The role of extracranial carotid abnormalities in the genesis of cerebral aneurysms

Transcription

1 J Neurosurg 55: , 1981 The role of extracranial carotid abnormalities in the genesis of cerebral aneurysms ALDO SPALLONE, M.D., AND GIANPAOLO CANTORE, M.D. Department of Neurosurgery, University of Rome School of Medicine, Rome, Italy ~/ The incidence of extracranial internal carotid artery (ICA) abnormalities, namely kinks, coils, and stenoses, was evaluated in a consecutive unselected series of 76 cases of single supratentorial saccular aneurysms submitted to bilateral carotid angiography. These patients were compared with a control group of 120 patients who had undergone either uni- or bilateral carotid angiography for causes other than cerebrovascular occlusive diseases or intracranial arterial aneurysms. Both groups had a total of 152 angiograms. Extracranial carotid abnormalities were significantly higher in aneurysm patients (p < 0.001). Arterial kinks and coils were seen on 42 of 152 angiograms in the saccular aneurysm group and 17 of 152 in the control group (p < 0.001); however, there was no significant difference regarding ICA stenoses (0.16 > p > 0.15). In the 76 aneurysm patients, abnormalities were mostly either located or on the side opposite the aneurysm (in 22 as opposed to 11 on the same side, p < 0.004). It is suggested that extracranial ICA anomalies have a role in the pathogenesis of intracranial arterial aneurysms, possibly by increasing the hemodynamic stress on the side opposite to the carotid lesion. The combination of the hydrodynamic theory, suggested by the present study, with other possible factors, might lead to a better understanding of the mechanism underlying development of human cerebral arterial aneurysms. KEY WORDS extracranial internal carotid artery 9 arterial kinking 9 stenosis intracraniai aneurysm circle of Willis hemodynamics S EVERAL factors have been thought to be involved in the pathogenesis of intracranial saccular aneurysms. These factors include congenital defects in the tunica media, 14,27,3v,64 embryonic remnants, 7,38 atherosclerosis, 8,42,51,~~ degenerative changes in the elastic intimal membrane, 1~ systemic hypertension, 1~ and anomalies of the circle of Willis/9,3~176 None, however, provides an entirely acceptable explanation. Patients undergoing angiography for occlusive cerebrovascular diseases present a remarkable incidence of intracranial aneurysms, 4'19'49'54 and this observation raises the question of whether the development of the aneurysms might be related to abnormalities of the extracranial carotid arteries. Scattered reports of intracranial aneurysms associated with extracranial carotid anomalies seem to support this hypothesis. 1Az,33,39-41,43,47,48,54,58 The present study has been undertaken in order to assess the incidence of extracranial internal carotid artery (ICA) abnormalities in a series of single intracranial supratentorial saccular aneurysms. Lesions of the common carotid arteries were excluded, partly because of their very low incidence. 6 Clinical Material and Methods We reviewed the angiograms of 76 recent, unselected, consecutive cases of single intracranial aneurysms of the anterior portion of the circle of Willis. A prerequisite for inclusion in the study was that bilateral carotid angiography had been performed, with good visualization of both carotid arteries from at least 1 cm below the bifurcation. All patients presented signs of subarachnoid hemorrhage (SAH) except one, for whom the evidence was symptomatic of extracranial ICA occlusion. This was the only incidental finding of intracranial aneurysm in a small series of about 30 patients who had recently undergone angiography for occlusive carotid diseases. The location of the aneurysms, sex and age of the patients, and number of hypertensive (160 mm Hg or J. Neurosurg. / Volume 55 / November,

2 A. Spallone and G. Cantore FIG. 1. Bilateral carotid angiograms, anteroposterior (a: fight, b: left) and lateral (c: fight, d: left) views, showing a large anterior communicating artery aneurysm filling mainly from the left anterior cerebral artery. A bilateral coiling of the extracranial internal carotid artery is also evident (arrows). FIG. 2. Right carotid angiograms, anteroposterior (left) and lateral (center) views. An aneurysm of the internal carotid artery (ICA) and posterior communicating artery is present. The extracranial ICA is normal. Left carotid angiogram, lateral view, is seen at right. A kinking of the extracranial ICA is shown (arrow). 694 J. Neurosurg. / Volume 55 / November, 1981

3 Extracranial carotid abnormalities and intracranial aneurysms FIG. 3. Left: Left carotid angiogram, anteroposterior view, showing a large aneurysm of the internal carotid artery (ICA) and posterior communicating artery. The extracranial ICA is normal. Right: Right carotid angiogram, oblique view. The extracranial aneurysm of the ICA is evident. The intracranial circulation is normal. greater) versus normotensive (less than 160 mm Hg) individuals are summarized in Tables 1 and 2. The patients fell into two subgroups according to the location of their aneurysms, namely, those with midline aneurysms (aneurysms of the anterior communicating and distal anterior cerebral arteries); and those with lateralized aneurysms (aneurysms of the ICA, posterior communicating, and middle cerebral arteries). The following abnormalities were considered: 1) coiling of the extracranial ICA (Fig. 1); 2) kinking of the extracranial ICA (Fig. 2); 3) stenosis (with at least TABLE 1 Location of aneurysms in 76 patients Location of Aneurysms* No. of Cases midline aneurysms ACA l ACoA 40 lateralized aneurysms ICA-PCoA 25 MCA 10 * ACA = distal anterior cerebral artery; ACoA = anterior communicating artery; ICA = internal carotid artery; PCoA = posterior communicating artery; and MCA = middle cerebral artery. 50% reduction of the diameter of the artery) or occlusion of the extracranial ICA, and extracranial ICA aneurysms (Fig. 3). The same angiographic findings were evaluated in a control group of 120 patients undergoing cerebral angiography for causes other than aneurysms or cerebrovascular occlusive diseases (Table 3). Of these TABLE 2 Sex, age, and blood pressure levels of aneurysm patients Midline Lateralized All Feature Aneurysms Aneurysms Aneurysms No. Percent No. Percent No. Percent males females age < 30 yrs yrs > 60 yrs normotensive (< 160 mm Hg systolic) hypertensive (7 160 mm Hg systolic) total 4l J. Neurosurg. / Volume 55 / November,

4 A. SpaUone and G. Cantore TABLE 3 Indications for angiography in the control group Type of No. of Angiographic Lesion Cases Examinations brain tumors 75 unilateral miscellaneous (he- 13 unilateral matomas, epilepsy, etc) small arteriovenous 9 bilateral malformations hematomas 16 bilateral no abnormal Findings* 7 bilateral total * Excluding patients with subarachnoid hemorrhage. TABLE 4 Sex, age, and blood pressure levels of control patients Feature No. Cases Percent males females age < 30 yrs yrs > 60 yrs normotensive (< 160 mm Hg systolic) hypertensive (~ 160 mm Hg systolic) total patients, 75 were evaluated for brain tumors, and, along with 13 other patients with miscellaneous lesions, underwent only one-sided carotid angiography. The total number of 152 angiograms in the control group was the same as in the aneurysm group. The control group was fairly comparable as to sex and age (Table 4). The different incidence of hypertensive patients, which was higher in the aneurysm group, did not reach statistical significance (25 of 76 as compared with 29 of 120, 0.18 > p > 0.17). Results The results were evaluated for the whole aneurysm group and for the two subgroups with midline and "lateralized" aneurysms (Table 5). The incidence of ICA coils, kinks, and stenoses in the control group is given in Table 6. It is significantly lower than for the whole aneurysm group (22 of 152 compared with 49 of 152, p < 0.001), and for both midline (22 of 152 compared with 27 of 82, p < 0.001) and lateralized aneurysms (22 of 152 compared with 22 of 70, p < 0.004), taken singly. However, on separate analysis of coils, kinks, and stenoses, the difference in the latter subgroups is not significant (0.16 > p > 0.15), but that of the former is highly significant (17 of 152 compared with 42 of 152, p < 0.001). Similar results emerge when the number of extracranial ICA abnormalities is compared in different individuals rather than in different angiograms (Table 7). TABLE 5 Incidence of extracranial 1CA abnormalities in aneurysm patients* Lateral- Midline ized Aneurysm Aneurysm Abnormalities Group Group coils unilateral 3 ipsilateral 0 contralateral 3 bilateral 6 ipsilaterallyt 1 contralaterallyt 1 no side predominance 45 kinks 9 11 unilateral 3 ipsilateral 1 contralateral 2 bilateral 3 ipsilaterally 0 contralaterally 1 no side predominance 2 stenoses-occlusions unilateral 3 ipsilateral 0 contralateral 3 bilateral 0 ipsilaterauy 0 contralaterally 0 no side predominance 0 extracranial ICA aneurysms 1 unilateral 1 ipsilateral 0 contralateral 1~ bilateral 0 total aneurysms 82 All Aneurysms No. % No. % No. % ~ :~ * Percent is to total angiograms. In the midline aneurysm group, the side was considered to be that from which the aneurysms were filled. For a description of midline and lateralized aneurysm groups, see Table 1. ICA = internal carotid artery. t Mild stenosis and/or angulation of the coiled segment in one side. :~ In one patient, a bilateral coil and an extracranial ICA aneurysm, located on the side opposite to the intracranial aneurysm, were associated. Unilateral and bilateral abnormalities occurred at similar rates in the 76 patients in the aneurysm group (17 compared with 16), but the incidence of bilateral coils was higher in midline than in lateralized aneurysms (six of 41 compared with three of 45), although not significantly so (0.30 > p > 0.29). On the other hand, the incidence of extracranial carotid abnormalities located on the side opposite to the aneurysm, or on both sides, but contralaterally, J. Neurosurg. / Volume 55 / November, 1981

5 Extracranial carotid abnormalities and intracranial aneurysms TABLE 6 Incidence of extracranial ICA abnormalities in control patients* Abnormalities Unilat- Bilat- Total eral eral No. % coils kinks stenoses extracranial ICA aneurysms 0 * Percent is of total angiograms. ICA = internal carotid artery. was significantly higher than that of abnormalities located bilaterally and ipsilaterally (22 of 76 compared with 11 of 76, p < 0.004). In this respect, the side of midline aneurysms was considered to be that from which the aneurysms were fiued. Discussion The importance of hemodynamic factors in the development and growth of cerebral aneurysms is widely recognized, a3,26,z9,a~176 A direct causal relationship between hemodynamic stress due to "anterior trifurcation" and anterior communicating artery aneurysms has been suggested by several authors. 29,3~ In fact, a higher incidence of anomalies of the anterior part of the circle of Willis in patients harboring aneurysms of the anterior communicating artery has been noted by others 29,3~176 as well as by us in the present study, although this point was not specifically considered. On the other hand, aneurysms in other locations failed to show a clear correlation with this and other hemodynamic anomalies of the circle of Willis. ~176 Experimental 23-26,34,35,57 and clinical 12,39-41,47,54 evidence has suggested the possibility that carotid stenosis or occlusion is a causal factor in the development of intracranial aneurysms, the idea being that it alters the hemodynamics of cerebral circulation and increases blood flow and pressure in the intracranial vessels on the side opposite to the lesion. This seems to be confirmed indirectly by the higher rate of inci- dental intracranial aneurysms found in patients undergoing angiography for cerebrovascular occlusive diseases 4,19,49,54 although as yet there is no clear clinical evidence for this from large, homogeneous series of intracranial aneurysms. The suggestion in the present study that extracranial carotid abnormalities are related to the pathogenesis of intracranial saccular aneurysms, particularly if located or prominent on the side opposite to the aneurysm, lends further support to this hypothesis. It might be postulated that ICA lesions in the present cases could have increased the hemodynamic stress on the opposite carotid system, although the hemodynamic significance of coils is controversial. 6,9,62 However, the present data do not offer clear evidence of a relationship between extracranial ICA stenosis, when considered separately, and intracranial aneurysms. This perhaps means that the hemodynamic effect of extracranial carotid lesions per se is not enough to trigger the development of intracranial aneurysms. Other, possibly congenital, factors might also be necessary. Clear evidence in this regard emerges from the present study for both kinks and coils, the congenital origin of which is widely recognized, ~,9,15,2~ although the role of acquired conditions in the pathogenesis of kinks has also been stressed. 6,28,a2,a6,6~,62 It is also worth noting that the age distribution of these lesions 32,61 resembles that of large series of intracranial aneurysms27 The present findings might point also to a correlation between extracranial ICA and intracranial aneurysms. Such a correlation is possibly t'urther supported by the published data indicating the rarity of spontaneous extracranial ICA aneurysms. 2,16,1a,22,31,44,6a Although there are too few figures available to permit any conclusion to be drawn, it is remarkable that in both the cases in which they were noted, extracranial ICA aneurysms occurred contralateral to the intracranial aneurysms. The possibility of intracranial aneurysms merely expressing an aspect of elastic tissue degeneration should be considered. 1~ Degenerative changes in the elastic membrane might also play a role in the TABLE 7 Statbtwalcompa~on ~theresults ~an~sm Aneurysm Group Control Group FaVor Anomaly Total Anomaly Total incidence of coils on no. of angiograms in no. of individuals incidence of kinks on no. of angiograms in no. of individuals incidence of stenoses on no. of angiograms in no. of individuals * Not significant. ~o~ versuscontrolgro~ Statistical Analysis p < p < p < 0.03 p < > p > 0.31" 0.16 > p > 0.15" J. Neurosurg. / Volume 55 / November,

6 A. Spallone and G. Cantore pathogenesis ofextracranial carotid abnormalities. 32,61 Accordingly, the present results might simply indicate the occurrence of such a defect involving at the same time both the intracranial and the extracranial vessels. However, we believe this does not satisfactorily explain the fact that in the present cases extracranial ICA abnormalities occurred mostly on the side opposite to the intracranial aneurysms. Experimental data might help to clarify this point. Lathyrism, a pathological condition artificially inducible in different species, 57 may be assumed to reproduce with reasonable approximation the effects of elastic membrane degeneration in human vessels. Hashimoto and co-workers 2a-26,34,35 found that fl-aminopropionitrile feeding, which is one of the known lathyrogens, 24 was an important element in the experimental induction of cerebral aneurysms in rats. However, increased systemic blood pressure and unilateral carotid ligation were prerequisites for induction of the aneurysms. Similar results were reported by others? 7 It must be stressed that, although experimental aneurysms occasionally occurred in the absence of fl-aminopropionitrile feeding, 24 they were never observed without either carotid ligation or hypertension. 23,26,3~ It is also remarkable that a hemodynamic correlation emerged between the side of carotid ligation and the location of the experimental aneurysm. 26 It appears that both these experimental data and the present results support the hemodynamic role of extracranial carotid lesions in the pathogenesis of cerebral aneurysms, although it is probable that other factors also play an important part in this process. We are aware of the fact that the present control group is not above possible criticism, since only a minority of patients underwent bilateral carotid angiography. In our institute, as a rule, patients are not subjected to bilateral cerebral angiography for causes other than cerebrovascular diseases. However, although present results should await confirmation by further studies, we believe that the evidence offered here is highly suggestive. On this assumption, we put forward the following theory for the pathogenesis of intracranial aneurysms. A congenital gap in the tunica media acts as a weak point, which may suddenly expand under the continuous effect of bloodstream impact and blood pressure. 13,5~ Degenerative changes in the elastic intimal membrane also may play a part in this process. 1~ Any intensification of either of these hemodynamic forces helps to increase the chances of aneurysm formation. Systemic hypertension and/or increased pressure on one side of the circle of Willis, related to contralateral extracranial ICA anomalies, enhance the turbulence of flow and the hemodynamic stress on the potential, developing aneurysm, by increasing the pressure on the parent artery. These are also of importance in the subsequent development and growth of such lesions. 1a,26,41,47 In this respect, the role of other factors, such as degenerative changes occurring within the aneurysm itself, may also be considered. 46,5a,55 The higher incidence of carotid abnormalities 9,a2,61 and systemic hypertension s associated with older age groups would increase the chances of ruptured intracranial aneurysms in adults. Acknowledgment The authors are greatly indebted to Dr. Italo Nofroni, Institute of Medical Statistics, University of Rome School of Medicine, who performed the statistical analysis of these data. References 1. 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8 A. Spallone and G. Cantore communicating aneurysms as a basis for surgical approach. J Neurosurg 32: , Walker AE, Allegre GW: The pathology and pathogenesis of cerebral aneurysms. J Neuropathol Exp Neuroi 13: , Weibel J, Fields WS: Tortuosity, coiling, and kinking of the internal carotid artery. I. Etiology and radiographic anatomy. Neurology 15:7-18, Weibel J, Fields WS: Tortuosity, coiling, and kinking of the internal carotid artery. II. Relationship of morphological variation to cerebrovascular insufficiency. Neurology 15: , Wemple JB, Smith GW: Extracranial carotid aneurysm. Report of four cases. J Neurosurg 24: , Wilson G, Riggs HE, Rupp C: The pathologic anatomy of ruptured cerebral aneurysms. J Neurosurg 11: , Yaw MG, Fox JL, Ray MW: The operative approach to aneurysms of the anterior communicating artery, in Krayenbiihl H (ed): Advances and Technical Standards in Neurosurgery. New York/Wien: Springer- Verlag, 1975, Vol 2, pp Manuscript received December 30, Accepted in final form May 22, Address reprint requests to: Aldo Spallone, M.D., Istituto di Neurochirurgia deu'universita di Roma, Viale delruniversita, 30, 00185, Rome, Italy. 700 J. Neurosurg. / Volume 55 / November, 1981