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Pseudo-occlusion of the internal carotid artery in raised intracranial pressure
Clin. RadioL (1967) 18, 245-252
PSEUDO-OCCLUSION RAISED
OF THE INTERNAL CAROTID INTRACRANIAL PRESSURE
ARTERY
IN
E. R. DAVIES* and DAVID SUTTON~
From the Departments of Radiology, St. Mary's Hospital, London, W.2., and Maida Vale Hospital (the National Hospitals for Nervous Diseases), London, W.9 Five cases of pseudo-occlusion of the internal carotid artery due to raised intra cranial pressure have been seen in the past 12 years. Four not previously reported are described in detail. One patient had pneumococcal meningitis, a condition previously unreported in this context. The previous literature is reviewed. The characteristic radiographic appearances are described, and the haemodynamic circumstances giving rise to them are discussed. The essential feature is that the intracranial pressure is so high that the cerebral circulation is profoundly slowed. U n d e r these conditions, contrast medium injected into the carotid artery will separate into a dense layer which is responsible for the typical radiographic appearances. Rarely, similar appearances may be encountered in cerebro-vascular disease, when the cerebral circulation is slowed by either a proximal stenosis at the origin of the internal carotid artery, or a distal obstruction beyond the origin of the ophthalmic artery. The prognosis in patients with raised intracranial pressure is grave except when the underlying cause is potentially remediable, e.g. meningioma. The value and hazards of bilateral carotid arteriography in the differentiation of these various conditions is discussed. COMPLETEfailure to fill the internal carotid artery at angiography is usually due to carotid occlusion which gives rise to typical appearances. However, non-filling of the intracranial vessels sometimes follows a technical mishap, such as subinfimal or extra-vascular injection, or a direct injection into the external carotid artery (Newton and Couch, 1960). These appearances are also typical and are unlikely to confuse the experienced radiologist (Sutton, 1962). More rarely, the internal carotid artery fails to fill in its intracranial course even in the absence of arterial occlusion or faulty technique. Riishede and Ethelberg (1953) were the first to describe this phenomenon in 5 moribund patients with acutely raised intracranial pressure. None of these patients survived and at autopsy the internal carotid arteries and their branches were patent in all cases. The paradox between the radiological and pathological appearances is reflected in the term "pseudoocclusion" which has been given to this condition (Newton and Couch, 1960). The characteristic radiological appearances (Fig. 1) are:-1. The external carotid artery and its branches fill well.
2. In the cervical portion of the internal carotid artery there is only a narrow spindly column of contrast medium, which dwindles even further near the base of the skull. 3. The amount of intracranial filling is variable and may even be nil, but delayed films (up to 15 sec. after the injection) often show that some contrast medium has trickled into the carotid syphon (Riishede and Ethelberg, 1953) where it may accumulate (Fox and Hugh, 1964). 4. No contrast medium is usually discernible beyond the carotid syphon. The clinical association between acutely raised intracranial pressure and these appearances is well recognised (Horwitz and Dunsmore, 1956, Pribram, 1961, Mitchell et al., 1962, Aronson and Scatliff, 1962). One such case has already been reported from this hospital (Sutton, 1962), but there is no other account in the British radiological literature. We now report 4 further cases, which illustrate the variety of underlying conditions that may give rise to these appearances, including one cause which has not been described previously. CASE REPORTS Case I . - - A . B . . male. aged 54. He had suffered episodic headaches for 2 years and these had become progressively
* Present address: Bristol General Hospital, Bristol + Reprint requests to this a u t h o r 245
246
C L I N I C A L RADIOLOGY
A B Fro. 1 c D FIG. 1--Case 1. A.B., Male, aged 54. (A) Early phase of R. carotid arteriogram. The external carotid artery and its branches are filling well. The internal carotid artery is filling only in the neck. (B) Later phase. Contrast has cleared from the external carotid system butthereis stillaspindlycolumnofcontrastinthecervicalpartoftheinternalcarotidartery. Thecarotid syphon has filled slowly but there is no filling beyond this. (c) & (D) Similar appearances on the left. The internal carotid artery is filling even less well than on the right. worse for 2 weeks. He was taken to hospital after collapsing at work with severe headache, nausea, and vomiting. On admission his B.P. was 180/95, pulse 65. There were no localising C.N.S. signs. He soon became unconscious with pinpoint pupils and muscular rigidity. After transient recovery of consciousness he was transferred to Maida Vale Hospital for Nervous Diseases, where be was found to be in a deep coma, with fixed dilated pupils. The retinal veins were engorged but there was no papilloedema. Respirations were Cheyne-Stokes in character. Bilateral carotid arteriograms were done under controlled respiration and showed the typical appearances of pseudo-occlusion already described (Fig. 1). A ventrieulogram was then performed. The C.S.F. was heavily blood stained and a large subfrontal mass was shown, mainly on the right side. The clinical diagnosis was ruptured aneurysm of the anterior communicating artery. He died on the day after admission and an autopsy confirmed this diagnosis. The carotid arteries were entirely patent. Case 2.--H. M., male, aged 57. For 6 weeks he had noticed a pain over his right eye; At 12.30 a.m., on the day of admission he awoke with severe headache, vomiting and sweating. His speech was slurred and the left side of his body was weak. He then lost consciousness and fell out of bed. He was admitted to St. Mary's Hospital in a deep coma with pinpoint pupils and extensor plantar responses. There were no localising neurological signs. B.P. 180/115, pulse 64. A lumbar puncture showed uniformly blood stained cerebrospinal fluid under very high pressure. Several hours alter admission spontaneous respiration stopped and artificial respiration was begun. Bilateral carotid arteriograms at this time showed typical appearances of pseudo-occlusion. He died 6 hours later and an autopsy showed a large left intra-
cerebral haemorrhage which had burst into the lateral ventricle. The carotid arteries were entirely patent. Case 3.--F.M., male, aged 59. For 3 weeks he had had anorexia, thirst, polyuria and weakness, with severe frontal headaches. His wife had noticed that he had become increasingly drowsy and irritable, and that he tended to fall. His hands were clumsy, and he h a d been incontinent for a few days before admission. He was a heavy smoker and had a severe cough. On examination his B.P. was 110/80, pulse 50. He was dehydrated and drowsy, with slurred speech, and he frequently licked his lips. The right pupil was larger than the left and both reacted to the light. There was slight papilloedema on the left and optic atrophy on the right. The left side of his face, and all 4 limbs were weak, and there was some loss of pain sensation in the left arm and leg. The blood sugar on admission was 340 mg. ~ . Within 1 hour of admission he suddenly became deeply unconscious and the weakness of his left arm increased. Both pupils were dilated and fixed. Respirations were Cheynes-Stokes in character. A right carotid arteriogram was carried out under controlled respiration and showed typical appearances of pseudoocclusion (Fig. 2): A chest x-ray showed 2 opacities in the right lower lobe). The clinical and radiological diagnosis was diabetes mellitus with primary bronchial carcinoma and cerebral metastasis. He died on the day after admission° An autopsy confirmed the presence of a peripheral carcinoma of the right lung with widespread visceral and glandular deposits. There was a solitary intracraniat deposit, 4 cm. diameter, in the right occipital lobe, with diffuse cerebral oedema, more on the right than on the left. There was no evidence of tentorial herniation, and the cerebral arteries were entirely normal. Case 4.--Schoolboy, aged t4. On 22nd January 1965,
P S E U D O - O C C L U S I O N OF THE I N T E R N A L CAROTID ARTERY
247
A FIO. 2 B Fro. 2. Case 3. F.M., Male, aged 59. (A) Early phase of typical pseudo-occlusion of the right internal carotid artery. (B) Later phase of the same injection. The films are viewed in the position in which they were taken, and the contrast is seen to form a dense layer along the most dependent wall of the artery.
Fm. 3 Case 4. D.A. Male, aged 14. Consolidation in the leR lower lobe.
respiratory effort. He was drowsy, responding only to simple commands, and had neck stiffness and brisk reflexes. A lumbar puncture produced dear cerebrospinal fluid at a pressure of 90 mm. Hg., with free rise and fall. The fluid contained protein 900 mg./100 ml., glucose 1 rag./100 ml. ; polymorphonuclear leucocytes 400/c.mm., and many Gram positive diplococci with the characteristics of pneumococci. Similar organisms were found in the sputum, but cultures of both cerebrospinal fluid and sputum were negative. The clinical diagnosis was lobar pneumonia and pneumococcal meningitis, and he was treated with penicillin, given intramuscularly, intrathecally, and intravenously. On the 2rid day of admission he developed a widespread erythema, which was thought to be allergic. Penicillin was therefore discontinued. At this time his temperature became too low to be recorded, all spontaneous respiration ceased, and his reflexes could not be elicited. A right carotid arteriogram showed typical appearances of pseudo-occlusion with non-filling beyond the base of the skull (Fig. 4). He died later that day. Autopsy confirmed the pneumonia and meningitis. The brain was oedematous and the cerebral convolutions were flattened. There was a considerable amount of pus in the subarachnoid space especially over the frontal lobes and vertex, as well as at the base of the brain. There was nolocalised intracerebral abscess, and there was no evidence of coning. The cerebral arteries were entirely normal. DISCUSSION
while at school, he developed left chest pain, with vomiting and shivering. His temperature was 103°F., and he had a productive cough with green sputum. On the 3rd day of the illness, he became delirious and was given Novobiocin and Tetracycline by his practitioner. (He had a past history of giant urticaria, asthma, and rhinitis, triggered by excitement, and by aspirin. Nevertheless, he had been given penicillin at the age of 5 without ill effect.) On the 4th day of the illness he was admitted to St. Mary's Hospital. He had signs of a left lower lobe pneumonia, which was confirmed by x-ray (Fig. 3). A tracheostomy was carried out because of respiratory distress, and he was put on a Bennett respirator which was triggered by his own
PATHOLOGY P s e u d o - o c c l u s i o n h a s b e e n r e p o r t e d in t h e c a r o t i d a r t e r y in 25 cases, a n d in t h e b a s i l a r a r t e r y in o n e case ( P r i b r a m , 1961). P o s t m o r t e m c o n f i r m a t i o n w a s o b t a i n e d in 24 o f t h e s e 26 cases. T h e c o m m o n est u n d e r l y i n g c a u s e w a s i n t r a c r a n i a l h a e m o r r h a g e (15 cases), b u t p r i m a r y n e o p l a s m , a b s c e s s , a n d t r a u m a h a v e also b e e n r e c o r d e d ( T a b l e 1 ), illustrating t h e w i d e r a n g e o f a n t e c e d e n t c a u s e s t h a t m a y be found.
248
CLINICAL
RADIOLOGY
A FI~. 4 FIG. 4.--Case 4. Right carotid arteriograms to show typical pseudo-occlusion. (A) Early phase. (B) Later phase. There is no intracranial filling. TABLE 1 CAUSES OF PSEUDO-OCCLUSION IN 27 CASES PREVIOUSLY REPORTED IN THE LITERATURE~ AND EXCLUDING PRESENT SERIES
Aetiology
No. of cases
7/
I. Intracranial Haemorrhage (a) Subarachnoid (i) Aneurysm (ii) No Aneurysm (b) Intracerebral
3
12 2. Neoplasm (a) Angioma (b) Glioblastoma (bilateral) (c) Meningioma (d) Cerebellar cyst
3. Trauma (a) Cerebral laceration (b) Subdural h a e m a t o m a
-
4
4. Infection (a) Pyogenic abscess (b) Tuberculous abscess -
!
~ Total
f
/
4 27
The clinical feature common to all these cases was acutely raised intracranial pressure. All except 2 were in coma at the time of the examination and 16 required artificial respiration. The intracranial pressure was similarly raised in our cases, all of which were examined under controlled respiration. The underlying pathology was different in each of our cases. Ruptured intracranial aneurysm (Case 1) and cerebral haemorrhage (Case 2) have been reported frequently in other series (Table 1). A cerebral metastasis (Case 3), though not reported previously, presumably behaves in this respect like a primary tumour or abscess, both of which have been reported. However, Case 4 in our series is unique, because it is the first time that pseudo-occlusion has been described in any form of meningitis. There was no localised expanding lesion in this patient, but there was a thick purulent exudate in the basal cisterns and over the vertex, which is one of the characteristic features ofpneumococcal meningitis. An exudate in these sites impairs the absorption of cerebrospinal fluid by the arachnoid villi and obstructs its outflow from the 4th ventricle, giving rise t o an internal hydrocephalus (Brain, 1955), thereby increasing the intracranial pressure.
PSEUDO-OCCLUSION
OF T H E I N T E R N A L
A case previously reported from this hospital and included in Table 1 is also of considerable interest (Sutton, 1962). The patient, a vagrant, was admitted in coma, without any available previous history, and carotid arteriography showed typical pseudoocclusion, without intracranial filling. The patient did not recover consciousness, and died shortly afterwards. Surprisingly, the autopsy showed a large frontal meningioma, which had been unsuspected clinically. Because of the absence of intracranial arterial filling, the arteriogram did not help either. However, in a similar case reported by Riishade and Ethelberg (1953), the arteriogram was of great value, because it showed an unsuspected meningioma which was partly supplied from the external carotid artery. As a result, they were able to remove the tumour, and the patient recovered from the operation, but died from a pulmonary embolus 24 days later. These 2 cases are the only recorded examples of pseudo-occlusion due to meningioma and they are important because they illustrate that the condition is potentially reversible in some patients. Usually it is not reversible, and the high incidence of intracranial haemorrhage in the reported series reflects the greater frequency of sudden coma in this condition. AETIOLOGY The way in which raised intracranial pressure brings about the characteristic appearances of the arteriogram has been poorly understood until recently. The main possibilities which have been considered are : Spasm of smaller intracranial arteries after subarachnoid haemorrhage is not uncommon (Johnson et al., 1958; Pribram, 1961), but spasm of a major vessel, such as the internal carotid artery in the neck, has only been reported in the presence of direct trauma (Ecker, 1945), faulty injection (Decker, 1956), or surgical traction (Ecker and Riemenschneider, 1951). Thus spasm could not explain the appearances in many cases. Tentorial Herniation after a sudden rise of intracranial pressure may lead to aqueduct compression. This could lead to a vicious circle, raising the supratentorial pressure until the carotid arteries are obliterated (Riishede and Ethelberg, 1953), and survival depends on the patency of the basilar artery. The absence of any postmortem evidence of herniation in 8 of the reported cases, and in our 3rd case, together with the demonstration of basilar pseudo-occlusion by Pribram (1961), make this theory untenable.
CAROTID
ARTERY
249
Total Occlusion by External Pressure.--If there were a general rise in intracranial pressure sufficient to occlude the internal carotid artery completely, the basilar artery would be occluded also, and the patients would not have survived even as long as they did. In fact contrast medium is not always held up precisely at the point where the artery enters the cranium, but often extends up to 1 cm. beyond this. This makes total occlusion by external pressure very unlikely, and it becomes illogical to assume that the arteries are totally occluded or that the flow has ceased completely. Thus in order to explain the radiological appearances it is necessary to consider some recent studies. The Physiological Effects of Raising the Intracranial Pressure.--The mechanisms which control the cerebral circulation are complicated and incompletely understood, and the level of intracranial pressure is only 1 of the factors concerned (Evans et al., 1951). Experimental work by Mitchell et aI. (1962), using angiographic techniques, in the dog and the monkey showed that there were 2 significant levels of intracranial pressure. Intracranial Pressure Equal to Diastolic Blood Pressure.--At this level spontaneous respiration invariably ceased. The parallel between this observation and the clinical observation that most of the patients with pseudo-occlusion were in need of artificial respiration is clear. Intraeranial Pressure Equal to Systolic Blood Pressure.--At this level the intracranial vessels could not be filled under standard conditions of injection, although it was still possible to produce some filling by means of a forced injection under very high pressure. If the intracranial pressure were then reduced, the vessels could be filled immediately. The clinical significance of these observations had already been anticipated by Pribram (1961). In 1 of his cases, a typical example of carotid pseudoocclusion, the intra-carotid needle was left in situ while the brain was decompressed. A further injection then showed good intracranial filling and outlined a large inoperable choroid plexus angioma. It remains undecided whether or not the intracranial pressure in man ever rises as high as the systolic blood pressure. The important point is that even at levels below this there is a profound fall in cerebral perfusion (Mitchell et al.. 1962), and the implications of this will be discussed in the following section. The Haemodynamic Effect of Injecting Contrast into a Slow Circulation.--Fox and Hugh (1964) have made a detailed study of haemodynamics and their results are of the greatest importance. They
250
CLINICAL
have shown that angiographic contrast material vail always tend to separate out from the blood after initial mixing produced by rapid injection. Differences of temperature and specific gravity increase this tendency, but under normal conditions of flow, complete filling of the arterial tree is apparently unaffected. However, if the flow is poor, contrast medium separates much more readily, forming a layer along the most dependent aspect of the vessel. When the patient is supine contrast will run along the posterior wall of the internal carotid artery as it lies in the neck. This is best understood if the radiograph is viewed in the position in which it was taken (Fox and Hugh, 1964). This clearly shows the upper level of the contrast layer (Fig. 2). If the head is at a higher level than the origin of the common carotid artery, some contrast will even run back into the thorax. Most of it will trickle gradually into the carotid syphon, and some of it will accumulate there because it is heavier than blood, and the head of pressure is too small to raise it further. In this way it can have the same effect as an air lock, and so obstruct the flow of blood altogether (Fox and Hugh, 1964).
RADIOLOGY
Thus the radiographic appearances of pseudoocclusion can be explained in terms of the haemodynamic effect of injecting dense contrast material into a circulation which has been greatly slowed by rising intracranial pressure. Among those reported cases which had bilateral arteriograms, there are three cases in whom the appearances were unilateral (Riishede and Ethelberg, 1953; Horwitz and Dunsmore, 1956; Pribram, 1961), an event which does not seem to conform to this theory. However the reported clinical histories of these cases suggests that the intracranial pressure had changed between the 2 examinations, either because of cerebral decompression, with improvement; or because of progression of the symptoms, with deterioration. Thus the theory may also be valid in these cases. PROGNOSIS Immediate.--The immediate prognosis is always poor, because the patients are usually gravely ill when arteriography is undertaken. Death has been reported during or immediately after arteriography in 4 cases (Horwitz and Dunsmore, 1956; Pribram,
A Fro. 5 B FIG. 5--J., Female, aged 33. The internal carotid artery is occluded immediately beyond the origin of the ophthalmic artery, which fills well.(T ) (A) Early phase. The superficial temporal artery is superimposed on the obstruction. (~) Later phase showing layering in the internal carotid artery after contrast has cleared from the external carotid system.
PSEUDO-OCCLUSION
OF T H E I N T E R N A L C A R O T I D A R T E R Y
1961; Mitchell et al., 1962). Arteriography itself may make a major contribution to this because the pooling of contrast in the carotid syphon, which has already been described, can obstruct the flow of blood altogether. Bilateral examination under these conditions could easily be fatal (Fox and Hugh, 1964). The effect can be countered by lowering the patient's head during the examination to help forward arterial flow, and raising the head after the injection to allow the denser contrast to run back into the aorta (Fox and Hugh, 1964). Long Term.--The long term prognosis is that of the underlying condition and nearly all the reported cases have died within a few days of admission to hospital. There are 2 notable exceptions. The first of these had a parasagittal meningioma which was partly outlined from the external carotid, and which was completely removed. Unfortunately the patient, a 74-year-old man, died of a pulmonary embolus on the 24th postoperative day (Riishede and Ethelberg, 1953). The second reported survivor recovered after bleeding from an angioma of the
251
choroid plexus which had been demonstrated after cerebral decompression (Pribram, 1961). The possibility Of survival in exceptional cases emphasises the need to establish the cause of the raised intracranial pressure, however ill the patient may be. Ventriculography is sometimes valuable (Riischede and Ethelberg, 1953; Horwitz and Dunsmore, 1956; Mitchell et al., 1963). Bilateral carotid arteriography before and after cerebral decompression has been advocated by Pribram (1961). DIFFERENTIAL DIAGNOSIS The demonstration of contrast medium layering in the carotid arteries of comatose patients is generally regarded as pathognomonic of raised intracranial pressure from any of the many causes already listed. We have already seen that the only essential prerequisite for such layering is a slow cerebral circulation. Therefore layering might be expected to occur even in the absence of raised intracranial S
A Fro. 6 B FIG. 6 (A & B)--E. Male, aged 65. Left carotid arteriogram. The appearances of the late film resemble pseudo-occlusion, but the layering is due to a stenosis of the origin of the internal carotid artery, which can be recognised clearly in the early arterial phase.
252
CLINICAL RADIOLOGY
pressure provided that the cerebral circulation were slow enough. Thus it may occur following internal carotid occlusion distal to the origin of the ophthalmic artery (Murphey and Shillitoe, 1959; Newton and Couch, 1960; Pribram, 1961). These authors suggest that a distal obstruction will not stop the internal carotid flow altogether provided there is a patent run-off via the ophthalmic artery, but will produce sufficient slowing of the circulation to cause layering. Fig. 5 shows such an appearance in a 33 year old woman who presented with hemiplegia. This is a unique case because both internal carotid arteries were congenitally hypoplastic distal to the ophthalmic arteries and had become occluded at this level. Those patients in whom the layering is due to distal obstruction can usually be distinguished by their clinical features. Nearly all those so far reported presented with hemiplegia; none were in coma or had any evidence of raised intracranial pressure. Appearances similar to layering but due to stenosis at the origin of the internal carotid artery are readily distinguished arteriographically (Fig; 6).
The importance of distinguishing the cause of the raised intracranial pressure in the comatose group has been discussed already. REFERENCES ARONSON,H. A., SCATLIFF,J. H. (1962). J. Neurosurg., 19, 691. BRAIN,R. (1955). Diseases of the Nervous System. London: Oxford University Press. DECKER, K. (1956). Acta radioL, 46, 351. ECKER,A. D. (1945). or. Neurosurg., 2, 47. ECKER,A. & RIEMENSCHNEIDER,P. A. (1951). J. Neurosurg., 8, 660. EVANS,J. P., ESPEY,F. F., KRISTOFF,F. V., KIMBELL,F. D., & RYDER,H. W. (1951). Arch. Surg. (Chic.), 63, 107. Fox, J. A., HUGH,A. E. (1964). Clin. RadioL, 15, 183. HORWITZ, N. H. & DUNSMORE, R. I'{. (1956). J. Neurosurg., 13, 155. JOHNSON,R. J., POTTER,J. M., REID,R. G. (1958). J. Neurol. Neuro~'urg. Psychiat., 21, 68. MITCHELL, O. C., DE LA TORRE, E., ALEXANDER, E.,
DAVIE,C. H. (1962). or. Neurosurg., 19, 766. NEWTON,T. H., COUCH,R. S. C. (1960). Radiology, 75, 766. PR~BRAM,H. F. W. (1961). Neurol. (Minneap.), 11, 10. RIISHEDE,J. & ETI-rSLBERG,S. (1953). Arch. Neurol. Psychiat., 70, 399. SUTTON,D. (1962). Arteriography. Edinburgh: Livingstone.
PSEUDO-OCCLUSION RAISED
OF THE INTERNAL CAROTID INTRACRANIAL PRESSURE
ARTERY
IN
E. R. DAVIES* and DAVID SUTTON~
From the Departments of Radiology, St. Mary's Hospital, London, W.2., and Maida Vale Hospital (the National Hospitals for Nervous Diseases), London, W.9 Five cases of pseudo-occlusion of the internal carotid artery due to raised intra cranial pressure have been seen in the past 12 years. Four not previously reported are described in detail. One patient had pneumococcal meningitis, a condition previously unreported in this context. The previous literature is reviewed. The characteristic radiographic appearances are described, and the haemodynamic circumstances giving rise to them are discussed. The essential feature is that the intracranial pressure is so high that the cerebral circulation is profoundly slowed. U n d e r these conditions, contrast medium injected into the carotid artery will separate into a dense layer which is responsible for the typical radiographic appearances. Rarely, similar appearances may be encountered in cerebro-vascular disease, when the cerebral circulation is slowed by either a proximal stenosis at the origin of the internal carotid artery, or a distal obstruction beyond the origin of the ophthalmic artery. The prognosis in patients with raised intracranial pressure is grave except when the underlying cause is potentially remediable, e.g. meningioma. The value and hazards of bilateral carotid arteriography in the differentiation of these various conditions is discussed. COMPLETEfailure to fill the internal carotid artery at angiography is usually due to carotid occlusion which gives rise to typical appearances. However, non-filling of the intracranial vessels sometimes follows a technical mishap, such as subinfimal or extra-vascular injection, or a direct injection into the external carotid artery (Newton and Couch, 1960). These appearances are also typical and are unlikely to confuse the experienced radiologist (Sutton, 1962). More rarely, the internal carotid artery fails to fill in its intracranial course even in the absence of arterial occlusion or faulty technique. Riishede and Ethelberg (1953) were the first to describe this phenomenon in 5 moribund patients with acutely raised intracranial pressure. None of these patients survived and at autopsy the internal carotid arteries and their branches were patent in all cases. The paradox between the radiological and pathological appearances is reflected in the term "pseudoocclusion" which has been given to this condition (Newton and Couch, 1960). The characteristic radiological appearances (Fig. 1) are:-1. The external carotid artery and its branches fill well.
2. In the cervical portion of the internal carotid artery there is only a narrow spindly column of contrast medium, which dwindles even further near the base of the skull. 3. The amount of intracranial filling is variable and may even be nil, but delayed films (up to 15 sec. after the injection) often show that some contrast medium has trickled into the carotid syphon (Riishede and Ethelberg, 1953) where it may accumulate (Fox and Hugh, 1964). 4. No contrast medium is usually discernible beyond the carotid syphon. The clinical association between acutely raised intracranial pressure and these appearances is well recognised (Horwitz and Dunsmore, 1956, Pribram, 1961, Mitchell et al., 1962, Aronson and Scatliff, 1962). One such case has already been reported from this hospital (Sutton, 1962), but there is no other account in the British radiological literature. We now report 4 further cases, which illustrate the variety of underlying conditions that may give rise to these appearances, including one cause which has not been described previously. CASE REPORTS Case I . - - A . B . . male. aged 54. He had suffered episodic headaches for 2 years and these had become progressively
* Present address: Bristol General Hospital, Bristol + Reprint requests to this a u t h o r 245
246
C L I N I C A L RADIOLOGY
A B Fro. 1 c D FIG. 1--Case 1. A.B., Male, aged 54. (A) Early phase of R. carotid arteriogram. The external carotid artery and its branches are filling well. The internal carotid artery is filling only in the neck. (B) Later phase. Contrast has cleared from the external carotid system butthereis stillaspindlycolumnofcontrastinthecervicalpartoftheinternalcarotidartery. Thecarotid syphon has filled slowly but there is no filling beyond this. (c) & (D) Similar appearances on the left. The internal carotid artery is filling even less well than on the right. worse for 2 weeks. He was taken to hospital after collapsing at work with severe headache, nausea, and vomiting. On admission his B.P. was 180/95, pulse 65. There were no localising C.N.S. signs. He soon became unconscious with pinpoint pupils and muscular rigidity. After transient recovery of consciousness he was transferred to Maida Vale Hospital for Nervous Diseases, where be was found to be in a deep coma, with fixed dilated pupils. The retinal veins were engorged but there was no papilloedema. Respirations were Cheyne-Stokes in character. Bilateral carotid arteriograms were done under controlled respiration and showed the typical appearances of pseudo-occlusion already described (Fig. 1). A ventrieulogram was then performed. The C.S.F. was heavily blood stained and a large subfrontal mass was shown, mainly on the right side. The clinical diagnosis was ruptured aneurysm of the anterior communicating artery. He died on the day after admission and an autopsy confirmed this diagnosis. The carotid arteries were entirely patent. Case 2.--H. M., male, aged 57. For 6 weeks he had noticed a pain over his right eye; At 12.30 a.m., on the day of admission he awoke with severe headache, vomiting and sweating. His speech was slurred and the left side of his body was weak. He then lost consciousness and fell out of bed. He was admitted to St. Mary's Hospital in a deep coma with pinpoint pupils and extensor plantar responses. There were no localising neurological signs. B.P. 180/115, pulse 64. A lumbar puncture showed uniformly blood stained cerebrospinal fluid under very high pressure. Several hours alter admission spontaneous respiration stopped and artificial respiration was begun. Bilateral carotid arteriograms at this time showed typical appearances of pseudo-occlusion. He died 6 hours later and an autopsy showed a large left intra-
cerebral haemorrhage which had burst into the lateral ventricle. The carotid arteries were entirely patent. Case 3.--F.M., male, aged 59. For 3 weeks he had had anorexia, thirst, polyuria and weakness, with severe frontal headaches. His wife had noticed that he had become increasingly drowsy and irritable, and that he tended to fall. His hands were clumsy, and he h a d been incontinent for a few days before admission. He was a heavy smoker and had a severe cough. On examination his B.P. was 110/80, pulse 50. He was dehydrated and drowsy, with slurred speech, and he frequently licked his lips. The right pupil was larger than the left and both reacted to the light. There was slight papilloedema on the left and optic atrophy on the right. The left side of his face, and all 4 limbs were weak, and there was some loss of pain sensation in the left arm and leg. The blood sugar on admission was 340 mg. ~ . Within 1 hour of admission he suddenly became deeply unconscious and the weakness of his left arm increased. Both pupils were dilated and fixed. Respirations were Cheynes-Stokes in character. A right carotid arteriogram was carried out under controlled respiration and showed typical appearances of pseudoocclusion (Fig. 2): A chest x-ray showed 2 opacities in the right lower lobe). The clinical and radiological diagnosis was diabetes mellitus with primary bronchial carcinoma and cerebral metastasis. He died on the day after admission° An autopsy confirmed the presence of a peripheral carcinoma of the right lung with widespread visceral and glandular deposits. There was a solitary intracraniat deposit, 4 cm. diameter, in the right occipital lobe, with diffuse cerebral oedema, more on the right than on the left. There was no evidence of tentorial herniation, and the cerebral arteries were entirely normal. Case 4.--Schoolboy, aged t4. On 22nd January 1965,
P S E U D O - O C C L U S I O N OF THE I N T E R N A L CAROTID ARTERY
247
A FIO. 2 B Fro. 2. Case 3. F.M., Male, aged 59. (A) Early phase of typical pseudo-occlusion of the right internal carotid artery. (B) Later phase of the same injection. The films are viewed in the position in which they were taken, and the contrast is seen to form a dense layer along the most dependent wall of the artery.
Fm. 3 Case 4. D.A. Male, aged 14. Consolidation in the leR lower lobe.
respiratory effort. He was drowsy, responding only to simple commands, and had neck stiffness and brisk reflexes. A lumbar puncture produced dear cerebrospinal fluid at a pressure of 90 mm. Hg., with free rise and fall. The fluid contained protein 900 mg./100 ml., glucose 1 rag./100 ml. ; polymorphonuclear leucocytes 400/c.mm., and many Gram positive diplococci with the characteristics of pneumococci. Similar organisms were found in the sputum, but cultures of both cerebrospinal fluid and sputum were negative. The clinical diagnosis was lobar pneumonia and pneumococcal meningitis, and he was treated with penicillin, given intramuscularly, intrathecally, and intravenously. On the 2rid day of admission he developed a widespread erythema, which was thought to be allergic. Penicillin was therefore discontinued. At this time his temperature became too low to be recorded, all spontaneous respiration ceased, and his reflexes could not be elicited. A right carotid arteriogram showed typical appearances of pseudo-occlusion with non-filling beyond the base of the skull (Fig. 4). He died later that day. Autopsy confirmed the pneumonia and meningitis. The brain was oedematous and the cerebral convolutions were flattened. There was a considerable amount of pus in the subarachnoid space especially over the frontal lobes and vertex, as well as at the base of the brain. There was nolocalised intracerebral abscess, and there was no evidence of coning. The cerebral arteries were entirely normal. DISCUSSION
while at school, he developed left chest pain, with vomiting and shivering. His temperature was 103°F., and he had a productive cough with green sputum. On the 3rd day of the illness, he became delirious and was given Novobiocin and Tetracycline by his practitioner. (He had a past history of giant urticaria, asthma, and rhinitis, triggered by excitement, and by aspirin. Nevertheless, he had been given penicillin at the age of 5 without ill effect.) On the 4th day of the illness he was admitted to St. Mary's Hospital. He had signs of a left lower lobe pneumonia, which was confirmed by x-ray (Fig. 3). A tracheostomy was carried out because of respiratory distress, and he was put on a Bennett respirator which was triggered by his own
PATHOLOGY P s e u d o - o c c l u s i o n h a s b e e n r e p o r t e d in t h e c a r o t i d a r t e r y in 25 cases, a n d in t h e b a s i l a r a r t e r y in o n e case ( P r i b r a m , 1961). P o s t m o r t e m c o n f i r m a t i o n w a s o b t a i n e d in 24 o f t h e s e 26 cases. T h e c o m m o n est u n d e r l y i n g c a u s e w a s i n t r a c r a n i a l h a e m o r r h a g e (15 cases), b u t p r i m a r y n e o p l a s m , a b s c e s s , a n d t r a u m a h a v e also b e e n r e c o r d e d ( T a b l e 1 ), illustrating t h e w i d e r a n g e o f a n t e c e d e n t c a u s e s t h a t m a y be found.
248
CLINICAL
RADIOLOGY
A FI~. 4 FIG. 4.--Case 4. Right carotid arteriograms to show typical pseudo-occlusion. (A) Early phase. (B) Later phase. There is no intracranial filling. TABLE 1 CAUSES OF PSEUDO-OCCLUSION IN 27 CASES PREVIOUSLY REPORTED IN THE LITERATURE~ AND EXCLUDING PRESENT SERIES
Aetiology
No. of cases
7/
I. Intracranial Haemorrhage (a) Subarachnoid (i) Aneurysm (ii) No Aneurysm (b) Intracerebral
3
12 2. Neoplasm (a) Angioma (b) Glioblastoma (bilateral) (c) Meningioma (d) Cerebellar cyst
3. Trauma (a) Cerebral laceration (b) Subdural h a e m a t o m a
-
4
4. Infection (a) Pyogenic abscess (b) Tuberculous abscess -
!
~ Total
f
/
4 27
The clinical feature common to all these cases was acutely raised intracranial pressure. All except 2 were in coma at the time of the examination and 16 required artificial respiration. The intracranial pressure was similarly raised in our cases, all of which were examined under controlled respiration. The underlying pathology was different in each of our cases. Ruptured intracranial aneurysm (Case 1) and cerebral haemorrhage (Case 2) have been reported frequently in other series (Table 1). A cerebral metastasis (Case 3), though not reported previously, presumably behaves in this respect like a primary tumour or abscess, both of which have been reported. However, Case 4 in our series is unique, because it is the first time that pseudo-occlusion has been described in any form of meningitis. There was no localised expanding lesion in this patient, but there was a thick purulent exudate in the basal cisterns and over the vertex, which is one of the characteristic features ofpneumococcal meningitis. An exudate in these sites impairs the absorption of cerebrospinal fluid by the arachnoid villi and obstructs its outflow from the 4th ventricle, giving rise t o an internal hydrocephalus (Brain, 1955), thereby increasing the intracranial pressure.
PSEUDO-OCCLUSION
OF T H E I N T E R N A L
A case previously reported from this hospital and included in Table 1 is also of considerable interest (Sutton, 1962). The patient, a vagrant, was admitted in coma, without any available previous history, and carotid arteriography showed typical pseudoocclusion, without intracranial filling. The patient did not recover consciousness, and died shortly afterwards. Surprisingly, the autopsy showed a large frontal meningioma, which had been unsuspected clinically. Because of the absence of intracranial arterial filling, the arteriogram did not help either. However, in a similar case reported by Riishade and Ethelberg (1953), the arteriogram was of great value, because it showed an unsuspected meningioma which was partly supplied from the external carotid artery. As a result, they were able to remove the tumour, and the patient recovered from the operation, but died from a pulmonary embolus 24 days later. These 2 cases are the only recorded examples of pseudo-occlusion due to meningioma and they are important because they illustrate that the condition is potentially reversible in some patients. Usually it is not reversible, and the high incidence of intracranial haemorrhage in the reported series reflects the greater frequency of sudden coma in this condition. AETIOLOGY The way in which raised intracranial pressure brings about the characteristic appearances of the arteriogram has been poorly understood until recently. The main possibilities which have been considered are : Spasm of smaller intracranial arteries after subarachnoid haemorrhage is not uncommon (Johnson et al., 1958; Pribram, 1961), but spasm of a major vessel, such as the internal carotid artery in the neck, has only been reported in the presence of direct trauma (Ecker, 1945), faulty injection (Decker, 1956), or surgical traction (Ecker and Riemenschneider, 1951). Thus spasm could not explain the appearances in many cases. Tentorial Herniation after a sudden rise of intracranial pressure may lead to aqueduct compression. This could lead to a vicious circle, raising the supratentorial pressure until the carotid arteries are obliterated (Riishede and Ethelberg, 1953), and survival depends on the patency of the basilar artery. The absence of any postmortem evidence of herniation in 8 of the reported cases, and in our 3rd case, together with the demonstration of basilar pseudo-occlusion by Pribram (1961), make this theory untenable.
CAROTID
ARTERY
249
Total Occlusion by External Pressure.--If there were a general rise in intracranial pressure sufficient to occlude the internal carotid artery completely, the basilar artery would be occluded also, and the patients would not have survived even as long as they did. In fact contrast medium is not always held up precisely at the point where the artery enters the cranium, but often extends up to 1 cm. beyond this. This makes total occlusion by external pressure very unlikely, and it becomes illogical to assume that the arteries are totally occluded or that the flow has ceased completely. Thus in order to explain the radiological appearances it is necessary to consider some recent studies. The Physiological Effects of Raising the Intracranial Pressure.--The mechanisms which control the cerebral circulation are complicated and incompletely understood, and the level of intracranial pressure is only 1 of the factors concerned (Evans et al., 1951). Experimental work by Mitchell et aI. (1962), using angiographic techniques, in the dog and the monkey showed that there were 2 significant levels of intracranial pressure. Intracranial Pressure Equal to Diastolic Blood Pressure.--At this level spontaneous respiration invariably ceased. The parallel between this observation and the clinical observation that most of the patients with pseudo-occlusion were in need of artificial respiration is clear. Intraeranial Pressure Equal to Systolic Blood Pressure.--At this level the intracranial vessels could not be filled under standard conditions of injection, although it was still possible to produce some filling by means of a forced injection under very high pressure. If the intracranial pressure were then reduced, the vessels could be filled immediately. The clinical significance of these observations had already been anticipated by Pribram (1961). In 1 of his cases, a typical example of carotid pseudoocclusion, the intra-carotid needle was left in situ while the brain was decompressed. A further injection then showed good intracranial filling and outlined a large inoperable choroid plexus angioma. It remains undecided whether or not the intracranial pressure in man ever rises as high as the systolic blood pressure. The important point is that even at levels below this there is a profound fall in cerebral perfusion (Mitchell et al.. 1962), and the implications of this will be discussed in the following section. The Haemodynamic Effect of Injecting Contrast into a Slow Circulation.--Fox and Hugh (1964) have made a detailed study of haemodynamics and their results are of the greatest importance. They
250
CLINICAL
have shown that angiographic contrast material vail always tend to separate out from the blood after initial mixing produced by rapid injection. Differences of temperature and specific gravity increase this tendency, but under normal conditions of flow, complete filling of the arterial tree is apparently unaffected. However, if the flow is poor, contrast medium separates much more readily, forming a layer along the most dependent aspect of the vessel. When the patient is supine contrast will run along the posterior wall of the internal carotid artery as it lies in the neck. This is best understood if the radiograph is viewed in the position in which it was taken (Fox and Hugh, 1964). This clearly shows the upper level of the contrast layer (Fig. 2). If the head is at a higher level than the origin of the common carotid artery, some contrast will even run back into the thorax. Most of it will trickle gradually into the carotid syphon, and some of it will accumulate there because it is heavier than blood, and the head of pressure is too small to raise it further. In this way it can have the same effect as an air lock, and so obstruct the flow of blood altogether (Fox and Hugh, 1964).
RADIOLOGY
Thus the radiographic appearances of pseudoocclusion can be explained in terms of the haemodynamic effect of injecting dense contrast material into a circulation which has been greatly slowed by rising intracranial pressure. Among those reported cases which had bilateral arteriograms, there are three cases in whom the appearances were unilateral (Riishede and Ethelberg, 1953; Horwitz and Dunsmore, 1956; Pribram, 1961), an event which does not seem to conform to this theory. However the reported clinical histories of these cases suggests that the intracranial pressure had changed between the 2 examinations, either because of cerebral decompression, with improvement; or because of progression of the symptoms, with deterioration. Thus the theory may also be valid in these cases. PROGNOSIS Immediate.--The immediate prognosis is always poor, because the patients are usually gravely ill when arteriography is undertaken. Death has been reported during or immediately after arteriography in 4 cases (Horwitz and Dunsmore, 1956; Pribram,
A Fro. 5 B FIG. 5--J., Female, aged 33. The internal carotid artery is occluded immediately beyond the origin of the ophthalmic artery, which fills well.(T ) (A) Early phase. The superficial temporal artery is superimposed on the obstruction. (~) Later phase showing layering in the internal carotid artery after contrast has cleared from the external carotid system.
PSEUDO-OCCLUSION
OF T H E I N T E R N A L C A R O T I D A R T E R Y
1961; Mitchell et al., 1962). Arteriography itself may make a major contribution to this because the pooling of contrast in the carotid syphon, which has already been described, can obstruct the flow of blood altogether. Bilateral examination under these conditions could easily be fatal (Fox and Hugh, 1964). The effect can be countered by lowering the patient's head during the examination to help forward arterial flow, and raising the head after the injection to allow the denser contrast to run back into the aorta (Fox and Hugh, 1964). Long Term.--The long term prognosis is that of the underlying condition and nearly all the reported cases have died within a few days of admission to hospital. There are 2 notable exceptions. The first of these had a parasagittal meningioma which was partly outlined from the external carotid, and which was completely removed. Unfortunately the patient, a 74-year-old man, died of a pulmonary embolus on the 24th postoperative day (Riishede and Ethelberg, 1953). The second reported survivor recovered after bleeding from an angioma of the
251
choroid plexus which had been demonstrated after cerebral decompression (Pribram, 1961). The possibility Of survival in exceptional cases emphasises the need to establish the cause of the raised intracranial pressure, however ill the patient may be. Ventriculography is sometimes valuable (Riischede and Ethelberg, 1953; Horwitz and Dunsmore, 1956; Mitchell et al., 1963). Bilateral carotid arteriography before and after cerebral decompression has been advocated by Pribram (1961). DIFFERENTIAL DIAGNOSIS The demonstration of contrast medium layering in the carotid arteries of comatose patients is generally regarded as pathognomonic of raised intracranial pressure from any of the many causes already listed. We have already seen that the only essential prerequisite for such layering is a slow cerebral circulation. Therefore layering might be expected to occur even in the absence of raised intracranial S
A Fro. 6 B FIG. 6 (A & B)--E. Male, aged 65. Left carotid arteriogram. The appearances of the late film resemble pseudo-occlusion, but the layering is due to a stenosis of the origin of the internal carotid artery, which can be recognised clearly in the early arterial phase.
252
CLINICAL RADIOLOGY
pressure provided that the cerebral circulation were slow enough. Thus it may occur following internal carotid occlusion distal to the origin of the ophthalmic artery (Murphey and Shillitoe, 1959; Newton and Couch, 1960; Pribram, 1961). These authors suggest that a distal obstruction will not stop the internal carotid flow altogether provided there is a patent run-off via the ophthalmic artery, but will produce sufficient slowing of the circulation to cause layering. Fig. 5 shows such an appearance in a 33 year old woman who presented with hemiplegia. This is a unique case because both internal carotid arteries were congenitally hypoplastic distal to the ophthalmic arteries and had become occluded at this level. Those patients in whom the layering is due to distal obstruction can usually be distinguished by their clinical features. Nearly all those so far reported presented with hemiplegia; none were in coma or had any evidence of raised intracranial pressure. Appearances similar to layering but due to stenosis at the origin of the internal carotid artery are readily distinguished arteriographically (Fig; 6).
The importance of distinguishing the cause of the raised intracranial pressure in the comatose group has been discussed already. REFERENCES ARONSON,H. A., SCATLIFF,J. H. (1962). J. Neurosurg., 19, 691. BRAIN,R. (1955). Diseases of the Nervous System. London: Oxford University Press. DECKER, K. (1956). Acta radioL, 46, 351. ECKER,A. D. (1945). or. Neurosurg., 2, 47. ECKER,A. & RIEMENSCHNEIDER,P. A. (1951). J. Neurosurg., 8, 660. EVANS,J. P., ESPEY,F. F., KRISTOFF,F. V., KIMBELL,F. D., & RYDER,H. W. (1951). Arch. Surg. (Chic.), 63, 107. Fox, J. A., HUGH,A. E. (1964). Clin. RadioL, 15, 183. HORWITZ, N. H. & DUNSMORE, R. I'{. (1956). J. Neurosurg., 13, 155. JOHNSON,R. J., POTTER,J. M., REID,R. G. (1958). J. Neurol. Neuro~'urg. Psychiat., 21, 68. MITCHELL, O. C., DE LA TORRE, E., ALEXANDER, E.,
DAVIE,C. H. (1962). or. Neurosurg., 19, 766. NEWTON,T. H., COUCH,R. S. C. (1960). Radiology, 75, 766. PR~BRAM,H. F. W. (1961). Neurol. (Minneap.), 11, 10. RIISHEDE,J. & ETI-rSLBERG,S. (1953). Arch. Neurol. Psychiat., 70, 399. SUTTON,D. (1962). Arteriography. Edinburgh: Livingstone.