Frequency (%) of soil contamination of public areas by Toxocara spp. eggsT and Ancylostoma spp. eggs/larvaeA in different continents.
The soil is an important route for transmission of numerous human pathogens, including the five major soil-transmitted helminths (STHs), also known as geohelminths, namely: roundworm (
Zoonotic agents, comprising a wide variety of bacteria, viruses, and parasites, account for almost two thirds of all known human infections. Some helminthoses that commonly infect canids and felids are typically soil-transmitted. This chapter focuses on two major groups of STHs that cause disease in humans: (a) the ascarids
A third soil-transmitted ascarid species that can cause human disease is
Toxocara canisand Toxocara cati
The causal agents of human toxocariasis are the ascarid nematodes (roundworms)
The age of definitive hosts, particularly dogs, correlates negatively with the burden of infection with adult worms. Adult
T. canis larvae arrested in the tissues may be transmitted from bitches to offspring via the placenta (transplacental transmission). However, this phenomenon is not observed in T. cati infections of cats. During the last trimester of pregnancy of the bitch, tissue-arrested larvae become mobile due to hormonal influence. Larvae migrate to the lungs of the fetus. In the newborn puppy, the life cycle is complete when the larva migrates, via trachea, to the intestinal lumen, where the final molts take place. Adult worms can be found at two weeks of age, whereas large numbers of eggs can be detected in the feces after a minimum pre-patent period of 16 days (Barriga, 1988, 1991).
Embryonated eggs present in environment may be ingested by a variety of accidental, paratenic hosts, such as rodents, sheep, pigs, cattle, birds, and humans. When such eggs from the soil or contaminated food are accidentally ingested by humans, L3 larvae hatch into small intestine, reach the lung and the heart and are carried to the systemic circulation.
3. Ancylostoma caninum and Ancylostoma braziliense
CLM is a relatively common clinical entity in humans caused by larval migration of zoonotic hookworms, mainly A. braziliense but also A. caninum and a few other species. Infective larvae penetrate the skin and migrate through the epidermis, but are usually confined to the dermis and do not develop into adult worms. Less common clinical manifestations are eosinophilic pneumonitis, localized myositis, folliculitis and erythema multiforme but eye involvement is rarely reported. Larval infection of humans with Anc. ceylanicum may occasionally give rise to adult worms that inhabit the small intestine and may cause abdominal discomfort and eosinophilic enteritis. The presence of immature Anc. caninum worms in the intestinal lumen of humans has rarely been reported (Bowman et al., 2010).
Infection of both definitive and paratenic hosts with these nematodes is most commonly acquired when third-stage hookworm larvae penetrate in their skin, although these infective larvae may also be ingested. In adult dogs infected with Anc. caninum, some larvae may undergo somatic migration and subsequently infect puppies by the transmammary route (Bowman et al., 2010; Soulsby, 1982). These larvae invade the skeletal muscle or gut wall and remain in an arrested state, becoming reactivated during the last two weeks of pregnancy (Barriga, 1988). Adult worms inhabit the small intestine of the definitive hosts (dogs for Anc. caninum, Anc. braziliense, Anc. ceylanicum and U. stenocephala; cats for Anc. tubaeforme, Anc. braziliense, Anc. ceylanicum and U. stenocephala) and may cause blood loss and anemia. Female worms shed eggs, typically two weeks after ingestion of larvae and about one month after skin penetration, which are passed in the host’s feces. Once in the soil, first-stage larvae hatch and develop into infective third-stage larvae (Figure 2).
4. Soil contamination with infective stages of zoonotic helminths
T. canis is transmitted to humans mainly by incidental ingestion of embryonated eggs present in the soil or soil-contaminated food (Acha & Szyfres, 2003). Since adult female worms produce large number of eggs and nearly all puppies are infected prior to birth, dog populations excrete a huge number of Toxocara eggs into the environment (Barriga, 1988).
Under favorable conditions (absence of direct sunlight exposure and appropriate temperature, humidity and oxygenation), particularly in tropical countries, Toxocara eggs can survive in the soil for several years. However, heavy environmental contamination has also been found in countries with temperate climate, such as Germany (Düwell, 1984) and Japan (Shimizu, 1993). Most (51-95%) eggs recovered from the soil of temperate countries were fully embryonated and, therefore, infective (Holland et al., 1991; Jarosz et al., 2010).
Humans can also be infected with Toxocara by ingestion of raw infected tissues of other paratenic hosts, such as cows, sheep or chicken, containing encapsulated larvae (Finsterer et al., 2010; Nagakura et al., 1989; Salem & Schantz, 1992). Food-borne transmission appears to be relatively common in East Asia (Akao & Ohta, 2007). Larval development progresses no further, but parasites can remain viable for up to seven years after infection (Smith et al., 2009). Although direct contact with infected puppies and kittens is not classically considered a risk factor for human toxocariasis, since the eggs shed by these animals must embryonate in the soil before becoming infective, these pet animals may carry embryonated eggs within their fur (Wolfe &Wright, 2003), in a small numbers (Overgaauw et al., 2009).
The species most commonly involved in human CLM is Anc. braziliense. Eggs shed within the feces of infected hosts hatch in the soil and develop into third-stage larvae in the environment. Human infection occurs through contact with contaminated soil of beaches, parks and schools (Bowman et al., 2010).
Eggs of Toxocara and zoonotic hookworm larva are found in soils worldwide, especially in public parks, playgrounds, sandpits, and beaches. Reports of soil contamination with infective stages of Toxocara and hookworm in public areas are available for several countries (Table 1).
Environmental and technical factors, such as soil type, pre-processing sieving, washing, and re-suspension of sediment, solution employed for washing and flotation, and the specific density of flotation solutions are all presumed to influence the recovery of ascarid eggs (Coelho et al., 2001; Nunes et al., 1994; Oge & Oge, 2000; Ruiz de Ybáñez et al., 2000; Santarém et al., 2009; Santarém et al., 2010).
Other variables, such as climatic conditions (temperature, rainfall, sunlight, etc.) or the amount of herbage and the presence of animals, number amongst other important factors contributing to soil contamination that may influence recovery of eggs.
The presence of dogs and cats may also play an important role on soil contamination by agents of larva migrans. Cassenote et al. (2011) observed that the number of dogs frequenting parks had an impact on soil contamination in public spaces.
The lack of standardisation of techniques as well as the wide range of factors influencing the process of egg recovery can lead to false-negative results and underestimation of the occurrence of contamination, hampering comparison of findings of different reports, and the assessment of their implications for public health (Coelho et al., 2001).
Fahrion et al. (2010) observed that the mean sizes of T. cati (62.3 by 72.7 µm) and T. canis (74.8 by 86.0 µm) eggs recovered from feces differed statistically. According to Fogt-Wyrwas et al. (2007), the differentiation of Toxocara spp. eggs from soil by ocular microscopy is extremely difficult due to the similarity in morphological characteristics of T. canis and T. cati eggs. As a consequence, studies have been carried out in an effort to provide molecular techniques for amplification of Toxocara spp. DNA that can be applied in routine examinations.
|Continent /Country||Site||Frequency (%)||Reference|
|Kaduna||9.0A||Maikai et al. (2008)|
|Connecticut||14.4T||Chorazy & Richardson (2005)|
|Argentina||Buenos Aires||13.2T||Fonrouge et al. (2000)|
|Cassenote et al. (2011)|
|Itabuna||47.9A||Campos Filho et al. (2008)|
|Mirante do Paranapanema||76.9T||Santarém et al. (2010)|
|Praia Grande||45.9A||Castro et al. (2005)|
|Ribeirão Preto||20.5T||Capuano & Rocha (2005)|
|São Paulo||29.7T||Muradian et al. (2005)|
|Sorocaba||53.3T||Coelho et al. (2001)|
|Chile||Santiago||66.7 T||Castillo et al. (2000)|
|Venezuela||Ciudad Bolívar||61.1A||Devera et al. (2008)|
|Thailand||Bangkok||5.71T||Wiwanitkit & Waenlor (2004)|
|Turkey||Ankara||45.0T||Avcioglu & Burgu (2008)|
|Italy||March||33.6T||Hábluetzel et al. (2003)|
Zhu et al. (2001) constructed specific primers for T. canis and T. cati DNA amplification by the PCR technique, by extracting genomic material from adult worms from dogs and cats. Previously, Jacobs et al. (1997) obtained genomic material from adult worms or from embryonated eggs collected from the uteri of female worm, and devised a polymerase chain reaction-linked to restriction fragment length polymorphism (PCR-linked RFLP) targeting the second internal transcribed spacer (ITS-2) of ribosomal DNA (rDNA) for Toxocara spp. and other zoonotic ascaridoid identification.
Subsequently, further studies based on Jacobs et al. (1997) have been undertaken to detect and differentiate Toxocara spp. in soil (Borecka, 2004; Fogt-Wyrwas et al., 2007; Borecka & Gawor, 2008) and in fecal samples (Fahrion et al., 2010).
Fogt-Wyrwas et al. (2007) developed a technique based on a step PCR method for identification of T. canis and T. cati in soil samples. First, the authors recovered eggs using a flotation technique. Genetic analyses were then carried out after the crushing the eggs by pressing a cover slip on a microscope slide, to produce the embryonic material. Successful results were obtained only when a single or large numbers of eggs were recovered from 40 g soil samples. Both T. canis and T. cati genetic material were amplified. Borecka & Gawor (2008) verified that the use of proteinase K enabled amplification of genomic DNA from the soil without the need to isolate eggs using flotation or to inactivate PCR inhibitors present in the sample, thus making PCR easier and less laborious for routine use.
Another method developed to amplify DNA is the loop-mediated isothermal amplification (LAMP) assay. Based on a previous review, Parida et al. (2008) stated that LAMP is characterized by the use of six different primers. Amplification and detection of a gene can be completed in a single step, by incubating the mixture of samples, primers, DNA polymerase with strand displacement activity and substrates, at a constant temperature. The result is based on naked eye observations of a white precipitate (magnesium pyrophosphate). Thus, the method does not require expensive equipments, such as thermal cyclers or reagents.
5. Global prevalence of soil-transmitted zoonotic helminth infections in humans and associated risk factors
Human Toxocara infection has a cosmopolitan distribution, but reliable prevalence estimates are hard to derive from available serosurvey data, which comprises demographically diverse population samples that may not be representative of the general population of their respective countries, provinces or cities (Table 2).
|Site(s)||No. of samples||Positive|
|90 districts||387C||92.8||Magnaval et al. (1994)|
|Various areas||20,395AC||13.9||Won et al. (2008)|
|Argentina||La Plata||156AC||46.9||Radman et al. (2000)|
|Resistencia||206C||37.9||Alonso et al. (2000)|
|Brazil||Assis Brasil and Acrelândia||606C||21.5||Ferreira et al. (2007)|
|São Paulo city||399C||38.8||Alderete et al. (2003)|
|Campinas||138AC||27.7||Anaruma et al. (2002)|
|Granada||403AC||26.8||Rubinsky-Elefant et al. (2008)|
|Pres. Prudente||252C||11.1||Santarém et al. (2011)|
et al. (2008)
|São Paulo city||338C||26.9||Muradian et al. (2005)|
|Sorocaba||180C||38.3||Coelho et al. (2004)|
|Peru||Lima||303AC||20.5||Espinoza et al. (2010)|
|Sari City||1,210C||25.0||Sharif et al. (2010)|
|Taiwan||Districts in East||329C||76.6||Fan et al. (2004a)|
|Santiago de Compostela||463A||28.6||Gonzalez-Quintela et al. (2006)|
Toxocariasis tends to be more prevalent in tropical settings, compared to temperate regions, while rural populations are usually more exposed than urban populations in the same region (Rubinsky-Elefant et al., 2010). Reported seroprevalence rates in apparently healthy subjects range from 2.4% in Denmark (3247 subjects ≤ 40 years old; Stensvold et al., 2009) to 92.8% in La Réunion (387 subjects> 15 years old; Magnaval et al., 1994).
Although some risk factors for toxocariasis have been identified in human populations, results remain largely inconsistent. Male gender, for example, was suggested to be associated with both higher (Alonso et al., 2000; Kanafani et al., 2006; Roldán et al., 2009; Won et al., 2008) and lower (Abo-Shehada et al., 1992; Magnaval & Baixench, 1993) risk of infection, whereas several large studies showed no association between gender and risk (Chieffi et al., 1990; Rubinsky-Elefant et al., 2008. Young age (Fan et al., 2004b; Rubinsky-Elefant et al., 2008), low socioeconomic status (Campos Junior et al., 2003; Lynch et al., 1988a; Santarém et al., 2011; Won et al., 2008), low parental education (González-Quintella et al., 2006; Won et al., 2008), poor sanitation (Alderete et al., 2003; Magnaval et al., 1994) and playing in sandpits (Paludo et al., 2007) are additional factors contributing to Toxocara exposure.
Having a dog has been recognized as a risk factor in most (Chiodo et al., 2006; Fan et al., 2004b; González-Quintella et al., 2006; Jarosz et al., 2010; Won et al., 2008), but not all studies of human toxocariasis (Ajayi et al., 2000; Rubinsky-Elefant et al., 2008). Discrepancies are not altogether surprising, especially in tropical settings where dogs roam freely and spread eggs across large areas. As a result, infection may be acquired, especially in sandpits of children′s playgrounds, regardless of the presence of pet dogs in the households. The contribution of cat ownership to Toxocara seropositivity has been less studied. Having cats as pets has been described, in two recent serosurveys in Brazil, as representing both a risk (Paludo et al., 2007) and a protective factor (Rubinsky-Elefant et al., 2008). A third survey in Poland (Jarosz et al., 2010), but not a large nationwide study in the United States (Won et al., 2008) found cat ownership to be a significant predictor of Toxocara seropositivity.
The antigen used in ELISA (Enzyme-linked immunosorbent assay) contains both species-specific epitopes and epitopes that are shared between T. canis and T. cati (Kennedy et al., 1987). If species-specific epitopes predominate, serology would preferentially diagnose exposure to T. canis. Nevertheless, if cross-reactive epitopes predominate and exposure to T. cati is frequent, ELISA would be unable to distinguish between exposure to T. canis and T. cati with both dog and cat ownership emerging as a risk factor for seropositivity.
Positive associations have been described between Toxocara seropositivity and current infection with other nematodes, such as whipworm (Cancrini et al., 1998) and hookworm (Rubinsky-Elefant et al., 2008). These results may reflect some degree of cross-reactivity of antibodies to TES with proteins excreted by other tissue- or lumen-dwelling nematodes. Although test sera in most laboratories are pre-incubated with an Ascaris suum extract to prevent cross-reactivity with this common human nematode (Elefant et al., 2006), other highly prevalent helminths may still elicit cross-reactive antibodies (Lynch et al., 1988b). Alternatively, Toxocara and other soil-transmitted helminths may co-infect the same host due to the similar ways of acquiring these infections.
Prevalence and geographic distribution of infections with zoonotic hookworms in humans and their definitive hosts remain relatively unknown (Bowman et al., 2010). As a rule, human CLM is more prevalent in children living in regions with warm and humid climates. U. stenocephala infects dogs and cats in the Americas, Europe, Asia and Oceania, while Anc. ceylanicum is commonly found in South and Southeast Asia, Australia, and most parts of South America. Anc. braziliense can be found from the southeastern coast of North America (but not on the Pacific Coast of United States and Mexico) down to South America, in African countries and Southeast Asia, but less frequently in Australia.
Human CLM, known or presumed to be caused by Anc. braziliense, has been reported in many tropical and subtropical regions, including North and South America, Southern Europe, India, and the Philippines. The distribution of human infection overlaps with the geographic range of Anc. caninum. CLM is the most common dermatologic condition that affects North American and European tourists returning from tropical countries. These imported cases are often reported after exposure to beaches in regions where Anc. caninum is commonly found in their definitive hosts.
6. Laboratory diagnosis, clinical spectrum and treatment of human toxocariasis
Because larvae do not develop into adult worms in humans, these paratenic hosts do not pass Toxocara eggs in their feces. As a consequence, fecal examination does not contribute to the laboratory diagnosis of human toxocariasis. Definitive diagnosis of current infection can only be obtained by histological examination of infected tissue, but biopsies are rarely obtained for diagnostic purposes. Less commonly, ultrasonography, computed tomography, and nuclear resonance imaging are also used to detect and localize lesions suggestive of granulomas (Magnaval et al., 2001; Watthanakulpanich, 2010).
Virtually all Toxocara infections in humans are diagnosed serologically. The standard test to diagnose human toxocariasis is the indirect ELISA with antigens excreted-secreted by T. canis (TES) L3 larvae (de Savigny, 1975, 1979). The TES-based ELISA for IgG antibodies has been reported to be 78% sensitive and 92% specific (Glickman et al., 1986), although putatively more specific recombinant antigens have been obtained for serology. Since cross-reactive antibodies elicited by exposure to other helminths may reduce the specificity of TES-based serology in tropical populations (Lynch et al., 1988b; Watthanakulpanich et al., 2008), serum samples are usually pre-incubated with antigens of related nematodes, to remove cross-reacting antibodies. Our test samples are routinely pre-incubated with an adult worm extract of A. suum (Elefant et al., 2006).
Positive ELISA results can be confirmed by Western blot (Magnaval et al., 1991), but this technique is more expensive and labour-intensive than ELISA. Recombinant T. canis antigens, which are species-specific, have been expressed and used in prototype ELISAs for detection of antibodies, with promising results (Yamasaki et al., 2000). Among the four human IgG subclasses, specific IgG2 antibodies to TES antigens yield the highest sensitivity in ELISA (Watthanakulpanich et al., 2008), while detection of IgG4 antibodies contributes to increased specificity (Noordin et al., 2005).
Immunoblotting (IB) techniques, based on TES antigens, have been applied to improve serodiagnosis, and for follow-ups after chemotherapy (Rubinsky-Elefant et al., 2011).
Antigen-capture ELISAs with monoclonal antibodies have been developed (Gillespie et al., 1993; Robertson et al., 1988) but poor specificity precludes their use in routine diagnosis. Polymerase chain reaction (PCR)-based methods for Toxocara identification in clinical and environmental samples have been described (Fogt-Wyrwas et al., 2007; Zhu et al., 2001), but are not widely available.
The clinical spectrum of toxocariasis in humans, ranging from asymptomatic infection to severe organ injury, is determined by parasite load, sites of larval migration, and the host′s inflammatory response. Two severe clinical syndromes are classically recognized: VLM (systemic disease caused by larval migration through major organs) and OLM (disease limited to the eye and optic nerve). Half a century ago, Beaver and colleagues described Toxocara larvae in eosinophilic granulomas in the liver of young children with extreme eosinophilia, hepatomegaly, respiratory symptoms, anemia and geophagia, and introduced the term VLM to describe this clinical syndrome (Beaver et al., 1952). Wilder found nematode larvae in eosinophilic granulomas of enucleated eyes of children with suspected retinoblastoma, providing the first description of the condition currently known as OLM (Wilder, 1950).
Classical VLM occurs typically in children aged 2-7 years, but infections in adults, at least some of which are acquired by ingesting raw organs of paratenic hosts, are relatively frequent in East Asia (Akao & Ohta, 2007). The full-blown VLM syndrome usually includes fever, lower respiratory symptoms such as cough, dyspnea and bronchospasm associated with larval migration, hepatomegaly, abdominal pain and decreased appetite. Laboratory findings include hypergammaglobulinemia, increased isohemagglutinin titres to A and B blood group antigens, anaemia and leukocytosis with marked eosinophilia (Jacob et al., 1994). As a rule, seropositive subjects in population-based surveys are asymptomatic or have rather nonspecific and mild symptoms. A case-control study in Ireland led to the description of a new clinical entity in seropositive children, called “covert toxocariasis”, comprising mainly fever, headache, behavioural and sleep disturbances, cough, anorexia, abdominal pain, hepatomegaly, nausea and vomiting (Taylor et al., 1987). Another case-control study, in French adults, led to the definition of “common toxocariasis”, a syndrome comprising chronic dyspnea and weakness, cutaneous rash and pruritus, as well as abdominal pain (Glickman et al., 1987).
The liver is the most commonly affected visceral organ. Typical hepatic granulomas have multinucleated giant cells and epithelioid cells surrounding necrotic debris or amorphous eosinophilic material. Eosinophils and mononuclear cells are often seen in the outer layers of the granulomas (Musso et al., 2007). On computed tomography, hepatic lesions are typically ill-defined, low-attenuating nodules (Cameron et al., 1997) that have sometimes been confounded with metastatic cancer (Ota et al., 2009).
The cutaneous manifestations of human toxocariasis have been recently reviewed (Gavignet et al., 2008) and include chronic prurigo, pruritus and urticaria, eczema, exanthema (Bernardeschi et al., 2011), and vasculitis.
Central nervous system involvement in toxocariasis comprises eosinophilic meningitis and encephalitis (Moreira-Silva et al., 2004), myelitis (Lee et al., 2009), cerebral vasculitis (Helbok et al., 2007) and optic neuritis, while manifestations of peripheral nervous system involvement include radiculitis (Moreira-Silva et al., 2004) and cranial nerve palsy (Finsterer & Auer, 2007). Central nervous system involvement in VLM has been associated with epilepsy (Woodruff et al., 1966), behavioral changes and cognitive deficits. Toxocara may represent a co-factor in idiopathic seizures (Critchley et al., 1982), and especially in partial epilepsy (Nicoletti et al., 2007). The presence of granulomas in the brain has been suggested to elicit focal seizures (Critchley et al., 1982). Research to verify increased risk of cognitive deficits in infected children has remained inconclusive (Jarosz et al., 2010).
There are very few controlled trials on anthelmintic drugs for VLM in the literature. Since parasitological cure in patients cannot be assessed, the end-point of published trials is a decrease in the severity of clinical signs and symptoms. A dose of 500 mg of albendazole twice a day for 5 days is currently recommended. Albendazole seems to be superior to thiabendazole (50 mg/kg of body weight daily for 3-7 days) (Stürchler et al., 1989). Diethylcarbamazine (3-4 mg/kg of body weight daily for 21 days, starting at 25 mg/day and increasing the dose progressively) is also effective (Magnaval, 1995). Most human infections with Toxocara, however, cause much less severe systemic manifestations, if any, and treatment is not required.
Eosinophilia and elevated levels of IgE are commonly found in toxocariasis, as well as high titres of Toxocara antibodies. Covert and common toxocariasis are likely to represent slight variations in the clinical spectrum of mild infections in children and adults, respectively.
Although wheezing is a common presenting feature of VLM, whether or not Toxocara infection predisposes to asthma remains uncertain. Some epidemiological studies have shown a positive association between wheezing or asthma and Toxocara seropositivity (Desowitz et al., 1981; Ferreira et al., 2007; González-Quintella et al., 2006), while others failed to detect such an effect (Fernando et al., 2009; Sharghi et al., 2001). Asthma symptoms can result from larval migration through the lungs, but a role has also been proposed for parasite-induced atopy (Cooper, 2009).
Compared with systemic disease, ocular toxocariasis or OLM usually affects older children, with an average age at onset of 7.5 years (range, 2-50 years) (Taylor, 2001). About 80% of cases are diagnosed in patients younger than 16 years of age (Brown, 1970). Males tend to be more frequently affected than females (Brown, 1970; Taylor, 2001). The clinical condition currently known as OLM or ocular toxocariasis was first described by Wilder (1950), who found nematode larvae or their residual hyaline capsules during the histological analysis of 24 eyes that had been enucleated from children with suspected retinoblastoma.
The clinical presentation of OLM depends on the primary anatomic site involved and the immune response of the host. A single eye is affected in most patients (Taylor, 2001). The most common symptoms are strabismus, unilateral decreased vision and leukocoria (white eye). Peripheral, posterior pole retinal granuloma and endophthalmitis are the usual presentations on the eye exam.
The presence of a vitreous band, or a membrane extending between the posterior pole and high-reflective peripheral mass, detected by ocular ultrasound, may help in the diagnosis when the ocular medium is opaque (Figure 3).
Other uncommon clinical presentations of OLM include optic disc inflammation (papillitis or neuroretinitis), motile intraocular nematode (retina, vitreous body and anterior chamber), keratitis and cataract.
The diagnosis of OLM is usually suggested by the presence of the clinical findings mentioned above, but the detection of specific antibodies is required. However, serum antibodies can often be undetectable (Sharkey & McKay, 1993), possibly due to the relatively low parasite load in these infections (Schantz, 1989). Even low ELISA serum titres may be of diagnostic value in OLM, but there is no consensus on the cut-off titres for diagnosis. Specific antibodies can be also detected in the aqueous humor (AH). The intraocular production of antibodies to Toxocara can be assessed by comparing serum and AH samples obtained simultaneously from the same patients and calculating the Goldmann-Witmer (GW) coefficient as: ([levels of specific IgG in AH/levels of specific IgG in serum]/[total IgG in AH/total IgG in serum]). A GW coefficient > 3 indicates intraocular production of specific antibodies (De Visser et al., 2008).
Sight-threatening ocular inflammation secondary to OLM requires aggressive anti-inflammatory therapy, combined with albendazole (800 mg for adults and 400 mg for children daily) over a 2-4 week period. Oral steroids (prednisone 0.5 mg/kg/day) are used to reduce the inflammatory response induced by larvae. Surgical treatment may be required for retinal detachment or intravitreal fibrovascular membrane proliferation.
7. Cutaneous larva migrans
CLM is a clinical entity caused in humans by larval migration of zoonotic hookworms, mainly Anc. braziliense but also Anc. caninum. Less common clinical manifestations are eosinophilic pneumonitis, localized myositis, folliculitis and erythema multiforme but eye involvement is rarely reported. Human infection occurs when infective L3 larvae penetrate the skin. The infection site may or may not present an erythematous popular or vesicular rash.
The larvae do not undergo further molts in the human host, but as they migrate across in the skin, at a rate of 2.7 mm per day, they leave an erythematous, serpiginous track. The cutaneous lesions can last several weeks and may be severely pruritic, but eventually resolved spontaneously. Secondary bacterial infection may result from scratching.
The most commonly affected sites are those in close contact with the soil (Araújo et al., 2000). A recent case series of CLM in Brazil, for example, showed that cutaneous lesions are more frequently observed on the feet (73.3%), buttocks (14.7%), genital and inguinal areas (8.0%), legs (2.7%), and hands (1.3%) (Jackson et al., 2006). Other sites, such as the face (Bouchad et al., 2000) and the scalp (Guimarães et al., 1999), are rarely affected. Clinical diagnosis is reached based on the typical skin lesions, while biopsies have little diagnostic value, showing an eosinophilic inflammatory infiltrate. Chemotherapy is seldom needed, since larvae die out within a matter of weeks if left untreated, but oral albendazol (400-800 mg/day for 3-5 days), oral ivermectin (200 μg/kg, single dose) or topical thiabendazole (10% aqueous suspension four times a day) may be used.
Larval infection of humans with Anc. ceylanicum may occasionally give rise to adult worms that inhabit the small intestine and can cause eosinophilic enteritis (Bowman et al., 2010). In addition to cutaneous lesions, Anc. caninum has also been reported to cause eosinophilic enteritis and may be a cause of diffuse unilateral subacute neuroretinitis in humans (Sabrosa & de Souza, 2001).
8. Prevention and control of zoonotic soil-transmitted helminth infections in humans and companion animals
Contaminated soil is the most important route of transmission of zoonotic helminths to humans. Environmental contamination is particularly relevant when public areas (parks, playgrounds, beaches) are affected. Effective preventive measures include covering sandboxes in public parks and playgrounds when not in use, allowing no dogs and cats on bathing beaches, and controlling stray dog and cat populations.
In southeastern Brazil, Santarém et al. (2004) reported a significant decrease in the incidence of LMC after replacement of soil in sandboxes and enclosure of playground areas with fences. Also in southern Brazil, Cassenote et al. (2011) observed that the frequency of geo-helminthes in fenced parks (11.1%) was significantly lower than that verified in non-fenced off areas (45.3). Similarly, Avcioglu & Balkaya (2011) observed in Turkey that fenced parks were free of Toxocara eggs, while 64.3% of open areas were contaminated with eggs.
Periodic prophylactic deworming of companion animals and educational measures aimed at pet owners are also critical for controlling infections by soil-transmitted helminths (Stull et al., 2007). A strategic program for decreasing soil contamination with zoonotic helminths should include elimination of intestinal parasites from puppies and kittens. Since puppies and kittens harbor adult Toxocara and hookworm due to infections via placenta and/or milk, treatment must target newborn animals, before eggs are first shed in the feces.
The WHO (2011), based on considerations by Barriga (1988, 1991), currently recommends treatment for puppies at two weeks of age to eliminate larvae acquired through transmammary or transplacentary transmission. Treatment is repeated at 4, 6 and 8 weeks. For kittens, treatment must be done at third, fifth, seventh and ninth weeks of life to eliminate the larva passed through milk. A single dose of anthelmintic for queens, 10 days after delivery, is also recommended (Barriga, 1991). Laboratory confirmation of infection, with stool examination using concentration methods (most often based on flotation procedures), is normally required prior to treatment of animals older than six months of age, to prevent uncontrolled use of anthelminthic drugs and the emergence of resistant parasites.
Veterinarians are thought to be on the ‘front line’ of prevention of pet-associated zoonotic parasitic infections (Smith et al., 2009). However, recent surveys have revealed that veterinarians often misinterpret and misuse the available protocols for deworming newborn pets. In Canada, 80-90% of the protocols recommended for puppies and kittens were inappropriate (Stull et al., 2007), and in the USA only 16% of the veterinarians interviewed knew how to deworm puppies (Harvey et al., 1991). In addition, veterinarians’ perception concerning small animal-derived zoonoses should be improved, with emphasis on their role in disseminating information about these diseases to their clients (Stull et al., 2007).
Human infections with canine and feline helminths ranks among the most common zoonotic infections worldwide, yet remain relatively unknown to the public and pet owners. Katagiri & Oliveira-Siqueira (2008), in São Paulo, Brazil, observed a low level of risk perception of zoonotic infection by dog owners in Brazil. Pet owners should know how to prevent environmental contamination and to reduce the risk of human infection with zoonotic helminths. This requires a clear understanding of zoonoses acquired from small animals, of the need for appropriate deworming strategies for pets, and the need for removing feces from the environment where their dogs evacuate.
The public must also be informed about the risks of exposing children to public parks and beaches frequented by animals and of eating soil or biting nails, as well as about the benefits of washing hands after handling fecal material or playing with pets.
The American Veterinary Medical Association (AVMA, 2008) considers that the convergence of people, animals, and our environment has created a new dynamic in which the health of each group is inextricably interconnected. The Association proposed a holistic, collaborative approach aimed at improving animal and human health globally through collaboration among all the health sciences, especially between the veterinary and human medical professions to address critical needs.
Based on the findings in this review, it can be asserted that the lack of standardisation of techniques coupled with the host of factors influencing the process of egg/larvae recovery can lead to false-negative results and underestimation of the occurrence of soil contamination. Thus, the development of new methods is necessary to provide more reliable data under field conditions. Molecular analyses, based on amplification of genetic material extracted from eggs/larvae present in soil, are promising techniques both for identifying and characterizing of helminths present in soil.
It was also observed that soil contamination in public areas can be reduced by adopting a number of measures including: restriction of uncontrolled dogs and cats, cleaning up dog feces from soil and pavements by their owners, preventing access of dogs and cats to public spaces (especially children's playgrounds) and by use of strategic anthelmintic treatment of dogs and cats with emphasis on puppies, kittens, nursing bitches and queens.
Programs designed through collaborative efforts of both human and veterinary doctors/researchers are essential to create fresh tools for diagnosis and new strategies for controlling the transmission of soil-transmitted helminthic zoonoses to humans, until new technologies become available.
According to the WHO (2011), one of the main strategies for controlling zoonotic diseases is to promote advocacy so as to emphasize their burden on society and create demand at all levels of society to control them. The American Veterinary Medical Association (AVMA, 2008) has considered that the convergence of people, animals, and our environment has created a new dynamic in which the health of each group is inextricably interconnected. The Association has proposed a holistic, collaborative approach aimed at improving animal and human health globally through collaboration among all the health sciences, particularly between the veterinary and human medical professions to address critical needs.
Many diseases are considered neglected zoonotic diseases, including soil-transmitted helminths. Thus, efforts to design public educational programs raising awareness of agents of larva migrans are fundamental to prevent the burden of diseases in companion animals and humans. Further, improvements in diagnostic testing and expansion of epidemiologic surveillance should be promoted in parallel with control and prevention efforts.
Abo-Shehada M. N. Sharif L. el -Sukhon S. N. Abuharfeil N. Atmeh R. F. 1992Seroprevalence of
Acha P. Szyfres B. 2003Parasitosis: Larva migrans cutanea. Larva migrans visceral and toxocaryasis. In: Zoonosis y enfermedades transmissibles al hombre y a los animales. 3. ed., 3 9-27531-993-6
Ajayi O. O. Duhlinka D. D. Agwale S. M. Njoku M. 2000Frequency of human toxocariasis in Jos, Plateau state, Nigeria.
Akao N. Ohta N. 2007Toxocariasis in Japan.
Alderete J. M. S. Jacob C. M. A. Pastorino A. C. Elefant G. R. Castro A. P. M. Fomin A. B. F. Chieffi P. P. 2003Prevalence of
Alonso J. M. Bojanich M. V. Chamorro M. Gorodner J. O. 2000
American Veterinary Medical Association (AVMA). 2008One Health initiative task force: final report. 71 pp. July 2008, Available from: http://www.avma.org/onehealth/onehealth_final.pdf
Anaruma Filho. F. Chieffi P. P. Correa C. R. Camargo E. D. Silveira E. P. Aranha J. J. Ribeiro M. C. 2002Human toxocariasis: a seroepidemiological survey in the municipality of Campinas (SP), Brazil.
Araújo F. R. Araújo C. P. Werneck M. R. Górski A. 2000Larva migrans cutânea em crianças de uma escola em área do Centro-Oeste do Brasil.
Avcioglu H. Balkaya I. 2011The relationship of public park accessibility to dogs to the presence of
Avcioglu H. Burgu A. 2008Seasonal prevalence of
Aydenizöz-Özkayhan M. 2006Soil contamination with ascarid eggs in playgrounds in Kirikkale, Turkey.
Barriga O. O. 1988A critical look at the importance, prevalence and control of toxocariasis and the possibilities of immunological control
Barriga O. O. 1991Rational control of canine toxocariasis by the veterinary practitioner.
Beaver P. C. Snyder C. H. Carrera G. M. Dent J. H. Lafferty J. W. 1952Chronic eosinophilia due to visceral larva migrans: report of three cases.
Bernardeschi C. Monsel G. Francés C. Bricaire F. Paris L. Caumes E. 2011Febrile exanthema revealing toxocariasis: A case report.
Bethony J. Brooker S. Albonico M. Geiger S. M. Loukas A. Diemert D. Hotez P. J. 2006Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm.
Borecka A. 2004Differentiation of
Borecka A. Gawor J. 2008Modification of gDNA extraction from soil for PCR designed for the routine examination of soil samples contaminated with
Bouchaud O. Houzé S. Schiemann R. Durand R. Ralaimazava P. Ruggeri C. Coulaud J. P. 2000Cutaneous larva migrans in travelers: a prospective study with assessment of therapy with ivermectin.
Bowman D. D. Montgomery S. P. Zajac A. M. Eberhard M. L. Kazacos K. R. 2010Hookworms of dogs and cats as agents of cutaneous larva migrans.
Brooker S. Clements A. C. A. Bundy D. A. P. 2006Global epidemiology, ecology and control of soil-transmitted helminth infections.
Brown D. H. 1970Ocular
Cameron F. J. Sohaib S. A. Scheimberg I. Dicks-Mireaux C. 1997The significance of hepatic lesions associated with small adrenocortical tumours in childhood.
Campos Filho. P. C. Barros L. M. Campos J. O. Braga V. B. Cazorla I. M. Albuquerque G. R. Carvalho S. M. 2008Zoonotic parasites in dog feces at public squares in the municipality of Itabuna, Bahia, Brazil.
Pratesi, R. ( Campos Junior. D. Elefant G. R. de Melo e. Silva E. O. Gandolfi L. Jacob C. M. Tofeti 2003Frequency of seropositivity to
Cancrini G. Bartoloni A. Zaffaroni E. Guglielmetti P. Gamboa H. Nicoletti A. Genchi C. 1998Seroprevalence of
Capuano D. M. Rocha G. M. 2005Environmental contamination by
Cassenote A. J. F. Pinto Neto. J. M. Lima-Catelani A. R. A. Ferreira A. W. 2011Contaminação do solo por ovos de geo-helmintos com potencial zoonótico na municipalidade de Fernandópolis, Estado de São Paulo, entre 2007 e 2008.
Castillo D. Paredes C. Zañartu C. Castillo G. Mercado R. Muñoz V. Schenone H. 2000Environmental contamination with
Castro J. M. Santos S. V. Monteiro N. A. 2005Contaminação de canteiros da orla marítima do Município de Praia Grande, São Paulo, por ovos de
CDC- Centers for Disease Control and Prevention. 2011Parasites and Health: Hookworm. Available from: http://www.dpd.cdc.gov/dpdx/html/hookworm.htm
Chieffi P. P. Ueda M. Camargo E. D. de Souza A. M. Guedes M. L. Gerbi L. J. Spir M. Moreira A. S. 1990Visceral larva migrans: a seroepidemiological survey in five municipalities of São Paulo state, Brazil
Chiodo P. Basualdo J. Ciarmela L. Pezzani B. Apezteguía M. Minvielle M. 2006Related factors to human toxocariasis in a rural community of Argentina.
Chorazy M. L. Richardson D. J. 2005A survey of environmental contamination with ascarid ova, Wallingford, Connecticut.
Coelho L. M. P. S. Dini C. Y. Milman M. H. S. A. Oliveira S. M. 2001
Coelho L. M. Silva M. V. Dini C. Y. Giacon Neto. A. A. Novo N. F. Silveira E. P. 2004Human toxocariasis: a seroepidemiological survey in schoolchildren of Sorocaba, Brazil.
Cooper P. J. 2009Interactions between helminth parasites and allergy.
Critchley E. M. Vakil S. D. Hutchinson D. N. Taylor P. 1982
De Savigny, D.H 1975In vitro maintenance of
De Savigny D. H. Voller A. Woodruff A. W. 1979Toxocariasis: serological diagnosis by enzyme immunoassay.
De Visser L. Rothova A. de Boer J. H. van Loon A. M. Kerkhoff F. T. Canninga-van Dijk. M. R. Weersink A. Y. de Groot-Mijnes J. D. 2008Diagnosis of ocular toxocariasis by establishing intraocular antibody production.
Desowitz R. S. Rudoy R. Barnwell J. W. 1981Antibodies to canine helminth parasites in asthmatic and nonasthmatic children.
Despommier D. 2003Toxocariasis: Clinical aspects, epidemiology, medical ecology, and molecular aspects.
Devera R. Blanco Y. Hernández H. Simoes D. 2008
Düwell D. 1984The prevalence of
Elefant G. R. Shimizu S. H. Sanchez M. C. A. Jacob C. M. A. Ferreira A. W. 2006A serological follow-up of toxocariasis patients after chemotherapy based on the detection of IgG, IgA and IgE antibodies by enzyme-linked immunosorbent assay.
Espinoza Y. A. Hua Paya. P. E. Roldán W. H. Jiménez S. Abanto E. P. Rojas C. A. Cavero Y. A. Gutiérrez C. A. 2010Seroprevalence of human Toxocariasis in Andean communities from the northeast of Lima, Peru.
Fahrion A. S. Schnyder M. Wichert B. Deplazes P. 2010
Fan C. K. Hung C. C. Du W. Y. Liao C. W. Su K. E. 2004aSeroepidemiology of
Fan C. K. Lan H. S. Hung C. C. Chung W. C. Liao C. W. Du W. Y. Su K. E. 2004bSeroepidemiology of
Fernando D. Wickramasinghe P. Kapilananda G. Dewasurendra R. L. Amarasooriya M. Dayaratne A. 2009
Ferreira M. U. Rubinsky-Elefant G. Castro T. G. Hoffmann E. H. E. da-Nunes Silva. M. Cardoso M. A. Muniz P. T. 2007Bottle feeding and exposure to
Finsterer J. Auer H. 2007Neurotoxocarosis.
Finsterer J. Kallab V. Auer H. 2010Neurotoxocariasis associated with lower motor neuron disease. Report of one case.
Fisher M. 2003
Fogt-Wyrwas R. Jarosz W. Mizgajska-Wiktor H. 2007Utilizing a polymerase chain reaction method for the detection of
Fonrouge R. Guadis M. V. O. L. Radman N. E. Archelli S. M. 2000Contaminacion de suelos com huevos de
Gavignet B. Piarroux R. Aubin F. Millon L. Humbert P. 2008Cutaneous manifestations of human toxocariasis.
Gillespie S. H. Bidwell D. Voller A. Robertson B. D. Maizels R. M. 1993Diagnosis of human toxocariasis by antigen capture enzyme linked immunosorbent assay.
Glickman L. T. Schantz P. M. Grieve R. B. 1986Toxocariasis. In:
Glickman L. T. Magnaval J. F. Domanski L. M. Shofer F. S. Lauria S. S. Gottstein B. Brochier B. 1987Visceral larva migrans in French adults: a new disease syndrome?
González-Quintella A. Gude F. Campos J. Garea M. T. Romero P. A. Rey J. Meijide L. M. Fernández-Merino M. C. Vidal C. 2006
Guimarães L. C. Silva J. H. Saad K. Lopes E. R. Meneses A. C. O. 1999Larva migrans within scalp sebaceous gland.
Hábluetzel A. Traldi G. Ruggieri S. Attili A. R. Scuppa P. Marchetti R. Menghini G. Esposito F. 2003An estimation of
Harvey J. B. Roberts J. M. Schantz P. M. 1991Survey of veterinarians’ recommendations for treatment and control of intestinal parasites in dogs: public health implications.
Helbok R. Brenneis C. Engelhardt K. Beer R. Lackner P. Brössner G. Pfausler B. Schmutzhard E. 2007A rare case of
Holland C. V. O’Connor P. Taylor M. Hughes G. Girdwood R. Smith H. 1991Families, parks, gardens, and toxocariasis.
Jackson A. Heukelbach J. Calheiros C. M. Soares V. de L. Harms G. Feldmeier H. 2006A study in a community in Brazil in which cutaneous larva migrans is endemic.
Jacob C. M. Pastorino A. C. Peres B. A. Mello E. O. Okay Y. Oselka G. W. 1994Clinical and laboratorial features of visceral toxocariasis in infancy.
Jacobs D. E. Zhu X. Gasser R. B. Chilton N. B. 1997PCR-based methods for identification of potentially zoonotic ascaridoid parasites of the dog, fox and cat.
Jarosz W. Mizgajska-Wiktor H. Kirwan P. Konarski J. Rychlicki W. Wawrzyniak G. 2010Developmental age, physical fitness and
Kanafani Z. A. Skoury A. Araj G. F. El -Khoury M. Sawaya R. A. Atweh S. F. Kanj S. S. 2006Seroprevalence of toxocariasis in Lebanon: a pilot study.
Katagiri S. Oliveira-Siqueira T. C. 2008Prevalence of dog intestinal parasites and risk perception of zoonotic infection by dog owners in São Paulo State, Brazil.
Kennedy M. W. Maizels R. M. Meghji M. Young L. Qureshi F. Smith H. V. 1987Species-specific and common epitopes on the secreted and surface antigens of
Lee J. Y. Kim B. J. Lee S. P. Jeung Y. J. Oh M. J. Park M. S. Paeng J. W. Lee B. J. Choi D. C. 2009Toxocariasis might be an important cause of atopic myelitis in Korea.
Lynch N. R. Eddy K. Hodgen A. N. Lopez R. I. Turner K. J. 1988aSeroprevalence of
Lynch N. R. Wilkes L. K. Hodgen A. N. Turner K. J. 1988bSpecificity of
Magnaval J. F. 1995Comparative efficacy of diethylcarbamazine and mebendazole for the treatment of human toxocariasis.
Magnaval J. F. Baixench M. 1993Toxocariasis in the Midi Pyrenées region. In:
Magnaval J. F. Fabre R. Maurières P. Charlet J. P. De Larrard B. 1991Application of the Western blotting procedure for the immunodiagnosis of human toxocariasis.
Magnaval J. F. Glickman L. T. Dorchies P. Morassin B. 2001Highlights of human toxocariasis.
Magnaval J. F. Michault A. Calon N. Charlet J. P. 1994Epidemiology of human toxocariasis in La Réunion.
Maikai B. V. Umoh J. U. Ajanusi O. J. Ajogi I. 2008Public health implications of soil contaminated with helminth eggs in the metropolis of Kaduna, Nigeria.
Moreira-Silva S. F. Rodrigues M. G. Pimenta J. L. Gomes C. P. Freire L. H. Pereira F. E. L. 2004Toxocariasis of the central nervous system: with report of two cases.
Muradian V. Gennari S. M. Glickman L. T. Pinheiro S. R. 2005Epidemiological aspects of visceral larva migrans in children living at São Remo community, São Paulo (SP), Brazil.
Musso C. Castelo J. S. Tsanaclis A. M. Pereira F. E. 2007Prevalence of
Nagakura K. Tachibana H. Kaneda Y. Kato Y. 1989Toxocariasis possibly caused by ingestiong raw chicken.
Nicoletti A. Bartoloni A. Sofia V. Mantella A. Nsengiyumva G. Frescaline G. Preux P. M. 2007Epilepsy and toxocariasis: a case control study in Burundi.
Noordin R. Smith H. V. Mohamad S. Maizels R. M. Fong M. Y. 2005Comparison of IgG-ELISA and IgG4-ELISA for
Nunes C. M. Sinhoroni I. L. Agassawara S. 1994Influence of soil texture in the recovery of
Oge H. Oge S. 2000Quantitative comparison of various methods for detecting eggs of
O´ Lorcain. P. 1994Prevalence of
Ota K. V. Dimaras H. Héon E. Babyn P. S. Yau Y. C. W. Read S. Budning A. Gallie B. L. Chan H. S. L. 2009Toxocariasis mimicking liver, lung, and spinal cord metastases from retinoblastoma.
Overgaauw P. A. M. 1997Aspects of
Overgaauw P. A. van Zutphen L. Hoek D. Yaya F. O. Roelfsema J. Pinelli E. van Knapen F. Kortbeek L. M. 2009Zoonotic parasites in fecal samples and fur from dogs and cats in The Netherlands.
Paludo M. L. Falavigna D. L. Elefant G. R. Gomes M. L. Baggio M. L. Amadei L. B. Falavigna-Guilherme A. L. 2007Frequency of
Parida M. Sannarangaiah S. Dash P. K. Rao P. V. L. Morita K. 2008Loop mediated isothermal amplification (LAMP): a new generation of innovative gene amplification technique; perspectives in clinical diagnosis of infectious diseases.
Prestes-Carneiro L. E. Santarém V. A. Zago S. C. S. Miguel N. A. Farias S. de F. Villas R. Vaz A. J. Rubinsky-Elefant G. 2008Sero-epidemiology of toxocariasis in a rural settlement in São Paulo state, Brazil.
Radman N. E. Archelli S. M. Fonrouge R. D. Guardis M. del V. Linzitto O. 2000Human toxocarosis. Its seroprevalence in the city of La Plata.
Robertson B. D. Burkot T. R. Gillespie S. H. Kennedy M. W. Wanbai F. Maizels R. M. 1988Detection of circulating parasite antigen and specific antibody in
Roldán W. H. Espinoza Y. A. Huapaya P. E. Huiza A. F. Sevilla C. R. Jiménez S. 2009Frequency of human toxocariasis in a rural population from Cajamarca, Peru determined by DOT-ELISA test.
Rubinsky-Elefant G. da-Nunes Silva. M. Malafronte R. S. Muniz P. T. Ferreira M. U. 2008Human toxocariasis in rural Brazilian Amazonia: seroprevalence, risk factors, and spatial distribution.
Rubinsky-Elefant G. Hirata C. E. Yamamoto J. H. Ferreira M. U. 2010Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms.
Rubinsky-Elefant G. Hoshino-Shimizu S. Jacob C. M. A. Sanchez M. C. A. Ferreira A. W. 2011Potential immunological markers for diagnosis and therapeutic assessment of toxocariasis.
Sabrosa N. A. de Souza E. C. 2001Nematode infections of the eye: toxocariasis and diffuse unilateral subacute neuroretinitis.
Salem G. Schantz P. 1992Toxocaral visceral larva migrans after ingestion of raw lamb liver.
Santarém V. A. Felix A. Rodenas R. S. Assis A. P. D. da Silva. A. V. 2010Contaminação por ovos de
Santarém V. A. Giuffrida R. Zanin G. A. 2004Larva migrans cutânea: ocorrência de casos humanos e identificação de larvas de
Santarém V. A. Leli F. N. C. Rubinsky-Elefant G. Giuffrida R. 2011Protective and risk factors for toxocariasis in children from two different social classes of Brazil.
Santarém V. A. . Magoti L. P. Sichieri T. D. 2009Influence of variables on centrifuge-flotation technique for recovery of
Schantz P. 1989
Sharghi N. Schantz P. M. Caracmco L. Ballas K. Teague B. A. Hotez P. J. 2001Environmental exposure to
Sharif M. Daryani A. Barzegar G. Nasrolahei M. Khalilian A. 2010Seroprevalence of toxocariasis in schoolchildren in Northern Iran.
Sharkey J. A. Mc Kay P. S. 1993Ocular toxocariasis in a patient with repeatedly negative ELISA titre to
Shimizu T. 1993Prevalence of
Smith H. Holland C. Taylor M. Magnaval-F J. Schantz P. Maizel R. 2009How common is human toxocariasis? Towards standardizing our knowledge.
Soulsby E. J. L. 1982Ascaris. In:
Stensvold C. R. Skov J. Moller L. N. Jensen P. M. Kapel C. M. O. Petersen E. Nielsen H. V. 2009Seroprevalence of human toxocariasis in Denmark.
Stull J. W. Carr A. P. Chomel B. B. Berghaus R. D. Hird D. W. 2007Small animal deworming protocols, client education, and veterinarian perception of zoonotic parasites in western Canada.
Stürchler D. Schubarth P. Gualzata M. Gottstein B. Oettli A. 1989Thiabendazole vs. albendazole in treatment of toxocariasis: a clinical trial.
Taylor M. R. Keane C. T. O’Connor P. Girdwood R. W. Smith H. 1987Clinical features of covert toxocariasis
Taylor M. R. H. 2001The epidemiology of ocular toxocariasis.
Diagnostic trends of human toxocariasis. ( Watthanakulpanich D. 2010
Watthanakulpanich D. Smith H. V. Hobbs G. Whalley A. J. Billington D. 2008Application of
Watts C. S. Liang J. L. Schantz P. M. 2006
Wilder H. C. 1950Nematode endophthalmitis.
Wiwanitkit V. Waenlor W. 2004The frequency rate of
Wolfe A. Wright P. 2003Human toxocariasis and direct contact with dogs.
Won K. Y. Kruszon-Moran D. Schantz P. M. Jones J. L. 2008National seroprevalence and risk factors for zoonotic
Woodruff A. W. Bisseru B. Bowe J. C. 1966Infection with animal helminths as a factor in causing poliomyelitis and epilepsy.
Woodruff A. W. de Savigny D. H. Hendy-Ibbs P. M. 1982Toxocaral and toxoplasmal antibodies in cat breeders and in Icelanders exposed to cats but not to dogs.
World Health Organization (WHO). (January 2011Neglected zoonotic diseases. 31.01.2011. Available from http://www.who.int/neglected_diseases/zoonoses/en.
Wu Z. Nagano I. . Xu D. Takahashi Y. 1997Primers for polymerase chain reaction to detect genomic DNA of
Yamasaki H. Araki K. Lim P. K. C. Zasmy N. Mak J. W. Taib R. Aoki T. 2000Development of a highly specific recombinant
Zhu X. Q. Gasser R. B. Chilton N. B. Jacobs D. E. 2001Molecular approaches for studying ascaridoid nematodes with zoonotic potential, with an emphasis on