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a
Department of Neurology, King George Medical University, Uttar Pradesh, Lucknow 226003, India
b
Department of Microbiology, King George Medical University, Uttar Pradesh, Lucknow 226003, India
c
Department of Radiodiagnosis, King George Medical University, Uttar Pradesh, Lucknow 226003, India
KEYWORDS Summary Background: Hydrocephalus is one of the most common complications of tubercu-
Tuberculosis; lous meningitis. The present study evaluated the incidence, predictive factors and impact of
Meningeal tuberculosis; hydrocephalus on overall prognosis of tuberculous meningitis.
Tuberculoma; Material and methods: In a prospective cohort study, all patients fulfilling the inclusion crite-
Cerebrospinal fluid; ria of tuberculous meningitis underwent clinical and cerebrospinal fluid evaluation, together
Stroke; with magnetic resonance imaging of the brain. Patients were treated with antituberculosis
Ventriculo-peritoneal drugs and dexamethasone. Follow up neuroimaging was done after 6 months. Hydrocephalus
shunt was assessed using Evan’s index.
Results: Of 80 patients with tuberculous meningitis, 52(65%) had hydrocephalus at presenta-
tion. During follow up, 8 new patients developed hydrocephalus. Factors associated with hy-
drocephalus included advanced stage of disease, severe disability, duration of illness > 2
months, diplopia, seizures, visual impairment, papilledema, cranial nerve palsy, hemiparesis,
CSF total cell count > 100/cu.mm, CSF protein > 2.5 g/l. Neuroimaging factors that were sig-
nificantly associated with hydrocephalus included basal exudates, tuberculoma and infarcts.
Multivariate analysis revealed visual impairment, cranial nerve palsy and the presence of basal
exudates as significant predictors of hydrocephalus. In 13 patients, with early tuberculous
meningitis, there was complete resolution of hydrocephalus. Hydrocephalus was significantly
associated with mortality and poor outcome.
0163-4453/$36 ª 2012 The British Infection Association. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jinf.2012.12.009
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The scans were reviewed by an experienced neuroradiolo- gray matter on both spin density and T2-weighted images.
gist, who was unaware of treatment and patient outcome. These lesions were hypointense on T1-weighted images.
Hydrocephalus was defined as ventriculomegaly with Evan’s All included patients were treated with an antituberculosis
ratio (maximal width of frontal horns/maximal width of regimen as recommended by World Health Organization for
inner skull) more than >0.30; and/or size of one or both the treatment of central nervous system tuberculosis.
temporal horns greater than 2 mm. Other imaging changes, Patients received 2 months of daily oral isoniazid (5 mg/
like presence of sulcal effacement, periventricular ooze kg of body weight; maximum, 300 mg), rifampicin (10 mg/
(transependymal flux of CSF into the periventricular paren- kg; maximum, 600 mg), pyrazinamide (25 mg/kg; maxi-
chyma, particularly at the tips of the frontal, occipital and mum, 2 g/day) and intramuscular streptomycin (20 mg/kg;
temporal horns), type of hydrocephalus (communicative or maximum 1 gm/day), followed by 7 months administration
obstructive), meningeal enhancement, exudates, tuber- of isoniazid and rifampicin.14 Patients also received dexa-
culomas and infarcts, were also recorded. Communicating methasone for eight weeks. Corticosteroid regimen con-
hydrocephalus was defined as hydrocephalus with a dilated sisted of intravenous dexamethasone for 4 weeks
fourth ventricle. There was no evidence of an obstruction (0.4 mg/kg body weight per day and then tapered off de-
of the intraventricular CSF pathways, including the fourth creasing 0.1 mg/kg every week) and then oral treatment
ventricular outflow and the cerebral aqueduct. Size of for 4 weeks, starting at a total of 4 mg per day and decreas-
fourth ventricle remained unchanged in obstructive hydro- ing by 1 mg each week. Antiepileptic drugs were used in the
cephalus.4,12 (Fig. 1) Mild, moderate, and severe hydro- patients who had seizures. Pyridoxine was given orally
cephalus were categorized if Evan’s ratios were <0.34, 20e40 mg/day to all the patients. In patients with clinical
0.35e0.40, and >0.40 respectively.13 evidence of elevated intracranial pressure, 20% mannitol
and acetazolamide were used. Mannitol was used in dosage
Definition of other neuroimaging findings schedule of 0.25e1.0 g/kg body weight every 6 hourly for
2e7 days. Neurosurgical opinion sought in patients with un-
On gadolinium-enhanced MRI, meningeal inflammation was satisfactory response to medical treatment.
defined as the enhancement of pia-arachnoid, which extends
into the subarachnoid spaces of the sulci, basal cisterns and Follow up and outcome assessment
enhancement along the inner table of the skull and in the
dural folds of the falx and tentorium. The exudates were Disability assessment was done using modified Barthel index
defined as a thick area of enhancement in the regions of basal (MBI), which is a 20 point scoring system. Assessment of
cisterns and Sylvian fissure. Tuberculoma was defined as disability included degree of dependence for bowel and
discrete or coalescing lesions which were showing homoge- bladder, grooming, toilet use, transfer, mobility, dressing,
neous nodular contrast enhancement or showing a ring feeding, use of stairs and bathing. For each activity, a score
enhancement. Infarct was defined as an area of abnormal of 0 indicated a complete dependence, and a score of 2 or 3
signal intensity in a vascular distribution without any indicated that the patient was able to perform activities
evidence of mass effect. Infarcts were hyperintense to independently. A score of <12 indicated poor functional
Figure 1 (A) Axial T2 FLAIR sequence shows calculation of Evans’s ratio (in this case more than 30%). Periventricular T2 FLAIR
hyperintensity indicates periventricular CSF ooze suggestive of active hydrocephalus (marked by arrows). (B) Axial T2 FLAIR
sequence shows measurement of temporal horn width.
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status and a score of >12 indicated good functional status. at the time of inclusion, were in stage- II. In our study,
Assessment of disability as per MBI was done at baseline and there were 36 (45%) bacteriologically confirmed cases.
at the end of 1st, 3rd and 6th month of follow up. MBI >12, Four patients were lost to follow up and their last observa-
at the end of 6 months, was considered as good outcome. tions were carried forward up to 6 months. None of the pa-
Follow up MR study was done after 6 months. tient was HIV positive. In none of the patients drug
resistance to antituberculosis drug was demonstrated.
Statistical analysis Other base-line characteristics have been shown in Table 1.
The statistical analysis was performed using the Statistical Incidence of hydrocephalus
Package for Social Sciences, version 16 for windows (SPSS,
Chicago IL, USA) and Microsoft Excel. Both univariate and At inclusion, hydrocephalus was demonstrated in 52 (65%)
multivariate analysis were done to evaluate the predictors patients of tuberculous meningitis. Twenty patients (38.5%)
for hydrocephalus. Univariate analysis was performed by had mild hydrocephalus. Remaining, 32 (61.5%) patients had
Chi-square test for non-parametric data and student’s “t” moderate or severe hydrocephalus (Evan’s ratio equal or
test for independent variables for parametric data. Rela- more than 0.34). Periventricular ooze was present in 20
tive risks with95% confidence interval were ascertained. For (38.5%) patients. Five patients had asymmetric dilatation of
multivariate analysis, binary logistic regression was per- lateral ventricles. Sulcal effacement was seen in 32 patients
formed to see the impact of individual predictors of (61.5%). Among patients with hydrocephalus, acute infarcts
hydrocephalus. KaplaneMeier analysis was performed to were noted in 22 patients (42.4%), basal exudates in 38
estimate the event free survival for the outcome with or (73.1%) and tuberculoma in 27 patients (51.9%). Among 32
without baseline hydrocephalus using the Log Rank test. patients with moderate to severe hydrocephalus, 25 (48%)
Statistical significance was defined at p value of <0.05. Sta- had a communicating type of hydrocephalus. And 7 (13.4%)
tistical analysis was two-tailed. patients had possible obstructive type of hydrocephalus.
Table 1 Baseline characteristics in patients of tuberculous meningitis with and without hydrocephalus (n Z 80).
Characteristics Total N Z 80 Baseline No baseline Level of
hydrocephalus N Z 52 hydrocephalus N Z 28 significance
n % n % n % P
Age > 25 years 46 57.5 30 57.7 16 57.1 0.850
Male 43 53.8 29 55.8 14 50.0 0.573
Female 37 46.3 23 44.2 14 50.0
Duration of illness 43 53.8 35 67.3 08 28.6 0.002
> 2 months
Pulmonary tuberculosis 18 22.5 14 26.9 04 14.3 0.653
MRC stage I 25 31.3 11 21.2 14 50.0 0.001
MRC stage II 34 42.5 21 40.4 13 46.4
MRC stage III 21 26.3 20 38.5 01 03.6
Fever 76 95.9 51 98.1 25 89.3 0.192
Headache 73 91.3 48 92.3 25 89.3 0.079
Vomiting 59 73.8 41 78.9 18 64.3 0.088
Seizures 30 37.5 26 50.0 04 14.3 0.006
Altered sensorium 31 38.8 23 44.3 08 28.6 0.117
Meningeal signs 71 88.8 48 92.3 23 82.1 0.170
Diplopia 51 63.8 41 78.9 10 35.7 0.001
Cranial nerve 62 77.5 49 94.2 13 46.4 0.000
involvement
Papilledema 50 62.5 41 78.9 09 32.1 0.001
Optic atrophy 10 12.5 08 15.4 02 07.2 0.001
Normal vision 44 55.0 21 40.4 23 82.1
Low vision 36 45.0 31 59.6 05 17.9 0.002
CSF AFB stain 21 26.3 18 34.6 03 10.7 0.06
CSF AFB culture 28 35.0 21 40.4 7 25.0 0.258
CSF TB PCR 36 45.0 28 53.8 8 28.6 0.076
Definite TBM 36 45.0 28 53.8 8 28.6
Probable TBM 25 31.3 15 28.9 10 35.7
Possible TBM 19 23.8 11 21.2 8 28.6 0.445
Meningeal enhancement 74 92.5 50 96.2 24 85.7 0.091
Basal exudates 42 52.5 38 73.1 04 14.3 0.000
Tuberculoma 31 38.8 27 51.9 04 14.3 0.001
Infarct 26 32.5 22 42.3 04 14.3 0.011
Good outcome (MBI > 12) 57 71.3 31 59.6 26 92.9
Poor outcome MBI (<12) 23 28.8 21 40.4 02 07.2 0.002
AFB Z acid-fast bacilli; MRC Z Medical Research Council; CSF Z cerebrospinal fluid; PCR Z polymerase chain reaction;
TB Z tuberculosis; TBM Z tuberculous meningitis; MBI Z modified barthel index.
>2.5 g/l (p Z 0.05) were also associated with hydrocepha- hydrocephalus. Of 52 patients with hydrocephalus, 6 were
lus. Among the neuroimaging features, presence of basal subjected to surgery (4 later died and 2 had partial
exudates (p Z 0.001), tuberculomas (p Z 0.001) and in- improvement). Among patients with baseline hydrocepha-
farcts (p Z 0.011), were associated with occurrence of hy- lus, 31 (59.6%) had a good outcome (MBI > 12). Twenty-one
drocephalus. On binary logistic regression analysis, factors patients had improved completely after six months. Eleven
that were significantly associated with presence of hydro- cases (21.2%) had a poor outcome (MBI 12); clinical
cephalus included vision impairment (p Z 0.005), cranial condition of 5 patients had worsened. In 28 patients without
nerve involvement (p Z 0.012) and presence of basal exu- baseline hydrocephalus, 26 (92.8%) had a good outcome
dates (p Z 0.001). These three predictors had a very high (MBI > 12); among these patients 21 (75%) had improved
sensitivity, specificity (>80%) and a high positive predictive completely. Only 2 patients of later group had a poor
value (90.2%) with a fair accuracy (86.3%), for prediction of outcome, both experienced deterioration during follow up.
hydrocephalus. Follow up neuroimaging was done in 54 (32 with
hydrocephalus and 22 without hydrocephalus, at inclusion)
patients. Among patients with baseline hydrocephalus, 13
Follow up patients had complete resolution and 12 patients had
partial resolution. In 3 patients hydrocephalus persisted
During the course of study, 10 patients died (median survival while in another 4 patients, ventricles size further in-
50 days, range 25e110 days). All 10 patients, who died, had creased. Of the 22 patients without baseline
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Prognosis among patients with baseline Figure 3 KaplaneMeier survival curves in patients of tuber-
hydrocephalus culous meningitis with or without hydrocephalus at observed
at the time of inclusion in the study.
Factors associated with poor outcome (death or disability),
among patients with baseline hydrocephalus, were pres- the incidence of hydrocephalus ranging from 17 to 95%.15e19
ence of hemiparesis (p Z 0.029), stage III tuberculous men- Earlier, air encephalography was used for the diagnosis of
ingitis (p Z 0.002), pulmonary tuberculosis (p Z 0.006) and hydrocephalus. In an air encephalography based study, hy-
poor baseline MBI 12 (p Z 0.03). KaplaneMeier cumula- drocephalus was observed in 62% of the pediatric patients
tive survival curve analysis showed that the patients with of tuberculous meningitis.20
baseline hydrocephalus had significantly higher incidence Hydrocephalus can develop early in the course of the
of death and severe disability comparable to those without disease or can develop paradoxically, following antituber-
hydrocephalus (p Z 0.006). (Fig. 3). culosis treatment.21,22 The predictive factors of hydroceph-
alus, in patients with tuberculous meningitis, have scantly
been evaluated. In a study, long duration of illness, ad-
Discussion vanced stage of disease, focal neurological deficit, and
presence of infarcts were significantly associated with hy-
In our study, hydrocephalus was present in majority (65%) drocephalus.21 In our study as well, hydrocephalus was
of the patients. During follow up, hydrocephalus developed more frequent in patients with advanced disease, severe
in 8 new cases. Various studies, in the past, have reported disability and a long-duration of illness. Presence of
Table 2 Baseline characteristics predicting complete resolution of baseline hydrocephalus after 6 months (Univariate analy-
sis) (n Z 32).
Characteristic Total Complete resolution (n Z 13) Partial or no resolution (n Z 19) P value
n n % n %
Duration of illness < 2 months 13 7 53.5 06 31.6 0.281
MRC stage I & II 19 11 84.6 08 42.1 0.028
Seizures 13 05 38.5 08 42.1 0.873
Initial GCS 15/15 18 11 84.6 07 36.8 0.012
Normal vision 21 11 84.6 10 52.6 0.136
Hemiparesis 08 01 07.7 07 36.8 0.146
Baseline MBI > 12 19 12 92.3 07 36.8 0.003
CSF TLC < 100/cu.mm 17 11 84.6 06 31.6 0.005
CSF protein < 2.5 g% 17 11 84.6 06 31.6 0.005
Mild hydrocephalus 16 12 92.3 04 21.1 0.001
Basal exudates 12 03 23.1 09 47.4 0.307
Infarct 12 03 23.1 09 47.4 0.307
Tuberculoma 09 02 15.4 07 36.8 0.355
CSF Z cerebrospinal fluid; GCS- Z Glasgow coma scale; TLC Z total leucocyte count; MRC Z Medical Research Council.
Values in bold are statistically significant.
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hydrocephalus is, in fact, an indication of severe disease. scan image at which the frontal horns and maximal inner
Most of the complications of tuberculous meningitis, includ- skull diameters are measured.30 However, Evan’s ratio is
ing hydrocephalus, develop because of thick copious exu- still frequently used method to diagnose hydrocephalus.31
dates, which are dominantly present in the The distinction between two types of hydrocephalus (com-
interpeduncular, suprasellar, and Sylvian cisterns. Opto- municating and obstructive type) is often not clear cut. For
chiasmatic arachnoiditis is a devastating form of tubercu- example, if all the ventricles are enlarged, then it is diffi-
lous meningitis and often associated with profound vision cult to establish whether the hydrocephalus is due to ob-
loss and hydrocephalus.2,21 Hydrocephalus is often associ- struction of the fourth ventricular outlets or due to
ated with raised intracranial pressure and several other an obstruction to the CSF pathways in the basal subarach-
complications of tuberculous meningitis. Increased intra- noid spaces. In patients with tuberculous meningitis com-
cranial pressure, if remains untreated, results in alteration municating hydrocephalus is much more common than
in consciousness. In addition to this, elevated intracranial obstructive hydrocephalus.4
pressure can lead to stretching of already compromised In conclusion, hydrocephalus is a common complication
vessels (like the pericallosal arteries) and may produce in- of tuberculous meningitis.
farcts.23 Optic nerve may be compressed by enlarged di- If a patient had neurological deficits, seizures or is in bad
lated third ventricle resulting in vision loss and optic clinical conditions, cranial imaging should be performed to
atrophy. Thus, clinical parameters like vision impairment check for hydrocephalus. Majority of patients having mild
and cranial nerve palsy can act as important clinical indica- hydrocephalus had a good outcome and complete resolu-
tors for the presence of hydrocephalus, even before neuro- tion with medical management. CSF diversion procedures
imaging is obtained. may not bring desired results in rapidly deteriorating
In earlier studies, hydrocephalus had been found a de- patients.
terminant of poor outcome and mortality.1,17,21,24 In our
study, as well, hydrocephalus unfavorably affected overall
prognosis in patients with tuberculous meningitis. Hydro-
Appendix A. Supplementary data
cephalus resolution was more frequent in patients with
milder form of disease. Corticosteroids have shown to re-
duce the number of deaths and increase the survival in adult Supplementary data related to this article can be found at
patients, however, role of dexamethasone, in the treatment http://dx.doi.org/10.1016/j.jinf.2012.12.009.
of hydrocephalus, is uncertain.25 Thwaites and co-workers
could not observe any significant reduction in the proportion
of patients with meningeal enhancement or hydrocephalus References
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