Parameters Derived from Myocardial Tissue Doppler Imaging Associated with Major Events in Patients with Uremia

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1 Original Acta Cardiol Sin 2007;23: Parameters Derived from Myocardial Tissue Doppler Imaging Associated with Major Events in Patients with Uremia Shih-Hung Hsiao, Shih-Kai Lin, Wei-Chen Huang, Chiu-Yen Lee, Shu-Hsin Yang, Kuan-Rau Chiou and Chun-Peng Liu Background: High cardiovascular mortality in uremic patients is still a problem. This study was designed to assess some echocardiographic parameters to predict prognosis. Methods: We enrolled 95 patients (19 with coronary arterial disease). All underwent conventional echocardiography and tissue Doppler imaging within 30 minutes before and after hemodialysis (H/D). We measured the ratio of the early-diastolic velocity of mitral inflow (E) to the early-diastolic velocity of the mitral annulus (Em). Patients received 4-year follow-up for major events (any-cause mortality and nonfatal cardiovascular events requiring hospitalization). Results: Thirteen deaths and 11 nonfatal major events occurred. The prevalence of underlying coronary arterial disease was higher in patients with major events than in others (33% vs. 7%), as was the degree of left ventricular (LV) systolic dysfunction (LV ejection fraction 46% 10 vs. 52% 8). Baseline E/Em, either pre-dialytic or post-dialytic, was significantly lower in event-free patients (pre-dialytic vs , p = 0.01; post-dialytic vs , p = 0.002). On Cox regression, factors significantly affecting outcomes were age, LV ejection fraction, LV mass index (hazard ratio [HR] = 1.021, 95% confidence interval [CI] , p = 0.021), and post-dialytic E/Em 12 (HR = 3.054, 95% CI , p = 0.009). Conclusion: Like LV dysfunction and LV mass index, a high post-dialytic E/Em was prognostic of major events. Key Words: Echocardiography Tissue Doppler imaging Uremia Cardiovascular mortality INTRODUCTION Received: September 18, 2007 Accepted: November 12, 2007 Cardiovascular Center, Department of Internal Medicine, Kaohsiung Veterans General Hospital, Kaohsiung, Taiwan. Address correspondence and reprint requests to: Dr. Chun-Peng Liu, MD, Cardiovascular Center, Department of Internal Medicine, Kaohsiung Veterans General Hospital, No. 386, Da-Chung 1st Rd., Kaohsiung 813, Taiwan. Tel: ext. 2011; Fax: ; a841120@ms3.hinet.net Findings on tissue Doppler imaging (TDI) of the mitral annulus accurately and reproducibly represent global LV systolic or diastolic function Many TDIderived parameters are useful for assessing cardiovascular risk. The ratio of early-diastolic mitral inflow velocity divided by early-diastolic mitral annular velocity (E/Em) is correlated with LV relaxation and LV filling pressure, and this ratio has prognostic value in many cardiovascular diseases. 9,16-18 An E/Em of > 12 is associated with a high event rate in patients with heart failure. 19 Uremic patients under regular hemodialysis (H/D) for chronic renal failure are associated with a high mortality rate, and cardiovascular events are the major cause of death. 20 Accelerated coronary atherosclerosis seems to be closely related to this excessive mortality. 21,22 Other factors implicated in ventricular dysfunction and mortality are increased LV mass and diastolic dysfunction. 23,24 This study was undertaken to evaluate the prognostic value of an E/Em in patients with uremia. Acta Cardiol Sin 2007;23:

2 Echocardiographic Prediction of Uremic Events METHODS Patient population Beginning in June 2002, we prospectively enrolled 95 patients with uremia (49 women, 50 men) who were receiving regular H/D. We obtained written informed consent from the patients and approval by our hospital s committee on clinical investigation. All patients received maintenance H/D for 6 months. Patients were excluded if they had any rhythm other than a sinus rhythm or if their images were of inadequate quality for analysis. All patients received conventional echocardiography and myocardial TDI within 30 minutes before or after H/D. A nephrologist performed dry-weight adjustments and regular follow-up for routine blood and biochemical studies. The prevalence of coronary artery disease (CAD) at the initiation of this study was based on past history of positive stress test, perfusion scan, documented myocardial infarction and previous revascularization. Conventional echocardiographic study Using a commercially available ultrasound system (Sonos 5500, Philips, Andover, MA) and a 2.5- or 2.0- MHz phased-array transducer, we examined patients in the left lateral decubitus position using standard parasternal long-axis, short-axis, and apical views. One author obtained all measurements according to recommendations of the American Society of Echocardiography. Doppler measurements were made at end-expiration to ensure that patients were not straining. Echocardiographic maximum left atrial volume was measured by biplane area-length from apical 4- and 2-chamber views and indexed to body surface area, 25,26 according to the American Society of Echocardiography method for calculation of left atrial volume. LV mass was estimated from measurements of septal and posterior-wall thickness and from dimensions of the LV cavity at end-diastole by using the following anatomically validated equation: LV mass = 0.8[1.04(IVS + LVIDd + LVPW) 3 LVIDd 3 ] + 0.6, where IVS is the diastolic septal thickness, LVIDd is the diastolic dimension of the LV cavity, and LVPW is the diastolic thickness of the posterior wall. The LV mass index was calculated as LV mass divided by the estimated body surface area. LV and right ventricular ejection fractions were estimated by using the Simpson and modified Simpson methods, respectively. 27 Pulsed-wave myocardial TDI TDI was performed with spectral pulsed Doppler signal filters by adjusting the Nyquist limit to cm/s and by using the minimal optimal gain. The apical view was chosen to quantitatively assess regional wall motion and to minimize the incidence angle between the Doppler beam and the area of longitudinal wall motion. On the apical 4-chamber view, a 3-mm, pulsed-doppler sample volume was placed at the level of the basal mitral annulus. Tissue Doppler velocities of longitudinal mitral annular motion were recorded in all six segments of the basal mitral annulus. Pulsed-wave TDI tracings were recorded over five cardiac cycles at a sweep speed of 100 mm/s and used for offline calculations. Peak systolic myocardial velocity (Sm), Em, and peak late-diastolic myocardial velocity (Am) over the mitral annulus were measured. Mean TDI parameters over the six segments were calculated, and the mean Em was used to estimate E/Em. The first echocardiographic study was performed about minutes before H/D. Paired measurements were repeated immediately after H/D. Particular care was taken to position the sample volume in the same location whenever possible. Follow up After echocardiography, patients were followed up at our nephrologic clinic for 4 years (mean SD 44 7 months). Records and causes of their admissions were ascertained from detailed chart review and from final comments of the nephrologists and cardiologists. We recorded major events, which were defined as anycause mortality and nonfatal cardiac or vascular events with hospitalization. Stroke was considered a vascular event, and positive results on treadmill testing or perfusion scanning with scheduled coronary angioplasty or bypass surgery were included as cardiac events. Unstable angina was defined as angina pectoris with resting, new-onset, and/or crescendo angina. Myocardial infarction was identified as clinical symptoms, new ST-segment change of > 1 mm in two contiguous leads, and increased serum cardiac enzyme levels 2 times the upper limit of normal in our laboratory. Some cases of decompensated septic shock or ulcerative bleeding with concomitant ST-segment changes and elevated cardiac enzyme levels were classified as occult CAD. 255 Acta Cardiol Sin 2007;23:254 62

3 Shih-Hung Hsiao et al. Statistical analysis All data were expressed as the mean SD. A Paired t-test was used to compare the differences before and after H/D. For multivariate comparison, the study cohort was grouped by whether or not they had major events. Receiver-operating characteristic (ROC) curve analysis was performed to select optimal cut-off values of E/Em to predict major events. Using regular Cox proportional hazards regression, we compared the major-event risks of patients receiving H/D according to the cutoff values of E/Em, with adjustments for potential confounders. Covariates for adjustment were age at study entry, previous CAD, size of the LV chamber, LV ejection fraction, and LV mass index. Patient event-free survival was recorded when mortality or nonfatal cardiac or vascular events occurred or at the end of follow-up, whichever came first. Kaplan-Meier curves of cumulative event-free survival were plotted according to E/Em values. Differences were significant if p <0.05 with a 95% confidence interval (CI). To determine interobserver variability, mean values from one observer were compared with those of a second observer blinded to the initial results. Mean differences between their measurements were calculated, and the percentage variability was derived as the absolute difference between sets of measurements divided by the mean of the two observations. Intraobserver variability was also calculated with this method. RESULTS During follow-up, we recorded 24 major events, including 13 deaths and 11 nonfatal cardiovascular events (Table 1). Eight deaths (cardiac ischemic with decompensated septic shock or with a bleeding peptic ulcer, and sudden death) were associated with myocardial ischemia. CAD was the leading cause of nonfatal events. Baseline characteristics, except for LV mass index and CAD, were similar between patients with and those without major events (Table 2). LV mass indexes and Table 1. Major events and causes No. of cases Death Cardiac ischemia with decompensated 4 septic shock Septic shock 3 Cardiac ischemia with bleeding peptic ulcer 2 and shock Sudden death of unknown cause 2 Malignancy 1 Intracranial hemorrhage 1 Nonfatal cardiac or vascular event Stroke 3 Stable angina treated with revascularization 2 Heart failure with hospitalization 2 Non-ST-elevation myocardial infarction 2 Unstable angina 1 ST-elevation myocardial infarction 1 Table 2. Baseline characteristics Patients without major events (n = 71) Patients with major events (n = 24) p value Age (yrs) Body weight (kg) H/D amount (kg) Diabetes 22 (31) 08 (33) Hypertension 33 (46) 11 (46) LV mass index (g/m 2 ) Albumin (g/dl) Calcium (mg/dl) Phosphorus (mg/dl) Total cholesterol (mg/dl) Low-density lipoprotein cholesterol (mg/dl) Hemoglobin (g/dl) CAD 5 (7) 14 (58) < < Deaths 0 (0) 13 (54) < < Data are the mean SD or the number (percentage). CAD = coronary artery disease; H/D = hemodialysis; LV = left ventricular. Acta Cardiol Sin 2007;23:

4 Echocardiographic Prediction of Uremic Events prevalence of CAD were highest in patients with events. Table 3 shows conventional echocardiographic parameters and TDI measurements. Among patients without events, cardiac chambers were small, but baseline LV ejection fractions were high; their chamber sizes, mitral inflows, and pulmonary venous flow velocities significantly decreased after H/D. LV and right ventricular ejection fractions were relatively constant during H/D. Of interest, diastolic velocities of the six segments of the mitral annulus, especially Em, were significantly reduced after dialysis in eventfree patients, and the phenomenon was not observed in those having events. The mean Em of the six mitral segments before and after dialysis notably changed in patients without events but not in those with events. When E/Em was used to reflect LV compliance, pre-h/d E/Em values in patients without major events was significantly lower than in the others ( vs , p = 0.008). In patients with events, E/Em values were similar before ( ) and after ( , p = 0.892) dialysis, but they were significantly reduced in eventfree patients (before vs after dialysis vs , p = 0.002). On bivariate analysis, post-h/d E/Em was correlated with age (r = 0.353, p = 0.001), post-h/d diameter of the left atrium (r = 0.355, p = 0.001), end-diastolic LV Table 3. Echocardiographic characteristics Patients without major events (n = 71) Patients with major events (n = 24) p value, event vs event-free groups Pre-H/D Post-H/D p value Pre-H/D Post-H/D p value Pre-H/D Post-H/D Heart rate (beats/minute) Dimension (mm) Aortic root Left atrial < Left ventricular end diastolic < Left ventricular end systolic Ventricular septal wall (mm) Peak velocity of mitral inflow (cm/s) Early diastolic < Late diastolic < Deceleration time (cm/s) Peak velocity, pulmonary vein (cm/s) Systolic < Diastolic < Atrial reverse Ejection fraction (%) Left ventricular Right ventricular Left atrial volume indexed to body surface area (ml/m 2 ) The mean velocities of six basal mitral annular segments (cm/s) Sm Em Am E/Em Data other than p values are the mean SD. Am = peak late-diastolic myocardial velocity; E = early-diastolic velocity of mitral inflow; Em = early-diastolic velocity of the mitral annulus; H/D = hemodialysis; Sm = peak systolic myocardial velocity. 257 Acta Cardiol Sin 2007;23:254 62

5 Shih-Hung Hsiao et al. 95% CIs for each covariate. Post-H/D E/Em ³ 12 was an independent predictor of major events even after controlling for potential confounders (age, albumin, left ventricular mass index, phosphorus level, and left ventricular ejection fraction). Intraobserver differences were as follows: mitral E velocity, 4.5 ± 3.5%; mitral late-diastolic velocity, 3.5 ± 3.1%; Sm, 0.3 ± 0.3 cm/s (variability 3.9 ± 3.2%); Em, 0.2 ± 0.2 cm/s (variability 2.6 ± 1.9%); and Am, 0.4 ± 0.3 cm/s (variability 4.2 ± 3.0%). Interobserver differences were as follows: mitral E velocity, 5.6 ± 4.5%; mitral late-diastolic velocity, 4.5 ± 3.7%; Sm, 0.5 ± 0.4 diameter after dialysis (r = 0.425, p < 0.001), LV mass index (r = 0.391, p = < 0.001), and LV ejection fraction before dialysis (r = , p = 0.001). Pre-H/D E/Em values had a similar pattern and were correlated with age (r = 0.305, p = 0.003), pre-h/d diameter of the left atrium (r = 0.449, p = 0.001), pre-h/d end-diastolic LV diameter (r = 0.334, p = 0.003), and LV mass index (r = 0.368, p = 0.001). Pre-H/D E/Em and LV ejection fraction were weakly related (r = -0.28, p = 0.045). ROC curve analysis was performed, and a post-h/d E/Em ³ 12 was an optimal cutoff to predict major events. This cutoff was associated with an AUC (areas under ROC curve) of 0.833, p < , a sensitivity of 74%, and a specificity of 86% (Figure 1). Although pre-h/d ³ 12 was another cutoff weakly to predict major events, this cutoff valve was only associated with an AUC of 0.62, p = 0.031, a sensitivity of 65%, and a specificity of 64%. Using this cutoff value, post-h/d E/Em ³ 12 effectively stratified patients by Kaplan-Meier curves of cumulative event-free survival (Figure 2). The relationship between post-h/d E/Em and cumulative major events is shown in Figure 3. On regular Cox proportional hazards regression, pre-h/d E/Em values weakly affected prognoses (hazard ratio [HR] 1.6, 95% CI , p = 0.13), but post-h/d E/Em values were significantly associated with outcomes. Multivariable predictors of major events were older age, left ventricular systolic dysfunction, diabetes, left ventricular mass index and posth/d E/Em ³ 12. Table 4 shows the adjusted HRs with Figure 1. Analysis of the receiver-operating characteristic curve showed that a post-dialytic (H/D) E/Em ³ 12 could be used to predict major events with a sensitivity of 74% and a specificity of 86%, but preh/d E/Em ³ 12 could not provide adequate sensitivity and specificity. Acta Cardiol Sin 2007;23: Figure 2. Kaplan-Meier curves of cumulative event-free survival in uremic patients. (A) Curve based on pre-dialytic (H/D) E/Em. (B) Curve based on post-h/d E/Em. 258

6 Echocardiographic Prediction of Uremic Events Figure 3. Unadjusted 4-year major event rates according to postdialytic (H/D) E/Em. Table 4. Adjusted HRs for major events HR 95% CI p value Age (per yr) LV ejection fraction < 50% Post-H/D E/Em > LV mass index (per g/m 2 ) CI = confidence interval; E = early-diastolic velocity of mitral inflow; Em = early-diastolic velocity of the mitral annulus; H/D = hemodialysis; HR = hazard ratio; LV = left ventricular. cm/s (variability %); Em, cm/s (variability %); and Am, cm/s (variability %). DISCUSSION E/Em is correlated with pulmonary capillary wedge pressure and LV filling pressure. 4,9,16 E/Em has been appliedtocad, 28 chronic heart failure, 19 and intubations in intensive care units. 17 In a relatively healthy population with a low anticipated mortality rate, LV filling pressure, as determined from cardiac catheterization and E/Em, was also an independent predictor of future heart failure. 29 Patients with uremia may have relative fluid overload before dialysis but relative fluid deficiency after H/D. As a well-known phenomenon, peak trans-mitral flow is dependent on the interaction between left atrial pressure and LV pressure-volume relationship, so conventional trans-mitral flow is preload-dependent. For the assessment of LV diastolic function, preload-independent echocardiographic parameters such as tissue Doppler were expected. Although TDI parameters were believed to be relatively preload-insensitive, 4 our recent investigation in a uremic cohort revealed different results. Em and Am in patients with preserved LV systolic function were significantly reduced after H/D, especially when > 2 kg of fluid was removed. 30 For detailed comparison, the present study was designed to measure echocardiographic parameters just before and after H/D. For patients with CAD and abnormalities in regional wall motion, regional TDI parameters are unlikely to represent global LV diastolic function. Therefore, the mean Em was used to estimate E/ Em. A post-h/d E/Em 12 significantly affected outcomes and was the strongest predictor among all covariates (HR = 3.054). On the contrary, a pre-h/d E/Em 12 did not provide adequate power to predict prognosis in the Cox model. LV filling pressure and pulmonary capillary wedge pressure decrease as preload reduced. 31,32 This means that E/Em, like LV filling pressure, is lower after preload reduction with H/D and hints that high post-h/d E/Em values are more important than pre-h/d data. Our method is different to the report of Ie et al, 33 but the result is similar. Ie and coauthors concluded that conventional echocardiographic and tissue Doppler parameters were limited in ability to assess the diastolic function just before dialysis due to relative fluid-overloading status. They found those parameters measured twenty-four hours after dialysis did not differ from those taken one hour after dialysis. Therefore, echocardiographic parameters including tissue Doppler imaging are not so good to assess left ventricular diastolic function just before dialysis, so pre-h/d E/Em doesn t provide adequate prognostic significance, as in our study. Among event-free patients, E decreased more than Em after dialysis, lowering post-h/d E/Em. Em was relatively constant during dialysis among patients with events, though E was somewhat reduced. The combined effect was that E/Em did not change after dialysis. Of interest, pre-h/d and post-h/d E/Em values were highest in patients with events. Event-free patients had low LV 259 Acta Cardiol Sin 2007;23:254 62

7 Shih-Hung Hsiao et al. filling pressures regardless of dialysis; therefore, their low event rate is predictable. Study limitations First, invasive hemodynamic data were not included. However, our purpose was to assess the prognoses of patients with uremia by using simple and noninvasive methods. We did find that echocardiographic parameters were significant predictors for major events. Second, patients with cardiac rhythms other than a sinus rhythm were excluded. Atrial fibrillation may represent a relatively severe condition in uremic patients. Therefore, selection bias was possible. Third, we used the mean Em of six basal mitral segments to calculate E/Em because of high prevalence of CAD and because of the abnormalities in regional wall motion in our cohort. The representativeness and accuracy of our method should be tested in further studies. In addition, the prevalence of CAD was possibly underestimated due to lack of non-invasive or invasive CAD screen in this study cohort. 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9 Original Acta Cardiol Sin 2007;23: 以組織都卜勒超音波參數來預測洗腎病人的癒後 蕭世宏林士凱黃偉春李秋燕楊淑馨邱寬饒劉俊鵬高雄市高雄榮民總醫院心血管中心 背景心血管疾病造成的死亡仍是洗腎病人的大問題, 本研究在於使用心臟超音波來預測洗腎病人的癒後 方法九十五位洗腎病人接受心臟超音波及心肌組織超音波, 在洗腎前後, 測量舒張早期二尖瓣血流速與舒張早期二尖瓣心肌組織移動速度比例 (E/Em), 以此來推測洗腎病人四年內的出事率 結果四年內的共有十三人死亡, 十一人發生非死亡性之重大事件, 研究發現洗腎病人的重大事件多與心血管疾病相關, 將病人依出事與否分為兩組, 可以發現出事組有較高比例的冠心症患者及心收縮功能不良, 洗腎前及洗腎後的 E/Em 也比較高, 使用 Cox regression model, 發現年紀 心收縮功能 LV mass index (hazard ratio [HR] = 1.021, 95% confidence interval [CI] , p = 0.021) 及洗腎後 E/Em (HR = 3.054, 95% CI , p = 0.009) 對於評估癒後有重大影響 結論洗腎後 E/Em 如同心收縮功能一樣, 對於評估洗腎病人的癒後有重大影響 關鍵詞 : 洗腎病人 心肌組織超音波 心血管疾病 癒後 262