Clinical spectrum of symptoms in cerebral Toxocariasis (Review)
- Authors:
- Published online on: March 22, 2021 https://doi.org/10.3892/etm.2021.9953
- Article Number: 521
Abstract
1. Introduction
The incidence of parasitic infections remain prevalent disregarding the advancement in different countries. This increased incidence is generated partially by a rising number of travelers abroad and pet owners (1). In some countries, the food habits and preferences are varied and this factor can make humans in these countries more prone to this disease (1). Forms of toxocariasis in literature have been described after the ingestion of meat from chickens, cows and quails in Japan in adult patients with pulmonary and liver affections (1).
At the time of intrusion in the host gastro-intestinal system, the progression continues through the portal vein to the liver, where it can be cantonated, but also, with the possibility of by-passing the liver and continuing to migrate through the circulation in systemic organs, causing the manifest form of the disease depending on the concerned organ (1).
A categorical diagnosis of Toxocara cati or Toxocara canis infection can be established after the discovery of the larvae and eggs originating from the patient, but this situation is infrequent. Broadly, the diagnosis is determined in the hospital using the anamnesis of a history of eating uncooked meat, paraclinical laboratory exams hypereosinophilic syndrome with the existence of specific antibodies. The severity of this disease may be directly proportionate to the dose of inoculation (2). Glickman et al raised the concern about a high risk of potential infections with parasites from Canis and Felids in the situations of hunting and possessing hunting dogs inside human establishments (2).
Toxocara cati (T. cati) and Toxocara canis (T. canis) are the etiological factors of human toxocariasis. In addition, these ubiquitary zoonotic nematodes belong to the family Ascaridae (2). The adult parasites from T. cati and T. canis are located in the first part of the small intestine of the terminal host. T. cati and T. canis can be hosted in various types of paratenic beings such as humans, mammals, birds and rodents (3). The natural evolution of the presence of the larva in these organisms involves migration to certain tissues and organs of the hosts and long-term survival (3). This fact has been demonstrated by experimental studies on various animals such as chickens or mice, which have shown the migration of the pathogen in certain parts of the organism of the host (3).
2. Neuroinvasion in animals
Studies and experimental studies on animals have reported the presence of T. canis larvae in the brain, liver and other organs of the hosts, confirming migration of the larva in the organism of the host (3,4). Fenoy et al presented the theory that larvae are not always prevalent in histopathological lesions because of the motility of the larvae (5). Studies with animals have demonstrated that the most prevalent organ preferred by larvae in migration is the liver of the host, especially in the case of the chicken as the paratenic host (6,7).
Azizi et al demonstrated for the first time that following experimental infection with embryonated eggs in chicken with T. cati, the larvae had the capacity to migrate to other tissues and organs in the host besides the gastrointestinal tract. In this study, the migration of the larvae to the brain and liver of the hosts was reported along with the presence of mild infection. In addition, the research team recovered larvae from the brain and the liver of two chickens that were infected. The authors concluded by projecting an awareness of raw meat consumption, especially raw chicken brain and liver (8).
Studies involving mice infected with T. canis, reported ‘congestion, thickening of arterioles, moderate inflammatory infiltrate and severe gliosis’ (8,9). In addition, similar results related to the morphological aspects in toxocariasis were reported by Oryan et al in studies with chickens infected with T. cati (9).
In a study by Oryan et al with chicken infected with T. cati, the authors discovered, after 240 days after the inoculation of the larvae eggs, larvae recovery in 3 chicken brains and also modifications as hemorrhages and infiltrations (mostly lymphocytic, less eosinophilic) located in the meninges and also in the vessels in cerebral parenchyma and in the region of the cerebellum. The brain infection was mild, without any impairment of behavioral pattern observed in the infected chickens. Furthermore, histopathological changes were found in the organs of all the infected chickens (9).
In addition, Janecek et al reported similar structural brain damage in the cerebrum of T. canis-infected mice with the presence of activated microglia and focal accumulation of phagocytic cells (10). Similarly, Othman et al reported many T. canis larvae scattered in brain tissues of the infected group of mice inducing vascular congestion but without inflammatory infiltrate (11).
In a study by Pegg, common flies were infected with eggs of T. canis and afterwards, Beagle puppies were fed with the flies, after being treated with antihelminthics. From the puppies in the group, 80% became infected with T. canis after ingestion of the flies. Larvae and eggs were collected from various tissues of the dogs. This study has enormous importance in considering flies as sources of infection with T. canis not only for dogs, but as well as humans (12).
3. Neuroinvasion in humans
Neurotoxocariasis is a severe disease that has been associated with a decrease in mental activity, social changes and neurodegenerative diseases. The importance of the disease is determined by its ubiquitous spread as a zoonosis generated by T. canis or T. cati (9-11).
Toxocariasis in humans is produced by the presence in the digestive system of eggs in the embryonate stage or the tissues of hosts that contain the infective larvae. Humans develop the infectious disease after consumption of embryonated eggs coming from soil (geophagia, pica) or in the case of contact with dirty hands, raw vegetables, or larvae from undercooked or raw meat consumption (9-11). Present in the human body, the larvae begin their exodus using the blood flow to migrate to various organs in the body.
Toxocariasis can be categorized into four main stages: Asymptomatic-the most prevalent phase, visceral, ocular and neurotoxocariasis. The factors that contribute to the stage of the disease include: The quantity and quality of the infection, the patient's immune response and the concerned organs (9-11).
Toxocariasis that is located in the nervous system is a chronic disease that may recur for a considerable amount of time and may interfere with the functions of the nervous system, characterized by a decrease in cognitive capacity, neuropsychological impairment, depression, behavioral alteration and neurodegenerative diseases (11-13).
As a consequence of this localization, the treatment of neurotoxocariasis is difficult and consists of many challenges, as drugs destined to treat this disease have variable effects. In addition, effective treatment must take into consideration the difficulty of penetrating the blood-brain barrier, and on the other hand, the treatment can sometimes cause more detrimental effects than the disease itself due to allergic responses that may occur during treatment (11). Another challenge in the treatment of neurotoxocariasis is the fact that the treatment combines anti-inflammatory drugs to reduce the generalized inflammatory reaction, which also decreases the effectiveness of treatment on the pathogenic larvae, especially taking into consideration the fact that the immune reactions occur in the brain; thus, it is difficult to eradicate this disease.
The cells mainly involved in the defense process against the penetration of pathogens and parasites into the brain are astrocytes, which also modulate neuroinflammation. Through these processes, astrocytes maintain homeostasis in the brain (11). Taking into consideration the disruptions that occur in the neurotoxocariasis pathology, it is assumed that the function of astrocytes is impaired (11).
4. Case reports from the literature
The clinical intensity and type of manifestations in neurotoxocariasis are related to the quantity of the larvae that penetrate the blood-brain barrier and also are related to the severity of the destruction and inflammatory response (11). The clinical manifestations of neurotoxocariasis are distributed on a broad extent, generating varied syndromes: Encephalitis, seizures, brain vasculitis, extramedullary space-occupying lesion and meningitis (9-12).
The first case of neurotoxocariasis was reported in 1951 by Beautyman and Woolf (13), in the case of a child with clinical and pathological findings of a neurological disorder caused by an encapsulated larva recovered from serial sections of the brain at autopsy (the child's death was due to poliomyelitis) that was firstly wrongly assumed to be Ascaris lumbricoides. In 1956, Nichols (14) described the morphological features of Toxocara and Beautyman and Woolf (13) concluded that in their case report the child presented with T. canis, rather than the initial larvae believed. As the response of the infection with these zoonotic agents, at the molecular level, there appears a demyelination of the nerve fibers. In observations in mice, it was demonstrated that T. canis has a higher prevalent inclination of migration in the central motor system than T. catis (10). The terminology of neurotoxocarosis was first introduced in the literature in 2007(15).
In a case report by Marx et al (16), a 2-year-old girl presented with impairment of gait and ataxic gait, dysarthria, nystagmus, hyperreflexia of the lower limbs, cutaneous plantar reflex in extension bilaterally, nuchal rigidity and Brudzinski sign. Cerebrospinal fluid (CSF) analysis showed pleocytosis with the predominance of lymphocytes. Magnetic resonance was suggestive for acute disseminated encephalomyelitis, but the laboratory analysis tests of the blood and CSF showed the presence of antibodies against T. canis. This case report was the first case reported in an article of neurotoxocariasis with acute disseminated encephalomyelitis pattern images in magnetic resonance imaging (MRI).
The systemic symptomatology may be absent in most cases, but regarding the neurological symptomatology, the most prevalent are: Deterioration in the motor area, seizures of the epileptic type and impairments in the neuropsychological area (17).
The eating patterns of individuals are particularly important because of the prevalence of human ingestion of animal raw organs, especially the liver and brain, a situation reported by Morimatsu et al in a familial case of ingestion of raw chicken liver that presented visceral larva migrans caused by T. canis larvae. Both patients in this family presented with mainly systemic and pulmonary signs and symptomatology, but one of the patients also presented neurological symptoms in anamnesis, before admission to the hospital which included posterior headache and neurologic abnormality of the front of the right arm of 3-week duration (18).
In a case report by Goffette et al, a woman presented with the following neurological findings: Subacute weakness located in the right leg and dysesthesia located in the right Th8-Th10 dermatomes; the cerebrospinal fluid findings showed eosinophilic pleocytosis and also the levels of T. canis were more significant in the CSF than in the blood (19).
Mikhael et al presented a case of an 18-month-old male who was admitted twice to the hospital; firstly with inconclusive diagnosis and laboratory findings, being probable a case of visceral larva migrans. At the second admission, the child presented with ataxia and went into status epilepticus repeatedly and became comatose. The patient's exitus came after 3 days. The pathological findings showed T. canis larvae in the brain and other organs. Numerous granulomatous inflammatory regions located both in the white and gray matter were found in both cerebral hemispheres, cerebellum and brain stem and also, observed parts of the larvae were found in these regions (20). Table I summarizes the results from the literature regarding the cases of cerebral toxocariasis in chronological order (13,16-19,20-51).
5. Conclusions
The specificity of the clinical manifestations of neurotoxocariasis has not been clearly determined, but the clinical manifestations reflect in an insightful way the provenience of the lesions located in the central nervous system. In the literature, a prevalence of male gender has been reported among cases of neurotoxocariasis, with 75% of the cases cited with a mean age of 42.5±15.5(52); compared with cases of visceral larvae migrans that are more prevalent among children (53).
The cerebral localization was most prevalent in Europe and subsequently America with reference to the geographical classification. A few cases of encephalic localization were reported in Asia, in contrast to the large number of cases of spinal cord localization reported in this area (54).
The most encountered form of debut in neurotoxocariasis is the isolated myelitis that is prevalent in approximately 70% of the cases (52,54,55). The symptoms are represented by sensory and motor impairments, mostly being located in the lower limbs and usually being followed by autonomic dysfunction. In a study by Lee et al, 33 patients that presented with atopic myelitis were positive for the Toxocara excretory-secretory antigens in immunological tests, developing a new branch of research and differential diagnosis for the patients that present with unusual cases of myelitis (56). In a study by Lee et al in 2010, the authors investigated retrospectively the MRI findings of visceral larva migrans of neurotoxocariasis located in the spinal cord of 8 patients, and the authors found only one patient that presented a migration of lesion (56). Furthermore, in a study by Jabbour et al that contained the examination of 17 patients with myelitis due to T. canis infection, only one lesion in the spinal cord revealed characteristic MRI spinal cord imaging (42). These three studies on myelitis caused by Toxocara infection represent a number of 56 cases, about half of all cases of neurotoxocariasis reported in the literature. Moreover, most cases of myelitis due to Toxocara infection were diagnosed in Korea and Japan and several cases were reported in Western countries (52,54,55).
The cerebral localization of Toxocara infection is revealed through presentation of meningitis, encephalitis, meningoencephalitis, encephalomyelitis, and meningoencephalomyelitis, but cerebral abscesses have been reported in several cases (56,57). Encephalic and meningeal toxocariasis implication is correlated with a large area of clinical symptoms containing headache, seizures, focal deficits, confusional state, and cognitive impairment, the presence of fever not being mandatory (56,57).
Another important factor to be taken into consideration as a symptom of neurotoxocariasis is the presence of epileptic seizures, as demonstrated in a study by Luna et al (57). Another theory targets the implication of neurological disorders that are evolving in a paraclinical frame of high Toxocara seropositivity (58,59). Depressive symptoms, mental confusion, cognitive impairment and even schizophrenia have been reported to be prevalent among patients with neurotoxocariasis (60,61). Furthermore, in a study by Hotez, the significance of infections is viewed as a factor that causes lower academic achievement between students that come from rural areas, due to the presence of the effects that infections have on the human brain (62). In light of all of the cases presented, awareness must be maintained concerning the implications of Toxocara infection on the whole organism, but especially in the nervous system. It is extremely important to consistently consider infection with Toxocara as a differential diagnosis.
Neurotoxocariasis represents a rare diagnosis. It is possible to be underdiagnosed especially due to the vague and wide-ranging characteristics of the symptomatology aggravated by an insufficiency of supporting diagnostic investigations. This is also the reason why MRI investigation has become so important and vital in this disease. Therefore, a classification of brain imaging conclusions have been described in connection with neurotoxocariasis, firstly being assessed by computed tomography and currently with the aid of magnetic resonance imaging (63). Regardless of the obvious significance of interpretation of neuroimaging conclusions, only several clinicians use MRI to diagnose and evaluate neurotoxocariasis (63).
MRI could represent the most accessible aid for evaluating the efficacy of treatment and to pursue the evolution of the disease, facts that alternatively could be otherwise challengeable or unattainable, particularly for patients which present sporadic seizures. In an article by Rüttinger and Hadidi (63), which assessed the importance of MRI in neurotoxocariasis, it was concluded that gadolinium-enhanced MRI could be significantly valuable for determining the requirement of treatment, as well as to assess a disrupted blood brain-barrier to an active inflammation.
Acknowledgements
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Funding
No funding was received.
Availability of data and materials
All information in this review is documented by relevant references.
Authors' contributions
ADA, AEG and AZS conceived and designed the review. AZS, AEG and ADA performed the literature research. ADA, AEG, AP, DCJ, AZS and DDA were involved in the interpretation of the findings in the literature. ADA, AZS, AEG and DDA were involved in the writing of the manuscript. All authors have read and approved the final manuscript.
Ethics approval and consent to participate
Not applicable.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
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