Carotid disease in acute stroke.
Background: the Oxfordshire Community Stroke Project (OCSP) devised a simple clinical classification for acute stroke which predicted mortality, functional recovery and patterns of recurrent stroke. We aimed to determine whether this could predict the presence of carotid disease and be used to select which patients with acute stroke should be referred for carotid imaging with a view to subsequent carotid endarterectomy.
Methods: we assessed patients with acute stroke admitted to seven hospitals over a 10-month period. Patients were classified according to the OCSP system and their carotid arteries investigated using portable continuous-wave Doppler. Those with abnormal portable assessments had colour duplex Doppler imaging.
Results: of 305 patients with proven or probable cerebral infarction, severe (70-99%) ipsilateral carotid stenosis was found in 16 (16%) of the 101 with partial anterior circulation infarct (PACI), four (4%) of the 100 with total anterior circulation infarct (TACI), none of the 80 with lacunar infarct (LACI) and one (4%) of the 24 with posterior circulation infarct (POCI). Complete ipsilateral carotid occlusion was found in 25 (25%) of the TACI group, 11 (11%) of the PACI group, three (4%) of the LACI group and none of the POCI group. Severe carotid stenosis or occlusion was more common in the ipsilateral than the contralateral carotid artery for the TACI and PACI groups ([chi square] P [is less than] 0.05), but there was no difference between ipsilateral and contralateral carotid disease in the LACI and POCI groups. If the OCSP classification is used to detect patients with 70-99% carotid stenosis, then the sensitivity is 76% and specificity is 70%.
Conclusion: these findings suggest that ipsilateral carotid disease is an important cause of stroke for those with anterior circulation infarcts but not for those with LACI or POCI. Subjects with PACI should be referred for early carotid imaging to identify those with severe disease who may be suitable for elective carotid surgery.
Keywords: acute stroke, carotid disease, Doppler imaging
The Oxfordshire Community Stroke Project (OCSP) devised a classification for acute stroke based on symptoms and signs only . The classification is now widely used. It has prognostic value by predicting mortality, functional recovery and patterns of recurrent stroke . For example, patients with partial anterior circulation infarct (PACI) are at particularly high risk of early stroke recurrence. This pattern of recurrence is consistent with an active source of emboli such as carotid atherosclerosis, but the prevalence of carotid disease in the OCSP subtypes of acute stroke is uncertain. Carotid stenosis in acute stroke has important clinical implications, because carotid endarterectomy in patients with a history of ischaemic stroke and 79-99% ipsilateral carotid stenosis reduces the risk of further stroke [3, 4].
The relationship between the OCSP classification and carotid disease has been previously investigated, but one study failed to differentiate between a complete carotid occlusion (where carotid surgery is contraindicated) and a severe stenosis, and the other recruited a very small number of patients [5, 6].
The aim of this study was to investigate the relationship between the OCSP classification and carotid disease, in order to determine whether the OCSP could be used to select which patients with acute stroke should be preferentially referred for carotid imaging.
Referral of patients
We collaborated with 44 consultants in seven Manchester hospitals by asking all junior doctors to refer urgently any patient admitted with a possible acute stroke using a 24-h `air call' system. We visited the patients at the referring hospital as soon as possible after admission. Patients were assessed neurologically by a stroke research fellow. Acute stroke was defined as `sudden onset of acute neurological disturbance lasting over 24 h, and assumed to be of vascular origin' . Subjects with transient ischaemic attacks (TIAs), whose stroke onset was over 7 days previously or who had not suffered an acute stroke were excluded. Patients with intracerebral haemorrhage on computed tomography (CT) scanning or by Siriraj stroke score were also excluded . The remaining patients were categorized according to the OCSP classification .
Classification of acute ischaemic stroke
Patients with hemiparesis, homonymous hemianopia and new disorders of higher cerebral dysfunction e.g. dysphasia, were classified in the total anterior circulation infarct (TACI) group. Those with only two of the above features or with isolated cortical dysfunction (e.g. dysphasia) were classified in the PACI group. Patients with isolated motor or sensory deficits, or sensorimotor strokes or ataxic hemiparesis were classified in the lacunar infarct (LACI) group and those with brainstem or cerebellar signs in the posterior circulation infarct (POCI) group. The maximum recorded deficit was used in the classification. For example, if the initial neurological assessment recorded in the case notes included dysphasia and hemiparesis, the patient was placed in the PACI group, even if the dysphasia had resolved by the time of our assessment. We did not modify the clinical classification according to CT findings, because CT was requested by the referring doctor in only just over half the patients.
The carotid arteries were investigated bilaterally by the stroke research fellow using portable continuous-wave Doppler ultrasound after the neurological assessment. The stroke research fellow was therefore blind to the results of the Doppler ultrasound at the time of the neurological assessment. We had previously validated this equipment and demonstrated a sensitivity of 99% and specificity of 83% for diagnosing significant carotid stenosis or occlusion compared with colour duplex Doppler undertaken by an experienced vascular technologist . The low specificity was mainly due to a false-positive diagnosis of carotid occlusion when an internal carotid signal could not be detected for technical reasons (e.g. high carotid bifurcations or a tortuous vessel).
Patients with peak systolic frequencies of over 3.5 kHz (suggesting [is greater than] 50% stenosis) on the portable equipment who were fit for transfer to our vascular studies unit had colour duplex Doppler imaging (ATL Ultramark 9). Disease severity was classified as [is less than] 50% stenosis, 50-69% stenosis, 70-99% stenosis or complete occlusion. Patients who were unfit for transfer were classified according to the portable carotid Doppler assessment alone. Those with possible occlusion who were fit for surgery were also investigated by intra-arterial digital subtraction angiography in order to distinguish a very tight carotid stenosis from an occlusion. The presence of a major source of cardiac emboli (e.g. atrial fibrillation, prosthetic valve, mitral stenosis, recent myocardial infarct, left atrial or left ventricular thrombus, atrial myxoma, infective endocarditis and dilated cardiomyopathy) was noted .
[chi square] tests were used to compare the prevalence of carotid disease in the different OCSP subtypes and 95% confidence intervals (CI) were calculated for the point estimates of the prevalence in the different subtypes.
Classification of patients
During the study period, 485 patients were referred. Of these, 341 presented with focal neurological disturbance lasting between 24h and 7 days and were classified as acute stroke. Brain CT results were available in 192 (56%). Eighteen (9%) were found to have intracerebral haemorrhage, five had an intracranial tumour and one had a subdural haematoma. A further two patients were subsequently diagnosed as having hypertensive encephalopathy by the referring physician but did not undergo brain CT. Of the remaining 149 patients who did not have a CT scan, 10 (7%) had Siriraj stroke scores of [is greater than] 1 and were classified as cerebral haemorrhage--a proportion which was not significantly different from those who did undergo CT ([chi square] P [is greater than] 0.05). Hence, 305 patients were classified as cerebral infarcts. CT results were available for 170 of these 305 patients: 140 of these showed an infarct (or multiple infarcts) and 30 showed no infarct. The OCSP classification divided the 305 patients into 100 with TACIs (33%), 101 with PACIs (33%), 80 with LACIs (26%) and 24 with POCIs (8%). The median time from stroke onset to assessment was 2 days (range 0-7).
Accuracy of diagnosis of carotid occlusion by portable Doppler
A total of 70 internal carotid arteries were thought to be occluded on portable Doppler (including patients with `old stroke', TIAs and `not strokes'). Colour duplex Doppler results were available on 48 of these arteries, which confirmed occlusions in 37 (77%). For the purposes of this analysis, it was therefore decided that 77% of those who were too unwell for transfer to our vascular studies unit, and had apparently complete occlusion on portable Doppler, would be categorized as having complete occlusions and the remaining 23% as having [is less than] 50% stenosis. This is particularly relevant to the diagnosis of carotid occlusion in the TACI group (see below).
Severe (70-99%) carotid stenosis
Severe ipsilateral carotid stenosis was found in 16 (16%; 95% CI 9-23%) of the PACI group, four (4%; 0-8%) of the TACI group, none (0%; 0-4%) of the LACI group and one (4%; 0-8%) of the POCI group ([chi square] P [is less than] 0.05). All these findings were confirmed on colour duplex Doppler.
Complete carotid occlusion
Complete carotid occlusion was found on portable Doppler in 28 (28%; 19-37%) of the TACI group compared with only 13 (13%; 6-20%) of the PACI group, three (3%; 0-7%) of the LACI group and none (0%; 0-14%) of the POCI group ([chi square] P [is less than] 0.05).
In the TACI group, 13 of the 28 who were thought to have carotid occlusion on portable Doppler had these findings confirmed on colour duplex Doppler. We categorized 12 (i.e. 77%) of the remaining as complete occlusion. All 13 in the PACI group had complete carotid occlusion on portable Doppler (nine of which were confirmed on colour duplex Doppler and two more by digital subtraction angiography). All three of the LACI group who had complete occlusion had the findings confirmed on colour duplex Doppler; one of these had a temporo-parietal infarct on CT.
Comparison between ipsilateral and contralateral carotid disease
The numbers of patients with TACIs, PACIs and LACIs with ipsilateral and contralateral internal carotid disease are shown in Figure 1. In the TACI and PACI groups, there was a significant difference between ipsilateral and contralateral internal carotid disease ([chi square] P [is less than] 0.05). For the LACI group, there was no significant difference between the two sides. For the 24 patients with POCIs, severe internal carotid stenosis was found in one ipsilateral internal carotid and one contralateral internal carotid ([chi square] P = n.s.).
[Figure 1 ILLUSTRATION OMITTED]
Contralateral carotid disease in patients with ipsilateral carotid occlusion
The effect of contralateral carotid disease in patients with complete ipsilateral internal carotid occlusion was also assessed. Of the 28 patients in the TACI group thought to have ipsilateral carotid occlusion, five (18%) had severe contralateral carotid stenosis or occlusion. Of the 13 patients in the PACI group with ipsilateral occlusion, two (15%) had severe contralateral internal carotid stenosis (no significant difference between TACI and PACI groups).
Atrial fibrillation and carotid stenosis
Atrial fibrillation was found in 30 (30%; 95% CI 21-39%) of the TACI group, 13 (13%; 6-20%) of the PACI group, five (6%; 0-10%) of the LACI group and two (8%; 0-13%) of the POCI group ([chi square] P [is less than] 0.001). Fourteen (28%) of the 50 patients in atrial fibrillation had carotid occlusion on either portable Doppler or colour duplex Doppler, compared with 30 of the 225 (13%) patients in sinus rhythm ([chi square] P [is less than] 0.01). Only three patients in atrial fibrillation (6%) had severe carotid stenosis as well. There were no patients with other major potential sources of cardiac emboli.
Selection of patients for carotid imaging using OCSP
If the OCSP is used to select patients for carotid imaging to identify those with severe stenosis, then an adequate sensitivity and specificity for detecting severe carotid stenosis is important. A 2x2 table can be constructed to demonstrate the clinical significance of selecting only those with PACIs for carotid imaging (Table 1). The sensitivity of selecting subjects with PACI alone would be 16/21 (76%) and the specificity would be 195/280 (70%).
Table 1. The clinical significance of selecting only patients with partial anterior circulation infarct (PACI) for carotid imaging
No. of subjects, by degree of stenosis Group 70- 99% Occlusion, moderate/none Total PACI 16 85 101 TACI, LACI and POCI 5 195 200 All 21 280 301
Sensitivity = 16/21 (76%); specificity = 195/280 (70%): positive predictive value = 16/101 (16%); negative predictive value = 195/200 (97.5%).
TACI, total anterior circulation infarct: LACI, lacunar infarct; POCI, posterior circulation infarct.
This is the largest study to investigate the relationship between the OCSP classification and carotid disease. We have shown that the OCSP predicts the likely prevalence of carotid disease, with severe stenosis being most common in patients with PACIs and complete carotid occlusion in patients with TACIs. Furthermore, there was a significant difference in the prevalence of ipsilateral and contralateral carotid disease in the PACI and TACI groups, but not in the LACI or POCI groups, suggesting that ipsilateral carotid stenosis is an important causative (rather than coincidental factor) in total and partial anterior circulation infarct but not in lacunar or posterior circulation infarct.
Severe carotid stenosis was most common in the PACI group. This may explain why early stroke recurrence is a particular feature of these patients . We did attempt to compare early stroke recurrence in patients with PACIs with and without carotid stenosis as some of the patients in the PACI group underwent urgent carotid endarterectomy as part of a randomized controlled trial comparing urgent with elective carotid endarterectomy .
Complete carotid occlusion was most common in the TACI group, with 28% of subjects having occlusion on portable Doppler (half of these confirmed by colour duplex Doppler). This is higher than in the other OCSP subtypes of stroke. Not all our patients underwent digital subtraction angiography, so a few of those with occlusion may have had a `trickle' flow undetectable on colour duplex Doppler. Previous studies have suggested that sudden occlusion of the internal carotid artery often causes severe neurological deficit (which is in keeping with our finding that occlusion is most common in subjects with TACIs), although carotid occlusion may cause mild neurological deficits or even no symptoms at all [11, 12]. The variability in clinical effects of sudden internal carotid occlusion is thought to be related to the collateral supply, mediated in part by the contralateral carotid artery . However, there were no important differences in contralateral carotid disease between TACI and PACI occlusions, which probably reflects the importance of other factors such as the anatomical integrity of the circle of Willis and collateral flow via the external carotid arteries [14-16].
Post mortem studies suggest that the most common mechanism for stroke in patients with carotid occlusion is probably thrombus formation on a severely diseased internal carotid artery . The low prevalence of severe stenosis in subjects with TACIs and a high prevalence of complete occlusion is consistent with the conversion of a tight stenosis into an occlusion. A previous history of TIA may indicate the presence of severe carotid stenosis, and early carotid imaging is important in these patients to prevent progression to occlusion. Post mortem studies also suggest that cardiogenic emboli may occlude a normal or stenosed internal carotid and cause complete occlusion . This possibility is supported by the association between atrial fibrillation and carotid occlusion in our study. The mechanism of stroke with carotid occlusion may be cerebral emboli at the time of occlusion, intracranial propagation of thrombus, or alternatively watershed infarction due to a fall in systemic arterial pressure with a pre-existing occlusion . Differentiating between these mechanisms is difficult, partly because of the unreliability of diagnosing watershed infarction on CT due to the variability of the collateral supply .
Only three of the LACI group had carotid occlusion and none had severe carotid stenosis. Small cortical infarcts, particularly in the non-dominant hemisphere, may present with lacunar syndromes, due the insensitivity of clinical examination in the detection of nondominant parietal lobe signs . If the OCSP classification is modified according to CT findings, then the single LACI subject with carotid occlusion and a cortical infarct on CT would be reclassified as having PACI, which would make the prevalence of carotid occlusion in the LACI group even lower. The low prevalence of ipsilateral carotid disease in the LACI group, with no difference between contralateral and ipsilateral carotid disease, suggests that ipsilateral carotid stenosis in lacunar infarcts are a coincidental finding. Previous studies have also demonstrated a low prevalence of carotid stenosis in lacunar infarction, suggesting that lacunar infarcts are due to small vessel disease (micro-atheroma or lipohyalinosis) and not large vessel atheroma [22-27].
Can the OCSP be used to select which patients with acute stroke should be referred for carotid imaging? The sensitivity of using the PACI classification to detect severe stenosis was 76% and the specificity 70%. An ideal screening test has a high sensitivity to ensure that all patients with significant disease are detected. If the PACI classification had been used to select patients for carotid imaging, then some patients with severe disease would have been missed. Does this matter? The remaining five patients in our series with severe stenosis had TACIs. Most subjects with TACIs would probably not be suitable for elective carotid endarterectomy because prophylaxis of further strokes is inapplicable due to the severity of the initial neurological deficit. There were no subjects with LACIs and severe stenosis, and one of the three who had LACIs and carotid occlusion had a cortical infarct on CT and could be reclassified as having a PACI. Therefore, a reasonable strategy would be to offer the following patients preferential carotid imaging: all who had PACIs, those with TACIs who make a good recovery and, finally, subjects with LACIs and cortical infarcts on CT. This strategy now needs prospective evaluation.
In summary, we have demonstrated that the prevalence of carotid disease in acute stroke is predicted by the OCSP subtype and we recommend that the OCSP be used to select which patients with acute stroke should be referred for carotid imaging.
* The Oxford Community Stroke Project (OCSP) classification of acute stroke can be used to determine which patients have carotid disease.
* Severe carotid stenosis is most common in partial anterior circulation infarct (16%).
* Complete carotid occlusion is most common in total anterior circulation infarct (28%).
* The OCSP classification has a sensitivity and specificity of 76% and 70% respectively for detecting severe carotid stenosis, and may be useful in selecting patients for carotid imaging.
We are grateful to our colleagues R. Ashleigh, consultant radiologist, A. Picton, vascular technician, and Brian Faragher, head of medical statistics.
We would particularly like to thank the collaborating consultants: P. Ackrill, J. R. Crampton, E. Freeman, A. Heagarty, M. A. Horan, P. E. Jones, J. J. Manns, P. A. O'Neill, D. Pearson, A. J. Ralston, R. M. Rash, J. M. Robinson, V. Srinivas and P. Whorwell at South Manchester University NHS Trust; J. A. Anandadas, T. Kondratowicz, S. N. Laha, B. Leahy, F. McKenna, S. R. Musgrave and W. P. Stephens at Trafford General Hospital; G. J. Archer, B. Cheadle, R. J. Cryer, M. C. Dattta-Chaudhuri, J. Downton, I. W. Dymock, P S. Lewis and M. A. Martin at Stepping Hill Hospital; M. P. Chopra, M. H. Husaini, O. M. P. Jalobe, M. A. Matin, N. M. O'Mullane, C. R. Payne and H. H. Wan at Tameside General Hospital; S. P. Hanley, E. N. Iyengar, V. Khanna, M. G. Pattrick, R. B. Shukla and P. J. Wiles at North Manchester General Hospital; and P. Bannister and M. Connolly at Manchester Royal Infirmary.
Funding for this study came from North West Regional Health Authority, University of Manchester Bequest Fund and Mason Medical Research Trust.
[1.] Bamford J, Sandercock P, Dennis M, Burn J, Warlow c. Classification and natural history of clinically identifiable subtypes of cerebral infarction. Lancet 1991; 337:1521-6.
[2.] Lindley RI, Warlow CP, Wardlaw JM, Dennis MS, Slattery J, Sandercock PAG. Interobserver reliability of a clinical classification of acute cerebral infarction. Stroke 1993; 24: 1801-4.
[3.] European Carotid Surgery Trialists' Collaborative Group. MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (70-99%) or with mild (0-29%) carotid stenosis. Lancet 1991; 337: 1235-43.
[4.] North American Symptomatic Carotid Endarterectomy Trial Collaborators. Beneficial effects of carotid endarterectomy in symptomatic patients with high grade carotid stenosis. N Engl J Med 1991; 325: 445-53.
[5.] Naylor AR, Sandercock PAG, Warlow CP. Patterns of vascular pathology in acute, first-ever cerebral infarction. Scot Med J 1993; 38:41-4.
[6.] Lindgren A, Roijer A, Norrving B, Wallin L, Eskilsson J, Johansson BB. Carotid artery and heart disease in subtypes of cerebral infarction. Stroke 1994; 25: 2356-62.
[7.] Hatano S. Experience from a multicentre stroke register: a preliminary report. Bull WHO 1976; 54: 541.
[8.] Poungvarin N, Viriyavejakul A, Komontri C. Siriraj stroke score and validation study to distinguish between supratentorial intracerebral haemorrhage from infarction. Br Med J 1991; 302: 1565-7.
[9.] Mead GE, Picton AJ, Farrell A, O'Neill PA, McCollum CN. Is portable carotid Doppler scanning cost effective? J Vasc Investigation 1996; 2: 49-52.
[10.] Mead GE, O'Neill PA, McCollum CN. Carotid surgery in acute stroke. Eur J Vasc Endovasc Surg 1997; 13: 112-21.
[11.] Thompson JE, Talkington CM. Acute carotid occlusion. In: Greenhalgh RM, Hollier LH eds. Emergency Vascular Surgery. Philadelphia: WB Saunders, 1992; 139-44.
[12.] Nicholls SC, Bergelin R, Strandness DE. Neurological sequelae of unilateral carotid artery occlusion: immediate and late. J Vasc Surg 1989; 10: 542-8.
[13.] Norris JW, Krajewski A, Bornstein NM. The clinical role of the cerebral collateral circulation in carotid occlusion. J Vasc Surg 1990; 12; 113-8.
[14.] Radu EW, Mosely IF. Carotid artery occlusion and computed tomography: a clinico-radiological study. Neuroradiology 1978; 17: 7-12.
[15.] Wiener LM, Berry RG, Kundin J. Intracranial circulation in carotid occlusion. Arch Neurol 1964; 11: 554-61.
[16.] Pitts FW. Variations of collateral circulation in internal carotid occlusion. Comparison of clinical and X-ray findings. Neurology 1962; 12: 467-71.
[17.] Castaigne P, Lhermitte F, Gautier J-C, Escourelle R, Derousne C. Internal carotid occlusion: a study of 61 instances in 50 patients with post-mortem data. Brain 1970; 93: 231-58.
[18.] Berry RG, Alpers BJ. Occlusion of the carotid circulation. Pathologic considerations Neurology 1957; 7: 223-37.
[19.] Ringelstein EB, Zeumer H, Angelou D. The pathogenesis of strokes from internal carotid occlusion. Diagnostic and therapeutic implications. Stroke 1983; 14: 867-75.
[20.] Van De Zwan A, Hillen B, Tulleken CAF, Dujovny M, Dragovic L. Variability of the territories of the major cerebral arteries. J Neurosurg 1992; 77: 927-40.
[21.] Toni D, Del Duca R, Fiorelli M et al. Pure motor hemiparesis and sensorimotor stroke. Accuracy of very early clinical diagnosis of lacunar strokes. Stroke 1994; 25: 92-6.
[22.] Landi G, Anzalone N, Cella E, Boccardi E, Musicco M. Are sensorimotor strokes lacunar strokes? A case control study of lacunar versus non-lacunar infarcts. J Neurol Neurosurg Pyschiatry 1991; 54: 1063-8.
[23.] Tei H, Uchiyama S, Maruyam S. Capsular infarcts: location size and etiology of pure motor hemiparesis, sensorimotor stroke and ataxic hemiparesis. Acta Neurol Scand 1993; 88: 264-8.
[24.] Boiten J, Lodder J. Lacunar infarcts: pathogenesis and validity of the clinical syndromes. Stroke 1991; 22: 1374-8.
[25.] Lodder J, Boiten J, Heuts-van Raak L. Sensorimotor syndrome relates to lacunar rather than non-lacunar cerebral infarction (letter). J Neurol Neurosurg Psychiatry 1992; 55: 1097.
[26.] Landi G, Cella E, Boccardi E, Musicco M. Lacunar versus non-lacunar infarcts: pathogenesis and prognostic differences. J Neurol Neurosurg Psychiatry 1992; 55: 441-5.
[27.] Horowitz DR, Tuhrim S, Wieinberger JM, Rudolph SH. Mechanisms of lacunar infarction. Stroke 1992; 23: 325-7.
Received 19 June 1997; accepted 31 October 1997
GILLIAN E. MEAD, HELEN SHINGLER(1), ANNE FARRELL(1), PAUL A. O'NEILL, CHARLES N. McCOLLUM(1) Department of Geriatric Medicine and (1) University Department of Surgery, South Manchester University NHS Trust, Nell Lane, West Didsbury, Manchester M20 8LR, UK
Address correspondence to: G. E. Mead, Bramwell Dart Building, Department of Clinical Neurosciences, Western General Hospital, Edinburgh EH4 2DN, UK
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|Author:||MEAD, GILLIAN E.; SHINGLER, HELEN; FARRELL, ANNE; O'NEILL, PAUL A.; McCOLLUM, CHARLES N.|
|Publication:||Age and Ageing|
|Date:||Nov 1, 1998|
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