Spirometra erinaceieuropaei (Rudolphi, 1819)
ETYMOLOGY:Spiro = spiral and metra = uterus (referring to the spiral-shaped uterus as opposed to the rosette-shaped uterus in Diphyllobothrium) and erinaceieuropaei for the European hedgehog (genus=Erinaceus) from which the larval stage was originally recovered and named.
SYNONYMS: The following list of synonyms is taken from Schmidt (1986) who did not recognize the genus Spirometra, considering it a synonym of Diphyllobothrium: Bothriocephalus decipiens Railliet, 1866; Bothriocephalus felis Creplin, 1825; Bothriocephalus maculatus Leuckart, 1848; Bothriocephalusmansoni (Cobbald, 1882) Blanchard, 1888; Bothriocephalus liguloides (Diesing, 1859), Bothriocephalus sulcatus Molin, 1858; Dibothrium serratum Diesing, 1850; Dibothrium mansoni Ariola, 1900; Diphyllobothrium fausti Vialli, 1931; Dubium erinacei-europaei Rudolphi, 1819; Ligula mansoni Cobbold, 1882; Ligula pancerii Polonio, 1860; Ligula ranarum Gastaldi, 1854; Ligula reptans Diesing, 1850; Sparganum affine Diesing, 1854; Sparganum ellipticum Molin, 1858; Sparganum mansoni (Cobbold, 1882) Stiles and Taylor, 1902; Sparganum philippinensis Tubangui, 1924; Sparganum proliferum Ijima, 1905; Sparganum reptans Diesing, 1854; Spirometra decipiens Faust, Campbell, and Kellogg, 1929; Spirometra erinacei Faust, Campbell, and Kellogg, 1929; Spirometra houghtoni Faust, Campbell, and Kellogg, 1929; Spirometra okumurai Faust, Campbell, and Kellogg, 1929; Spirometra raillieti (Ratz, 1913) Wardle, McLeod, and Stewart, 1947; Spirometra ranarum Meggitt, 1925; Spirometra reptans (Diesing, 1850) Meggitt, 1924; Spirometra tangalongi (MacCallum, 1921).
HISTORY: In 1819, Rudolphi described a larval tapeworm recovered from a European hedgehog as the species erinaceieuropaei. Faust et al. (1929) recovered larval stages from a Chinese hedgehog (Erinaceus dealbatus) and reared the adult stage by feeding this form to dogs. These authors believed this form identical to that described by Rudolphi from the European hedgehog. While this was occurring, Dr. Patrick Manson in 1882 recovered 12 tapeworm larvae, spargana, during an autopsy in Amoy, China, and these worms came to be known as Manson’s sparganum, or Sparganum mansoni. In 1917, Yoshida obtained adult worms by feeding sparganids obtained from humans to dogs. Joyeux and Houdemer (1928) described Spirometra mansoni (as Diphyllobothrium mansoni) using sparganids obtained from different animals in Southeast Asia. Odening (1982) reexamined the biology of the European form. Work of Fukumoto et al. (1992) on the isoenzyme patterns of Spirometra erinaceieuropaei from Japan and Australia, indicated that these two forms were similar.
GEOGRAPHIC DISTRIBUTION: Spirometra mansoni has been reported from numerous occasions from the orient (Fujinami et al., 1983; Tang, 1935 [sparganosis in cat], Wu, 1938; Rhode, 1962; Shanta et al., 1980). Schmidt et al. (1975) found Spirometra in cats from Taiwan and the Philippines; Tongson and San Pablo (1979) also reported Spirometra mansoni from the Philippines. It has been reported from the Americas (Mueller et al., 1975; Torres and Figueroa, 1982). Spirometra mansoni has also been reported in cats from Hawaii (Olsen and Hass, 1976) and Puerto Rico (Acholonu, 1977). Australia can also be considered to be within the range of Spirometra mansoni (Gregory and Munday, 1976; Thompson et al., 1993). Reports from Europe include those of Odening (1982) and Manfredi and Felicita (1993).
LOCATION IN HOST: Adult worms are found in the small intestine. Cats can on occasion be infected with the plerocercoid larval stage (see section of Sparganosis).
PARASITE IDENTIFICATION: The strobila of this tapeworm is about 1 m long and less than 1 cm in width. The bothria is similar to that of Diphyllobothrium. The uterus of Spirometra spp. appears spiral as the uterine loops from the posterior to the anterior pile up on each other; the uterus of Diphyllobothrium appears to have a rosette formation. Each proglottid has separate openings of the cirrus and vaginal pore that are in the anterior portion of each segment, while the uterine pore is in the posterior of each segment. In contrast, the cirrus and vaginal pores of Diphyllobothrium are fused into a single pore. Also, the cirrus sac and seminal vesicle are fused together in Spirometra.
The proglottids of Spirometra erinaceieuropaei contain a uterus that is not expanded terminally into a U-shaped portion as is the case with Spirometra mansonoides.
The egg of Spirometra resembles the egg of a digenetic trematode, that is, it is oval and possesses a distinct operculum at one pole of the shell. The eggs are oval, yellow-brown and have dimensions that average 60 µm by 36 µm. The eggs have an asymmetric appearance and tend to be pointed at one end. On eggs that are ruptured, a distinct operculum is visible. 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: It is reported that the Asian and African forms of Spirometra erinaceieuropaei, typically prefer the dog as the final host (Mueller, 1974). The life cycle has been completed experimentally through all stages in the laboratory (Lee et al., 1990). The egg that is passed in the feces is not embryonated. After a few days in the water, a ciliated larva with 6 hooklets typical of tapeworms (called a coracidium) hatches and swims about. This larva is ingested by copepods of the genus Mesocyclops and Eucyclops, and within the body cavities of these minute crustaceans, a small larval stage called a procercoid develops. Once the larva is 15 days old, it is infective to tadpoles. Once this stage in the tadpole, which is called a plerocercoid, is 15 days old, it is capable of infecting murine paratenic hosts. After cats are orally infected with plerocercoids, eggs appear in the feces in 15 to 18 days.
Odening (1982) compiled the literature on the prepatent period and life expectancy of Spirometra erinaceieuropaei using experimental infections with plerocercoids obtained from hosts from Poland, Burma, Japan, North America, Thailand, and Russia made observations on these events. He found the prepatent period in cats to be between 10 and 25 days and found that the worms in cats lived between 178 to 763 days, or about 6 months to 2 and one-half years. Odening also reported that the shedding of eggs and proglottids appeared to occur in cycles where the cats would shed eggs for about a month and then would undergo a similar period where no eggs were found in the feces. The necropsy cats in the "negative phase” revealed that only the scolex and anterior body were present during this period, and it was felt that this occurred if even more than one tapeworm from the same initial infection were present, i.e., that somehow the shedding of the "spent” proglottids became synchronized.
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. There has been very little reported on the signs associated with infection, so it can be assumed that infection is asymptotic in the cat.
TREATMENT: Oral, subcutaneous, or intramuscular administration of praziquantel at 30 mg/kg body weight to cats experimentally infected with Spirometraerinaceieuropaei cleared all animals of their infections (Fukase et al., 1992). Treatment of 22 cats with naturally acquired infections by the intramuscular or subcutaneous administration of 34 mg/kg body weight eliminated the cestodes from the treated animals. Note: this treatment is with dosages of praziquantel that are greater than those required to treat intestinal dipylidiasis and taeniasis in cats.
EPIZOOTIOLOGY: Dogs and cats serve as major hosts of the adults of Spirometra erinaceieuropaei. Cats become infected when they eat infected prey The plerocercoids are present in amphibia, reptiles, and small mammals. Thus, the infection would be expected in cats that hunt. Uga and Yatomi (1992) reported that a survey of cats in Japan revealed that there were almost no cases where cats were infected with both Spirometra erinaceieuropaei and with Dipylidium caninum. Experimental infection of cats with larval stages from both parasites revealed that only adults of Spirometra erinaceieuropaei developed in cats given larvae of both types suggesting that somehow infection with this species prevented the development of Dipylidium caninum through some form of competition.
HAZARD TO OTHER ANIMALS: The hazard posed by the stage passed in the feces of the cat is minimal because it requires a period of development in water to produce the larval stage infectious to copepods. However, infected cats are shedding eggs into the environment that might infect copepods that would then pose a threat to any animal that might be drinking unfiltered water. Thus, infected cats should be treated even if they show no untoward signs from their infection..
HAZARD TO HUMANS: Humans have been reported to be infected with both the larval stage and the adult stage of this parasite.
Infection with the larval stage of Spirometra is termed sparganosis and for a summary of the human cases of sparganosis the reader is referred to texts on human parasitology (Beaver et al., 1984; Gutierrez, 1990). Humans may become infected in three ways: 1) by the accidental ingestion of the aquatic crustacean Cyclops infected with procercoids. These procercoids migrate to the subcutaneous tissues and develop to plerocercoids; 2) by the ingestion of plerocercoids within the second intermediate host. These plerocercoids are found in the connective tissue of the muscles, particularly of the abdomen and hind limbs and under the peritoneum, pericardium and pleura of the second intermediate host. When these plerocercoids are ingested by humans, they migrate to the various tissue sites and reestablish in the human; and 3) by the application of poultices. When infected frog or snake flesh is used as a wound dressing or applied to the eyes, the plerocercoids may migrate to these sites. The plerocercoids migrate subcutaneously producing inflammation, urticaria, edema and eosinophilia. Spargana are often found in the periorbital area, in the subcutaneous tissues and in the muscles. The most probable source of infection is contaminated drinking water (Taylor, 1976).
There have been five cases where humans have been infected with the adult stage of this parasite (Suzuki et al., 1982).
CONTROL/PREVENTION: Prevention would require that cats be dissuaded from hunting which is liable to be an impossibility. Thus, it will be necessary to perform fecal examinations on cats living in areas where this parasite is present. Because of the nature of this parasite to undergo periods when eggs are not present in the feces, it may be necessary to perform more than one fecal examination each year to insure that a cat is free of this parasite.
Acholonu AD. 1977. Some helminths of domestic fissipeds in Ponce, Puerto Rico. J Parasitol 63:757-758.
Beaver PC, RC Jung, EW Cupp. 1984. Clinical Parasitology, 9th edition. Lea & Febiger, Philadelphia, USA.;
Faust EC, Campbell HE, Kellogg CR. 1929. Morphological and biological studies on the species of Diphyllobothrium in China. Am J Hyg 9:560-583.
Fujinami F, Tanaka H, Ohshima S. 1983. Prevalence of protozoan and helminth parasites in cats for experimental use obtained from Kanto Area, Japan. Exp Anim 32:133-137.
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.
Fukumoto S, Tsuboi T, Hirai K, Phares CK. 1992. Comparison of isozyme patterns between Spirometra erinacei and Spirometra mansonoides by isoelectric focusing. J Parasitol 78:735-738.
Gregory GG, Munday BL. 1976. Internal parasites of feral cats from the Tasmanian Midlands and King Island. Aust Vet J 52:317-320.
Gutierrez Y. 1990. Diagnostic Pathology of Parasitic Infections with Clinical Correlations. Lea & Febiger, Philadelphia, USA. 532 pages.
Joyeux C, Houdemer E. 1928. Recherches sur la faune helminthologique d l’Indochine (cestodes et trématodes). Ann Parasitol Hum Comp 6:27-58.
Lee SH, We JS, Sohn WM, Hong ST, Chai JY. 1990. Experimental life history of Spirometraerinacei. Kor J Parasitol 28:161-173.
Manfredi MT, Felicita A. 1993. Recenti rilievi epidemiologici sui cestodi del cane e del gatto. Prax Vet Milano 14:5-7.
Mueller JF. 1974. The biology of Spirometra. J Parasitol 60:3-14.
Mueller JF, Miranda Fróes O, Fernández T. 1975. On the occurrence of Spirometramansonoides in South America. J Parasitol 61:774-775.
Odening K. 1982. Zur Strobilaperiodizität von Spirometra (Cestoda: Diphyllobothriidae). Angew Parasitol 24:14-27.
Olsen OW, Hass WR. 1976. A new record of Spirmetra mansoni, a zoonotic tapeworm, from naturally infected cats and dogs in Hawaii. Hawaii Med J 35:261-263.
Rhode K. 1962. Helminthen aus Katzen un Junden in Malaya; Bermerkungen zu ihrer epidemiologischen Bedeutung für Menschen. Ztsch Parasitenk 22:237-244.
Rudolphi CA. Entozoorum synopsis cui accedeunt mantiss duplex et indices locupletissimi. 811 pages, Berolini.
Schmidt GD. 1986. Handbook of Tapeworm Identification. CRC Press, Boca Raton, Florida, USA, 675 pages.
Schmidt GD, Fuerstein V, Kuntz RE. 1975. Tapeworms of domestic dogs and cats in Taiwan with remarks on Spirometra spp. BS Chauhan Comm Vol 41-46.
Shanta CS, Wan SP, Kwong KH. 1980. A survey of the endo- and ectoparasites of cats in and around Ipoh, West Malaysia. Malay Vet J 7:17-27.
Suzuki N, Kumazawa H, Hosogi H, nakagawa O. 1982. A case of human infection with the adult of Spirometra erinacei (Rudolphi, 1819) Faust, Campbell and Kellogg, 1929. Jap J Parasitol 31:23-26. 1982)
Tang CC. 1935. A survey of helminth fauna of cats in Foochow. Pek Nat Hist Bull 10:223-231.
Thompson RCA, Meloni BP, hopkins RM, Deplazes P, Reynoldson JA. 1993. Observations on the endo- and ectoparasites affecting dogs and cats in aboriginal communities in the north-west of western Australia. Aust Vet J 70:268-270.
Tongson MS, San Pablo FG. (1979) A study on the prevalence of gastrointestinal worms of cats in metropolitan Manila. Philip J Vet Med 18:1-15.
Torres P, Figueroa L. 1982. infeccion por Spirometra mansoni (Cestoda, Pseudophyllidea) en el sur de Chile. Bol Chileno Parastiol 37:72-73.)
Uga S, Yatomi K. 1992. Interspecific competition between Spirometraerinacei (Rudolphi, 1819) and Dipylidiumcaninum (Linnaeus, 1758) in cats. Jap J Parasitol 41:414-419.
Wu K. 1938. Helminthic fauna in vertebrates of the Hangchow area. Pek Nat Hist Bull 12:1-8.
Yoshida S. 1917. The occurrence of Bothriocephalus liguloides Leuckart, with special reference to its development. J Parasitol 3:171-176.