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Am J Physiol Heart Circ Physiol 289: H1131-H1136, 2005. First published April 29, 2005; doi:10.1152/ajpheart.00345.2004
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Validation of echocardiographic and Doppler indexes of left ventricular relaxation in adult hypertensive and normotensive rats

Michel Slama,1 Jwari Ahn,2 Marcel Peltier,1 Julien Maizel,1 Denis Chemla,3 Jasmina Varagic,2 Dinko Susic,2 Christophe Tribouilloy,1 and Edward D. Frohlich2

1ERI 12, UPRES 3906, INSERM Faculté de Médecine, Université Jules Verne, Amiens, France; 2Research Division, Ochsner Clinic Foundation, New Orleans, Louisiana; and 3UPRES 2705-APHP, Université Paris, Paris, France

Submitted 13 April 2004 ; accepted in final form 16 April 2005


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This study was performed to validate echocardiographic and Doppler techniques for the assessment of left ventricular (LV) diastolic function in spontaneously hypertensive rats (SHR) and normotensive Wistar rats. In 11 Wistar rats and 20 SHR, we compared 51 sets of invasive and Doppler LV diastolic indexes. Noninvasive indexes of LV relaxation were related to the minimal rate of pressure decline (–dP/dtmin), particularly isovolumic relaxation time (IVRT), the Tei index, the early velocity of the mitral annulus (Em) using Doppler tissue imaging, and early mitral flow propagation velocity using M-mode color (r = 0.28–0.56 and P < 0.05–0.0001). When the role of systolic load was considered, the correlation between Doppler indexes of LV diastolic function and relaxation rate [(–dP/dtmin)/LV systolic pressure] improved (r = 0.48–0.86 and P = 0.004–0.0001, respectively). Similarly, Doppler indexes of LV diastolic function and the time constant of isovolumic LV relaxation ({tau}) correlated well (r = 0.50–0.84 and P = 0.0002–0.0001, respectively). In addition, eight SHR and eight Wistar rats were compared; their LV end-diastolic diameters were similar, whereas the SHR LV mass was greater. Furthermore, IVRT and Tei index were significantly higher and Em was lower in SHR. Moreover, {tau} was higher in SHR, demonstrating impaired LV relaxation. In conclusion, LV relaxation can be assessed reliably using echocardiographic and Doppler techniques, and, using these indexes, impaired relaxation was demonstrated in SHR.

spontaneously hypertensive rats; diastolic function; left ventricle; echocardiography

MOST HEMODYNAMIC STUDIES in rats have been performed using invasive techniques resulting in the loss of the animal and preventing longitudinal follow-up. The development of echocardiographic techniques permits analysis of left ventricular (LV) geometry, wall thickness, and mass (13, 14). Recently, echocardiographic and Doppler techniques have been employed to assess systolic and diastolic function in the rat (3, 7, 11, 16, 17, 22, 24, 29, 33). Because these techniques are noninvasive, they provide an excellent opportunity to study cardiac function in the same animal over a long time, thereby permitting longitudinal examination of natural and pathological events. The spontaneously hypertensive rat (SHR) is an excellent model of LV diastolic dysfunction. Little information is available concerning the accuracy of echocardiography and cardiac Doppler techniques for assessing diastolic function in rats (16, 17, 30). Moreover, no study has systematically compared echocardiographic and Doppler parameters of LV diastolic function with invasive indexes of relaxation such as the maximal rate of pressure decline (–dP/dt) and the time constant of isovolumic LV relaxation ({tau}) in the rat. Therefore, this study was designed to compare LV relaxation indexes obtained by echocardiographic and cardiac Doppler techniques with the invasive method in SHR and normotensive Wistar rats.


   METHODS
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 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animals. Male Wistar and SHR rats were purchased from Charles River Breeding Laboratories and were maintained thereafter in temperature- and humidity-controlled rooms with a 12:12-h light-dark cycle. They were given standard chow (PMI Nutrition; St. Louis, MO) and tap water ad libitum. All rats were handled in accordance with National Institutes of Health guidelines and our Institutional Animal Care and Use Committee approved the protocol. Before the study, all rats were screened using echocardiography to detect any comorbid congenital abnormalities (27).

Procedures. All measurements were made in anesthetized rats (Inactine). For the measurement of arterial pressure, a polyethylene catheter was placed into the abdominal aorta and connected to a transducer (Statham). A catheter-tipped transducer (Millar) was introduced into the LV through the right carotid artery. Arterial and LV pressures were recorded simultaneously using a data-acquisition system (IOX, EMKA Technologies), and minimal –dP/dt (–dP/dtmin) and {tau} were calculated automatically from LV tracings. The LV catheter permitted measurements of LV systolic (LVSP) and end-diastolic pressures (LVEDP). Because –dP/dtmin was demonstrated to be related and dependent on LVSP (31), we divided –dP/dtmin by LVSP [(–dP/dtmin)/LVSP]. The echocardiographic measurements were made in parallel (simultaneously) with hemodynamic measurements at a heart rate of ~350 beats/min.

Echocardiography. Transthoracic echocardiographic (TTE) measurements were performed in the left lateral decubitus position using a commercially available echocardiographic system (Sonos 4500 with an 8- to 12-MHz transducer or Sonos 2000 with a 7.5-MHz transducer, Agilent Technologies). The TTE probe was placed to obtain short- and long-axis views and four- and five-chamber apical cardiac views. From the cardiac long axis, an M-mode tracing of the LV was obtained, and measurements of LV end-diastolic diameter (LVEDD), LV end-systolic diameter (LVESD), and diastolic posterior (PW) and septal wall thicknesses (SW) were made according to American Society of Echocardiography guidelines (25). LV weight (LVW) was calculated as LVW = 1.04 x [(LVEDD + PW + SW)3 – LVEDD3], and shortening fraction (SF) was calculated as SF = (LVEDD – LVESD)/LVEDD. From the five-chamber apical view, aortic flow was recorded using pulsed Doppler with the smallest sample volume (0.06 cm) placed at the level of the aortic annulus.

LV ejection time (ET) was measured from the beginning to end of the aortic flow wave. Mitral flow was recorded at the tip of the mitral valve from an apical view using Doppler. Heart rate ranged between 195 and 375 beats/min, and mitral E and A waves were merged in more than half the rats. Because neither the deceleration time of the E or A wave nor velocity time integral (VTI) and maximal velocity were not measurable in all rats, they are not reported herein. Maximal velocity and VTI of the E wave (VE) were measured (1, 9, 12, 15), and the isovolumic relaxation time (IVRT) was measured as the interval between aortic closure and the start of mitral flow. Using the same tracing, we measured the time between the closing and opening of the aortic valve (DD) and between the opening and closing of the mitral valve (MD). The myocardial index (MI) described by Tei et al. (31) was calculated as follows: MI = (DD – MD)/ET. From an apical view, flow propagation velocity (Vp) was measured using a color M-mode Doppler echocardiographic image recorded as previously described (21, 22). Using pulsed Doppler tissue imaging, we also recorded early lateral mitral annulus movement (Em) from the apical view and posterior wall movement (Epw) from the long-axis view as previously described (21, 26, 27). All measured and calculated indexes are presented as the average of three to five consecutive measurements.

Statistical analysis. Data are reported as means ± SD. Correlations were sought between all TTE parameters and invasive relaxation parameters [–dP/dtmin, {tau}, and (–dP/dtmin)/LVSP]. Correlation was significant if P < 0.05 was satisfied. Relationships were also sought between echocardiographically determined LV mass (LVM) and LVW, and bias and precision were calculated (27). Measurements of intraobserver reproducibility have been published previously (30).


   RESULTS
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 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Validation of echocardiographic and Doppler indexes of LV relaxation. In 20 SHR (mean weight: 393 ± 32 g) aged 33–80 wk old and 11 Wistar rats aged 30 wk (mean weight: 370 ± 39 g), we obtained 51 sets of data permitting comparison between invasive and noninvasive LV indexes (Tables 1 and 2). A good correlation was found between LVW and echocardiographically measured LVM (r = 0.82 and P < 0.001; y = 1.09x – 0.12) with a bias of 0.03 g and a precision of 0.30 g. In all rats, every index was measured with good reproducibility (30). Previously described noninvasive indexes of LV relaxation were related to {tau}, –dP/dtmin, and (–dP/dtmin)/LVSP, particularly IVRT, the Tei index, Em, Epw, and Vp (Table 2 and Fig. 1). Doppler indexes of LV diastolic function and –dP/dtmin were significantly correlated (r = 0.28–0.56 and P < 0.05–0.0001, respectively). When the influence of systolic load was taken into account, the correlation between Doppler indexes of LV function and relaxation rate [(–dP/dtmin)/LVSP] improved (r = 0.48–0.86 and P = 0.004–0.0001, respectively). Similarly, Doppler indexes of LV diastolic function and {tau} were significantly correlated (r = 0.50–0.84 and P = 0.0002–0.0001, respectively; Fig. 1).


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  		Table 1. Rat characteristics

 

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  		Table 2. Correlation between invasive and noninvasive indexes of LV relaxation

 


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  		Fig. 1. Correlations between the time constant of isovolumic left ventricular (LV) relaxation ({tau}) and Doppler LV relaxation indexes. IVRT, isovolumic relaxation time; Em, early velocity of the mitral annulus; Vp, propagation velocity.

 
Comparison between normotensive and hypertensive rats. Eight SHR and eight Wistar rats were studied (respective weight: 406 ± 22 and 386 ± 11 g; not significant). LVSP was higher in SHR (200 ± 43 vs. 130 ± 34 mmHg, P < 0.001). Noninvasive and invasive LV relaxation indexes were compared (Tables 3 and 4 and Figs. 2 and 3). LVEDD was similar, whereas SW, PW, and LVM as well as measured LVW were greater in SHR. IVRT and MI were significantly higher, and Epw as well as Em were lower in SHR. Similarly, {tau} was higher in SHR, demonstrating an impaired LV relaxation compared with normotensive rats. –dP/dtmin was more negative in SHR.


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  		Table 3. HR and LV and RV characteristics in SHR and Wistar rats

 

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  		Table 4. Invasive and Doppler LV diastolic function parameters in SHR and Wistar rats

 


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  		Fig. 2. IVRT, myocardial index, Em, and Vp of the mitral E wave in spontaneously hypertensive rats (SHR) and Wistar rats.

 


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  		Fig. 3. Invasive diastolic indexes in SHR and Wistar rats. LVEDP, LV end-diastolic pressure; LVSP, LV systolic pressure.

 
However, when the influence of LV systolic load on relaxation rate was taken into consideration, the load-independent index of relaxation, namely, (–dP/dtmin)/LVSP, demonstrated a slower relaxation rate in SHR, and this was also confirmed by the significantly higher {tau} value.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results of the present study demonstrate a close correlation between noninvasive echocardiographic indexes of diastolic function and invasive relaxation indexes. IVRT, mitral and diastolic duration time, and the Tei index as well as early mitral annulus velocity (analyzed using Doppler tissue imaging) and early diastolic mitral flow velocity (using color M-mode) were good indexes of LV relaxation. The best correlations were obtained between IVRT, Vp, Em, and Epw on the one hand and both (–dP/dtmin)/LVSP and {tau} on the other. Importantly, it must be recognized that IVRT is heart rate dependent (20, 28). Furthermore, whereas most echocardiographic relaxation indexes are load dependent, Vp is relatively independent on loading conditions in clinical studies (5, 8). However, Vp is more difficult to measure and has a lower intraobserver reproducibility compared with other Doppler indexes (30). In the present study, we reported a reasonably good correlation between the Tei index and invasive relaxation indexes, thus confirming a previous report (31). However, the Tei index is dependent on both systolic and diastolic function (31) and, therefore, may be altered by systolic dysfunction. Recently, Derumeaux et al. (7) demonstrated a close relationship between the Tei index and diastolic LV wall velocity gradient using color Doppler tissue imaging. This index of LV diastolic strain was used to compare ventricular relaxation in rats with physiological and pathological LV hypertrophy, but this method requires specific software and is not suitable for routine performance.

We also compared LV relaxation and diastolic function in SHR and Wistar rats using invasive measurements and echocardiographic and Doppler indexes. Confirming previous findings, we found –dP/dtmin to be more negative in SHR, suggesting an increased rate of relaxation (6). However, –dP/dtmin depends on LVSP, and, therefore, (–dP/dtmin)/LVSP may provide a more reliable and load-independent estimate of the initial part of the LV isovolumic relaxation (10, 32). In SHR, less negative (–dP/dtmin)/LVSP indicates a slower initial part of LV isovolumic relaxation compared with normal Wistar rats. Furthermore, the 50% higher {tau} value in SHR accounts for the slower late part of LV isovolumic relaxation. In previous isolated myocytes or isolated heart studies, the Tei index was increased in SHR compared with Wistar-Kyoto (WKY) rats (19). Cingolani et al. (6) showed in an in vivo study that the {tau} and mitral E-to-A (E/A) ratio were greater in SHR compared with WKY rats. However, the E/A ratio is dependent on many factors including heart rate and loading conditions, and, therefore, its interpretation should be made with caution. In our study, because heart rate was high, the E and A waves were often merged, and this compromised the value of the E/A ratio.

Many factors account for the impaired ventricular relaxation in SHR, including abnormal myocytic calcium kinetics, myofilament properties, cellular energetics, and neurohormonal activation (34). This impaired relaxation occurred early in the life of SHR.

Impaired LV compliance has been reported in older SHR and may be attributed to an increased fibrosis as well as altered cross-linked collagen (4). Ventricular wall compliance may be analyzed using Doppler techniques. Thus the slope of the mitral E wave was fitted to define indexes that closely related to the invasive LV stiffness constant (30, 33).

In the present study, heart rate was too rapid and the E and A waves were merged, preventing the analysis of the E wave slope.

The present study has several limitations. First, the anesthetic agent may modify diastolic as well as systolic functions and not necessarily similarly in different strains. Second, systematic modifications of preload, afterload, and contractility were not performed in this study. Third, neither strain (using Doppler tissue imaging) nor asynchrony (using Doppler tissue imaging or color kinesis) was quantified in this study (7, 18). Finally, statistical methods could be regarded as a possible limitation of this study. We used a classic statistical approach, and, as an estimate of variability, standard deviation and standard error were given. We have used these analyses in our prior reports with the physiological methods we used here (27–30). Other methods to assess variability, such as uncertainty analysis, might be appropriate, particularly for indexes that are not directly measured but derived from measured variables, such as the MI. This method should be used in the future. However, after review of these analyses, we decided to adhere to classic statistics for several reasons. First, we could not find a single example of evaluating physiological data by uncertainty analysis in the literature. This fact would, by inference, suggest that the majority of potential readers will not be familiar with the method and, consequently, will not appreciate our effort. We also emphasize that the intention of our study was to demonstrate usefulness of a comprehensive echocardiographic examination for the assessment of overall cardiac performance in rats rather than to scrutinize the validity of each echocardiographic index.

In conclusion, LV relaxation may be assessed validly using echocardiographic and Doppler techniques that permit long follow-up of rats. We demonstrated that IVRT was the best index in the assessment of LV relaxation; however, this index is sensitive to heart rate and may be used only if the same heart rate can be obtained in all animals. Two other indexes seem to be useful: flow Vp measured using color M-mode Doppler and Em from the apical view (or Epw) using pulsed Doppler tissue imaging. Using measured indexes, we demonstrated impaired relaxation in the hypertensive SHR compared with normotensive Wistar rats.


   ACKNOWLEDGMENTS
 
We thank Philips Medical System, who kindly loaned us the echocardiographic instrument used this study.


   FOOTNOTES
 

Address for reprint requests and other correspondence: M. Slama, Unité de Réanimation, Service de Néphrologie, CHU Sud Amiens 80054 Cedex 1, France (E-mail: MSlama0508{at}aol.com)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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