The nematode worms Toxocara canis and Tox-ocara cati were first described by Werner (1798) and Schrank (1788), respectively. Ransom and Foster (1920) recognised that T. canis infected hosts other than the dog. These authors found the larvae of T. canis in the lungs of rats following the ingestion of embryonated eggs. Sprent (1952) noted the presence of larvae in the intestine, liver, lungs, kidneys, skeletal muscles and nervous tissue of mice following infection. Levine (1980) showed that many mammals and birds could be infected. Basic features of the life-cycles of T. canis and T. cati were first described by Sprent (1957, 1958).
Three clinical syndromes have now been associated with human infection with Toxocara-, visceral larva migrans, ocular larva migrans and covert toxocariasis. Historically speaking these syndromes were described as follows.
Visceral Larva Migrans (VLM)
In the early 1920s and 1930s a number of authors recognised that larval Toxocara spp. were potentially infective to humans (Fulleborn, 1921; Chandler, 1925; Schwartz, 1932) but it was not until 20 years later that a clinical syndrome in children, characterised by persistent eosinophilia, was attributed to infection with ascarid larvae. Four reports described chronic extreme eosinophilia accompanied by eosinophilic granulomatous lesions in an enlarged liver, together with some degree of pulmonary infiltration, fever, cough and hyperglobulinaemia (Zuelzer and Apt, 1949; Perlingiero and Gyorgy, 1947; Mercer et al., 1950; Behrer, 1951). Parasites were not described by Zuelzer and Apt, but the other three reports suggested that the infective agent was Ascaris lumbricoides (this was disputed by Beaver and colleagues in their subsequent paper and Toxocara was put forward as a more credible aetiological agent). Then Beaver et al. (1952) described three further human cases and identified T. canis larvae in a liver biopsy specimen. This led to the designation of the term 'visceral larva migrans' to describe the migration of larvae through the tissues and the consequent clinical symptoms and pathogenesis associated with the larval presence. The essentials for diagnosis of visceral larva migrans have been regarded as eosinophilia of over 30% in children with a history of eating dirt and with no other cause of eosinophilia (Snyder, 1961).
Ocular Larva Migrans (OLM)
The second major clinical syndrome associated with toxocariasis is ocular larva migrans and this was first recognised by Wilder (1950), who observed microscopic evidence of nematode infection in eyes which had been enucleated because retinoblastoma was suspected. In 24 of
Edited by Stephen Gillespie and Richard D. Pearson © 2001 John Wiley & Sons Ltd the 46 eyes, either the larva or a residual hyaline capsule was seen. These larvae were later identified as Toxocara spp. by Nichols (1956). Prior to this, Calhoun (1937) had recorded invasion of the anterior chamber of a child's eye by a nematode larva, which he identified as an Ascaris larva.
Covert Toxocariasis (CT)
The third, much more recently described syndrome associated with human toxocariasis is covert toxocariasis. This term was put forward by Taylor et al. (1987) to describe a series of comparatively non-specific but recognisable symptoms and signs associated with raised Tox-ocara titres but not falling into either of the categories of ocular larva migrans or classical visceral larva migrans. That such an entity might exist had been suggested by Bass et al. (1983). Taylor et al. (1987) recorded symptoms and signs, including abdominal pain, anorexia, nausea, vomiting, hepatomegaly, splenomegaly, lethargy and weakness, limb pains, cough, wheeze, asthma, cervical adenitis and pharyngitis.
Recent reviews of toxocaral disease, mainly from the viewpoint of human disease, have been published both as papers (Gillespie, 1993; Magnaval et al., 1994) and in book form (Lewis and Maizels, 1993).
DESCRIPTION OF THE ORGANISM Taxonomic Classification
Toxocara spp. belong to the Phylum Nematoda, Subclass II Secernentea, Order 2 Ascaridida, Superfamily Ascaridoidea (Smyth, 1994). The order Ascaridida is described as a group of large intestinal worms with a three-lipped mouth, pharynx bulbed or cylindrical, vagina elongate, male usually with ventrally curled tail and two spicules, alae may be present.
Morphology Adult Worms
The two species Toxocara canis (Werner, 1782) Johnstone, 1916, and Toxocara cati (Shrank,
1788; Brumpt, 1927), are ascaridid nematodes which live as adult worms in the proximal intestine of dogs and cats, respectively (Coombs and Crompton, 1991). Adult female T. canis worms measure 6-18 cm and males 4-10 cm; female T. cati measure 4-12 cm and males 3-6 cm
The eggs of the two species are indistinguishable at the light microscopic level, both being described as nearly or almost spherical, sometimes oval, with a thick, rough pitted shell and dark brown to black granular contents. The eggs of T. canis are sometimes larger, measuring 75 x 90 in contrast to T. cati at 65 x 75 ^ (Thienpoint et al., 1979).
The infective larvae of T. canis and T. cati are about 400 ^ long and 15-21 ^ in diameter. The two species are almost identical morphologically, differing only in their maximum diameter (T. canis 18-21 p.m, T. cati 15-17 p.m).
The life-cycle of T. canis in the dog, T. cati in the cat and Toxocara infection in the paratenic host, including humans, will be described separately. It should be stated that there is a perception, albeit based upon circumstantial evidence, that T. cati is less significant as an aetiological agent in human infections, but at this stage it is not routinely possible to distinguish between the two species serologically.
However, Petithory et al. (1993) reported, out of a total of nine human cases of ocular larva migrans, the presence of antibody to T. cati in the vitreous humour of six subjects. In all cases but one, antibody to T. canis was also present. On the basis of these observations, the authors put forward the suggestion that T. cati may play a more important role in ocular larva migrans than previously thought.
One significant factor in reducing the likelihood of human T. cati infection may be the
I Predators including Man |
Fig. 19a.1 Life-cycle of Toxocara canis more fastidious defaecation habits of cats compared with dogs, and hence the lower number of T. cati eggs compared to T. canis eggs detected in soil samples (O'Lorcain, 1994). Under experimental conditions, O'Lorcain (1995) recorded that embryonated T. cati ova exhibited greater resistance to freezing than those of T. canis, a factor that might influence the relative survival of the ova under certain climatic conditions.
Lloyd (1993) has suggested that the life-cycle in the dog (Figure 19a.1) is best understood if divided into two parts: (a) adult T. canis infections in the intestines of puppies and the lactating bitch, and (b) adult T. canis infections in mature dogs.
Adult T. canis infections in the intestines of puppies and the lactating bitch arise from three sources—somatic migration of larvae, maternal transmission of larvae to the puppies and infection of immature worms from puppies to the mother. Embryonated and hence infective eggs in the environment are ingested by the bitch (and other mature dogs), hatch in the intestine, and then the larvae undergo a somatic migration to the tissues. Larvae are first found in the liver, then the lungs and finally the skeletal muscles, they can also be found in other sites, including the brain. Maternal transmission of larvae from mother to offspring usually occurs transplacen-tally and arises from somatic larvae accumulated prior to or in early pregnancy (Burke and Roberson, 1985). Transplacental migration occurs after the 42nd day of pregnancy and has been attributed to hormonal changes in the pregnant bitch. Larvae can also be transmitted via the mammary glands and the milk. Once the puppies are born, larvae from their tissues complete their migration via the lungs and end up as adult worms in the small intestine. Lactating bitches can become infected with Toxocara eggs by cleaning up after their puppies and ingesting faeces or vomitus containing eggs.
Mature dogs, like bitches, can become infected by ingesting infective T. canis eggs from the environment. These hatch and the larvae undergo a tracheal migration and end up as mature adult worms in the intestine. This tracheal migration involves the penetration of larvae into the pulmonary blood vessels, followed by entrance into the alveoli, migration up the bronchi and trachea and eventual swallowing of larvae and their emergence into the small intestine. Some larvae may also become arrested in the tissues and become dormant. In addition, adult dogs may become infected as a consequence of ingesting the tissues of a variety of infected paratenic hosts (see below). Infection with T. canis occurs in a range of other carnivores, particularly the red fox (Vulpes vulpes) (Richards and Lewis, 1993).
The life-cycle of T. cati is essentially similar to that of T. canis. The major difference lies in the fact that transplacental infection from mother to offspring does not occur but transmammary infection is common (Oldham, 1965; Soulsby, 1982). Infection derived from paratenic hosts is likely to be important in cats, due to their predatory nature and the fact that sources of infective eggs will be less common due to their fastidious defaecatory behaviour.
Toxocara canis Infection in the Paratenic Host, Including Humans
Toxocara infective eggs can be ingested by a variety of non-canid paratenic or transport hosts. These include earthworms, rats, mice, pigeons, chickens, lambs, pigs and, most significantly, humans. The eggs hatch to produce second stage larvae that undergo a somatic migration but fail to mature into adult worms in the intestine. It should be noted that there is some debate as to the number of moults the larvae undergo at this stage. Following maturation in the soil, the embryonic eggs undergo one moult within the egg and then infective larvae hatch in the host intestine to produce the invasive L2 stage. The larvae remain arrested in a variety of tissues and organs and only upon ingestion by an appropriate definitive host will they develop to maturity in the host intestine. There is also evidence from experimentally infected rodents that these Toxocara larvae are capable of accumulation in the brain (Dunsmore et al., 1983). Human infection has classically been associated with geophagia (earth eating). Infection may also occur from ingestion of eggs from soil-contaminated hands or from soil-contaminated vegetables, eaten raw, or from undercooked or raw animal products (Salem and Schantz, 1992; Nagakura et al., 1989).
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