Neurnradiologg

Neuroradiology 11,185-190 (1976)

@ by Springer-Verlag 1976

Rupture of Intracranial Aneurysm during Carotid Angiography B. Liliequist, M. Lindqvist and F. Probst Department of Neuroradiology,University of Ume~, S-901 85 Ume~, Sweden

Summary. The reports of rupture of an aneurysm during carotid angiography are very few but the actual incidence is doubtless higher than recorded. The case presented is documented with the demonstration of a large middle cerebral artery aneurysm with an intratemporal hematoma, and, in sequence, the rupture of the aneurysm during the height of the injection and the subsequent extensive leakage of the contrast medium. The factors which which can lead to rupture of an aneurysm during the angiographic procedure are discussed.

Key words: Rupture of aneurysms, Carotid angiography.

Rupture of an intracranial arterial aneurysm during carotid angiography is an unusual event. Only about 25 cases have been recorded in the literature although the number of actually burst aneurysms is probably larger. The number of aneurysms actually bursting during cerebral angiography is remarkably low in consideration of the great number of cerebral angiographies performed on patients with recent subarachnoid bleeding. According to a cooperative study on subarachnoid hemorrhage [16] only one case of extravasation of contrast medium was noted in 5,484 patients with subarachnoid bleeding studied angiographically. Therefore the risk of rupture being caused by the angiographic procedure seems to be low. There are, hovever, certain unfavourable circumstances which, when brought into function simultaneously, could cause a rupture. Some of these factors were evidently present in our case and can also be recognized when searched for in the records of other published cases. There are also some relevant findings

registered experimentally which point in the same direction. An actual pressure increase in the carotid artery has thus been documented by several investigators [5, 11] during the injection of contrast medium, and this casts a doubt upon the prevailing theory that cerebral angiography is an innocuous procedure.

Case Report A woman, 46 years of age, with known hypertension, was suddenly taken ill with severe headache. She recovered but sustained a new attack 11/2months later. On admission to the hospital she was somnolent and severly ill. Blood pressure was 210/100 and the pulse rate 60. She had slight signs of a left sided hemiparesis with facial weakness and spasticity. On the same day, right carotid angiography was performed. The common carotid artery was punctured and a catheter was placed in the internal carotid artery with the tip 2-3 cm distal to the bifurcation. Three injections of 7.5 ml Isopaque cerebral ® were performed, and an arterial aneurysm on the middle cerebral artery was visualized as well as signs of a temporal lobe mass (Fig. 1). The injection time was 0.8 sec. Cross circulation was evident. During the fourth injection a rupture of the aneurysm occurred with leakage of contrast medium into the brain substance and the subarachnoid space (Fig. 2). A fifth injection showed spasm of the intracranial arteries and very slow circulation together with signs of a newly formed intracerebral mass (Fig. 3). The examination was performed under general anaesthesia and the blood pressure was continously registered. It was 180/130 at the beginning and 130/110 at the time of the third injection. At the time of the fourth and fifth injections the blood pressure

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had risen to a still higher level, 180/130 and 230/150 respectively. Clinically the patient showed signs of tentorial herniation and an operation was performed immediately. There was a 2-3 mm thick subdural hematoma with blood in the subarachnoid space as well. A large cavity filled with blood was evacuated from the temporal lobe and the neck of the aneurysm was located and clipped. A resection of the anterior part of the temporal lobe was done. Postoperatively the patient did well and left the hospital with a residual left hemiparesis.

Discussion

Fig. 1. Right internal carotid angiography with spontaneous cross circulation, large middle cerebral artery aneurysm and imratemporal hematoma

The paramount role of cerebral angiography in the diagnosis and management of patients with subarachnoidal bleeding has never been questioned. A fear for performing the procedure in close relationship to a recent hemorrhage has, however, been expressed previously. The result of the investigations published by Bakay and Sweet [1], as well as by Greitz [6], showing that there was no measurable elevation of pressure in the carotid artery during carotid angiography convinced most neurosurgeons and neuroradiologists that

Fig. 2. Oblique view, fourth inj ection showing in a 2 film/sec sequence a rupture of aneurysm a) during height of injection, b) 0.5 sec later with extensive leakage of contrast medium

B. Liliequist et al.: Rupture of Intracranial Aneurysm during Carotid Angiography

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Fig. 3. Lateral view with arterial spasm in carotid syphon and peripheral branches of middle cerebral artery and a large intracerebral cavity filled with contrast medium

the procedure could be used without danger to the patient even immediately after a recent bleeding. The results mentioned above [1, 6] were based upon a few measurements in a limited number of patients. The amount of contrast medium injected was 10-12 ml and 4 ml respectively and the injection times 2-3 sec and 1-1.5 sec, corresponding to a flow rate of contrast medium of less than 6 ml/second, which can be considered the average value of the flow rate in the carotid artery [2]. Nadjmi et al. [12] noted a rise of 20-30 mm Hg in the systemic blood pressure of patients examined by retrograde injection in the brachial artery and an elevation of pressure in the carotid artery has been recorded [5, 11] when large amounts of contrast medium (50-60 ml) were injected into the brachial artery in a retrograde direction. A rise of the systemic blood pressure following the injection of contrast medium into the aortic arch has recently been confirmed by J6rgensen et al. [10]. The most extensive study of the pressure relationship in the carotid artery during cerebral angiography

hitherto undertaken is found in the work of Bergleiter [2] who performed measurements in the carotid artery distal to the injection site. He could document a rise in pressure amounting to 5-30 mm Hg in the carotid artery. The volume of contrast medium used was 8-10 ml, injected in 1.2 sec, which corresponds to a flow rate exceeding 6 ml/sec. Hilal [7] discussed the hemodynamic changes associated with intraarterial injection of contrast medium and postulated the conditions during which a rise of pressure would appear distally. Under normal conditions the vascular bed distal to the site of injection communicates freely with the general systemic vascular bed and any pressure increase due to the additional injection pressure will dissipate peripherally and probably without challenging the cerebral arterial autoregulation. In pathological conditions, i. e. inelastic vessels or cerebral oedema, the rise of pressure probably will also reach the smaller vessels and the autoregulation would be called forth and constriction as well as dilatation of the vascular bed would result. Pressure changes will also

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dissipate in a proximal direction as well as into the territory of the external carotid artery. An increase of pressure, distal to the puncture site, will occur when there is a narrowing of the arterial lumen caused by the needle or catheter or with a narrowing located proximal to the puncture site. When a marked narrowing appears around the tip of the catheter the conditions are similar to those of a catheter placed in the wedge position in a pulmonary artery where injection of contrast medium can cause an extensive increase in pressure [18]. The rate of injection is also significant. If the rate of injection exceeds the local flow rate, contrast medium will escape proximally. This will usually not cause a significant rise in pressure unless there is a reduction of the lumen of the artery at the puncture site or proximally. Rupture of the aneurysm occurred in the case reported by Osgood and Martin [14] when the injection of the contrast medium was made distal to a ligature of the common carotid artery. In another case the injection was performed into the internal carotid artery immediately above a local stenosis resulting in extensive cross circulation and rupture of the aneurysm [9]. In discussing the circumstances leading to the rupture of an aneurysm during carotid angiography the phenomenon of cross circulation must be considered. Spontaneous cross circulation is fairly often seen during carotid angiography. It is usually transient and seen only on films exposed during the actual injection of the contrast medium. It is more often seen when the catheter is placed in the internal carotid artery than in the common carotid artery. It is also well known that direct injection of one vertebral artery usually will cause reflux of contrast medium into the contralateral vertebral artery. The phenomenon of cross circulation is used as a diagnostic test for demonstrating the anatomical continuity of the anterior communicating artery. Normally there is a rythmic shift of blood from one side to the other through the anterior communicating artery. This is due to the fact that there is a difference in phase of the pulse wave between the right and left sides. The amount of blood passing through the anterior communicating artery depends upon the length and width of the artery and the size of the pressure gradient. Assuming that this length and width are known, the pressure needed to move a certain amount of contrast medium across the anterior communicating artery can be calculated according to the law of Poiseille. Although this law is strictly applicable only if the liquid is of uniform viscosity, and its flow is streamlined and nonpulsatile, it has been shown to apply relatively well also to the mean laminar flow in arteries [4] and is considered largely valid for hemodynamic

studies [15, 17]. If, for instance, the length of the anterior communicating artery is 5 mm and its diameter is 1 ram, a flow of 1 ml of contrast medium per sec through the artery indicates a pressure gradient of approximately 6 mm Hg. Since, however, the flow is proportional to the fourth power of the radius, the same flow rate in an artery with a diameter of 0.5 mm indicates a pressure gradient of approximately 96 mm Hg. A significant increase of the intraarterial pressure on the injected side will cause reflux of contrast medium to all parts of the circle of Willis, and if this reflux is extensive, it should be regarded as a warning signal. This is true also in cases where the reflux has been provoked by increasing the cerebrovascular resistance by artificial hyperventilation in patients examined under general anaesthesia. A pressure increase in the carotid artery will normally be dissipated in all directions and probably the rise of pressure is without significance unless unfavourable conditions are present. Unfavourable conditions are all which will counteract the normal moderating mechanisms. Thus, extensive spasm of the cerebral arteries and/or a high degree of arteriosclerosis lowering the elasticity of the vessels, as well as the presence of increased intracranial pressure, are circumstances which will act in an unfavourable direction and together with a narrowing around the tip of the catheter can help to build up pressure during the injection of the contrast medium. A tight spasm around the tip of the catheter with a marked cross circulation and a rupture of an ipsilateral aneurysm was reported by Teal et al. [18]. When the contralateral carotid artery is compressed the pressure is lowered distally and contrast medium easily fills the vascular bed in both hemispheres. Cross circulation can, thus, be induced either by increasing the flow rate on the injected side, especially when a large volume of contrast medium is used, or by compressing the contralateral carotid artery. Cross circulation can usually be avoided or diminished by lowering the injection pressure and/or the volume of contrast medium. Patients harbouring an intracranial aneurysm which has recently bled are in a different situation than other patients as regards the risk of an angiographic procedure. The wall of an aneurysm which has recently bled is brittle and the site of rupture is probably covered by a platelet plug only. Not until this has been resolved and replaced by granulation tissue, which will take 3 weeks, will the risk of rebleeding be eliminated. It is generally accepted that the cause of rebleeding is often a rise in arterial pressure causing a rise of the pressure gradient across the wall of the aneurysm. According to Hinshaw et al. [8] there is a non-linear pressure volume relationship in aneurysms

B. Liliequist et al.: Rupture of Intracranial Aneurysm during Carotid Angiography

which means that a critical pressure causing sudden enlargement of the aneurysms can result in a rupture. A lowering of the pressure outside the aneurysm would bear the same risk and lumbar puncture with evacuation of large amounts of CSF following a bleeding episode should be avoided [13]. Spasm around the catheter can not always be prevented and is a warning sign. Spasm will more easily occur if the tip of the catheter is advanced far distally into the internal carotid artery. The common carotid artery is less sensitive than the internal carotid artery [3] and the puncture should therefore always be in the common carotid artery. The advantage of a selectively performed internal carotid angiography is so great that positioning of the tip of the catheter proximally in the internal carotid artery should be favoured whenever possible. In order to investigate the anterior communicating artery a cross circulation must be provoked. This can be done by compressing the contralateral artery in the neck. Probably this is not dangerous since, if the compression is applied to the region of the internal carotid artery, the pressure in the opposite carotid artery is lowered. If the common carotid artery is compressed low in the neck a slight rise of pressure can be recorded in the contralateral carotid artery [19]. Ideally a cross circulation test should therefore be performed with compression of the internal carotid artery on the same side as the aneurysm during injection of the contrast medium in the contralateral artery. Two ruptures of aneurysms have occurred during compression of the contralateral artery in the neck. Wright [19] noted a rupture in the same situation in 3 other cases during or immediately following the X-ray procedure. In the case discussed here a spontaneous cross circulation did occur. Furthermore the examination was performed on the same day as the last bleeding episode and the injection flow rate exceeded 6 ml/sec. Together with a rise in the general blood pressure, the presence of a temporal lobe mass and spasm of the cerebral arteries, conditions for a rupture were present. This happened as is the case with all published ruptures during the actual injection of the contrast medium. When studying the cases reported it is evident that nearly all ruptures occurred during examinations performed in close or very close time relation with the last bleeding. Thus, only in a few cases was a time interval of 2 weeks reported, the longest being 17 days. In at least 8 of the 24 cases reported a cross circulation was evident. Another very remarkable fact is that only 3 of 25 cases were men and 17 were women. The sex was not stated in 4. The incidence of aneurysm in the cooperative study [16] was 54% women and 46% men. The

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reason for the predominance of women over men with rupture of aneurysm during carotid angiography is not evident. In 18 of the cases the patient died, and a survival is reported in 5 cases only, including our case. Four of them were operated with success.

Conclusion

Injection of contrast medium during carotid angiography can, under certain circumstances, give rise to an increase of the intracranial arterial pressure. This is probably of no significance if there is no weak point in the arteries and is therefore well tolerated by patients without recent intracranial bleeding. Spasm along the tip of the catheter, increased blood pressure, increased intracranial pressure and spasm in the arteries may, all together or one at a time and in combination with a quick injection of a large volume of contrast medium, cause a dangerous rise in pressure which can cause a rupture of an aneurysm which has recently bled. Conditions leading to excessive spontaneous cross circulation should be avoided and cross circulation tests should be performed by compressing the contralateral carotid artery. Women who have recently bled are more liable to sustain a rupture during carotid angiography. The reason for this is unknown.

References 1. Bakay, L., Sweet, W. H.: Cervical and intracranial intraarterial pressures with and without vascular occlusion. Surg. Gyn. Obstet. 95, 67 (1952) 2. Bergleiter, R.: H~imodynamik der zerebralen Angiographie und Funktion der Kollateralgef~iBe des Circulus arteriosus Willisii. Habilitationsschrift, Freiburg i. Br. 1965 3. Bergstr6m, K., Jorulf, H.: Arterial spasm following puncture and percutaneous cateterization. (To be published) 4. Delin, N. A., Ekestr6m, S., Telenius, R.: Relation of degree of internal carotid artery stenosis to blood flow and pressure gradient. An angiographic and surgical study in man. Invest. Radiol. 3, 337 (1968) 5. Fiebach, O., Liesegang, J.: Blutdruckver~inderungen bei der retrograden Brachialisangiographie: Modellversuche und intraarterielle Messungen. Radiologe 13, 518 (1973) 6. Greitz, T.: A radiologic study of the brain circulation by rapid serial angiography of the carotid artery. Acta radiol. Suppl. No. 140, 1956 7. Hilal, S. K.: Hemodynamic changes associated with the intraarterial injection of contrast media. Radiology 86, 615 (1966) 8. Hinshaw, Jr., D. B., Simmons, C. R., Leech, W., Minckler, J., Austin, G.: Loculated intracranial aneurysms: Angiography and possible etiology. Radiology 113, 101 (1974) 9. Jenkinson, E. L., Sugar, O., Love, H.: Rupture of an aneurysm of the internal carotid artery during cerebral angiography. Case report. Amer. J. Roentgenol. 71, 958 (i954)

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10. J~rgensen, P. B., Karle, A , Rosenklint, A.: Changes in blood pressure and cardiac rhythm induced by arterial contrast injection. Neuroradiology 5, 215 (1973) 11. Lin, J. P.-T., Kricheff, I, I., Chase, N. E.: Blood pressure changes during retrograde brachial angiography. Radiology83, 640 (1964) 12. Nadjmi, M., Braun, H., Cavallini, L , Nippert, M.: H~imodynamische und physikalische Aspekte der retrograden Brachialis-Angiographie. Dtsch. Z. Nervenheilk. 194, 328 (1968) 13. Nornes, H.: The role of intracranial pressure in the arrest of hemorrhage in patients with ruptured intracranial aneurysm. J. Neurosurg. 39, 226 (1973) 14. Osgood, C., Martin, L. G.: Intraventricular contrast extravasation during carotid angiography. Surg. Neurol. 2, 49 (1974) 15. Rushmer, R.F.: Cardiovascular dynamics. Philadelphia: Saunders 1961 16. Sahs, A. L , Perret, G. E., Locksley, H. B., Nishioka, H.: Intracranial anenrysms and subarachnoid hemorrhage. A cooperative study. Philadelphia and Toronto: Lippineott 1969

17. Sodeman, St., W. A-.,Sodeman, Jr., W. A.: Pathologic physiology. Mechanism of disease. 5th ed. Philadelphia: Saunders 1974 18. Teal, J. S., Wade, P. J., Bergeron, R. T., Rumbauch, C. L., Segall, H. D.: Ventricular opacification during carotid angiography secondary to rupture of intracranial aneurysm. Case report. Radiology 106, 581 (1973) 19. Wright, R. L.: Pressure considerations in carotid compression during angiography. J. Neurosurg. 19, 375 (1962)

Received." April5, 1976

Dr. B. Liliequist Department of Neuroradiology University of Ume~ S-901 85 Umefi, Sweden

Rupture of intracranial aneurysm during carotid angiography.

Neurnradiologg Neuroradiology 11,185-190 (1976) @ by Springer-Verlag 1976 Rupture of Intracranial Aneurysm during Carotid Angiography B. Liliequist...
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