:Acta l
Acta Neurochir (Wien) (1992): 116:107 - 118
. . urochlrurglca
9 Springer-Verlag 1992 Printed in Austria
Management of Giant Intracranial Aneurysms* L. Symon Gough-Cooper Department, Institute of Neurology, National Hospital for Neurology and Neurosurgery, London, U.K.
Summary Based on an own material of 64 cases a survey is given on the management of giant intracranial aneurysms. Essential investigations are as well CT and Magnetic Resonance Scanning as detailed angiographic studies. With regard to the operative handling the following questions are discussed: approach; use of temporary vascular occlusion and related monitoring; preparation of the aneurysm neck for occlusion. In cases without recent subarachnoid haemorrhage morbidity and mortality were less than 10%. It was 15% in cases where recent haemorrhage had occurred.
Keywords: Giant aneurysm; management; diagnostic; operative technique; results.
Giant aneurysms pose a problem to the neurosurgeon. While like their smaller counterparts they may present with haemorrhage, they may also present with compression of neighbouring structures to which they tend to become very adherent. They may be further complicated by the presence within the sac of massive clot rendering the whole formidable mass quite difficult to handle. This paper is based on a total of sixty-four giant aneurysms treated by myself up until 1990. Their distribution is shown in Table 1. Thirty of them presented without subarachnoid haemorrhage and thirtyfour had a history of subarachnoid haemorrhage either recently or in the past. In addition to this group of aneurysms treated by direct intracranial exposure, another twelve patients have been treated by internal carotid ligation only, two treated by balloon embolization: one successfully, one unsuccessfully, and two in whom no treatment was felt justified. The age distribution of these sixty-four aneurysms does not support the earlier view that they tended to
* Invited Lecture, presented at the European Congress of Neurosurgery, Moscow, June 23-29, 1991.
Table 1 Giant aneurysms - LS
1990
Terminal carotid Middle cerebral Anterior cerebral Posterior cerebral
30 11 7 16
Total
64
present rather later in life than their smaller counterpart.
Essential Investigation More than in any other facet of the cerebral circulation, modern imaging techniques have greatly advanced the management of the giant intracranial aneurysm. In times past the surgeon might find himself operating on what angiographically might appear a small lesion but one which at operation turned out to be a formidable partly clotted sac whose relationship to the surrounding vessels had not been appreciated. Illustrations of this are shown in Fig. 1.
CT and Magnetic Resonance Scanning The earliest and most rapid improvement in diagnostic capability arrived with CT scanning. A mass could be delineated on plain scan sometimes with calcification and often with the appearance of contained clotted blood and a contrast scan would demonstrate the flowing blood. Comparison of these two scans would clearly show the amount of clot within the lesion and one could compare the contrast scan picture with subsequent arteriography to determine accurately whether or not there was substantial clot within the lesion.
Fig. I. (A) and (B) AP and lateral views of what appears a small middle cerebral aneurysm. The stretching of the perforating vessels would indicate that this is not the case. (C) Enhanced CT scans showing a giant aneurysm. (D) and (E) AP and lateral views post-operatively, showing that the neck was indeed relatively small and could be occluded by a single clip
L. Symon: Management of Giant Intracranial Aneurysms
A
109
B
Fig. 2. Correspondence of the flow void in Fig. 2 A with angiographic filling in Fig. 2 B indicating the absence of clot within this giant aneurysm
Magnetic resonance scan has added a further dimension, being particularly valuable in the demonstration of laminated clot and in the comparison of the fluid containing component of the aneurysm and the clot. Appropriate manipulation of the image weighting by the neuroradiologist is important in this regard. Examples are shown in Fig. 2, 3 C, 4 C.
Detailed Angiography The keystone of the management of these lesions however remains detailed angiography. Even in the absence of modern scanning technology, careful analysis of good quality high definition magnified arteriograms will usually indicate the presence of a very much larger unfilled sac in an apparently small aneurysm. Figure 1 shows displacement of perforating vessels in relation to what appears a relatively small sac. In discussing angiography one particular caveat should be introduced. The modern tendancy to digital subtraction angiography may in a number of instances subtract out valuable information such as the relationship between the aneurysm and important bony structures. An example of this is shown in Fig. 3 where digital subtraction angiography removed the relationship of the neck to the posterior elinoid process, a relationship which could be restored by consideration of the MR scan as seen in Fig. 3 C. An attempt to treat this aneurysm by the standard pterional approach in another clinic resulted in failure to reach the neck of
the aneurysm, which was in fact finally clipped by an approach from below the tentorium through a combined supra- and infra-tentorial approach. Angiography may fail to fill the lesion completely. An elegant example of this is shown in a giant vertebral aneurysm which on CT scan appeared to be simply an enhancing mass anterior to the brainstem (Fig. 4). Nonfilling of one vertebral artery was regarded as suspicious but not diagnostic although there was a suggestion of a faint vascular shadow on certain of the angiograms suggesting poor filling of a large sac. This was readily demonstrable on magnetic resonance imaging and the sac opened in the appropriate fashion and decompressed. Notes on Handling of a Giant Aneurysm
The maximum relevant information about the size nature and relationship of the aneurysm is a prerequisite before any surgery. One must appreciate the relationship to neighbouring vessels, perforating arteries and important structures such as the brain stem or the chiasm and optic apparatus. This can now be much more confidently inferred by careful analysis of magnified arteriograms, high quality CT and MR scanning with and without Gadolinium enhancement. One of the major advantages of high field strength MRI is its anatomical delineation of structures close to the base or the mid-line where even thin cut fourth generation CT cannot compare in anatomical detail.
110
L. Symon: Management of Giant Intracranial Aneurysms
A
C
B
Fig. 3. (A) and (B) Digital subtraction angiograms of basilar aneurysm. Note that all the bony detail has been subtracted. (C) MR scan of the same lesion. The fact that the neck of the aneurysm is below the posterior clinoid is easily appreciated. Laminated clot in the aneurysm is also seen
The Attack on a Giant A n e u r y s m - t h e Approach The approach to a giant aneurysm must be designed to enable control of proximal circulation as soon as possible. Where we are dealing with the terminal carotid artery, the surgeon must decide whether adequate access to the carotid proximal to the neck of the aneurysm will be feasible from an intracranial approach or whether the internal carotid artery should be exposed in the neck. Giant aneurysms one must remember partially occlude intra-cranial vessels and m a y stimulate an unusual degree of collateral supply. This in certain circumstances, as in the middle cerebral circulation, is
of enormous help to the surgeon since the peripheral brain m a y remain relatively well supplied while the proximal vessel is occluded. In the carotid ophthalmic region however despite proximal occlusion, there may be very considerable blood flow through the aneurysm still and in this particular circumstance the manoeuvre described by Samson and his colleagues from Dallas is particularly valuable 3. Instead of simply occluding the carotid circulation in the neck, a closed segment of the carotid circulation between the neck and the carotid artery distal to the aneurysm is evacuated by suction. The original Dallas manoeuvre described this by cath-
L. Symon: Management of Giant Intracranial Aneurysms
.#,
111
B
C
D
Fig. 4. (A) Enhanced CT scan of a mass causing brain stem compression. (B) Vertebral angiography, non-tilling of the left vertebral artery but no apparent pathological circulation. (C) MR scan shows a giant aneurysm with laminated clot within it. (D) An early post-operative CT scan, the greater part of the clot in the aneurysm has been removed and the aneurysm clipped. The wall remains. The patient was asymptomatic
eterisation of the carotid artery above temporary ligation of the common and external carotids. In my experience however this is occasionally dangerous as suction to such a long area of artery may result in postoperative thrombosis as it did in one of my own cases with tragic hemiplegia some days post-operatively. It
is on the whole safer while occluding the common carotid artery to cannulate one of the branches of the external carotid artery, temporarily occluding the rest, and to apply suction to the branch rather than to the internal carotid artery itself. Under these circumstances however even quite large and difficult necks in the
112
carotid and ophthalmic region may become handlable sometimes even without the necessity to remove the anterior clinoid process. In the basilar circulation, particularly at the top of the basilar artery it is extremely important to assess the relationship of the aneurysm neck to the posterior clinoid. This will determine whether or not the approach can simply be a pterional one, or whether a small temporal lobectomy or perhaps the capacity to divide the tentorium should be added to the approach in order to get sufficiently low on the basilar artery to occlude the neck. One should also attempt, from analysis of the pre-operative scans, to determine whether or not the basilar artery aneurysm is likely to be adherent to the elivus or posterior clinoids, this sometimes producing embarrassing complications actually during surgery.
The Use of Temporary Vascular Occlusion Most senior surgeons will agree that temporary vascular occlusion was regarded with great disfavour for many years. A great flood of experimental and clinical evidence attests to the rapid failure of electrical activity in the brain consequent upon complete arrest of the circulation7, 15, 29, 32. We have ourselves annotated the disruption of normal cellular metabolism with failure of ionic homeostasis within a few minutes and if prolonged this results in a reversible cell change. The death of cells is inevitable within 5-I 0 minutes following complete circulatory arrest. Our experimental work has demonstrated however that there are thresholds of cerebral blood flow to suppress brain electrical activity, above the level of 20mls/100gm/min brain electrical activity being perfectly preserved s' 16. While all electrical activity fails at such levels of CBF, ionic homeostasis does not tend to be disrupted until levels of around 10mls/100 gm have been reached when potassium and calcium ions move across cell membranes accompanied by considerable neurotransmitter release and the death of the cell probably after the passage of one to two hours of such intense ischemia2' 17. Other laboratory experiments have shown a reversal of potassium movement after an hour of transient vascular occlusion in the primate and confident full recovery of electrical potential has been shown at normotension and normothermia in the primate following periods of occlusion lasting 15-20 minutes6. On this basis therefore we have felt that temporary vascular occlusion of any major artery for periods of up to 15 minutes may be adopted as a rule. One should
L. Symon: Management of Giant Intracranial Aneurysms
be particularly cautious where temporary vascular occlusion results in withdrawal of the blood supply to the deep nuclei supplied by perforating vessels either in the brainstem or in the basal ganglia, as the collateral circulation in these areas is very poor. One also should be particularly careful that proximal vascular occlusion alone is not employed if the aneurysm is going to be opened. Opening the aneurysm in the presence of proximal occlusion alone results in bleeding out of the distal collateral circulation with fall of peripheral perfusion pressure practically to zero and the induction of very intense ischemia in the area distal to the proximal clip. One should therefore include with proximal vascular occlusion, vascular occlusion of the run-off vessel so that the collateral circulation may preserve perfusion in the distal distribution of the occluded vessel. We were not the first to use proximal vascular occlusion. Lawrence Pool 22 in 1961 reported a series of twenty-three cases in which temporary clips had been used during extensive bifrontal approaches but his initial enthusiasm was not reproduced in other hands. One must be careful since the effects of temporary vascular occlusion assessed by scanning or traditional electron microscopy have shown quite evident arterial endothelial damage and there is a potential for postoperative thrombosis at the site of temporary clips 1' 8, 9, 10, 11, 12, 13, 14, 20, 21, 23, 24, 25, 26, 30, 31 O u r o w n analysis of the situation however has indicated that the use of a temporary Scoville clip with closing pressure of less than 80 gm is apparently safe in that a review of sixtysix patients who underwent such temporary occlusion compared to one hundred and nineteen cases operated on by the same surgeon over the same period in which temporary clips were not used, failed to reveal any difference between the outcome or complication rate in the two groups 19. Similar findings have been reported by Suzuki in an analysis of three hundred and eightyfour patients 28. It is important to note that temporary vascular occlusion is a phenomenon which should be applied electicly. It should not be used as an emergency measure when the aneurysm is ruptured and the situation is rapidly threatening to get out of control.
Monitoring During Temporary Arterial Occlusion The demonstration of flow thresholds for synaptic transmission following temporary vascular occlusion in baboons 4' 5 has been paralleled by the demonstration in man of a relationship between central conduction time and the hemispheral cerebral blood flow measured
L. Symon: Management of Giant Intracranial Aneurysms
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Fig. 5. (A) AP view of an apparently broad necked middle cerebral aneurysm. (B) Evoked response recording during temporary occlusion of intracranial carotid proximal anterior and proximal middle cerebral vessels. The N20 of the SSEP almost but not quite disappeared and recovered on reperfusion. There was no post-operative deficit. (C) Postoperative view showing a single clip to the aneurysm a t the C2 level a n d a t the s o m a t o s e n s o r y cortex 18' 29 W e have d e m o n s t r a t e d t h a t flow values o f m o r e t h a n 3 0 m l s / l O O g m / m i n a r e u n a t t e n d e d b y significant
114 change in CCT but progressive prolongation of conduction time occurs in hemispheres subjected to perfusion of below 30 mls/100 gm/min 25. We have shown experimentally that restoration of the electrical activity is possible to complete normality from complete silence after 20 minutes of vascular occlusion in the baboon. In 1987 we reported 2~the use of evoked response monitoring in over one hundred operations for intracranial aneurysms including forty in which temporary clips had been applied to major vessels of the circle of Willis. Central conduction time to hand stimulation of 5.4 + 0.4 milliseconds is now standard in several laboratories. While halogenated anaesthetics cause prolongation of conduction time this occurs bilaterally and it is therefore essential to compare one hemisphere with the other. Such monitoring is expecially valuable where temporary vascular occlusion is being applied either to the middle cerebral or to the proximal carotid artery. Where the anterior cerebral circulation is involved, we have demonstrated that somatosensory evoked responses are of no guide to the intensity of ischemia induced by temporary vascular occlusion, but from our experience with transcranial motor evoked responses both experimentally and in man we have concluded that the thresholds of time in relation to damage are the same for the anterior cerebral artery as for arteries serving the somatosensory cortex, and since routine motor monitoring is rather more difficult, we do not as a rule employ it in relation to the anterior cerebral circulation. We have shown that there are two significant parameters in relation to evoked response monitoring. Provided the evoked response fails slowly over a period of longer than 4 minutes, we have never seen a permanent disability. Where the evoked response fails quickly, so that within 2 minutes or almost within repetitive sweeps, since averaging is necessary, then anxiety must be expressed and one should conclude that less than 10 minutes are available before there is a threat to irretrievable damage. While this is not invariable all our patients who have suffered damage from temporary vascular occlusion in relation to giant aneurysms have fallen into this group of rapid failure of the evoked response. When the evoked response has failed, if it is restored within 10 minutes following reperfusion, permanent damage is unlikely 2~
L. Symon: Management of Giant Intracranial Aneurysms An example of somatosensory evoked response recording in relation to a middle cerebral aneurysm is shown in Fig. 5, an aneurysm whose broad neck had resulted in attempted occlusion elsewhere being abandoned, but in which with control of terminal carotid, proximal middle cerebral, proximal and anterior-cerebral it was possible to empty the aneurysm and apply a clip while the evoked response showed signs of declining but it was rapidly restored on restoration of perfusion.
Preparation of the Aneurysm Neck for Occlusion With the afferent and efferent circulation safely under control and by preference some monitoring indicating the safety or otherwise of the procedure, the surgeon is now in a position to prepare the neck for occlusion. At this stage it is easiest to collapse the aneurysm. If the aneurysm contains only fluid blood it is a simple matter to puncture it either with a needle attached to a suction apparatus, or with the suction apparatus itself and control any slight residual bleeding in the aneurysm as for example by the ophthalmic circulation unless the Dallas manoeuvre has been employed. The Dallas manoeuvre of course will absolve one from the necessity of opening a carotid ophthalmic aneurysm. A small sucker applied directly to the puncture area mounted on a needle will usually be sufficient to control any residual bleeding; the sac will collapse and a clip may be applied if necessary with some dissection to ensure non-inclusion of a portion of the segment of the aneurysm bearing artery. A more considerable problem arises however when the sac is partially occupied by thrombus. It is then necessary to open the aneurysm and at this point one should emphasise that the opening should be a good way away from the neck so that any rip will not run down to the neck and involve one in a hurried repair of the main vessel. The contained clot should be evacuated from the area of the neck and in this respect the ultrasonic dissector is of particular value. One must remember that in the area of the neck and sometimes within the main vessel there may be areas of atheroma, and it may be necessary to carry out a small endarterectomy of the major vessel to obtain a segment of the major vessel sufficiently pliable to accommodate a clip applied to the aneurysm. Where there is any doubt
Fig. 6. (A), (B), and (C) Views of a giant terminal carotid aneurysm previously operated on elsewhere. (D) and (E) Post-operativeviews, neck has been occludedby a ligature, the silverclip holds the two ends of the ligature together, an added security to even a triple knot
m
0
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116
L. Symon: Management of Giant Intracranial Aneurysms
Fig. 7. Giant middle cerebral aneurysm. (A) Pre-operativelateral view. (B) Pre-operative MR scan showing lamination and flow voids within the aneurysm. (C) Post-operative lateral angiogram (the print accidentally reversed). (D) Post-operative CT scan twelve months later. The wall of the aneurysm is still seen. The central clot has been evacuated in large measure and has subsequently almost disappeared
of course a small segment of aneurysm neck should be left rather than attempting the apply a clip which may embarrass circulation through the main vessel. It is not necessary completely to evacuate contained clot from the aneurysm but only to evacuate enough from the region of the neck to make the neck pliable. A further possibility in a very fibrous and thick neck is to apply
a crushing clamp to the aneurysm neck carefully distal to the main vessel, of course. This appears to be quite a safe manoeuvre, it results in a suitable groove to take a clip and enables even a long clip to close satisfactorily, something which it may be impossible to achieve in the presence of a very thick aneurysm wall. The excellent clips developed by Drake, Sugita and others I have
L. Symon: Management of Giant Intracranial Aneurysms
found of enormous value in this regard, one should remember that a clip which is easy to put on should also be easy to take off since one may very well wish to adjust it, and each surgeon will develop a preference for a particular type of clip which he finds most easy to handle. Before the permanent clip is applied to the neck of the aneurysm it is wise particularly in the presence of atheroma in the region of the neck to release the distal occlusion on the aneurysm bearing vessel to enable collateral circulation to wash out any debris. The permanent clip may then be applied and the proximal occlusion released. Where Sugita clips are used I have found that although they are excellent clips it is usually wise to place two rather than one since they may very well open in the presence of a completely restored perfusion pressure. Very occasionally still I use a ligature on the neck of aneurysms particularly in the region of the terminal carotid artery (Fig. 6). However where the neck is partially strengthened by dura as in the carotid ophthalmic aneurysm there is an unfortunate tendency for the neck to tear when such a ligature is applied and an appropriately shaped clip is now almost always available. Following the application of the clip and the exclusion of the aneurysm from the circulation one may then consider the evacuation of the remainder of the clot. It is unnecessary to remove the wall of the aneurysm from structures to which it is attached, the aneurysm wall will shrink down satisfactorily washed as it will be by CSF. Figures 4 D and 7 D show the residuum of large aneurysms whose wall was incompletely removed but which have shrunk down in the post-operative period and are asymptomatic.
The Results of Surgery However careful the planning of surgery may be, giant aneurysms remain formidable lesions and morbidity and mortality are unlikely ever to reach the extremely low levels which we have now obtained in the surgery of unruptured aneurysms of moderate size. In a series of fifty-four aneurysms with protracted follow-up, the results are shown in Table 2. It will be evident that in cases where there was no recent subarachnoid haemorrhage satisfactory results were obtained in thirty-one of thirty-four cases, two patients died and there was one unsatisfactory result, the patient being disabled. On the other hand where recent subarachnoid haemorrhage had been present good results were obtained
117 Table 2. Outcome of Surgery, Giant Aneurysm Outcome
No recent S.A.H
Recent S.A.H
Excellent/good Unsatisfactory Dead
31 1 (3%) 2 (6%)
17 2 (10%) 1 (5%)
Total
34
20
in seventeen cases of this current group, an unsatisfactory result obtained in two cases and there was one death. Mortality and morbidity therefore of less than 10% could be achieved in the absence of recent haemorrhage, but where recent haemorrhage had occurred combined morbidity and mortality was 15%. It is likely that each individual surgeon will achieve a minimum morbidity and mortality with these lesions as he becomes more experienced but I am afraid that one must continue to expect some problems. Counselling of the patient and the relatives must therefore indicate distinct possibility of death or disablement when such a lesion is approached. It should also be evident that where the probability of catastrophe seems unduly high and the symptoms are not pressing, then conservatism may be the best policy.
References 1. Acland R (1973) Thrombus formation in microvascular surgery: an experimental study of the effects of surgical trauma. Surgery 73:766-771 2. Astrup J, Symon L, Branston NM etal (1977) Cortical evoked potential and extra-cellular K + and H + critical levels of brain ischaemia. Stroke 8:51-57 3. Batjer HH, Samson DS (1990) Retrograde suction decompression of giant paraclinoidal aneurysms. J Neurosurg 73:305-306 4. Branston NM, Symon L, Crockard HA (1976) Recovery of the cortical evoked response following temporary middle cerebral artery occlusion in baboons: Relation to local blood flow and PO2. Stroke 7:151-157 5. Branston NM, Symon L, Crockard HA, Pasztor E (1974) Relationship between the cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusions in the baboon. Exp Neurol 45:195-208 6. Branston NM, Symon L, Crockard HA (1976) Recovery of the cortical evoked response following temporary middle cerebral artery occlusion in baboons: Relation to local blood flow and PO2. Stroke 7:151-157 7. Dennis C, Kabat H (1939) Behaviour of dogs after complete temporary arrest of the cephalic circulation. Proc Soc Exp Biol Med 40:559-561 8. Dodson RF, Tagashire Y, Chu LWF (1976) Acute ultrastructural changes in the middle cerebral artery due to the injury and ischaemia of surgical clamping. Can J Neurol Sci 3:23-27
118 9. Dujovny M, Kossovsky N, Laha RK, Left L, Wackenhut N, Perlin A (1979) Temporary microvascular clips. Neurosurgery 5:456-463 10. Dujovny M, Osgood CP, Barrionuevo PJ, Perlin A, Kossovsky N (1978) SEM evaluation of endothelial damage following temporary middle cerebral artery occlusion in dogs. J Neurosurg 48:42-48 11. Dujovny M, Wackenhut N, Kossovsky N, Gomes CW, Laha RK, LeffL, Nelson D (1979) Minimum vascular occlusive force. J Neurosurg 51:662-668 12. Ebina K, Iwabuchi T, Suzuki S (1982) Histological change in permanently clipped or ligated cerebral arterial wall, Part II. Autopsy cases of aneurysmal neck clipping. Acta Neurochir (Wien) 66:23-42 13. Gertz SD, Rennels ML, Forbes MS, Kawamura J, Sunaga T, Nelso E (1976) Endothelial cell damage by temporary arterial occlusion with surgical clips. Study of the clip site by scanning and transmission electron microscopy. J Neurosurg 45:514-519 14. Gregorius FK, Rand RW (1975) Scanning electron microscopic observations of common carotid artery endothelium in the rat. II. Sutured arteries. Surg Neurol 4:258-264 15. Grenell RG (1946) Central nervous system resistance. 1. The effects of temporary arrest of cerebral circulation for a period of two to ten minutes. J Neuropathol Exp Neurol 5:131-154 16. Hargadine JR, Branston NM, Symon L (1980) Central conduction time in primate brain ischaemia: a study in baboons. Stroke 11:637-642 17. Harris R J, Symon L, Branston NM et al (1981) Changes in extracellular calcium activity in cerebral ischemia. J Cereb Blood Flow Metab 1:203-209 18. Hume AL, Cant BR (1978) Conduction time in somatosensory pathways in man. Electroencephalogr Clin Neurophysiol 45: 361-375 19. Jabre A, Symon L (1987) Temporary vascular occlusion during aneurysm surgery. Surg Neurol 27:47-63 20. Momma F, Wang AD, Symon L (1987) Effects of temporary arterial occlusion on somatosensory evoked responses in aneurysm surgery. Surg Neurol 27:343-352 21. Osgood CP, Dujovny M, Faille RN (1976) Early scanning elec-
L. Symon: Management of Giant Intracranial Aneurysms
22.
23.
24. 25.
26. 27.
28.
29.
30. 31.
32.
tron microscopic evaluation of microvascular manoeuvres. Angiology 27:96-105 Pool JL (1961) Aneurysms of the anterior communicating artery, bifrontal craniotomy, and routine use of temporary clips. J Neurosurg 18:98-112 Poole JCF, Cromwell SB, Benditt EP (1971) Behaviour of smooth muscle cells and formation of extracellular structures in the reaction of arterial wall to injury. Am J Pathol 62: 391414 Rosenbaum TJ, Sundt TM Jr (1978) Interrelationship of aneurysm clips and vascular tissue. J Neurosurg 48:929-934 Rosenstein J, Wang AD, Symon L, Suzuki M (1985) Relationship between hemispherical CBF, CCT, and clinical grade in aneurysmal subarachnoid hemorrhage. J Neurosurg 62:25-30 Slayback JB, Bowen WW, Hinshaw DB (1976) Intimal injm3~ from arterial clamps. Am J Surg 132:183-188 Sugita K, Hiroti T, Iguchi I, Mizutani T (1976) Comparative study of the pressure of various aneurysm clips. J Neurosurg 44:723-727 Suzuki J (1979) Prognosis of 1000 pure saccular aneurysms operated upon. In: Pia HW, Langmaid C, Zinski J (eds) Cerebral aneurysms: Advances in diagnosis and therapy. Springer, Berlin Heidelberg, pp 413-418 Symon L, Branston NM, Strong AJ etal (1977) The concepts of thresholds of ischaemia in relation to brain structure and function. J Clin Pathol 30:149-154 Symon L, Vajda J (1984) Surgical experience with giant intracranial aneurysms. J Neurosurg 61:1009-1028 Thurston JB, Buncke JH, Chater NL (1976) A scanning electron microscopy study of micro-arterial damage and repair. Plast Reconstr Surg 57:197-203 Weinberger LM, Gibbon MH, Gibbon JH Jr (1940) Temporary arrest of the circulation to the central nervous system. 2. Pathological effects. Arch Neurol Psychiatry 43:961-986
Correspondence and Reprints: Prof. Lindsay Symon, TD, FRCS, FRCSE, Gough-Cooper Department of Neurological Surgery, National Hospital, Queen Square, London WC1E 3BG, U.K.
Acta Neurochir (Wien) (1992): 116:107 - 118
. . urochlrurglca
9 Springer-Verlag 1992 Printed in Austria
Management of Giant Intracranial Aneurysms* L. Symon Gough-Cooper Department, Institute of Neurology, National Hospital for Neurology and Neurosurgery, London, U.K.
Summary Based on an own material of 64 cases a survey is given on the management of giant intracranial aneurysms. Essential investigations are as well CT and Magnetic Resonance Scanning as detailed angiographic studies. With regard to the operative handling the following questions are discussed: approach; use of temporary vascular occlusion and related monitoring; preparation of the aneurysm neck for occlusion. In cases without recent subarachnoid haemorrhage morbidity and mortality were less than 10%. It was 15% in cases where recent haemorrhage had occurred.
Keywords: Giant aneurysm; management; diagnostic; operative technique; results.
Giant aneurysms pose a problem to the neurosurgeon. While like their smaller counterparts they may present with haemorrhage, they may also present with compression of neighbouring structures to which they tend to become very adherent. They may be further complicated by the presence within the sac of massive clot rendering the whole formidable mass quite difficult to handle. This paper is based on a total of sixty-four giant aneurysms treated by myself up until 1990. Their distribution is shown in Table 1. Thirty of them presented without subarachnoid haemorrhage and thirtyfour had a history of subarachnoid haemorrhage either recently or in the past. In addition to this group of aneurysms treated by direct intracranial exposure, another twelve patients have been treated by internal carotid ligation only, two treated by balloon embolization: one successfully, one unsuccessfully, and two in whom no treatment was felt justified. The age distribution of these sixty-four aneurysms does not support the earlier view that they tended to
* Invited Lecture, presented at the European Congress of Neurosurgery, Moscow, June 23-29, 1991.
Table 1 Giant aneurysms - LS
1990
Terminal carotid Middle cerebral Anterior cerebral Posterior cerebral
30 11 7 16
Total
64
present rather later in life than their smaller counterpart.
Essential Investigation More than in any other facet of the cerebral circulation, modern imaging techniques have greatly advanced the management of the giant intracranial aneurysm. In times past the surgeon might find himself operating on what angiographically might appear a small lesion but one which at operation turned out to be a formidable partly clotted sac whose relationship to the surrounding vessels had not been appreciated. Illustrations of this are shown in Fig. 1.
CT and Magnetic Resonance Scanning The earliest and most rapid improvement in diagnostic capability arrived with CT scanning. A mass could be delineated on plain scan sometimes with calcification and often with the appearance of contained clotted blood and a contrast scan would demonstrate the flowing blood. Comparison of these two scans would clearly show the amount of clot within the lesion and one could compare the contrast scan picture with subsequent arteriography to determine accurately whether or not there was substantial clot within the lesion.
Fig. I. (A) and (B) AP and lateral views of what appears a small middle cerebral aneurysm. The stretching of the perforating vessels would indicate that this is not the case. (C) Enhanced CT scans showing a giant aneurysm. (D) and (E) AP and lateral views post-operatively, showing that the neck was indeed relatively small and could be occluded by a single clip
L. Symon: Management of Giant Intracranial Aneurysms
A
109
B
Fig. 2. Correspondence of the flow void in Fig. 2 A with angiographic filling in Fig. 2 B indicating the absence of clot within this giant aneurysm
Magnetic resonance scan has added a further dimension, being particularly valuable in the demonstration of laminated clot and in the comparison of the fluid containing component of the aneurysm and the clot. Appropriate manipulation of the image weighting by the neuroradiologist is important in this regard. Examples are shown in Fig. 2, 3 C, 4 C.
Detailed Angiography The keystone of the management of these lesions however remains detailed angiography. Even in the absence of modern scanning technology, careful analysis of good quality high definition magnified arteriograms will usually indicate the presence of a very much larger unfilled sac in an apparently small aneurysm. Figure 1 shows displacement of perforating vessels in relation to what appears a relatively small sac. In discussing angiography one particular caveat should be introduced. The modern tendancy to digital subtraction angiography may in a number of instances subtract out valuable information such as the relationship between the aneurysm and important bony structures. An example of this is shown in Fig. 3 where digital subtraction angiography removed the relationship of the neck to the posterior elinoid process, a relationship which could be restored by consideration of the MR scan as seen in Fig. 3 C. An attempt to treat this aneurysm by the standard pterional approach in another clinic resulted in failure to reach the neck of
the aneurysm, which was in fact finally clipped by an approach from below the tentorium through a combined supra- and infra-tentorial approach. Angiography may fail to fill the lesion completely. An elegant example of this is shown in a giant vertebral aneurysm which on CT scan appeared to be simply an enhancing mass anterior to the brainstem (Fig. 4). Nonfilling of one vertebral artery was regarded as suspicious but not diagnostic although there was a suggestion of a faint vascular shadow on certain of the angiograms suggesting poor filling of a large sac. This was readily demonstrable on magnetic resonance imaging and the sac opened in the appropriate fashion and decompressed. Notes on Handling of a Giant Aneurysm
The maximum relevant information about the size nature and relationship of the aneurysm is a prerequisite before any surgery. One must appreciate the relationship to neighbouring vessels, perforating arteries and important structures such as the brain stem or the chiasm and optic apparatus. This can now be much more confidently inferred by careful analysis of magnified arteriograms, high quality CT and MR scanning with and without Gadolinium enhancement. One of the major advantages of high field strength MRI is its anatomical delineation of structures close to the base or the mid-line where even thin cut fourth generation CT cannot compare in anatomical detail.
110
L. Symon: Management of Giant Intracranial Aneurysms
A
C
B
Fig. 3. (A) and (B) Digital subtraction angiograms of basilar aneurysm. Note that all the bony detail has been subtracted. (C) MR scan of the same lesion. The fact that the neck of the aneurysm is below the posterior clinoid is easily appreciated. Laminated clot in the aneurysm is also seen
The Attack on a Giant A n e u r y s m - t h e Approach The approach to a giant aneurysm must be designed to enable control of proximal circulation as soon as possible. Where we are dealing with the terminal carotid artery, the surgeon must decide whether adequate access to the carotid proximal to the neck of the aneurysm will be feasible from an intracranial approach or whether the internal carotid artery should be exposed in the neck. Giant aneurysms one must remember partially occlude intra-cranial vessels and m a y stimulate an unusual degree of collateral supply. This in certain circumstances, as in the middle cerebral circulation, is
of enormous help to the surgeon since the peripheral brain m a y remain relatively well supplied while the proximal vessel is occluded. In the carotid ophthalmic region however despite proximal occlusion, there may be very considerable blood flow through the aneurysm still and in this particular circumstance the manoeuvre described by Samson and his colleagues from Dallas is particularly valuable 3. Instead of simply occluding the carotid circulation in the neck, a closed segment of the carotid circulation between the neck and the carotid artery distal to the aneurysm is evacuated by suction. The original Dallas manoeuvre described this by cath-
L. Symon: Management of Giant Intracranial Aneurysms
.#,
111
B
C
D
Fig. 4. (A) Enhanced CT scan of a mass causing brain stem compression. (B) Vertebral angiography, non-tilling of the left vertebral artery but no apparent pathological circulation. (C) MR scan shows a giant aneurysm with laminated clot within it. (D) An early post-operative CT scan, the greater part of the clot in the aneurysm has been removed and the aneurysm clipped. The wall remains. The patient was asymptomatic
eterisation of the carotid artery above temporary ligation of the common and external carotids. In my experience however this is occasionally dangerous as suction to such a long area of artery may result in postoperative thrombosis as it did in one of my own cases with tragic hemiplegia some days post-operatively. It
is on the whole safer while occluding the common carotid artery to cannulate one of the branches of the external carotid artery, temporarily occluding the rest, and to apply suction to the branch rather than to the internal carotid artery itself. Under these circumstances however even quite large and difficult necks in the
112
carotid and ophthalmic region may become handlable sometimes even without the necessity to remove the anterior clinoid process. In the basilar circulation, particularly at the top of the basilar artery it is extremely important to assess the relationship of the aneurysm neck to the posterior clinoid. This will determine whether or not the approach can simply be a pterional one, or whether a small temporal lobectomy or perhaps the capacity to divide the tentorium should be added to the approach in order to get sufficiently low on the basilar artery to occlude the neck. One should also attempt, from analysis of the pre-operative scans, to determine whether or not the basilar artery aneurysm is likely to be adherent to the elivus or posterior clinoids, this sometimes producing embarrassing complications actually during surgery.
The Use of Temporary Vascular Occlusion Most senior surgeons will agree that temporary vascular occlusion was regarded with great disfavour for many years. A great flood of experimental and clinical evidence attests to the rapid failure of electrical activity in the brain consequent upon complete arrest of the circulation7, 15, 29, 32. We have ourselves annotated the disruption of normal cellular metabolism with failure of ionic homeostasis within a few minutes and if prolonged this results in a reversible cell change. The death of cells is inevitable within 5-I 0 minutes following complete circulatory arrest. Our experimental work has demonstrated however that there are thresholds of cerebral blood flow to suppress brain electrical activity, above the level of 20mls/100gm/min brain electrical activity being perfectly preserved s' 16. While all electrical activity fails at such levels of CBF, ionic homeostasis does not tend to be disrupted until levels of around 10mls/100 gm have been reached when potassium and calcium ions move across cell membranes accompanied by considerable neurotransmitter release and the death of the cell probably after the passage of one to two hours of such intense ischemia2' 17. Other laboratory experiments have shown a reversal of potassium movement after an hour of transient vascular occlusion in the primate and confident full recovery of electrical potential has been shown at normotension and normothermia in the primate following periods of occlusion lasting 15-20 minutes6. On this basis therefore we have felt that temporary vascular occlusion of any major artery for periods of up to 15 minutes may be adopted as a rule. One should
L. Symon: Management of Giant Intracranial Aneurysms
be particularly cautious where temporary vascular occlusion results in withdrawal of the blood supply to the deep nuclei supplied by perforating vessels either in the brainstem or in the basal ganglia, as the collateral circulation in these areas is very poor. One also should be particularly careful that proximal vascular occlusion alone is not employed if the aneurysm is going to be opened. Opening the aneurysm in the presence of proximal occlusion alone results in bleeding out of the distal collateral circulation with fall of peripheral perfusion pressure practically to zero and the induction of very intense ischemia in the area distal to the proximal clip. One should therefore include with proximal vascular occlusion, vascular occlusion of the run-off vessel so that the collateral circulation may preserve perfusion in the distal distribution of the occluded vessel. We were not the first to use proximal vascular occlusion. Lawrence Pool 22 in 1961 reported a series of twenty-three cases in which temporary clips had been used during extensive bifrontal approaches but his initial enthusiasm was not reproduced in other hands. One must be careful since the effects of temporary vascular occlusion assessed by scanning or traditional electron microscopy have shown quite evident arterial endothelial damage and there is a potential for postoperative thrombosis at the site of temporary clips 1' 8, 9, 10, 11, 12, 13, 14, 20, 21, 23, 24, 25, 26, 30, 31 O u r o w n analysis of the situation however has indicated that the use of a temporary Scoville clip with closing pressure of less than 80 gm is apparently safe in that a review of sixtysix patients who underwent such temporary occlusion compared to one hundred and nineteen cases operated on by the same surgeon over the same period in which temporary clips were not used, failed to reveal any difference between the outcome or complication rate in the two groups 19. Similar findings have been reported by Suzuki in an analysis of three hundred and eightyfour patients 28. It is important to note that temporary vascular occlusion is a phenomenon which should be applied electicly. It should not be used as an emergency measure when the aneurysm is ruptured and the situation is rapidly threatening to get out of control.
Monitoring During Temporary Arterial Occlusion The demonstration of flow thresholds for synaptic transmission following temporary vascular occlusion in baboons 4' 5 has been paralleled by the demonstration in man of a relationship between central conduction time and the hemispheral cerebral blood flow measured
L. Symon: Management of Giant Intracranial Aneurysms
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Fig. 5. (A) AP view of an apparently broad necked middle cerebral aneurysm. (B) Evoked response recording during temporary occlusion of intracranial carotid proximal anterior and proximal middle cerebral vessels. The N20 of the SSEP almost but not quite disappeared and recovered on reperfusion. There was no post-operative deficit. (C) Postoperative view showing a single clip to the aneurysm a t the C2 level a n d a t the s o m a t o s e n s o r y cortex 18' 29 W e have d e m o n s t r a t e d t h a t flow values o f m o r e t h a n 3 0 m l s / l O O g m / m i n a r e u n a t t e n d e d b y significant
114 change in CCT but progressive prolongation of conduction time occurs in hemispheres subjected to perfusion of below 30 mls/100 gm/min 25. We have shown experimentally that restoration of the electrical activity is possible to complete normality from complete silence after 20 minutes of vascular occlusion in the baboon. In 1987 we reported 2~the use of evoked response monitoring in over one hundred operations for intracranial aneurysms including forty in which temporary clips had been applied to major vessels of the circle of Willis. Central conduction time to hand stimulation of 5.4 + 0.4 milliseconds is now standard in several laboratories. While halogenated anaesthetics cause prolongation of conduction time this occurs bilaterally and it is therefore essential to compare one hemisphere with the other. Such monitoring is expecially valuable where temporary vascular occlusion is being applied either to the middle cerebral or to the proximal carotid artery. Where the anterior cerebral circulation is involved, we have demonstrated that somatosensory evoked responses are of no guide to the intensity of ischemia induced by temporary vascular occlusion, but from our experience with transcranial motor evoked responses both experimentally and in man we have concluded that the thresholds of time in relation to damage are the same for the anterior cerebral artery as for arteries serving the somatosensory cortex, and since routine motor monitoring is rather more difficult, we do not as a rule employ it in relation to the anterior cerebral circulation. We have shown that there are two significant parameters in relation to evoked response monitoring. Provided the evoked response fails slowly over a period of longer than 4 minutes, we have never seen a permanent disability. Where the evoked response fails quickly, so that within 2 minutes or almost within repetitive sweeps, since averaging is necessary, then anxiety must be expressed and one should conclude that less than 10 minutes are available before there is a threat to irretrievable damage. While this is not invariable all our patients who have suffered damage from temporary vascular occlusion in relation to giant aneurysms have fallen into this group of rapid failure of the evoked response. When the evoked response has failed, if it is restored within 10 minutes following reperfusion, permanent damage is unlikely 2~
L. Symon: Management of Giant Intracranial Aneurysms An example of somatosensory evoked response recording in relation to a middle cerebral aneurysm is shown in Fig. 5, an aneurysm whose broad neck had resulted in attempted occlusion elsewhere being abandoned, but in which with control of terminal carotid, proximal middle cerebral, proximal and anterior-cerebral it was possible to empty the aneurysm and apply a clip while the evoked response showed signs of declining but it was rapidly restored on restoration of perfusion.
Preparation of the Aneurysm Neck for Occlusion With the afferent and efferent circulation safely under control and by preference some monitoring indicating the safety or otherwise of the procedure, the surgeon is now in a position to prepare the neck for occlusion. At this stage it is easiest to collapse the aneurysm. If the aneurysm contains only fluid blood it is a simple matter to puncture it either with a needle attached to a suction apparatus, or with the suction apparatus itself and control any slight residual bleeding in the aneurysm as for example by the ophthalmic circulation unless the Dallas manoeuvre has been employed. The Dallas manoeuvre of course will absolve one from the necessity of opening a carotid ophthalmic aneurysm. A small sucker applied directly to the puncture area mounted on a needle will usually be sufficient to control any residual bleeding; the sac will collapse and a clip may be applied if necessary with some dissection to ensure non-inclusion of a portion of the segment of the aneurysm bearing artery. A more considerable problem arises however when the sac is partially occupied by thrombus. It is then necessary to open the aneurysm and at this point one should emphasise that the opening should be a good way away from the neck so that any rip will not run down to the neck and involve one in a hurried repair of the main vessel. The contained clot should be evacuated from the area of the neck and in this respect the ultrasonic dissector is of particular value. One must remember that in the area of the neck and sometimes within the main vessel there may be areas of atheroma, and it may be necessary to carry out a small endarterectomy of the major vessel to obtain a segment of the major vessel sufficiently pliable to accommodate a clip applied to the aneurysm. Where there is any doubt
Fig. 6. (A), (B), and (C) Views of a giant terminal carotid aneurysm previously operated on elsewhere. (D) and (E) Post-operativeviews, neck has been occludedby a ligature, the silverclip holds the two ends of the ligature together, an added security to even a triple knot
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116
L. Symon: Management of Giant Intracranial Aneurysms
Fig. 7. Giant middle cerebral aneurysm. (A) Pre-operativelateral view. (B) Pre-operative MR scan showing lamination and flow voids within the aneurysm. (C) Post-operative lateral angiogram (the print accidentally reversed). (D) Post-operative CT scan twelve months later. The wall of the aneurysm is still seen. The central clot has been evacuated in large measure and has subsequently almost disappeared
of course a small segment of aneurysm neck should be left rather than attempting the apply a clip which may embarrass circulation through the main vessel. It is not necessary completely to evacuate contained clot from the aneurysm but only to evacuate enough from the region of the neck to make the neck pliable. A further possibility in a very fibrous and thick neck is to apply
a crushing clamp to the aneurysm neck carefully distal to the main vessel, of course. This appears to be quite a safe manoeuvre, it results in a suitable groove to take a clip and enables even a long clip to close satisfactorily, something which it may be impossible to achieve in the presence of a very thick aneurysm wall. The excellent clips developed by Drake, Sugita and others I have
L. Symon: Management of Giant Intracranial Aneurysms
found of enormous value in this regard, one should remember that a clip which is easy to put on should also be easy to take off since one may very well wish to adjust it, and each surgeon will develop a preference for a particular type of clip which he finds most easy to handle. Before the permanent clip is applied to the neck of the aneurysm it is wise particularly in the presence of atheroma in the region of the neck to release the distal occlusion on the aneurysm bearing vessel to enable collateral circulation to wash out any debris. The permanent clip may then be applied and the proximal occlusion released. Where Sugita clips are used I have found that although they are excellent clips it is usually wise to place two rather than one since they may very well open in the presence of a completely restored perfusion pressure. Very occasionally still I use a ligature on the neck of aneurysms particularly in the region of the terminal carotid artery (Fig. 6). However where the neck is partially strengthened by dura as in the carotid ophthalmic aneurysm there is an unfortunate tendency for the neck to tear when such a ligature is applied and an appropriately shaped clip is now almost always available. Following the application of the clip and the exclusion of the aneurysm from the circulation one may then consider the evacuation of the remainder of the clot. It is unnecessary to remove the wall of the aneurysm from structures to which it is attached, the aneurysm wall will shrink down satisfactorily washed as it will be by CSF. Figures 4 D and 7 D show the residuum of large aneurysms whose wall was incompletely removed but which have shrunk down in the post-operative period and are asymptomatic.
The Results of Surgery However careful the planning of surgery may be, giant aneurysms remain formidable lesions and morbidity and mortality are unlikely ever to reach the extremely low levels which we have now obtained in the surgery of unruptured aneurysms of moderate size. In a series of fifty-four aneurysms with protracted follow-up, the results are shown in Table 2. It will be evident that in cases where there was no recent subarachnoid haemorrhage satisfactory results were obtained in thirty-one of thirty-four cases, two patients died and there was one unsatisfactory result, the patient being disabled. On the other hand where recent subarachnoid haemorrhage had been present good results were obtained
117 Table 2. Outcome of Surgery, Giant Aneurysm Outcome
No recent S.A.H
Recent S.A.H
Excellent/good Unsatisfactory Dead
31 1 (3%) 2 (6%)
17 2 (10%) 1 (5%)
Total
34
20
in seventeen cases of this current group, an unsatisfactory result obtained in two cases and there was one death. Mortality and morbidity therefore of less than 10% could be achieved in the absence of recent haemorrhage, but where recent haemorrhage had occurred combined morbidity and mortality was 15%. It is likely that each individual surgeon will achieve a minimum morbidity and mortality with these lesions as he becomes more experienced but I am afraid that one must continue to expect some problems. Counselling of the patient and the relatives must therefore indicate distinct possibility of death or disablement when such a lesion is approached. It should also be evident that where the probability of catastrophe seems unduly high and the symptoms are not pressing, then conservatism may be the best policy.
References 1. Acland R (1973) Thrombus formation in microvascular surgery: an experimental study of the effects of surgical trauma. Surgery 73:766-771 2. Astrup J, Symon L, Branston NM etal (1977) Cortical evoked potential and extra-cellular K + and H + critical levels of brain ischaemia. Stroke 8:51-57 3. Batjer HH, Samson DS (1990) Retrograde suction decompression of giant paraclinoidal aneurysms. J Neurosurg 73:305-306 4. Branston NM, Symon L, Crockard HA (1976) Recovery of the cortical evoked response following temporary middle cerebral artery occlusion in baboons: Relation to local blood flow and PO2. Stroke 7:151-157 5. Branston NM, Symon L, Crockard HA, Pasztor E (1974) Relationship between the cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusions in the baboon. Exp Neurol 45:195-208 6. Branston NM, Symon L, Crockard HA (1976) Recovery of the cortical evoked response following temporary middle cerebral artery occlusion in baboons: Relation to local blood flow and PO2. Stroke 7:151-157 7. Dennis C, Kabat H (1939) Behaviour of dogs after complete temporary arrest of the cephalic circulation. Proc Soc Exp Biol Med 40:559-561 8. Dodson RF, Tagashire Y, Chu LWF (1976) Acute ultrastructural changes in the middle cerebral artery due to the injury and ischaemia of surgical clamping. Can J Neurol Sci 3:23-27
118 9. Dujovny M, Kossovsky N, Laha RK, Left L, Wackenhut N, Perlin A (1979) Temporary microvascular clips. Neurosurgery 5:456-463 10. Dujovny M, Osgood CP, Barrionuevo PJ, Perlin A, Kossovsky N (1978) SEM evaluation of endothelial damage following temporary middle cerebral artery occlusion in dogs. J Neurosurg 48:42-48 11. Dujovny M, Wackenhut N, Kossovsky N, Gomes CW, Laha RK, LeffL, Nelson D (1979) Minimum vascular occlusive force. J Neurosurg 51:662-668 12. Ebina K, Iwabuchi T, Suzuki S (1982) Histological change in permanently clipped or ligated cerebral arterial wall, Part II. Autopsy cases of aneurysmal neck clipping. Acta Neurochir (Wien) 66:23-42 13. Gertz SD, Rennels ML, Forbes MS, Kawamura J, Sunaga T, Nelso E (1976) Endothelial cell damage by temporary arterial occlusion with surgical clips. Study of the clip site by scanning and transmission electron microscopy. J Neurosurg 45:514-519 14. Gregorius FK, Rand RW (1975) Scanning electron microscopic observations of common carotid artery endothelium in the rat. II. Sutured arteries. Surg Neurol 4:258-264 15. Grenell RG (1946) Central nervous system resistance. 1. The effects of temporary arrest of cerebral circulation for a period of two to ten minutes. J Neuropathol Exp Neurol 5:131-154 16. Hargadine JR, Branston NM, Symon L (1980) Central conduction time in primate brain ischaemia: a study in baboons. Stroke 11:637-642 17. Harris R J, Symon L, Branston NM et al (1981) Changes in extracellular calcium activity in cerebral ischemia. J Cereb Blood Flow Metab 1:203-209 18. Hume AL, Cant BR (1978) Conduction time in somatosensory pathways in man. Electroencephalogr Clin Neurophysiol 45: 361-375 19. Jabre A, Symon L (1987) Temporary vascular occlusion during aneurysm surgery. Surg Neurol 27:47-63 20. Momma F, Wang AD, Symon L (1987) Effects of temporary arterial occlusion on somatosensory evoked responses in aneurysm surgery. Surg Neurol 27:343-352 21. Osgood CP, Dujovny M, Faille RN (1976) Early scanning elec-
L. Symon: Management of Giant Intracranial Aneurysms
22.
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tron microscopic evaluation of microvascular manoeuvres. Angiology 27:96-105 Pool JL (1961) Aneurysms of the anterior communicating artery, bifrontal craniotomy, and routine use of temporary clips. J Neurosurg 18:98-112 Poole JCF, Cromwell SB, Benditt EP (1971) Behaviour of smooth muscle cells and formation of extracellular structures in the reaction of arterial wall to injury. Am J Pathol 62: 391414 Rosenbaum TJ, Sundt TM Jr (1978) Interrelationship of aneurysm clips and vascular tissue. J Neurosurg 48:929-934 Rosenstein J, Wang AD, Symon L, Suzuki M (1985) Relationship between hemispherical CBF, CCT, and clinical grade in aneurysmal subarachnoid hemorrhage. J Neurosurg 62:25-30 Slayback JB, Bowen WW, Hinshaw DB (1976) Intimal injm3~ from arterial clamps. Am J Surg 132:183-188 Sugita K, Hiroti T, Iguchi I, Mizutani T (1976) Comparative study of the pressure of various aneurysm clips. J Neurosurg 44:723-727 Suzuki J (1979) Prognosis of 1000 pure saccular aneurysms operated upon. In: Pia HW, Langmaid C, Zinski J (eds) Cerebral aneurysms: Advances in diagnosis and therapy. Springer, Berlin Heidelberg, pp 413-418 Symon L, Branston NM, Strong AJ etal (1977) The concepts of thresholds of ischaemia in relation to brain structure and function. J Clin Pathol 30:149-154 Symon L, Vajda J (1984) Surgical experience with giant intracranial aneurysms. J Neurosurg 61:1009-1028 Thurston JB, Buncke JH, Chater NL (1976) A scanning electron microscopy study of micro-arterial damage and repair. Plast Reconstr Surg 57:197-203 Weinberger LM, Gibbon MH, Gibbon JH Jr (1940) Temporary arrest of the circulation to the central nervous system. 2. Pathological effects. Arch Neurol Psychiatry 43:961-986
Correspondence and Reprints: Prof. Lindsay Symon, TD, FRCS, FRCSE, Gough-Cooper Department of Neurological Surgery, National Hospital, Queen Square, London WC1E 3BG, U.K.
