Toxocar iasis of the centr al ner vous system: with r epor t of two cases
Toxocaríase do sistema nervoso central: com descrição de dois casos
Sandr a F. Mo r eir a- Silva
1, Mur ilo G. Ro dr igues
1, Jo ão L. Pimenta
1,
Camila P. Go mes
1, Lar issa H. Fr eir e
1and Fausto E.L. Per eir a
2ABSTRACT
Clinica l invo lve m e nt o f the ne rvo us syste m in visce ra l la rva m igra ns due to
Toxocara
is ra re , a ltho ugh in e xpe rim e nta l a nim a ls
the la rva e fre q ue ntly m igra te to the b ra in. A re vie w o f the lite ra ture fro m the e a rly 50’s to da te fo und 29 ca se s o f b ra in
invo lvem ent in to xo ca ria sis. In 20 ca ses, va rio us clinica l a nd la bo ra to ry m a nifesta tio ns o f eo sino philic m eningitis, encepha litis,
m ye litis o r ra diculo pa thy we re re po rte d. We re po rt two childre n with ne uro lo gica l m a nife sta tio ns, in which the re wa s
ce re b ro spina l fluid ple o cyto sis with m a rk e d e o sino philia a nd a po sitive se ro lo gy fo r
Toxoc ara
b o th in se rum a nd CSF. Se ro lo gy
for Sc histosoma mansoni
,
Cystic erc us c ellulosae, Toxoplasma
a nd c yto m e ga lo virus
we re ne ga tive in CSF, tha t wa s ste rile in b o th
ca se s. Im pro ve m e nt o f signs a nd sym pto m s a fte r spe cific tre a tm e nt ( a lb e nda zo le o r thia b e nda zo le ) wa s o b se rve d in the two
ca se s. A sum m a ry o f da ta de scrib e d in the 25 ca se s pre vio usly re po rte d is pre se nte d a nd we co nclude tha t in ca se s o f
e nce pha litis a nd m ye litis with ce re b ro spina l fluid ple o cyto sis a nd e o sino philia , pa ra sitic infe ctio n o f the ce ntra l ne rvo us
syste m sho uld b e suspe cte d a nd se ro lo gy sho uld b e pe rfo rm e d to e sta b lish the co rre ct dia gno sis a nd tre a tm e nt.
Ke y-words:
To xo ca ria sis.
Toxoc ara c anis. Eosinophilic meningitis. Eosinophilic enc ephalitis.
RESUMO
En vo lvim e n to do siste m a n e rvo so , c o m m a n ife sta ç õ e s c lín ic a s, n a in fe c ç ã o pe lo
Toxoc ara
é ra ro , e m b o ra , n o s m o de lo s
e xpe rim e n ta is a la rva fre q ü e n te m e n te se lo c a lize n o siste m a n e rvo so c e n tra l. Um a re visã o da lite ra tu ra a pa rtir de 1956,
q u a n do a sín dro m e fo i de sc rita , a té 2002, m o stro u a pu b lic a ç ã o de 29 c a so s de n e u ro to xo c a ría se , do s q u a is e m 20 ha via
re la to de a lte ra ç õ e s c línic a s e la b o ra to ria is indic a tiva s de m e ningite , o u e nc e fa lite , o u m ie lite o u ra dic ulite e o sino fílic a s.
Ne ssa c o m u n ic a ç ã o e sta m o s re la ta n do o b se rva ç õ e s e m du a s c ria n ç a s q u e a pre se n ta ra m sin a is e sin to m a s n e u ro ló gic o s,
co m ple o cito se e e o sino filia a ce ntua da no líq uo r e co m so ro lo gia po sitiva pa ra
Toxoc ara
no so ro e no liq uo r. So ro lo gia pa ra
Sc histosoma mansoni
,
Cystic erc us c ellulosae
,
Toxoplasma
e cito m e ga lo virus fo ra m ne ga tiva s no liq uo r, q ue e ra e sté ril no s do is
c a so s. Ho u ve m e lho ra do s sin a is e sin to m a s a pó s o tra ta m e n to e spe c ífic o ( a lb e n da zo l e tia b e n da zo l) n o s do is c a so s. É
a pre se nta do um sum á rio do s princ ipa is a c ha do s no s c a so s re la ta do s na lite ra tura e se c o nc lue q ue e m c a so s de m e ningite ,
e n c e fa lite o u m ie lite c o m líq u o r a pre se n ta n do ple o c ito se c o m e o sin o filia a c e n tu a da , a su spe ita de in fe c ç ã o pa ra sitá ria
de ve se r le va nta da , se ndo ne c e ssá rio so ro lo gia e spe c ific a pa ra dia gnó stic o e tra ta m e nto a de q ua do s.
Palavr as-chave s:
Toxoc aríase
. To xo c a ra c a nis. Me ningite e o sino fílic a . Enc e fa lite e o sino fílic a .
1 . Hospital Infantil Nossa Senhora da Glória, Vitória, ES. 2 . Núc leo de Doenç as Infec c iosas do Centro B iomédic o da Universidade Federal do Espirito Santo, Vitória, ES.
Addr e ss to: Dr. Fausto E.L. Pereira. Núc leo de Do enç as Infec c io sas/CB M/UFES. Av. Marec hal Campo s 1 4 6 8 , 2 9 0 4 0 -0 9 1 Vitó ria, ES, B rasil. Fax: 5 5 2 7 2 3 5 -7 2 0 6
e-mail: felp@ ndi.ufes.br
Rec ebido para public aç ão em 4 /4 /2 0 0 3 Ac eito em 1 6 /2 /2 0 0 4
The expression visc eral larva migrans was first used by
Beaver
5to desc ribe the syndrome assoc iated with any infec tion
c aused by paratenic nematode larvae that migrate through
organs. Although no consensus has been reached, some authors
include the unusual migration of any nematode larvae, including
those that naturally infec t humans, as visc eral larva migrans
4 4.
The syndr o me is typic ally e xpr e sse d b y fe ve r, pe r siste nt
eosinophilia, hepatomegaly and pulmonary symptoms and
usually results in a benign self-limited c ourse
5.
Central nervous system involvement in visceral larva migrans
syndrome is usually infrequent, but frequency can vary with different
species of migrating larvae. Clinical involvement of the nervous
system in visceral larva migrans due to
To xo ca ra
is rare, although
The frequenc y and loc alization of
To xo c a ra
larvae in the
c entral nervous system in humans is unknown. Autopsy studies
of isolated cases have revealed
Toxocara
larvae in leptomeninges
7,
gray and white matter of c erebrum and c erebellum
1 5 2 6 2 7 4 0 ,thalamus
4and spinal c ord
7. Most of these c ases did not present
c linic al ne ur o lo gic al signs. Fo r this r e aso n the c linic al
signific anc e and true frequenc y of c erebral loc alization of
To xo c a ra
larvae in non-fatal c ases remain unc lear. At the
Children’s Hospital Nossa Senhora da Glória, in Vitoria, where
the frequenc y of positive serology for
To xo ca ra
is around 3 0 %
of admissions
2 8, the frequenc y of granulomas due to larva
migrans in the c entral nervous system was 0 .6 8 % in a random
sample of 3 0 8 autopsies of c hildren 1 to 1 5 years old ( Musso et
al: unpublished data)
Lewis et al
2 0reviewed 5 8 c ases of visc eral larva migrans
syndrome and found mention of c onvulsions in only three
patients. In a c ase c ontrol study Magnaval et al
2 2demonstrated
that
To xo c a ra
infec tion is not assoc iated with a rec ognizable
neurologic al syndrome, although several c ases had a positive
Western blot for both c erebrospinal fluid and serum. However
a signific ant assoc iation between seizures and positive serology
for
To xo c a ra
has been reported in Italy
1and in B olivia
2 9.
A r e vie w o f the lite r atur e fr o m the e ar ly 5 0 ’s to the
pr e s e n t da te fo un d 2 9 c a s e s o f b r a in in vo lve m e n t in
toxoc ariasis
2 3 4 7 8 1 1 1 2 1 3 1 4 1 5 1 7 1 9 2 6 2 7 3 0 3 1 3 4 3 5 3 7 3 8 3 9 4 0 4 3 4 5 4 7 4 8 4 9.
Of these 2 8 c ases, 2 0 reported different c linic al and laboratory
manifestations of eosinophilic meningitis, encephalitis, myelitis
or radic ulopathy ( the main data of eac h reported c ase are
summarized in Table 1 ) . Here we report two c ases of
To xo ca ra
infec tion in whic h the most prominent manifestations were
neurological, with cerebrospinal fluid eosinophilia and positive
serology for
To xo c a ra
in both serum and c erebrospinal fluid.
CASE REPORTS
Case 1
- A five-year-old girl was admitted with a four day
flu-like, febrile illness, whic h was treated with aspirin. Three days
later the c hild c omplained of abdominal pain and was vomiting
with bloody streaks. After admission, endosc opy revealed ac ute
hemorrhagic gastritis and the child received ranitidine. Five days
after admission the c hild was lethargic , with slurred speec h,
nystagmus, right c onvergent squint and left deviation of labial
c ommissure. There was paresis of both inferior and superior
members, nuc hal rigidity and bilateral Kernig and Lasègue
responses. There were right paralyses of the VI, VII and XII
c ranial nerves, urinary retention and fec al inc ontinenc e. The
cerebrospinal fluid contained: 54mg/dL glucose, 31mg/dL protein
and 1 8 7 leukoc ytes/ul ( 2 % monoc ytes, 4 1 % lymphoc ytes and
5 7 % e o sino phils) . The white b lo o d c e ll c o unt was 4 9 0 0
leukoc ytes/ul ( band neutrophils 7 9 /ul, neutrophils 4 5 8 2 /ul,
eosinophils 7 1 1 /ul, lymphoc ytes 2 3 7 0 /ul, monoc ytes 1 5 8 /ul) .
The blood and c erebrospinal fluid were sterile and bec ause of
the high level of eosinophils in the cerebrospinal fluid, a hypothesis
o f a par asitic m e ningo e nc e phalitis was pr o po se d. Sto o l
examinations revealed larvae of
Stro ngylo ide s ste rco ra lis
, but
were negative for other helminths in the five samples examined.
Treatment with thiabendazole was initiated. A second lumbar puncture
was performed three days after the first puncture, and the results
were similar, with a marked eosinophilic pleocytosis. Serology for
Toxocara
( ELISA IgG with secretory-excretory antigen) was positive
in both the serum and cerebrospinal fluid. Serology for
Schistosom a
m ansoni
,
Cysticercus cellulosae
and toxoplasmosis were negative
in the cerebrospinal fluid. Cranial MRI ( performed 25 days after
admission) showed small irregular lesions situated in the posterior
portion of the spine-bulbar transition and pedunculus cerebellaris,
with hyperintense signal in T2 and DP, but intermediary signal in T1.
There was no enhancement after intravenous contrast, nor were
there signs of tissue compression. An inflammatory lesion was
suggested, most likely produced by
Toxocara
larvae. After 14 days of
thiabendazole the child received albendazole for 10 days. Improvement
was evident after the use of albendazole. The child was discharged 36
days after admission with discrete dysarthria and dysmetria and a
mild paresis of VI and VII cranial nerves. Six months later the child
presented without neurological manifestations.
Case 2 -
A five-year-old boy was admitted with palsy of the
inferior limbs and urinary retention. Cerebrospinal fluid was clear
with 63 mg/dL glucose, 17.5mg/dL proteins and 23 leukocytes/ul
( 3% neutrophils, 57% eosinophils, 25% lymphocytes and 15%
monocytes) . The total leukocyte count was 22100/ul( 442 myelocytes,
221 metamyelocytes, 1547 band neutrophils, 15028 neutrophils,
2 2 1 eosinophils, 4 1 9 9 lymphoc ytes, 4 4 2 monoc ytes) . Fec al
examination was negative ( five samples) . Cerebrospinal fluid was
sterile and presented negative serology for toxoplasmosis,
Schistosom a m ansoni
and
Cysticercus cellulosae
. Corticotherapy
was started until a positive serology for
To xo ca ra
was detected in
both the serum and cerebrospinal fluid. Corticotherapy was replaced
with thiabendazole for 15 days. Diagnosis of possible transverse
myelitis produced by
To xo ca ra la rva e
was noted. The child was
discharged 34 days after admission with partial improvement of
palsy. One month later the palsy had disappeared, and the child
presented no signs of sequelae.
DISCUSSION
In both cases reported here there were signs of neurological
lesions and pleocytosis with eosinophilia in sterile cerebrospinal
fluid. In Case 1 MRI showed lesions in the spine-bulbar border
and in the pedunc ulus c erebellaris. The loc alization of these
lesions was compatible with the clinical manifestations. In Case 2
image examination was not performed. Sterile cerebrospinal fluid,
with pleoc ytosis and marked eosinophilia, was an indic ation of
the possible parasitic origin of the neural and meningeal lesions,
reinforc ed by the positive serology for
To xo ca ra
.
Neural involvement by
To xo c a ra la rva e
is highly probable
in both c ases if one takes into ac c ount: a) c erebrospinal fluid
pleocytosis with marked eosinophilia; b) positive serology, with
IgM anti-
To xo ca ra
, in both serum and c erebrospinal fluid, and
negative serology for
Sc histo so m a m a nso ni
and
Cystic e rc us
c e llu lo sa e
( parasites that reac h the nervo us system mo st
Ta b le 1- Sum m a ry o f ca se s o f ne uro to xo ca ria sis re po rte d fro m 1956 to 2002.
Author Age/Gender Summary of main observations
Ca se s studie d a t a uto psy
1 -Dent et al 1 9 5 6 7 1 .5 /M Multiple granulomas with larvae in CNS
2 -VanThiel 1 9 6 04 7 6 .0 /M Granuloma with larvae ( cerebellum) *
3 -Moore 1 9 6 2 2 7 2 .0 /M Granuloma with larvae ( cerebellum and medulla)
4 -Schoenfield et al 1 9 6 43 9 5 .0 /M Multiple granuloma and larvae in CNS*
5 -Beautyman et al 1 9 6 64 6 .0 /F Granuloma with larvae ( thalamus)
6 -Schochet et al 1 9 6 74 0 2 .0 /M Multiple granulomas with larvae in CNS*
7 -Mikhael et al 1 9 7 42 6 1 .5 /M Multiple granulomas with larvae in CNS*
8 -Hill et al 1 9 8 51 5 2 .5 /F Larvae ( cerebrum, cerebellum and pons)
9 -Nelson J et al 1 9 9 03 0 3 .0 /M Larvae and granulomas ( cerebrum and liver)
Cases with clinical data
1 -Sumner & Tinsley 1 9 6 74 6* 5 7 /F
2 -Kapur et al 1 9 7 61 7 * * 2 2 /M
3 -Engel et al1 1 1 9 6 7 2 5 /M
4 -Anderson et al 1 9 7 52 1 .5 /F
5 -Wang et al 1 9 8 34 9 4 3 /F
6 -Gould et al 1 9 8 51 4 1 1 /F
7 -Russeger & Schmutzhard 1 9 8 93 7 5 5 /F
8 -Ruttinger & Hadidi 1 9 9 13 8 2 6 /F
9 -Fortenberry et al 1 9 9 11 2 1 /M
1 0 -Sellal et al 1 9 9 24 1 2 4 /F
1 1 -Villano et al 1 9 9 24 8 5 3 /F
1 2 -Sommer et al 1 9 9 44 3 4 8 /M
Mental confusion. Bilateral extensor plantar responses. CSF: normal. Blood: 4606 eosinophils/
µ
l. Liver biopsy: eosinophilic granuloma with nematode larva ( 6 0 4 um length and 5 4 mm wide) . Serology for To xo ca rawas not performed.
B e h a vio r c h a n ge s , de c r e a s e d c o n s c io us n e s s , hyperreflexia. Nematode larva identified in brain ( biopsy) .
Meningomyelitis. CSF 8 0 c ells/
µ
l1 7 % eosinophils. Precipitating anti-To xo ca ra antibodies in the serumProgressive weakness of right arm and leg. Blood e o sino phils: 5 2 2 0 /
µ
l. CSF: 3 5 6 c e lls/µ
l, 8 0 % eosinophils. Serology for To xo ca ra positive in blood and CSF.Ac ute retention of urine. Nec k rigidity, lower limb weakness, brisk tendon reflexes and flexor plantar responses. CSF 8 d after admission: 5 2 cells/
µ
l 9 5 % lym pho c yte s. Lar va c o m patib le with To x o c a radetected in the CSF. Improvement after treatment with thiabendazole.
Pronounced meningism: Kernig’s sign positive and generalized hyperreflexia. CT scan was normal. CSF: 150 cells/3 0 % eosinophils. Blood: 1 3 0 0 eosinophils/
µ
l. Serology positive for Toxocara. Although spontaneous recovery the patient was treated with diethylcarbamazine.Severe paraparesis. Myelography: space occupying le sio n T7 - T1 1 . CSF: 1 7 7 c e lls/
µ
l. B lo o d: 2 9 1 eosinophils/µ
l. Positive serology for To xo ca ra in the blood. Epithelioid granuloma with foreign body type giant cell in the biopsy.Epileptic seizures. MRI: multiple hyperintense, irregular lesions in CNS. B lood eosinophils: 5 4 6 c ells/ml. Serology positive in the blood and negative in the CSF.
Recurrent seizures, truncal ataxia and lethargy. Blood eosinophils: 3 0 0 0 -1 7 0 0 0 /
µ
l. Serology positive in the blood.Paresthesis of legs. Positive serology in blood and CSF. Blood eosinophils: 1 5 0 0 /
µ
l. CSF: 50 cells/µ
l, 1 0 % eosinophils.Four-year history of progressive spastic tetraparesis and hypoanesthesia in four limbs and trunk. CT scan: complete C4 block like intradural and extra spinal-cord expansive process. Surgical removal of fibrotic tissue in ar ac hno ide a. Histo patho lo gy sho we d chronic granulomatous inflammation with To xo ca ra
larvae
Ataxia, rigor and neuropsychological disturbances. CT scan and MRI: diffuse and circumscribed lesions in white matter. Positive serology for To xo ca ra in the blood.
with albendazole and thiabendazole. Furthermore,
To xo c a ra
infection is frequent in children that are treated at the Children’s
Hospital Nossa Senhora da Glória in Vitória
2 8.
These arguments are not irrefutable bec ause eosinophilic
me ningitis o r me ningo e nc e phalitis may b e idio pathic o r
produc ed by larvae of suc h human helminths ( reviewed in
r efer enc e 1 9 ) as
Asc a ri s
lu m b ri c o i de s
o r
Stro n gylo i de s
ste rc o ra lis
2 4 2 5,
Asc a ris su u m
1 6 1 8 2 3 3 2,
Tric hin e lla spira lis
1 0or by larvae of other paratenic nematodes suc h as the rat
nemato de
An gi o stro n gylu s c a n to n e n si s
3 3 4 2and r ac c o o n
asc arid,
Ba ylisa sca ris pro cyo nis
3 4.
Sinc e
Asca ris
antigens c an
c ross reac t with
To xo c a ra
antigens, one c ould argue that the
positive serology observed in the two c ases reported here may
be due to this c ro ss reac tio n. Ho wever, the sero lo gy was
performed after absorption with
Asc a ris
antigen. In one c ase
( Case 2 ) there was
Stro ngylo ide s ste rco ra lis
larvae in the feces.
Although there are reports of
Stro ngylo ide s
larvae entering the
c entral nervous system, this oc c urrenc e is extremely rare and
is assoc iated with the disseminated form of the infec tion
9. The
other paratenic nematodes that can cause eosinophilic meningitis
or enc ephalitis have not yet been desc ribed in B razil.
Ta b le 1 - Co ntinue .
Author Age/Gender Summary of main observations Cases with clinical data
1 3 -Kumar & Kimm 1 9 9 4 1 9* * 2 2 /F
1 4 -Ota et al 1 9 9 43 1 * a 2 2 /F
1 5 -Duprez TP et al 1 9 9 68* * 5 8 /M
1 6 -Strupp et al 1 9 9 94 5 4 9 /M
1 7 -Goffete et al 2 0 0 01 3 4 0 /F
1 8 -Ardiles et al 2 0 0 13 6 1 /M
1 9 -Richartz E, Buchkremer G 2 0 0 23 4* * 6 5 F
20- Robinson A, Tannier C, Magnaval JC 200235* * N.I
2 1 - Moreira-Silva et al# 5 /F
* The c ause of death was attributed to T. ca nis encephalitis. * * Information collected from abstract. CSF = cerebrospinal fluid. a the same case
was reported in Journal of Neurology Neurosurgery and Psychiatry 5 9 :1 9 7 -1 9 8 ,1 9 9 5 . N.I.: age of patient was not informed in the abstrac t. # cases reported in this publication.
MRI: cervical cord lesions. Improvement after treatment
Meningeal irritation signs and cerebellar ataxia. MRI: c ortic al and subc ortic al lesions in c erebrum and c e r e b e llum. CSF: 3 3 0 c e lls/
µ
l 3 0 % e o sino phils. Serology positive in the blood and CSF. Treatment with diethylcarbamazine and corticoids but other lesions developed in spinal cord.Subacute weakness of quadriceps muscles. Difficulty with bladder and bowel functions and erectile failure. Paraparesis with discrete hyperesthesia and hypalgesia. CSF: 1 2 8 c e lls /
µ
l 3 3 % e o s in o ph ils . No b lo o d eosinophilia. Serology was positive in the blood and CSF. The patient was treated with albendazole and there was partial rec overy of signs and symptoms. MRI performed four months after treatment was normal.Weakness of right leg and dysesthesia in the right T8 -T1 0 dermatomes. MRI: hypoinsensitivity in the T8 --T1 0 spinal cord area. CSF: pleocytosis with eosinophilia. Serology positive in blood and CSF rec overy after treatment with thiabendazole.
faciobrachycrural Hemiparesis. CT scan: hypodense areas in the right posterior temporal area. Serology positive in the plasma and negative in CSF. No information on CSF cell counts.
Depressive symptoms and cognitive deficits. Normal EEG and CT.De pr e ssive sympto ms and c o gnitive defic its. Normal EEG and CT. CSF eosinophilia and po sitive ser o lo gy fo r To xo c a ra. Impr o vement o f cognitive deficits one year later.
Meningoradiculitis. CSF eosinophilia. Positive serology for To xo ca ra both in the serum and CSF.
Paresis of both superior and inferior members, nuchal rigidity and bilateral Kornig and Lasègue responses. Urinary retention and fec al inc ontinenc e. CSF: 1 8 7 leukocytes, 5 7 % eosinophils. Blood eosinophils: 7 1 1 / ul. Positive serology for To xo ca ra both in blood and CSF. Cr anial MRI: small ir r e gular le sio ns in the po ster io r po r tio n o f spine-b ulb ar tr ansitio n and pedunculus cerebellaris. Improvement after treatment with albendazole.
Palsy of inferior members and urinary retention. CSF: 2 3 l e u k o c yte s /m l . 5 7 % e o s i n o p h i l s . B l o o d eosinophils 2 2 1 /ul. Positive serology for To xo c a ra
both in blood and CSF. Improvement after treatment with thiabendazole
5 /M
As de m o n s tr a te d in Ta b le 1 , n e ur a l in vo lve m e n t in
toxoc ariasis has been reported in all ages without a signific ant
gender prevalenc e. Eosinophilia oc c urred in both peripheral
blood ( 7 /9 cases) and cerebrospinal fluid ( 8 /1 1 cases) in those
cases in which eosinophil counts were reported. It is noteworthy
that some c ases oc c urred without presenc e of eosinophilia in
blood and c erebrospinal fluid. Serology is useful for diagnosis
although c ross reac tion is frequent with larval antigens from
other nematode spec ies. For this reason absorption of serum
or cerebrospinal fluid with larval antigens from other nematode
spec ies would improve the spec ific ity of serology. Additionally,
further development of methods to detec t IgM anti-
To xo c a ra
larvae would help to identify rec ent infec tion. We c onc lude that
in c ases of enc ephalitis and myelitis with c erebrospinal fluid
pleoc ytosis and eosinophilia, parasitic infec tion of the c entral
nervous system may be suspic ious and serology should be
performed to establish the c orrec t diagnosis and treatment.
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