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J Am Coll Cardiol, 2002; 39:625-631
© 2002 by the American College of Cardiology Foundation
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CLINICAL STUDY: STRESS TESTING

Prognostic value of exercise echocardiographyin 5,798 patients: is there a gender difference?

Adelaide M. Arruda-Olson, MD, PhD*, Eldyn M. Juracan, MD*, Douglas W. Mahoney, MS*, Robert B. McCully, MD, FACC*, Veronique L. Roger, MD, FACC* and Patricia A. Pellikka, MD, FACC*,*

* Division of Cardiovascular Diseases and Internal Medicine, Mayo Clinic and Mayo Foundation, Rochester, Minnesota, USA

Manuscript received May 31, 2001; revised manuscript received November 7, 2001, accepted November 29, 2001.

* Reprint requests and correspondence: Dr. Patricia A. Pellikka, Mayo Clinic, Division of Cardiovascular Diseases and Internal Medicine, 200 First Street SW, Rochester, Minnesota 55905, USA.
pellikka.patricia{at}mayo.edu


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 Conclusions
 References
 
OBJECTIVES: This study was designed to determine the effect of gender on the prognostic value of exercise echocardiography.

BACKGROUND: Limited information exists regarding gender differences in prognostic value of exercise echocardiography.

METHODS: We obtained follow-up (3.2 ± 1.7 years) in 5,798 consecutive patients who underwent exercise echocardiography for evaluation of known or suspected coronary artery disease.

RESULTS: There were 3,322 men (mean age 62 ± 12 years) and 2,476 women (mean age 62 ± 12 years) (p = 0.7). New or worsening wall motion abnormalities developed with exercise in 35% of men and 25% of women (p = 0.001). Cardiac events, including cardiac death (107 patients) and nonfatal myocardial infarction (148 patients), occurred in 5.3% of men and 3.1% of women (p = 0.001). Addition of the percentage of ischemic segments to the clinical and rest echocardiographic model provided incremental information in predicting cardiac events for both men (X2 = 137 to 143, p = 0.014) and women (X2 = 72 to 76, p = 0.046). By multivariate analysis, exercise electrocardiographic and exercise echocardiographic predictors of cardiac events in both men and women were workload and exercise wall motion score index. There was no significant interaction effect of rest echocardiography (p = 0.79), exercise electrocardiography (p = 0.38) or exercise echocardiography (p = 0.67) with gender.

CONCLUSIONS: Although cardiac events occurred more frequently in men, the incremental value of exercise echocardiography was comparable in both genders. Of all exercise electrocardiographic and exercise echocardiographic variables, workload and exercise wall motion score index had the strongest association with outcome. The results of exercise echocardiography have comparable implications in both men and women.

Abbreviations and Acronyms
  WMSI
  CAD
  coronary artery disease
  CI
  confidence interval
  ECG
  electrocardiogram
  METs
  metabolic equivalents
  MI
  myocardial infarction
  RR
  relative risk
  WMSI
  wall motion score index

Ischemic heart disease is the most common cause of death for American men and women (1). In women, the diagnosis of this disease by exercise electrocardiography is limited by lower accuracy when compared with men (2–5). The American College of Cardiology/American Heart Association exercise test guidelines (2) state that "the difficulties posed by clinical evaluation of women for possible coronary artery disease (CAD) have led to speculation that stress imaging approach may be an efficient initial alternative to exercise electrocardiography in women... ."

In women, the accuracy of exercise echocardiography is higher than the accuracy of exercise electrocardiography (6,7). However, lower sensitivity and higher specificity of exercise echocardiography in women compared with men has been reported (8). Because only a small percentage of patients undergoing clinically indicated exercise echocardiography are referred for coronary angiography, attempts to determine the true accuracy of the test are confounded by post-test referral bias. The usefulness of exercise echocardiography in women might be best established by studying its prognostic value.

The purposes of the present study were to determine if gender differences exist in the prognostic value of exercise echocardiography and to assess the incremental value of exercise echocardiography in predicting cardiac events in men and women.


   Methods
Top
 Abstract
 Methods
Results
 Discussion
 Conclusions
 References
 
Patients.   The study was approved by the Institutional Review Board. From January 1990 to December 1995, a total of 6,421 patients were referred for clinically indicated exercise echocardiography for evaluation of known or suspected CAD. Of the patients, 254 (4%) had inadequate echocardiographic images and 136 patients (2%) refused to participate in research. Among the remaining 5,798 patients, follow-up was obtained in 5,728 (95%); these make up the study population.

Data regarding patients’ cardiac history and risk factors were entered in our computerized database at the time of the exercise echocardiogram. Hypercholesterolemia was defined as total cholesterol >200 mg/dl or use of a cholesterol-lowering agent. Hypertension was defined as blood pressure ≥140/90 mm Hg or use of antihypertensive medication. Diabetes mellitus was defined by the presence of a fasting blood glucose concentration ≥140 mg/dl or requirement for insulin or orally administered hypoglycemic agents.

Exercise echocardiography protocol.   All patients underwent symptom-limited treadmill exercise testing. Standard blood pressure and 12-channel electrocardiographic monitoring were performed. Exercise was performed according to the Bruce protocol in 3,003 men (90%) and 2,126 women (86%), the Naughton protocol in 190 women (8%) and 150 men (5%), and modified Bruce protocol in 169 men (5%) and 160 women (6%) (overall p = 0.001).

Two-dimensional echocardiographic images were obtained from the parasternal and apical windows at rest and immediately after exercise. Studies were recorded on videotape. The standard views were also digitized and stored in quad screen format (9).

Exercise echocardiographic interpretation.   Both digitized and videotape-recorded images were used for interpretation (10). Regional wall motion was assessed semiquantitatively by an experienced echocardiographer (11) blind to clinical information. Wall motion at rest and with exercise was scored 1 through 5 according to a 16-segment model (12). Wall motion score index (WMSI) was calculated at rest and with exercise as the sum of the segmental scores divided by the number of visualized segments multiplied by 100%. The development of new or worsening wall motion was considered indicative of myocardial ischemia. A wall motion abnormality present at rest and unchanged with exercise was classified as fixed. Exercise echocardiography results were defined as abnormal if ischemia or fixed wall motion abnormalities were present. The percentage of segments that were abnormal was calculated as abnormal segments divided by the number of visualized segments multiplied by 100%. The percentage of ischemic segments was calculated similarly. Ejection fraction at rest was measured using a previously validated modification of the method of Quinones et al. (13) or by visual estimation (14). The exercise electrocardiogram (ECG) was positive for ischemia if there was horizontal or downsloping ST-segment depression of ≥1 mm at 80 ms after the J point, nondiagnostic if there was baseline ST-segment deviation or negative for ischemia in the absence of these criteria. Workload was measured in metabolic equivalents (METs).

Follow-up.   Follow-up was obtained by mailed questionnaires, scripted telephone interviews and review of medical records. Events were verified by contacting the patients’ primary physicians and reviewing medical records and death certificates.

The end points considered were cardiac events, including nonfatal myocardial infarction (MI) and cardiac death. Sudden death occurring without another explanation was included as cardiac death. Myocardial infarction was a clinical diagnosis, based on the usual clinical, electrocardiographic and enzymatic criteria. Patients who had coronary revascularization (angioplasty or coronary artery bypass surgery) before other events were censored at the time of revascularization.

Statistical analysis.   Continuous variables were reported as mean ± standard deviation and categorical variables as percentages. Comparisons between men and women were based on the Wilcoxon rank-sum test for continuous variables and Pearson’s chi-square test for categorical variables.

For outcome analyses, a time to first event approach was used. Survival free of the end point of interest was estimated by the Kaplan-Meier method. Univariable and multivariable association of clinical and exercise echocardiographic variables with the end points were assessed using the Cox proportional hazards model. Variables were selected in a stepwise forward selection manner, with entry and retention in the model set at a significance level of 0.05. All interaction terms were tested jointly by using the global change in the model log likelihood as the test statistic. The results of the univariable and multivariable analyses were summarized as risk ratios with corresponding 95% confidence intervals (CIs). For a continuous multivariate predictor, a dichotomized cut-off value of the multivariate predictor that resulted in the largest change in the likelihood function was used to classify patients into risk groups. This was done separately for each gender.

The incremental value of exercise echocardiography was assessed in two modeling steps. The first step consisted of fitting a multivariable model of clinical, rest echocardiographic and exercise electrocardiographic data. Variables selected from this first step were then used as baseline risk factors, and exercise echocardiographic variables were added in a stepwise forward selection manner. Entry and retention were set at a significant level of 0.05 for each of the three modeling steps.


   Results
Top
 Abstract
 Methods
 Results
Discussion
 Conclusions
 References
 
Study group.   Of the 5,798 patients, 1,632 underwent stress echocardiography for evaluation of known CAD, 3,294 for the evaluation of chest pain or dyspnea, 136 for preoperative cardiac risk assessment, 222 because of nondiagnostic or positive exercise ECG and 521 for evaluation of risk factors. There were 3,322 men (57%) and 2,476 women (43%) . The mean age was 62 ± 12 years for men and 62 ± 12 years for women (p = 0.7). The baseline characteristics of the patients are summarized in Table 1. Men more often had typical angina; women more often had atypical chest pain. Risk factors of smoking, hypertension and family history differed significantly in men and women.


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  		Table 1 Population Characteristics

 
Exercise echocardiography.   The exercise electrocardiographic and exercise echocardiographic characteristics are summarized in Table 2. The rest and exercise echocardiograms were normal in 1,514 men (46%) and 1,657 women (67%); in 549 men (17%) and 411 women (17%) the echocardiogram was normal at rest but ischemic with exercise; in 641 men (19%) and 193 women (8%) there were wall motion abnormalities at rest without ischemia; in 617 men (19%) and 215 women (9%) there were wall motion abnormalities at rest and ischemia with exercise (overall p = 0.001).


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  		Table 2 Exercise Echocardiographic Characteristics

 
Outcomes.   During a median follow-up of 3.2 ± 1.7 years, there were 255 cardiac events. Cardiac death occurred in 74 men and 33 women and nonfatal MI in 105 men and 43 women. Causes of cardiac death included sudden death in 12 men and 7 women, MI in 33 men and 10 women and congestive heart failure in 16 men and 6 women. Of the patients, 178 (31%) underwent revascularization before any cardiac event and were censored. For cardiac death, the estimated one-, three- and five-year survival rates were significantly worse for men (99.5%, 98.0% and 96.7%, respectively) than for women (99.8%, 99.2% and 97.6%, respectively) (p = 0.04). For cardiac events, event-free survival was also worse for men (98.6%, 95.1% and 90.4%, respectively) than for women (99.5%, 97.6% and 94.9%, respectively) (p < 0.0001).

Predictors of cardiac events.   Univariable associations with cardiac events are shown in Table 3; all of these variables were considered as potential predictors for multivariable models. Positive exercise ECG and angina during the exercise test were not predictive. Multivariable predictors of cardiac events are reported in Table 4.


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  		Table 3 Univariable Predictors of Cardiac Events

 

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  		Table 4 Multivariable Predictors of Cardiac Events (Cox Regression Analysis) in Patients Undergoing Exercise Stress Echocardiography

 
The independent predictors for events in both men and women included history of MI, workload and exercise WMSI. In men, an increase of 1 MET in workload was associated with a reduction of 10% in the risk of events. In women, an increase of 1 MET in workload was associated with a reduction of 14%. In men, a 0.5-unit increase in exercise WMSI carried a 52% increase in the risk of events. In women, this change was associated with a 48% increase in the risk of events. The survival free of cardiac events for both genders according to workload and exercise WMSI is shown in Figures 1 and 2, respectively. Workload ≤6 METs and exercise WMSI ≥1.25 were the best discriminators of increased risk for both men and women. The relationship of exercise WMSI and cardiac events per person-year of follow-up is shown in Figure 3.



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  		Figure 1 Survival free of cardiac death and myocardial infarction are shown in men and women, with exercise capacity ≥6 metabolic equivalent (METs) and <6 METs.

 


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  		Figure 2 Survival free of cardiac death and myocardial infarction are shown in men and women, with exercise wall motion score index (WMSI) <1.25 and ≥1.25.

 


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  		Figure 3 The relationship of cardiac events per person-year of follow-up is plotted against exercise wall motion score index.

 
For men, the independent predictors for cardiac death were: workload (relative risk RR = 0.78; 95% CI 0.71 to 0.85; p = 0.0001); rest ejection fraction (RR = 0.53; 95% CI 0.45 to 0.64 per 10 units of change; p = 0.0001); and change in WMSI from rest to exercise (RR = 1.67; 95% CI 1.15 to 2.43 per 0.5 unit change; p = 0.01). Independent predictors in women were: typical angina (RR = 2.60; 95% CI 1.27 to 5.35; p = 0.009); previous MI (RR = 3.42; 95% CI 1.68 to 6.97; p = 0.007); diabetes mellitus (RR = 2.26; 95% CI 1.04 to 4.89; p = 0.04); and workload (RR = 0.82; 95% CI 0.70 to 0.95; p = 0.10).

Incremental value of exercise echocardiography.   For both genders, the clinical, rest echocardiogram and exercise electrocardiographic predictors of cardiac events included age, diabetes mellitus, typical angina, prior MI, rest ejection fraction and workload (men: X2 = 137; women: X2 = 72). Addition of the exercise echocardiographic variable, percentage of ischemic segments, improved both models (men: X2 = 143, p = 0.014; women: X2 = 76, p = 0.046). There was no significant interaction effect of rest echocardiography (p = 0.79), exercise electrocardiography (p = 0.38) or exercise echocardiography (p = 0.67) with gender, indicating comparable risk stratification for both genders.


   Discussion
Top
 Abstract
 Methods
 Results
 Discussion
Conclusions
 References
 
In this study of 5,798 patients, the treadmill exercise echocardiogram provided significant incremental value when compared with clinical, rest echocardiographic and exercise electrocardiographic variables for predicting cardiac death and cardiac events in both genders. Although cardiac events were more common in men, there was no interaction effect of gender with predictors for events, suggesting that exercise echocardiography as a method for assessment of prognosis is comparable in both men and women. The best exercise echocardiographic predictor of events was the exercise WMSI, an indicator of the extent and severity of exercise-induced ischemia.

Detection of CAD in women.   Noninvasive detection of CAD is challenging in women, in part because of the lower prevalence of disease (15). Because of the lower pretest probability of disease in women, tests are more often false positive. The exercise electrocardiogram has been shown to be less accurate in women than in men (2–5). Differences in the prevalence of multivessel CAD and prior MI (16–18), differences in exercise capacity (16) and microvascular function and in the prevalence of syndrome X and mitral valve prolapse (2) may account for these distinctions. These difficulties have led to the suggestion that stress imaging may be the preferred strategy in women (7). However, intrinsic gender differences have been noted with exercise radionuclide angiography (19). Breast artifact is a recognized difficulty of nuclear perfusion imaging (20).

Stress echocardiography has been recommended as a cost-effective approach to the diagnosis of CAD in women (7). However, in several large studies, the accuracy for detection of angiographic disease (7,8,21,22) has varied. When test referral bias is considered, the positive predictive value and adjusted sensitivity are lower in women than in men (8). Because test results influence the decision whether to perform coronary angiography, with only 9% of the population undergoing stress echocardiography subsequently referred to angiography, the utility of the test is difficult to discern (8). Therefore, this study was undertaken to examine the outcomes of all patients undergoing exercise echocardiography.

Current study.   In our study, women presented less often with typical angina, were less likely to have had prior MI or prior coronary revascularization and less often had electrocardiographic evidence of ischemia. Wall motion score index, at rest and with stress, was lower in women. Cardiac events occurred less frequently in women. These differences are compatible with the lower prevalence and lesser severity of CAD in women (15,16). Despite these differences, the clinical, exercise electrocardiographic and echocardiographic predictors of cardiac events and cardiac death were very similar in men and women. The clinical variable prior MI was an independent predictor for events in both genders. This variable has been described as a predictor of the presence of multivessel CAD (18). In the current study, an increase in workload was associated with decreased risk of cardiac events and cardiac death in both men and women. Similarly, other investigators using exercise electrocardiography (23–25) as well as exercise imaging tests (26,27) have reported that a higher workload was associated with a reduction in the risk of events in both genders.

The presence of myocardial ischemia detected by exercise echocardiography was previously reported as a predictor of cardiac events in women (28). In the present study, the exercise WMSI and the percentage of ischemic segments detected by exercise were independent predictors of events for both genders. These echocardiographic variables reflect the extent and severity of CAD and were superior to the dichotomous variable, ischemia. We have previously reported satisfactory agreement between experienced observers for scoring of the 16 segments at rest and with stress (29). Thus, efforts should be made to quantify the extent of ischemia by scoring the individual segments.

Study limitations.   In our population, exercise echocardiographic results were used in managing patients; this may have reduced the prognostic value of the test. Therefore, an analysis was performed using only MI and cardiac death as end points, because the decision for revascularization might be most influenced by test results. Follow-up was available for only 95% of patients. Lastly, baseline characteristics differed in men and women. However, the intent of this study was to describe a large consecutive series of men and women referred for clinically indicated exercise echocardiography.


   Conclusions
Top
 Abstract
 Methods
 Results
 Discussion
 Conclusions
References
 
Exercise echocardiography provides independent prognostic information for both men and women that is incremental to clinical, rest echocardiographic and exercise electrocardiographic data. Of all exercise electrocardiographic and exercise echocardiographic variables, workload and exercise WMSI had the strongest association with outcome. Although cardiac events occurred more frequently in men, the incremental prognostic value of exercise echocardiography was comparable in both genders.


   Footnotes
 
Dr. Arruda-Olson was supported by grants from the CAPES Foundation (Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), Brasília, Brazil, and the Mayo Foundation. The study was supported by a grant from the Mayo Foundation.


   References
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 Methods
 Results
 Discussion
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 References
 

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Stress echocardiography for the diagnosis and risk stratification of patients with suspected or known coronary artery disease: a critical appraisal. Supported by the British Society of Echocardiography
Heart, April 1, 2005; 91(4): 427 - 436.
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 Eur Heart JHome page
L. J. Shaw, C. Vasey, S. Sawada, C. Rimmerman, and T. H. Marwick
Impact of gender on risk stratification by exercise and dobutamine stress echocardiography: long-term mortality in 4234 women and 6898 men
Eur. Heart J., March 1, 2005; 26(5): 447 - 456.
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R. Bigi and L. Cortigiani
Stress testing in women: sexual discrimination or equal opportunity?
Eur. Heart J., March 1, 2005; 26(5): 423 - 425.
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 CirculationHome page
J. H. Mieres, L. J. Shaw, A. Arai, M. J. Budoff, S. D. Flamm, W. G. Hundley, T. H. Marwick, L. Mosca, A. R. Patel, M. A. Quinones, et al.
Role of Noninvasive Testing in the Clinical Evaluation of Women With Suspected Coronary Artery Disease: Consensus Statement From the Cardiac Imaging Committee, Council on Clinical Cardiology, and the Cardiovascular Imaging and Intervention Committee, Council on Cardiovascular Radiology and Intervention, American Heart Association
Circulation, February 8, 2005; 111(5): 682 - 696.
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 J Am Coll CardiolHome page
E. Biagini, A. Elhendy, J. J. Bax, V. Rizzello, A. F.L. Schinkel, R. T. van Domburg, M. D. Kertai, B. J. Krenning, M. Bountioukos, C. Rapezzi, et al.
Seven-year follow-up after dobutamine stress echocardiography: Impact of gender on prognosis
J. Am. Coll. Cardiol., January 4, 2005; 45(1): 93 - 97.
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 Arch Intern MedHome page
K. Nasir, R. F. Redberg, M. J. Budoff, E. Hui, W. S. Post, and R. S. Blumenthal
Utility of Stress Testing and Coronary Calcification Measurement for Detection of Coronary Artery Disease in Women
Arch Intern Med, August 9, 2004; 164(15): 1610 - 1620.
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 CirculationHome page
B. D. Johnson, L. J. Shaw, S. D. Buchthal, C. N. Bairey Merz, H.-W. Kim, K. N. Scott, M. Doyle, M. B. Olson, C. J. Pepine, J. den Hollander, et al.
Prognosis in Women With Myocardial Ischemia in the Absence of Obstructive Coronary Disease: Results From the National Institutes of Health-National Heart, Lung, and Blood Institute-Sponsored Women's Ischemia Syndrome Evaluation (WISE)
Circulation, June 22, 2004; 109(24): 2993 - 2999.
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 J Am Coll CardiolHome page
S. Bergeron, S. R. Ommen, K. R. Bailey, J. K. Oh, R. B. McCully, and P. A. Pellikka
Exercise echocardiographic findings and outcome of patients referred for evaluation of dyspnea
J. Am. Coll. Cardiol., June 16, 2004; 43(12): 2242 - 2246.
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 CirculationHome page
L. J. Shaw, J. F. Lewis, M. A. Hlatky, W. A. Hsueh, S. F. Kelsey, R. Klein, T. A. Manolio, A. R. Sharrett, R. P. Tracy, and Endorsed by the American College of Cardiology Fou
Women's Ischemic Syndrome Evaluation: Current Status and Future Research Directions: Report of the National Heart, Lung and Blood Institute Workshop: October 2-4, 2002: Section 5: Gender-Related Risk Factors for Ischemic Heart Disease
Circulation, February 17, 2004; 109 (6): e56 - e58.
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 LupusHome page
S Codish, N Liel-Cohen, M Rovner, S Sukenik, and M Abu-Shakra
Dobutamine stress echocardiography in women with systemic lupus erythematosus: increased occurrence of left ventricular outflow gradient
Lupus, February 1, 2004; 13(2): 101 - 104.
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 J Am Coll CardiolHome page
A. Elhendy, D. W. Mahoney, B. K. Khandheria, T. E. Paterick, K. N. Burger, and P. A. Pellikka
Prognostic significance of the location of wall motion abnormalities during exercise echocardiography
J. Am. Coll. Cardiol., November 6, 2002; 40(9): 1623 - 1629.
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 JAMAHome page
R. F. DeBusk, S. Malozowski, J. T. Sahlroot, P. A. Pellikka, and A. M. Arruda-Olson
Sildenafil and Physical Exertion in Men With Coronary Artery Disease
JAMA, May 8, 2002; 287(18): 2359 - 2360.
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