ClinicalRadiology(1985) 36,233-239 © 1985 Royal College of Radiologists
0009-9260/85/428233 $02.00
Surface Enhancement of the Brain E. H_ B U R R O W S
Department of Neuroradiology, Wessex Neurological Centre, Southampton General Hospital, Southampton Surface enhancement of the brain is a valuable computed tomographic sign. The patterns of enhancement and their differential-diagnostic significance are discussed on the basis of 14 illustrative cases.
Tissue e n h a n c e m e n t is an integral part of examination of the brain by c o m p u t e d t o m o g r a p h y (CT) and, often, it yields the information from which the diagnosis is made. Linear and other surface enhancement is a particular pattern of e n h a n c e m e n t that merits discussion because its presence should p r o m p t the radiologist to consider several diagnostic options. A review is presented here of this important sign based on 14 illustrative cases.
I L L U S T R A T I V E CASE R E P O R T S Fourteen cases are illustrated in Figs 1-11, the individual captions providing details of the histories and diagnoses. These patients are examples of the three pathological patterns of surface enhancement, namely: (1) rim or linear e n h a n c e m e n t (Figs 1-6), (2) gyriform e n h a n c e m e n t (Figs 7-10) and (3) basal-cistern e n h a n c e m e n t (Fig. 11).
Fig. 1- Normal enhanced convexitydura (arrows), visiblein the defect of a head injury craniotomy 12 years before.
DISCUSSION The p h e n o m e n o n of e n h a n c e m e n t is produced by rendering some of the body tissues m o r e dense than others to the X-ray beam. It is an artificial manoeuvre which is achieved by introducing 20-25 g of iodine into the circulation. Within the head, the results bring benefits to neurological diagnosis which are of the magnitude of those of intravenous urography in nephrology (Paxton and A m b r o s e , 1974)_ Not all parts of the normal brain enhance to the same degree. For example, the rich leptomeningeal anastomosis ensures that the cerebral cortex enhances preferentially. The falx, because of its greater density, is usually visible before enhancement, but an intravenous injection of iodine converts it into a vivid line in the enhanced vertex slices. It is necessary to r e m e m b e r that the convexity dura, which is part of the same m e m b r a n e , behaves in the same way but it is not seen in a normal subject, being hidden by the outline of the skull. If brought into view by a surgical defect or an extradural collection, the normal convexity dura shows the same attenuation characteristics as the falx (Figs 1, 2).
1. Rim or Linear Enhancement An enhanced linear shadow over the convexity of a hemisphere signifies the presence of an abnormal collection over the surface of the brain. This collection, which is almost always pus or blood, may be fresh or mature and it may lie outside or inside the dural m e m b r a n e . The appearances on CT usually include features which indicate whether the mass is pus or blood and whether it is extradural or subdural.
Fig. 2 - Extradural haematoma, 13 days old. The patient showed progressive right-sided weakness after a head injury. The haematoma has a lentiform shape and a density compatible with a blood clot 2 weeks old. These slices were made after enhancement and show that the tim has the same thickness and density as the falx.
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Fig. 3 - Subdural haematomas in two patients, shown on enhanced vertex slices. (a) A demented alcoholic with bilateral collections. (b) An elderly woman with sudden dysphasia and right-sided weakness. In each patient the blushing cortical edge indicates the boundary line between haematoma and hemisphere and emphasises the absence of an enhancing membrane as dense as the falx. All three haematomas are less dense than normal brain, indicating that they have been present for weeks or months.
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Fig. 4 - Extradural empyemas in two patients shown on enhanced slices. (a) A 61-year,old man complaining of a chronic discharging sinus behind his left ear. Operation revealed extradural and subgaleal pus and an infected bone flap. The lcntiform enhancing dural membrane was thicker and denser that the falx (not shown) and the overlying scalp tissues are puffy, features compatible with the presence of infection. (b) A 35-yea>old man with left weakness and a right parietal swelling for 6 weeks Note the displaced dural membrane (arrow), thicker and more dense than the falx.
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Fig 5. - Haematoma or empyema? An elderly alcoholic with a chronic left subdural haematoma who became dysphasic 2 months after the haematoma had been evacuated. (a) Unenhanccd slice. (b) Enhanced slice. This lesion was wrongly thought to represent reaccumnlated subdural blood, but burr-hole exploration yielded 30 ml of pus. Unlike uninfected subduraI haematomas, empyemas show a membrane after enhancement which is thicker than the falx and often scrpiginous in outline.
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Fig. 6 - Infected subdural haematomas in two patients shown on enhanced slices. (a) A 53-year-old man complained of right weakness after craniotomy for left subdural haematoma 2 years before. Operation revealed an infected subdural collection bounded by a membrane which the surgeon described as 'the thick wash-leather of an organised subdural haematoma'. (b) A 12-year-old boy, retarded and hydrocephalic after neonatal meningitis, had been treated 10 years before by ventriculo-atrial shunting after bilateral burr-hole ventriculography. Operation showed that the left collection consisted of brownish-black fluid blood in the subdural space, bounded by a tough, organised membrane.
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Fig. 7 (a, b) Pyogenic meningeal reaction shown on enhanced slices. A comatose 28-year-old diabetic was found, on analysis of the cerebrospinal fluid, to have pneumococcal meningitis. The gyriform enhancement pattern involved the convexities of both hemispheres diffusely but spared the basal cisterns.
The density of an extracerebral h a e m a t o m a alters with its age and a diagnostically useful rule is this: fresh blood, i.e. days old, is denser than n o r m a l brain,
weeks-old blood is isodense and months-old blood is h y p o d e n s e (Figs 2, 3). E m p y e m a s usually also undergo density changes but the time-scale of change is shorter, all e m p y e m a s usually being h y p o d e n s e after some days (Figs 4, 5).
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(a) Density of Collection
Fig. 8 - Neoplastic meningeal reaction. (a) Unenhanced slice; (b) enhanced slice at the same level. Autopsy revealed a malignant parietal astrocytoma which had spread diffusely through the subarachnoid space.
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Fig. 9 - (a, b) Granulomatous meningeal involvcmcnt shown on enhanced slices. A middle-aged woman presented with a complicated neurological picture, including progressive multiple nerve palsies, and brain biopsy revealed sarcoidosis. The scans show diffuse meningeal enhancement and hydrocephalus with {ranscpendymal extravasation.
(b) Abnormal Rim This is either a segment of the normal dural membrane which has been displaced medially by a collection in the extradural space (Figs 2, 4) or the arachnoid membrane displaced by a collection in the subdural space (Figs 5, 6).
(c) Significance Several explanations have been proffered to explain why the dura appears to enhance. De Vries and his colleagues (1981) described a chronic extradural haematoma with an enhancing rim in which a thick layer of granulation tissue was found at operation. They attributed the rim to the granulation tissue. Handa et al. (1979) reported similar appearances in a patient in whom semidigested blood but no granulation tissue or membrane was found. Omar and Binet (1978) speculated that the enhancing rim in extradural haematomas might simply be a medially displaced segment of normal dura, rather than indicate an abnormal tissue reaction. Analogous doubts beset the significance of the enhancing rim in subdural collections, in which, unlike extradural collections, it is not invariably present. Not all subdural abscesses show a rim (Luken and Whelan, 1980): in the Southampton material two out of l l had normal scans and Blaquiere (1983), in seeking an explanation, found that both patients had been ill for only a short time, i.e. for periods too brief for a capsule to have formed or for pus to have become loculated. He suggested that an enhancing rim may be related to the age of the subdural empyema, thus
confirming the view previously advanced by Danziger and his colleagues (1980). By contrast, subdural haematomas do not usually have an enhancing membrane (Fxg. 3). A membrane could be found in only three cases out of 100 subdural haematomas of varying ages reviewed for this purpose in Southampton. One of these cases proved to be infected (Fig. 5) and, possibly, another (Fig. 6a). The third case, a surgical complication of many months' standing following ventriculo-atrial shunting in a hydrocephalic (Fig. 6b), was probably also an infected haematoma. Appearances similar to the third case were recorded by Hammock and Milhorat (1981).
(d) Differential Diagnosis In order to diagnose collections outside the dura, two criteria must be fulfilled in respect of the displaced dural membrane; namely, the rim must be lentiform relative to the skull vault and it must have a regular outline. Although all extradural collections show these features, other information, for example, a history of trauma, clinical signs of brain infection or osteomyelitis, is sometimes necessary to distinguish between empyema and mature haematoma in the extradural space. Within the dura, collections of blood and pus are easier to differentiate, notably by the presence of the enhancing membrane which separates empyemas or infected haematomas from the compressed brain_ This membrane in empyemas is distinctive, outlining a loculated collection and often being serpiginous. This is an important diagnostic feature. When present, the serpiginous outline distinguishes subdural empyemas
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Fig. 10 - Empyema complication. An 18-year-old youth with streptococcal sinusitus developed signs of cerebral irritation and a left subdural empyema was evacuated. Two days later the patient developed a right hemiparesas which necessitated investigation by carotid angiography. (a) Enhanced vertex scan after craniotomy, showing gyral enhancement of the left cerebral cortex caused by acute infarction. (b) Left carotid angiogram made 2 days later, showing spasm of the siphon (arrowheads) and patulous sylvian branches but no arterial occlusion.
from uninfected subdural haematomas as well as from all extradural collections. In the rare cases of subdural haematoma with enhancing membranes referred to above which have been seen by the author, the rim was thicker than the falx - as thick as the membrane of subdural empyema - and this feature indicated that the lesion was infected. In the patient shown in Fig. 6(a), the straight outline of the rim suggested that the collection was unlikely to be a subdural empyema. In the patient shown in Fig. 6(b), the large segment of the convexity surface that was involved ruled out a collection outside the dura. 2. Gyriform Enhancement This is a distinctive pattern which is readily recognisable and diagnostically important. The enhanced areas appear as surface smearing over both cerebal hemispheres and vary from being just perceptible to simulating full gyral involvement (Figs 7, 8, 9). The lesions are bilateral, they exert no effect and they are not accompanied by oedema.
(a) Significance Fig. 11 - Tuberculous meningitis. A 3-year-old boy with a tuberculous mother suffered a devastating intracranial infection which rendered him blind and demented. The enhanced basal slice shows intense cisternal enhancement complicated by gross hydrocephalus and multiple infarcts: a characteristic picture of tuberculous meningitis. Post-lumbar puncture air is present in the left temporal horn.
Ascherl and his colleagues (1981) first identified this phenomenon as the CT sign of disseminated meningeal malignancy in 1976, and they reported a series of 50 patients with primary and secondary cancer and lymphoma who showed it. Subsequent experience has shown that meningeal infection (purulent, viral or tuberculous) is probably more often responsible. The
SURFACE ENHANCEMENT OF THE BRAIN
picture is thought to be produced by enhancement occurring in focal accumulations of tumour cells or inflammatory exudate in the perivascular (VirchowRobin) spaces. The pial membrane acts as a barrier which prevents invasion of the underlying parenchyma; hence, no oedema can occur.
(b) Diagnosis Several pathological processes, differing widely in their nature and situated inside and outside the pial membrane, may simulate this appearance (Table 1). For example, parenchymal lesions such as glioma, infarction or encephalitis may infiltrate the cortex and obliterate the sulci, producing true gyral enhancement (Fig. 10a). Cortical arterio-venous malformations, situated in the subarachnoid (extrapial) space, may mimic this picture and require angiography for diagnosis. However, all of these lesions have a focal nature, each usually involving only a single arterial territory or lobe of the brain. None shows the pattern of widespread, bilateral hemispherical involvement without mass effect or oedema, which is the diagnostic feature of disseminated meningeal neoplasm or infection.
Table 1 - Gyral patterns of enhancement
Widespread (Gyriform), i.e. meningeal dissemination Neoplasm - primary or secondary (Fig. 8) Infection- viral, purulent or tuberculous (Fig. 11) Sarcoidosis (Fig. 9) Lymphoma
Focal Gyriform - arteriovenous malformation Gyral - infarction (Fig. 10a) - encephalitis - glioma
3. Basal-cistern Enhancement Although probably a variety of the gyriform pattern, this form of surface enhancement merits separate consideration because of its diagnostic and prognostic implications.
(a) Significance Pathologists identify tuberculous meningitis as a thick gelatinous exudate filling the basal cisterns and enmeshing the arteries at the base of the brain, the latter cafising endarteritic infiltration. Neuroradiologists in pre-CT days were familiar with the radiological signs it produced, namely flaky calcification and arterial stenoses confined to the region of the basal cisterns (Leeds and Goldberg, 1971).
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(b) Diagnosis Computed tomographic evidence of this exudate is found in about two-thirds of patients with advanced tuberculous meningitis. Other infective lesions, such as torulosis and also neoplasms in the meninges, may exhibit cisternal enhancement, but tuberculous meningitis is the diagnosis to consider if this sign is accompanied by hydrocephalus and infarction (Fig. 11). Infarcts are also found in cases of purulent meningitis (Fig. 10) but the presence of the abovementioned triad of signs favours tuberculosis. In proven cases of tuberculosis, all three signs appear to have been prognostic pointers, since children with vivid basal exudates, ganglionic infarcts or a severe degree of hydrocephalus did badly (Rovira et al., 1980; Snyder et al., 1981; Bhargava et al., 1982; Bullock and Welchman, 1982).
REFERENCES
Ascherl, G. F., Hilal, S. K. & Brislnan, R. (1981). Computed tomography of disseminated meningeal and cpendymal malignant neoplasms. Neurology, 31,567-574. Bhargava, S., Gupta, A. K. & Tandon, P. N. (1982). Tuberculous meningitis - a CT study. Briush Journal of Radiology, 55, 189-196. Blaqui~re, R. M. (1983). The computed tomographic appearances of intra- and extracerebral abscesses. British Journal of Radiology, 56, 171-181. Bullock, M. R. R. & Welchman, J. M. (1982). Diagnostic and prognostic features of tuberculous meningitis on CT scanning. Journal of Neurology, Neurosurgery and Psychiatry, 45, 10981101. Danziger, A., Price, H. & Schechter, M. M. (1980). An analysis of 113 intracranial infections. Neuroradiology. 19, 31-34. De Vries, J., Wattendorff, A. R., & Hekster, R. E. M. (1981). Chronic epidural haematoma with partial rim enhancement. Neuroradiology, 22,167-168. Hammock, M. K & Milhorat, T. H. (1981). Cranial Computed Tomography in Infancy and Childhood, p. 119. Williams and Wilkins, Baltimore. Handa, J., Handa, H. & Nakano, Y. (1979). Rim enhancement in CT with chronic epidural hematoma. Surgical Neurology, 11, 217-220. Leeds, N. E. & Goldberg, H. I. (1971). Angiographic manifestations of cerebral inflammatory disease. Radiology, 98, 595-604. Luken, M. G. & Whelan, M. A. (1980). Recent diagnostic experience with subdural empyema. Journal of Neurosurgery, 52, 764-771. Omar, M. M. & Binet, E. F. (1978). Peripheral contrast enhancement in chronic hematomas. Journal of Computer Assisted Tomography, 2, 332-335. Paxton, R. & Ambrose, J. (1974). The EMI scanner. A brief revaew of the first 650 patients. British Journal of Radiology, 47, 53(~565. Rovira, M., Romero, F., Torrent, O. & Ibarra, B. (1980). Study of tuberculous meningitis by CT. Neuroradiology, 19, 137-141. Snyder, R. D., Stovring, J., Cushing, A. H., Davis, L. E. & Hardy, T. L. (1981). Cerebral infarction in childhood bacterial meningitis. Journal of Neurology, Neurosurgery and Psychiatry, 44, 581-585.