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Revista do Instituto de Medicina Tropical de São Paulo

On-line version ISSN 1678-9946

Rev. Inst. Med. trop. S. Paulo vol.49 no.5 São Paulo Sept./Oct. 2007

http://dx.doi.org/10.1590/S0036-46652007000500002 

REVIEW

 

Neurotoxocarosis

 

Neurotoxocaríase

 

 

Josef FinstererI; Herbert AuerII

INeurological Department, Krankenanstalt Rudolfstiftung
IIDepartment of Medical Parasitology, Institute of Hygiene and Medical Microbiology, Medical University of Vienna, Vienna, Austria

Correspondence to

 

 


SUMMARY

Infection of humans with embryonated eggs of Toxocara canis (larva migrans) remains asymptomatic, or results in covert or common toxocarosis, visceral larva migrans syndrome, or ophthalmologic and neurologic impairment. Though neurological manifestations of Toxocara canis larvae are rare, toxocarosis remains an important differential diagnosis of various neurological disorders. Manifestations of the central nervous system are dementia, meningo-encephalitis, myelitis, cerebral vasculitis, epilepsy, or optic neuritis. Manifestations of the peripheral nervous system comprise radiculitis, affection of cranial nerves, or musculo-skeletal involvement. If toxocarosis is neglected, ignored, or refused as a differential of these abnormalities, it may be easily overlooked for years. Early recognition and treatment of the infection is, however, of paramount importance since it reduces morbidity and mortality and the risk of secondary superinfection. Like the visceral manifestations, neurological manifestations of toxocarosis are treated by benzimidazole components, most frequently albendazole, corticosteroids, or diethylcarbamazine. If detected and treated early, the prognosis of neurological manifestations of toxocarosis is favourable.

Keywords: Toxocarosis; Parasitosis; Nervous system; Infection; Larva migrans syndrome; Helminthosis; Albendazole.


RESUMO

Infecção humana com ovos embrionados de Toxocara canis (larva migrans) pode permanecer assintomática ou resultar em toxocaríase acentuada ou comum, síndrome da larva migrans visceral ou manifestações neurológicas ou oftalmológicas. Embora manifestações neurológicas das larvas de Toxocara canis sejam raras, a toxocaríase permanece como importante diagnóstico diferencial de várias manifestações neurológicas. Manifestações do sistema nervoso central são demência, meningoencefalite, mielite, vasculite cerebral, epilepsia, ou neurite ótica. Manifestações do sistema nervoso periférico compreendem radiculite, agressão de nervos cranianos ou envolvimento músculo-esquelético. Se a toxocaríase é negligenciada, ignorada, ou recusada como diferencial destas anormalidades, ela pode ser facilmente desapercebida por anos. Reconhecimento precoce de tratamento da infecção é portanto de fundamental importância uma vez que reduz sua morbidade e mortalidade e o risco de superinfecção secundária. Da mesma maneira que as manifestações viscerais, as neurológicas são tratadas por benzimidazólicos, mais freqüentemente albendazole, corticosteróides ou dietilcarbamazine. Se detectado e tratado precocemente, o prognóstico das manifestações neurológicas da toxocaríase é favorável.


 

 

INTRODUCTION

Despite increased knowledge about hygiene worldwide and availability of potent anti-helminthic drugs, the prevalence of helminthoses is still high. This is because of inappropriate application of hygienic measures and because of the globalization and mobility, which allows worldwide distribution of parasites also to the Western world. One of the most frequently occurring helminthosis is the infection with the larvae of the nematodes Toxocara canis and Toxocara cati respectively [KAYES, 1997; MAGNAVAL et al., 2001]. Though these parasites rarely affect the central or peripheral nervous system (CNS, PNS), toxocarosis remains a differential diagnosis of various neurological disorders. The following review gives an overview on the current knowledge about the neurological implications of toxocarosis, which are frequently overlooked if toxocarosis is neglected, ignored, or refused as a differential. Early recognition and treatment of the infection is of paramount importance since it reduces morbidity and mortality and the risk of secondary superinfection [MAGNAVAL et al., 2001].

 

HISTORY

Human infection with Toxocara canis has been first described in the late fourties and early fifties. First evidence for CNS toxocarosis has been given by BEAUTYMAN & WOOLF in 1951. On autopsy they found a larva in the left thalamus of a child, whose death was attributed to poliomyelitis [BEAUTYMAN & WOOLF, 1951]. In 1952 the term "visceral larva migrans syndrome" (VLM) was coined for children with eosinophilia and long-term multi-system disease [BEAVER et al., 1952]. Further evidence for CNS toxocarosis came from a case report by DENT et al. in 1956. Also in 1956 the causative organism of toxocarosis was detected [TAYLOR, 2001] and NICHOLS et al., 1956 provided more data on the morphology of the worm and its eggs and larvae. Since then several case studies and case reports and a high number of animal studies has augmented the knowledge about all aspects of toxocarosis, particularly about neurotoxocarosis. The term covert toxocarosis was coined and defined by BASS et al. and TAYLOR et al. in 1987. About 50 patients with CNS or PNS toxocarosis have been reported so far.

 

INFECTIOUS AGENT AND WAY OF TRANSMISSION

Toxocarosis is caused by ingestion of the eggs of Toxocara canis, a roundworm in dogs, puppies, and cats [GARCIA-PEDRIQUE, 2004; PREISS, 1982]. The Toxocara roundworm is a nematode of the Ascaridae family which normally parasites the small intestine of its hosts [GLICKMAN & SCHANTZ, 1981; MAGNAVAL et al., 2001; PECINALI et al., 2005]. Female worms produce up to 200000 eggs/d, which pass to the feces, are not infective, and require an incubation period in the soil to embryonate [GLICKMAN & SCHANTZ, 1981]. Humans are accidentally infected by direct contact with dogs [WOLFE & WRIGHT, 2003], ingestion of embryonated eggs from soil (geophagia, pica), or after exposure to dirty hands (poor hygiene), raw vegetables, or to larvae from undercooked giblets [NAGAKURA et al., 1989; SALEM & SCHANTZ, 1992; XINOU et al., 2003]. After ingestion embryonated eggs hatch in the intestines, larvae penetrate the intestinal wall, and then migrate via the blood circulation to the liver, lungs, and left heart, from where they disseminate via the systemic circulation to eyes, brain, and muscle [DUNSMORE et al., 1983; KAPLAN et al., 2004; MAGNAVAL et al., 2001]. Larvae do not grow at these sites but become encapsulated by a collagenous reaction, manifesting as eosinophilic granuloma, and are metabolically active [XINOU et al., 2003]. They secrete an array of enzymes, waste products, and cuticular components, which cause tissue damage, necrosis, and a marked inflammatory reaction, with eosinophils as the major component [XINOU et al., 2003]. There are indications that toxic proteins from these eosinophils are released and contribute to the pathology and symptomatology of toxocarosis [KAYES, 1997].

The migratory pathway of Toxocara canis larvae after oral ingestion or artificial inoculation has been extensively studied in various animals. According to these studies Toxocara canis embryonated eggs reach the liver of NIH mice two days after infection and the lung three days after oral infection [ABO-SHEHADA & HERBERT, 1984]. Also the kidneys may be affected early. Larvae are then dispersed throughout the body and enter the myotropic/neurotropic phase (affection of the CNS or musculature) by day seven [ABO-SHEHADA & HERBERT, 1984; PECINALI et al., 2005]. If larvae are experimentally injected into the brain they are also capable of migrating from the brain to the viscera and musculature. Considerable pathology occurs due to larval migration and acute and chronic disease is recorded [ABO-SHEHADA & HERBERT, 1984]. There is a significant relation between the duration of infection, inoculum size, and dispersal rate of the larvae [EL-SHAZLY et al., 1991].

 

EPIDEMIOLOGY

As many as one billion humans are infected with animal parasites [DONOVICK AND BURRIGHT, 1987]. One of the most prevalent is Toxocara canis [MAGNAVAL et al., 2001]. The seroprevalence is particularly high in developing countries, especially in rural areas, and also some tropical islands [XINOU et al., 2003]. Human toxocarosis is predominantly frequent in areas where the stray and Toxocara canis infected dog population is big [KAPLAN et al., 2004]. The prevalence of Toxocara canis infections in dogs is variable and amounts to 4.3% in Japan [ITOH et al., 2004], 17% in Austria, or 66% in the USA [DONOVICK & BURRIGHT, 1987]. Particularly, in many rural areas worldwide infection rates may be even higher. Additionally, 40% of the foxes and up to 67% of the cats are infected in Austria [AUER & ASPÖCK, 1998]. An area is considered to pose a high risk for Toxocara canis infection when the infection rate among dogs is > 7% [XINOU et al., 2003]. There is a strong correlation between the infectious risk, life style and Toxocara sero-prevalence. Children are more frequently affected than adults [GARCIA-PEDRIQUE et al., 2004]. On the average, 7% of all humans carry antibodies against Toxocara canis [DONOVICK AND BURRIGHT, 1987], but there is a broad range depending on the tested location [DE ANDRADE LIMA COELHO et al., 2005; GARCIA-PEDRIQUE et al., 2004; AGUIAR-SANTOS et al., 2004]. From Reunion a seroprevalence of 93% in adults and from Saint-Lucia a seroprevalence of 86% in children has been reported [THOMPSON et al., 1986]. In a study on mountain aboriginal schoolchildren in Taiwan the overall seroprevalence of toxocarosis was 77% [FAN et al., 2004]. In Bali a seroprevalence of 63% has been found [MAGNAVAL et al., 1994]. In a study on 386 Brazilian children the frequency of IgG antibodies against Toxocara was 39% [AGUIAR-SANTOS et al., 2004]. Intestinal helminths were present in 52% of individuals that underwent coprological examination [AGUIAR-SANTOS et al., 2004]. In another Brazilian study the frequency of positive serology for toxocara was 30% [MOREIRA-SILVA et al., 2004]. In a study on 150 Lebanese subjects the seroprevalence was 19% [KANAFANI et al., 2006]. The annual incidence rate in a study on 75 individuals from the São Paulo area was 18% [ANARUMA FILHO et al., 2003].

 

VISCERAL MANIFESTATIONS

Humans who ingest Toxocara canis eggs may remain unaffected or may manifest a mono- or multi-system disease with symptoms arising from larval invasion of different organs [BACHLI et al., 2004; RUTTINGER & HADIDI, 1991]. The degree of host damage is dependent on the tissue affected, the number of migrating juveniles, the level of immunocompetence, and the host's age [DESPOMMIER, 2003]. Additionally, pathological consequences are dependent on the death of the juveniles [DESPOMMIER, 2003]. Death of larvae induces immediate-type and delayed-type hypersensitivity responses. Immediate-type hypersensitivity responses manifest clinically as classical VLM [DESPOMMIER, 2003]. The organs most frequently affected are the liver, lungs, eyes, CNS, myocardium, or musculature [HARALAMBIDOU et al., 2005; RUTTINGER & HADIDI, 1991]. Accordingly, toxocarosis can be classified as: 1. Classical or incomplete VLM. 2. Neurological toxocarosis, including ocular involvement (ocular larva migrans syndrome). 3. Covert or common toxocarosis [TAYLOR et al., 1987]. 4. Asymptomatic toxocarosis [AUER & ASPÖCK, 2004; BASS et al., 1987; HAYASHI et al., 2003; TAYLOR et al., 1987; TRABELSI et al., 2004]. In the majority of the cases, Toxocara canis infection remains clinically unapparent. Covert toxocarosis is present when in patients with only mild, focal impairment without systemic manifestations, toxocarosis remains unrecognized [AUER & ASPÖCK, 2004; KAWAJIRI et al., 2001]. Overt toxocarosis usually manifests in children as fever, anorexia, vomiting, lethargy, sleep and behavior disorders, pharyngitis, pneumonia, cough, wheeze, limb pain, cervical lymphadenitis, or hepatomegaly [MAGNAVAL et al., 2001]. Common toxocarosis is only loosely related to a clinical form but is most frequently associated with weakness, pruritus, rash, impaired breathing, and abdominal pain [MAGNAVAL et al., 2001]. VLM is usually seen in preschool children [PREISS, 1982] and characterized by general illness with fever, skin rash, abdominal symptoms due to hepatomegaly or splenomegaly, respiratory symptoms (particularly bronchospasm) due to pulmonary infiltrations, myalgias, arthralgias, anorexia, persistent eosinophilia of more than 30%, leucocytosis, and hyper-gammaglobulinemia [BARRA et al., 1996; OTA et al., 1994; PREISS, 1982; PECINALI et al., 2005; XINOU et al., 2003]. In the liver of patients with VLM granulomatous lesions can be found [HILL et al., 1985; LEONE et al., 2005]. In rare cases toxocarosis may manifest as colicky abdominal pain and ascites [CHIRA et al., 2005]. VLM usually results in a benign self-limited course [MOREIRA-SILVA et al., 2004]. Toxocarosis has been also associated with allergy-related syndromes, like chronic urticaria, reactive arthritis, or angioedema [ISMAIL & KHALAFALLAH, 2005; MAGNAVAL et al., 2001].

 

NEUROLOGICAL MANIFESTATIONS

A) CNS involvement: CNS involvement due to Toxocara sp. has been documented only in about 50 patients [BACHLI et al., 2004; BOUCHARD et al., 1998; GOFFETTE et al., 2000; HUISMANS, 1980; MOREIRA-SILVA et al., 2004; OSOEGAWA 2004] although in experimental animals larva migrans frequently migrates to the brain [FAN et al., 2003; GOOD et al., 2001; COX & HOLLAND, 1998]. The exact frequency of CNS involvement in toxocarosis is unknown and varies with different species of migrating larvae [MOREIRA-SILVA et al., 2004]. In a study on 308 autopsies of children the frequency of CNS granulomas due to larva migrans was 0.68%. In another study epilepsy was found in 5% of the patients with VLM [LEWIS et al., 1962]. Other studies however, showed that toxocara infection is frequently not associated with obvious neurological abnormalities although antibodies against Toxocara canis were repeatedly found in the CSF of these patients [MOREIRA-SILVA et al., 2004].

The site of the CNS invasion depends on multiple factors, like number of ingested larvae, genetic factors of the host, and whether previous exposure had occurred [XINOU et al., 2003]. CNS involvement comprises meningitis [ENGEL et al., 1971; MOREIRA-SILVA et al., 2004; OSOEGAWA, 2004], encephalitis [MOREIRA-SILVA et al., 2004; OTA et al., 1994], myelitis [ENGEL et al., 1971; GOFFETTE et al., 2000; KAWAJIRI et al., 2001; OSOEGAWA, 2004; OTA et al., 1994; SELLAL et al., 1992; YOSHIDA et al., 2004], cerebral vasculitis [DOUSSET et al., 2003], or optic neuritis [HAYASHI et al., 2003; KOMIYAMA et al., 1995] (Table 1). CNS toxocarosis is related to the number of larvae entering the brain and to the severity of CNS damage and inflammation [XINOU et al., 2003]. Following these manifestations, affected patients complain about headache, fever, over-sensitivity to light, weakness, dorsalgia, confusion, tiredness, and visual impairment. In mice behavioral changes have been reported and were related to the number of larvae accumulated in the brain [COX & HOLLAND, 1998; HAMILTON et al., 2006; SKERRETT & HOLLAND, 1997]. Despite the identification of the risk factors rural residence, ownership of dogs, and dementia for CNS toxocarosis by a multivariate logistic regression analysis, a recognizable neurologic defect has not been identified [MAGNAVAL et al., 1997]. Most of the cases with CNS toxocarosis on autopsy did not present with clinical CNS manifestations [MOREIRA-SILVA et al., 2004]. CNS toxocarosis may occur at all ages and it appears that there is no gender preponderance [MOREIRA-SILVA et al., 2004]. There may be eosinophilia exclusively in the CSF and vice versa focal CNS lesions with blood eosinophilia but normal CSF findings [VIDAL et al., 2003], why a negative spinal tap does not rule out CNS toxocarosis. In animals CNS toxocarosis manifested as cerebellar ataxia [AKAO et al., 2003].

 

 

1. Dementia: Dementia and depression have been reported only in a single patient as a manifestation of CNS toxocarosis [RICHARTZ & BUCHKREMER, 2002]. In a 65-year-old woman with a long-lasting history of depression and cognitive decline CSF investigations revealed eosinophilia and antibodies against Toxocara canis antigen. Treatment with albendazole improved the cognitive deficits. The infection was assumed to have occurred years before when the woman was working as a shepherd in close contact with dogs [RICHARTZ & BUCHKREMER, 2002]. Even if the infection had occurred already years before the clinical manifestations, affected patients may profit from specific anti-helminthic therapy [RICHARTZ & BUCHKREMER, 2002]. CNS toxocarosis may also manifest as behavioral disturbances [CRITCHLEY et al., 1982]. In a study on 155 children seropositivity to Toxocara was associated with adverse neuropsychological effects [MARMOR et al., 1987]. In a study on 77 children seropositivity was associated with poor reading achievement, marked distractibility, and lower intelligence [WORLEY et al., 1984].

2. Eosinophilic meningo-encephalitis: Eosinophilic encephalitis is a rare manifestation of a Toxocara canis infestation and has been reported in single patients [BARRA et al., 1996; GOULD et al., 1985; MIKHAEL et al., 1974; MIMOSO et al., 1993; MRISSA et al., 2005; SOMMER et al., 1994; VILLANO et al., 1992]. In a 21-year-old woman eosinophilic meningo-encephalitis manifested as frontal headache, fever, ataxia, meningeal irritation, epilepsy, and pleocytosis [OTA et al., 1994]. She had been in close contact with a dog. Cerebral MRI showed several T2-hyperintense cortical and subcortical lesions, which enhanced with gadolinium [OTA et al., 1994]. Antibodies against the Toxocara canis antigen were positive in the serum and CSF. Under a therapy with diethyl-carbamazine and corticosteroids the manifestations resolved [OTA et al., 1994]. In a 2-year-old boy with headache, confusion, weakness, clinical neurologic examination revealed lethargy, irritability, nuchal rigidity, weakness and accentuated deep tendon reflexes, extensive diagnostic work-up disclosed eosinophilic pleocytosis, and antibody testing revealed a Toxocara canis infection [VIDAL et al., 2003]. In a 54-year-old female encephalitis manifested on cerebral MRI as several enhancing subcortical white matter lesions in both lobes [XINOU et al., 2003]. A 48-year-old patient with Toxocara canis encephalitis presented with ataxia, rigor, and neuropsychological disturbances [SOMMER et al., 1994]. Imaging studies revealed diffuse, circumscribed white matter lesions and occlusion of various branches of the middle cerebral artery [SOMMER et al., 1994]. Antihelminthic therapy was only initially effective and, because of progression, had to be enhanced by corticosteroids and azathioprine [SOMMER et al., 1994]. Cerebral lesions of toxocarosis locate predominantly in the cerebral and cerebellar white matter with or without the presence of larvae [KAYES & OAKS, 1978]. The presence or absence of larvae within these lesions is due to the fact that larvae are not permanently trapped by the host reaction but can escape from the reaction, migrate elsewhere and elicit the same reaction anew [XINOU et al., 2003]. This is why the cellular composition of granulomas does not indicate the length of the infection [KAYES & OAKS, 1978].

3. Myelitis: Affection of the myelon by the larvae has been repeatedly reported [DAURIAC-LE MASSON et al., 2005; GOFETTE et al., 2000], usually in association with encephalitis or meningitis [EBERHARDT et al., 2005; ENGEL et al., 1971] but also isolated [SELLAL et al., 1992]. In a 40-year-old woman, eosinophilic myelitis resulted in subacute weakness of the right leg and dysesthesias in the dermatomas Th8-10. MRI studies of the myelon revealed an abnormal hyperintensity within the spinal cord and CSF investigations revealed eosinophilic pleocytosis [GOFETTE et al., 2000]. The neurological abnormalities resolved completely after mebendazole therapy [GOFETTE et al., 2000]. In a young woman recurrent myelitis was attributed to larva migrans infection after detection of eosinophilia in the serum and CSF, antibodies against Toxocara and a favorable response to diethylcarbamazine (DEC) [SELLAL et al., 1992]. Meningo-myelitis was also reported by others [DAURIAC-LE MASSON et al., 2005; ENGEL et al., 1971; SELLAL et al., 1992]. In these reports spinal MRI showed solitary or multiple, strongly and homogeneously enhancing T2-hyperintense lesions [DUPREZ et al., 1996; GOFETTE et al., 2000; KUMAR & KIMM, 1994; STRUPP et al., 1999]. In most of these cases the CNS was the organ exclusively affected by the infection [XINOU et al., 2003]. Some Japanese cases presented with sensory disturbances (positive Lhermitte sign, paresthesias, hyperesthesia), extensive, enhancing spinal cord lesions on T2-weighted MR images, and mild CSF eosinophilia [OSOEGAWA, 2004]. In a 27-year-old woman Toxocara canis myelitis manifested as back pain, positive Lhermitte sign, mild blood eosinophilia, mildly increased IgE levels, and CSF eosinophilia. In a single case toxocarosis manifested as spinal dural abscess [RUSSEGGER & SCHMUTZHARD, 1987].

4. Cerebral vasculitis: Only single angiographically documented cases with cerebral vasculitis have been reported [DOUSSET et al., 2003; HAMIDOU et al., 2002; OUJAMAA et al., 2003; SOMMER et al., 1994]. In one of these cases occlusion of multiple small branches of the middle cerebral artery with multiple consecutive brain infarcts has been found. Cerebral infarction close to the cerebral granulomas was also detected in another case [XINOU et al., 2003]. Cerebral vasculitis may even develop during antihelminthic treatment. Whether infarctions in these cases were due to the acute inflammatory reaction against the antigen or due to a delayed-type hypersensitivity to antihelminthic therapy remains questionable [XINOU et al., 2003].

5. Epilepsy: There are several reports showing an association between a positive Toxocara canis serology and seizures [ARPINO et al., 1990; NICOLETTI et al., 2002; OTA et al., 1994]. There are estimations according to which 12000-15000 of epilepsy cases in Britain are attributable to CNS toxocarosis [PIEKARSKI, 1987]. In another study epilepsy was found in three of 58 patients with VLM [LEWIS et al., 1962]. Seizures have been reported as the initial CNS manifestation of toxocarosis in quite a number of patients [BACHLI et al., 2004]. In an 11-year-old girl with generalized epileptic seizures due to a focal cerebral mass lesion and blood eosinophilia, toxocarosis was diagnosed after resection of the lesion [BACHLI et al., 2004]. After albendazole the patient recovered completely without sequelae.

6. Optic neuropathy: Ocular abnormalities are a frequent complication of toxocarosis. Ocular Toxocara canis infection usually manifests as visual loss from optic neuritis when there is simultaneous cerebral toxocarosis [KOMIYAMA et al., 1995]. Uveitis, or chorio-retinitis may also occur [MACARIE et al., 2005; STEWART et al., 2005]. Toxocara canis uveitis usually manifests unilaterally and may present as peripheral granuloma of the retina, papillitis, macular granuloma, or as vitreous inflammation, mimicking endophthalmitis [STEWART et al., 2005]. Secondary glaucoma can follow [DESPOMMIER, 2003]. In a study on 68 patients with posterior pole granuloma antibodies against Toxocara were detected in 17% of them [MIRDHA & KHOKAR, 2002]. According to findings in Mongolian gerbils, a useful animal model for toxocarosis, larvae migrate from the cerebrum to the eye through the optic nerve arriving there by day nine after inoculation [HAYASHI et al., 2003]. Other studies demonstrated ocular affection by the infection already three days after oral infection [HAYASHI et al., 2003]. According to these data there are two migration pathways to the retina in ocular toxocarosis, an early hematogenic pathway and a late pathway along the optic nerve [HAYASHI et al., 2003].

B) Peripheral nervous system involvement: PNS manifestations of toxocarosis are rare and comprise radiculitis, affection of cranial nerves, or musculo-skeletal involvement. However, PNS manifestations are presumably more frequent than previously reported.

1. Radiculitis: Radiculitis is a rare manifestation of neurotoxocariasis and usually occurs together with meningitis [ROBINSON et al., 2002]. The diagnosis is based on the clinical findings (reduced tendon reflexes, muscle weakness, muscle wasting fasciculations), CSF findings (eosinophilia, positive antibodies against Toxocara canis antigen), and abnormal nerve conduction studies (abnormal F-wave studies, proximal neuropathy), or electromyography (neurogenic electromyogram).

2. Cranial nerves other than the optic nerve: Larva migrans of Toxocara canis involving cranial nerves almost exclusively concerns the optic nerve [HAYASHI et al., 2003]. Larva migrans of Toxocara canis associated with affection of other cranial nerves has not been reported but peripheral facial palsy with atypical facial pain and swollen cervical lymph nodes may be a rare PNS manifestation of toxocarosis [personal communication]. In a patient with a peripheral seventh cranial nerve palsy diagnostic work-up revealed antibodies against Toxocara canis in the CSF. This patient profited shortly from a therapy with albendazole. That he did not develop neurological abnormalities other than the cranial nerve palsy is surprising, but may be attributed to the generally mild CNS manifestations of neurotoxocarosis. Obviously, more patients than assumed carry larvae but do not develop clinical neurological manifestations of the disease. Arguments for CNS toxocarosis in this case were the presence of Toxocara canis antibodies in the CSF, and bilaterally enlarged cervical lymph nodes. Transmigration of serum Toxocara canis antibodies via the blood brain barrier into the CSF is rather unlikely given the absence of any reports confirming such a scenario. On the other hand absence of pleocytosis and eosinophilia in the CSF does not exclude CNS toxocarosis, particularly after three previous albendazole cycles and the presumably long interval between the acute infection and antibody determination. Also repeatedly normal imaging studies of the brain do not exclude CNS toxocarosis. Assuming CNS toxocarosis as the cause of a Bell's palsy, either the infundibular (intracerebral) portion of the nerve must have been affected from focal encephalitis, meningitis, or radiculitis, or the larvae infiltrated the nerve and migrated centrifugally.

3. Skeletal muscle involvement: Migration of larva migrans to the musculature has been only rarely reported in humans [RAYES & LAMBERTUCCI, 1999; RAYES et al., 2000; SUGANE & OSHIMA, 1982]. Usually, muscular toxocarosis manifests as pyomyositis, accompanied by the development of muscular abscesses, granuloma formation around larvae, and tissue necrosis [RAYES & LAMBERTUCCI, 1999; SUGANE & OSHIMA, 1982]. In single cases muscular affection may also manifest as focal myositis, resulting in unilateral swelling of a leg [WALSH et al., 1988] or as severe necrotic pyomyositis, requiring urgent surgical debridement [LAMBERTUCCI et al., 1998]. In mice however, affection of the skeletal muscles by the infection is a frequent finding [FAN et al., 2003].

Diagnosis: Diagnosis of CNS and PNS involvement of toxocarosis is based on the history, the clinical neurologic investigation, blood tests, including differential blood cell count, and CSF investigations, including determination of antibodies against Toxocara canis antigen in the CSF, and imaging methods, including cerebral CT scans, cerebral MRI, and cerebral angiography. PNS involvement can be recognized when applying nerve conduction studies, F-wave studies, electromyography, CSF investigations, or muscle/nerve biopsy. Granuloma formation around larvae within the skeletal muscle can also be detected by imaging methods like ultrasound, CT, or MRI of the muscle [SUGANE & OSHIMA, 1982]. Since the prevalence of toxocarosis is high in patients with unknown eosinophilia, these patients should undergo antibody testing [KWON et al., 2006]. Generally, the diagnosis of neurotoxocarosis requires the following findings: 1. High titres of Toxocara canis antibodies in the serum. 2. High titers of Toxocara canis antibodies in the CSF. 3. Eosinophilia in the serum or CSF. 4. Clinical and radiologic improvement and normalization of CSF abnormalities upon anti-helminthic therapy [XINOU et al., 2003].

1. Blood chemical investigations: Eosinophilia can be almost always found in VLM, but may be absent in single patients with covert or common toxocarosis [MAGNAVAL et al., 2001]. On the contrary, in ocular or CNS toxocarosis eosinophilia is frequently absent [MAGNAVAL et al., 2001]. Another promising diagnostic parameter is elevated serum IgE [MAGNAVAL et al., 2001]. The most commonly used diagnostic test is the ELISA with TES-antigen. A positive ELISA can be confirmed by Western blot [MAGNAVAL et al., 2001], which is as sensitive as the ELISA and quite specific [MAGNAVAL et al., 2001]. Concerning the interpretation of the serological results, individuals with positive antibodies but absent clinical manifestations rather represent past than present infection [MAGNAVAL et al., 2001]. Seropositivity associated with eosinophilia, however, indicates active toxocarosis. In patients with covert or common toxocarosis but absent eosinophilia, increase in IgE provides evidence for active toxocarosis [MAGNAVAL et al., 2001]. Care must be taken concerning the reliability of Toxocara canis antibody titers in the serum and even CSF, since they are often normal or borderline, particularly in patients with sole CNS manifestations [XINOU et al., 2003].

2. Radiological investigations: Cerebral MR images show cortical or sub-cortical, multifocal, circumscribed, homogeneously enhancing T2-hyperintense lesions or a combination of circumscribed and diffuse changes [KOMIYAMA et al., 1995; RUTTINGER & HADIDI, 1991; SOMMER et al., 1994; ZACHARIAH et al., 1994]. These lesions are hypodense on cerebral CT and hypointense on T1-weighted MR images. Along with the CNS inflammation, areas of hemorrhage can be detected [XINOU et al., 2003]. Occasionally, there is focal meningeal enhancement suggesting extension of the inflammation to the subarachnoidal space [XINOU et al., 2003]. T1- and T2-hyperintense cortical areas are interpreted as cortical necrosis, presumably due to multiple brain infarcts caused by immune vasculitis [XINOU et al., 2003]. Generally, cerebral CT and MRI findings in neurotoxocarosis are non-specific and for establishing the diagnosis the above mentioned criteria need to be fulfilled. Serial MR imaging studies, however, are a valuable tool to monitor the disease course. In case of myelitis spinal MRI may show enhancing T2-hyperintensities [OSOEGAWA, 2004].

Differential diagnoses: Toxocarosis is not the only helminthic infection, which causes eosinophilic meningo-encephalitis. Eosinophilic meningo-encephalitis may also occur together with infections from Baylisascaris procyonis, Gnathostoma spinigerum, Angiostrongylus cantonensis, Coccidioides immitis, or together with cysticercosis, ascaridiosis, trichinosis, strongyloidosis, echinococcosis, schistosomiosis, paragonimiosis, or fascioliosis [VIDAL et al., 2003]. Transient CSF eosinophilia can be also observed in tuberculosis, syphilis, or lymphoma involving the meninges [VIDAL et al., 2003].

Therapy: There is a general lack of well-controlled studies on the therapy of neurotoxocarosis, being attributed to the rarity of the disease. Amongst all available drugs albendazole is the most commonly used and the treatment of choice [PAWLOWSKI, 2001]. However, other benzimidazole components, like oxibendazole, flubendazole, or thiabendazole [FOK & KASSAI, 1998; LEONE et al., 2005] have a similar effect [PAWLOWSKI, 2001]. Positive experiences also exist with DEC [REY et al., 2005]. Concerning the efficacy of ivermectin, it cannot be recommended for human toxocarosis at the moment [MAGNAVAL et al., 2001]. The blood-brain barrier is principally permeable for all available antihelminthic drugs [FOK & KASSAI, 1998], but benzimidazoles other than albendazole are poorly absorbed outside the gastrointestinal tract. Administration of albendazole three times per day is more effective than a single daily dose [DELGADO et al., 1989]. Albendazole gives better results than other antihelminthic drugs, because it reaches higher serum concentrations, has a better penetration into the CSF, and is less toxic [VIDAL et al., 2003]. Neurotoxocarosis may also resolve from thiabendazole [RUSSEGGER & SCHMUTZHARD, 1987] or DEC [RUTTINGER & HADIDI, 1991] alone, or from a combination of corticosteroids with DEC [KOMIYAMA et al., 1995], corticosteroids and mebendazole [DUPREZ et al., 1996], or corticosteroids and thiabendazole [KUMAR & KIMM, 1994].

In case of ocular involvement the additional administration of corticosteroids is recommended [RICHARTZ & BUCHKREMER, 2002]. Particularly, the Toxocara canis optic neuropathy is sensitive to corticosteroids [COX et al., 1993]. Except for ophthalmologic toxocarosis there is no consensus concerning the utility of corticosteroids for CNS toxocarosis [VIDAL et al., 2003]. Corticosteroids administered during Toxocara canis infestation may even result in a significant increase in brain parasitism and total larval count [MOHAMED et al., 1994]. If Toxocara canis endophthalmitis is non-responsive to the common surgical and medical approach (vitrectomy, antihelminthics, corticosteroids) cyclosporine A may be helpful [BARISANI-ASENBAUER et al., 2001; MORA et al., 2005; LESCANO et al., 2004].

Administration of specific antihelminthic drugs for CNS toxocarosis usually resolves the clinical neurologic impairment, but morphological lesions, found on imaging studies, only rarely decrease in size or number [RUTTINGER AND HADIDI, 1991]. Several experimental approaches resulted in promising results, like the glucan immunemodulator combined with immunoglobulin and zinc [SOLTYS et al., 1996]. In addition to the pharmacological treatment, CNS toxocarosis requires thorough prevention of recontamination by deworming dogs and sanitary education [MAGNAVAL et al., 2001].

 

CONCLUSIONS

Toxocara canis infestation is a worldwide problem and manifests as VLM, ocular larva migrans syndrome, covert toxocarosis or common toxocarosis or remains asymptomatic. Rarely, CNS and PNS are involved, manifesting as encephalopathy with cognitive decline, meningo-encephalitis, cerebral vasculitis, epilepsy, visual impairment, myelitis, radiculitis, cranial nerve involvement, or skeletal muscle affection. Transmission from animal to human is favored by the cohabitation with dogs and cats, poor hygiene, and by frequenting public parks and playgrounds. Prophylactic measures aim to limit access to contaminated soil, to regularly deworm pets, to reduce the number of domestic animals, and to limit their access to areas frequented by young children. Future control programs require cheap and effective diagnostic approaches, the development of vaccines, which offer lifelong protection, and effective and safe single-dose treatments. If detected and treated early, the prognosis of neurological manifestations of toxocarosis is favorable. Monitoring of CNS involvement in toxocarosis is best carried out by repeated MRI investigations. Serial serum tests for Toxocara antibodies are not useful for monitoring the disease course, since they may remain positive for months or years, even after clinical recovery. Blood eosinophilia should be thoroughly examined for helminthosis. CSF eosinophilia is no prerequisite for CNS toxocarosis.

 

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Correspondence to:
Univ. Prof. DDr. J. Finsterer
Postfach 20, 1180
Vienna, Austria
Tel. +43-1-71165-92085. Fax. +43-1-4781711
E-mail: fifigs1@yahoo.de

Received: 12 September 2006
Accepted: 16 April 2007

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