Content uploaded by Daofeng Tian
Author content
All content in this area was uploaded by Daofeng Tian on Mar 30, 2015
Content may be subject to copyright.
ORIGINAL PAPER
Clinical and Imaging Characteristics of Cerebral Schistosomiasis
Liquan Wu •Mingcan Wu •Daofeng Tian •Shijie Chen •Baohui Liu •
Qianxue Chen •Junmin Wang •Qiang Cai •Baowei Ji •Long Wang •
Shenqi Zhang •Dong Ruan •Xiaonan Zhu •Zhentao Guo
Published online: 25 September 2011
ÓSpringer Science+Business Media, LLC 2011
Abstract In recent years, there has been a trend for
increased incidence of cerebral schistosomiasis. It is often
misdiagnosed because of the diversity of clinical symp-
toms. We wished to explore clinical characteristics and
imaging findings in cerebral schistosomiasis. We retro-
spectively analyzed clinical data, laboratory tests, CT, and
MRI results in 11 patients with cerebral schistosomiasis.
All patients had chronic cerebral schistosomiasis (five with
epilepsy type, five with brain tumor type, and one patient
with stroke type). All patients with brain tumor type were
misdiagnosed as having gliomas. There were typical find-
ings on CT and MRI. In conclusion, clinical manifestations
of cerebral schistosomiasis are variable, and the rate of
misdiagnosis is high. For more precise diagnosis, a com-
bination of laboratory and imaging data is required.
Keywords Cerebral schistosomiasis Clinical
characteristics Imagining Diagnosis Treatment
Schistosoma japonicum Surgery Epilepsy
Introduction
Schistosomiasis is one of the most common parasitic
infections in the world [1]. The cerebral schistosomiasis is
the main manifestation of endometriotic lesion in schisto-
somiasis [2,3]. There are two main pathways by which
schistosomes cause cerebral schistosomiasis: egg embolism
and worm migration through either artery or vein system,
especially the valveless perivertebral Batson’s plexus.
Adult worms migrate through these pathways to central
nervous system (CNS) [4].
In recent years, there has been a trend for increased inci-
dence of the disease. Unfortunately, it is often misdiagnosed
because of the diversity of clinical symptoms [5]. Therefore, it
is important to enhance the knowledge of cerebral schisto-
somiasis. Here, we present the findings of a retrospective
analysis of clinical data, laboratory tests, and CT and MRI
results in 11 patients with cerebral schistosomiasis.
Materials and Methods
Patients
We analyzed data from 11 patients who were treated at
Renmin Hospital, Wuhan University between January 1998
and December 2004. The diagnosis was confirmed by
pathology (Division of Pathology of Renmin Hospital,
Wuhan University). There were nine male and two female
patients. The patients’ age ranged from 22 to 62 years
(average age of 39.2 years). Five patients were 20–40 years
old, three patients 40–50 years old, and three patients over
60 years old (Table 1).
Methods
All patients underwent blood, urine, and stool routine tests,
tests for liver and kidney function, electrolyte tests, indirect
hemagglutination (IHA) test, enzyme-linked immunosorbent
L. Wu D. Tian B. Liu Q. Chen (&)J. Wang Q. Cai
B. Ji L. Wang S. Zhang D. Ruan X. Zhu Z. Guo
Renmin Hospital, Wuhan University, 238 Jiefang Street,
Wuhan, Hubei 430060, China
e-mail: chenqx666@sohu.com
M. Wu S. Chen
Jingzhou First Hospital, First Affiliated Hospital of Yangtze
University, Jingzhou, Hubei 434000, China
123
Cell Biochem Biophys (2012) 62:289–295
DOI 10.1007/s12013-011-9294-1
test (ELISA), worm counts in stool, electrocardiogram, and
abdominal B ultrasound. Further, cerebrospinal fluid (CSF)
cytology, routine, biochemical, full immune, and parasite
inspection were also conducted. All patients had head CT and
MRI examinations; six patients underwent pathological
examination.
Results
Clinical Classification
Eight patients had been exposed to the schistosomiasis
endemic water, and three patients had previous episodes of
schistosomiasis before coming to the Hospital. Other
patients denied any exposure to the schistosomiasis ende-
mic water or previous history of schistosomiasis (Table 1).
All patients had chronic schistosomiasis, including epi-
lepsy type (five patients), brain tumor type (five patients),
and stroke type (one patient).
Clinical Manifestations
Clinical manifestations are presented in Table 2. Four
patients with epilepsy type had partial seizures, and one
patient had generalized tonic–clonic seizures without
increased intracranial pressure performance. Patients with
brain tumor type exhibited different symptoms of increased
intracranial pressure, such as headache or vomiting. Two
patients had swelling, three had seizures, and four patients
had uni- or bi-lateral limb weaknesses, and asymmetric
numbness. Two patients reported fuzzy or declining eye-
sight, and one patient reported decreased hearing and tin-
nitus. The patient with stroke type reported acute
headaches, fatigue, and walking instability. This patient
exhibited an active bilateral leg tendon reflex and active
signs of Romberg.
Laboratory Tests
The laboratory results are presented in Table 3. Routine
laboratory tests (urine and stool routine, liver and kidney
function, and electrolytes) were normal in all patients.
Further, the white blood cell count did not significantly
change from normal values. Four patients exhibited
increased percentage of eosinophils ([10%), and one
patient had 67% eosinophils. The albumin/globulin ratio,
an indicator of the liver function, was decreased in three
patients. One patient had elevated levels of transaminase.
Serum IHA or ELISA tests were positive in six patients,
and stool worm count was positive in two patients. Further,
abdominal B ultrasonic examination revealed liver schis-
tosomiasis in two patients; one patient had the left
liver lobe enlargement and another presented slight
spleen enlargement. Seven patients showed abnormal
Table 1 Characteristics of study patients
Number
of patients
%
Total patients 11
Male/female 9/2 81.8/18.2
20 to 40 years old 5 45.4
40 to 50 years old 3 27.3
Over 60 years old 3 27.3
Primary schistosomiasis 8 27.3
Recurrent schistosomiasis 3 72.7
Exposed to endemic water 8 72.7
Spontaneous 3 27.3
Table 2 Clinical manifestations
Type Clinical
manifestations
Number of
patients
Epilepsy type,
5 patients
Partial seizures 4
Generalized tonic–clonic seizures 1
Increased intracranial pressure 0
Brain tumor type,
5 patients
Increased intracranial pressure 5
Swelling 2
Seizures 3
Limb weaknesses 4
Fuzzy or declining eyesight 2
Decreased hearing and tinnitus 1
Stroke type,
1 patient
Acute headaches, fatigue,
and walking instability
1
Table 3 Laboratory tests
Laboratory tests Normal, number
of patients
Abnormal, number
of patients
Urine and stool routine 11 0
Liver and kidney function 11 0
Electrolytes 11 0
White blood cell count 11 0
Eosinophils 7 4
Albumin/globulin ratio 8 3
Transaminase 10 1
Serum IHA or ELISA tests 5 6
Stool worm count 9 2
Abdominal B ultrasonic 9 2
Liver lobe enlargement 10 1
Slight spleen enlargement 10 1
Electroencephalogram 4 7
290 Cell Biochem Biophys (2012) 62:289–295
123
electroencephalogram and one patient had explosive spike
and ware wave. Eleven patients had normal levels of CSF
glucose, chloride, and immune parameters. The IHA and
ELISA tests were positive in seven patients.
Imaging
The head CT manifestations were observed in five patients
with epilepsy type (Fig. 1a). Specifically, we observed
flake or nodular low-density areas in uni- or bi-lateral brain
parenchyma. Inside these areas, there were nodular foci
with enhanced density and without obvious strengthening.
Five patients with brain tumor type showed lesions which
mainly involved 1–3 brain lobes, especially the temporal
and parietal lobes (Fig. 2a). CT scans showed irregular
low-dense and isodense lesions that were mixed in the
focus area, as mixed boundary was not very clear. One
patient had calcification within the lesions. We further
observed irregular edema around lesions (Fig. 3a) and
manifestations of the ‘‘glove sign’’ with obvious mass
effect. The enhanced scan showed a solid mass in mixed-
density areas. This mass had a varying degree of a flake,
speckled, or nodular enhancement. Peripheral low-density
area was without any obvious enhancement. One patient
with stroke type showed multiple low densities in the alba,
and enhancement without reinforcement.
There were the following head MRI manifestations: five
patients with epilepsy type demonstrated a T1WI flake
lower signal and a T2WI slightly higher signal without
obvious edema around the lesions. The Gd-DTPA-
enhanced scan showed no obvious strengthening. Five
patients with brain tumor type demonstrated a large sheet
or mass-like abnormal T1WI low signal and a T2WI high
signal. In addition, a large finger-like or irregular-shaped
zone of edema was seen around lesions. The lateral ven-
tricle or quadrigeminal cistern were narrowly compressed,
and the midline structure shift was light to moderate. The
Gd-DTPA enhanced scan showed a scattered gyrus-like,
nodular, or irregular-shaped spots of strengthening. One
patient with stroke type showed an abnormal blade shape
T1WI low signal and a T2WI high signal in the right
frontal lobe. The boundary was less clear with the size
about 20 918 mm. The pairs of lateral ventricle were
slightly larger, the cerebral sulcus slightly wider. There
was no significant midline shift. The Gd-DTPA enhanced
scan had no obvious strengthening lesions. Representative
MRI images are shown in Figs. 1(epilepsy type), 2(brain
tumor type), and 3(stroke type).
Pathological Examination
Five patients with brain tumor type schistosomiasis were
pathologically diagnosed as having brain type schistosome
granulomas. One patient had a foreign body giant cell
reaction, one patient showed schistosome eggs and
inflammatory changes. One patient with epilepsy type
underwent stereotactic biopsy. The pathology showed a
large number of lymphocytes, epithelioid cells, small lob-
ulated white blood cells, and schistosome eggs.
Treatment and Prognosis
Five patients with brain tumor type were misdiagnosed as
having gliomas. The post-operative pathology revealed
brain schistosomiasis granulomas which were subsequently
resected. Two patients had only a partial surgical resection
because their lesions were located in important functional
area. These patients were then treated for 7 days with
praziquantel. The remaining six patients underwent routine
conservative treatment: a combination of praziquantel with
dehydration drugs to reduce intracranial pressure and anti-
epilepsy drugs. Praziquantel was administered for 2 days at
Fig. 1 a CT scan shows a large
low-density, ‘‘glove sign’’ zone
of edema and a cortical nodular
lesion of equal density in the
right temporal parietal lobe.
bMRI scan shows a large long
T2 signal area and an equally
long nodular lesion in the right
temporal parietal lobe, T2
cortex
Cell Biochem Biophys (2012) 62:289–295 291
123
10 mg/kg t.i.d. After 15 days, blood routine analysis,
serum IHA, ELISA, lumbar puncture and cerebrospinal
fluid routine, biochemistry, cytology, and a full set of
immunology, and parasite tests were repeated. If these
were positive, treatment with praziquantel was continued
for another 2 days.
Ten patients were followed for 1–4 treatment periods
(3 months–2 years after discharge from the hospital), and
one patient was lost for a follow-up. The laboratory tests
were negative in all patients. Clinical symptoms improved
or even disappeared. All patients underwent head CT scans.
The scans showed that lesions disappeared in four patients
and were significantly reduced in six patients (Fig. 4).
Discussion
Cerebral schistosomiasis can be divided into acute and
post-infection phases. Acute symptoms occur a few weeks
after contraction of infection; chronic symptoms occur
after being infected for 3 months to several years [6].
Chronic infections are more frequently seen. All eleven
patients in this report had chronic cerebral schistosomiasis.
Five patients exhibited epilepsy type of the disease. This
type is the most common in China. It is caused by eggs that
followed blood circulation to the meninges or cortex and
caused a limited meningoencephalitis. The seizure format
resembled limited epilepsy with non-intracranial hyper-
tension symptoms.
Five patients had brain tumor type. These patients
exhibited an intracranial space-occupying mass caused by
diffuse peripheral edema, neuronal degeneration, necrosis,
and glial cell proliferation due to the eggs. Clinically, this
type is often misdiagnosed as glioma, brain tuberculoma,
brain metastases, etc. These five patients underwent head
CT because of suspected glioma, followed by a visit to
neurosurgery.
One patient had stroke type of the disease. Patients with
this type showed cerebral infarction symptoms because of
the embolism of blood vessels caused by schistosome eggs.
Sometimes, these patients show stroke-like episodes. These
stroke symptoms should be differentiated from arterio-
sclerotic cerebrovascular disease which often manifests
with a history of hypertension, diabetes, and atherosclero-
sis. Patients with stroke symptoms who are younger and
live in endemic areas for schistosomiasis should be
Fig. 2 a CT scan; b,c,
denhanced MRI scan. Both
scans show multiple patchy,
sand-like, and nodular lesions in
right temporal parietal cortex
292 Cell Biochem Biophys (2012) 62:289–295
123
considered for differential diagnosis for this type of
schistosomiasis. There are also other rare types such as
spinal cord compression-type, multiple peripheral neuritis
type, the acute spinal cord inflammation type, etc.
Cerebral schistosomiasis is often caused by the schis-
tosome eggs deposited in the brain tissue [7], the eggs in
the portal venous system, or in the intracranial venous
sinus. The eggs in the portal venous system arrive into
intracranial tissues through communicating branches in the
left ventricle, or spinal vein, or portal vein system anas-
tomosis with the Baston vein [8].
CT scans in patients with epilepsy type showed large
irregular or patchy low-density areas with visible calcifica-
tion present most of the time; the mass effect was not obvi-
ous. Sometimes, local cortical atrophy could be seen. The
enhanced small nodules could also be seen in the enhanced
scan. CT scans in patients with brain tumor type showed
lesions mostly located under the cerebral cortex or in the
cerebellum which displayed a flaky, radiation-like, or a fin-
ger-like mixed-density area. Sometimes, high-density nod-
ules could be seen, as well as large ‘‘finger-like’’ or flaky
irregular edema areas around lesions, and the mass effect was
obvious. The enhanced scan showed cortical or subcortical,
spotted, sanded, or nodular enhancement. CT scans in the
stroke type patients showed small pieces of clear-border,
low-density lesions. The enhanced scan showed mostly no
enhancement, while some patients exhibited a gyrus-like
enhancement.
The MRI showed that lesions are mostly localized in the
cortex of the cerebral hemisphere, especially in the parietal
lobe and occipital lobe. Some lesions appeared in the cere-
bellum, brain stem, pia mater, and arachnoids. In the T1WI
image, the signal intensity was equal or slightly lower than
brain tissue, whereas the intensity of the T2WI image was
slightly higher than brain tissue. After injection of contrast
medium, multiple nodules with lump enhancement were
observed in clusters or scattered. These were regarded as
radiological changes of localizing and qualitative value. The
enhanced MRI image could also reveal irregular or small
roundish or ring-shaped, enhanced lesions. These lesions are
often localized in the cortex, or in the area where subcortical
gray matter meets white matter, or the cerebellum, or
brainstem. The lesions could occur alone or coincide with
cerebral hemispheres. A few lesions were not enhanced, and
large ‘‘finger-like’’ or irregular-shaped edema zone could be
seen around these lesions [9,10].
Fig. 3 a CT scan; cMRI scan;
b,denhanced scan. All scans
show a large low-density area of
edema in the right cerebellar
hemisphere. Further, CT- and
MRI-enhanced scan shows
patchy, sand-like, and nodular
lesions in the right cerebellar
hemisphere cortex
Cell Biochem Biophys (2012) 62:289–295 293
123
If CT or MRI does not unequivocally identify schisto-
somiasis, the diagnosis should be made in combination
with clinical history and laboratory examination [11]. If
necessary, the diagnosis can be made during treatment with
praziquantel; the diagnosis is confirmed when the lesion is
reduced under therapy.
In conclusion, clinicians should strengthen their aware-
ness of cerebral schistosomiasis. It is necessary to combine
the history of exposure to infected water, symptoms, signs
and etiology, serology, comprehensive analysis, and eval-
uation of imaging tests for early diagnosis and early
treatment of cerebral schistosomiasis [12–14].
References
1. Hayashi, M., Matsuda, H., Tormis, L. C., Nosenas, J. S., & Blas,
B. L. (1984). Clinical study on cerebral schistosomiasis japonica
on Leyte Island, Philippines: Follow-up study 6 years after
treatment with antischistosomal drugs. Southeast Asian Journal
of Tropical Medicine and Public Health, 15, 502–506.
2. Hayashi, M., Matsuda, H., Chigusa, Y., Kubota, T., & Matsu-
naga, K. (2002). Post-treatment follow-up studies on the clinical
features of Schistosomiasis japonica over a 35-year period in
Kofu district, Japan. Medical Tribune, 1, 35–57.
3. Ohta, N., Hayashi, M., Tormis, L. C., Blas, B. L., Nosenas, J. S.,
& Sasazuki, T. (1987). Immunogenetic factors involved in the
pathogenesis of distinct clinical manifestations of Schistosomiasis
japonica in the Philippine population. Transactions of the Royal
Society of Tropical Medicine and Hygiene, 81, 292–296.
4. Wang, P., Wu, M. C., Chen, S. J., Luo, G. C., Cheng, X. L., Zhu,
Z. S., et al. (2010). Research development of the pathogenesis
pathways for neuroschistosomiasis. Neuroscience Bulletin, 26,
168–174.
5. Ling, Y. J., Xu, S. S., & Li, Z. Q. (1995). Analysis of 8 cases of
cerebral schistosomiasis granuloma. Chinese Journal of Neuro-
surgery, 11, 301–302.
6. Miyazaki, I. (1991). An illustrated book of helminthic zoonoses (pp.
151–170). Tokyo: International Medical Foundation of Japan.
7. Mielcarek, N., Riveau, G., Remoue, F., Antoine, R., Capron, A.,
& Locht, C. (1998). Homologous and heterologous protection
after single intranasal administration of live attenuated recombi-
nant Bordetella pertussis.Nature Biotechnology, 16, 454–457.
8. Chen, M. (1999). Progress in schistosomiasis control in China.
Chinese Medical Journal (England), 112, 930–933.
9. Shu, K., Zhang, S., Han, L., & Lei, T. (2009). Surgical treatment
of cerebellar schistosomiasis. Neurosurgery, 64, 941–943.
10. Liu, H., Lim, C. C., Feng, X., Yao, Z., Chen, Y., Sun, H., et al.
(2008). MRI in cerebral schistosomiasis: Characteristic nodular
enhancement in 33 patients. AJR American Journal of Roent-
genology, 191, 582–588.
11. George, J., Rose, D., Hazrati, L. N., Majl, L., & Hodaie, M.
(2009). Cerebral schistosomiasis—an unusual presentation of an
intracranial mass lesion. Canadian Journal of Neurological Sci-
ences, 36, 244–247.
Fig. 4 a CT scan shows a large
‘‘glove sign’’ area of edema, a
nodular lesion of equal density
in the left temporal lobe. bCT
enhanced scan shows multiple
nodular enhanced lesions in the
junction area with the gray
matter. cCT scan shows that
nodules are disappeared and
edema is reduced after 2 months
of anti-schistosomiasis
treatment. dCT scan shows
disappearance of edema and the
presence of mild brain atrophy
after 2 months of anti-
schistosomiasis treatment
294 Cell Biochem Biophys (2012) 62:289–295
123
12. Carod-Artal, F. J. (2008). Neurological complications of schis-
tosoma infection. Transactions of the Royal Society of Tropical
Medicine and Hygiene, 102, 107–116.
13. Roberts, M., Cross, J., Pohl, U., Lucas, S., & Dean, A. (2006).
Cerebral schistosomiasis. Lancet Infectious Disease, 6, 820.
14. Betting, L. E., Pirani, C., Jr., de Souza, Q. L., Damasceno, B. P.,
& Cendes, F. (2005). Seizures and cerebral schistosomiasis.
Archives of Neurology, 62, 1008–1010.
Cell Biochem Biophys (2012) 62:289–295 295
123
