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Intracranial Neurosurgical Treatment of Occlusive Cerebrovascular Disease

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26. Pilgeram L, Chee A, Von Dem Bussche G: Evidence for abnormalities in clotting and thrombolysis as a risk factor for stroke. Stroke 4: 643-657,

1973

27. Collaborative Group for the Study of Stroke in Young Women: Oral contraception and increased risk of cerebral ischemia or thrombosis. New Engl J Med 288: 871-878, 1973

28. Alkjaersig N, Fletcher A, Burstein R: Association between oral con-traceptive use and thromboembolism: A new approach to its investigation

Academic Press, vol. 5 (Blood), pp 135-174, 1974

33. Fletcher A, Alkjaersig N: Prophylactic and therapeutic uses of an-tithrombotic drugs in cerebral vascular disease. In Siekert RG (ed): Cerebrovascular Survey Report, revised January 1976, fourth edition. Rochester, Minnesota, Whiting Press, pp 198-212, 1976

34. Millikan CH: Anticoagulant or surgical treatment of cerebral ischemia.

In Ingelfinger F, et al (eds): Controversy in Internal Medicine: II.

Philadelphia, WB Saunders, pp 787-803, 1974

Intracranial Neurosurgical Treatment of Occlusive

Cerebrovascular Disease

JOSE L. SALAZAR, M.D., F.A.C.S., ABDUL R. C. AMINE, M.D., AND OSCAR SUGAR, M.D., F.A.C.S.

SUMMARY Anastomosis of the extracranial superficial temporal artery to the intracranial middle cerebral artery offers an additional source of blood to the cerebral circulation in patients with transient ischemic episodes. Fourteen cases are reported. Two representative

cases with three anastomoses demonstrate the use of this technique in occlusion of the internal carotid artery, occlusion of the middle cerebral artery and stenosis of the middle cerebral artery. Indications and contraindications of the procedure are discussed.

SURGICAL TREATMENT of arteriosclerotic occlusive

disease of coronary, aortic, and extremity vessels is well

known. Until recently, only a few investigators

16

have

applied microsurgical techniques to deal with severe

cere-bral arteriosclerotic disease, hitherto considered inaccessible

or technically out of reach of usual vascular surgical

tech-niques. In 1967, Donaghy and Yasargil

6

proposed a new

bypass operation to provide additional blood supply to the

ischemic brain in patients with carotid occlusion or middle

cerebral artery stenosis or occlusion. This procedure entails

an anastomosis of the superficial temporal artery (STA) to a

cortical branch of the middle cerebral artery (MCA) by way

of a 4-cm craniotomy above the ear (fig. 1). We have carried

out such a procedure in 13 cases; in another, the anastomosis

was made between the occipital branch of the external

carotid artery and the middle cerebral artery (table 1).

Another shunting procedure (which we have not yet carried

out) was designed by Lougheed

7

using a saphenous vein graft

to carry blood from the common carotid artery in the neck

through a craniotomy into the intracranial portion of the

in-ternal carotid artery in cases of inin-ternal carotid occlusion in

the neck, when the superficial temporal artery is too small to

Department of Neurosurgery, Abraham Lincoln School of Medicine, University Hospitals, University of Illinois at the Medical Center, 912 South Wood Street, Chicago, Illinois 60612.

Reprint requests to Dr. Salazar, Department of Neurosurgery, 912 South Wood Street, Chicago, Illinois 60612.

permit an effective anastomosis with the middle cerebral

branches. In the two patients presented here, transient

ischemic attacks (TIAs) led to angiography which disclosed

occlusive disease; one patient had stenosis of the right MCA

and occlusion of the left MCA; and the other had occlusion

of the right internal carotid artery.

Report of Cases

Casel

A 50-year-old man was admitted to the University of

Illinois Hospital because of episodes of transient numbness

and weakness of the left face, arm, hand, and leg and

associated speech difficulty lasting three to four minutes,

oc-curring five times during the month prior to admission. He

was not receiving treatment for arterial hypertension known

for about one or two years. Examination showed blood

pressure of 160/110 mm Hg; the left nasolabial fold was

flattened; and the carotid pulses were somewhat decreased.

Chemical tests indicated borderline diabetes, and a

Frederickson type IV hyperlipoproteinemia. The EEG and

brain scan were normal. Carotid and vertebral angiography

showed stenosis of the right MCA (fig. 2) and occlusion of

the left MCA, with retrograde flow into the distribution of

this artery by way of the left posterior cerebral artery

(fig. 3).

The patient had an uneventful recovery from a right

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SUPERFICIAL TEMPORAL ARTERY

FIGURE 1. Site of craniectomy for superficial temporal-middle

cerebral artery anastomosis.

MCA anastomosis. Eleven days after this procedure, a left STA-MCA anastomosis was carried out. A week later, bilateral external carotid angiograms via the femoral artery showed patency of both STA-MCA anastomoses, with fill-ing of the entire MCA, particularly on the formerly occluded side (figs. 4 and 5). Postoperative brain scan and blood flow study with 99mTc pertechnetate showed changes due to surgery, and good flow bilaterally. The patient was stable neurologically at the time of discharge, taking Ascrip-tin 250 mg b.i.d. and diphenylhydantoin (DilanAscrip-tin) 100 mg t.i.d. on a prophylactic basis.

TABLE 1 Summary of Superficial Temporal MCA Anastomoses

FIGURE 2. Right brachial angiogram shows the stenosis of the

right middle cerebral and collateral circulation to the left hemisphere via the posterior cerebral branches.

Date Pt., age Diagnosis Postoperative angiogram, date Postoperative results 2/24/74 2/25/74 6/17/74 7/11/74 8/12/74 8/13/74 9/17/74 9/23/74 10/18/74 10/31/74 11/ 1/74

R.K.,

H.N.,

M.A.,

E.E.,

N.C.,

Z.C.,

B.M.,

N.B.,

S.A.,

H.L.,

B.W.,

64 58 63 51 70* 54 54 74 50* 67 74

Occlusion L MCA, stroke-in-evolution

TIAs, occlusion R internal carotid

R cerebral thrombosis

(recovered), stenosis R MCA TIAs, occlusion L internal

carotid, mild cerebellar dysfunction

N.C., 70* TIAs, occlusion R internal carotid

TIAs, 90% occlusion L MCA

Occluded anastomosis, 3/8/74 Not done Patent anastomosis, 6/26/74 and 8/13/74 Patent anastomosis, 7/18/74 Patent anastomosis, 8/19/74 Occluded anastomosis, 12/20/74 Patent anastomosis TIAs, bilateral internal carotid

occlusion

TIAs, occlusion L internal carotid

TIAs, 90% occlusion R carotid artery, occlusion L MCA

TIAs, 60% occlusion L internal Occluded anastomosis,

R hemiplegia and aphasia; slightly improved

Pt. died due to MI three weeks postoperatively

Asymptomatic, returned to work Essentially unchanged, no more TIAs

Asymptomatic

Pt. unchanged as of 7/26/75 Pt. still has intermittent weakness

in L leg, otherwise improved Asymptomatic 12/16/74 2/ 4/75 V.L, 67 H.E., 37 carotid

Small L cerebral infarct (dysphasia recovered), 90% occlusion L MCA, 60% occlusion L anterior cerebral artery

TIAs, L internal carotid Occlusion L internal carotid,

residual (minimal) L hemiparesis

Occluded (L occipital MCA anastomosis), 9/30/74

Patent bilateral anastomoses, Asymptomatic, returned to work 11/5/74

Pt. died due to MI one month postoperatively

Small L cerebral infarct, mild dysphasia — improved 11/74

(Pt. had bilateral anastomoses 11/12/74.) One anastomosis patent

Occluded anastomosis, 12/30/74

Patent anastomosis, 2/11/75

Small L cerebral infarct, residual confusion one month postoperatively Pt. stable, no further neurological

deficit postoperatively, returned to work

*Oases reported in this paper.

L = left, R = right, MCA = middle cerebral artery, MI = rayocardial infarction, TIAs = transient ischemic attacks.

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FIGURE 3. A P view, left carotid shows occlusion of the left middle

cerebral (large arrow) and a 1.2-mm superficial temporal artery (small arrow).

cardial infarcts, and his long-standing hypertension was be-ing treated with hydrodiuril. The admission blood pressure was 220/190 mm Hg. Neurological examination was within normal limits. The brain scan (99mTc pertechnetate) was nor-mal but the isotope blood flow study showed decreased flow in the right carotid system and hemisphere, with "flip-flop" phenomenon (decreased density on the right initially, in-creased density on the right at a time when there was mally decreased flow on the left). The EEG was within nor-mal limits. Angiographical studies showed occlusion of the right internal carotid artery in the neck, but the right hemisphere was irrigated by collateral flow from posterior circulation via the posterior communicating and posterior cerebral arteries (fig. 6). Left carotid angiography showed normal flow in the left cerebrum without cross-flow into the right side. The patient underwent right STA-MCA

FIGURE 4. AP view, selective right externalcathelerization shows

the anastomosis functioning well.

FIGURE 5. AP view, selective left externalcatheterization showing

the anastomosis (vertical arrow) to be functioning well. Horizontal arrow shows the MCA occlusion.

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FIGURE 6. AP view shows occlusion of the right internal carotid

and collateral flow to the right hemisphere.

anastomosis with excellent postoperative course. Post-operative selective external carotid angiogram showed ex-cellent filling of most of the branches of the MCA by way of the anastomosis (fig. 7). Postoperative brain scan and isotope flow study showed evidence of craniotomy and in-creased flow to the right hemisphere. The patient was dis-charged on Ascriptin and prophylactic diphenylhydantoin. Both patients have been followed (eight and ten months respectively) and both have been asymptomatic with subjec-tive feeling of improvement.

Results

Patent anastomoses have been demonstrated in 8 of 14

in-stances (7 of 13 patients) by angiography and MmTc isotope cerebral blood flow study. Six patients are free of TIAs, feel subjectively improved, and have resumed their usual oc-cupations. These have no neurological deficit demonstrable in follow-up examinations. One patient had mild dysphasia

FIGURE 7. AP postoperative angiogram shows the superficial

temporal artery (small arrow) and the area of anastomosis (large arrow) filling the entire middle cerebral artery territory.

postoperatively, from which he recovered and is doing well. Occlusion of the anastomosis has been demonstrated by angiography in five patients. One patient (R.K.) had a stroke-in-evolution, resembling TIAs — he was evaluated within 24 hours. Embolectomy of the MCA was attempted but was not completed because of cerebral edema. Super-ficial temporal artery anastomosis was done but the diam-eter of the superficial temporal artery was smaller than 1 mm and there was evidence of intracranial arteriosclerosis. The condition of another patient (Z.C.) was unchanged on July 26, 1974, seven months after the anastomosis was demonstrated to be occluded.

One patient (N.B.) is essentially asymptomatic. One (H.L.) died due to myocardial infarction, one month post-operatively. Another (V.L.) is alive, complaining of poor memory. Signs and symptoms of residual infarction have disappeared postoperatively.

One patient (H.N., the only one who did not have follow-up angiography) died three weeks after the operation from a myocardial infarction.

Discussion

The treatment of cerebrovascular insufficiency is sum-marized in table 2. The medical treatment of the risk factors appears to be of value, especially treatment of hypertension

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II. Surgical

A. Endarterectomy of cervical vessels B. Endarterectomy of intracranial vessels

C. Revascularization procedures (grafts or bypass of occluded vessels)

1. Superficial temporal or occipital anastomosis to middle cerebral artery

2. Vein graft from cervical to intracranial carotid artery

which appears to have a statistically valid effect in decreas-ing stroke incidence.8 The role of the vasodilators is still dis-puted, with anecdotal reports of improvement, but no statistically demonstrable benefit. Acetylsalicylic acid may well help prevent platelet emboli, but at a risk of provoking bleeding from the gastrointestinal tract; the role of anti-coagulants is still disputed, especially by those who have treated patients for coronary artery disease and have had nonhemorrhagic strokes appear during this time.

Baker et al.B concluded that from the standpoint of mor-tality, long-term anticoagulant therapy plays no beneficial role in the treatment of thrombotic cerebrovascular disease and may be harmful.

Whisnant et al.10 evaluated anticoagulants in the

treat-ment of TIAs and they felt that the effect of anticoagulant therapy can be expected to occur in the first two months following the onset of TIAs. So the difference between the two groups of patients studied occurred in the first two months. There was little difference in the probability of a stroke occurring after that time between the treated and un-treated groups.

Endarterectomy of the carotid vessels for stenosis with, presumably, emboli into the cerebral circulation would appear to have merit, but only when the stenosis is accessi-ble. Treatment by endarterectomy or removal of thrombus has been disappointing when the internal carotid is occluded, unless this is quite acute."•12 Reports of success in up to 42.8% of cases13 must be balanced by the neurological com-plications during surgery (e.g., 2.93% mortality and 5.86% morbidity in the 613 cases of Bland et al.14). Sundt et al.ls consider direct surgical treatment for an occluded internal carotid artery hazardous, with high risk, and not to be done except in rare circumstances. Endarterectomy of intra-cranial vessels16- " has not been widely undertaken because of lack of proof of value, but recent reports are en-couraging.18

Revascularization procedures, such as have been reported here, appear to hold great promise in delivering more blood to an ischemic or potentially ischemic brain. The difficulties (table 3) lie in identification of candidates for operation, and finding vessels of adequate diameter for maintaining an open anastomosis. Up to now, the patency of the anastomosis is reported to be between 60% and 70% (e.g., 66% of

6. Inadequate diameter of recipient cortical vessel ( < 1 mm)

anastomoses performed by Yasargil in 1971 reviewed by Chater were patent19); with experience and better selection of patients, the patency rate should improve. Table 4 gives a summary of the indications for this type of operation. Although numerous tests have been designed to diagnose vascular disease in the cervical and cerebral vessels,20 the key test is angiography, perhaps signaled by cerebral flow studies using 99mTc scanning or actual measurements of flow with 133Xe. Proper diagnosis of the vascular lesion involves three-vessel or four-vessel angiography, although some authorities in the field of cervical carotid endarterectomy feel that for practical purposes bilateral carotid visualization is sufficient.21 Chater et al.2 include as indication for opera-tion multiple cerebrovascular occlusions associated with low perfusion syndromes such as mental deterioration, memory loss, vertigo, ataxia, etc. Very small vessel disease may be identified with new sophisticated techniques. Bradac et al.22 have shown direct stenotic or occlusive lesions of the middle cerebral trunk but also indirect evidence of lesions such as delayed or retrograde filling of one or several branches of the main artery, slow progression of the contrast material, or lack of filling in the area of infarction. Austin et al.6 suggest that in addition to TIAs and lesions demonstrated to be in-accessible to operation in the neck, another indication for anastomosis may be a reduction of 20% to 25% in the cere-bral blood flow on the side of the lesion. Spetzler et al.28 have discussed the importance of flow measurements in revas-cularization procedures. Postoperative angiograms may show not only the patent anastomosis but also the number of branches of the middle cerebral artery which fill. Relief of TIAs without subsequent strokes has been reported by Austin et al.24 in all the cases with patent anastomoses. In an 18-month follow-up, Tew4 had five of eight functioning anastomoses, but no patient had recurrence of symptoms or infarction. As with carotid endarterectomy and anti-coagulant therapy, so with this new anastomosis firm proof is as yet lacking that treatment of cerebrovascular disease

TABLE 4 Clinical Indications for Superficial

Temporal-Mid-dle Cerebral Arterial Anastomosis

1. TIAs with demonstrable intracranial lesions sufficient to explain the attacks

2. Reversible ischemic neurological deficit (RIND) 3. Occlusion of one or more vessels in the neck producing

cerebrovascular insufficiency

4. Mild neurological deficit with focal ischemia with demonstrated lesion sufficient to explain infarct and with potential for more severe lesion

5. Vertebrobasilar insufficiency (?)

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itself increases survival rate, but improved quality of sur-vival and reduced numbers of TIAs appear to be benefits to be derived. With TIAs, the incidence of infarction, hem-orrhage, or death within two to three years has reached 10% to 4 0 % " " while disabling stroke may rise to 18% to 60% of cases of TIA within one year. There is insufficient informa-tion concerning long-term results in cases of cerebral revascularization procedures, but the short-term follow-up indicates enough promise to warrant cautious extension of the procedure and, perhaps, even extension to insufficiency of the vertebrobasilar system when this appears to steal blood from the carotid system.

References

1. Donaghy RMP: What's new in surgery? Surg Gynec Obstet 134: 269-271, 1972

2. Chater N, Mani J, Tonnemacher K: Superficial temporal artery bypass in occlusive cerebral vascular disease. Calif Med 119: 9-13 (Aug) 1973 3. Lazar ML, Clark K: Microsurgical cerebral revascularization. Concepts

and practice. Surg Neurol 1: 355-359, 1973

4. Tew JM: Cerebral revascularization, by arterial anastomosis vein bypass graft and embolectomy. Presented to the 23rd annual meeting of the Congress of Neurological Surgery, October 15, 1973, Honolulu, Hawaii 5. Austin G, Laffin D, Hayward W: Physiologic factors in the selection of patients for superficial temporal artery-to-middle cerebral artery anastomosis. Surgery 75: 861-868, 1974

6. Donaghy P, Yasargil G: Extra intracranial blood flow diversion. Presented at the American Association of Neurological Surgeons, April, 1968, Chicago, Illinois

7. Lougheed W, Marshall BM, Hunter M, et al: Common carotid to in-tracranial internal carotid bypass venous graft. J Neurosurg 34: 114-118,

1971

8. Freis ED: The Veterans Administration cooperative study on an-tihypertensive agents. Implications for stroke prevention. Stroke 5: 76-77 (Jan-Feb) 1974

9. Baker RN, Broward JA, Fang HC, et al: Anticoagulant therapy in cere-bral infarction. Neurology 12: 823-829, 1962

10. Whisnant JP, Matsumoto N, Elveback LR: The effect of anticoagulant therapy on the prognosis. Mayo Clin Proc 48: 844-849 (Dec) 1973

11. Thompson JE, Austin DJ: Surgical treatment of arteriosclerotic occlusions of the carotid artery in the neck. Surgery 5 1 : 74-83, 1962 12. DeBakey ME: cited in Thompson JE, Austin DJ: Surgical treatment of

arteriosclerotic occlusions of the carotid artery in the neck. Surgery 51: 74-83, 1962

13. Garamella JJ, Lynch MF, Jensen NK, et al: Endarterectomy and thrombectomy for the totally occluded extracranial internal carotid. Ann Surg 164: 325-333, 1966

14. Bland JE, Chapman RD, Wylie EJ: Neurologic complications of carotid artery surgery. Ann Surg 171: 459-464 (Apr) 1970

15. Sundt TM Jr, Sandok BA, Whisnant JP: Carotid endarterectomy: Complications and preoperative assessment of risk. Mayo Clin Proc 50: 301-306, 1975

16. Chou SN: Embolectomy of middle cerebral artery. Report of a case. J Neurosurg 20: 161-163, 1963

17. Jacobson JH II, Wallman LJ, Schumacher GA, et al: Microsurgery as an aid to middle cerebral artery endarterectomy. J Neurosurg 19: 108-115, 1962

18. Zlotnik El: Thrombectomy of the middle cerebral artery. J Neurosurg 42: 723-725 (Jun) 1975

19. Chater NL, Yasargil MG: Results of temporal artery bypass procedures in the treatment of cerebrovascular disease. Presented at Congress of Neurological Surgeons, October 1971, Miami, Florida

20. Smith KR Jr, Cova RR Jr: Correlation of ophthalmodynamometry, in-frared thermography, and auscultation with four-vessel arteriography in the diagnosis of carotid occlusive disease. Presented to the annual meeting of the AANS, 1974

21. Javid H: Surgical management of cerebral vascular insufficiency. Arch Surg 80: 883-889, 1960

22. Bradac GB, Simon RS, Heitzeberg H: Angiographic findings in the region of the middle cerebral artery in ischemic disease. Neurochirurgia 16: 26-34, 1973

23. Spetzler R, Chater N: Superficial temporal artery-middle cerebral artery blood flow measurements. Presented to the annual meeting of the AANS, 1974

24. Austin G, Thompson J, Laffin D, et al: Technical consideration regarding direction and perfusion of blood flow in patients undergoing STA-MCA anastomosis. Presented to the annual meeting of AANS, 1974 25. Marshall J: The natural history of transient ischemic cerebrovascular

at-tacks. Q J Med 33: 309-324, 1964

26. Baker RN, Ramseyer JC, Schwartz WS: Prognosis in patients with tran-sient cerebral ischemic attacks. Neurology 18: 1157-1165, 1968 27. Toole JF, Janeway R, Miller H, et al: Transient episodes of

cerebro-vascular ischemia (TIAs). Effects of medical or surgical management on natural history of the illness. Trans Am Clin Climatol Assoc 84: 71-77, 1973

Correction

An error appeared in the second paragraph of the legend of figure 2 (STROKE 7: 289 [May-June] 1976): hypoxemia should be hyperemia.

References

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