Spirometra mansonoides Mueller, 1935

Figures 3-4 and 3-5

ETYMOLOGY:Spiro = spiral and metra = uterus (referring to the spiral-shaped uterus as opposed to the rosette-shaped uterus in Diphyllobothrium) and mansonoides because it was "like” Spirometramansoni the synonym that Mueller used as representing Spirometraerinaceieuropaei.

SYNONYMS:Diphyllobothrium mansonoides, Mueller, 1935.

HISTORY: Faust et al. (1929) created a subgenus called Spirometra within the genus Diphyllobothrium. Mueller (1935) described Diphyllobothrium mansonoides using specimens recovered from dogs and cats in the area around Syracuse, New York, USA. In 1937, Mueller raised Spirometra to generic rank, and hence, Diphyllobothrium mansonoides became Spirometra mansonoides.

GEOGRAPHIC DISTRIBUTION: Spirometra mansonoides is considered a parasite of the eastern United States that extends into parts of South America where it has been reported from Colombia, Ecuador, and Brazil (Fernandez TE, 1978; Lillis and Burrows, 1964; Mueller et al., 1975; Ogassawara and Benassi, 1980.).

LOCATION IN HOST: The adults of Spirometra mansonoides are found within the small intestine of the feline host.

PARASITE IDENTIFICATION: Mueller (1935) provided the original description of this tapeworm. At that time he stated that the maximum length of the strobila was 60 cm with a maximum width of 7 mm. Following almost forty years of study, he later determined that in a large dog, this tapeworm may attain a length of 1.5 meters with a maximum width of a centimeter or more (Mueller, 1974). The margins of this tapeworm are serrate. The strobila appears to be delicate in the neck region and robust posteriorly. Like the adult Diphyllobothrium latum, Spirometra mansonoides selectively absorb large quantities of vitamin B12 (Marchiondo et al., 1989). This absorption gives the adult tapeworms a characteristic pinkish color (Mueller, 1974). This tapeworm is unique due to the fact that while attached in the host's intestine, the mature proglottids often separate along the longitudinal axis for a short distance; the tapeworm will appear to become "unzipped," hence its common name, the zipper tapeworm (Hendrix, personal observation).

The scolex of Spirometra mansonoides lacks suckers but instead possesses two shallow longitudinal grooves called bothria (Mueller, 1935). It varies in diameter from 0.2 mm to almost 0.5 mm with bothria approximately 1.0 mm in length. The bothria are shallow, broad and flat bottomed. Each proglottid of Spirometra possesses a centrally located spiraled uterus and associated uterine pore through which eggs are released (Fig. 3-4). The uterus is composed of two sections: an anterior series of heavy "outer" coils and an posterior series of narrow "inner" coils. These two regions are joined by a narrow duct that will accommodate only three or four eggs. The uterine and genital apertures open on the ventral surface of the proglottid. These tapeworms characteristically release the eggs until they become exhausted of their uterine contents. Segments are not discharged into the feces until groups of segments have shed all their eggs and are passed as "spent” segments (Kirkpatrick and Sharninghausen, 1983). The uterus in the proglottids of Spirometra mansonoides terminates in the anterior of the proglottid in a distinct "U”-shaped uterus packed full of eggs. This distinct uterine formation does not occur in Spirometra erinaceieuropaei.

The egg of Spirometra resembles the egg of a digenetic trematode, that is, it is oval, yellow-brown and possesses a distinct operculum at one pole of the shell (Fig. 3-5). The eggs have dimensions that average 60 µm by 36 µm. Spirometra eggs have an asymmetric appearance and tend to be pointed at one end. There may be a slight bump on the abopercular end. The eggs are unembryonated when passed in the feces. It is possible that cats will go for extended periods with negative fecal samples that will be followed by periods when eggs are present in the feces.

LIFE CYCLE: Domestic and wild felids serve as the principal definitive hosts for Spirometra mansonoides, although dogs and racoons may harbor the adult cestodes; Mueller believes the natural host in the Americas was probably the bobcat, Lynx rufus. Unembryonated eggs pass through the uterine pore of each of the adult cestode's gravid proglottids. The eggs are discharged to the external environment with the cat's feces. Eggs can be stored at 4C for at least a year without any significant decreases in viability. In the presence of aeration at room temperature, the eggs develop to the infective stage and can then be stored at 4C for at least a year. Eggs are induced to hatch by exposure to direct sunlight and cold temperature shock. In fresh water, the first developmental stage, the ciliated coracidium emerges from the egg and is eaten by the first intermediate host, a freshwater crustacean of the genus Cyclops. The second developmental stage, the procercoid, develops within the copepod. When the procercoid is ingested by the second intermediate host, a frog, water snake or rodent, the procercoid develops into a plerocercoid or sparganum, the third developmental stage. These white, ribbon-like spargana are found primarily in subcutaneous sites. Cats become infected with Spirometra mansonoides by preying on frogs, water snakes, fish, birds or rodents containing the infective plerocercoids. Within ten to thirty days, the tapeworm develops to the mature stage in the cat's small intestine. Some of the plerocercoids may develop in the wall of the intestine and Mueller hypothesized that they may eventually migrate back into the lumen of the gut to begin an infection with the adult tapeworm. The adult tapeworm may survive for as long as 3.5 years in the cat (Mueller, 1974).

Cats can be infected with the larval form of Spirometra mansonoides (described below under feline sparganosis.)

CLINICAL PRESENTATION AND PATHOGENESIS: Most of the reports of infection with Spirometra species in domestic cats have been from results from parasitologic surveys or from results of fecal assays. Muller (1938) described the signs of infection with adult worms in cats as causing marked signs. Infected animal loose weight but remain hungry. The wall of the intestine of the infected cat became thickened, particularly in the layers of circular muscles. If a cat is given an anthelminthic, recovery is rapid, unless animals have been infected for long periods causing stunted growth in which cases deworming fails to result in the animals reaching target weights. If nursing kittens become infected, there is a marked retardation in growth. Muller believed that a severe anemia developed in infected cats, but no specific parameters were reported to substantiate this claim. One cat infected with adult Spirometra in the United States did exhibit an intermittent watery diarrhea of two months duration which resolved following therapy (Kirkpatrick and Sharninghausen, 1983).

TREATMENT: It is expected that treatment of cats with Spirometra mansonoides with praziquantel at the elevated dosage of 30 to 35 mg/kg body weight would cause the elimination of these parasites as they do Spirometra erinaceieuropaei (Fukase et al., 1992).

The Spirometra in a domestic cat reported by Kirkpatrick and Sharninghausen (1983) was likely to be Spirometra mansonoides. This tapeworm was refractory to treatment with albendazole (25 mg/kg BID for 6 consecutive days) and with 1500 mg of niclosamide following an overnight fast. A single treatment of the cat with 100 mg of bunamidine HCl appeared to remove the worms from this cat based on postmortem performed a month later after death due to other causes. Bunamidine (Scolaban) is administered orally to cats at a rate of 25 to 50 mg/kg body weight up to a maximum of 600 mg. The tablets should not be broken, crushed, mixed with food or dissolved in liquid because bunamidine irritates the oral mucosa. Bunamidine should be administered on an empty stomach and food should be withheld for 3 hours following medication. Treatment with bunamidine should not be repeated within 14 days. It should not be concurrently administered with butamisole (Stiquin), to unweaned kittens, or to cats with cardiac or hepatic disease. Cats should not be allowed to exercise or become excited immediately after treatment with bunamidine. Vomiting, diarrhea, and ventricular fibrillation are the most frequent side effects (Sakamoto, 1977).

EPIZOOTIOLOGY: Cats become infected when they eat water snakes, tadpoles, other amphibians, and small mammals, e.g. rats and mice containing the infective plerocercoid stage. Domestic and wild felids serve as the principal definitive hosts for Spirometra mansonoides, although dogs and racoons may harbor the adult cestodes (Mueller, 1974). In a survey of animals from Louisiana in the United States, plerocercoids were found in two amphibian, eight reptilian and three mammalian species. The mammalian species included the opossum, the racoon, and the grey fox (Corkum, 1966).

HAZARD TO OTHER ANIMALS: The egg passes in the feces of the cat is not directly infectious to other hosts, the, the hazard to other animals is mainly in the form of the plerocercoid that can be obtained from the drinking of water containing copepods infected with the procercoid stage.

HAZARD TO HUMANS: The procercoids of Spirometra mansonoides are of public health significance as a cause of sparganosis in human beings in the United States; most of the American cases in humans have occurred in the southeastern United States. Mueller and Coulston (1941) had spargana from experimentally infected mice surgically implanted in their arms to show that the sparganum of Spirometra mansonoides was capable of persisting in humans. The introduced spargana were about 2 mm long, and when the larvae were recovered from the investigators three to four months later, the spargana were 12 to 60 mm long. One was fed to a cat, and the cat developed a patent infection. Mueller et al. (1963 a&b) reported on the first naturally acquired human case of sparganosis in the United States. There have been rare cases of sparganosis that are apparently of the Spirometra erinaceieuropaei type and a second form of proliferating sparganosis reported from humans in Florida, but these seem to be the exception rather than the majority of cases. Muller (1974) believes that the characters of the plerocercoid stage is rather characteristic for the two species: that of Spirometra mansonoides is thin and elongate while that of the Spirometra erinaceieuropaei type is massive and rather fragile; the growth factors produced by the two species also appear to have different effects on mice and rats (Mueller, 1972) There have been over fifty cases of human sparganosis reported in the United States, and for further information the readers are referred to Taylor (1976) and the texts by Beaver et al., 1984 and Gutierrez, 1990.

CONTROL/PREVENTION: At no time should cats be allowed to ingest frogs, water snakes or rodents. Such habits may lead to infections with the infective plerocercoid stages of Spirometra. Cats should not be allowed to roam freely or to scavenge carcasses. Predation and carrion feeding may lead to parasitism if prey animals such as frogs, water snakes, rodents or their carcasses contain the infective plerocercoid stages (Hendrix and Blagburn, 1983).

REFERENCES:

Beaver PC, RC Jung, EW Cupp. 1984. Clinical Parasitology, 9th edition. Lea & Febiger, Philadelphia, USA.;

Corkum KC. 1966. Sparganosis in some vertebrates of Louisiana and observations and observations on a human infection. J Parasitol 52:444-448.

Faust EC, Campbell HE, Kellogg CR. 1929. Morphological and biological studies on the species of Diphyllobothrium in China. Am J Hyg 9:560-583.

Fernandez TE. 1978. Reporte del Diphyllobothrium (Spirometra) en el Ecuador. Rev Ecuator Hig Med Trop 31:93-97.

Fukase T, Suzuki M, Igawa H, Chinone S, Akihama S, Itagaki H. 1992. Anthelmintic effect of an injectable formulation of praziquantel against cestodes in dogs and cats. J Jap Vet Med Assoc 45:408-413.

Gutierrez Y. 1990. Diagnostic Pathology of Parasitic Infections with Clinical Correlations. Lea & Febiger, Philadelphia, USA. 532 pages.

Hendrix CM and Blagburn BL. 1983. Common gastrointestinal parasites. Vet Clin N Am: Sm An Prac 13:627-645.

Kirkpatrick CE and Sharninghausen F. 1983. Spirometra sp in a domestic cat in Pennsylvania. J Am Vet Med Assoc 183:111-112.

Lillis WG and Burrows RB. 1964. Natural infections of Spirometra mansonoides in New Jersey cats. J Parasitol 50:680.

Marchiondo AA, Weinstein PP, Mueller JF. 1989. Significance of the distribution of 57Co-Vitamin B12 in Spirometra mansonoides (Cestoidea) during growth and differentiation in mammalian intermediate and definitive hosts. Int J Parasitol 19:119-124.

Mueller JF. 1935. A Diphyllobothrium from cats and dogs in the Syracuse region. J Parasitol 21:114-122.

Mueller JF. 1937. A repartition of the genus Diphyllobothrium. J Parasitol 23:308-310.

Mueller JF. 1938. The life history of Diphyllobothrium mansonoides Mueller, 1935, and some considerations with regard to sparganosis in the United States. Am J Trop Med 18:41-58.

Mueller JF. 1972. Failure of oriental spargana to immunize the hypophysectomized rat against the sparganum growth factor of Spirometra mansonoides. J Parasitol 58:872-875.

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

Mueller JF, Coulston F. 1941. Experimental human infection with the sparganum larva of Spirometramansonoides (Mueller, 1935). Am J Trop Med 21:399-425.

Mueller JF, Hart EP, Walsh WP. 1963a. First reported case of naturally-occurring human sparganosis in New York State. NY State J Med 63:715-718.

Mueller JF, Hart EP, Walsh WP. 1963b. Human sparganosis in the United States J Parasitol 49:294-296.

Mueller JF, Miranda Fróes O, Fernández T. 1975. On the occurrence of Spirometramansonoides in South America. J Parasitol 61:774-775.

Ogassawara S, Benassi S. 1980. Spirometra mansonoides Mueller, 1935, em animal da especie felina no estado de Sao Paulo. Arq Inst Biol Sao Paulo 47:43-46.

Sakamoto T. 1977. The anthelmintic efficacy of Droncit on adult tapeworms of Hydatigera taeniaeformis, Mesocestoidescorti, Echinococcus multilocularis, Diphyllobothrium erinacei, and D. latum. Vet Med Rev 1:64-74.

Taylor RL. 1976. Sparganosis in the United States. Am J Cl Path 66:560-564.

FIGURES:

Figure 3-4. Gravid segment of Spirometra mansonoides showing the compact anterior of the uterus in this genus.

Figure 3-5. Egg of Spirometra mansonoides (Specimen courtesy of Dr. Raab, Florida, USA).

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