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Hemodynamic mechanism in the angiographic disappearance of ruptured cerebral aneurysm
412
Surg Neurol 1984;22:412-4
Hemodynamic Mechanism in the Angiographic Disappearance of Ruptured Cerebral Aneurysm Francesco Tognetti,
M.D., Alvaro Andreoli, M.D., and Claudio Testa, M.D.
First Division of Neurosurgery, Ospedale Bellaria, Bologna, Italy
Tognetti F, Andreoli A, Testa C. Hemodynamic mechanism in the angiographic disappearance of ruptured cerebral aneurysm. Surg Neurol 1984;22:412-4.
Failure of unilateral carotid angiography to opacify a saccular aneurysm of the anterior communicating artery was observed; this occurred despite excellent visualization of the parent artery with spontaneous cross-filling and adequate demonstration of the intracranial carotid system bilaterally. In the absence of thrombosis of the aneurysm (which was discounted by contralateral carotid angiograms), vasospasm, and hypoplasia of the afferent arteries, a hemodynamic mechanism involving velocity of blood flow and intravascular turbulence is considered. KEYWORDS: Anterior communicating artery; Cerebral aneurysm; Intravascular turbulence; Streamlined blood flow; Crossfilling
Cerebral aneurysms may escape angiographic detection due to the following primary causes: (a) vasospasm of the arterial afferent with decrease in blood flow towards the lesion [9]; (b) thrombosis, which may or may not be permanent, o f the aneurysmal sac [2,7]; (c) hypoplasia o f a supplying artery, e.g., o f either proximal (A1) anterior cerebral artery in association with aneurysm of the anterior communicating artery, resulting in poor or none ipsilateral flow to the lesion [1,10]. We describe a case o f an aneurysm o f the anterior communicating artery in which carotid angiography failed to reveal the lesion in the absence o f any o f the above mentioned mechanisms. Case Report A 57-year-old woman was admitted to our unit on March 11, 1983. Occasional arterial hypertension was the unique
Address reprint requests to: Dr. Francesco Tognetti, Divisione di Neurochirurgia I, Ospedale Bellaria, 40139 Bologna, Italia.
© 1984 by Elsevier Science Publishing Co., Inc.
significant complaint in her past medical history. Four hours before admission she had developed increasing headache, which was followed by drowsiness and eventual coma. Neurological examination showed an unconscious patient with marked stiffness o f her neck. Painful stimulation elicited brisk, purposeful movements in all limbs. The brainstem reflexes were normal. Systemic blood pressure was 210/110 mmHg. Computed tomography scanning showed diffuse subarachnoid hemorrhage and thick accumulation of blood in the anterior interhemispheric fissure. Intraventricular hemorrhage was also present. Bilateral carotid angiography was performed immediately. This took 20 minutes, and it was performed while the patient was anesthetized, intubated, and mechanically ventilated. Systolic blood pressure was 120 and 100 m m H g at the beginning and the end of the procedure, respectively. Each injection resulted in spontaneous and complete bilateral staining of the intracranial carotid circulation. Right carotid angiograms were consistent with a saccular aneurysm of the anterior communicating artery (Figure 1). Left carotid angiography, in turn, yielded a clear demonstration of the anterior communicating artery but, surprisingly, did not demonstrate the aneurysm. T h e following findings were noted: 1. The separation o f the postcommunicating segments (A2) of the anterior cerebral arteries, which could indirectly indicate the presence o f the malformation. 2. The presumed neck of the aneurysm that, in the light of the right carotid angiograms, was somehow identified on the parent artery near its right extremity (Figure 2). Standard supportive therapy with antifibrinolytic and hypotensive drugs was instituted. Some 10 hours after admission the patient exhibited anisocoria and weakening of the motor responses. H e r clinical condition deteriorated steadily, and she died 3 days later. Permission for autopsy was not granted. 0090-3019/84/$3.00
Disappearing Cerebral Aneurysm
Surg Neurol 1984;22:412-4
413
Discussion
Figure 1. Right carotid angiography showing a saccular aneurysm of the anterior communicating artery, Cross-filling results in nearly complete visualization of the intracranial carotid circulation.
Figure 2. Left carotid angiography confirming a significant cross-filling through a well contrasted an,~erior communicating artery but failing to reveal the aneurysm. The neck of the lesion is probably identifiable at the junction of the anterior communicating artery with the right "dominant" anterior cerebral artery.
Cross-filling is a rather frequent occurrence in carotid angiography. In most cases the spontaneous visualization of the contralateral cerebral circulation is limited to the anterior cerebral artery. The presence of spontaneous bilateral cross-filling with increased flow from each carotid system to completely fill the contralateral anterior and middle cerebral arteries and distal carotid syphon, as documented in our patient, represents an uncommon hemodynamic pattern. It has been found only in 0.4% of cases by Krayenbiihl and Yasargil in a series of 1000 carotid angiograms [5]. It has been suggested that adequate cross-filling may obviate the need of further investigations of the contralateral carotid circulation by direct percutaneous procedure [6]. Our case of unilateral visualization of an aneurysm of the anterior communicating artery indicates that possible exceptions must be taken into consideration. Aneurysms of the anterior communicating artery have long since been demonstrated to coexist with an increased incidence of anomalies of the anterior circle of Willis, primarily the asymmetry of the AI segments [1,10,12]. In such instances, as in our own, aneurysms often arise near the junction of the anterior communicating artery with the larger AI [1,12] (Figure 1). In our case, both A1 segments appeared adequately demonstrated and both were able to deliver a significant amount of blood to the opposite hemisphere (Figures 1 and 2). According to the hyperdynamic theory, this augmented flow may well have given rise to enhanced stress on the wall of the anterior communicating artery due to intravascular turbulence; thus, it would have played a critical role in either the initiation or enlargement of the aneurysm, or both [3,4,8,11]. The carotid angiograms made in our case study suggest that hemodynamic forces in proximity to and within the anterior communicating artery--at a given instant during the examination--prevented the blood stream from entering the aneurysm: The contrast-medium bolus injected into the left carotid artery failed to opacify the sac in spite of clear filling of the parent artery and, probably, of the initial portion of the neck. It is reasonable that--depending upon the timing and rate of carotid injection, the volume of the contrast bolus, intracarotid pressure gradients, arterial systemic pressure, cardiac rhythm [6], and other less defined factors--the random fluctuations of intravascular hemodynamic forces accounted for the alternating appearance and disappearance of the aneurysmal sac in our case. A possible explanation is that blood flow became temporarily "streamlined" in the anterior communicating artery during left carotid angiography; in this condition the threshold of the critical Reynolds' number was not reached
414
Surg N e u r o l 1984;22:412-4
and turbulence with irregular fluctuations of blood into the sac did not take place [3,4]. Systolic pressure was low (120 mmHg) at the beginning of angiography and showed further decrease (down to 100 mmHg) throughout the procedure; this probably then resulted in a decreased rate of flow across the anterior communicating artery, which created locally streamlined blood flow. Our case confirms the importance of complete and possibly repeated angiographic examinations in studying all cases of subarachnoid hemorrhage that are suspected to be of aneurysmal origin, even though a satisfactory visualization of the cerebral circulation has been obtained bilaterally from a single angiographic procedure. Factors such as vasospasm [9], the small size of the lesion, and observer or technical errors [2] can be discounted in our case. Furthermore, the possibility of blood clotting within the aneurysmal sac during the few minutes that elapsed between right and left carotid angiography is merely conjectural: Spontaneous thrombosis of cerebral aneurysms is exceptional and has generally been proved to be slowly progressive [2,7].
References 1. Andrews RJ, Spiegel PK. Intracranial aneurysms: characteristics of aneurysms by site, with special reference to anterior communicating artery aneurysms. Surg Neurol 1981; 16:122 -6.
T o g n e t t i et al
2. Bohmfalk GL, Story JL. Intermittent appearance of a ruptured cerebral aneurysm on sequential angiograms. J Neurosurg 1980;52:263-5. 3. Ferguson GG. Turbulence in human intracranial saccular aneurysms. J Neurosurg 1970;33:485-97. 4. Ferguson GG. Physical factors in the initiation, growth, and rupture of human intracranial saccular aneurysms. J Neurosurg 1972;37:666-77. 5. Krayenbi~hl H, Yasargil MG. L'angiografia cerebrale. Piccin, ed. Padua: 1967:130. 6. M611er A, Ericson K. Some aspects of contralateral compression in carotid angiography. Radiology 1977;125:725-9. 7. Moritake K, Handa H, Ohtsuka S. Vanishing cerebral aneurysm in serial angiography. Surg Neurol 1981;16:36-40. 8. Sehkar LN, Heros RC. Origin, growth, and rupture of saccular aneurysms: a review. Neurosurgery 1981;8:248-60. 9. Spetzler RF, Winestock D, Newton HT. Disappearance and reappearance of cerebral aneurysm in serial arteriograms. J Neurosurg 1974;41:508-10. 10. Stehbens WE. Intracranial arterial aneurysms. In: Pathology of the cerebral blood vessels. St Louis: CV Mosby, 1972:351-470. 11. Tognetti F, Limoni P, Testa C. Aneurysm growth and hemodynamic stress. Surg Neurol 1983;20:74-8. 12. Yasargil MG, Fox JL, Ray MW. The operative approach to aneurysms of the anterior communicating artery. In: Krayenb/ihl H, ed. Advances and technical standards in neurosurgery. Vol 2. Vienna-New York: Springer, 1975:114-70.
Surg Neurol 1984;22:412-4
Hemodynamic Mechanism in the Angiographic Disappearance of Ruptured Cerebral Aneurysm Francesco Tognetti,
M.D., Alvaro Andreoli, M.D., and Claudio Testa, M.D.
First Division of Neurosurgery, Ospedale Bellaria, Bologna, Italy
Tognetti F, Andreoli A, Testa C. Hemodynamic mechanism in the angiographic disappearance of ruptured cerebral aneurysm. Surg Neurol 1984;22:412-4.
Failure of unilateral carotid angiography to opacify a saccular aneurysm of the anterior communicating artery was observed; this occurred despite excellent visualization of the parent artery with spontaneous cross-filling and adequate demonstration of the intracranial carotid system bilaterally. In the absence of thrombosis of the aneurysm (which was discounted by contralateral carotid angiograms), vasospasm, and hypoplasia of the afferent arteries, a hemodynamic mechanism involving velocity of blood flow and intravascular turbulence is considered. KEYWORDS: Anterior communicating artery; Cerebral aneurysm; Intravascular turbulence; Streamlined blood flow; Crossfilling
Cerebral aneurysms may escape angiographic detection due to the following primary causes: (a) vasospasm of the arterial afferent with decrease in blood flow towards the lesion [9]; (b) thrombosis, which may or may not be permanent, o f the aneurysmal sac [2,7]; (c) hypoplasia o f a supplying artery, e.g., o f either proximal (A1) anterior cerebral artery in association with aneurysm of the anterior communicating artery, resulting in poor or none ipsilateral flow to the lesion [1,10]. We describe a case o f an aneurysm o f the anterior communicating artery in which carotid angiography failed to reveal the lesion in the absence o f any o f the above mentioned mechanisms. Case Report A 57-year-old woman was admitted to our unit on March 11, 1983. Occasional arterial hypertension was the unique
Address reprint requests to: Dr. Francesco Tognetti, Divisione di Neurochirurgia I, Ospedale Bellaria, 40139 Bologna, Italia.
© 1984 by Elsevier Science Publishing Co., Inc.
significant complaint in her past medical history. Four hours before admission she had developed increasing headache, which was followed by drowsiness and eventual coma. Neurological examination showed an unconscious patient with marked stiffness o f her neck. Painful stimulation elicited brisk, purposeful movements in all limbs. The brainstem reflexes were normal. Systemic blood pressure was 210/110 mmHg. Computed tomography scanning showed diffuse subarachnoid hemorrhage and thick accumulation of blood in the anterior interhemispheric fissure. Intraventricular hemorrhage was also present. Bilateral carotid angiography was performed immediately. This took 20 minutes, and it was performed while the patient was anesthetized, intubated, and mechanically ventilated. Systolic blood pressure was 120 and 100 m m H g at the beginning and the end of the procedure, respectively. Each injection resulted in spontaneous and complete bilateral staining of the intracranial carotid circulation. Right carotid angiograms were consistent with a saccular aneurysm of the anterior communicating artery (Figure 1). Left carotid angiography, in turn, yielded a clear demonstration of the anterior communicating artery but, surprisingly, did not demonstrate the aneurysm. T h e following findings were noted: 1. The separation o f the postcommunicating segments (A2) of the anterior cerebral arteries, which could indirectly indicate the presence o f the malformation. 2. The presumed neck of the aneurysm that, in the light of the right carotid angiograms, was somehow identified on the parent artery near its right extremity (Figure 2). Standard supportive therapy with antifibrinolytic and hypotensive drugs was instituted. Some 10 hours after admission the patient exhibited anisocoria and weakening of the motor responses. H e r clinical condition deteriorated steadily, and she died 3 days later. Permission for autopsy was not granted. 0090-3019/84/$3.00
Disappearing Cerebral Aneurysm
Surg Neurol 1984;22:412-4
413
Discussion
Figure 1. Right carotid angiography showing a saccular aneurysm of the anterior communicating artery, Cross-filling results in nearly complete visualization of the intracranial carotid circulation.
Figure 2. Left carotid angiography confirming a significant cross-filling through a well contrasted an,~erior communicating artery but failing to reveal the aneurysm. The neck of the lesion is probably identifiable at the junction of the anterior communicating artery with the right "dominant" anterior cerebral artery.
Cross-filling is a rather frequent occurrence in carotid angiography. In most cases the spontaneous visualization of the contralateral cerebral circulation is limited to the anterior cerebral artery. The presence of spontaneous bilateral cross-filling with increased flow from each carotid system to completely fill the contralateral anterior and middle cerebral arteries and distal carotid syphon, as documented in our patient, represents an uncommon hemodynamic pattern. It has been found only in 0.4% of cases by Krayenbiihl and Yasargil in a series of 1000 carotid angiograms [5]. It has been suggested that adequate cross-filling may obviate the need of further investigations of the contralateral carotid circulation by direct percutaneous procedure [6]. Our case of unilateral visualization of an aneurysm of the anterior communicating artery indicates that possible exceptions must be taken into consideration. Aneurysms of the anterior communicating artery have long since been demonstrated to coexist with an increased incidence of anomalies of the anterior circle of Willis, primarily the asymmetry of the AI segments [1,10,12]. In such instances, as in our own, aneurysms often arise near the junction of the anterior communicating artery with the larger AI [1,12] (Figure 1). In our case, both A1 segments appeared adequately demonstrated and both were able to deliver a significant amount of blood to the opposite hemisphere (Figures 1 and 2). According to the hyperdynamic theory, this augmented flow may well have given rise to enhanced stress on the wall of the anterior communicating artery due to intravascular turbulence; thus, it would have played a critical role in either the initiation or enlargement of the aneurysm, or both [3,4,8,11]. The carotid angiograms made in our case study suggest that hemodynamic forces in proximity to and within the anterior communicating artery--at a given instant during the examination--prevented the blood stream from entering the aneurysm: The contrast-medium bolus injected into the left carotid artery failed to opacify the sac in spite of clear filling of the parent artery and, probably, of the initial portion of the neck. It is reasonable that--depending upon the timing and rate of carotid injection, the volume of the contrast bolus, intracarotid pressure gradients, arterial systemic pressure, cardiac rhythm [6], and other less defined factors--the random fluctuations of intravascular hemodynamic forces accounted for the alternating appearance and disappearance of the aneurysmal sac in our case. A possible explanation is that blood flow became temporarily "streamlined" in the anterior communicating artery during left carotid angiography; in this condition the threshold of the critical Reynolds' number was not reached
414
Surg N e u r o l 1984;22:412-4
and turbulence with irregular fluctuations of blood into the sac did not take place [3,4]. Systolic pressure was low (120 mmHg) at the beginning of angiography and showed further decrease (down to 100 mmHg) throughout the procedure; this probably then resulted in a decreased rate of flow across the anterior communicating artery, which created locally streamlined blood flow. Our case confirms the importance of complete and possibly repeated angiographic examinations in studying all cases of subarachnoid hemorrhage that are suspected to be of aneurysmal origin, even though a satisfactory visualization of the cerebral circulation has been obtained bilaterally from a single angiographic procedure. Factors such as vasospasm [9], the small size of the lesion, and observer or technical errors [2] can be discounted in our case. Furthermore, the possibility of blood clotting within the aneurysmal sac during the few minutes that elapsed between right and left carotid angiography is merely conjectural: Spontaneous thrombosis of cerebral aneurysms is exceptional and has generally been proved to be slowly progressive [2,7].
References 1. Andrews RJ, Spiegel PK. Intracranial aneurysms: characteristics of aneurysms by site, with special reference to anterior communicating artery aneurysms. Surg Neurol 1981; 16:122 -6.
T o g n e t t i et al
2. Bohmfalk GL, Story JL. Intermittent appearance of a ruptured cerebral aneurysm on sequential angiograms. J Neurosurg 1980;52:263-5. 3. Ferguson GG. Turbulence in human intracranial saccular aneurysms. J Neurosurg 1970;33:485-97. 4. Ferguson GG. Physical factors in the initiation, growth, and rupture of human intracranial saccular aneurysms. J Neurosurg 1972;37:666-77. 5. Krayenbi~hl H, Yasargil MG. L'angiografia cerebrale. Piccin, ed. Padua: 1967:130. 6. M611er A, Ericson K. Some aspects of contralateral compression in carotid angiography. Radiology 1977;125:725-9. 7. Moritake K, Handa H, Ohtsuka S. Vanishing cerebral aneurysm in serial angiography. Surg Neurol 1981;16:36-40. 8. Sehkar LN, Heros RC. Origin, growth, and rupture of saccular aneurysms: a review. Neurosurgery 1981;8:248-60. 9. Spetzler RF, Winestock D, Newton HT. Disappearance and reappearance of cerebral aneurysm in serial arteriograms. J Neurosurg 1974;41:508-10. 10. Stehbens WE. Intracranial arterial aneurysms. In: Pathology of the cerebral blood vessels. St Louis: CV Mosby, 1972:351-470. 11. Tognetti F, Limoni P, Testa C. Aneurysm growth and hemodynamic stress. Surg Neurol 1983;20:74-8. 12. Yasargil MG, Fox JL, Ray MW. The operative approach to aneurysms of the anterior communicating artery. In: Krayenb/ihl H, ed. Advances and technical standards in neurosurgery. Vol 2. Vienna-New York: Springer, 1975:114-70.