surgical aspects of carotid-vertebral insufficiency · vertebral artery lesions, it is fortunate,...

Postgraduate Medical Journal (May 1971) 47, 282-296.

Surgical aspects of carotid-vertebral insufficiency

J. A. GILLESPIEM.D., Ch.M., F.R.C.S.

Surgeon, St George's Hospital, London, S. W.Reader in Surgery, University of London

THE ASSOCIATION between obstructive lesions of theextra-cranial portions of the carotid and vertebralarteries and symptoms of cerebro-vascular in-sufficiency has long been recognized (Todd, 1844),and with the development of reconstructive arterialsurgery during the past 20 years it is hardly surprisingthat a great deal more attention has been focusedon the condition. However, in spite of the ease ofdemonstration of the lesions by arteriography, andthe technical competence of vascular surgeons inrestoring arterial patency, the role of surgery in themanagement ofocclusive extra-cranial arterial diseaseis not yet clearly defined: indeed, it is the subject ofmuch controversy. This state of affairs results froma number of factors-a lack of basic knowledge ofthe natural history of the untreated disease; theuncertainty of the relationship between a demon-strated carotid or vertebral artery obstruction andischaemic cerebral symptoms; and, not least, thelack of published results of large, properly controlledclinical trials of surgical versus conservative manage-ment 15 years after Eastcott, Pickering & Rob (1954)reported their first experience of carotid endarte-rectomy.The present paper is concerned chiefly with a

consideration of the role of surgery in management,but it is necessary also to review briefly currentthinking on the pathology and investigation ofextra-cranial cerebro-vascular disease, and to beclear as to what one hopes to achieve by restorationof full arterial patency.

PathologyAtheroma is, of course, by far the most important

cause of occlusive disease of the extra-cranial vessels.It most often takes the form of a fibrous stenosinglesion with superficial thrombosis (Fig. 1), the lattertending to lead to complete occlusion, perhaps pre-ceded by embolization. Ulcerating lesions of theatheromatous plaque also occur frequently, and area likely source of emboli to the intracranial arteries(Fig. 2). There is, however, a wide range of otherpathological conditions which may, in varyingdegrees of rarity, cause extra-cranial occlusions and

FIG. 1. An extreme, smooth stenosis of the internalcarotid artery.

they must be kept in mind-emboli from the heart,spontaneous dissecting aneurysms, giant cell arteritis,Takayasu's disease, scleroderma or even trauma(Little et al., 1969). As an extreme rarity the vertebralor even carotid artery may be occluded by anembolus resulting from retrograde thrombosis froma vegetation in the post-stenotic dilatation of thesubclavian artery distal to a cervical rib compression(Shucksmith, 1963). More common, though its rolein pathogenesis may be difficult to assess in theindividual patient, is tortuosity of the internalcarotid vessels, often with extreme angulation orkinking in certain positions of the neck.The demonstration of an extra-cranial arterial

copyright. on July 26, 2021 by guest. P

rotected byhttp://pm

j.bmj.com

/P

ostgrad Med J: first published as 10.1136/pgm

j.47.547.282 on 1 May 1971. D

ownloaded from

http://pmj.bmj.com/

Carotid-vertebral insufficiency

FIG. 2. An irregular, ulcerating lesion of the internalcarotid artery. This is unlikely to reduce blood flow, butthe patient's multiple transient cerebral ischaemicepisodes may well be due to liberation of micro-emboli.

obstruction in a patient with cerebral ischaemia doesnot necessarily mean that this is the causal lesion:indeed, as Crompton (1969) has put it, there is anembarrassing failure of correlation. For example,there have been many post-mortem studies in whichan observed high incidence of arterial obstructionwas unremarked by cerebral symptoms in life(Samuel, 1956; Martin, Whisnant & Sayre, 1960).The overall autopsy incidence of atheromatousdisease of the extra-cranial vessels in unselectedseries of middle aged and elderly subjects has beenvariously stated to be between 40%4 (Martin et al.,1960) and 8%y (Kameyama & Okinaka, 1963), thefigure obviously depending in part on whetherstenoses of the cervical vessels are counted, or onlycomplete occlusions. It follows, therefore, that notevery obstructive lesion is clinically significant, andthe problem is to recognize those which are. Thesituation is further complicated by the frequentassociation of intra-cranial obstructions with extra-cranial. The former often are of the greater impor-

tance in the production of symptoms, yet they maybe unrecognized unless the intra-cranial vessels areroutinely visualized arteriographically in the in-vestigation of the patient.With regard to the situation of carotid and

vertebral artery lesions, it is fortunate, from theviewpoint of surgical access, that they are at theorigins of these vessels in the vast majority of cases.Indeed, the internal carotid artery is rarely affectedby atheroma between the sinus and the siphon,though lesions along the course of the vertebralarteries are more frequent, especially in the left(Schwartz & Mitchell, 1961). The relative incidenceof carotid and vertebral lesions in post-mortem andarteriographic studies appears to be about equal(Stein et al., 1962; Faris& Poser, 1963; Svare, Taveras& Stein, 1964). The occurrence of significantatheromatous lesions at other sites in the extra-cranial arteries is much less common, accountingfor perhaps only 5'/. of extra-cranial atheromatouslesions (Svare et al., 1964). Acute thrombotic andulcerating atheroma, as opposed to slowly formingfibrotic stenosis, is much more commonly seen atthe origin of the internal carotid arteries than else-where, and is rare in the vertebral arteries. Its othersite of occurrence is in the proximal subclavianarteries, where it may lead to the rather intriguingsteal syndrome (Contorni, 1960).

It is therefore important when considering investi-gation and treatment of extra-cranial cerebro-vascular disease to practise four vessel angiographyas a routine, whenever possible, otherwise multipleand perhaps significant lesions are liable to be missedin a considerable proportion of cases. Similarly, ashas already been pointed out, intra-cranial angio-grams should also be obtained routinely: forexample, Hutchinson & Yates (1957) found that50V% of a series of patients coming to autopsy as aresult of a cerebral infarct had both intra- and extra-cranial disease associated. Other investigations havesuggested that a combination of intra- and extra-cranial arterial occlusion is the important factor inthe production ofmany cerebral infarcts (Kameyama& Okinaka, 1963; Weiner, Berry & Kundin, 1964).It may well be, of course, that a proportion of theseintra-cranial lesions are the result of emboli from aproximal internal carotid lesion, rather than beingprimary atheroma.Only by having full information about the state

of the intra-cranial vessels can the possible pathologi-cal significance of any accessible extra-cranial lesionbe judged, and surgery be applied more rationally.

The natural history of atheromatous extra-cranialcerebro-vascular diseaseThe difficulties in obtaining clear-cut useful

information about the natural history of occlusive

283copyright.

on July 26, 2021 by guest. Protected by

http://pmj.bm

j.com/

Postgrad M

ed J: first published as 10.1136/pgmj.47.547.282 on 1 M

ay 1971. Dow

nloaded from

http://pmj.bmj.com/

J. A. Gillespie

extra-cranial cerebro-vascular disease are consider-able, stemming first from the impossibility in apatient with cerebral infarction of being certain onclinical grounds of the primary site of the arterialocclusion (Lascelles & Burrows, 1965). Similarly,clinical differentiation between embolic and occlusivelesions as the cause of an infarct is usually equallyuncertain. Even more fundamental is possible un-certainty in distinguishing between cerebral haemor-rhage and infarction. Complete angiography wouldfacilitate a proper study of natural history, but itshazards, particularly in the elderly, preclude its useas a routine investigation, so that this useful toolis only applied in selected cases.

In general, therefore, it is not possible in thecurrent state of knowledge to predict the effects ofuntreated extra-cranial cerebro-vascular disease,and this greatly increases the difficulty of definingthe place of surgical treatment. Rather betterinformation is available about one more readilydefined form of cerebral ischaemia, namely thetransient variety, in which the episodes of neuro-logical deficit last no longer than an hour or two.When these attacks are associated with demonstrablestenotic disease in the extra-cranial vertebral orcarotid vessels they are regarded by vascular surgeonsas the best indication for arterial reconstruction: itis therefore important to consider what is known ofprognosis in the untreated patient.

Transient cerebral ischaemia appears to have itseffects about equally often in the vertebral andcarotid territories, asjudged by clinical investigation.Of eighty-two such patients followed by Acheson &Hutchinson (1964), half developed a stroke duringthe period of follow-up of 3 years, the averageinterval between the onset of ischaemic attacks andthe stroke being 13 months. Strokes appeared rathermore often in their series in patients with vertebralischaemia than carotid, and resulted in total dis-ability or death in about a third of the patients.Marshall (1964) showed that stroke occurred earlierin carotid ischaemia than in vertebro-basilar, at 14and 23 months respectively, in the untreated patientsin his large series. He emphasizes (1969) that as therisk of a completed stroke is high in transientischaemic attacks associated with a carotid stenosistreatment is urgently required. This urgency is notso marked in vertebral lesions. The variability withwhich progression to stroke occurs in patients withtransient cerebral ischaemia is well known, andattacks may cease spontaneously at any time. Rathercuriously, the risk of stroke does not seem to berelated to the frequency of the attacks (Bradshaw &Casey, 1957). Parry (1969) suggests that once apatient has had a stroke he has a 20% chance ofhaving another within a year and a 10-40% chanceof being dead within 5 years.

The special investigation of patients with suspectedextra-cranial carotid or vertebral artery diseaseAngiographyAngiography is the mainstay of investigation.

There is still some controversy as to whether directpuncture of the neck vessels is desirable, or whetheraortic injection through a catheter passed via aperipheral artery is safer and better. The moderntrend is towards the latter technique. Wood & Hilal(1969) have laid down four basic guide lines for thechoice of arteriographic technique, and these havemuch to commend them: first, all four vessels shouldbe visualized throughout their cervical passage fromtheir origins; second, multiple radiographic projec-tions may be needed to give complete informationabout the significance of plaques involving only partof the vessel circumference, and the significance ofkinks in tortuous vessels; third, the whole intra-cranial circulation must also be visualized to ex-clude other cerebral pathology and to show theextent of intra-cranial atheroma; finally, the arterio-graphic technique used must have a minimalmorbidity.Apart from showing the existence of disease in

the intra- and extra-cranial arteries, arteriographywill also demonstrate the site and extent of collateralarterial pathways, and a knowledge of these may beof importance in planning surgical treatment.

Dangers of arteriographyMany workers have pointed out the higher inci-

dence of neurological complications of angiographyin patients with ischaemic arterial disease, comparedwith that in patients being investigated for cerebraltumours and other non-ischaemic conditions. How-ever, De Bakey and his colleagues (Crawford, DeBakey & Weibel, 1969) report a mortality of less than1 from angiography in an enormous number ofinvestigations in occlusive extra-cranial cerebro-vascular disease. The danger of arteriography isperhaps greatest when direct vessel puncture isemployed, especially by less experienced radiologists,the chief hazard lying in the intra-mural injection ofthe contrast medium. This may result in acutestenosis or obstruction of the artery, and to a lessextent in the detachment of atheromatous emboli atthe site of puncture. For example, it is a commonsurgical experience to find a complete internal carotidocclusion at operation, due to recent red thrombussuperimposed on an atheromatous plaque, in apatient in whom arteriography only a few daysbefore had shown a tight stenosis. This situation maysometimes have been precipitated by manual com-pression of the vessel to stop bleeding after removalof the arteriography needle.

It is to avoid these complications of direct needlepuncture that non-selective aortic arch injection is

284copyright.


http://pmj.bm

j.com/

Postgrad M


ay 1971. Dow

nloaded from

http://pmj.bmj.com/


so often advocated now, a short catheter being passedup the left brachial artery, preferably, to just beyondthe aortic valve. A bolus of contrast material is veryrapidly injected, and, ideally, multiple exposures aremade with a biplane apparatus. The injection maybe repeated with the patient changed in posture ifthis appears to be indicated by the first series offilms. This technique gives X-rays of good diagnosticvalue for boththe extra-and intra-cranial arteries, andalso shows well the origins of the common carotid,vertebral, subclavian and innominate arteries.

Intravenous arteriography by the simultaneousinjection of large volumes of contrast medium intoa superficial vein in each arm has been advocated asa much simpler technique, avoiding any possiblearterial trauma, but the resulting arteriograms arefrequently of too poor quality for diagnostic useful-ness, and the method has not been widely adopted.

Other methods of studying thc effects of ischaemicdiscase on the cerebral bloodWhile arteriography is essential in the proper

investigation of patients other simpler techniqueshave been employed, particularly as screening tools,and in the follow up of patients after surgery. Noneis wholly reliable, but three are still in the experi-mental stage: thermography, isotope techniques, andDoppler ultrasonography. Thermography (Wood,1964, 1965; Wood & Hill, 1966; Mawdsley et al.,1968) is particularly applicable in internal carotidartery disease as the frontal and supra-orbitalbranches of the ophthalmic artery supply the skinon the forehead. The temperature of this area andof the inner canthus of the eye is reduced in over80% of patients in the presence of a carotid obstruc-tion or significant stenosis. The Doppler ultrasono-graphic technique (Brisman et al. 1970) is alsoapplicable to cervical carotid disease, indicatingwhen carotid blood flow is reduced. O'Brien et al.(1967) and others have applied isotope scanningmetheds to the intact skull, with the object ofdetecting diminished hemispheric blood flow in thepresence of ischaemia due to extra-cranial disease,but the correlation with arteriographic findings hasbeen poor.

It seems unlikely that any ofthese indirect methodscurrently available can be developed to give con-stantly reliable information about blood flow, andarteriography remains the essential investigation inall patients in whom surgery is contemplated. It mustroutinely demonstrate the entire extra- and intra-cranial course of all the major vessels supplying thebrain.

The effects of cerebral ischaemia due to extra-cranialcarotid and vertebral artery diseaseA wide variety of clinical presentations of cerebral

ischaemia occur, ranging from the major dramaticstroke to the 'little stroke' or transient ischaemicattack, the latter tending to recur with varying fre-quency. Clinical differentiation between carotid andvertebro-basilar ischaemia may be difficult, symp-toms depending so much on the ability of the colla-teral circulation to compensate for diminished bloodflow in one major vessel, but certain observationsmay be helpful in pointing to the artery involved(Williams, 1969).

In carotid disease anterior cerebral symptoms arerare, except in bilateral occlusion, because of thenormally good cross-flow via the anterior com-municating artery. It is the middle cerebral arteryterritory which is so often affected, resulting in thewell recognized syndromes of speech disturbances,hemiplegia, in which the legs may be spared due toadequate collateral blood flow, and hemianopic fielddefects. Vertebro-basilar ischaemia also producessome well recognized symptoms (Williams & Wilson,1962), such as vertigo, visual disturbances, which areoften transient, drop attacks, and numbness andclumsiness of the arm. Epileptic fits may occur, andoccipital headaches are not uncommon. Vertebro-basilar symptoms tend to be recurrent, and are ofwide variety.However, the symptoms of carotid and vertebro-

basilar ischaemia are variable, and may co-existtogether, so that when arteriography has beendecided upon it is essential, as has already beenstressed, to visualize all four vessels in both theirextra-cranial and intra-cranial course.

Selection of patients for angiographyIt is clear that only a small proportion of patients

with symptoms suggestive of carotid or vertebralartery lesions will be candidates for surgery, butbefore surgery itself can be considered those patientswho will be submitted to arteriography must beselected. This is a task of paramount importance,yet inevitably controversial and difficult in thepresent state of knowledge. The selection processwill be initiated by the physician or neurologist whohabitually sees the whole range of patients withcerebro-vascular ischaemia and other cerebrallesions. He has three diagnostic steps to take beforedeciding that a patient should be submitted toarteriography (Williams, 1969).

First, he must decide that the symptoms are mostlikely to be due to cerebral ischaemia: second, hemust decide that the cause of the ischaemia is mostlikely to be mainly in the extra-cranial arteries, andthat there is no evidence of gross intra-cranialartery disease: third, having made the two previousdecisions he must finally decide whether othergeneral aspects of the patient's health and age willpermit surgery, should this be proved feasible.

28#5copyright.


http://pmj.bm

j.com/

Postgrad M


ay 1971. Dow

nloaded from

http://pmj.bmj.com/

J. A. Gillespie

There is no point in performing arteriography unlessit is to be followed by operation, if indicated, unlesssome other cause for the symptoms, e.g. tumour, issuspected.The preliminary selection is thus completed before

any patient reaches the surgeon, so that an awarenessof the possible role which surgery may play intreatment is necessary in physicians routinely seeingpatients with cerebral ischaemia. The final decisionwhether or not to operate now lies with the surgeon,and he will be influenced in large part by the natureof the lesions shown by arteriography. Two coursesare open to him: he may attempt to reconstructalmost every lesion in which this is possible, or hemay modify his selection by reference to the neuro-logical state of the patient, by his assessment of thepossible benefits of restoration of normal arterialpatency, and in consideration of the possible risksof surgery in the individual. It is clear that muchcontroversy is again possible, so that the rationaleand risks of surgery must be considered in somedetail.

Rationale of surgical treatment of occlusive carotidand vertebral artery disease

If the results of large controlled clinical trials ofsurgical versus non-surgical treatment were availablemuch of the controversy over the role of surgerywould disappear. In the absence of this statisticalmaterial the place of surgery must be justified byarguments setting out the theoretical advantages ofrestoring blood flow to normal, and converting anirregular, atheromatous arterial segment to a regular,smoothly lined one of normal or larger calibre. It isnecessary to consider separately internal carotidstenoses, carotid occlusions and vertebral arterylesions.

Internal carotid artery stenosisA carotid stenosis may produce cerebral ischaemic

symptoms either because it reduces blood flowdistally to a critical extent which cannot be com-pensated for by the collateral arrangements, orbecause the irregular surface of the lesion leads toliberation of emboli, often small and multiple.

It originally seemed that the former, a diminishedblood flow beyond the stenosis, provided a simpleexplanation for a major stroke or transient cerebralischaemic attack. Poiseuille's law is often quoted insupport of this, it being suggested that a progressivereduction in blood flow occurs as the stenosisincreases. However, this law applies to flow in tubeswith a free outflow: in arteries there is a peripheralresistance which is normally so large that theadditional resistance imposed by a proximal stenosisis insignificant till this has reached a critical point,only after which is distal blood flow markedly

reduced. Brice, Dowsett & Lowe (1964) measuredthis critical stenosis in man by applying a micrometerscrew clamp to healthy carotid arteries which werebeing tied for the control of intra-cranial berryaneurysms. The degree of stenosis was thus calcul-able, and blood flow proximal and distal to it wasmeasured with an electromagnetic flow-meter.Their conclusion was that blood flow was onlylessened when the lumen area was reduced to between2 and 5 mm2, corresponding to about an 85%.stenosis in an average-sized artery. In the longirregular stenoses seen frequently in atheromatouslesions, however, it may be that rather lesser degreesof stenosis reduce blood flow. For example, if bloodpressures are measured above and below a stenosisby intra-arterial needle at the time of operation asystolic gradient is frequently found when thestenosis appears on the arteriogram to be of about500/o. Such a pressure gradient, under conditions ofstable peripheral resistance, is a good indication ofa reduced blood flow (Figs. 3 and 4), and aftersuccessful reconstruction of the stenosis it shoulddisappear.

FIG. 3. An advanced, irregular, high grade stenosisprobably leading to marked reduction of blood flow(see Fig. 4).

286copyright.


http://pmj.bm

j.com/

Postgrad M


ay 1971. Dow

nloaded from

http://pmj.bmj.com/


S. B. (61) Internal carotid stenosis

250 1

150

50 E

FIG. 4. The operative pressure recordings made on thevessels illustrated in Fig. 3. Pressures below (top) andabove (bottom) block, before disobliteration. There is amarked systolic and diastolic pressure gradient suggest-ing a large reduction in blood flow beyond the stenosis.

It is thus likely that a stenosis has to be of severedegree before ischaemic symptoms can be attributedto it, and when this degree of stenosis is reached it isdifficult to see how it may be associated with multipletransient ischaemic attacks rather than a frankinfarction. Denny-Brown (1960) and others, how-ever, have suggested that if hypotensive episodesoccur in a patient with a carotid or vertebral stenosisthese may lead to a temporary reduction in bloodflow beyond the stenosis, and hence to a transientcerebral ischaemic episode. Millikan (1965) con-sidered the role of transient hypotensive episodes inthe production of 'little strokes', and suggested thatthere may often be associated intra-cranial occlusionswith a collateral circulation normally of only amarginally successful quality. Vascular spasm is nolonger invoked as a cause.Much attention has centred on the causation of

strokes by emboli liberated from the cervical athero-matous lesion. While a large embolus may occludethe middle cerebral artery to cause death or majordisability, more interesting are the showers of micro-emboli (Gunning et al., 1964) which are now widelyheld to be a cause of transient cerebral ischaemicattacks. There is no doubt that surgical restorationof a smooth lumen can prevent further embolization,and this has been invoked as a major justification foroperation. However, note must be taken of the veryvariable natural history of transient cerebralischaemia, with liability to spontaneous remission,and the good results claimed for anticoagulanttherapy. Marshall (1969), however, only advocatesthe use of anticoagulants in this condition in threecircumstances: where the atheromatous lesion isbeyond the reach of surgery, in particular in thecarotid siphon; to tide a patient over till surgery canbe arranged; and, rarely, in patients who for generalreasons are not regarded as suitable subjects forsurgery.

It would seem that where transient ischaemicattacks are associated with a carotid stenosis a goodtheoretical case for vascular reconstruction does

exist. If the attacks are due to micro-embolizationthey will stop, and in a severe grade of stenosisrestoration of normal distal blood flow will beachieved.

Progression of untreated carotid stenoses to com-plete occlusions. It is well known from serial arterio-grams over a period, particularly in the limb vessels,that stenoses tend to progress to complete occlusions,and when this occurs in the internal carotid artery amajor stroke may be the sequel. For example, apreviously observed cervical bruit, due to a carotidstenosis, may be noted to have disappeared when thepatient presents with a major stroke, the stenosishaving become an occlusion, with a consequentsevere and uncompensated reduction of cerebralblood flow. Similarly, post-mortem examination inpatients dying of stroke frequently reveals recentoccluding red thrombus superimposed on a long-standing stenosing atheromatous lesion. Finally, theocclusion by clamping of a stenotic internal carotidartery at operation under local anaesthesia maysometimes result in the patient's loss of conscious-ness, with recovery if the clamp is quickly removed,thus suggesting the effect of natural progression ofthe stenosis to occlusion if sufficient collateral path-ways did not appear.A reasonable case, from the prophylactic view-

point, may thus be made out for surgical treatmentof carotid stenoses to prevent them becoming com-plete occlusions. Further, should occlusive diseasedevelop in the other cervical arteries then a bettercollateral potential has been provided. Four arteriesmust always be better than three, and so on.

Hazards of endarterectomy for carotid stenosis.However desirable reconstruction of a carotidstenosis might appear from the above, it is alsonecessary, before advocating it, to be aware of thepossible ill-effects of the operation. The actualmortality rate of carotid reconstruction varies widelyin different reported series, ranging, for example,from an 8-9%. hospital mortality in a collected seriesof carotid reconstructions of all types in 1329patients reported by Rainer et al. (1966), to onedeath in fifty-one operations for carotid stenosisreported by Kenyon & Thompson (1965). Certainly,the sort of mortality generally quoted today inoperations for stenosis is about 2 or 3 YO (Bland et al.1970).However, a consideration of the risk of serious

neurological damage, short of death, occurring atoperation is hardly less important, and here reportedfigures vary much more widely than those quotedfor mortality: consideration of the literature andpersonal experience would suggest that about5Y/ of patients suffer some degree of neurological

287copyright.


http://pmj.bm

j.com/

Postgrad M


ay 1971. Dow

nloaded from

http://pmj.bmj.com/

J. A. Gillespie

deterioration as a result of operation, though re-covery occurs in a significant number of these.Another problem which arises when claiming that

operation has produced neurological improvement,or a cessation of transient ischaemic attacks, is thedifficulty of proving that the reconstruction hasremained patent. For example, transient ischaemicepisodes due to liberation of emboli will certainly bestopped if total occlusion of the internal carotidartery results, and if the collateral circulation isadequate no neurological sequelae will arise. Apartfrom arteriography there is no certain method ofproving that the internal carotid artery remainspatent, and the surgeon is rarely any more anxiousto suggest, than an apparently well recovered patientis to accept, further arteriography with its dis-comfort and slight hazard.

Blaisdell, Lim & Hall (1967), however, have madewhat is perhaps the most complete arteriographicfollow-up of extra-cranial arterial reconstructions todate. Out of 100 patients ninety-nine were proved tohave patent reconstructions at the close of operation.Ninety-five of these patients had repeat arteriographybetween 10 and 60 days later and in ninety-four thereconstruction remained patent. Further arterio-graphy in fifteen patients available for study 5 yearsafter operation showed none to have re-occluded,but two had become stenosed.There is thus evidence that if the carotid recon-

struction is carried out with meticulous care, andproved to be patent at the termination of operationlater re-occlusion is rare.An occasionally observed sequel to carotid recon-

struction is a spell of extreme hypertension, andhypotensive measures may need to be instituted toreduce the risk of a cerebral haemorrhage. The causeof the hypertension is not certainly known, but maybe ascribed either to cerebral ischaemia duringoperation or to carotid sinus stimulation.

Internal carotid artery occlusionWhen complete occlusion of the internal carotid

artery occurs it is liable to be associated with asevere degree of brain damage, unless the collateralcirculation is abundant. Once cerebral infarction hasoccurred there can be little hope of reversing theresults by reconstructive carotid artery surgery. Ifinfarction has not occurred then the natural collateralcirculation is adequate. In these circumstances,therefore, the justification for attempting surgerywould be the resulting improvement in the collateralpotential as a prophylaxis against the effects ofocclusions developing later elsewhere. If a stroke isin a state of evolution, however, restoration ofblood flow may reduce the final extent of the neuro-logical deficit. Hard evidence that this occurs isdifficult to find.

Even if a case can be made out for attempting toreconstruct complete internal carotid artery occlu-sions, restoration of flow, in practice, is frequentlyimpossible. This is because occlusion of the internalcarotid at its origin is so frequently followed bysuperimposition of thrombus up the length of theunbranched vessel into the skull, and this thrombusrapidly becomes adherent to the vessel wall andcannot be removed from below: if no bleed-backcan be obtained from the cranial end of the arteryrestoration of onward flow is not possible and noth-ing useful can be achieved by operation. The timetaken for this irrevocable situation to arise is veryvariable, restoration of flow being impossible toachieve within 6 hr of a stroke in one patient whileit may be restored in another months afterwards.An explanation in the latter case may sometimes liein the existence of an aberrant ascending pharyngealartery which arises above the occlusion and permitssome collateral flow through the distal internalcarotid and thus prevents thrombosis: in other casesan apparently complete occlusion on the arteriogramdoes have a small patent channel through its centrepermitting some flow to occur. In a collected seriesof 151 complete occlusions explored by varioussurgeons, flow could only be restored in forty-threepatients, and the number in whom the neurologicalstate was thought to be improved was ten (Gillespiel1967). Of particular interest is the fact that severa,authors reported that as much clinical improvementtook place in those patients in whom flow could notbe restored as in those in whom it was, though itmay be that the long-term prognosis is worse in theformer group.There is thus little hope of achieving useful im-

mediate results by operating on patients with com-plete carotid occlusions and strokes, particularly ifseveral days have elapsed (Thompson, Austin &Patman, 1967), so that the possible prophylacticvalue of a successful reconstruction must remainspeculative (Perdue et al., 1970).

Hazards of attempted reconstruction of completeinternal carotid occlusions. When complete occlusionof the internal carotid artery occurs the externalcarotid usually becomes a most important collateralpathway for cerebral blood flow, especially via itsanastomotic connections with the branches of theophthalmic artery round the orbit. It is thereforeessential that flow in the external carotid is not im-paired by operation on the internal carotid, or aworsening of the patient's neurological state is likely.Indeed, when flow in the internal carotid cannot beachieved, a formal reconstruction of a stenosedexternal carotid artery (Fig. 5) may be worth whileto facilitate its usefulness as a collateral (Deithriclbet al., 1968).

288copyright.


http://pmj.bm

j.com/

Postgrad M


ay 1971. Dow

nloaded from

http://pmj.bmj.com/

Carotid-vertebral insufficiency 289

.+i:. 'I : Y'1'I

.......

FIG. 5. There is a complete occlusion of the internalcarotid artery and marked stenotic disease of the ex-ternal. Reconstruction of the latter might be worthwhile if flow cannot be re-established in the internalcarotid artery.

A further, more recently recognized, hazard ofoperating on complete internal carotid occlusionsassociated with a recent stroke is the risk of haemor-rhage into the cerebral infarct, with serious or fatalresults (Bruetman et a!., 1963; Wylie, Hemn &Adams, 1964) The extent of this risk cannotcertainly be expressed, and depends greatly on theneurological state of the patient at the time of opera-tion, and also on the interval of time elapsing be-tween the stroke and the surgery. The risk seems tobe greatest in patients operated on very soon after amajor stroke, and in whom the neurological state isin rapid evolution, either improving or worsening.It is now widely accepted that if operation is to beattempted in such patients it should be delayed forat least a month by this time, of course, the chanceof restoring flow will have been much reduced.

The acutely kinked internal carotid artery as acause of cerebral ischaemia. Acutely angulated loopsof a redundant tortuous internal carotid artery maybe termed kinks (Figs. 6 and 7), and such kinks may

__~~~~~~~~~~M....._~~~~~~~~~~~~~~~~~~~~~~~~~~~. ......l..........

FIG. 6. An acutely angulated or 'kinked' internal carotidartery.

produce functional stenoses (Najafi et al., 1964).Occasionally atheroma may form in a kink leadingto structural stenosis, or even to liberation of micro-emboli. However, it must be stressed that all otherpossible causes of cerebral ischaemia should beexcluded before considering operating on a kink.When a kink does appear to be associated withsymptoms, these are usually ofthe transient ischaemictype, and they may be produced by certain neckmovements. It is only when the symptoms are of thetransient ischaemic type that operation is worthcarrying out, and the experience is that the ischaemicepisodes are stopped.

Embolic occlusion of the internal carotid arteryThe occlusion by an embolus, usually of cardiac

origin, of the internal carotid artery is an uncommoncause of a stroke. As no time elapses to permit thedevelopment of a collateral circulation the stroke isliable to be profound. The chances of improving thesituation by embolectomy are obviously small, butif this is done at all it must be done quickly, and therisk of producing haemorrhage into an infarct, ifflow is re-established, must be accepted. The writer,



j.bmj.com

/P


j.47.547.282 on 1 May 1971. D

ownloaded from

http://pmj.bmj.com/

J. A. Gillespie

FIG. 7. The operative appearance of a 'kinked' internalcarotid artery in a patient who suffered from multipletransient cerebral ischaemic attacks. These ceased afterreconstruction of the vessel.

for example, has operated on five patients under theage of 35 years with embolic carotid occlusion andprofound stroke of less than 8 hr duration. Flowcould be restored only in three of the five, and inonly one of these three was there a dramatic completerecovery within a couple of hours of operation.

It would therefore appear that carotid embolec-tomy for stroke is not likely to be a very fruitfulfield for surgery.

Final selection of patients with carotid arterylesions for surgery. As has been discussed, arterialreconstruction may have either a curative role instopping transient cerebral ischaemic attacks andimproving the neurological state of patients withstroke in evolution, or have a prophylactic role inpreventing carotid stenoses progressing to occlusions,and improving total cerebral blood flow in extremestenoses and occlusions to reduce the effects of othersubsequently developing occlusive lesions, eitherintra- or extra-cranial. It is therefore possible tojustify operating on almost every patient with ananatomically correctable lesion. Results of surgery,however, suggest that certain groups of patients aremost likely to benefit, and that some lesions arerarely worth reconstruction.

Surgery probably has its most curative role in thetreatment of multiple transient cerebral ischaemicattacks associated with a stenotic internal carotidartery lesion. Whatever their mode of productionthe attacks usually cease after operation, and itwould seem that the benefit of surgery far outweighsthe risks. Much less consistently, restoration ofbloodflow in a patient with a stroke in evolution may beassociated with marked improvement in the neuro-logical picture, and it is in this group of patientsthat reconstruction is most controversial. A patientwith a completed stroke, however, cannot be curedor improved neurologically by carotid reconstruc-tion and should probably not be subjected to opera-tion if the stroke has left a severe neurological de-ficit. Similarly, in complete carotid occlusion opera-tion is seldom worthwhile as restoration of flow isnot possible in a high proportion of patients.The value of the other or prophylactic role of

surgery in restoring normal blood flow in tightlystenosed or occluded carotid arteries is morespeculative. However, as atheroma tends to affectmore than one of the extra-cranial arteries theremust be a potential benefit in having as manyprimary arterial pathways open to maintain colla-teral circulation as possible, and this is particularlyso if intra-cranial occlusions or congenital anomaliesimpair the efficiency of the circle of Willis (Kame-yama & Okinaka, 1963). Patients who have re-covered well neurologically, but have one or moretightly stenosed vessels, can reasonably be submittedto surgery. The risk of major cerebral infarction iftheir carotid stenosis, particularly if bilateral, pro-gresses to complete occlusion, far outweighs anyhazard of operation. Similarly, patients who haverecovered from an infarct and have one occludedinternal carotid artery with stenosis of the other arein real danger of a future major stroke. In them it isperhaps worth trying to restore flow in the occludedvessel first, to increase collateral brain blood-flow,and, if this is not possible, to ensure optimumpatency in that external carotid artery. The stenoticinternal carotid vessel should then be dealt with, ashunt usually being essential to maintain cerebralblood flow during the reconstruction. There wouldseem to be little doubt about the future value of asuccessful reconstruction in such a patient (Fig. 8aand 8b).

Vertebral artery lesionsThe commonest, and certainly the most accessible,

site of occlusive disease in the vertebral artery is justat its origin from the subclavian artery. The lesionmay be a stenosis (Fig. 9) or a complete occlusion,and in the latter case propagated thrombus mayextend far up the vessel. Vertebral artery lesionssituated elsewhere in the vessel are rarely amenable

290copyright.


http://pmj.bm

j.com/

Postgrad M


ay 1971. Dow

nloaded from

http://pmj.bmj.com/


FIG. 8. This 36-year-old patient was recovering from a left hemiplegia. The completely occluded right internal carotidartery (Fig. 8a) was explored first, but blood flow could not be re-established. As the left internal carotid artery showed asignificant stenosis (Fig. 8b) it was deemed essential to reconstruct this vessel as a prophylactic procedure a monthlater.

to surgical access and reconstruction so will not beconsidered further.An important feature of the vertebro-basilar

system is that the basilar artery may be adequatelyperfused by either one of the vertebral arteries alone,if patent, so that vertebral artery lesions tend onlyto produce symptoms when they are bilateral. Theexceptions to this are where one vertebral artery isdominant, the other being very small, or where thevertebral arteries do not both join the basilar artery.It should also be stressed that when significantvertebral artery lesions are present there are lesionsin the other extra-cranial arteries in a high propor-tion of cases (Crawford et al., 1969).The decision to operate on vertebral artery lesions

will be taken when there are symptoms suggestive ofpredominantly vertebro-basilar insufficiency andmarked disease of both vertebral artery origins. It isusually necessary only to restore normal flow in onevertebral artery. Complete occlusions are rarely

suitable for reconstruction. Frequently, operationon a vertebral artery will be carried out at the sametime as a carotid reconstruction.

The technique of operation for internal carotid arterylesionsCarotid stenosisIn the early days of reconstruction of carotid

stenoses much thought was given to methods ofreducing the risk of a cerebral infarct when flow wascompletely stopped during the time the common,internal and external carotid arteries were occludedby the arterial clamps. Techniques used to minimizethis ischaemic risk included operating under hypo-thermia, complicated external shunts, internalshunts, operating under local anaesthesia, or asystem of temporarily wakening the patient for atrial period of arterial occlusion (Coleman &Gillespie, 1963) so as to permit close neurologicalobservation. Further experience, however, has shown



j.bmj.com

/P


j.47.547.282 on 1 May 1971. D

ownloaded from

http://pmj.bmj.com/

292 J. A. Gillespie

.......... S .!¢.

¢ | |~~~~~~~~~~~~~~~~~~.. .L:..:. ..i':S.. .. AM <,>>

*"]*!,~~~~~~~~~~~~~~~~~~~~~~~~~~....... .._we #e8

FiC;. 9. A smooth stenosis of the left vertebral arterynear its origin.

that these techniques, with the exception of the useof the internal shunt in certain circumstances, areunnecessary. It is now the almost universal practiceto conduct the reconstruction under general anaes-thesia, care being taken to keep the patient's bloodpressure at or slightly above the preoperative level,to use oxygen rich anaesthetic mixtures, and tomaintain slight hypercarbia (Young et al., 1969).Where the arteriograms show a tight bilateral

carotid stenosis, or a complete internal carotidocclusion on the contra-lateral side to a stenosis tobe reconstructed, the risk of serious cerebralischaemia during operation is greatly increased, andhere an internal polythene shunt should be usedroutinely. Preoperative carotid compression tests,and ophthalmodynamometry with carotid compres-sion, may give some indication of the likely result ofoperative carotid occlusion, but the absence of ill-effects on such testing does not certainly rule outthe risk of cerebral infarction during operation.The technique of carotid reconstruction is illus-

trated in Fig. lOa-d. In this instance the arteriotomy,after endarterectomy, has been closed with an onlay

cts

FIG. 10 (a-d). The technique of carotid bifurcationendarterectomy illustrating the use of the temporarypolythene shunt, and patch graft closure of the arterio-tomy. Actual removal of the atheromatous material iseasily accomplished if care is taken to enter the correctseparation plane.Reproduced from Extra-Cranial Cerebro- Vascular

Disease and its Management, by courtesy of Butter-worths, London.

'.. .}... .-_ _A

.. ..::os....:

.:;.:}..::':.:::'.:q:.:.:j: .: : .i::....,,.i:i}:i::e....!:;.::': ii.........:....,.............!.i'''''a' .. ..} ... : : .... w.>:,f; .,,~~~~~~~~~~~~~~~~~~~~~~~~~~~~.........

-.;. i....,....i.:..;;.:

je j;~~~~~~~~~~~~~~~~~~~~~~~~~~~.9.;.-'.:.H..f'..l.... o°_x.'..S...t..}.

FIG. lOb

patch graft. This may either be of vein or lightweighDacron material, and it serves to widen the infloNto the internal carotid artery (Fig. 11). There imuch divergence of surgical opinion as to the valuof the patch graft in this situation and it is by no



j.bmj.com

/P


j.47.547.282 on 1 May 1971. D

ownloaded from

http://pmj.bmj.com/


~~~~.,9.9 9~~~~~~~~~~~~~~~~~

FIG IlOC

FIG. IOd

means always necessary. The desirability ofremovingall the atheromatous material sufficiently fardistally in the internal carotid artery to reach ahealthy and well-adherent intima must be stressed.Any distal intimal shelf which has to be left must becarefully tacked down to avoid dissection of bloodinto the wall of the artery when flow is restored. Theexternal carotid artery origin must also be endart-erectomized in the same way as this vessel may bean important collateral channel for cerebral bloodflow.

FIG. 11. Operative photograph of a vein patch graftillustrating the marked increase resulting in the size ofthe vessel.

In common with many other surgeons the writerfinds no use for heparin during or after carotidreconstruction: it will not redeem the results oftechnical imperfection, while a proper reconstruc-tion needs no heparin to ensure continuing patency.

Carotid occlusionWhen the internal carotid artery is completely

occluded there is little risk of cerebral ischaemiaoccurring during operation except in extensive multi-vessel disease where blood flow via the externalcarotid collateral pathway is vital for cerebraloxygenation. The likelihood that flow up the internalcarotid cannot be restored in complete occlusionshas already been discussed, and in this instanceevery effort must be made to ensure that externalcarotid artery flow will be maximal. This may some-times involve using part of the internal carotidartery in a plastic repair of the origin of the external(Fig. 12a-d) (Jackson, 1967).

The kinked internal carotid arteryThis relatively common arteriographic finding is

probably seldom the cause of symptoms, but, whenit appears to be, the elongated internal carotid arterycan be dealt with as illustrated in Fig. 13a and b.



j.bmj.com

/P


j.47.547.282 on 1 May 1971. D

ownloaded from

http://pmj.bmj.com/

294 J. A. Gillespie

.. S FR ,,,

*~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.. .:.e:_

... .. ..

.-.'.."',..w...^.'.'.''w |~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ .....~~~~~~~~~~~~~~~~~~~... j ,., ..

FIG. 12 (a-d). If flow in a totally occluded internalcarotid artery cannot be restored its origin may be usedafter endarterectomy to reconstruct a stenotic externalcarotid artery, thus increasing this vessel's collateralpotential.Reproduced from Extra-Cranial Cerebro- Vascular


"a'

FIG. 12b.

This is much more satisfactory haemodynamicallythan excising a portion and reconstituting this rela-tively small calibre vessel by end-to-end suture.

Technical hazards of operation on internal carotidartery lesionsThe main risk of carotid reconstruction is a

worsening of the patient's neurological state, eitheras a result of the liberation ofemboli during handlingof the vessels, or by the cutting off of a vital part ofthe cerebral circulation during the time the arterialclamps are applied. Rarely, the hypoglossal or vagus

',..,X,l9'X:i&;,_ ~~~~~~~~~~~..., .. ...,

..^ .i: .i,j}, ...} }... ..... s.;...... ,, .e 8} .j:.. .. e..S . .

j. .. ..4...,''...''. i; 'i

' j:: ;. ^.;.F:................. ......:::

* : :*: :: :: . .: : ::::.:0:=}:;.:::., ::!::;:.5::.:...*,..':.:-'.....i.;:

*..-i-w..... .. ............ O-e}Xi

*.::.:::..!:,.. .:::},:.:'.:w .. .,i.::;: ..... .:. i:. . ::

*: .:........ ... :!.:::::.....

FIG. 12c.

......... :;...

1o^ ;;!lsr i~: ;;

}}-"::.:..::..:::.::....... -x ... :.:::'..........}: 'g ; | ... i q i. . ~~~~~~~~~~~~~. ... . . . . . . .i }~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.. .{w~;.-X:. :.... :' .. . ;:t s? >,., .....................~~~~~~~~~~~... ... _,, . . .. . , w.i- p4 ;-_iS;E <* :it: B .e ...:S-:.>.a}t<.:.:as~~~~~~~~~~~~~~~~~~~~s

FIGr__.12d t!--5: :! }}< e=_ **fivb . <. ;' }}^z

nerve may be injured, and the cervical branch of thefacial nerve may be divided or temporarily damagedby a retractor when the skin incision has to becarried upwards close to the angle of the mandible,leading to some paresis of the corner of mouth.

The technique of operation for orificial vertebralartery stenosis

Anaesthesia is similar to that for carotid recon-struction. The vertebral artery origin is approachedby a supra-clavicular incision. The clavicular headof the sternomastoid is divided, and the jugularvein and the tissues medial to the scalenus anteriormuscle are separated to reach the arching subclavianartery, from which the vertebral arises superiorly.The arteriotomy is made through the anterior wallof the lower part of the vertebral artery and extends



j.bmj.com

/P


j.47.547.282 on 1 May 1971. D

ownloaded from

http://pmj.bmj.com/


.....}s

..... '-...- ..< < > . '.'

0~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.... .......gi.. -s? SE ..

....4i. t#*H _ e -...>M>...; ^: ,>A~~~~~~~~~~. ..fnS.......:

FIG. 13 (a and b). Reconstruction ofan acutely 'kinked'internal carotid artery.Reproduced from Extra-Cranial Cerebro- Vascular


~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~....:..."':__..i...>~~~~~~~~~~~~ ~ ~~~~~~~.>. .......

; ..^. 5.:'.'_g _ w . .8. ;..~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~....

FIG .:.'::::

into the subclavian artery. After endarterectomy thevessel may be closed directly, if it is large enough,otherwise a vein or Dacron patch graft is inserted.The technical hazards of vertebral artery recon-

struction include lymphatic fistulae, Homer'ssyndrome from sympathetic damage, pneumothorax,and the turning of stenotic into occlusive disease asa result of postoperative thrombosis. All thesecomplications are rare, and are largely avoidable withcareful technique.

ConclusionFrom both the curative and prophylactic aspect

a good case can be made out for reconstructivesurgery in atherosclerotic disease of the internalcarotid and vertebral arteries. The risks of arterio-graphy and operation are acceptably low, and thelikelihood of reconstructions remaining patentseems high.

ReferencesACHESON, J. & HUTCHINSON, E.C. (1964) Observations on

the natural history of transient cerebral ischaemia. Lancet,ii, 871.

BLAISDELL, F.W., LIM, R. & HALL, A.D. (1967) Technicalresult of carotid endarterectomy: Arteriographic assess-ment. American Journal of Surgery, 114, 239.

BLAND, J.E., CHAPMAN, R.D. & WYLIE, E.J. (1970) Neuro-logical Complications of carotid artery. Annals of Surgery,171, 459.

BRADSHAW, P. & CASEY, E. (1967) Outcome of medicallytreated stroke associated with stenosis or occlusion of theinternal carotid artery. British Medical Journal, 1, 201.

BRICE, J.G., DOWSETT, D.J. & LowE, R.D. (1964) Haemo-dynamic effects of carotid artery stenosis. British MedicalJournal, 2, 1363.

BRISMAN, R., GROSSMAN, B.L. & CORRELL, J.W. (1970)Accuracy of transcutaneous Dopper ultrasonics inevaluating extra-cranial vascular disease. Journal ofNeurosurgery, 32, 529.

BRUETMAN, M.E., FIELDS, W.S., CRAWFORD, E.S. & DEBAKEY, M.E. (1963) Cerebral hemorrhage in carotidartery surgery. Archives of Neurology, 9, 458.

COLEMAN, D.J. & GILLESPIE, J.A. (1963) Management ofcarotid endarterectomy with special reference to anaes-thesia. British Journal of Surgery, 50, 856.

CONTORNI, L. (1960) The vertebro-vertebral collateral cir-culation in obliteration of the subclavian artery at itsorigin. Minerva Chirurgica, 15, 268.

CRAWFORD, E.S., DE BAKEY, M.E. & WEIBEL, J. (1969)Extra-Cranial Cerebro- Vascular Disease and its Manage-ment (Ed. by J. A. Gillespie), p. 145. Butterworths,London.

CROMPTON, M.R. (1969) Extra-Cranial Cerebro-VascularDisease and its Management (Ed. by J. A. Gillespie), p. 1.Butterworths, London.

DENNY-BROWN, D. (1960) Recurrent cerebrovascularepisodes. Archives of Neurology, 2, 194.

DIETHRICH, E.B., LIDDICOAT, J.E., MCCUTCHEN, J.J. &DE BAKEY, M.E. (1968) Surgical significance of theexternal carotid artery in the treatment of cerebrovascularinsufficiency. Journal of Cardiovascular Surgery, 9, 213.

EASTCOTT, H.H.G., PICKERING, G.W. & ROB, C.G. (1954)Reconstruction of internal carotid artery in a patient withintermittent attacks of hemiplegia. Lancet, ii, 994.

FARIS, A.A. & POSER, C.M. (1964) Experimental productionof focal neurologic deficit by systemic hyponatremia.Neurology, 14, 206.

GILLESPIE, J.A. (1967) Modern Trends in Neurology 4 (Ed.by D. Williams), Butterworths, London.

GUNNING, A.J., PICKERING, G.W., ROBB-SMITH, A.H.T. &RUSSELL, R.W.R. (1964) Mural thrombosis of the internalcarotid artery and subsequent embolism. QuarterlyJournal of Medicine, 33, 155.

HUTCHINSON, E.C. & YATES, P.O. (1957) Carotico-vertebralstenosis. Lancet, 1, 2.

JACKSON, B.B. (1967) The external carotid as a brain colla-teral. American Journal of Surgery, 113, 375.



j.bmj.com

/P


j.47.547.282 on 1 May 1971. D

ownloaded from

http://pmj.bmj.com/

296 J. A. Gillespie

KAMEYAMA, M. & OKINAKA, S. (1963) Collateral circulationof the brain with special reference to atherosclerosis ofthe major cervical and cerebral arteries. Neurology, 13,279.

KENYON, J.R. & THOMPSON, A.E. (1965) Surgery of carotidartery stenosis. British Medical Journal, 1, 1460.

LASCELLES, R.G. & BURROWS, E.H. (1965) Occlusion of themiddle cerebral artery. Brain, 88, 85.

LITTLE, J.M., MAY, J., VANDERFIELD, G.K. & LAMOND, S.(1969) Traumatic thrombosis of the internal carotidartery. Lancet, ii, 926.

MARSHALL, J. (1964) The natural history of transient,ischaemic cerebro-vascular attacks. Quarterly Journal ofMedicine, 33, 309.

MARSHALL, J. (1969) Extra-Cranial Cerebro- Vascular Diseaseand its Management (Ed. by J. A. Gillespie), p. 112.Butterworths, London.

MARTIN, J.M., WHISNANT, J.P. & SAYRE, G.P. (1960)Occlusive vascular disease in the extracranial cerebralcirculation. Archives of Neurology, 3, 530.

MAWDSLEY, C., SAMUEL, E., SUMERLING, M.D. & YOUNG,G.B. (1968) Thermography in occlusive cerebrovasculardiseases. British Medical Journal, 3, 521.

MILLIKAN, C.H. (1965) The pathogenesis of transient focalcerebral ischemia. Circulation, 32, 438.

NAJAFI, H., JAVID, H., DYE, W.S., HUNTER, J.A. & JULIAN,O.C. (1964) Kinked internal carotid artery: Clinical evalua-tion and surgical correction. Archives of Surgery, 89, 134.

O'BRIEN, M.D., VEALL, N., LUCK, R.J. & IRVINE, W.T.(1967) Cerebral-cortex perfusion-rates in extracranialcerebrovascular disease and the effects of operation.Lancet, ii, 392.

PARRY, E.W. (1969) Lecture to Royal College of Surgeonsof Edinburgh. Cited by G. E. Mavor (1969). Practitioner,203, 468.

PERDUE, G.D., SMITH, R.B., RHODES, L. & LONG, W.D.(1970) Carotid revascularisation in the treatment ofcerebral ischaemia. Archives of Surgery, 100, 562.

RAINER, W.G., FEILER, E.M., BLOOMQVIST, C.D. & MCCRORY,C.B. (1966) Surgical approach to carotid arterial in-sufficiency: Risks and results. Annals of Thoracic Surgery,2, 640.

SAMUEL, K.C. (1956) Atherosclerosis and occlusion of theinternal carotid artery. Journal of Pathology and Bacterio-logy, 71, 391.

SCHWARTZ, C.J. & MITCHELL, J.R.A. (1961) Atheroma ofthe carotid and vertebral arterial systems. British MedicalJournal, 2, 1057.

SHUCKSMITH, H.S. (1963) Cerebral and peripheral embolicaused by cervical ribs. British Medical Journal, 2, 835.

STEIN, B.M., MCCORMICK, W.F., RODRIGUEZ, J.N. &TAVERAS, J.M. (1962) Post-mortem angiography of cerebralvascular system. Archives of Neurology, 7, 545.

SVARE, G.T., TAVERAS, J.M. & STEIN, B.M. (1964) Post-mortem angiography of the cerebral vascular system.Neurology, 14, 1149.

THOMPSON, J.E., AUSTIN, D.J. & PATMAN, R.D. (1967)Endarterectomy of the totally occluded carotid artery forstroke. Results in 100 operations. Archives of Surgery, 95,791.

TODD, R.B. (1844) Account of a case of a dissecting aneurysmof the aorta innominata and right carotid arteries givingrise to suppression of urine and white softening of thebrain. Medico-Chirurgical Transactions (2nd Series), 9, 301.

WIENER, L.M., BERRY, R.G. & KUNDIN, J. (1964) Intra-cranial circulation in carotid occlusion. Archives ofNeurology, 11, 554.

WILLIAMS, D. (1969) Extra-Cranial Cerebro- Vascular Diseaseand its Management (Ed. by J. A. Gillespie), p. 25. Butter-worths, London.

WILLIAMS, D. & WILSON, T.G. (1962) The diagnosis of themajor and minor syndromes of basilar insufficiency. Brain,85, 741.

WOOD, E.H. (1964) Thermography in the diagnosis ofcerebro-vascular disease: Preliminary report. Radiology,83, 540.

WOOD, E.H. (1965) Thermography in the diagnosis ofcerebro-vascular disease. Radiology, 85, 270.

WOOD, E.H. & HILAL, S.K. (1969) Extra-Cranial Cerebro-Vascular Disease and its Management (Ed. by J. A.Gillespie), p. 45. Butterworths, London.

WOOD, E.H. & HILL, R. (1966) Thermography in the diag-nosis ofcerebrovascular occlusive disease. Acta Radiologica,5, 961.

WYLIE, E.J., HEIN, M.F. & ADAMS, J.E. (1964) Intracranialhemorrhage following surgical revascularization fortreatment of acute strokes. Journal of Neurosurgery, 21,212.

YOUNG, J.R., HUMHPRIES, A.W., BEVEN, E.G. & DE WOLFE,V.G. (1969) Carotid endarterectomy without a shunt:Experiences using hyperbaric general anesthesia. Archivesof Surgery, 99, 293.



j.bmj.com

/P


j.47.547.282 on 1 May 1971. D

ownloaded from

http://pmj.bmj.com/

surgical aspects of carotid-vertebral insufficiency · vertebral artery lesions, it is fortunate,...

Documents