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Highlights of Human Toxocariasis

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Highlights of Human Toxocariasis ─1─ The Korean Journal of Parasitology Vol. 39, No. 1, 1-11, March 2001 � Mini-Review � Highlights of human toxocariasis Jean-François MAGNAVAL1)*, Lawrence T. GLICKMAN2), Philippe DORCHIES3) and Bruno MORASSIN1) Service de Parasitologie1), Centre Hospitalier Universitaire Rangueil 31403 Toulouse 4, France, Department of Veterinary Pathobiology2), School of Veterinary Medicine, Purdue University, West Lafayette, IN 47907, USA, Laboratoire de Parasitologie3), École Nationale Vétérinaire, 31076 Toulouse, France Abstract: Human toxocariasis is a helminthozoonosis due to the migration of Toxocara species larvae through human organism. Humans become infected by ingesting either embryonated eggs from soil (geophagia, pica), dirty hands or raw vegetables, or larvae from undercooked giblets. The diagnosis relies upon sensitive immunological methods (ELISA or western-blot) which use Toxocara excretory-secretory antigens. Seroprevalence is high in developed countries, especially in rural areas, and also in some tropical islands. The clinical spectrum of the disease comprises four syndromes, namely visceral larva migrans, ocular larva migrans, and the more recently recognized “common” (in adults) and “covert” (in children) pictures. Therapy of ocular toxocariasis is primarily based upon corticosteroids use, when visceral larva migrans and few cases of common or covert toxocariasis can be treated by anthelmintics whose the most efficient appeared to be diethylcarbamazine. When diagnosed, all of these syndromes require thorough prevention of recontamination (especially by deworming pets) and sanitary education. Key words: Toxocara, toxocariasis, helminthiasis, visceral larva migrans has greatly improved our knowledge of INTRODUCTION toxocariasis, which certainly is the most prevalent helminthiasis in industrialized countries. Human toxocariasis is a helminthozoonosis due to the infestation of humans by ascarid EPIDEMIOLOGY larvae belonging to the genus Toxocara. The first description was made in the early 1950’s, Toxocariasis in the definitive host and for many years this helminthiasis was Among nematodes of the genus Toxocara, regarded as an uncommon pediatric disease. only two species, Toxocara canis and T. cati, Since roughly two decades, the availability of are recognized as causative agents of human sensitive and specific immunodiagnostic tests disease (Beaver et al., 1952; Nagakura et al., 1990). The adult form of both ascarids live in �Received 7 November 2000, accepted after the upper digestive tract of their definitive revision 7 February 2001. hosts, canids and felids, respectively. Female *Corresponding author Prof. J-F. MAGNAVAL, worms may produce up to 200,000 eggs per Service de Parasitologie, Centre Hospitalier Universitaire Rangueil, 31403 Toulouse 4, day. Eggs passed in the feces are not infective France. Phone 33 5 61 32 28 90; fax: 33 5 61 14 and require an incubation period in the soil to 59 72; e-mail: [email protected] embryonate (Glickman and Schantz, 1981). ─2─ Swallowing of infective eggs by adult dogs or positive for T. canis eggs in parks and cats rarely results in the presence of adult playgrounds has ranged from 15 to 78 per Toxocara worms in the digestive tract. The cent (Barriga, 1988). Recent studies have embryonated eggs hatch in the small intestine demonstrated that soil samples taken from where the released larvae perforate the wall. gardens of homes where a clinical case of They then enter a blood vessel and go through toxocariasis is found, are likely to be the liver and lungs to the left heart where they contaminated (Magnaval and Baixench, 1993). are disseminated by the systemic circulation Toxocara eggs have been recovered from salads (somatic migration). Eventually, these larvae and other raw vegetables taken from such penetrate through capillary vessels and gardens (Vazquez et al., 1997). migrate to surrounding tissues where they may survive for years without undergoing Toxocariasis in humans further development (“hypobiosis”). When a Human toxocariasis is primarily a soil- bitch becomes pregnant, the dormant larvae transmitted zoonosis. Geophagia or soil eating can be reactivated by hormonal stimuli and is a specific type of pica that increases the risk migrate transplacentally to the fetus (Dubey, of toxocariasis, especially in children living in 1978). This explains why new-born puppies homes with puppies that have not been are likely to be infected. In contrast, dewormed. Poor personal hygiene as well as transplacental migration of larvae does not consumption of raw vegetables grown in occur in cats. The primary route of infection of contaminated kitchen gardens may result in kittens is by transmammary transmission of chronic low-dose infections. Less commonly, larvae that are found in the milk, whereas this zoonotic toxocariasis infection is associated type of transmission is less important in dogs with consumption of raw meat from potential (Burke and Robertson, 1985). paratenic hosts, such chickens (Nagakura et Infective eggs that are ingested by non-canid al., 1989), lambs (Salem and Schantz, 1992) or and non-felid species follow a somatic cycle rabbits (Sturchler et al., 1990). Among similar to that described above. This leads to veterinary students in Toulouse (France), the the presence of larvae in tissues where they seroprevalence of toxocariasis was significantly are potentially infective to predators on these higher among persons frequently eating raw or animals. This type of transmission is called undercooked calf liver than in persons who ate “paratenesis”. When a dog or a cat preys upon their meat well-done (Baixench et al., 1992). an infected paratenic host, the larvae are This suggests that infective larvae can be liberated from the tissues during the digestion released from animal tissues during digestion process and then complete their development and subsequently cause human toxocariasis. in the intestinal tract (Glickman and Schantz, Toxocariasis is one of the most commonly 1981). reported zoonotic helminth infections in the The prevalence of infection of dogs with world. Seroprevalence surveys in Western adult Toxocara worms was reported to be countries found that 2 to 5 per cent of about 25 per cent in Western countries apparently healthy adults from urban areas (Barriga, 1988), while the rate in cats in had a positive result compared with 14.2 to 37 France was 30 to 60 per cent (Petithory et al., per cent of adults in rural areas (Magnaval et 1996). The prevalence of infection tends to al., 1994a). In tropical countries the decrease with increasing age of the animal and seroprevalence of Toxocara infection was is lower in well-cared pet dogs than in stray or higher, namely 63.2 per cent in Bali (Chomel pound dogs. This high prevalence together et al., 1993), 86 per cent in Saint-Lucia, West with the high fecundity of Toxocara, and the Indies, among children (Thompson et al., increasing number of pet animals in Western 1986), and 92.8 per cent in adults in La countries as well, explain the high level of soil Reunion (French Oversea Territories, Indian contamination with Toxocara eggs in parks, Ocean) (Magnaval et al., 1994b). playgrounds, and other public places. For example, the proportion of soil samples ─3─ unpublished data). PATHOGENESIS OF HUMAN TOXOCARIASIS CLINICAL FEATURES In humans, after ingestion of embryonated Toxocara eggs, the larvae follow the same Advances in the knowledge of the disease somatic route of migration as for paratenic demonstrated that Toxocara infection elicits in hosts. The hatched larvae have been found in humans several different syndromes. the liver, lungs, heart, eye, and brain (Wilder, 1950; Dent et al., 1956). They are often Visceral larva migrans associated with migratory tracks characterized Visceral larva migrans (VLM) was first by hemorrhage, necrosis, and inflammation, described in 1952, in children with an with eosinophils predominating. Larvae may enlarged liver and hypereosinophilia (Beaver et become encapsulated within granulomas al., 1952). The typical VLM patient is a child where they are either destroyed or persist in a between the ages of 2-7 years with a history of viable state for many years. In the eye where geophagia and exposure to puppies in the the migration of a single larva can be home. The acute signs of VLM associated with observed, the inflammatory response can lead hepatic and pulmonary larval migration often to partial or total retinal detachment with include abdominal pain, decreased appetite, visual loss (Neafie and Connor, 1976). The restlessness, fever, coughing, wheezing, host immune responses to migrating larvae asthma, and hepatomegaly. In this phase of appear to be directed against the larval the infection, there is usually a marked excretory-secretory antigens (TES-Ag). These eosinophilia (>2,000 cells/mm3), leukocytosis, antigens are released by larvae from their and hyper-gammaglobulinemia. In Western epicuticle, which is readily sloughed off when countries, the VLM syndrome is rarely bound by specific antibodies (Page et al., encountered, and a review of the literature 1992). The antigens are a mix of glycoproteins from 1952 to 1979 found only 970 such including a potent allergenic component reports (Ehrard and Kernbaum, 1979). (Sugane and Oshima, 1983) which could be similar to the so-called TBA-1 found in adult Ocular larva migrans Toxocara worms. Ocular larva migrans (OLM) typically occurs The mechanism by which larvae in tissues unilaterally in children and young adults. The are killed
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