POSTGRAD. MED. J. (I962), 38, 396

ISCHAEMIC STROKESGEOFFREY C. KNIGHT, F.R.C.S.

Surgeon in Charge, Regional Neurosurgical Unit. Brook Hospital, S.E. i 8; Neurosurgeon, British PostgraduateMedical School; Hon. Senior Surgeon, West End Hospital for Neurology and Neurosurgery

SIMON BEHRMAN, M.R.C.P.(Lond.), B.Sc.(Hon.)(Lond.)Consultant Neurologist, Regional Neurosurgical Unit, Brook Hospital, S.E. i8; Consultant Physician,

Moorfields Eye Hospital

BY 'strokes' we understand the sudden disordersof function of the central nervous system, due toclosure or rupture of a blood vessel contributingto the cerebral circulation. We shall confine our-selves to a brief consideration of some of theeffects of occlusive disease of these vessels.The discovery that there was a close relationship

between strokes and hiemorrhage in the cerebralhemisphere, on the side contralateral to the hemi-plegia, is comparatively recent, and dates fromthe I7th century. This discovery greatly influencedmedical thought throughout the i8th century,since cerebral himorrhage became synonymouswith strokes and apoplexy. The alternativeischemic causation of strokes became graduallyrecognized only in the Igth century and RobertGraves was certainly not aware of this patho-genesis of apoplexy when writing his 'ClinicalMedicine' in I843.

'. . . To quote one ofmany examples I myself have seen:a man named Thomas Lynch was admitted into SirPatrick Dun's Hospital, afflicted with symptoms indica-tive of cerebral disease. During his residence in thehospital he suffered four or five attacks of hemiplegia,in every respect complete, and depriving him of the useof his speech. Some of these attacks lasted only fifteenminutes, while the longest continued about an hourand a half; they ceased as suddenly as they com-menced, and left no traces of hemiplegia behind them.The circumstances of this case evidently prevent usfrom assigning each attack to a separate effusion ofblood: for were it owing to this cause, it would beimpossible to account at once for the sudden appearanceand sudden cessation of so extensive and complete aparalysis. Let it not be imagined, however, that I wishto throw doubts upon the beneficial influence of morbidanatomy on the diagnosis and treatment of diseases ofthe brain-my object in making these observations isnot to retard, but to advance, the progress of morbidanatomy by pointing out errors of some generallyreceived opinions' (Graves, I884).

Robert Graves further contended that 'patientscould be rendered for the time more or less com-A paper read to a Conference of Physicians 'of the

South East Metropolitan Region at the Brook Hospital,March 17, I 962.

pletely hemiplegic, and yet recover in the courseof a few minutes or hours the use of the affectedside so suddenly and so perfectly, as to precludethe idea of local lesion, such as could be detectedby the scalpel of the anatomist'. This conceptionof sudden recurrent reversible abolition of cerebralfunction without any demonstrable changes inthe nerve tissue has received a good deal ofattention in the medical literature since then.William Russell attributed the 'intermittent clos-ing of cerebral arteries' to their 'abnormal irrita-bility' (Russell, 1909). A case described by Oslerseemed to reinforce the cerebral 'vasospasm'theory. This was an individual presenting similarrecurrent paralytic attacks, and who in additionwas subject to vessel spasm in the extremities,due to Raynaud's disease (Osler, 9i9I). It was asurgeon, Howard C. Naffziger (Fleming andNaffziger, I927), who was first to criticize thisexplanation. He had noted 'great thickening andhardening of the vessels' in patients with inter-mittent strokes and he suggested that the lattercould 'best be explained by a fall of the generalblood pressure, below the patient's optimum,without the necessity of presuming a questionablevessel spasm. Many causes may be operative inbringing about the lowering of blood pressure.Myocardial weakness may precede faults ofcerebral circulation as well as elsewhere'. Thenext important milestone in our better under-standing of strokes was the publication of thepaper by Hicks and Warren in 1951. They hadstudied ioo brains with apoplectic infarctions, thelesions of which were sufficiently large to permita careful study. In 6o brains no 'mechanicalocclusion' of the cerebral vessels could be demon-strated, i.e. all the cerebral vessels were patent.In a somewhat similar but smaller series Yatesand Hutchinson (I96I) found 'no significantstenosis or occlusion of intracranial arteries' in46% of their cases with cerebral infarction. Theexplanation for this observation was soon pro-vided by the results of carotid angiography which,

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KNIGHT and BEHRMAN: Ischamic Strokes

following the introduction of the percutaneoustechnique, was being performed with increasingfrequency. Many unsuspected cases of carotidocclusion were thus being revealed, and theextracranial arteries contributing to the formationof the circle of Willis were subjected to greaterscrutiny. The outcome of these studies, whichare still in progress, is that atheromatous stenosisof carotid and vertebral arteries is relativelycommon in individuals above the age of 50. Ina consecutive study of 1,I75 cases, severe athero-sclerosis of the circle of Willis and of the arteriescontributing to it, was found in close on 50% ofindividuals above the age of 50 (Baker andlannone, I96I). A somewhat similar study ofI00 unselected autopsies of bodies over the ageof 50 showed occlusion of at least one arterysupplying the brain in II% (Martin, Whisnantand Sayre, I960). So great is the functionalefficiency of the circle of Willis that not onlymay individuals with even bilateral carotid occlu-sion remain symptom-free, but they may show anormal basal cerebral blood flow, which can beaugmented to a normal extent by inhalation of5% carbon dioxide and 9500 oxygen (Fazekas,Yaan, Gallow, Paul and Alman, I962).As we have seen, in the study of strokes the

pathologist's purview has gradually extended soas to include not only the cranial and extracranialarteries but also the aorta within the range of hisexamination (Yates and Hutchinson, I96I). Thesestudies reveal that in a good many individualsover the age of 50 the blood-carrying capacity ofthe cerebral vessels, and of the main arteries con-veying blood to the cerebrum, can be greatlyreduced without the causation of 'strokes'.Thus it can be concluded that only a small

proportion of the individuals with severe athero-matous stenosis of these vessels develop strokes.The gravest consequences of atherosclerosis ofthe aorto-cranial vasculature is, therefore, not inthe diminution of blood-carrying capacity but inthe thrombotic lesions which they cause. Theliability to thrombotic lesion-in presence ofatherosclerosis-may well be subject to individualvariations. This conclusion is perhaps supportedby a study of atherosclerosis in a variety ofanimals. Despite the high incidence of this con-dition in animals, 'there was a surprising paucityof athero-thrombosis in comparison with man'(Finlayson, Symonds and T-W-Fiennes, I962).The pathology of the occlusive process affecting

the carotid arteries was reviewed by one of theauthors in this journal (Behrman, I954). Thevertebral arteries, while subject to similar morbidprocesses, may in the elderly become occludedwhen the already atheromatous artery is greatlydisplaced by osteoarthritic bony protuberances of

the cervical spine. Very exceptionally, any of thepre-Willisian arteries can become the seat ofgiant-cell arteritis.

Factors Giving Rise to Intermittent StrokesAs already mentioned, Naffziger had suggested

a 'fall of blood pressure below the patient'soptimum level' might account for these transientdisturbances of cerebral circulation. An asso-ciated pathological narrowing of the arteries ofthe circle of Willis or of the pre- or post-Willisianarterial channels would be an essential pre-requisite. The following case illustrates theoccurrence of recurrent hemiparesis consequentupon a fall of blood pressure during high pyrexia.

Case i.-A student of 22 who was operated uponby one of us (G.C.K.) in I954 on account of sub-arachnoid heemorrhage. Arteriography revealed ananeurysm of the anterior communicating artery withthe right anterior cerebral in spasm. As an emergencymeasure the left common carotid was ligated. Laterthat night he developed a fall in blood pressure withtransient aphasia and right hemiparesis which recoveredcompletely. Subsequently he remained well but wastreated for urinary obstruction due to a valve in theprostatic urethra. He has from time to time sufferedfrom recurrent attacks of catheter fever and in each ofthese he has an episode of aphasia and hemiparesiswhich recovers when the fever abates. Presumably theefficiency of the circle of Willis is embarrassed by theaneurysm on the anterior communicating artery, andthe obstruction of the left common carotid artery.

Grimson, Orgain, Rowe and Sieber (1952) havedescribed a patient who was under treatment withhypotensive drugs, and they noted that hemi-plegia developed whenever the blood pressure fellbelow a certain level. This would suggest thatco-existing arterial stenosis reduced the bloodflow to one hemisphere. Cases have been describedin which correction of either anemia or of in-creased blood viscosity due to polycytlimiaresulted in the cessation of intermittent 'strokes'(Millikan, Siekert and Whisnant, Ig60a and b).These various cases of intermittent 'strokes',

in which the nature of the immediate precipitatingfactors can be clearly established, are of con-siderable importance in furthering our knowledgeof the possible underlying pathological mechan-isms. It must, however, be admitted that in thevast majority of cases deliberate provocation ofthe 'strokes' by simple lowering of the systemicblood pressure is not possible, and no fall inblood pressure can as a rule be observed at thecommencment of these attacks. Nevertheless,the association of 'strokes' with myocardial in-farction (Cole and Sugarman, 1952), excessivedehydration and occult gastro-intestinal bleedingare sufficiently common to call for their con-.sideration in the clinical investigation of 'strokes'.

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Extra-cranial Arterial ReconstructiveSurgery

-If in the investigation of recurrent transientaphasia or hemiparesis an obstructed carotidartery is found, it is easy to consider that this isthe sole cause of the patient's symptoms and theobjective to which treatment should be directeda view which has given a false impetus to arterialsurgery in recurrent transient cerebral palsies, forin fact, cerebral ischkmia is not produced bystenosis of a single vessel alone. Cases are knownin which both carotids are thrombosed yet thecerebral circulation is fully maintained by thevertebral and basilar systems. Vertebral throm-bosis occurring in association with cervicalspondylosis may be quite symptomless despitethe distortion of vessels which occurs duringmovements of the neck, which may also twist thecarotid branches at the bifurcation. It is notuntil- both vertebral vessels are seriously involvedthat symptoms of basilar ischemia are produced.For circulatory insufficiency to arise in associationwith a segmental stenosis in one artery there mustbe other factors at work, and perhaps more thanone factor which will lead to impairment of themultiple pathways by which the blood supply tothe brain is normally assured. Provided that thecircle of Willis is patent and provided that thestate of the aortic branches and the cardiac func-tion are satisfactory, blockage of the carotid willnot produce symptoms, indeed, when cerebralarteriography is performed after the carotid onthe opposite side is compressed, the contrastmedium flows readily to fill the contralateralhemisphere showing how easily nutrition can bemaintained after carotid obstruction in normalcircumstances.There is a clear indication for surgery in the

unilateral segmental lesion in a young subjectwithout generalized arterial or cardiac disease.Even in these cases there must undoubtedly be asecond factor, in that the cross-circulation throughthe circle must be ineffectual, but the indicationsfor operation are clear-cut. There must be apartial obstruction of a short segment whichusually has an audible bruit, often very high-pitched, over the affected area and no evidence ofgeneralized or progressive disease elsewhere. Insuch cases thrombectomy is the operation ofchoice. The artery is opened, the obstructionremoved and the artery resutured. This is asmall procedure which can be rapidly completedand the results are generally good. Excision andresuture of a segment is less likely to be suc-cessful. For either method to succeed operationmust be performed early, before long-standingischemia or complete obstruction has producedan irreversible change. Surgery, and indeed

398 EDICAL JOURNAL July I962

arterial investigations, should never be employedwhen the iscliemic episode arises late in an estab-lished syndrome which has already given evidenceof a progressive course, and probably investiga-tion is best avoided in the absence of an audiblebruit. The following two cases illustrate thecomplexities of this problem.Case 2.-A man of 68, a sufferer from chronic

bronchitis since the 1914 war, who developed coronarythrombosis in November ii96I. On examination he wasbreathless at rest, his lips slightly cyanotic, his apex beati inch to the left, blood pressure I60/90 mm. Hg.Pulsation in the left brachial and radial arteries muchreduced. The fundi showed marked narrowing of thearteries and nipping of the veins. Since 1959 he hadhad recurrent attacks of weakness in the left arm andleg and loss of central vision in the right eye, whichpersisted for about 5 minutes on each occasion beforenormal compensatory mechanisms were brought intoplay and terminated the attacks. Angiography revealedtwo areas of constriction of the internal carotid, butdespite this the cerebral vessels were well filled; obvi-ously there could be no indication for intervention.

Case 3.-This illustrates the danger of the increasingthrombotic lesion. This was a high-powered alertbusiness tycoon who developed an attack of confusionwhilst crossing the road, as a result of which he wasknocked down by a cyclist. He was admitted to hospitalwith severe symptoms including right hemiparesis andaphasia but recovered rapidly within a week, which hewould not have done had these symptoms been dueentirely to associated head injury. He returned home,with normal speech and movement, but became severelyexhausted at the end of a tiring visit from many rela-tives and became confused and aphasic with recurrentmild paresis, thus illustrating the effect of fatigue inthese cases. His doctors decided to investigate him forcarotid artery thrombosis. Arteriography was per-formed-with disastrous results. He recovered fromthe anesthetic but with complete paralysis, was totallyaphasic and had frequent recurrent epileptic fits andsome mental impairment. As years have passed hispower of movement and speech have improved to someextent but his mental faculties and memory havedeteriorated even further and he is developing Parkin-sonian features and a Parkinsonian posture of the handfrom the steady progression of bis arterial degeneration,which probably showed its first symptoms immediatelyprior to his accident.

The published cases which have been treatedwith reconstructive surgery fall into two maingroups:

(i) Cases in which the operation has been per-formed as a prophylactic procedure, to preventfurther strokes. In the assessment of the valueof reconstructive arterial surgery in this group ofintermittent strokes we are handicapped by ourlack of knowledge of the natural history of suchcases.

(2) Cases with irreversible cerebral damage.As is to be expected, no significant change wasnoted in these cases following surgery (Rob, I960;De Bakey, Crawford and Fields, I96I).

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KNIGHT and BEHRMAN: Ischa-mic Strokes

'Strokes' Due to Spasm of Cranial ArteriesWe come now to the effects of ischlmia accom-

panying spasm of the arteries. It is well knownthat branches of the circle of Willis are liable topass into spasm when irritated by the bloodeffused in subarachnoid hamorrhage. It is prob-ably less well known that a relatively small sub-arachnoid can by this mechanism produce' anextensive cerebral infarction, sufficient to kill thepatient.

Case 4.-A recent case admitted to the British Post-graduate Medical School under the care of one of us(G.C.K.) was that of an office-cleaner who had de-veloped subarachnoid heemorrhage at 6 o'clock in themorning. On admission to the hospital at 7.30 a.m. shewas restless with increasing signs of brain stem failure,cessation of respiration occurring within three hours ofthe first hemorrhage. Arteriography performed onartificial respiration showed that there was completeobliteration of both carotids above the level of thecavernous sinus by spasm and presumably this spasmwas widespread and the cause of brain stem failure, forat post-mortem only a relatively small subarachnoidhaemorrhage was found.Case S.-A man, aged 37, was admitted elsewhere

for investigation of a splitting headache and pain behindthe right eye associated with vomiting and slowing ofthe pulse. These symptoms subsided spontaneously,but ten days later he again suffered a sudden change,with headache, vomiting, slow pulse and loss of con-sciousness; leucocytosis and a high ESR were demon-strated, and he was transferred for investigation.Examination revealed left-sided hemiparesis, astereog-nosis and hemianopia, and early papillcedema. Right-parietal biopsy revealed only soft brain into which theneedle dropped like a plummet. A malignant gliomawas suspected and nothing further was done. Thefollowing day his condition deteriorated with a pulserate down to 40. Although biopsy had not revealed atumour it was decided that urgent exploration wasindicated. It was found that the posterior portion of theright parietal and temporal lobes were grossly swollenand softened. Sufficient of the non-essential portionsof this area was removed to relieve urgent pressure,following which the dura could be easily sutured. Thepatient was considerably improved, but examination ofthe tissue removed showed only cerebral edema withsoftening. The patient has recovered and leads a usefullife with a minimal hemiparesis and occasional epilepticattacks. An arteriography performed later revealed asmall aneurysm on the posterior communicating arterywith marked vasospasm.

In face of such clinical evidence, neither thereality nor the magnitude of spasm of pre-Willisian arteries can be disputed. The con-traction of these arteries can give rise to 'strokes'albeit under special circumstances, even whenthese arteries are free from occlusive disease.Given a degree of stenosis by virtue of structuraldisease, it could be assumed that on occasions aphysiologically induced contraction of thesearteries might lead to a remitting or permanentstroke. As was already mentioned, classical re-mitting strokes, in individuals subject to them,

cannot be precipitated by lowering the systemicblood pressure. Some other agency must, there-fore, be invoked. The work of Seymour S. Kety(I96I) in recent years on the cerebral circulationled to a drastic revision of long-held conceptsthat cerebral blood flow followed passively andirrevocably the corresponding changes in bloodpressure.

Strokes Due to MigraineInfarction with permanent damage of tissue

resulting from vasospasm is also encountered incertain cases of severe hemiplegic migraine.

Case 6.-A patient of 33 had for some years sufferedfrom right and left hemicrania with teichopsia. Whilewalking down a street in a severe attack of migraine,she suddenly felt the right half of her body paralyzedand could not see the right half of the street. Therewas no loss of consciousness and no pain in the neck,yet on admission elsewhere she was investigated as asuspected case of subarachnoid hemorrhage with nega-tive results. Her right hemiparesis and hemianrsthesiaresolved in the course of some weeks, but she was leftwith persistent quadrantic hemianopia.

Recent review of a series of cases of cervicalsympathectomy performed in I954 for the treat-ment of migraine has shown that patients whoexhibited marked evidence of ischlemia such asparaesthesia, weakness or oculomotor paresis dur-ing the vasospastic stage of the migraine attack,may be completely relieved of these symptoms bycervical sympathectomy (Knight, I962). Theretherefore appears to be a strong indication for theemployment of this form of treatment as a pro-tective measure to prevent persistent sequekedeveloping from infarction in cases where ischemicphenomena are severe.

'Strokes' Due to Cerebral GliomasMany gliomas infiltrate between the nerve-

fibre tracts which at first continue to functionand conduct between the tumour cells; however,the blood supply of the white matter is so tenuousthat it cannot support indefinitely the circulatorydemands of the growth. Eventually the tumouroutgrows its blood supply with resulting infarctionand necrosis of the centre portions of the growth.Since fibres can no longer conduct by this routesymptoms suddenly appear like a vascular syn-drome in a subject who may not exhibit evidenceof arterial disease. Initial symptoms of contra-lateral weakness, confusion and headache mayimprove quite appreciably after the onset, againmimicking the vascular lesion, to be followed atan interval by a progressive course and papil-lcedema characteristic of a space-occupying lesion.Very rarely the bleeding from a glioma mayescape into the subarachnoid space, when the

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clinical picture will assume the features of a sub-arachnoid hemorrhage (Glass and Abbott, 1955).

'Progressive Strokes'Occasionally the apoplectic onset of disturbance

of neurological function is lacking, and symptomsappear gradually in the course of occlusive cerebro-vascular disease. This may occur when repeatedseparation of small emboli from the wall of ananeurysmal sac or mural thrombus leads to re-peated plugging of end-vessels producing aprogressive paralytic syndrome simulating acerebral neoplasm. Differentiation is occasion-ally possible when it can be established thatprogression occurred in step-like fashion.The following case illustrates the more con-

tinuous, tardy development of paralysis caused byocclusion of right carotid artery.

Case 7.-Man, aged 6 i.7.7.I96I: First began to complain of pain around the

right eye.I9.8.6I: Epileptic seizure.2.9.6I: 'Could not see properly with the right eye for

some minutes on awakening in the moming'.20.9.6I: Became 'strange' in his behaviour, and began

to have difficulty in using the left hand. Complainingof tingling and loss of sensation in the left hand, andaround lips and tongue. Paralysis of the left limbsincreased gradually during the following eight days.

In a recently published series of I53 carotidartery occlusions, symptoms commenced in sevenpatients with some minor neurological deficitwhich gradually increased without remission.Eventually a complete hemiplegia developed afteran interval ranging from five days to 14 months(Hardy, Linder, Thomas and Gurdjian, I962). Ifadded to this clinical picture are symptoms suchas headaches, seizures and oculomotor palsies, itwill be realized that the differential diagnosisfrom intracranial tumours may present greatdifficulties. It is exceptional for 'strokes' to giverise to clinical manifestations of raised intracranialpressure as in Case 5.

Collateral CirculationAn anastomosis between the branches of in-

ternal maxillary branch of the external carotidartery and the ophthalmic branch of the internalcarotid, is one of the better known collateralchannels connecting the internal and externalcarotid arteries. Carotid angiography has estab-lished the paramount importance of these col-lateral channels in cases of occlusion of theinternal carotid artery. The degree of develop-ment of these channels is subject to considerablevariation. A priori it must be assumed that thedevelopment of these compensatory channels

requires time, and can only become adequate ifthe occlusion of the carotid has appeared gradually.

AngiographyThe great diagnostic value of angiography of

the cranial arteries may perhaps tend to mask thehazards this procedure entails. With increasingimprovement in technique and skill of theoperators, the incidence of complications has beendiminishing steadily, but tragic results such asoccurred in Case 3, though rare, must always beborne in mind. There remains, however, a groupof cases in which the incidence of complicationsstill remains relatively high. This group com-prises cases in which one or more cranial arteriesare in spasm, especially after a subarachnoidhlimorrhage.The influence of angiography upon pre-existing

arterial spasm is well illustrated by some experi-ments described by Raynor and Ross (I960).The exposed carotid artery of cats under pentothalwas stroked by a blunt instrument some 20 timesfor a distance of i cm. By a photographic tech-nique it was possible to measure the extent andduration of the arterial spasm so produced. Whencontrast medium was injected immediately afterstroking, while the artery was in spasm, theduration of the spasm was prolonged aboutfivefold.

Summaryi. The ischwmic stroke is defined as disturbance

of neurological function resulting from cerebro-vascular occlusion.

2. A variety of ischemic strokes are considered,viz.: intermittent strokes, strokes due to spasmof cranial arteries, strokes due to migraine,strokes due to cerebral gliomas and 'progressive'strokes.

3. The limited scope of extra-cranial arterialreconstructive surgery is emphasized.

4. It is stressed that after the age of 50 theincidence is high of widespread narrowing of thearteries conveying blood to the brain.

5. This narrowing, whether associated withocclusion or not, is often symptomless. Thediminution of blood carrying capacity of thesevessels is therefore relatively unimportant.

6. The gravest consequence of this pathologicalprocess is due to consequent athero-thrombosis.

7. Given a degree of atherosclerosis, the lia-bility to athero-thrombosis may be subject toindividual variation. A recent study-of athero-sclerosis in a variety of animals revealed that'there was a surprising paucity of athero-thrombosis in comparison with man'.

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