Elderly Women Have Lower Rates of Stroke,
Cardiovascular Events, and Mortality After Hospitalization
for Transient Ischemic Attack
Judith H. Lichtman, PhD; Sara B. Jones, MPH; Emi Watanabe, MPH; Norrina B. Allen, MPH;
Yun Wang, PhD; Virginia J. Howard, PhD; Larry B. Goldstein, MD
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
Background and Purpose—Patients with transient ischemic attack (TIA) are at increased risk for stroke, cardiovascular
events, and death, yet little is known about whether these risks differ for men and women. We determined whether there
are sex-based differences in these outcomes 30 days and 1 year after TIA using a national sample of elderly patients.
Methods—Rates of 30-day and 1-year hospitalization for TIA (International Classification of Diseases, 9th Revision Code
435), stroke (International Classification of Diseases, 9th Revision Codes 433, 434, and 436), coronary artery disease
(International Classification of Diseases, 9th Revision Codes 410 to 414), all-cause readmission, and mortality were
determined for fee-for-service Medicare patients ⱖ65 years of age discharged with a TIA in 2002. Cox proportional
hazards models and random-effects logistic models compared outcomes with risk adjustment for demographics, medical
history, comorbidities, and prior hospitalizations.
Results—The study included 122 063 TIA hospitalizations (mean age, 79.0⫾7.6 years; 62% women; 86% white). Men
were younger but had higher rates of cardiac comorbidities than women. Women had lower unadjusted rates of stroke,
coronary artery disease, and mortality at 30 days and 1 year after TIA admission. These relationships persisted in
risk-adjusted analyses at 30 days for stroke (hazard ratio, 0.70; 95% CI, 0.64 to 0.77), coronary artery disease (hazard
ratio, 0.86; 0.74 to 1.00), and mortality (odds ratio, 0.74; 0.68 to 0.82) as well as at 1 year for stroke (hazard ratio, 0.85;
0.81 to 0.89), coronary artery disease (hazard ratio, 0.81; 0.77 to 0.86), and mortality (odds ratio, 0.78; 0.75 to 0.81).
Conclusion—These data suggest that women have a better prognosis than men within the first year after hospital
discharge for a TIA. Additional research is needed to identify factors that may explain these sex-related differences
in outcomes. (Stroke. 2009;40:2116-2122.)
Key Words: sex 䡲 transient ischemic attack (TIA) outcome
S
mortality within the first year after TIA. Findings from
studies that examined potential sex-related differences in
outcomes after TIA are inconsistent.4,6 – 8,15–21 Some report a
lower unadjusted 7-day stroke risk for women as well as
reduced risk-adjusted long-term rates of stroke, death, and the
composite outcome of stroke, myocardial infarction, or
death.7,15,20 Others report no sex-related differences in unadjusted4,17–19,21 or risk-adjusted8,16 analyses of stroke and
cardiac risk. Many of these studies combined TIA and stroke
in the index cohort and in the assessment of outcomes,7,15,16
were conducted in European populations,7,15,17,19 –21 used
clinical trial cohorts,7,15 or were restricted to specific US
geographic areas.4,8,16,18 Thus, only limited information is
available reflecting both early and long-term prognosis after
TIA in a US national cohort of elderly patients. In the present
study, we compared 30-day and 1-year outcomes for elderly
troke is the third leading cause of death in the United
States and a leading cause of disability. Because of their
longer lifespan, women have a higher stroke burden than
men, accounting for 61% of all stroke deaths in 2004.1
Transient ischemic attack (TIA) precedes approximately 15%
to 23% of strokes2,3 and carries a 90-day stroke risk of 9% to
17%.2 In addition to stroke, patients with TIA are also at
increased risk for recurrent TIA, coronary artery disease, and
death.3–7 With an estimated 240 000 TIAs diagnosed annually
in the United States,8 TIA represents an important target for
secondary stroke prevention and is an indicator of a patient’s
risk for myocardial infarction and vascular death.9 –13 Rapid
evaluation and treatment of patients with TIA can reduce
subsequent morbidity.5,14
Relatively little is known about whether elderly women
and men have comparable risks for recurrent events and
Received November 14, 2008; final revision received December 30, 2008; accepted January 16, 2009.
From the Section of Chronic Disease Epidemiology (J.H.L., S.B.J., E.W., N.B.A., Y.W.), Department of Epidemiology and Public Health, Yale
University School of Medicine, New Haven, Conn; the Department of Epidemiology (V.J.H.), School of Public Health, University of Alabama at
Birmingham, Birmingham, Ala; and the Department of Medicine (Neurology; L.B.G.), Duke Stroke Center, Center for Clinical Health Policy Research,
Duke University and Durham VAMC, Durham, NC.
Correspondence to Judith H. Lichtman, PhD, Yale University School of Medicine, PO Box 208034, New Haven, CT 06520-8034. E-mail
[email protected]
© 2009 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org
DOI: 10.1161/STROKEAHA.108.543009
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Lichtman et al
women and men after hospital discharge for TIA in a US
national cohort. Outcomes included hospitalization for recurrent TIA, stroke, cardiovascular events, all-cause rehospitalization, and mortality.
Methods
The study population included all fee-for-service Medicare beneficiaries ⱖ65 years hospitalized with a primary discharge diagnosis of
TIA from January 1, 2002, through December 31, 2002, who were
identified based on the International Classification of Diseases,
Ninth Revision, Clinical Modification (ICD-9-CM 435.x). Data were
obtained from the Medicare Provider Analysis and Review files that
included demographic information, primary and secondary discharge
diagnosis codes, and procedure codes for each hospitalization. We
excluded patients who were ⬍65 years of age, discharged from
nonacute care facilities, or transferred from another facility. We
further limited the cohort to patients with at least 12 months of
continuous fee-for-service status before the index TIA hospitalization to allow assessment of comorbid conditions.
Rehospitalization rates at 30 days and 1 year after the index TIA
hospital discharge were determined for recurrent TIA (ICD-9 435),
ischemic stroke (ICD-9 433, 434, 436), coronary artery disease
(CAD; ICD-9 410 to 414), and all-cause readmission. Mortality at 30
days and 1 year was obtained from the Medicare Enrollment
Database. The accuracy of ascertainment of vital status using these
data resources is high for this age group.22 Length of stay was
determined for each index hospitalization and discharge disposition
was categorized as home, skilled nursing facility, or other location.
Characteristics of Medicare Beneficiaries Hospitalized for TIA
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Age, years, mean⫾SD
65–74
Total (N⫽122 063), %
Women (N⫽76 108), %
Men (N⫽45 955), %
P Value*
79.0⫾7.6
79.7⫾7.7
77.8⫾7.3
⬍0.0001
30.2
27.1
35.4
⬍0.0001
75–84
44.8
44.3
45.6
85⫹
25.0
28.6
19.0
85.7
85.0
86.9
⬍0.0001
Race
White
Black
9.8
10.6
8.5
Other
2.4
2.3
2.4
Hispanic
2.2
2.1
2.2
⬍0.0001
Source of admission
Emergency department
78.6
78.3
Skilled nursing facility
0.7
0.8
0.5
20.7
20.9
20.4
Hospitalizations in past year ⱖ2
15.6
16.0
14.8
⬍0.0001
Deyo score ⱖ3
16.4
15.1
18.6
⬍0.0001
Other
79.1
Medical history and comorbidity
Cancer
2.5
1.8
3.6
⬍0.0001
Dementia
9.9
10.6
8.8
⬍0.0001
Chronic obstructive pulmonary disease
18.4
16.9
20.9
⬍0.0001
Ischemic stroke
11.4
11.6
11.2
0.0697
Diabetes
26.5
25.6
27.9
⬍0.0001
Smoking
6.2
4.8
8.6
⬍0.0001
65.4
68.6
60.2
⬍0.0001
9.2
7.5
12.1
⬍0.0001
Congestive heart failure
10.3
10.6
9.9
⬍0.0001
Atrial fibrillation
15.8
15.2
16.9
⬍0.0001
Prior coronary artery bypass graft
7.3
4.3
12.2
⬍0.0001
Prior percutaneous transluminal coronary
angioplasty
2.7
2.1
3.7
⬍0.0001
Home
70.6
68.0
74.9
Skilled nursing facility
13.5
15.3
10.6
0.3
0.2
0.3
Hypertension
Acute myocardial infarction
⬍0.0001
Discharge disposition
In-hospital death
Other
Length of stay, days, mean⫾SD†
2117
Outcomes
Study Population
Table 1.
Women Have Lower Event Rates After TIA
15.6
16.5
14.3
3.4⫾2.6
3.5⫾2.6
3.3⫾2.6
⬍0.0001
*P value is for difference between men and women using t tests for continuous variables and ␹2 statistics for categorical variables.
†Excludes 2174 patients due to in-hospital death, transfer to another acute care facility, and length of stay ⬎61 days.
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June 2009
Table 2.
Rates of Readmission and Mortality After Hospitalization for TIA
30-Day
1-Year
Total
(N⫽122 063), %
Women
(N⫽76 108), %
Men
(N⫽45 955), %
10.6
10.6
10.6
1.1
1.1
1.1
Total
(N⫽122 063), %
Women
(N⫽76 108), %
Men
(N⫽45 955), %
0.7740
48.3
48.8
47.6
0.0002
0.8636
5.2
5.3
4.9
⬍0.0001
P Value*
P Value*
Readmission†
All-cause
Recurrent TIA
Stroke
1.5
1.3
1.8
⬍0.0001
6.3
5.9
6.9
⬍0.0001
CAD
0.6
0.5
0.7
0.0010
5.0
4.5
5.8
⬍0.0001
Mortality
1.5
1.4
1.8
⬍0.0001
13.6
12.9
14.7
⬍0.0001
*P value is for difference between men and women using ␹ statistics.
†Censored for 2064 patients due to hospital transfers and in-hospital deaths.
2
Covariates
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Comorbidities were identified from Medicare Provider Analysis and
Review files in the year before the index hospitalization to avoid
misclassifying pre-existing conditions as complications. Demographic characteristics included age, sex, and race. Medical history
included previous diagnosis of cancer, dementia, chronic obstructive
pulmonary disease, ischemic stroke, diabetes, smoking status, hypertension, acute myocardial infarction, congestive heart failure, atrial
fibrillation, prior receipt of coronary artery bypass graft surgery or
percutaneous transluminal coronary angioplasty, Deyo score for
comorbidities (ⱖ3),23 and number of hospitalizations in the year
before the index TIA (dichotomized as ⬍2 or ⱖ2).
Statistical Analysis
Bivariate analyses were conducted to compare patient characteristics
by sex using t tests for continuous variables and ␹2 statistics for
categorical variables. Readmission rates were compared using Cox
proportional hazards models with censoring for deaths. Randomeffects logistic models were used to compare 30-day and 1-year
mortality from admission by sex taking into account the correlation
among patients treated at the same hospital. Models were adjusted
for demographics, medical history, comorbidities, and prior hospital
events. Risk-adjusted survival curves were used to illustrate the
timing of follow-up events by sex. All analyses were conducted
using SAS Version 9.1.3 (SAS Institute Inc, Cary, NC).
Results
The final study cohort included 122 063 patients (mean age,
79.0⫾7.6 years; 86% white) with a discharge code of TIA in
2002 (Table 1) . Women represented 62% of TIA cases and
were more likely to be older (mean age, 79.7⫾7.7 versus
77.8⫾7.3) and of black race (P⬍0.0001 for each). Women
were more likely to have been hospitalized 2 or more times in
the prior year but less likely to have 3 or more comorbidities
using the Deyo score. They had lower rates of cancer, chronic
obstructive pulmonary disease, and diabetes, but higher rates
of hypertension and congestive heart failure (P⬍0.0001 for
each). Men had a higher prevalence of cardiovascular risk
factors, including diabetes and smoking history as well as
prior acute myocardial infarction and cardiovascular procedures, than women. Discharge disposition varied by sex with
a higher percentage of women discharged to skilled nursing
facilities or other location and a greater percentage of men
discharged home (P⬍0.0001).
Unadjusted 30-day readmission rates were similar for
women and men for all-cause readmission (10.6% versus
10.6%) and recurrent TIA (1.1% versus 1.1%), but women
Figure 1. Risk-adjusted readmission and
mortality, women compared with men.
Lichtman et al
Women Have Lower Event Rates After TIA
2119
Figure 2. Risk-adjusted 365-day survival
curves of all-cause hospital readmission.
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had lower rates of stroke (1.3% versus 1.8%; P⬍0.0001) and
CAD hospitalizations (0.5% versus 0.7%; P⬍0.0001; Table 2).
At 1 year, women had higher rates of all-cause readmission
(48.8% versus 47.6%; P⫽0.0002) and TIA (5.3% versus
4.9%; P⬍0.0001) but lower readmission rates for stroke
(5.9% versus 6.9%; P⬍0.0001) and CAD (4.5% versus 5.8%;
P⬍0.0001). Mortality rates were lower for women at 30 days
(1.4% versus 1.8%; P⬍0.0001) and 1 year (12.9% versus
14.7%; P⬍0.0001) as compared with men.
In risk-adjusted analyses, there were no sex-related differences in all-cause readmission (hazards ratio [HR], 1.00; 95%
CI, 0.97 to 1.04) or hospitalizations for TIA (HR, 1.01; CI,
0.90 to 1.13), but women had a lower risk of stroke (HR,
0.70; CI, 0.64 to 0.77), CAD events (HR, 0.86; CI, 0.74 to
1.00), and death (OR, 0.74; 0.68 to 0.82) at 30 days (Figure
1). At 1 year, women had a slightly higher risk of recurrent
TIA relative to men (HR, 1.06; CI, 1.00 to 1.11; P⬍0.05) but
lower risk of stroke (HR, 0.85; CI, 0.81 to 0.89), CAD events
(HR, 0.81; CI, 0.77 to 0.86), and death (OR, 0.78; CI, 0.75 to
0.81). The risk of adverse events, including hospitalization
for TIA, stroke, cardiovascular events, all-cause readmission,
and mortality, in the first year after TIA in women and men
are shown in Figures 2 and 3. Men had a higher risk of
hospital admission for stroke, CAD, and death compared with
women throughout the 365-day period with increasing differences over time.
Discussion
Among elderly fee-for-service Medicare beneficiaries who
were hospitalized for a TIA, women had a lower risk of
subsequent hospitalization for major vascular events and
death within the first year as compared with men. Women
were 30% less likely to have a stroke, 14% less likely to have
a cardiac event, and 26% less likely to die within the first 30
days even after adjustment for comorbid conditions, including pre-existing coronary heart disease. Within 1 year,
women were 15% less likely to have a stroke, 19% less likely
to have a cardiac event, and 22% less likely to die. Women
had a marginally higher risk of recurrent TIA (6%) within 1
year, which was not evident within the first month.
Our findings are consistent with 2 European studies from
the Dutch TIA Trial, which included 3127 patients with TIA
or minor ischemic stroke.7,15 The first study reported an
increased combined risk of vascular death, stroke, or myocardial infarction for men (HR, 1.6; 95% CI, 1.3 to 2.0) and
a marginally higher risk of fatal or nonfatal stroke (HR, 1.3;
1.0 to 1.8) over an average 2.6-year follow-up.15 The second,
more recent study reported a higher 10-year risk of vascular
death, stroke, or myocardial infarction (HR, 1.38; 1.22 to
1.56) as well as fatal or nonfatal stroke (HR, 1.31; 1.07 to
1.59) for men.7 Our findings extend these results by providing
data on outcomes after TIA for recurrent TIA, stroke, and
other cardiovascular events as well as mortality using a more
contemporary, national population of elderly patients with
TIA in the United States.
Several studies reported no sex-related differences in
outcomes after TIA.4,8,16 –19,21 Many of these were based on
international populations,17,19,21 had relatively small samples,8,17–19,21 were not representative of the national elderly
population,4,8,16,18 combined TIA and mild stroke events,16
included patients ⬍65 years,4,8,17–19,21 and provided only
unadjusted rates by sex.4,17–19,21 Moreover, studies have
generally focused on stroke risk4,17–19,21 with few analyzing
cardiac risk16 or mortality8 after TIA. A study of Michigan
Medicare beneficiaries discharged with TIA or stroke found a
nonsignificant lower stroke risk (inclusive of TIA) for women
in adjusted analysis (HR, 0.83; 0.64 to 1.07).16 We found an
opposite risk profile for men and women; women had a lower
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June 2009
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Figure 3. Risk-adjusted 365-day survival curves for TIA, stroke, and coronary artery disease readmission, and mortality.
stroke risk but a slightly higher risk of recurrent TIA than
men. Some prior studies may have masked these sex effects
by combining TIA and stroke outcomes.
There are a number of plausible explanations for the
observed sex-based differences in outcomes after TIA. First,
they may be due to etiologic differences in TIA. Men may
have a higher proportion of TIAs caused by large artery
atherosclerosis, which is associated with greater stroke risk.6
Lower event rates among women could also be attributable to
differences in care-seeking behaviors, initial diagnostic evaluation, or in the receipt of and/or compliance with secondary
prevention measures. Studies of patients with TIA, however,
found no sex-related differences in recognition of TIA24 nor
were there differences in care-seeking behavior.25 It is unlikely that women receive more aggressive diagnostic evaluations. In fact, women receive comparable care or may be less
likely to receive acute therapies and discharge medications
than men.26 –30 Finally, women may be hospitalized more
often for conditions such as migraine that could potentially be
misclassified as a TIA. A study that validated a ICD-9 TIA
diagnosis with review by a neurologist, however, found that
fewer than 6% were attributable to these other causes,
although this was not analyzed by sex.4 Use of ICD-9 codes
for diagnosis of TIA is reasonably valid with positive
predictive values between 70% and 90%,31–34 but data are not
available to compare the validity of these codes by sex. Two
European studies evaluated the validity of international administrative data for diagnosis of ischemic stroke and did not
find a sex-based difference.33,34
In our sample, the overall 30-day stroke risk of 1.5% is
lower than cited in other studies,7,8,18,21,35–39 whereas our
estimate of 30-day mortality is more consistent with previous
work.7,18,21,38 There are no data directly comparable with our
study because we used national Medicare administrative data.
The relatively lower stroke rate could be due to demographic
differences of our cohort; Medicare patients are on average
older and consist of a higher percentage of women, who we
found to have lower short-term stroke risk after TIA. This
may also be due to our use of administrative discharge codes
for case selection and outcome ascertainment. The majority
of other studies used neurologist review to verify TIA cases,
identified events through patient follow-up interviews, and/or
included nonadmitted patients.7,8,18,21,35–39 For these reasons,
findings from our national study likely underestimate the true
risk in the community but accurately reflect the use of
hospital resources after hospital admission for TIA among
fee-for-service Medicare beneficiaries in the United States.
We found that the risk of recurrent stroke is almost 3 times
higher than the risk of cardiovascular events within the first
30 days after TIA, but the rates became roughly equivalent by
1 year. Similarly, Brown et al reported that an ischemic stroke
after a stroke or TIA is more common as the first recurrent
Lichtman et al
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event than an ischemic cardiac event.16 Other studies have
also found that cardiovascular events tend to rival stroke
events over longer periods of follow-up.3,7,40
The present study has a number of limitations. First,
assessment of comorbid conditions is dependent on the
accuracy of recorded secondary administrative codes, but we
would not expect sex-based differences in data coding. There
are additional unmeasured factors such as clinical data on
neurological symptoms, symptom duration, or etiology and
test results that are not part of the administrative record.
Medicare data does not contain information on medication
use; therefore, we are unable to address potential differences
in secondary stroke care by sex, although current research
indicates that women are not likely to receive more aggressive care than men.26 –29 The index TIA cases and vascular
outcomes were ascertained using ICD-9 codes and were
restricted to hospitalized events. Two population-based studies reported that 82% to 86% of TIA cases presented at the
emergency department,8,18 with 79% of these patients admitted to the hospital.8,18 Positive predictive values for the
selected codes for TIA, ischemic stroke, and CAD are
relatively high,41,42 and evidence suggests these do not vary
by sex.33,34
Patients hospitalized with TIA represent a high-risk population for stroke, cardiovascular events, and all-cause readmission. Almost one in 10 patients will be rehospitalized
within the first month, and half are rehospitalized within the
first year. Furthermore, women have better outcomes after
hospitalization for TIA than men, even after adjusting for
demographic and clinical factors. These short-term sex-based
differences persist for the first year after TIA. Our analysis
has the advantage of providing information about prognosis
after TIA based on a 100% national fee-for-service Medicare
population with a broad range of vascular outcomes. Further
investigation of the underlying causes for these sex-based
differences may help improve care and outcomes for both
men and women after TIA and will be critical in planning for
the future healthcare needs of these patients.
Women Have Lower Event Rates After TIA
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
Acknowledgments
The Centers for Medicare & Medicaid Services reviewed and
approved the use of its data for this work, and approved submission
of the manuscript; this approval is based on data use only, and does
not represent a Centers for Medicare & Medicaid Services endorsement of or comment on the manuscript content.
Source of Funding
The project described was supported by Grant R01NS043322 from
the National Institute of Neurological Disorders and Stroke. The
content is solely the responsibility of the authors and does not
necessarily represent the official views of the National Institute of
Neurological Disorders and Stroke or the National Institutes of
Health.
Disclosures
14.
15.
16.
None.
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Elderly Women Have Lower Rates of Stroke, Cardiovascular Events, and Mortality After
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Stroke. 2009;40:2116-2122; originally published online February 19, 2009;
doi: 10.1161/STROKEAHA.108.543009
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