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Toxascaris leonina

(Figures 4-36 through 4-37)

ETYMOLOGY:Tox = arrow + Ascaris; along with leonina referring to the lion

HISTORY: Sprent (1959) summarized the history and taxonomy of this species. In brief, von Linstow (1902) redescribed one of the ascaridoid parasites of the lion as Ascaris leonina. In 1809, Rudolphi had described the ascaridoid of the lion as Ascaris leptoptera and presented a description of a worm with narrow cervical alae. Unfortunately, in 1819, Rudolphi described some additional worms from the lion as Ascaris leptoptera, but these worms were probably Toxocara cati. Thus, Sprent suggested that the name “leptoptera” be suppressed. The genus name “Toxascaris” was created by Leiper (1907) to contain the arrow-headed ascaridoids with smooth eggs, and Ascaris leonina von Linstow, 1902 was designated at the type species.

GEOGRAPHIC LOCATION: Sprent and Barrett (1964) summarized much of the work on the prevalence of T. leonina in cats up to that time. It had been reported in 1 to 5 cats from North America, 2% to 20.5% of cats in Europe, and in 11% of cats in Ceylon. In 1996, 82% of farm cats in Oxfordshire, UK, were reported to be shedding eggs of this parasite (Yamaguchi et al., 1996); Nichol et al., 1981 found only 1.1% of 92 feral cats in London to bein infected with Toxascaris leonina. In Scotland (McColm and Hutchison, 1980), 3 of 72 stray cats were found to harbor infections with Toxascaris leonina. In Belgium (Vanparijs et al., 1991) 60% of 30 stray cats had fecal samples containing the eggs of Toxascaris leonina. The necropsy of 567 stray cats in Moscow revealed Toxascaris leonina in only 1.1% of the animals (Vereta et al., 1986). In Australia, fecal examination of 376 cats revealed eggs of Toxascaris leonina in 3.7% of the cats (Moore and O’Callaghan, 1985). Okoshi and Usui report that Toxascaris leonina had been previously reported from cats in Taiwan and Sakhalin, but had not been reported or probably seen in Japan until the early 1960's (Okoshi and Usui, 1967). In their paper, they describe five cases of feline toxascariasis, in which all cases were from imported cats (the sources were Hawaii or California) or from cats that had been housed with these imported cats. It was their belief that Toxascaris leonina infection in cats did not occur previously in cats in this country.

LOCATION IN HOST: The adult worms are found in the small intestine of the cat. Dubey (1969) confirmed earlier findings of larvae in the musculature of infected mice beginning seven days after infection where the appear after a lung migration. The larvae remained in the musculature where they encysted and were found in the muscles for up to 60 days after infection (Okoshi and Usui, 1968) and probably persist in the muscles of the carcase for much longer periods.

PARASITE IDENTIFICATION: The adults of Toxascaris leonina are cream colored to pinkish worms (Fig 4-36). The females are around 6 to 10 cm in length and the males are around 5 cm long (Okoshi and Usui, 1967). The cervical alae of Toxascaris leonina adults are longer and considerably narrower than those of Toxocara cati, and the head of Toxascaris leonina resembles a spear while the head of Toxocara cati resembles an arrow head (Sprent and Barrett, 1964). There is no ventriculus at the base of the esophagus of Toxascaris leonina (Sprent, 1968). The vulva of the female Toxascaris leonina is about one-third of the length of the body behind the anterior end of the worm (Okoshi and Usui, 1967). The males of Toxascaris leonina have tails which gradually taper to a point. The eggs of the Toxascaris leonina have a smooth shell, are ellipsoid, and have dimensions of about 70 um by 80 um (Fig 4-37); Warren (1971) reported ex utero eggs as having dimension of 54 by 74 um. The eggs of Toxascaris leonina typically appear clearer or more translucent than the eggs of Toxocara cati.

LIFE CYCLE: The adult male and female worms live in the small intestine, and the female produces eggs that are passed in the feces. Wright (1935) found that the eggs of Toxascaris leonina, unlike those of Toxocara canis, were capable of developing to the infective stage at 37C. Okoshi and Usui (1967) reported that around 95% of eggs contained infective-stage larvae after four days of culture at 25C. They reported that at 17 to 22C, it took 6 days for 99% of the eggs to reach the infective stage; at 30C, it took five days, and confirming the work of Wright, they found that 97% of the eggs reached the infective stage when held at 37C (Also, as reported by Wallace for Toxocara canis, the eggs of Toxocara canis and Toxocara cati failed to develop at 37C.). When the eggs of Toxascaris leonina were held at 40OC they were incapable of completing their development, and even after being returned to 25C after 24 hours at 40C were incapable of developing. For the purpose of this discussion, it is considered that the infective-stage larva is a third-stage larva. The tail of the infective-stage larva bears a small knob reminiscent of the small terminal projection present on the tail of the third-stage larva of Lagochilascaris spp. (See below).

Sprent (1959) and Okosh and Usui (1968) have examined the development of Toxascaris leonina in cats infected by the feeding of embryonated eggs. After ingestion of the eggs, Sprent found that the larvae enter the wall of the small intestine. Within the intestinal wall the larvae grow to a length of 0.5 to 0.6 mm. Then either within the wall or after returning to the intestinal lumen, the larvae molt to the fourth stage. The fourth-stage larvae grow to lengths of up to around 6 mm which is when the molt to the adult stage occurs. Adults appeared as early as 28 days after infection, but eggs did not appear in the feces until 74 days after infection. Okoshi and Usui found that adults were first present sometime between Day 22 to Day 48 after infection, and in their infections, the prepatent period was 62 to 63 days. Both Sprent and Okoshi and Usui were unable to infect cats with eggs recovered from naturally infected dogs, but Petrov and Borovkova (1959) had been successful in infecting cats and dogs with eggs recovered from foxes.

Sprent (1959) also showed that cats could be infected with the larvae present in experimentally infected mice. Infections with larvae in mice proved to be less successful than with eggs. Cats were capable of supporting larvae of both canine and feline isolates when murine tissues containing these larvae were ingested. Okoshi and Usui (1968) were also capable of recovering developing larvae of the canine isolates when the source of infection was infected murine tissue.

Sprent noted that a characteristic feature of infections with Toxascaris leonina in the cat was the persistence of small fourth-stage larvae in the wall and intestinal lumen of the cats for weeks to months after infection. These persistent fourth-stage larvae followed infections with either eggs from feces or larvae from mice.

Toxascaris leonina is capable of persisting in the tissues of paratenic hosts. Wright (1935) found that when eggs were fed to mice, rats, guinea pigs and dogs that larvae could be recovered from the intestinal wall and lumen 10 days after infection and that these larvae grew to a length of around 0.7 mm. Matoff (1949) studied the migration of Toxascaris leonina in experimentally infected mice and found that although many of the larvae became encysted in the wall, some larvae also underwent either a hepato-pulmonary or a lympho-pulmonary migration and that these larvae later appeared in an encysted state in the musculature of the head and carcass. In 1965, Matoff and Komandarev reported on additional studies where they found considerable larvae in the abdominal cavities of mice after infection, but with the majority in the wall of the intestine 10 days after infection. Okoshi and Usui (1968) infected fed the eggs of Toxascaris leonina to mice, chickens, and earthworms. In mice, they found that the larvae were mainly in the intestine up to seven days after infection, and that the number then decrease gradually and that the larvae disappeared from this organ by the 15th day after infection. They found small numbers of larvae in the liver and lungs between the 6th to the 13th day after infection, with larvae then being found in the carcass (39.6% of the inoculum was recovered from the carcass on the 12th day after infection. Living larvae were recovered from the carcass three months after inoculation. The larvae in the mice grew to about 0.87 mm in total length. In chickens, they found that the majority of larvae stayed in the intestinal wall although a very few were recovered from the lungs, liver, carcase, and brain. In earthworms, no larvae were recovered, although larvae of Toxocara canis and Toxocara cati were recovered from similar earthworms infected using the same methods. When larvae from mice were harvested from the carcass 20 to 60 days after infection and orally inoculated into additional mice, larva were again recovered from the carcasses of these mice. Larvae harvested from the carcass of one of the second group of mice 10 days after infection were infective to another mice. Thus, these authors showed that the infection could be perpetuated in mice by the repeated passage of the larvae. Dubey (1969) found larvae in the musculature of mice beginning 10 days after infection. The lungs of the mice killed 6 to 10 days after infection were found to have numerous hemorrhages and to contain larvae. Dubey however found few larvae in the liver and increasing numbers of larvae in the mesenteric lymph glands and concluded that the larvae underwent a migration to the lungs via the thoracic lymphatic duct. Prokopic and Figallova (1982) examined the migration of larvae in white mice for up to 135 days after infection. They found that although some larvae could be found in the intestinal wall during the entire observation period, the majority of larvae were present beginning 10 days after infection in the intercostal muscles and the muscles of the legs. They found larvae in the lungs as early as 4 days after infection. Karbach and Stoye (1982) found that mouse pups were not infected transplacentally inf the mothers were infected while pregnant. When mothers were infected with 1,000 larvae, the largest number of larvae were recovered from the pups if the mother was infected at parturition. However, infection of pups occurred with small numbers of mothers were infected 20, 40, 80, or even 160 days prior to parturition. Bowman (1987) described the morphology of the larvae of Toxascaris leonina recovered from mouse tissues 32 days after infection.

CLINICAL PRESENTATION AND PATHOGENESIS: There appear to be few clinical signs associated with Toxascaris leonina infections in cats. For puppies, Okoshi and Usui (1967) described clinical signs consisting of digestive disturbance, allotriophagia, and unthriftiness having appeared, but they saw no such signs in adult dogs. These same authors reported no such signs for the experimentally infected cats. Fei et al. (1986) reported a fatal case of toxascariasis in a kitten in Taiwan that was accompanied by bloody diarrhea.

TREATMENT: The treatment of cats for adults of Toxascaris leonina is relatively straightforward. Approved compounds include toluene, dichlorvos, pyrantel, piperazine, febantel, milbemycin, moxidectin, and emodepside. Mebendazole at 30 mg per kg body weight for two days is efficacious (Cardini et al., 1997). A single dose of nitroscanate at 50 mg per kg body weight was 100% effective in removing the adults of Toxascaris leonina from dogs (Boray et al., 1979).

EPIZOOTIOLOGY: Cats can become infected by ingesting either the egg or rodents that contain the larvae of Toxascaris leonina. The common occurrence of Toxascaris leonina in felids in zoological gardens would suggest that the egg is a very common source of infection. The ability of the egg to embryonate at a wide range of temperatures and to become infective as rapidly as four days after being passed in the feces would suggest that infective eggs can rapidly build up in the environment. Although the eggs will nt develop if held at 40C, Okoshi and Usui showed that if they were exposed to -15C for up to 40 days and then returned to 25C, that almost all would complete the development to the infective stage. Thus, freezing temperatures had very little effect on their ability to later develop.

Surveys of soil samples in cities have revealed the presence of the eggs of Toxascaris leonina. Pfeiffer (1983) reported eggs present in 4 of 334 soil samples collected from public gardens and children’s playgrounds in Vienna, Austria. Veteta and Mamykova (1984) found eggs in 5 of 311 soils collected in pre-school institutions in Moscow. Rapic et al. (1983) reported eggs of Toxascaris leonina in 10 or 100 urban soil samples collected in Zagreb, Yugoslavia. Bettini and Canestri-Trotti (1978) reported the presence of these eggs in 10 of 204 samples collected in Bologna, Italy. The most common egg in almost all these surveys was the egg of Toxocara spp., but there was no attempt to distinguish between the eggs of Toxocara canis and Toxocara cati.

HAZARDS TO OTHER ANIMALS:Toxascaris leonina is commonly found in canids and felids. This parasite very commonly infects large cats in zoos (Abdel-Rasoul and Fowler, 1979 and 1980) and can be a common problem also in foxes. Sprent (1969) gives a host list that includes the arctic fox, jackal, dingo, dog, coyote, wolf, arctic wolf, cape hunting dog, raccoon dog, grey fox, american red fox, indian fox, cheetah, lynx, bobcat, pumas, ocelots, servals, snow leopard, jaguar, tiger, lion, leopard, and other species. As in the cat host, usually there is little disease associated with the infections. Fenbendazole has been approved for use in the treatment of helminth infections in many zoo animals and would be a very good candidate for treating infections with this parasite.

HAZARD TO HUMANS: The biology of this parasite in mice is such that it would be expected that there are human infections with the larvae of this parasite acquired by the ingestion of eggs in contaminated soil or on contaminated foodstuffs; however, except for the report of BOWMAN (see below), there have been no reports of larval toxascarisis in humans. There are, however, two rather strange accounts of human parasitism with adult Toxascaris leonina. When Leiper (1907) described the genus Toxascaris he included humans in the host list. Grinberg (1961) reported on a 39-year-old male patient who complained of having chronic osteomyositis for the last 15 years. He presented with an abscessed area on the right shin with 5 tracts and a dark brown scab covering an inflamed area. Squeezing the area produced two worms. The patient had also brought 20 additional worms with him to the clinic and stated that he had extracted some 50 additional worms 5 years previously. The worms were 6 to 7 cm long, whitish-pink in color, with 3 lips, the female had a rounded tail, and the male had awl-shaped spicules.. The females contained eggs that had smooth shells. Based on the morphology of the 2 worms supplied by the patient and the two extracted in the clinic, a diagnosis of Toxascaris leonina was made.

Beaver and Bowman (1984) described a larvae from the eye of a child in East Africa that was about twice the size of Toxascaris larvae observed in tissues. However, no species of the other similar ascaridoid genus, Baylisascaris, are known to occur in Africa, and it was considered that it was possible that this larva represented a case of infection with a larva of some Toxascaris species.

CONTROL/PREVENTION: Due to the rapid development of the eggs of Toxascaris leonina, control in catteries requires excellent cleanliness. Abdel-Rasoul and Fowler (1980) reported finding viable eggs on the floors of cages and in the drinking water of a number of large felids in zoos in California. It also appear that older animals can be reinfected with this parasite, thus, regular deworming of cats is a must for good control to be obtained. Because domestic cats can probably also acquire their infections from hunting, if cats do go outside, it would be expected that they could be infected from either soil or from the ingestion of infected rodents. Thus, regular examination of the feces of such cats for parasites would be a prudent approach to control. The amount of ivermectin in Heartgard for cats (a maximum dose of 24 ug per kg body weight) is probably not sufficient for 100% control of the infections with this parasite.


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Figure 4-36. Toxascaris leonina. Adult male and female fixed in 10% formalin. Note that the male tail curls in the opposite direction as the head.

Figure 4-37. Toxascarisleonina. Egg passed in feces. Notice the thick shell that has a smooth exterior.