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1982, British Journal ofRadiology, 55, 189-196 MARCH 1982

Tuberculous meningitisa CT study


By S. Bhargava, M.D., D.M.R.D., F.A.M.S., Arun Kumar Gupta and
P. N. Tandon, M.S., F.R.C.S., F.A.M.S.
Department of Radiodiagnosis and Neurosurgery, All India Institute of Medical Sciences, New Delhi, India
(Received June 1981 and in revised form October 1981)

ABSTRACT recorded were direct readings and no attempt was made


This study comprises 60 cases of tuberculous meningitis to correct for the minification factor.
including both adults and children. Only three cases showed a
normal scan. Severe hydrocephalus was present in 87.09% RESULTS
children and only 12.09% adults. The incidence of hyd- Fifty-seven scans were abnormal and three were nor-
rocephalus increased with the duration of the illness and mal (Table I).
decreased with age. Exudates in the basal cisterns were graded
from mild to severe, the latter being seen only in children. Hydrocephalus
Visible infarcts were shown in 28.33% of cases, 10% showed
associated parenchymal tuberculomas. Serial follow-up scans This was shown at the time of presentation in 83.05%
indicate that patients with non-enhancing exudates have a good of cases and was graded as mild (8.47%), moderate
prognosis when medically treated, whereas in those cases with (22.03%) and severe (52.54%) on the basis of the cella
enhancing exudates the prognosis is poor in spite of medical media index (Meese et al, 1976). It was much more
treatment and surgical shunting; they either succumb to their frequent in children of ten years and under (71.42%)
illness or are left with irreversible sequelae. CT has proved than in those above ten years. Severe hydrocephalus was
sensitive in both the diagnosis and prognosis in clinically sus- more frequent in children (87.09%) than in adults.
pected tuberculous meningitis. Correlation of the degree of hydrocephalus with the
duration of illness is shown in Table II. Amongst
The study was planned to document the spectrum of patients with severe hydrocephalus, 21 (67.74%) had an
pathological changes seen in clinically diagnosed TBM illness of more than one month's duration, while seven
by CT scan and to correlate these with the clinical (53.84%) with moderate and only one (20%) with mild
assessment and carotid angiographic studies. Serial hydrocephalus had illness of more than one month's
follow-up scans were made to assess progress and evalu- duration.
ate any prognostic features which could be recorded. The anterior horn, posterior horn and Illrd ventricle
were quantitatively evaluated in each grade of hyd-
MATERIALS AND METHODS rocephalus (Table III). The degree of enlargement of
Sixty cases of tuberculous meningitis (TBM) (36 chil- the anterior horn varied significantly with the grade of
dren and 24 adults), diagnosed clinically in association hydrocephalus. No such difference was observed for the
with CSF biochemistry and cytology findings, were posterior horn and Illrd ventricle. Periventricular trans-
studied by CT. The diagnosis was confirmed in the three lucency was present in 61.66% of hydrocephalic cases of
cases which came to autopsy. In addition to the CT scan, which 72.97% had severe and 27.02% moderate hyd-
every patient had X-rays of the skull and chest, and on rocephalus.
14 cases carotid angiography was performed.
The EMI CT1010 head scanner was used for this Exudates in the subarachnoid cisterns
study. Enhanced scans were performed using Conray Enhancing exudates were seen in all the cisterns in a
420 as a bolus injection, 40 ml in adults and a corres- significant number, ranging from 60-82% in different
pondingly smaller dose in children. A few cases had both cisterns. The commonest sites were the suprasellar cis-
unenhanced and enhanced scans. The measurements tern, cisterna ambiens and Sylvian fissures, exudates
being present in 81.66% in each of these regions. The
TABLE 1 density of the exudates was graded as mild (+), moder-
PATHOLOGICAL LESIONS VISUALIZED ON CT ate (+ + ) and severe (+ + + ). In the mild grade, the

Lesion Percentage TABLE II


HYDROCEPHALUS VERSUS DURATION OF ILLNESS
Hydrocephalus 83.05
Exudates in the subarachnoid cisterns 81.66 Duration of illness
Infarct 28.33 Grade of Up to 1-3 4-6 More than
Tuberculoma/tuberculous abscess 10 hydrocephalus 1 month months months 6 months
White matter oedema 3.33
Border zone encephalitis 3.33 Severe 10 17
Intraventricular loculation 1.66 Moderate 6 3
Exudates over the convexity 1.66 Mild 4 1

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VOL. 55, No. 651
S. Bhargava, Arun Kumar Gupta and P. N. Tandon

FIG. 1.
Enhanced scan showing obliteration of the basal cisterns con-
sistent with mild (+) degree of exudates.

(A and B) Enhanced scans showing thick, copious severe degree


(+ ++) exudates, outlining Illrd ventricle, the suprasellar and
perimesencephalic cisterns. Exudate also seen in the Sylvian
fissures in B.

as low attenuation lesions in the basal ganglia or


heterogenous lesions on either side of the Sylvian fis-
FIG. 2. sure, single or multiple, unilateral or bilateral. Most
Enhanced scan showing moderate (++) degree of exudates. commonly, the middle cerebral artery (MCA) territory
Note a ring tuberculoma in the left temporal lobe and mod- alone was affected (82.35%). MCA and anterior cere-
erate ventricular dilatation. bral artery territories were involved in 11.76% of cases,
while the posterior cerebral artery area was affected in
cisterns are obliterated but do not enhance (Fig. 1). In only one case. In the 14 cases with MCA territory infarc-
the moderate grade, increased attenuations are seen tion, the basal ganglia on the left side were most fre-
outlining the obliterated cisterns (Fig. 2), and in the quently affected (ten cases).
severe grade there are copious and dense exudates with The site of visible infarction was correlated with the
increased attenuations, filling and enlarging the cisterns motor deficit (Table IV).
(Fig. 3). The severe grade occurred only in children, A feature of infarction in the basal ganglia region
while mild and moderate grades were seen in all age noted on the serial studies was gradual dilatation of the
groups. ipsilateral anterior horn and ipsilateral displacement of
Infarcts the septum pellucidum presumably due to shrinkage of
Seventeen (28.33%) cases had infarcts, visible on CT gliosed brain (Fig. 4).
190
MARCH 1982
Tuberculous meningitisa CT study
TABLE III
HYDROCEPHALUS EVALUATION

Grade of Anterior Posterior Illrd


hydrocephalus horn (mm) horn (mm) ventricle
Severe 7-12 6-12 3-6
Moderate 4-6 6-8 3-5
Mild 3-5 5-7 3

TABLE IV
MOTOR DEFICITS AND INFARCTS

Motor deficit Visible infarcts, %


Motor deficit explained by visible 52.94
infarct
Patient deeply comatose, no 29.41
evaluation possible
No deficit clinically 11.76
Abnormal limb movements explained 11.76
by infarct
Infarct seen on the same side as 5.88
motor deficit

Tuberculoma/tuberculous abscess
Only six cases (10%) showed associated tuberculomas
on CT, ranging in size from 2-12 mm (Fig. 5). They were
single or multiple and located both supra- and infra-
tentorially. In one case, the right cerebellopontine angle
cistern housed a large tuberculous mass. In two cases, a
tuberculoma less than 1 cm in diameter was not
documented by CT but was found at autopsy.
Other lesions visible on CT were: low attenuation in
the white matter considered to be oedema, and high
attenuating lesions outlining the gyri compatible with
encephalitis, in two cases each. Intraventricular locula-
tion and high attenuations in the sulci over the convexity
were present in one case each.
Two autopsies confirmed the CT findings of infarcts
and severe exudates in the Sylvian fissures and basal
subarachnoid cisterns (Figs. 6, 7).
(A and B) Progressive ipsilateral ventricular dilatation secon-
An attempt was made to correlate the carotid angio- dary to infarct in the left MCA territory. August 16, 1979 and
graphic and CT changes, in examinations performed February 27, 1980.
within days of each other. Two aspects were studied.
1. Relation between arterial narrowing on the angio-
gram and exudates and /or infarct in the affected artery (i) exudate, not documented by CT;
territory on CT. (ii) vasospasm playing a predominant role in the early
2. Ventricular dilatation diagnosed on angiogram was stages of meningitis, when narrowed arteries are
correlated with the degree revealed by CT. seen but no infarcts are demonstrated on CT.
In eight cases there were exudates in the suprasellar The patients showing arterial narrowing without
cistern on CT and arterial narrowing on angiogram enhancing exudates on CT improved remarkably on
(Figs. 8, 9); in three cases no exudates were evident and antituberculous treatment alone. We have therefore
the angiograms were normal. Therefore, in 11 out of 14 considered the arterial narrowing as vasospasm only.
cases there was good correlation between the presence After treatment the CT and the patient returned to
of exudates on CT and arterial narrowing. In another normal. On the other hand, the patients with narrowed
three cases, arterial narrowing was seen but no enhanc- vessels and enhancing exudates failed to improve, the
ing exudates were visible on CT. This discrepency could narrowed arteries being considered as arteritis (Greitz
be due to: 1964; Lehrer 1966).

191
VOL. 55, No. 651
S. Bhargava, Arun Kumar Gupta and P. N. Tandon
Of the eight cases diagnosed angiographically as hav-
ing hydrocephalus seven showed hydrocephalus on CT
while one had normal-sized ventricles.
Serial follow-up scans
Twenty-seven patients were followed by serial CT
scans and the following observations were made.
1. Cases with severe grades of exudate in the basal
cisterns showed no clinical improvement on follow-up,
even if the ventricular size reduced to normal after shunt
surgery.

FIG. 6.
(A) Enhanced scan showing a heterogeneous area in the right
FIG. 5. MCA territory consistent with infarct. Note obliteration of
(A and B) January 15, 1980, enhanced scan, showing a large right Sylvian fissure.
well-defined tuberculoma with perilesional oedema in the right (B) Axial cut of specimen showing thick exudate in right Sylvian
paraventricular region. Severe hydrocephalus with peri- fissure. Microscopically multiple small infarcts in the right
ventricular translucency. MCA territory present. Compare with CT scan Fig. 6A.
192
(A) Enhanced scan. Thick exudate on the right side of the
suprasellar cistern with extension into the right cisterna
ambiens.
(B) Right carotid angiogramlateral viewshowing marked
narrowing of supraclinoid part of ICA (i.e. in the region of the
exudate). ACA is blocked.

FIG. 7.
(A) Plain scan. A large area of decreased attenuation seen in
the right temporal region (which was extending to parietal
region in the higher cuts), compatible with a large infarct,
confirmed at autopsy Fig. 7c.
(B) Enhanced scan depicting enhancing exudates in the cisterns
around the brain stem.
(c) A large right temporo-parietal infarct, compressing and
obliterating right lateral ventricle and displacing septum con-
tralaterally. Compare CT scan Fig. 7A.
VOL. 55, No. 651
5. Bhargava, Arun Kumar Gupta and P. N. Tandon
due to organized exudates in the basal cisterns involving
the optic nerves and/or chiasm, did not recover.
3. Those patients who had clinical and CSF evidence
of TBM but had a normal CT scan showed remarkable
improvement on antituberculous treatment, returning
to complete normality.
4. Associated tuberculomas, small and large, show
marked reduction in size and even complete clearance,
with corresponding clinical improvement, on medical
treatment.

DISCUSSION
The present study has confirmed the work of Dastur et
al (1970) and Tandon et al (1973, 1975), who showed
that hydrocephalus in TBM is more common in children
than in adults. This has been explained by the greater
accommodative power of the larger ventricular system
and greater resistance to stretch of fully myelinated
white matter in adults. The study suggests a linear rela-
tion between the degree of hydrocephalus and the dura-
tion of illness, as reported by Lorber (1951), Foltz &
Sheehy (1956), Bharucha et al (1969) and Tandon et al
(1973,1975). Hydrocephalus is nearly always present if
the patient has survived more than four to six weeks. In
the majority it is communicating due to blockage of the
basal cisterns by tuberculous exudate in the acute stage
and adhesive leptomeningitis in the chronic stage. In
some cases hydrocephalus is of the obstructive variety,
the block being at the foramina of the IVth ventricle,
wherein the IVth ventricle is dilated (Tandon, 1978). In
this series dilatation of the IVth ventricle was present in
39 cases, and in 16 cases the obstruction was at the level
of the aqueduct. Frequently narrowing and block of the
aqueduct may be caused by circumferential compression
of the brain stem by meningeal exudate surrounding it
(Dastur and Lalitha, 1973). Uncommonly aqueductal
obstruction may be due to an intraluminal tuberculoma
(Dastur et al 1972).
The high incidence of enhancing exudates in the basal
cisterns conforms with the observations of Dastur et al
(1970) on an autopsy series. The amount and density of
the exudate has prognostic significance as revealed by
the present study. With antituberculous treatment, the
gelatinous exudate of the acute stage gives way to a grey
mass up to 2 cm thick and firm or even woody hard,
obliterating the subarachnoid space, caused by the lay-
ing down of a large amount of connective tissue (Levison
et al, 1950; Home, 1951) which becomes densely
(A) Areas of decreased attenuation seen in both the internal adherent to the underlying brain. In time the granulation
capsule regions consistent with infarcts. tissue is replaced by hyalinized tissue in some regions,
(B) Left carotid angiogram, AP view. Marked narrowing of signifying healed lesions, but in other areas, frank
supraclinoid part of ICA and of proximal part of MCA. The granulomatous meningitis may continue (Auerbach
ACA is blocked along with the striate group of vessels. 1951; Tandon & Tandon, 1975). According to Rich
(1951), complete resolution of the inflammatory
exudate may be expected only when the number of
2. Cases with mild to moderate exudate, who had bacilli causing inflammation is small or when inflamma-
shunt surgery at an early stage of the disease, showed tion is caused by free tuberculoprotein without live
some improvement in neurological status. Visual loss, bacilli. When large numbers of tubercular bacilli incite
194
MARCH 1982
Tuberculous meningitisa CT study
the inflammation, much of the exudate may resolve but a A good correlation was observed between the carotid
residue remains either in the form of tubercles, encapsu- angiographic changes and CT changes.
lated caseous foci or scar tissue. These encapsulated foci Correlation of the follow-up CT scans with the clinical
may be dormant, but constitute a potential source of condition confirmed that the presence of enhancing
danger to the patient. Like the basal exudates, the vascu- exudates had a poor prognosis, both in terms of survival
lar changes also progress to a fibrous endarteritis fol- and persistent sequelae.
lowing a necrotizing panarteritis of the acute stage. Con- In conclusion, one may say that CT is a valuable tool
comittant with the transformation of the exudate around with a very high diagnostic sensitivity and prognostic
the blood vessels, there is a fibrous thickening of the accuracy; it should be used as an early radiological inves-
intima, either diffusely or in one segment of the vessel tigation in suspected cases of TBM and for follow-up.
wall. In 1969, Lalitha (Dastur & Lalitha, 1973) is said to
have observed a possible relationship between adventi-
tial inflammatory reaction and the site of segmental
subintimal fibrosis with pillow formation. These changes REFERENCES
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DESHPANDE, D. H., 1969. Tuberculous meningitis in chil-
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series of Rich and McCordock (1933) and Dastur et Neuro Tuberculosis: an Epitome of Neuropathology, Vol. 2
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(ii) the effective CT slice thickness in our study was 1 1970. The brain and meninges in TBM. Gross pathology in
100 cases and pathogenesis. Neurology India, 18, 86-100.
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culomas are likely to be missed because of the par- hydrocephalus in tuberculous meningitis. Neurology (Bom-
tial volume effect. With the present-day equipment, bay), Supplement, 1, 73.
micro-tuberculomas are likely to escape detection DASTUR, D. K. & UDANI, P. M., 1966. Pathology and
in clinical material. pathogenesis of tuberculous encephalopathy. Ada
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main trunk of the MCA, the origins of the thalamoper- in tuberculous meningitis. American Review of Tuberculosis,
forating and lenticulostriate arteries are surrounded by 74, 835-855.
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easily blocked because of their small calibre. The basal HORNE, N. W., 1951. Tuberculous meningitis: problems in
ganglia region is thus a common site for infarcts, and pathogenesis and treatment. Edinburgh Medical Journal, 58,
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changes in 46 and frank infarcts in 41. In the present LEVISON, A., LUHAN, J., MAURELIS, W. P. & HERZON, H., 1950.
study, good correlation was observed between the site of The effect of streptomycin on tuberculous meningitis. A
infarct visible on CT and the clinical motor deficit. Some pathologic study. Journal of Neuropathology and Experimen-
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in tuberculous meningitis in children. Part II. A review of 100
size of the infarct. pneumoencephalograms. Archives of Disease in Childhood,
White matter oedema only was seen in, 3.33% of cases 26, 28-44.
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lighted the occurrence of tuberculous encephalopathy as post operative follow up studies of infantile hydrocephalus
a possible allergic phenomenon. It has been shown in using computerized tomography. In Cranial Computerized
27% of their cases. This marked discrepancy can be Tomography, Ed. W. Lanksch and E. Kazner (Springer-
explained by the physics of brain oedema recognition on Verlag, Berlin/Heidelberg/New York).
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threshold of brain edema recognition by computerized
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recognizable on CT. Thomas, Springfield, 111.).

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VOL. 55, No. 651
S. Bhargava, A run Kumar Gupta and P. N. Tandon
RICH, A. R. & MCCORDOCK, H. A., 1933. The pathogenesis of TANDON, P. N., RAO, M. A. P., BANERJI, A. K., PATHAK, S. N. &
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Book reviews
Cunningham's Textbook of Anatomy. Ed. by G. J. Romanes fact that CT scanning has been with us for several years, no
12th edit., pp. 1078, 1981 (Oxford University Press), 25.00. reference is made to the technique. This extraordinary omission
ISBN 0-19-263134-9 will, I believe, devalue the book for the current generation of
On entering medical school at the end of World War II, students, particularly in the United States, where whole-body
Cunningham's Anatomy, at 3.0.0, was the largest and most scans are a fact of daily clinical life and in constant use in
expensive book the reviewer had ever possessed. The Scottish anatomy departments. The authors have missed a golden
equivalent of Gray's Anatomy, it was rightly renowned for its opportunity in this new edition of being the first to incorporate
purity of style and clarity of illustration. It was therefore a whole body scanning as part of a standard anatomy textbook.
pleasant surprise to discover that Cunningham is alive and well However, in standard works of this type, it is difficult to
at 79 years of age and just entering its 12th edition. One decide how far to go with recent advances and as a textbook of
recognized many old friends among the illustrations, not least anatomy, Cunningham carries all its old authority presented in
the male model who has not aged a bit and still flexes his biceps a much more attractive format than of yore and at 25.00 it is
for us without the slightest sign of fatigue. However, the whole probably cheaper than it was in 1945.
format of the book has been restyled; many diagrams and J. T. PATTON.
dissections have been replaced or reproduced in less sombre
colours and there is much more emphasis on function. In the Computed Tomography of the Brain. By G. Salamon and Y. T.
chapter on the peripheral nervous system, as well as listing the Huang, pp. 155, 1980 (Springer-Verlag, Berlin), DM. 198/
muscles supplied by individual nerves there is a parallel table $116.50.
illustrating the functional effect of paralysis of that nerve or ISBN 3-540-08825-3
branch. Applied anatomy of this sort makes the book much This monograph is an atlas of normal cerebral anatomy and is
more interesting to read, and for the undergraduate gives it a collaborative study from 4 university centres, 3 in France and
more clinical relevance and vitality than it had 30 years ago. one in the USA. The authors have undertaken serial sections
As far as the text is concerned, there must be very few people through cadaver heads at 1 cm thickness in the sagittal, coronal
qualified to comment upon anatomical statements, least of all and axial planes and each slice has been scanned, photographed
the reviewer, but dare one suggest a mistake in the description and X-rayed. In addition, in vivo CT sections at the appropriate
of the dental formula on p. 416 (mesial v. lateral)? level and scan angle are also included for comparison. Axial
Earlier editions included a few radiographs as a gesture to sections have been taken in 3 planes similar to those used in
clinical relevance but radiology today is playing a much more scanning practice, namely, parallel to the orbito-meatal line and
important role in pre-clinical training and it is good to find in 15 extension and flexion respectively.
Cunningham reflecting this trend throughout the book with a The photographs and radiographs of the slices are clear and
wealth of radiographs illustrating both static and dynamic con- well annotated, although at times it was difficult to see the lines
cepts. Indeed the text is provided by eight anatomists and two indicating the various structures. The CT scans, however, vary
radiologists, which is a very enlightened approach and makes all in quality. The axial and coronal images are adequate, but as the
the more surprising what I believe is a serious omission. authors admit those in the sagittal plane have been reformatted
In my old medical school, a major feature of the anatomy from slices which are rather too thick to achieve satisfactory
museum was a collection of preserved specimens of transverse detail. However, this is not to decry the merits of the book,
sections through the trunk to demonstrate relationships at dif- which will be of value to all those who perform or interpret
ferent levels. At that time, slicing through the body with a cranio-cerebral CT. There is a wealth of practical information
band-saw was the only way of doing this: today these relation- in this relatively small volume and I strongly recommend it.
ships can be demonstrated in minutes by CT. Yet despite the D. P. E . KlNGSLEY.

196

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