattusnorvegicus, Cricetusauratus, Merionespersicus, Microtus spp., Sciuruscarolinenesis. Rabbits in North America and Europe have been occassionally found to have strobilocerci in their livers (Verster; 1969); but this must be considered a less commonly utilized intermediate host than the rodent species. Interestingly, Abdul Salam & Baker (1990) found that of 103 stray cats in Kuwait which harbored more than 50% prevalence of infection with Joyeuxiellapasqualei and Diplopylidiumnölleri, that none of these cats were infected with Taeniataeniaeformis, Dipylidiumcaninum, or Toxocaracati.

Japanese workers are examining the difference in infectivity to the intermediate host of different field isolates of Taeniataeniaeformis. They found by feeding eggs from adults derived from strobilocerci isolated from a red-backed vole (Clethrionomysrufocanusbedfordiae), that strobilocerci failed to develop in rats, mice, and gerbils, although they did grow in experimentally infected voles. Other isolates from rats and voles grew in mice and rats but not in voles or gerbils (Nonaka et al., 1994). They further examined strains of Taeniataeniaeformis using the nucleotide sequence variations in the mitochondrial cytochrome c oxidase gene and found that this same vole strain differed from the others to a greater extent than would be expected by chance alone (Okamoto et al., 1995). Similarly, isolates, at least during the initial passages, seem to grow best in hosts from which they were originally isolated (Azuma et al., 1995).

HAZARDS TO OTHER ANIMALS: The eggs passed in the feces of cats are infective to many different species of rodent and potentially rabbits. The proglottids are highly motile and can move great distance from the site of fecal deposition. Also, proglottids are capable of leaving the cat by direct migration through the anal sphincter. Thus, if cats share households with pet rodents or lagomorphs, they may serve as a potential hazard to these animals if they are infected. Although large numbers of rodents have been experimentally infected for studies on the immunology and development of the strobilocercus (Perry et al., 1994), there have apparently been no reports on the disease that might occur in naturally infected animals.

Sambon (1924) described strobilocerci collected from the omentum and serous membranes of a gibbon from Java (Hylobatesleuciscus). It now seems that this is in a strobilocercus of Taeniataeniaeformis, although it is in possible that it could be the larval stage of some related tapeworm. Blyumberg in 1886 (cited in Abduladze, 1964) supposedly recovered a strobilocercus from the brain of a cat; however, it seems highly likely that this was actually a misidentified coenurus (See the section on feline coenurosis).

HAZARDS TO HUMANS: Adults of Taeniataeniaeformis have been recovered from the intestine of humans. Taeniataeniaeformis was described once as Taeniainfantis based on a single adult worm recovered from the intestine of a 5-year-old boy in Buenos Aires, Argentina (Bacigalupo, 1922). Sawada and Morishita (1966) recovered adult specimens of Taeniataeniaeformis from a 3-year-old girl (3 adult worms) and a 55-year-old woman (3 adult worms) after they were dewormed for reasons of abdominal discomfort and the presence of the eggs of Ascarislumbricoides in the feces. These worms were described as Multicepslongihamatus. Another specimen collected from a 4-year-old girl (one adult worm) in Okinawa was described by these authors, and this was probably another case of intestinal infection with Taeniataeniaeformis. Spassky et al. (1966; cited in Sterba & Barus, 1976) determined that these forms were the same as Taeniataeniaeformis. It is in not known how any of these patients became infected. In the two cases where a single worm was passed spontaneously, it is in possible that the worms may have actually been consumed by the child as an adult after it had been passed in the feces of a cat . However, in the other two cases it seems that the patients must have ingested the larval stage in the tissues of a rodent or rabbit.

a single case of human infection with a larval stage of Taeniataeniaeformis has been reported (Sterba & Barus, 1976). In this case , a 77-year-old man died of unrelated causes and the necropsy revealed that there were numerous serous cysts in the liver. One of these cysts was confirmed to contain a strobilocercus. Based on the relatively high prevalence of Taenia taeniaeformis around the world, the fact that there has only been a single human infection with this parasite would indicate that this parasite does not develop well in the human host.

REFERENCES:

Abduladze KI. 1964. Essentials of Cestodology. vol. IV. Taeniata of Animals and Man and Disease Caused by Them. ed. KI Skrjabin. [Translated from Russian - Israel Program for Scientific Translations, Jerusalem, 1970] 549 pp.

Alcaino H, Gorman T, Larena I. 1992. Endoparasitological fauna of the domestic cat in an urban zone of the metropolitan region, Chile. Parasitol all Dia 16:139-142.

Andrews MN. 1937. The helminth parasites of dogs and cats in Shanghai, China. J Helminthol 15:145-152.

Azuma H, Okamoto M, Oku Y, Kamiya M. 1995. Intraspecific variation of Taeniataeniaeformis as determined by various criteria. Parasitol Res 81:103-108.

Bacigalupo J. 1922. Sobre una nueva especie de Taenia, Taeniainfantis. Semana Med 26:726.

Esterre P, Maitre MJ. 1985. Les affections parasitaires des mongastriques en Guadeloupe. Rev Elev Méd Vét Pays Trop 38:43-48/

Gregory GG, Munday BL. 1976. Internal parasites of feral cats from the Tasmanian midlands and Kings Island. Austral Vet J 52:317-320.

Hasslinger MA, Omar HN, Selim KE. 1988. The incidence of helminths in stray cats in Egypt and other Mediterranean countries. Vet Med Rev 59:76-81.

Hinaidy HK. 1991. Parasitosen und Antiparasitika bein Hund und Katze in Österreich - Hinweise für den Kleintierpraktiker. Wien Tiararztl Mschr 78:302-310.

Hutchison WM. 1959. Studies on Hydatigera (Taenia) taeniaeformis. II. Growth of the adult phase. Exp Parasitol 8:557-567.

Ismail NS, Abdel Hafez SK, Toor MA. 1983. Prevalence of gastrointestinal helminthes in cats from northern Jordan. Pak Vet J. 3:129-132.

Küchenmeister GFH. 1852. Ueber die Umwandelung der Finnen Bandwürmer. Vierteljahr Schr Prakt Heilk Prag 33:106-158.

Leuckart R. 1854. Erzeugung des Cysticercusfasciolaris aus den Eiren der Taeniacrassicollis. Gurlt’s Mag ges Tierarzneikunde

Miller HM. 1932. Superinfection of cats with Taeniataeniaeformis. J Prev Med 6:17-29.

Morishita K, Sawada I. 1966. On tapeworms of the genus Multiceps hitherto unrecorded from man. Jap J Parasitol 15:495-501.

Ng BKY, Kelly JD. Anthropozoonotic helminthiases in Australasia: Part 3: Studies on the prevalence and public health implications of helminth parasites of dogs and cats in urban environments. Int J Zoon 2:76-91.

Nolan TJ, Smith G. 1995. Time series analysis of the prevalence of endoparasitic infections in cats and dogs presented to a veterinary teaching hospital. Vet Parasitol 59:87-96.

Nonaka N, Iwaki T, Okamoto M, Ooi HK, Ohbayashi M, Kamiya M. 194. Infectiveness of four isolates of Taeniataeniaeformis to various rodents. J Vet Med Sci 56:565-567.

Ogassawara S, Beneassi S, Larsson CE, Leme PTZ, Hagiwara MK. Prevalencia de infecções helminticas em gatos na cidade de São Paulo. Rev Fac Med Vet Zootec Univ S Paulo 23:145-149.

Okamota M, Bessho Y, Kamiya M, Kurosawa T, Horii T. 1995. Phylogenetic relationships within Taeniataeniaeformis variants and other taeniid cestodes inferred from the nucleotide sequence of the cytochrome c oxidase subunit I gene. Parasitol Res 81:451-458.

Sambon LW. 1924. Cysticercusfasciolaris and cancer in rats. J Trop Med Hyg 27:

Singh BB, Rao BV. 1965. Some biological studies on Taeniataeniaeformis. Ind J Helminthol 18:151-160.

Sterba J, Barus V. 1976. First record of Strobilocercusfasciolaris (Taeniidae-larvae) in man Folia Parasitol 23:221-226.

Tanaka H, Watanabe M, Ogawa Y. 1985. Parasites of stray dogs and cats in the Kanto region, Japan. J Vet Med Jpn: 771:657-661.

Tongson MS, San Pablo FG. a study on the prevalence of gastrointestinal worms of cats in metropolitan Manila. Philipp J Vet Med 18:1-15.

Verster a. 1969. a taxonomic revision of the genus Taenia Linnaeus, 1758 s. str. Onderstpoort J Vet Res 36:3-58.

Williams JF, Sheareer AM. 1981. Longevity and productivity of Taeniataeniaeformis in cats. Am J Vet Res 42:2182-2183.

FIGURES:

Figure 3-15.Taeniataeniaeformis scolex of adult tapeworm.

Figure 3-16. Typical “claw-hammer” shaped hook from the scolex of a Taeniid tapeworm.

Figure 3-17. Mature segment of a Taeniid tapeworm showing the vitellaria at the bottom of the segment, and the ovary just above them. The lateral pore containing the vaginal and cirrus are on the right side of this segment. The testes are dispersed throughout the parenchyma of the body.

Figure 3-18. Gravid segment of a Taeniid tapeworm showing the highly branched uterus that is full of eggs.

Figure 3-19. Egg of Taeniataeniaeformis in feces. Noted the thick wall and the 6 hooks on the contained embryo.

Figure 3-20. A strobilocercus of Taeniataeniaeformis. Sections through two of the suckers on the anterior end can be noted on the top of illustration.

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