Reviews on Trichinellosis (II): Neurological Involvement

Abstract

Neurological involvement may occur in 0.2%–52% of cases with trichinellosis, generally in the most severely affected patients. This review focuses on neurotrichinellosis and includes a brief overview of selected cases reported in the literature. Our primary goal was to increase the awareness of infectious diseases specialists, neurologists, and general practitioners about these major complications with possible fatal outcome. Seventy seven of the cases, for which enough details were available, have been pooled for statistical analysis. The mean age of the investigated group was 34.6 ± 16.8 years. Patients with both focal and diffuse manifestations predominated (55.8%), and they were significantly older (40 ± 15.5 years old) than those who presented solely focal (28.9 ± 17.8 years old; p = 0.03) or diffuse lesions (27.9 ± 15.3 years old; p = 0.007). In most of the cases (59.7%), complete recovery was reported, whereas 23.4% of cases had sequelae and 16.9% of the patients died. Patients who died had significantly lower eosinophil counts (13.8% ± 14%) when compared with those who made complete recovery (28.7% ± 18%; p = 0.015) and the cases with sequelae (35% ± 17.9%; p = 0.006). To sum up, trichinellosis must be considered in the differential diagnosis of any patient with encephalitis or other central nervous system malady of ambiguous etiology.

Introduction

N eurological involvement of trichinellosis, sometimes referred as neurotrichinellosis, generally occurs in the most severely affected patients, with a prevalence that varies largely across different studies: 0.2% in a Turkish study analyzing 154 patients (Turk et al., 2006), 1.4% in a French study on 494 patients (Ancelle et al., 1998), 2.1% major neurological disturbances and 4% minor neurological disturbances in a Romanian study on 757 cases (Jifcovici, 2001), 4.8% in a Romanian study on 145 cases (Jifcovici, 2001), 18% in a Romanian study on 699 patients (Nemet et al., 2009), 37.2% in a Romanian study on 196 patients (Enache, 2005), and 52% in a 10-year German prospective study on 128 infected patients (Harms et al., 1993). Timely implementation of proper therapy may lower the frequency of these complications (Dupouy-Camet et al., 2002; Dupouy-Camet and Bruschi, 2007).

This review focuses exclusively on neurological complications of trichinellosis and includes a brief overview of selected cases reported in the literature. Our primary goal was to increase the awareness of infectious diseases specialists, neurologists, and general practitioners about these major complications with possible fatal outcome.

Pathology and Pathogenesis

Either gray or white matter of the brain, cerebellum, pons, or spinal cord may be involved in neurotrichinellosis (Taratuto and Venturiello, 1997). Peripheral nerves are less frequently affected (Kociecka et al., 2003). Central nervous system (CNS) damage (Fig. 1) is caused either directly by the parasitic larvae or indirectly (Taratuto and Venturiello, 1997). Trichinella larvae can migrate in CNS and cause diffuse lesions, obstruction of the blood vessels, and inflammatory infiltrate, or the larval and muscle breakdown products may mediate different pathologic alterations (Mawhorter and Kazura, 1993; Taratuto and Venturiello, 1997; Schantz and Dietz, 2001). An infiltration of pia-arachnoid generally involves lymphocytes, macrophages, fibroblasts, and gitter cells (Mawhorter and Kazura, 1993; Kociecka et al., 2003). The larvae either produce pathologic manifestations in tissues before returning into the circulation or may be trapped and consequently destroyed, causing inflammatory reactions (Bruschi and Murrell, 2002, 2006; Dupouy-Camet and Bruschi, 2007). Microscopic nodules, consisting of clear necrotic areas that surround the parasites, may be detected in the subcortical white matter (Muller and Wakelin, 2002). Trichinella larvae may be present in cerebrospinal fluid (CSF) or meninges (Muller and Wakelin, 2002). Edema, hyperemia, and punctuate hemorrhages occur most commonly in the brain substance (Muller and Wakelin, 2002). Nodules of glial cells and small hemorrhages develop in the periventricular and other regions of the white matter (Kociecka et al., 2003). Vascular alterations (vasculitis and granulomatous inflammatory reactions) surrounding the larvae are considered the main mechanisms that lead to neurological damage (Kociecka, 2000; Schantz and Dietz, 2001; Bruschi and Murrell, 2006; John and Petri, 2006). Eosinophils stimulated by either eosinophil chemotactic factor of anaphylaxis or cytokines, such as interleukin 5, may kill the larvae and determine vascular injuries (Taratuto and Venturiello, 1997; Bruschi et al., 2008). The products resulting from the degranulation of the eosinophils (eosinophil-derived neurotoxin and major basic protein) are also considered as potential harming factors for the neural cells (Bruschi and Murrell, 2002, 2006; Dupouy-Camet and Bruschi, 2007; Bruschi et al., 2008). Tumor necrosis factor-alpha is able to mediate endothelial cell damage and determine eosinophil toxicity in neural tissues also (Taratuto and Venturiello, 1997). Vascular occlusion could be produced by eosinophils through a direct prothrombotic effect (Del Brutto, 2005, 2009).

FIG. 1.

CNS pathogenesis in trichinellosis. CNS, central nervous system; TNF-α, tumor necrosis factor alpha; ECF-A, eosinophil chemotactic factor of anaphylaxis; IL-5, interleukin 5.

Nervous alterations in experimental trichinellosis are briefly overviewed in Supplementary Table S1 (Supplementary Data are available online at www.liebertonline.com/fpd).

Clinical Symptomatology

Neurological involvement of trichinellosis encompasses a variety of signs and symptoms (Table 1). Moderate headache exacerbated by head movement is one of the most frequently detected clinical manifestation (Bruschi and Murrell, 2002; Kociecka et al., 2003).

Table 1.

Neurological Signs and Symptoms Detected in Trichinellosis

Focal signs		Diffuse signs
Frontal lobe signs	Monoparesis/monoplegia	Signs of meningitis	Headache
	Hemiparesis/hemiplegia		Stiff neck/nuchal rigidity
	Seizures		Kernig's sign
	Change in personality		Photophobia
	Apathy		Altered mental status
	Unsteadiness in walking		Lethargy
	Incontinence (of urine or feces)		Delirium
Parietal lobe signs	Impairment of tactile sensation		Seizures
Temporal lobe signs	Cortical deafness
	Tinnitus
	Disturbance of memory
	Aggressive or antisocial behavior
Occipital lobe signs	Cortical blindness	Signs of encephalitis	Headache
	Visual agnosia		Confusion
	Homonymous hemianopsia		Drowsiness
Cerebellar signs	Ataxia		Disorientation
	Nystagmus		Loss of consciousness
Brainstem signs	Cranial nerves involvement (especially II, VI, VII, VIII)		IrritabilitySeizures
Spinal cord signs	Paraplegia

Diagnosis

Neurotrichinellosis should be considered in patients with brain infarctions accompanied by fever, myalgia, periorbital edema, and eosinophilia (Del Brutto, 2005, 2009).

Electroencephalogram (EEG) may indicate a total deceleration of the cortical electric activity without critical aspect, and electromyography reveals bioelectric disturbances by reduced amplitude of muscle contraction and incomplete interference (Kociecka, 2000; Dupouy-Camet and Bruschi, 2007; Gottstein et al., 2009).

Computed tomography (CT) scan is able to detect hypodense foci situated in the cortex, subcortex, or white matter (Schantz and Dietz, 2001; Dupouy-Camet et al., 2002; Kociecka et al., 2003; Dupouy-Camet and Bruschi, 2007). Lesions involving cortex and white matter may be enhanced by injection of a contrast substance (Dupouy-Camet and Bruschi, 2007). Magnetic resonance imaging (MRI) can also evidence small hypodensities in iso/hyposignal T1, and especially in hypersignal T2, and protonic density (Dupouy-Camet et al., 2002, 2010; Dupouy-Camet and Bruschi, 2007). Enhancement may be produced by injection of gadolinium diethylenetriamine penta-acetic acid (Dupouy-Camet and Bruschi, 2007; Gottstein et al., 2009). CT scan/MRI disturbances usually disappear in 1–2 months after infection (Dupouy-Camet et al., 2002; Dupouy-Camet and Bruschi, 2007).

In most of the cases, CSF is normal but the analysis may occasionally indicate a slight increase in protein content and moderate cellularity (lymphocytes and eosinophils) (Lowichik and Ruff, 1995; Clausen et al., 1996; Kociecka et al., 2003; Graeff-Teixeira et al., 2009). CSF alterations are of little known significance (Kociecka et al., 2003). In 8%–28% of patients with CNS symptoms, Trichinella larvae were detected in CSF (Mawhorter and Kazura, 1993; Taratuto and Venturiello, 1997).

Differential Diagnosis

Severe cephalalgia accompanied by nuchal pseudorigidity, confusion, lethargy, irritability, and other neurological symptoms must be distinguished of infectious meningitis and encephalitis produced by other pathogens (Kaufman, 1940; Kociecka, 2000; Dupouy-Camet et al., 2002; Kociecka et al., 2003; Dupouy-Camet and Bruschi, 2007; Gottstein et al., 2009). Typhoid fever should be considered more likely in case of neurological symptoms and high fever without eyelid edema, accompanied by decreased leukocyte and eosinophil counts and low antibody production (Evers, 1939; Dupouy-Camet et al., 2002; Kociecka et al., 2003; Dupouy-Camet and Bruschi, 2007; Gottstein et al., 2009). Trichinellosis with meningeal irritation must be differentiated from poliomyelitis (Meyer, 1918; Kaufman, 1940). Myasthenia gravis (Most and Abeles, 1937) and dermatomyositis (Kaufman, 1940) should also be considered in the differential diagnosis.

Treatment

Antihelminthics are the main drugs used for trichinellosis and they must always be administered before corticotherapy because the latter may prolong the presence of adult worms in the intestine (Kociecka, 2000; Muller and Wakelin, 2002). The most efficient antihelminthic drugs are albendazole (15 mg/kg/day divided into two doses for 10–15 days in adults and 10 mg/kg/day in children older than 2 years) and mebendazole (5 mg/kg/day divided into two doses for 10–15 days in adults) (Bruschi and Murrell, 2006). Thiabendazole is less frequently used because of its side effects. Corticosteroids are strongly recommended to suppress the vascular damage induced by eosinophils (Del Brutto, 2005, 2009). Their administration in patients with severe trichinellosis shortens the course of the illness by reducing the symptoms associated with early-type hypersensitivity (Kociecka, 2000). High dosage (prednisolone 40–60 mg daily; adrenocorticotrophic hormone 200 units or cortisone 25 mg four times daily, 4–5 weeks) is very important to alleviate neurological disturbances (Muller and Wakelin, 2002). Following the implementation of corticotherapy, the rate of fatality in neurotrichinellosis significantly decreased from 46% to 17% (Kociecka et al., 2003). Analgesic and antipyretic drugs may also be given and bed rest is recommended (Bruschi and Murrell, 2006). Generally, neurological complications that occur in early stages of the illness may be successfully treated with corticosteroids but those developed late in the course of the disease (after ∼1 month) may cause permanent sequelae and must be managed by a neurologist (Kociecka et al., 2003).

Overview of Selected Cases or Cluster of Cases Reported in the Literature

Methods

A literature search was initially performed in PubMed, Embase, and ISI Web of Knowledge databases using as keywords the terms “trichinellosis OR trichinosis OR Trichinella,” “neurological OR neurologic,” and “neurotrichinellosis OR neurotrichinosis.” Additionally, the archives of several high-ranking journals were searched. We also included unpublished cases from our own database containing information collected in five infectious diseases hospitals from western/central-western Romania.

Results

The most important cases or clusters of cases reported in literature are briefly overviewed below. Details of these cases and of others, without any outstanding particularities, are summarized in Supplementary Table S2. We emphasized on epidemiological aspects, neurological findings, and routine laboratory parameters.

Beginnings: Trichinella larvae in brain and CSF

In 1906, Trichinella larvae were detected in brain during an autopsy performed at Boston City Hospital (Frothingham, 1906). In 1914, the larvae were first evidenced in the spinal fluid of a patient in the United States (Van Cott and Lintz, 1914) and since then other similar cases have been reported in the same country (Bloch, 1915; Cummins and Carson, 1916; Elliott, 1916; Lintz, 1916; Meyer, 1918; Salan and Schwartz, 1928; Evers, 1939; Schmidt-Sidor et al., 1977). Fatality occurred in a young patient whose brain was invaded by Trichinella larvae. This was the first case where consistent descriptions of pathologic changes were provided (Hassin and Diamond, 1926).

Unusual, interesting, and rare presentations

A very interesting and atypical case of trichinellosis in a child was reported by Pund and Mosteller (1934). Unfortunately, the correct diagnosis was not established while patient was alive. Gordon et al. (1935) presented a fatal case of a young girl in whom digestive symptoms, muscular tenderness, and eosinophilia lacked until the day preceding death. Two cases of young patients both presenting with diplopia were described by Stoll (1929). Reimann et al. (1943) and Frayha (1981) reported cases with simultaneous renal and neurological involvement accompanied by periarteritis (polyarteritis) nodosa. MacAndrew and Davis (1948) noticed a case of unusual combination of neurological features. Perot et al. (1963) reported three cases of cerebral trichinellosis, with EEG and mental modifications. One of these patients presented a relapse with EEG abnormalities and episodes of stupor—the case was considered unique at that time. Dalessio and Wolff (1961) described a case with persistent neurological signs of unusual severity, which occurred early in the course of disease. The patient recovered from a comatose state but remained triplegic. Kennedy and Rege (1966) presented a case with both neurological (“stroke” picture) and liver involvement. Kramer and Aita (1972) described a single and interesting case complicated by rectal paresis. They stated that up to then, of 110 cases reported in literature, only 3 (2.7%) had been found with such type of severity. Davis et al. (1976) reported a patient with severe and unusual course of disease who survived and recovered completely despite presenting an extremely high concentration of larvae in muscle (over 4000 per gram). Describing the first case of trichinellosis associated with superior sagittal sinus thrombosis, Evans and Patten (1982) concluded that this severity should be added to the list of possible CNS complications of the malady. Gay et al. (1982) described a case with fatal outcome probably because of alterations caused by cortical vein thrombosis, and El Koussa et al. (1994) presented the case of a patient with sino-venous thrombosis. Kociecka et al. (1987) reported a fatal case with both neurological and renal involvement. A very interesting and rare case of trichino-echinococcosis in a young patient was notified by Bhatoe et al. (2000).

Simultaneous detection of neurological and cardiac manifestations

Gray et al. (1962) reported three cases with neurological and cardiac involvement, of which two presented residual CNS disturbances after hospital discharge. Another case involving a young adult with predominant CNS symptomatology and concomitant cardiac involvement was reported by Roehm (1954). Other two cases of interest were managed at the Ottawa Civic Hospital. Both patients were critically affected, and one of them developed sequelae (perineal and vaginal anesthesia) (Barr, 1966). Andy et al. (1977) evidenced minor neurological symptoms in a patient with extensive ventricular mural endocarditis and superimposed thrombosis. Gross and Ochoa (1979) reported a case who additionally presented ocular complications and severe myositis. Surprisingly, the enteric phase of the disease was absent. Lopez-Lozano et al. (1988) found these complications in a patient who was successfully managed. Fourestie et al. (1993) reported a cluster of nine patients with nervous complications, of whom eight presented various cardiovascular events also. One of them died and the autopsy revealed ischemic lesions with multiple arteriolar microthrombi in the brain and myocardium.

Technological advances: helpful or ineffective?

Ryczak et al. (1987) reported a case with quadriplegia and concluded that technological advances (CT scan, angiogram, EEG) may be of no value when compared with traditional and routine diagnostic methods. Ellrodt et al. (1987) described three cases that occurred during an epidemic caused by ingestion of horse meat, and in two of them, CT scan and MRI revealed multifocal lesions of CNS. Feydy et al. (1996) presented a case in which MRI with gadolinium diethylenetriamine penta-acetic acid enhancement revealed bilateral lesions in the white matter accompanied by numerous small subacute cortical infarcts. During the following years, other cases evaluated by MRI were discussed (De Graef et al., 2000; Knezevic et al., 2001; Gelal et al., 2005). A case was evaluated by both conventional and diffusion-weighted imaging MRI for the first time in 2005 (Gelal et al., 2005).

Authors' own experience

During the period 1990–2009, we have retrospectively collected data on 1852 cases of trichinellosis in western and central-western Romania. Noteworthy is that only eight patients (0.43%) had neurological involvement (R. Neghina, unpublished cases).

Analysis of Cases

Methods

Seventy seven of the overviewed cases were detailed enough (in terms of sex, age, absence or presence of the larva in CSF, absence or presence of focal and/or diffuse neurological involvement, outcome, and routine laboratory parameters) to allow pooled analysis.

Statistical evaluation was performed using the software package SPSS version 17.0 for Windows (SPSS, Chicago, IL). Descriptive statistics (percentage, mean, and standard deviation) were calculated for each variable where appropriate. Odds ratios with their respective 95% confidence interval were calculated to assess the associations between different variables and outcome (sequelae and/or death vs. complete recovery). Comparisons between patient groups were made by means of Mann–Whitney U statistics for quantitative data. A p-value of <0.05 was regarded as statistically significant.

Results

The mean age of the analyzed group was 34.6 ± 16.8 years (range: 4–72), with most of the cases in the age group of 19–59 years (70.1%, n = 54). Men slightly predominated (51.9%, n = 40) and their mean age (35.3 ± 15.2 years, range: 8–72) was comparable to the age of women (33.9 ± 18.5 years, range: 4–69).

The larva was evidenced in the CSF in seven cases (15.2%), of whom four were children (12 ± 4.3 years old, range: 6–16) and three were young adults (27.7 ± 10.3 years old, range: 19–39). All made complete recovery (Supplementary Table S3).

Patients with both focal and diffuse neurological involvement predominated within the analyzed group (55.8%, n = 43), and they were significantly older (40 ± 15.5 years old, range: 4–72) than those who presented solely focal neurological involvement (28.9 ± 17.8 years old, range: 8–65; p = 0.03) or diffuse neurological involvement (27.9 ± 15.3 years old, range: 6–54; p = 0.007).

The percentage of eosinophils was reported in 59 cases (27.7% ± 18.4%, range: 0%–76%), whereas absolute eosinophil count was given in seven cases (5971.4 ± 2903.3 cells/μL, range: 1800–10,400).

The leukocyte values were reported in 58 cases (14,628.8 ± 6181.3 cells/mm³, range: 5300–30,000).

Most of the patients made complete recovery (59.7%, n = 46), whereas 23.4% (n = 18) had sequelae and 16.9% (n = 13) died. Supplementary Table S3 shows the demographic data and neurological involvement in the analyzed group according to patients' outcome.

There was no significant difference between patients' mean age with respect to their outcome (complete recovery: 32.7 ± 15.5 years old, range: 6–62; sequelae: 40.3 ± 14.8, range: 13–65; death: 33.6 ± 22.3, range: 4–72).

Sequelae were significantly associated with focal and diffuse neurological involvement (odds ratio = 5.5; 95% confidence interval: 1.4–21.4; p = 0.02) (Supplementary Table S3).

Patients who died had significantly lower eosinophil counts (13.8% ± 14%, range: 0%–43%) when compared with those who made complete recovery (28.7% ± 18%, range: 1%–76%; p = 0.015) and the cases with sequelae (35% ± 17.9%, range: 8%–70%; p = 0.006).

Of patients in whom absolute eosinophil count was reported, two made complete recovery (7800 ± 3677 cells/μL, range: 5200–10,400), four had sequelae (5235 ± 3030.3 cells/μL, range: 1800–9200), and one died (4900 cells/μL).

Discussion and Conclusions

Neurological involvement of trichinellosis was evidenced for the first time in 1866 by Kratz, who described several cases with delirium, apathy, insomnia, and skin anesthesia (Most and Abeles, 1937; Mawhorter and Kazura, 1993). Since then, numerous cases have been reported demonstrating that presentations of CNS Trichinella infections are myriad, and consequently, diagnosis may be elusive (Ryczak et al., 1987). This may happen especially when the characteristic symptomatology of trichinellosis is missing (Ryczak et al., 1987) or in case of physicians' unfamiliarity with this uncommon course of disease (Mawhorter and Kazura, 1993). The explanation of such wide range of neurological signs and symptoms may reside in the fact that parasitic larvae have no predilection for any particular region of the CNS (Gray et al., 1962; Barr, 1966). Because these protean neurological manifestations are able to mimic acute psychosis (Gray et al., 1962), sometimes patients are initially hospitalized in psychiatric services unless the correct diagnosis of Trichinella encephalitis is considered (Ryczak et al., 1987).

Generally, the routine laboratory tests show hematological alterations such as leukocytosis and eosinophilia (Lopez-Lozano et al., 1988). Eosinophilia usually occurs in the first 10 days following infection and may be considered a clinical rule. Nevertheless, in severe cases it might be delayed even for a couple of weeks (Meyer, 1918; Dalessio and Wolff, 1961). According to some authors (Meyer, 1918; Dalessio and Wolff, 1961) and to our statistical results, there is usually an inverse relationship between eosinophil counts and the severity of symptoms. A poor, often fatal prognosis may be associated with the absence or sudden decrease of eosinophilia (Pund and Mosteller, 1934; Most and Abeles, 1937; Kramer and Aita, 1972). As stated by Evers (1939) and in the light of our pooled analysis, there seems to be no definite association between the presence of Trichinella larvae in CSF and the symptoms or signs of CNS involvement.

Regarding the technological investigative methods (CT scan, angiogram, EEG), it was demonstrated that, in some cases, these may be of no diagnostic assistance and may add nothing to traditional and routine diagnostic strategies based on eosinophilia, erythrocyte sedimentation rate, or muscle biopsy (Ryczak et al., 1987).

Generally, patients are expected to survive trichinellosis with CNS manifestations, even though focal signs may persist for an uncertain period of time (Dalessio and Wolff, 1961). The outcome of the disease depends upon the severity of infection, adequacy of treatment, host immune competence, and seriousness of the injury produced by the parasites in the brain (Dalessio and Wolff, 1961). Moreover, Romanian authors reported that severe mental impairment developed in trichinellosis led patients to commit suicide (Olteanu et al., 1999; Enache, 2005).

Based on clinical evidences, it has been recommended that all patients with neurological complications of trichinellosis should be evaluated for silent myocardial injury as well (Fourestie et al., 1993; Schantz and Dietz, 2001).

In conclusion, to establish a correct diagnosis and to administer the specific therapy as soon as possible, trichinellosis must be considered in the differential diagnosis of any patient with encephalitis or other CNS malady of ambiguous etiology.

Footnotes

Disclosure Statement

No competing financial interests exist.

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