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Am J Physiol Heart Circ Physiol 286: H181-H185, 2004. First published September 4, 2003; doi:10.1152/ajpheart.00642.2003
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Long-term left ventricular echocardiographic follow-up of SHR and WKY rats: effects of hypertension and age

Michel Slama, Jwari Ahn, Jasmina Varagic, Dinko Susic, and Edward D. Frohlich

Research Division, Ochsner Clinic Foundation, New Orleans, Louisiana 70121

Submitted 3 July 2003 ; accepted in final form 18 August 2003


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Long-term follow-up of left ventricular (LV) function using echocardiography has not been reported and, in this study, was carried out in normotensive (WKY) rats and spontaneously hypertensive rats (SHR). In 10 WKY rats and SHR, LV diastolic and systolic diameter (LVEDD and LVSD), shortening fraction (SF), and weight (LVW) were determined at 8, 15, 20, 35, and 80 wk of age. The ratio of early to late mitral flow and mitral annulus velocity (VE/VA and Em/Am), isovolumic relaxation time (IVRT), deceleration time of the E wave (DTE), Tei index, and mitral flow propagation velocity (Vp) were measured. No difference in LVEDD was found between SHR and WKY rats; however, LVEDD was increased at 80 wk in both strains. SF decreased slightly in old WKY rats. LVW progressively increased from 20 to 80 wk in both strains and was greater in SHR. VE/VA and Em/Am decreased at 80 wk in WKY rats. LV relaxation (IVRT, Tei index, and Vp) was progressively impaired in SHR compared with WKY rats. LV compliance (DTE) was altered in old SHR. Echocardiography permitted a long follow-up of LV function in SHR and WKY rats. Ventricular relaxation was impaired early in the life of SHR and progressed with aging. Furthermore, LV compliance was altered, but systolic function remained unchanged, in old SHR. In contrast, relaxation and SF were only slightly altered in old WKY rats, suggesting that pressure-related changes in LV function were the dominant features in the SHR.

left ventricle; diastolic function; echocardiography; Doppler; longitudinal follow-up study

MOST HEMODYNAMIC STUDIES in rats have been performed using invasive techniques that lead to loss of the animal, thereby preventing longitudinal follow-up. Development of echocardiographic techniques permits analysis of left ventricular (LV) geometry, wall thickness, and LV mass (LVW) (11, 12). More recently, echocardiographic and Doppler techniques were used to assess systolic and diastolic function (3, 6, 9, 15, 16, 22, 28). Because these techniques are noninvasive, they provide an excellent opportunity to study cardiac function in the same animal over a long time and, thus, permit examination of long-term effects of pathological and natural events. Furthermore, a long-term follow-up of LV function, particularly diastolic function in spontaneously hypertensive rats (SHR) and normotensive rats to differentiate between cardiac effects of hypertension and aging, has never been performed. Therefore, the purpose of this study was to monitor LV function in normotensive Wistar-Kyoto (WKY) rats and SHR over an extensive time period with the use of echocardiographic and Doppler techniques and, in so doing, to learn more about the cardiac effects of aging and hypertension.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animals. Male SHR and WKY rats were purchased from Charles River Breeding Laboratories (Wilmington, MA) at 7 wk of age. They were maintained in temperature- and humidity-controlled rooms with a 12:12-h light-dark cycle and given standard chow (PMI Nutrition International, 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, echocardiography was used to screen all the rats for any comorbid congenital abnormalities (29).

Procedure. Echocardiography was performed in 10 pentobarbital sodium-anesthetized (50 mg/kg ip) rats of each strain at 8, 15, 20, and 35 wk of age. Two separate groups of 80-wk-old WKY rats and SHR were also studied. A first set of echocardiographic measurements was obtained 10–30 min after anesthesia administration at a heart rate of ~300 beats/min. After 15 min, xylazine (2 mg ip) was injected to decrease the heart rate to 215 beats/min, and the final measurements were recorded. In five to eight different anesthetized SHR and WKY rats at 8, 15, 20, 35, and 80 wk of age, an arterial catheter was introduced through the right femoral artery and then pushed into the abdominal aorta for measurement of arterial pressure.

Echocardiography. Transthoracic echocardiographic measurements were performed in the left lateral decubitus position with 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) with high frame rate (100–100 Hz and 24–30 Hz, respectively) using bidimensional and color Doppler imaging. The transthoracic echocardiographic probe was placed to obtain short- and long-axis and four-chamber (ventricles and atria) and five-chamber (ventricles, atria, and aorta) apical cardiac views. From the cardiac long axis, an M-mode trace of the LV was obtained, and LV end-diastolic diameter (LVEDD), LV systolic diameter (LVSD), and posterior and septal diastolic wall thicknesses (PW and SW) were measured following the American Society of Echocardiography guidelines (26). LVW was calculated as follows: LVW = 1.04 x [(LVEDD + PW + SW)3 – LVEDD3]. Shortening fraction (SF) was calculated according to the following equation: SF = (LVEDD – LVSD)/LVEDD. From a five-chamber apical view, aortic flow was recorded using pulsed Doppler imaging, with the smallest sample volume placed at the level of the aortic annulus. LV ejection time (ET) was measured as the time from the beginning to the end of the aortic flow wave. Mitral flow was recorded at the tip of the mitral valve from an apical view using Doppler imaging. We measured maximal velocities of the E and A waves (VE and VA), the velocity-time integral (VTI) of the E and A waves (VTIE and VTIA), and deceleration time of the E wave (DTE) as the interval between the peak early diastolic velocity and the point where the steepest deceleration slope was extrapolated to the baseline (2, 7, 10, 14). VE/VA and VTI were calculated. Isovolumic relaxation time (IVRT) was measured as the interval between the aortic closure click and the start of mitral flow. Using the same tracing, we measured the time between the closure and opening of the aortic valve (DD) and between the opening and closure of the mitral valve (MD). Myocardial index (MI), described by Tei et al. (32), was calculated as follows: MI = (DD – MD)/ET. From an apical view, Vp was measured using a color M-mode Doppler echocardiographic image, recorded as previously described (4, 23). Using pulsed Doppler tissue imaging, we also recorded wall movement at the level of the lateral mitral annulus from the apical view, as previously described, and also measured maximal velocity of early (Em) and late (Am) diastolic waves. Em/Am was calculated (18, 27, 31). All measured and calculated indexes are presented as the average of three to five consecutive measurements.

Statistical analysis. Values are means ± SE. All indexes were compared using repeated-measures analysis of variance, with a 5% confidence level indicating significant differences. Measurement of intraobserver reproducibility was assessed in nine rats. Echocardiography was performed twice on each rat 2 days apart. This reproducibility was assessed as the mean difference between two measurements, presented as mean percent error (absolute difference divided by an average of the 2 observations).


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Intraobserver reproducibility of echocardiographic and Doppler measurements was excellent (Table 1). Arterial pressure and body weight values are presented in Table 2. During the follow-up period, arterial pressure was always greater in SHR than in WKY rats; it increased from 8 wk, reached a plateau at 15 wk, and increased further at 80 wk in both strains. LVEDD remained stable until 35 wk; it also increased at 80 wk in the WKY rats. LVEDD increased progressively over the lifetime of the SHR (Table 2). There were no differences between WKY rats and SHR with respect to LVEDD or LVSD. SF was similar in SHR and WKY rats and remained at the same level throughout the study period (Table 2). The absolute LVW increased with age in SHR and WKY rats (Table 2). LVW was significantly higher in SHR at 20, 35, and 80 wk than in WKY rats. IVRT was significantly greater in SHR than in WKY rats; it increased with age in SHR and remained at the same level from 8 to 80 wk in WKY rats (Fig. 1). Myocardial performance index (Tei index) was higher in SHR than in WKY rats; it increased from 8 to 15 wk and remained stable at 20, 35, and 80 wk in SHR (Fig. 2). Diastolic duration (MD) was shorter in SHR than in WKY rats and remained stable with aging (Fig. 3). Vp was slower in SHR than in WKY rats at 20, 35, and 80 wk. Moreover, Vp decreased from 8 to 80 wk in SHR but did not change in WKY rats (Fig. 4). DTE was higher in WKY rats than in SHR (Fig. 5). In WKY rats, DTE was greater at 80 wk than at earlier ages. At 300 beats/min only, VE and VTIE (as well as Em) were obtained in all WKY and SHR rats. Merging of E and A waves and Em and Am was observed in 70% of SHR and 20% of WKY rats. After injection of xylazine, heart rate decreased to ~215 beats/min when E and A waves and Am and Em became distinguished. VE/VA decreased at 80 wk in WKY rats. At 15, 20, and 35 wk, VE/VA was greater in SHR than in WKY rats (Table 3). Em/Am decreased at 35 and 80 wk in WKY rats.


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  		Table 1. Reproducibility of echocardiographic and Doppler parameters

 

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  		Table 2. Weight and echocardiographic measurements

 


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  		Fig. 1. Trends in isovolumic relaxation time (IVRT) measured at 300 beats/min in spontaneously rats (SHR) and Wistar-Kyoto (WKY) rats at 8, 15, 20, 35, and 80 wk. *P < 0.05 vs. 8 wk; {ddagger}P < 0.05 vs. WKY at the same age.

 


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  		Fig. 2. Trends in myocardial index measured at 300 beats/min in SHR and WKY rats at 8, 15, 20, 35, and 80 wk. *P < 0.05 vs. 8 wk; {ddagger}P < 0.05 vs. WKY at the same age.

 


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  		Fig. 3. Trends in duration of mitral flow measured at 300 beats/min in SHR and WKY rats at 8, 15, 20, 35, and 80 wk. *P < 0.05 vs. 8 wk; {ddagger}P < 0.05 vs. WKY at the same age.

 


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  		Fig. 4. Velocity of early mitral flow propagation into the left ventricle (Vp) measured at 300 beats/min in SHR and WKY rats at 8, 15, 20, 35, and 80 wk. *P < 0.05 vs. 8 wk; {ddagger}P < 0.05 vs. WKY at the same age.

 


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  		Fig. 5. Deceleration time of mitral E wave (DTE) measured at 215 beats/min in SHR and WKY rats at 8, 15, 20, 35, and 80 wk. *P < 0.05 vs. 8 wk; {ddagger}P < 0.05 vs. WKY at the same age.

 

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  		Table 3. Mitral flow and mitral annulus velocities at 215 beats/min

 


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results of this study demonstrate that echocardiography can be used to follow LV function over the lifetime of the rats. Hypertension adversely affected diastolic function in the SHR, inasmuch as echocardiographic and Doppler indexes demonstrated impaired LV relaxation before a measurable increase in LVW and an alteration of LV compliance. In contrast, diastolic function was only slightly modified by age in the WKY rats. LV relaxation declined in SHR, as demonstrated by a progressive increase in IVRT and a decrease in Vp. However, LV diameter and LVW increased with age in SHR and WKY rats without modification of systolic function. Therefore, adult SHR may be considered an excellent model of isolated diastolic dysfunction (with impaired relaxation) without systolic dysfunction.

Echocardiography has been demonstrated to be a reliable method to assess diastolic function in clinical and experimental settings (6, 15, 18), and a number of indexes, such as the E-to-A wave ratio (E/A) and Em/Am, IVRT, MI, and Vp, have been used for that purpose.

Recently, Masuyama et al. (15) described a model of diastolic dysfunction in Dahl salt-sensitive rats fed a high-salt diet. After 6 wk, they obtained an obvious impairment of LV relaxation with a high invasively obtained relaxation time constant ({tau}) and a decreased E/A. After 12 wk of the high-salt diet, E/A increased dramatically, although no further modification of {tau} was observed, as explained by an increased LV diastolic pressure. Therefore, in the absence of invasive measurement, it would be difficult to analyze and explain variations of E/A. Moreover, E/A could be analyzed, because heart rate had decreased to nonphysiological values as a result of anesthesia with xylazine and ketamine, which could have modified myocardial function (25). In the present study, we observed a merge of E/A in SHR at 300 beats/min, which could be considered a sign of diastolic dysfunction (17). However, it was not possible to analyze this ratio further, because, even in 20% of WKY rats, it was impossible to distinguish the E and A waves. To analyze E/A further, we injected xylazine to decrease heart rate. Under this condition, E/A was decreased in old WKY rats, and we interpreted this as a trivial LV relaxation impairment. E/A increased in adult SHR and returned to baseline values at 80 wk, which is difficult to interpret. In many clinical studies, E/A was modified not only by relaxation or compliance but also by heart rate, LV preload, contractility, afterload, and left atrial compliance (30). Therefore, interpretation of any modification of E/A in terms of relaxation or compliance impairment should be made with caution.

Em/Am has been described as a good index of diastolic dysfunction, either compliance or relaxation, but load independence of this index must be considered (18, 27, 31). No difference was found between WKY rats and SHR. A decreased value was found at 35 and 80 wk in WKY rats, and this should be interpreted with caution as an impaired relaxation or compliance. Myocardial velocity has been studied by Derumeaux et al. (6) using a new method of Doppler tissue imaging in a rat model of pressure-overload LV hypertrophy (LVH). They observed a systolic and diastolic myocardial velocity gradient, despite preserved systolic function (6). This technique requires special software, which was not used in the present study.

IVRT has been described as a strong index of relaxation in clinical studies (30). In our study, IVRT was not modified with age in WKY rats. In contrast, IVRT was longer in SHR than in WKY rats, and it increased further over the lifetime of the animals.

MI [developed by Tei et al. (32)] has been found to be correlated with +dP/dt and –dP/dt and increased with systolic or diastolic dysfunction in clinical studies (18); it has never been analyzed in rats. In the present study, MI remained unchanged with age in WKY rats, but in SHR; it increased from 8 to 15 wk and did not change during the follow-up period and was greater in WKY rats.

Vp has also been proposed as an index of relaxation (4). Brun et al. (4) found a good correlation between Vp and {tau}. Many clinical studies confirmed this early study and found a decreased velocity in patients with LVH or coronary disease (4, 8). This index was independent of different load situations (8), and there was no modification of Vp in WKY rats. In contrast, SHR demonstrated a progressive decrease of this index from 8 to 80 wk.

With the use of isolated myocytes or a heart preparation in vitro, relaxation was demonstrated to be normal in young SHR (21). In an in vivo study in which LV diastolic function was analyzed using {tau}, Nishimura et al. (19) demonstrated that this time was prolonged in the 28- and 50-wk-old SHR compared with WKY rats but not in 15-wk-old rats. In the same way, Cingolani et al. (5) demonstrated a diastolic dysfunction in adult rats (10- to 11-mo-old SHR) with increased {tau} associated with increased systolic performance when analyzed invasively. In the present study, for the first time, we followed LV relaxation in SHR and WKY rats. We demonstrated a normal LV systolic function, associated with an impairment of LV relaxation in SHR, which was present early in life and progressively increased over the lifetime of SHR.

The study of LV rigidity is more complicated with ultra-sound. DTE was described as an index of this rigidity (13). Recently, to better analyze diastolic chamber stiffness, a parameterized diastolic filling model was used clinically and in dogs (10, 13). However, rigidity implies diminished LV compliance and is also influenced by relaxation. To measure DTE in SHR, it is necessary to slow the heart rate. Thus, in this study, DTE was shorter in old SHR than in old WKY rats, suggesting greater LV stiffness.

A number of limitations could be identified in this study. Diastolic properties were studied without validation against a gold standard method, but we hypothesized that all the indexes validated in clinical studies could also be used to analyze ventricular function in rats. Furthermore, the present study was performed in anesthetized rats, in which there could be cardiovascular effects. Xylazine was used in this study to decrease heart rate. Therefore, data obtained after xylazine injection should be interpreted with caution, because xylazine might affect hemodynamics and sympathetic nervous system activity.

In conclusion, echocardiography permitted us to noninvasively follow LV function in SHR and WKY rats. Relaxation studied with Doppler techniques seemed to be impaired (even before development of massive LVH) progressively over the lifetime of SHR, suggesting that pressure-related changes in LV function, which are potentially treatable, are most dominant. To the contrary, we demonstrated a slight effect of age on diastolic function in WKY rats, as demonstrated in clinical studies (1, 33, 36, 37). Compliance was found to be impaired in old SHR (rather than in old WKY), and this could be related to LV fibrosis in SHR (34).


   ACKNOWLEDGMENTS
 
Philips Medical System kindly loaned the echocardiographic instrument used this study.

GRANTS

This work was supported by an award from the American Heart Association, Southeast Affiliate.


   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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 DISCUSSION
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