Abstract
Introduction:
Transient ischemic attack (TIA) is a frequent neurological emergency which management and definition have changed radically over the last 15 years. However, recent epidemiological studies of TIA are scarce. We report here on the impact of the shift from a time-based to a tissue-based definition of TIA on its incidence and risk of recurrence in a new population-based cohort with a high rate of patients investigated by MRI.
Materials and methods:
We prospectively included all TIAs that occurred between May 2017 and May 2021 from the Normandy Stroke Study, a population-based registry using multiple overlapping sources for exhaustive case identification in Caen la Mer area. TIAs were classified as either time-based (symptoms <24 h) or tissue-based (<24 h and no lesion on brain imaging). Attack and incidence rates were calculated, as was the 90-day ischemic stroke rate.
Results:
Five hundred and sixty-seven TIAs (549 single patients) were included, with 80.6% having a brain MRI. Four hundred and ten (72.3%) met the definition of tissue-based TIA. The age standardized attack (to the 2013 European population) rate was 39.5 (95% CI 35.7–43.5) and the age-standardized incidence rate (first ever cerebrovascular event) was 29.7 (95% CI 27.3–34.2). The overall recurrent stroke rate at 90 days was 2.7%, with no difference between patients with or without ischemic lesions on MRI.
Conclusion:
We found that the use of the tissue-based definition of TIA resulted in a 27.5% reduction in incidence as compared to the time-based definition, but had no impact on the 90-day stroke rate. The burden of TIA remains high, and is likely to increase as the population ages.
Keywords: Transient ischemic attack, stroke, epidemiology
Graphical abstract.
Transient ischemic attack (TIA) is a common neurological syndrome with an increased risk of subsequent ischemic stroke in the following days. A TIA precedes up to 15% of ischemic strokes. 1 Since the first diagnostic criteria for TIA were published in 19702,3 its diagnosis and management have undergone major changes. First, in 2009, a tissue-based definition of TIA was adopted by the American Stroke Association/American Heart Association (ASA/AHA), replacing the traditional time-based definition.4,5 Accordingly, a TIA is defined as a transient episode of neurological dysfunction caused by focal brain, spinal cord, or retinal ischemia, without evidence of acute infarction. This definition is highly dependent on imaging settings but excludes minor strokes, as around 30% of patients with symptoms compatible with a TIA have acute infarction on MRI. 6 Second, landmark studies have emphasized that urgent management of TIA in specialized care settings reduces the risk of subsequent stroke in the following days. 7 A recent meta-analysis included 206,455 individuals and 68 unique studies of various methodology and showed that the 90-day risk of stroke after a TIA decreased from 7.4% before 1999 to 3.9% after 1999. 8 A large multicenter cohort study of TIA clinics reported an even lower risk of stroke after a TIA, reaching 2.8% at 90 days. 9
In addition to the risk of recurrent stroke, the burden of TIA depends on its incidence, as patients with suspected TIA mobilize important resources. During the last 20 years, only few studies10–16 have examined the incidence of TIA using gold standard, population-based epidemiological methods and fewer reported data on stroke recurrence.13,15 Moreover, the impact of the tissue-based definition on the incidence of TIA has been rarely evaluated, 16 notably because the proportion of patients with brain diffusion weighted imaging (DWI) MRI at the acute phase is low in most routine settings. Yet, the availability of MRI for patients with suspected TIA has improved in most high-income countries in recent years, increasing the need for new epidemiological studies that reflect current clinical practices.
Our objectives were to report the incidence of TIA and the risk of ischemic stroke recurrence 90 days after a TIA using the time and tissue-based definition of TIA in the Normandy Stroke population-based study.
Methods
Population
The Normandy Stroke study is a prospective population-based study of all in- and outpatients with cerebrovascular events from May 2017 in residents of Caen-la-Mer (France). The Normandy Stroke study is registered by the French registry evaluation committee. The complete methods of the study have been published elsewhere. 17
Briefly, Caen-la-Mer is an urban, suburban, and rural area of 366 km² in the Northwest of France with 267,262 residents according to the 2017 national census. The area is deserved by 1 public academic hospital (Caen University hospital, called CHU Caen Normandie), 3 private hospitals, 3 emergency departments, 6 private neurologists, around 250 general practitioners (GP), and an emergency GP home service in the city of Caen (“SOS Médecins”). In the area of interest, the only neurology department is located at the CHU Caen, which corresponds to the comprehensive stroke center for a larger regional area. This center includes a stroke unit and a neurologist on call 24/7 to assess any patient suspected of having an acute stroke or a TIA in the area.
Screening of possible cases is performed according to the current gold standard in stroke epidemiological studies, using multiple overlapping prospective and retrospective sources.18–20 Prospective sources includes the daily checking of admissions to the CHU Caen Normandie stroke unit and emergency, neurology, and neurosurgery departments. The outpatient schedules of all physicians involved in stroke management are checked daily. General practitioners and private neurologists are repeatedly encouraged to refer all patients with a suspected stroke to the CHU Caen Normandy or to notify each case by a dedicated email.
Retrospective sources include yearly checking the files of patients discharged from the three private hospitals and their emergency departments and of patients seen by the SOS Médecins service. As the CHU Caen Normandy is the reference hospital for a broader area than Caen-la-Mer, it is unlikely that patients living in Caen-la-Mer sought medical attention in the neighboring areas. However, the files of patients admitted in the two hospitals closest from Caen-la-Mer are also checked yearly to identify possible cases.
A neurologist specialized in cerebrovascular diseases validate each possible new case of stroke or TIA. In case of doubt, the decision is taken after discussion with the principal investigator of the study (ET).
Case definition
We included all TIAs occurring in patients older than 30 days between May 15th, 2017 (beginning of the study) and May 14th, 2021. In line with current practices in population-based TIA studies, 19 an event was considered as a TIA if it met the traditional, time-based definition of TIA: a sudden, focal neurological deficit of presumed vascular origin lasting <24 h. Patients presenting symptoms compatible with TIA but who did not seek medical attention were not included. We considered a TIA as meeting the ASA/AHA – tissue-based – criteria if it met the time-based criteria for TIA without signs of acute infarction on imaging. The presence of an acute infarct was assessed by reviewing the medical record when direct access to the brain imaging was not possible. Isolated vertigo, gait disturbance, confusion, dysarthria, and diplopia were not included in the Normandy Stroke study accepted in the case of acute ischemic lesions. A TIA was considered incident if it was the first ever ischemic cerebrovascular event (CVE) and recurrent if the patient had a history of ischemic stroke or TIA before or during the study period. In order to avoid biases on attack rates due to possible cluster TIAs in some patients, we considered a new TIA as a distinct event if it was separated from the index TIA by at least 15 days or if it occurred in a new vascular territory.
Data collected
Demographic data, vascular risk factors (history of hypertension, diabetes mellitus, hypercholesterolemia, and current smoking), previous atrial fibrillation, prior coronary artery disease, prior peripheral artery disease, medication, and ABCD2 score 21 were collected for each case. Patients were considered hypertensive if they had a documented history of blood pressure above 140/90 mmHg or were under antihypertensive treatment. Dyslipidemia was defined as a history of dyslipidemia in the medical record or use of lipid-lowering therapy. Patients were classified as having a prior coronary artery disease if they had at least one of the following: previous myocardial infarction, stable or unstable angina, and previous coronary intervention (angioplasty, stenting, or bypass graft surgery). Prior peripheral artery disease was defined as having at least one of the following: previous acute limb ischemia, critical limb ischemia, intermittent claudication, previous angioplasty or stenting, and peripheral arterial bypass graft or amputation.
Stroke recurrence: Case definition and identification
Ischemic stroke recurrence or death was evaluated up to 90 days after the index TIA. Stroke was defined as rapidly developing clinical signs of focal (or global) disturbance of cerebral function, lasting more than 24 h or leading to death, with no apparent cause other than that of vascular origin. As the Normandy Stroke study was designed to exhaustively identify all cerebrovascular events developing in the territory, most recurrences were identified through the study. In addition, information on recurrent events was sought from medical records, from telephone interview of patients who had not returned to follow-up visit, or by contacting the treating GP. The vital status at 90 days was collected through the publicly available death list published weekly by the French national institute of statistics.
Statistical analyses
Statistical analyses were performed with R version 4.0.4. The crude incidence rate was defined as the number of first ever TIAs per 100,000 person-years and the crude attack rate as the number of incident and recurrent TIAs per 100,000 person-years. Incidence and attack rates were calculated for both the time-based and tissue-based TIA definitions. The 95% confidence intervals (CI) were calculated assuming a Poisson distribution. Population data was obtained from 2017 French census. Standardized incidence rates were calculated using the direct method with the 2013 European standard population as reference. 22
We compared baseline characteristics of first in study TIA cases according to the presence of an acute infarct on brain MRI and according to whether the TIA was incident or recurrent. To avoid multiple counting of a same patient, we limited these two analyses to first in study TIA cases. Recurrent events were nevertheless included in the calculation of attack rates. The comparison of patients with or without an acute infarct was restricted to these with a brain MRI to ensure better comparability between groups and because of the high rate of MRI in our study. Comparisons were done using t-tests for quantitative variables and odds-ratio or Chi-2 tests for categorical variables. A p < 0.05 was considered statistically significant, without adjustment for multiple comparisons. Missing data were not imputed.
Results are reported according to the STROND checklist for the reporting of incidence in neuroepidemiology 23 and the STROBE checklist for the reporting of observational studies. 24
Ethics and funding
An independent ethics committee approved the study. According to the French legislation, no written consent was needed for purely observational studies and only non-opposition was sought either by an information document at discharge or by mail. The Normandy district and the “Paul Bennetot Fondation de l’Avenir,” a private foundation, funded the study. They had no role in the design and conduct of the study, collection, management, analysis, and interpretation of the data, preparation, review, or approval of the manuscript.
Results
Time-based definition
During the study period, 567 events (549 patients, 273 males [48.1%], mean ± SD age 73.3 ± 14.4 years) met the time-based criteria for TIA (Figure 1). Four hundred and forty patients (77.6%) had a first CVE and 127 (22.4%) had a recurrent event (77 had a previous stroke, 49 a previous TIA and 1 a previous retinal artery occlusion). The crude attack rate was 53.0 [95% CI: 48.8–57.8] per 100,000 person-years. The standardized attack rate was 54.8 [95% CI: 50.4–59.6] per 100,000 person-years (Figure 2(a); Supplemental data Table 1). The crude incidence rate was 41.2 [37.4–45.2] per 100,000 persons-years. The standardized incidence rate was 42.9 [38.9–47.1] per 100,000 person-years (Figure 2(b); Supplemental data Table 2).
Figure 1.
Flow chart.
Figure 2.
Epidemiology of transient ischemic attack by age and TIA definition. (a) Attack rates (all TIA). (b) Incidence rate (first ever cerebrovascular event).
As shown in Table 1, patients with a first ever CVE were significantly younger than those with a recurrent event. The ABCD2 score was available in 468 patients (85.2%). A majority of patients (n = 406, 86.7%) had an ABCD2 score between 3 and 7, with no differences between incident and recurrent TIAs. Patients with a recurrent TIA had a higher prevalence of hypertension, dyslipidemia, atrial fibrillation, and were more likely to be on antiplatelet drugs or anticoagulants.
Table 1.
Comparison of first in the study TIAs with or without a history of ischemic cerebrovascular event.
| Variable | All patients N = 549 | First event N = 440 | Recurrent event N = 109 | OR [95% CI] or p value |
|---|---|---|---|---|
| Demographics | ||||
| Age, mean (SD) | 73.1 (14.5) | 71.8 (14.8) | 77.9 (11.8) | p < 0.001 |
| Male sex* | 267 (48.6) | 218 (49.5) | 49 (45.0) | 0.8 [0.5–1.3] |
| Vascular risk factors | ||||
| Hypertension (n = 547) | 355 (64.9) | 264 (60.2) | 91 (83.4) | 3.3 [2.0–5.8] |
| Dyslipidemia (n = 547) | 275 (50.3) | 201 (45.9) | 74 (67.9) | 2.5 [1.6–3.9] |
| Active smoking (n = 467) | 82 (17.6) | 69 (18.4) | 13 (14.1) | 0.7 [0.4–1.4] |
| Diabetes (n = 547) | 100 (18.3) | 76 (17.3) | 24 (22.0) | 1.3 [0.8–2.2] |
| Atrial fibrillation (n = 546) | 89 (16.3) | 62 (14.1) | 27 (24.8) | 2.0 [1.2–3.3] |
| Coronary artery disease (n = 546) | 69 (12.6) | 50 (11.4) | 19 (17.6) | 1.6 [0.9–2.9] |
| Peripheral artery disease (n = 546) | 27 (4.9) | 20 (4.6) | 7 (6.4) | 1.5 [0.6–3.4] |
| Pre-TIA medications | ||||
| Antiplatelet drug (n = 538) | 175 (32.5) | 106 (24.5) | 69 (65.1) | 5.7 [3.6–9.1] |
| Anticoagulant (n = 538) | 72 (13.4) | 47 (11.0) | 25 (23.5) | 2.5 [1.5–4.3] |
| TIA characteristics and management | ||||
| ABCD2 score (n = 468) | ||||
| 0–2 | 62 (13.2) | 52 (13.9) | 10 (10.6) | p = 0.32 |
| 3–4 | 213 (45.5) | 174 (46.5) | 39 (41.5) | |
| 5–7 | 193 (41.2) | 148 (39.6) | 45 (47.9) | |
| MRI | 445 (81.4) | 354 (80.4) | 91 (83.4) | 1.2 [0.7–2.2] |
| Acute infarct | 134 (24.4) | 108 (24.5) | 26 (23.9) | 1.0 [0.6–1.6] |
| Management | ||||
| Stroke unit | 308 (56.1) | 249 (56.6) | 59 (54.1) | p = 0.92 |
| Other hospital department | 124 (22.6) | 97 (22.0) | 27 (24.8) | |
| Emergency room only | 89 (16.2) | 72 (16.4) | 17 (15.6) | |
| Ambulatory care only | 28 (5.1) | 22 (5.0) | 6 (5.5) | |
| Recurrent stroke and death at 90 days | ||||
| Death at 90 days | 11 (2.0) | 8 (1.8) | 3 (2.8) | 1.4 [0.5–3.7]** |
| Recurrent stroke at 90 days | 14 (2.7) | 10 (2.6) | 4 (4.0) | 1.7 [0.2–2.0]** |
n (%) otherwise indicated.
Hazard Ratio.
Tissue-based definition
Among the 567 TIA cases, 546 of all TIA cases (96.2%) had a brain imaging, consisting of MRI in 457 (80.6%) and CT-only in 89 (16.0%). The median (IQR) time between TIA onset and MRI was 1 (0–2) day. Amongst patients with a first in study TIA, those without a brain MRI were significantly older, more likely to have hypertension, to not be managed in a stroke unit, to be on an anticoagulant, to have atrial fibrillation, and to have aphasia at TIA onset (Supplemental data Table 3).
An acute brain infarct was present in 136 (24.5%) TIA cases: 129 on brain MRI (positivity rate: 28.2%) and 7 in TIA cases with only brain CT-scan (positivity rate: 7.8%). Among the 410 (72.3%) TIA cases meeting the tissue-based definition of TIA (181 [44.1%] occurred in males), 317 (55.9%) were a first ever CVE.
The attack rate of tissue-based definition of TIA was 38.4 per 100,000 persons-years [34.7–42.3] (Figure 2(a), Supplemental data Table 4) and the incidence rate of TIA was 29.7 [26.5–33.1] per 100,000 person-years (Figure 2(b), Supplemental data Table 5). After standardization, the attack rate was 39.5 per 100,000 persons-years [35.7–43.5] and the incidence rate was 30.6 [27.3–34.2] per 100,000 person-years. Incidence and attack rates increased by age category regardless of sex or the tissue- versus time-based definition of TIA.
Among patients with a first TIA during the study period who had a MRI (n = 445), those with an acute infarct (n = 127, 28.5%) were more likely to be male than those without an acute infarct. Clinically, both groups had a similar duration of TIA, but those with an acute infarct had a higher proportion of motor symptoms (Table 2).
Table 2.
Factors associated with an acute infarct on brain MRI amongst patients with a first in study TIA.
| Variable | All patients n = 445 | Acute infarct n = 127 | No acute infarct n = 318 | Odds ratio [95% CI] or p value |
|---|---|---|---|---|
| Demographics | ||||
| Age, mean (SD) | 71.8 (14.2) | 72.0 (13.6) | 71.7 (14.5) | p = 0.8 |
| Male* | 222 (49.9) | 78 (61.4) | 144 (45.2) | 1.9 [1.3–3.0] |
| Vascular risk factors | ||||
| High blood pressure | 280 (62.9) | 81 (63.7) | 199 (62.5) | 1.1 [0.7–1.6] |
| Dyslipidemia | 221 (49.7) | 73 (58.6) | 148 (46.5) | 1.6 [1.0–2.3] |
| Active smoking (n = 409) | 72 (17.6) | 20 (17.1) | 52 (17.8) | 1.0 [0.5–1.7] |
| Diabetes | 85 (19.1) | 22 (16.3) | 63 (20.1) | 0.8 [0.5–1.5] |
| Atrial fibrillation | 65 (14.6) | 23 (19.8) | 42 (12.8) | 1.5 [0.8–2.5] |
| Coronary artery disease | 54 (12.1) | 19 (15.8) | 35 (10.6) | 1.4 [0.8–2.6] |
| Peripheral artery disease | 18 (4.0) | 5 (3.4) | 13 (4.3) | 1.0 [0.4–3.3] |
| Pre-TIA medications | ||||
| Antiplatelet drug (n = 444) | 152 (34.2) | 51 (40.4) | 101 (318) | 1.6 [1.0–2.5] |
| Anticoagulant | 49 (11.0) | 13 (11.3) | 36 (10.9) | 1.1 [0.6–2.3] |
| TIA characteristics and management | ||||
| TIA duration (min) (n = 415) | ||||
| <10 | 72 (17.3) | 23 (19.7) | 49 (16.4) | |
| 11–60 | 223 (53.7) | 53 (45.3) | 170 (57.0) | 0.1 |
| >60 | 120 (28.9) | 41 (35.0) | 79 (26.5) | |
| Aphasia (n = 440) | 157 (35.7) | 35 (27.8) | 122 (38.9) | 0.6 [0.4–0.9] |
| Motor symptoms (n = 443) | 199 (44.9) | 71 (56.3) | 128 (40.3) | 1.9 [1.3–2.9] |
| Recurrent stroke and death at 90 days | ||||
| Death at 90 days | 8 (1.8) | 0 (0.0) | 8 (2.5) | – |
| Recurrent stroke at 3 months | 10 (2.3) | 4 (3.2) | 6 (1.9) | 1.4 [0.6–4.6]** |
n(%) otherwise indicated.
Hazard ratio.
TIA management and prognosis
Among patients with a first in study TIA (time-based definition), 308 (56.1%) were managed in a stroke unit, 124 (22.5%) were hospitalized in another department, 89 (16.3%) were evaluated in an emergency department only and 28 (5.1%) were treated exclusively in an ambulatory setting. Direct or indirect information on stroke recurrence at 90 days was obtained in 514 (93.6%) patients. A recurrent stroke at 90 days was observed in 14 patients (2.7% [1.1–4.0]). We identified all recurrent strokes through the Normandy Stroke registry. The systematic screening of the records of from the medical centers of the area and calls to the referent GP in case of remaining missing data, did not identify other new recurrent strokes.
Eleven patients (2.0% [1.0–3.7]) were dead 90 days after the index event. The 90-day risk of death or stroke did not vary according to whether the TIA was incident or recurrent, nor according to the lesion status (Table 2).
Projecting data
By projecting the attack rates observed on our territory on the French population, the estimated number of TIAs in France is currently 39,391 and according to national demographic forecasts should increase to 48,908 in 2035 and around 54,875 by 2050 (Supplemental data Table 7).
Discussion
To our knowledge, our study is the first to investigate the impact of the tissue-based definition of TIA in a population-based cohort with such a high brain MRI rate. The use of the tissue-based definition of TIA reduces age-standardized attack and incidence rates by about 27.5% compared with the traditional time-based definition. The reduction in attack rates was overall similar for patients over and under 65 years of age. However, our study shows a slightly greater reduction rate in men (34%) than in women (22%). If true, this gender-effect remains to be confirmed in future study as it may have important clinical implications insofar as it induces gender bias in trials depending on the selected definition of TIA. Comparison of rates according to the two definitions may be biased by our choice to include patients with isolated diplopia, vertigo, dysarthria, or balance disorders with ischemic lesions on DWI, although with similar symptoms without lesion were excluded. However, given that only 9 events (1.6%) in the cohort met this definition, the impact on our results is negligible.
The incidence and attack rates of TIA (time-based definition) observed in our population-based study were in the range of rates found in other comparable studies10–16 (Supplemental data Table 6). As in all epidemiological studies of TIA, the incidence increased with age, reaching a maximum in patients over 85 years of age. The increase in incidence with age was found in both sexes regardless of the TIA definition.
Nevertheless, there is important heterogeneity across previous studies, with incidence rates ranging from 7.312 to 73.613 per 100,000 person-years. This heterogeneity can be explained not only by differences in populations and health care systems but also by varying strategies used for case detection and case definition.
The impact of using the tissue-based definition on the incidence of TIA has been estimated in one previous study, which had a lower incidence of TIA than in our study. 15 When using the tissue-based definition, the authors reported that the incidence of TIA decreased by 18.8%. We observed a similar effect, even though the rate of brain MRI was higher in our study (80%) than in this previous study (15%). The proportion of patients with an acute infarct on DWI observed in our study (28.5%) was lower than the pooled positivity rate (34.1%) of a 2017 meta-analysis of 47 hospital-based studies, 25 which identified high inter-study heterogeneity. However, in this meta-analysis, the pooled rate of acute infarcts on DWI amongst studies that included more than 200 TIAs was 29.1%, which is more concordant with our results.
With exception of the higher proportion of motor symptoms, we did not replicate the classical factors associated with the presence of an acute infarct on DWI in the literature.6,26,27 In particular, symptoms lasting more than 1 h, aphasia or a history of atrial fibrillation were not significantly associated with a higher proportion of acute infarcts on MRI in our study, which may be explained by a lack of power. A major finding from our study is the low proportion of recurrent ischemic stroke at 90 days (2.7% [1.1–4.0]),8,28 although 86.7% of TIA cases had an ABCD2 score >2 and only 55.6% of patients were managed in a stroke unit. The most likely explanation is improvement in management of acute TIAs in our area. Indeed, even if not all patients benefited from hospitalization in a stroke unit, almost all patients benefited from a vascular neurology assessment since a neurologist is on call 24/7. Moreover, among the 25% of patients hospitalized outside of the stroke unit, many were hospitalized in the neurology department a large proportion of patients, hospitalized or not benefited from a specialized vascular neurology visit within 3 months of the event. Similar low recurrence rates have been found in recent hospital-based cohorts and our results are therefore consistent with the data in the literature,29,30 which may be explained by better management of the risk factors for recurrence.
The 90-day ischemic stroke rate as well as the 90-day risks of death were similar in patients with an acute infarct compared with lesion-free patients, regardless of whether we considered only the TIAs with MRI or the entire cohort of TIAs, which is in line with previous population-based study. 31
The strength of this study is to provide epidemiological data on TIAs in a population-based study with a high rate of MRI and a more modern definition of TIA, more in line with current clinical practice. This study highlights the current importance of using both definitions as much as possible to ensure comparability with previous epidemiological studies and to ensure better clinical translatability. Finally, this study emphasizes that the absence of an acute infarct on imaging should not lead to considering TIAs as less at-risk for recurrence because the prognosis at 90 days was similar irrespective of the presence of an acute infarct. However, the major weaknesses of this work are that it was underpowered to study factors associated with recurrence because of the small number of recurrent events and the generalizability is limited due to the monocentric design.
Despite the low recurrence rate, the presence of high attack rates for TIA in the oldest patients suggests that TIA will represent a growing epidemiological burden. Indeed, the projections made in our study suggest that the number of TIAs in France is set to rise by around 25% between now and 2050. This underlines the importance in France, as in many countries with aging populations, of developing public health policies aimed at implementing specialized structures for the management of TIA.
Supplemental Material
Supplemental material, sj-docx-1-eso-10.1177_23969873241251722 for Epidemiology of transient ischemic attack in the normandy stroke population-based study by Romain Schneckenburger, Marion Boulanger, Ahmad Nehme, Marguerite Watrin, Gwendoline Le Du, Sophie Guettier, Lydia Guittet and Emmanuel Touzé in European Stroke Journal
Acknowledgments
The Normandy Stroke team, Normandy administrative district (https://www.normandie.fr/), Fondation de l’Avenir Matmut Paul Bennetot.
Footnotes
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The Normandy Stroke Study is funded by the Normandy administrative region and a private foundation (Fondation Matmut Paul Bennetot).
Ethical approval: Ethical approval for this study was obtained from the CPP Nord Ouest 1, ID : 2017-A00050-53.
Informed consent: Informed consent was not sought for the present study because according to the French legislation, no written consent is needed for purely observational studies. Only non-opposition was sought either by an information document at discharge or by mail.
Author contributions: RS and ET conceived the study. AN, MW, GD, LG, and SG were involved in protocol development, gaining ethical approval, patient recruitment, and data analysis. RS wrote the first draft of the manuscript. All authors reviewed and edited the manuscript and approved the final version of the manuscript.
Guarantor: Dr. Romain Schneckenburger.
ORCID iD: Romain Schneckenburger 
https://orcid.org/0000-0002-9018-7037
Supplemental material: Supplemental material for this article is available online.
References
- 1. Lovett JK, Dennis MS, Sandercock PA, et al. Very early risk of stroke after a first transient ischemic attack. Stroke 2003; 34: 138–140. [DOI] [PubMed] [Google Scholar]
- 2. World Health Organization. Cerebrovascular diseases: prevention, treatment, and rehabilitation, report of a WHO meeting [held in Monaco from 25 to 29 May 1970]. Geneva, Switzerland: World Health Organization, https://apps.who.int/iris/handle/10665/40898 (1971, accessed 1 May 2024). [PubMed] [Google Scholar]
- 3. Albers GW, Caplan LR, Easton JD, et al. Transient ischemic attack—proposal for a new definition. N Engl J Med 2002; 347: 1713–1716. [DOI] [PubMed] [Google Scholar]
- 4. Sacco RL, Kasner SE, Broderick JP, et al. An updated definition of stroke for the 21st century: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2013; 44: 2064–2089. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Easton JD, Saver JL, Albers GW, et al. Definition and evaluation of transient ischemic attack: a scientific statement for healthcare professionals from the American Heart Association/American Stroke. Stroke 2009; 40: 2276–2293. [DOI] [PubMed] [Google Scholar]
- 6. Moreau F, Asdaghi N, Modi J, et al. Magnetic resonance imaging versus computed tomography in transient ischemic attack and minor stroke: the more you see the more you know. Cerebrovasc Dis Extra 2013; 3:130–136. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Coull AJ, Lovett JK, Rothwell PM, et al. Population based study of early risk of stroke after transient ischaemic attack or minor stroke: implications for public education and organisation of services. BMJ 2004; 328: 326. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Shahjouei S, Sadighi A, Chaudhary D, et al. A 5-decade analysis of incidence trends of ischemic stroke after transient ischemic attack: a systematic review and meta-analysis. JAMA Neurol 2021; 78: 77–87. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Amarenco P, Lavallée PC, Monteiro Tavares L, et al. Five-year risk of stroke after TIA or minor ischemic stroke. N Engl J Med 2018; 378: 2182–2190. [DOI] [PubMed] [Google Scholar]
- 10. Béjot Y, Brenière C, Graber M, et al. Contemporary epidemiology of transient ischemic attack in Dijon, France (2013–2015). Neuroepidemiology 2017; 49: 135–141. [DOI] [PubMed] [Google Scholar]
- 11. Barber PA, Krishnamurthi R, Parag V, et al. Incidence of transient ischemic attack in Auckland, New Zealand, in 2011 to 2012. Stroke 2016; 47: 2183–2188. [DOI] [PubMed] [Google Scholar]
- 12. Fonseca PG, Weiss PA, Harger R, et al. Transient ischemic attack incidence in Joinville, Brazil, 2010: a population-based study. Stroke 2012; 43: 1159–1162. [DOI] [PubMed] [Google Scholar]
- 13. Felgueiras R, Magalhães R, Silva MR, et al. Transient ischemic attack: incidence and early risk of stroke in northern Portugal from 1998–2000 to 2009–2011. Int J Stroke 2020; 15: 278–288. [DOI] [PubMed] [Google Scholar]
- 14. Bahit MC, Coppola ML, Riccio PM, et al. First-ever stroke and transient ischemic attack incidence and 30-day case-fatality rates in a population-based study in Argentina. Stroke 2016; 47: 1640–1642. [DOI] [PubMed] [Google Scholar]
- 15. Lioutas VA, Ivan CS, Himali JJ, et al. Incidence of transient ischemic attack and association with long-term risk of stroke. JAMA 2021; 325: 373–381. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Degan D, Ornello R, Tiseo C, et al. Epidemiology of transient ischemic attacks using time- or tissue-based definitions: a population-based study. Stroke 2017; 48: 530–536. [DOI] [PubMed] [Google Scholar]
- 17. Schneckenburger R, Boulanger M, Watrin M, et al. Incidence and outcomes of acute cerebrovascular events: methodology of the population-based Normandy Stroke Study. Neuroepidemiology 2023; 57: 112–120. [DOI] [PubMed] [Google Scholar]
- 18. Sudlow CL, Warlow CP. Comparing stroke incidence worldwide: what makes studies comparable? Stroke 1996; 27: 550–558. [DOI] [PubMed] [Google Scholar]
- 19. Feigin V, Norrving B, Sudlow CLM, et al. Updated criteria for population-based stroke and transient ischemic attack incidence studies for the 21st century. Stroke 2018; 49: 2248–2255. [DOI] [PubMed] [Google Scholar]
- 20. Feigin VL, Carter K. Editorial comment-Stroke incidence studies one step closer to the elusive gold standard? Stroke 2004; 35: 2045–2047. [PubMed] [Google Scholar]
- 21. Rothwell PM, Giles MF, Flossmann E, et al. A simple score (ABCD) to identify individuals at high early risk of stroke after transient ischaemic attack. Lancet 2005; 366: 29–36. [DOI] [PubMed] [Google Scholar]
- 22. Pace M, Cayotte E, Agafitei L, et al. Revision of the European standard population–report of Eurostat’s task force-2013 edition. Luxembourg: Publications Office, 2013. [Google Scholar]
- 23. Bennett D, Brayne C, Feigin V, et al. Development of the standards of reporting of neurological disorders (STROND) checklist: a guideline for the reporting of incidence and prevalence studies in neuroepidemiology. Eur J Epidemiol 2015; 30: 569–576. [DOI] [PubMed] [Google Scholar]
- 24. Knottnerus A, Tugwell P. STROBE—a checklist to strengthen the reporting of observational studies in epidemiology. J Clin Epidemiol 2008; 61: 323. [DOI] [PubMed] [Google Scholar]
- 25. Brazzelli M, Chappell FM, Miranda H, et al. Diffusion-weighted imaging and diagnosis of transient ischemic attack. Ann Neurol 2014; 75: 67–76. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Calvet D, Touzé E, Oppenheim C, et al. DWI lesions and TIA etiology improve the prediction of stroke after TIA. Stroke 2009; 40: 187–192. [DOI] [PubMed] [Google Scholar]
- 27. Coutts SB, Moreau F, Asdaghi N, et al. Rate and prognosis of brain ischemia in patients with lower-risk transient or persistent minor neurologic events. JAMA Neurol 2019; 76: 1439–1445. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Shahjouei S, Li J, Koza E, et al. Risk of subsequent stroke among patients receiving outpatient vs inpatient care for transient ischemic attack: a systematic review and meta-analysis. JAMA Netw Open 2022; 5: e2136644. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. Sundararajan V, Thrift AG, Phan TG, et al. Trends over time in the risk of stroke after an incident transient ischemic attack. Stroke 2014; 45: 3214–3218. [DOI] [PubMed] [Google Scholar]
- 30. Appelros P, Háls Berglund M, Ström JO. Long-term risk of stroke after transient ischemic attack. Cerebrovasc Dis 2017; 43: 25–30. [DOI] [PubMed] [Google Scholar]
- 31. Hurford R, Li L, Lovett N, et al. Oxford Vascular Study. Prognostic value of “tissue-based” definitions of TIA and minor stroke: Population-based study. Neurology 2019; 92: e2455–e2461. [DOI] [PMC free article] [PubMed] [Google Scholar]
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Supplementary Materials
Supplemental material, sj-docx-1-eso-10.1177_23969873241251722 for Epidemiology of transient ischemic attack in the normandy stroke population-based study by Romain Schneckenburger, Marion Boulanger, Ahmad Nehme, Marguerite Watrin, Gwendoline Le Du, Sophie Guettier, Lydia Guittet and Emmanuel Touzé in European Stroke Journal