MS Dennis, JM Bamford, PA Sandercock and CP WarlowIncidence of transient ischemic attacks in Oxfordshire, England

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333

Incidence of Transient Ischemic Attacks inOxfordshire, England

M.S. Dennis, MD, MRCP, J.M. Bamford, MD, MRCP,

P.A.G. Sandercock, DM, MRCP, and C.P. Warlow, MD, FRCP

The Oxfordshire Community Stroke Project is a prospective register of all new cases of strokeand transient ischemic attack (TIA) in a population of 105,000 residents of Oxfordshire,England. Between November 1,1981, and October 31,1986,184 patients presented for the firsttime to a general practitioner or hospital with a TIA. The crude annual incidence rate was 0.35/1000, 0.42/1000 standardized to the 1981 population of England and Wales. We estimate thateach year approximately 21,000 patients in England and Wales (about half of whom are >70years old) consult a doctor for the first time with a TIA. Approximately 80% of our 184 patientshad TIAs in the carotid distribution; the remainder had TTAs in the vertebrobasilar distributionor TIAs of uncertain vascular distribution. The incidence of TIA increased sharply withincreasing age, and the overall incidence in men was very similar to that in women (incidenceratio 1.3). However, in middle age, men were much more likely to suffer a TIA than women(odds ratio 2.6), which probably explains the marked male predominance in most hospital-based studies and treatment trials in which the elderly, and thus women, are underrepresented.This has important implications for the design and interpretation of clinical trials of treatmentsfor TIAs. (Stroke 1989;20:333-339)

There have been relatively few community-based studies of the incidence of transientischemic attacks (TIAs), only one in Great

Britain.1 It is important to measure the incidence ofTIAs for several reasons. First, reliable incidencedata allow one to calculate the contribution oftreatments for TIAs to the primary prevention ofstroke, bearing in mind that TIAs may increase therisk of stroke sevenfold2 and may precede stroke in9.4%3 to 26%4 of cases. Second, if carotid angiog-raphy and carotid endarterectomy can be shown tobe worthwhile in the investigation and treatment ofTIAs, accurate incidence data will allow us toestimate the cost of providing these procedures.Third, one cannot plan trials of treatment for TIAswithout knowing the untreated natural history ofthe disease, the number of patients likely to beavailable, and in particular the number of patientslikely to fulfill entry criteria; only then can funda-mental decisions, such as whether the trial shouldbe performed in one center (e.g., the Newcastle

From the University Department of Clinical Neurology, Rad-cliffe Infirmary, Oxford, England.

Supported by grants from the Medical Research Council andthe Chest, Heart and Stroke Association.

Address for correspondence: Prof. C.P. Warlow, Departmentof Clinical Neurosciences, Western General Hospital, EdinburghEH4 2XU, Scotland.

Received June 16, 1988; accepted October 10, 1988.

Carotid Surgery Trial3), in several centers in onecountry (e.g., the UK-TIA Aspirin Trial6), in onecontinent (e.g., the European Carotid SurgeryTrial7), or even in several continents (e.g., the EC/IC Bypass Study8), be made. Of course, for thesepurposes one does not need to know the incidenceof all TIAs but rather the incidence of TIA patientswho seek medical attention and whose subsequentstrokes are at least potentially preventable. Personswho have had a TIA but do not seek medicalattention (and there is evidence that these may forma large percentage of the total; see below) are of lessinterest in these respects, although if such personscould be encouraged to seek medical help, theopportunities for primary stroke prevention wouldbe greatly enhanced.

Our study was designed to measure the incidenceof TIA in the population whose TIAs come to theattention of a doctor; it was based on primary-careas well as hospital physicians so that persons whowere not normally admitted or referred to hospitalclinics could be counted. Our study was designed toovercome many of the methodologic problems,including incomplete or biased case ascertainment(which tend to occur in retrospective or hospital-based studies) and a lack of precision in defining aTIA and more particularly an incident case, ofprevious studies.

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334 Stroke Vol 20, No 3, March 1989

Subjects and Methods

Our study of the incidence of TIAs formed part ofa larger study of the epidemiology of acute cere-brovascular disease, the Oxfordshire CommunityStroke Project (OCSP), the overall design of whichhas been described in detail.9-"

The study population comprised approximately105,000 people who were fully registered (i.e., nottemporary residents) with 50 general practitioners(GPs) working from 10 health centers distributedthroughout urban and rural Oxfordshire. The denom-inator for the incidence rates was calculated byaveraging the number of people in each 10-year ageband on the age/sex registers (ASRs) of the GPs atthe beginning and end of the study. The populationincreased by approximately 6% during the studyperiod. The figures obtained from the ASRs werevalidated against records held by the OxfordshireFamily Practitioners Committee (FPC), which aregenerally considered to be more accurate than ASRssince they form the basis for remuneration of GPs.12

It was impractical to use the FPC figures them-selves since these records are not computerized,are stored alphabetically, and are split into onlythree age bands (0-65, 65-75, and >75 years).

In the 5 years between November 1, 1981, andOctober 31, 1986, the collaborating GPs agreed tonotify the OCSP of all patients suspected of suf-fering a TIA. We also scrutinized hospital admis-sion and discharge records to detect patients whohad come directly to a casualty department. Eachpatient was assessed by one of us, in the patient'shome if necessary. A set of basic investigations(including computed tomography) was performed toexclude other causes of transient symptoms (e.g.,intracranial tumors, hypoglycemia, etc.). We exam-ined each patient's GP's and hospital records toexclude patients with previous (known to theirdoctor) TIAs and strokes as well as to provide dataon vascular risk factors collected prior to the TIA.

A TIA was defined as an acute loss of focalcerebral or ocular function with symptoms lasting<24 hours and that, after adequate investigation,was presumed to be due to embolic or thromboticvascular disease.13 We classified attacks of unilat-eral motor or sensory symptoms, dysphasia, ortransient monocular blindness as carotid-distributionTIAs while attacks of vertigo, diplopia, hemianop-sia, or bilateral (during a single attack) motor orsensory symptoms were classified as vertebrobasilar-distribution TIAs. Dysarthria was not used to clas-sify the vascular distribution of a TLA. We excludedpatients with isolated vertigo, diplopia, bilateralblindness, or drop attacks since such symptomsoccurring alone may result from either difruse cere-bral ischemia or from nonvascular pathologies. Wealso excluded patients with only nonfocal symp-toms (such as loss of consciousness) as well aspatients with features suggesting migraine (i.e.,progressive onset or a typical positive visual phe-

nomena even if headache was absent), epilepsy, ortransient global amnesia.

In studies of the epidemiology of stroke in whichaccurate measurements of incidence are required,it is important that only new (or incident) cases areregistered and that patients with previous strokesare not included.14 Furthermore, in studies ofnatural history it is important to include cases atan early and uniform point in the course of theirdisease.15 These considerations are even more impor-tant in the study of the epidemiology of TIAs, yetno previous study has attempted to provide a rigor-ous definition of an incident case. We define anincident case as a patient whose first TIA that led toconsultation with a doctor occurred during thestudy period. TIAs occurring before the study periodthat the patient had not brought to a doctor'sattention were ignored; if a patient suffered a fur-ther TIA during the study period that led him or herto consult a doctor, then the most recent attack wascounted as the incident TIA. Patients who sufferedattacks prior to the study period that, after consul-tation with a doctor, were diagnosed as TIAs wereclassified as prevalent cases. Occasionally patientshad seen a doctor prior to the study period withattacks that were not diagnosed as TIAs but thenpresented with a definite TIA during the studyperiod; if the previous attacks were identical to thepresent episode, then the patient was classified as aprevalent case. Therefore, we did not rely upon thediagnostic skills of GPs. We excluded patients whopresented to a doctor during the study period withtheir first TIA but who had already suffered a strokeeither before or after the TIA.

We excluded patients who had a TIA but did notseek medical advice until after a stroke had occurredsince their inclusion would inevitably have biasedthe prognosis and may have distorted the age/sex-specific incidence of TIA if the risk of strokeafter a TIA is influenced by age or sex. This rathercomplex definition is necessary to avoid ambiguitybecause, unfortunately, patients with TIAs often donot consult a doctor with their first TIA if, indeed,they consult a physician at all. Some of the moreimportant features of our definition of an incidentcase are illustrated in Figure 1.

Several authors have shown that the interob-server reliability of the diagnosis of TIAs is poor.1617

We attempted to optimize interobserver reliabilityby first discussing, using simple language17 at aweekly meeting that at least two of us attended, theclinical features of every patient referred. Second,we kept the delay between the attack and ourassessment of the patient as short as possible (median5 days) to obtain the most accurate history from thepatient. Third, we applied our definitions strictly,and to ensure their uniform interpretation through-out the study period, after all cases had beennotified to the OCSP one of us reviewed the notes ofevery patient notified to and assessed by the OCSP.

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Dennis et al Incidence of TIA in Oxfordshire 335

Included

STUDY PERIOD TIME

FIGURE 1. Diagram illustrating some important parts ofour definition of incident transient ischemic attack (TIA).Included, counted as incident case in this study; TIAsoccurring before study period (prevalent cases) or patientswho already had a stroke (S) at the time of medicalcontact were not included. • , first TIA; O, incident TIA,arrow, medical contact.

We calculated 95% confidence intervals (CIs) ofincidence rates and the approximate 95% CIs ofodds ratios (ORs) using standard methods.1819

Pooled ORs (see Figure 4) with 95% CIs wereobtained by the method described by Yusuf et al.20

ResultsThe age and sex structure of the study population

is shown in Table 1. The totals obtained from theASRs were slightly lower (-1.1%) in 1981 andslightly higher (2.3%) in 1986 than those from theFPC. Such small discrepancies made little differ-ence in the calculated incidence rates.

During the study period, 512 patients were referredby their GPs or presented at a hospital with tran-

sient symptoms. Following our assessment, weincluded 184 as incident TIAs; the remainder fellinto a variety of other diagnostic categories (Figure2). The mean age of the 184 incident cases was 69.4(range 20-100) years; 103 were men and 81 werewomen. The number of cases is shown by sex and10-year age band in Table 1 along with the age/sex-specific incidence rates and 95% CIs. The age/sex-specific incidence is shown graphically in Fig-ure 3, which illustrates that the incidence of TIAsrose sharply with increasing age in both men andwomen, although there was a tendency for theincidence to decrease in men >85 years old.

The overall incidence of TIAs was slightly greaterin men than in women (incidence ratio 1.3); how-ever, during middle age the difference in incidencebetween the sexes increased. This is illustrated inFigure 4, in which the ORs (i.e., the odds of a mansuffering a TIA divided by the odds of a womansuffering a TIA) with their approximate 95% CIs areshown for 10-year age bands. Only between 55 and74 years of age does the difference between menand women reach the conventional level of signifi-cance (p<0.05).

Our study population was slightly younger thanthat of England and Wales21 so, although the crudeincidence of TIAs in our study was 0.35/1000/yr(95% CI 0.3-0.4/1000/yr), the age/sex-adjusted inci-dence (standardized by the direct method to the1981 population of England and Wales21) was greater(i.e., 0.42/1000/yr). If our incidence rates are appliedto the 1981 England and Wales population,21 approx-imately 21,000 people, about 50% of whom wouldbe >70 years old, are likely to present for the firsttime to doctors each year with a TIA.

One hundred sixteen patients (63%) had cerebralattacks in the carotid distribution (two of these alsohad episodes of amaurosis fugax) and 32 (17%) hadamaurosis fugax only; approximately 80%, there-fore, had a carotid-distribution TIA. The remaining36 patients suffered either vertebrobasilar-distributionTIAs or TIAs of uncertain vascular distribution (e.g.,isolated dysarthria).

TABLE 1. Age/Sex-Speciflc Incidence Rates for Transient Iscbemk Attacks in Oxfordshire, England, November 1,1981, to October 31,1986

Age band(yr)

<1515-4445-5455-6465-7475-843:85

Total

5-year study period

Males

Cases

037

294023

1103

At risk

975427,953

5595475232971528285

53,164

Females

Cases

027

1517281281

At risk

921525,871

5386478937702446835

52,312

Total

Cases

05

1444575113

184

At risk

18,96953,82410,981

9541706739741120

105,476

Annual incidence/1000 population

Males

Incidence

0.000.020.251.222.433.010.700.39

95% CI

0.00-0.040.06-0.440.77-1.661.68-3.171.79-4.230.00-2.070.31-0.46

Females

Incidence

0.000.020.260.630.902.292.870.31

95% CI

0.00-0.040.07-0.450.31-0.940.47-1.331.45-3.131.26-4.490.24-0.38

Total

Incidence

0.000.020.250.921.612.572.320.35

95% CI

0.01-0.030.12-0.390.65-1.191.20-2.031.87-3.271.09-3.670.30-0.40

CI, confidence interval.

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336 Stroke Vol 20, No 3, March 1989

512 Patients Referred

195 TIAs

11 Prevalent TIAs

317 Others

184

\\\

\\\

Incident TIAs

MigraineSyncopePossible TIA

"Funny turn"Isolated vertigoEpilepsyTransient global amnesiaLone bilateral blindnessIsolated diplopiaDrop attackMeiiingioniflsMiscellaneous

524846453329171443224

FIGURE 2. Breakdown by diagnosis of allpatients with transient symptoms notifiedto Oxfordshire Community Stroke Project(November 1, 1981, to October 31, 1986).Possible TIA, patients with transient focalneurologic symptoms in whom clinical fea-tures were not sufficiently clear to makediagnosis of definite transient ischemicattack (TIA). Funny turn, episodes withonly nonfocal symptoms (e.g., confusion).

During 4 of the 5 years of our study, strokepatients were also registered," and 76 (11%) of 675patients who presented with a first-ever stroke alsogave a history of definite preceding TIAs. Fifty(66%) of these 76 patients had TIAs during thestudy period, and of these 50, 27 (54%) had not seena doctor about the TIA, 19 (38%) had been referredto the OCSP with TIAs previously and were includedas incident cases, and four (8%) had seen a doctorwith a TIA but had not been referred to the OCSP.Therefore, it appears that at least 54% (95% CI40-68%) of patients suffering TIAs did not consult adoctor until their stroke occurred. Of course, we donot know how many persons had a TIA and failed toconsult a doctor but did not suffer a stroke and as aconsequence did not come to our attention. If the 31patients presenting to the OCSP with a stroke butgiving a history of a definite previous TIA occurringduring the study period are included, the crudeincidence of TIA is increased from 0.35 to 0.41/1000/yr.

DiscussionStudies of TIA incidence have been performed

in Britain,1 Europe,22-28 the United States,329-32

and Asia.3334 However, problems arise when one

3 r

<15 15-44 45-54 55-64 65-74 75-84 >85Age (Years)

FIGURE 3. Age/sex-specific incidence (per 1000 popula-tion) of transient ischemic attacks in Oxfordshire, England,November 1,1981 to October 31,1986. U, men; a, women.

tries to compare the results of these studies. First,many studies give incidence rates for only limitedand differing age ranges23-2628-303234; other studiesgive only crude incidence rates '-24-27-30-31 s o t h a tdifferences between studies may simply reflect thediffering age and sex structures of the study pop-ulations. Most studies investigated only small pop-ulations and consequently identified very few casesso that their estimates of incidence rates lackprecision. Only two studies33-34 quote 95% CIs fortheir rates.

Several studies were hospital-based23-26-29 andtherefore presumably failed to count an unknown,but probably significant, number of cases remainingin the community. Certain studies used surveytechniques (i.e., questionnaires and interviews bynonmedical personnel) to detect all persons with a

S.O r

4.0 •

3.0 •

o

^ o -

1.0

0.0

-

\

•

11<45 45-54 55-64

Age (Years)65-75 >75 At Ages

FIGURE 4. Odds ratio (OR) of men having transient isch-emic attacks (TIAs) compared with women having TIAs indifferent age bands. OR of l.0 indicates equal risk while ORof > 1.0 indicates greater risk of TIA in men than women.Error bars indicate approximate 95% confidence intervals.Where confidence intervals are so wide as to extend beyondthe y axis scale dotted lines have been used. N.B: PooledOR (for all ages) is weighted to take into account differentnumbers of subjects in each age band.

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Dennis et al Incidence of TIA in Oxfordshire 337

TABLE 2. Crude and (When Available) Sex-Spedflc Incidence of Transient Iscbemlc Attacks in Different Populations

Study

BritishStroke, UK1

Oxford, UK (current study)European

Tartu, USSR22

Soderhamn, Sweden23

Dyon, France24

AmericanRochester, Minnesota3

Evans County, Georgia31

Lehigh Valley, Pennsylvania29

AsianSix cities, China33

Male

0.39

0.36

0.31

0.50

0.48

Incidence (no./1000/yr)

Female

0.31

0.33

0.31

0.48

0.49

Total

1.240.35

0.330.450.36

0.311.100.49

0.49

Incidence ratio(male/female)

1.26

1.09

1.00

1.04

0.98

Only studies publishing incidence rates for all age groups are included.

TIA whether they saw a doctor or not2728-31-34 whileother studies counted only those persons who con-sulted a doctor. 1.3,22-26.29,30 The former are clearlymore likely to produce higher incidence rates butmay include patients who did not have definiteTIAs. In the first incidence study, Acheson andcolleagues' defined a TIA as an attack lasting <1hour and might therefore be expected to producelower incidence rates than the other studies. How-ever, more subtle differences in the definitions of aTIA and an incident case and differences in themethods of case ascertainment may also contributeto the differences in the results of these studies. Theimportance of using standard methods to measurethe incidence of stroke has recently been high-lighted by Malmgren and colleagues,14 but many oftheir comments apply equally to the estimation ofTIA incidence. Despite these methodologic differ-ences, it is surprising how similar many estimates ofcrude incidence are (Table 2). However, the impre-cision of these rates and their methodologic differ-ences may actually obscure real differences in inci-dence that are not due solely to the different age/sexstructures of the study populations.

More interesting than this very rough comparisonof crude incidence rates is the comparison of age-specific rates (Figure 5). This is possible for only thethree studies that published such rates32229 for allages. Direct comparison is hampered by the dif-ferent age bands used, but in Figure 5 we haveadjusted our age bands to match those of the otherstudies. There appears to be little difference betweenthem, especially if one notes the fairly wide 95%CIs around these age-specific rates (shown only forthe OCSP). Certainly in one study,3 and perhaps inthe other two,22-29 patients were included even ifthey presented with a stroke, and this would tend toinflate the incidence rates. These studies were allretrospective and relied upon diagnostic indexes todetect cases. J.P. Whisnant (personal communica-tion) has recently revealed that the diagnostic indexat the Mayo Clinic may have failed to detect up to50% of cases of TIAs presenting to that institution,

and Whisnant et al3 may therefore have underesti-mated the TIA incidence. In the OCSP GPs mayhave failed to refer some patients with TIAs, but thesmall number of cases who came to our attentionvia other routes (i.e., hospital records) or perhapsafter they had gone on to suffer a stroke indicatedthat this was probably not a major problem. A verymuch more important problem is that so manypatients with TIAs simply do not report them to adoctor. The size of this problem may vary betweenpopulations, depending on several factors such ashow stoic the people are, their awareness of healthmatters, and perhaps the cost of medical care.

The higher relative odds of a TIA in men ofmiddle age (Figure 4) is interesting since it couldexplain differences in the sex ratios observed incommunity-based incidence studies compared withhospital series and treatment trials. In the former,the overall male:female incidence ratio is usuallyapproximately 1.0 (0.98-1.26; Table 2), while in thelatter, ratios of 2:1 and even 3: 16.35.36 are not uncom-mon, presumably because in hospital-based studiesand treatment trials young and middle-aged peoplepredominate to the exclusion of the elderly. Thishypothesis is supported by the fact that the averageage of patients in our study was 69.4 years while inmost hospital studies it is around 60 years and insome37 it is as low as 49 years. This underrepreSen-tation of the elderly, and thus women, in treatmenttrials may be important, especially as 50% of patientswith TIAs are >70 years old. The results of ran-domized controlled trials would be more preciseand generalizable to women if they included moreelderly (and thus female) subjects. Older patientsare bound to contribute more events (such as vas-cular deaths and strokes) in trials s.o that differencesbetween treatment groups might be identified moreeasily. This would be an argument for basing futuretrials of medical treatment for TIAs in the commu-nity rather than in hospitals.

AcknowledgmentsWe would like to thank all those who have helped

with this project including Sue Price, Liz Mogridge,

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338 Stroke Vol 20, No 3, March 1989

3.0

§ 2.0TJ2

0.0

3.0

OCSPRochester

<45 45-54 55-64

Age(Y«ars)

65-74 >75

ooo

0>TJ

2.0

a

I 1.0

0.020-29 30-39 40-49 50-59

Age (Years)

60-69 70-79 80+

4.0

3.0

2^ 2.0

1.0

0.0

OCSPLehigh Valley

<45 45-64 65-74

Age (Yure)75-84 >85

FIGURE 5. Graphs of age-specific incidence and 95%confidence intervals for transient ischemic attacks inOxfordshire Community Stroke Project (OCSP) com-pared with incidences from three studies that providedsuch information for all age groups. Top left: Rochester,Minnesota3; top right: Tartu, Estonia, USSR22; bottomleft: Lehigh Valley, Pennsylvania.29 Note different agebands used in each graph. These studies did not publish95% confidence intervals.

and Clare Clifford, our study nurses; Lesley Jones,the project's computer programmer; and HelenStorey, Vanessa Langsbury, Angie Dwyer, andAndrea Watts, who provided secretarial support.We especially thank all our collaborating generalpractitioners without whose help this researchwould be impossible. The collaborating practiceswere (name of liaison partner from each practiceonly): Dr. A. McPherson, Oxford; Dr. A. Marcus,Thame; Dr. D. Leggatt, Oxford; Dr. M. Agass,Berinsfield; Dr. D. Otterburn, Abingdon; Dr. S.Street, Kidlington; Dr. V. Drury, Wantage; Dr. R.Pinches, Abingdon; Dr. N. Crossley, Abingdon;and Dr. H. O'Donnell, Deddington.

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KEY WORDSEngland

cerebral ischemia, transient • epidemiology

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