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Am. J. Trop. Med. Hyg., 68(3), 2003, pp. 281-285
Copyright © 2003 by The American Society of Tropical Medicine and Hygiene

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EOSINOPHILIC MENINGITIS CAUSED BY ANGIOSTRONGYLUS CANTONENSIS ASSOCIATED WITH EATING RAW SNAILS: CORRELATION OF BRAIN MAGNETICRESONANCE IMAGING SCANS WITH CLINICAL FINDINGS

HUNG-CHIN TSAI, YUNG-CHING LIU, CALVIN M. KUNIN, PING-HONG LAI, SUSAN SHIN-JUNG LEE, YAO-SHEN CHEN, SHUE-REN WANN, WEI-RU LIN, CHUN-KAI HUANG, LUO-PING GER, HSI-HSUN LIN, AND MUH-YONG YEN
Section of Infectious Diseases, Department of Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; National Yang-Ming University, Taipei, Taiwan, Republic of China; Department of Internal Medicine, Ohio State University, Columbus, Ohio; Department of Radiology, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan; Department of Medical Research, Kaohsiung General Veterans Hospital, Kaohsiung, Taiwan; Graduate Institute of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan


ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Angiostrongylus cantonensis is the most common cause of eosinophilic meningitis worldwide. Human infection occurs after ingestion of the worms in raw snails or fish that serve as intermediate hosts. Two outbreaks of central nervous system infection with A. cantonensis occurred in Kaoshiung, Taiwan, during 1998 and 1999 among Thai laborers who ate raw snails. A detailed clinical studies of 17 of these patients was conducted, including study of 13 patients who underwent magnetic resonance imaging (MRI) scans of the brain. The MRI scans revealed high signal intensities over the globus pallidus and cerebral peduncle on TI-weighted imaging, leptomeningeal enhancement, ventriculomegaly, and punctate areas of abnormal enhancement within the cerebral and cerebellar hemisphere on gadolinium-enhancing T1 imaging, and a hyperintense signal on T2-weighted images. There was a significant correlation between severity of headache, cerebrospinal fluid (CSF) pleocytosis, and CSF and blood eosinophilia with MRI signal intensity in T1-weighted imaging (P < 0.05). Eosinophilic meningitis produced by A. cantonensis needs to added to the list of causes of hyperintense basal ganglia lesions found on T1-weighted MRI scans in tropical countries.


INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Angiostrongylus cantonensis, also known as the rat lung worm, is the most common cause of eosinophilic meningitis worldwide. This parasitic infection is endemic in the Southeast Asian and Pacific regions. The intermediate hosts are raw fish and snails. The typical clinical presentation is acute meningitis with an eosinophilic pleocytosis frequently accompanied by encephalopathy. The pathological findings in the central nervous system (CNS) include the following: 1) meningitis with a predominance of eosinophils and plasma cells, 2) tortuous tracks of various sizes in the brain and spinal cord surrounded by an inflammatory reaction and degenerating neurons, 3) granulomatous response to the dead parasites, and 4) nonspecific vascular reactions including thrombosis, rupture of vessels, arteritis, and aneurysm formation.1 The brain computed tomographic (CT) scan can be normal or can reveal cerebral edema, ventricular dilatation, or enhancing ring or disc lesions, resembling tuberculomas.2–6 The features of the brain MRI scan were previously limited to a few case reports.7–9 These revealed vascular thrombosis, tortuous tracts in the vicinity of small vascular lesions, adjacent tissue reaction, and meningeal enhancement.1,10

Two outbreaks of eosinophilic meningitis caused by A. cantonensis infection occurred in Kaohsiung, Taiwan, during 199811 and 1999.12 Seventeen Thai laborers who developed severe headache or meningitis after eating raw snails (Ampullarium caniculatus) were admitted to Kaohsiung Veterans General Hospital during this period. The diagnosis was established by serological methods.13 Third-stage larvae were found in the cerebrospinal fluid (CSF) in 2 patients. In this report, we describe the association between the clinical features of the patients and the MRI findings.


MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A detailed history was obtained from each patient; we included questions concerning foods eaten just before the outbreak. The incubation period was calculated from the time of ingestion of the putative source to onset of symptoms. Physical examination included neurologic and ophthalmic assessment. Cerebrospinal fluid was examined for cells, protein, glucose, and larvae. Laboratory tests included a complete blood cell and differential count, liver and renal function tests, creatinine phosphokinase levels, immunoglobulin E, and an indirect hemagglutination test for amoeba. Stools were examined for parasites and amebic trophozoites. Cranial MRI scans were performed with a 1.5-T imager (General Electric, Waukesha, Wisconsin). Intravenous administration of gadolinium-diethylenetriamine pentaacetic acid (Berlix Laboratories, Richmond, CA) in a dose of 0.1 mmol/kg on T1 imaging was used to visualize abnormal enhancement of the meninges and cerebrum. One patient (patient 9) underwent brain CT scan to exclude calcification as the cause of hyperintense basal ganglion lesions (Figure 1Go). The headache intensity in the second outbreak was rated on a 4-point scale ranging from none to severe (0 = none, 1+ = mild, 2+ = moderate, 3+ = severe).14 The hyperintense basal ganglia lesion on T1-weighted MRI was also graded as a 4-point scale ranging from none to severe by 2 independent radiologists. Blood and CSF manganese concentrations were determined during the second outbreak by the method described by Laker.15



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  		    FIGURE 1. Computed tomographic scan of the brain revealing absence of calcification over the bilateral basal ganglion (patient 9).

 
Spearman correlation (2 tailed) was used to analyze the correlation between the severity of headache, CSF findings, eosinophilia, and distribution of MRI signal intensities.


RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
All 17 patients in the current series were young Thai men (aged 23–39 years). They had worked as laborers in Taiwan for at least 5 months (range, 5 months to 2 years). The source of epidemic was ingestion of raw snails seasoned with lemon juice and red pepper. The incubation period ranged 4–23 days (mean ± SD, 13.36 ± 6.6 days). All had elevated levels of immunoglobulin E. Patients in the first outbreak in 1998 (patients 1–8) responded well to treatment with mebendazole and glucocorticosteroids. Patients in the second outbreak in 1999 (patients 9–17) only received supportive therapy. Two of these patients had demonstrable larvae in the CSF. Only 2 patients developed focal neurological deficits consisting of a transient facial palsy and abducens nerve palsy. Brain MRI scan was performed in 4 of the 8 patients during the first outbreak in 1998 because of severe or persistent CNS symptoms. The only finding was leptomeningeal enhancement. The MRI scan of the brain was performed in all of the 9 patients during the second outbreak. These studies revealed leptomeningeal enhancement and varying degrees of high signal intensities bilaterally in the globus pallidus and cerebral peduncle on T1-weighted imaging (Figures 2Go–5Go).



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  		    FIGURE 2. Axial T1-weighted magnetic resonance imaging scan with contrast disclosing meningeal enhancement (patient 9).

 


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  		    FIGURE 5. T1-weighted magnetic resonance imaging scan revealing increased signal intensity within the cerebral peduncle (patient 9).

 
The severity of headache, CSF findings, eosinophilia, and findings in the brain MRI scan are listed for each patient in Table 1Go. There was a significant correlation between severity of headache, CSF pleocytosis, CSF, and blood eosinophilia with MRI signal intensity in T1-weighted MRI (P < 0.05) (Table 2Go). The 2 patients found to have larvae in the CSF had more marked high intensity signals in globus pallidus bilaterally. Serum and CSF manganese concentrations were normal in all patients studied. Follow-up MRI studies 3 months later were available in 4 of the 9 patients from the second epidemic (patients 9–12). Two patients (patients 9 and 11) showed a reduction of the high signal intensity in the globus pallidus bilaterally, on T1-weighted image; but no changes were seen in the other 2 patients (Figure 6Go).


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TABLE 1
Severity of headache and laboratory and magnetic resonance imaging scan finding in 17 cases of eosinophilic meningitis caused by Angiostrongylus cantonensis*
 

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TABLE 2
Correlation of the severity of headache and laboratory findings with magnetic resonance imaging scan signal intensity in the globus pal lidus in 9 cases of eosinophilic meningitis caused by Angiostrongy lus cantonensis
 


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  		    FIGURE 6. Axial T1-weighted magnetic resonance imaging scan revealing mildly decreased signal intensity within the globus pallidus and cerebral peduncle 3 months later (patient 9).

 

DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
A previously undescribed nematode in the lungs of wild rats was reported by Professor H. T. Chen in the vicinity of Canton, China, in 1933.16 The name, Pulmonema cantonensis, was changed to Angiostrongylus cantonensis in 1946 for taxonomic reasons. Nomura and Lin reported the first human case of eosinophilic meningitis caused by A. cantonensis in Tainan, Taiwan, in 1945.17,18 The patient was a 15-year-old boy. He was found to have 10 worms in the CSF and died as a result of the infection. This case was followed by numerous reports in the literature.19–22

Angiostrongyliasis can present with protean clinical manifestations. The most common is diffuse eosinophilic meningoencephalitis produced in response to young worms in the subarachnoid space. The CT scan of the brain can be normal or can reveal nonspecific findings, including cerebral edema, ventricular dilatation,2–5 or enhancing ring or disc lesions, resembling a tuberculoma.6 The MRI features are limited in the English-language literature to 3 case reports.7–9 Noskin and others7 reported a 27-year-old woman who presented with a 2-week history of generalized pruritus, myalgia, and arthralgia associated with fever, headache, and nausea and vomiting after returning to the U.S. mainland from Hawaii. Analysis of the CSF revealed 294 cells/mm3 with 80% lymphocytes, 14% monocytes, and 6% eosinophils. The CSF total protein was 102 mg/dL. The MRI scan of the brain revealed nothing abnormal. Hsu and others8 described a 10-month-old girl presenting with fever and cough for 3 weeks. Examination of CSF revealed eosinophilic pleocytosis. The diagnosis was established by serology. A brain MRI scan revealed hyperintense signals throughout the cerebral cortex and ventriculomegaly on T2-weighted images. Gadolinium contrast studies revealed enhanced meninges and punctate areas within the cerebral cortex and the cerebellar hemispheres. The authors interpreted the findings as cerebral edema secondary to disruption of the blood-brain barrier with small areas of infarction caused by vasculitis, and leptomeningitis secondary to direct tissue damage from the worms or their products. Kanpittaya and others9 reported the clinical features and the findings revealed by MRI and magnetic resonance spectroscopy in 6 patients with eosinophilic meningoencephalitis caused by A. cantonensis. They found that the abnormal findings on MRI scans included prominence of the Virchow-Robin spaces, subcortical enhancing lesions, and abnormal high T2 signal lesions in the periventricular regions. They believed that the MRI studies were of diagnostic value and were helpful in understanding the pathogenic mechanisms of the disease.

All of the 13 Thai laborers who underwent MRI studies in the current series were found to have nonspecific meningeal enhancement. The increased bilateral signals in globus pallidus on T1-weighted MRI scan were observed only in the 9 patients in the second outbreak. The relative hyperintense signal on T1-weighted imaging in the cerebral peduncles were noted in only 2 patients (patients 9 and 10). It is possible that they may have had more worms. This notion is supported by the finding of worms in the CSF of 2 patients (patients 9 and 10) in the second outbreak and the significant correlation between severity of headache, CSF pleocytosis, CSF and blood eosinophilia, and signal intensity in the globus pallidus. Although patients in the first outbreak appeared to have higher CSF and blood eosinophils, this may not represent a greater infection severity because the most abnormal data were shown rather than the initial data at presentation, as in the second outbreak. It is difficult to compare the MRI findings between the 2 outbreaks because not every patient in the first outbreak underwent an MRI scan, and these imaging studies were performed at different points in time.

The presence of hyperintense T1-weighted MRI basal ganglia abnormalities is relatively nonspecific. It may be produced by a variety of noninfectious causes, such as deposition of calcium and lipids, hemorrhage, infarction, hypermagnesemia, parenteral nutrition, neurofibromatosis, hypoxic ischemic encephalopathy, and chronic hepatic failure.23–26 None of these conditions was present among the otherwise healthy Thai laborers in this series. Accordingly, CNS infection with A. cantonensis needs to be included in the differential diagnosis of basal ganglia abnormalities seen on MRI scans in tropical countries. Angiostrongylus cantonensis may produce substances or some immune mediators with a high affinity for the bilateral globus pallidus. Further studies in animals and humans are needed to confirm this notion.

In summary, the MRI findings in CNS infection with A. cantonensis are nonspecific, ranging from normal to leptomeningeal enhancement, ventriculomegaly, punctate area of abnormal enhancement, and hyperintense signal lesions on T2-weighted images. There appears to be a special predilection for involvement of the globus pallidus and cerebral peduncle in some patients. This is correlated with presence of worms in the CSF, severity of headache, CSF pleocytosis, and CSF and peripheral eosinophilia. Angiostrongyloidiasis needs to be considered in patients with eosinophilic meningitis associated with brain MRI abnormalities in tropical countries.





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  		    FIGURE 3. A, Axial T1-weighted magnetic resonance imaging (MRI) scan (600/20, TR/TE) revealing markedly increased signal intensity within the globus pallidus (patient 9). B, Axial T1-weighted MRI scan revealing moderately increased signal intensity within the globus pallidus (patient 10). C, Axial T1-weighted MRI scan revealing mildly increased signal intensity within the globus pallidus (patient 14).

 


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  		    FIGURE 4. T1-weighted magnetic resonance imaging scan revealing increased signal intensity within the globus pallidus (patient 9).

 

Received June 19, 2001. Accepted for publication November 18, 2002.

Authors’ addresses: Hung-Chin Tsai, Yung-Ching Liu, Susan Shin-Jung Lee, Yao-Shen Chen, Shue-Ren Wann, Wei-Ru Lin, Chun-Kai Huang, Hsi-Hsun Lin, and Muh-Yong Yen, Section of Infectious Diseases, Department of Medicine, Kaohsiung Veterans General Hospital, 386 Ta-Chung 1st Road, Kaohsiung, Taiwan, National Yang-Ming University, Taipei, Taiwan, Republic of China, Calvin M. Kunin, Department of Internal Medicine, Ohio State University, Room M110 Starling Loving Hall, 320 W 10th Avenue, Columbus, OH 43210. Ping H. Lai, Department of Radiology, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan. Luo-Ping Ger, Department of Medical Research, Kaohsiung General Veterans Hospital, Kaohsiung, Taiwan. Hung-Chin Tsai, Graduate Institute of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan.

Reprint requests: Yung-Ching Liu, Section of Infectious Diseases and Department of Medicine, Kaohsiung Veterans General Hospital, 386 Ta-Chung 1st Road, Kaohsiung, Taiwan, Telephone: 886-7-3468096, Fax: 886-7-3468292, E-mail: ycliu{at}isca.vghks.gov.tw


REFERENCES
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 ABSTRACT
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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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