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Am J Physiol Heart Circ Physiol 293: H496-H502, 2007. First published March 23, 2007; doi:10.1152/ajpheart.00087.2007
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Acute myocardial infarction in mice: assessment of transmurality by strain rate imaging

Hélène Thibault,1,2,* Ludovic Gomez,2,* Erwan Donal,3 Gerard Pontier,4 Marielle Scherrer-Crosbie,5 Michel Ovize,1,2 and Geneviève Derumeaux1,2

1Institut National de la Santé et de la Recherche Médicale E 0226, Université Claude Bernard Lyon I and 2Hôpital Louis Pradel, Hospices Civils de Lyon, Lyon, 3Hôpital Pontchaillou, Rennes, and 4Hôpital Charles Nicolle, Rouen, France; and 5Massachusetts General Hospital, Boston, Massachusetts

Submitted 20 January 2007 ; accepted in final form 19 March 2007


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In vivo evaluation of the transmural extension of myocardial infarction (TEI) is crucial to prediction of viability and prognosis. With the rise of transgenic technology, murine myocardial infarction (MI) models are increasingly used. Our study aimed to evaluate systolic strain rate (SR), a new parameter of regional function, to quantify TEI in a murine model of acute MI induced by various durations of ischemia followed by 24 h of reperfusion. Global and regional left ventricular (LV) function were assessed by echocardiography (13 MHz, Vivid 7, GE) in 4 groups of wild-type mice (C57BL/6, 2 mo old): a sham-treated group (n = 10) and three MI groups [30 (n = 11), 60 (n = 10), and 90 (n = 9) min of left coronary artery occlusion]. Conventional LV dimensions, anterior wall (AW) thickening, and peak systolic SR were measured before and 24 h after reperfusion. Area at risk (AR) was measured by blue dye and infarct size (area of necrosis, AN) and TEI by triphenyltetrazolium chloride staining. AN increased with ischemia duration (25 ± 2%, 56 ± 5%, 71 ± 6% of AR for 30, 60, and 90 min, respectively; P < 0.05). LV end-diastolic volume significantly increased with ischemia duration (30 ± 5, 34 ± 5, 43 ± 5 µl; P < 0.05), whereas LV ejection fraction decreased (63 ± 5%, 58 ± 6%, 46 ± 5%; P < 0.05). AW thickening decrease was not influenced by ischemia duration. Conversely, systolic SR decreased with ischemia duration (13 ± 5, 4 ± 3, –2 ± 6 s–1; P < 0.05) and was significantly correlated with TEI (r = 0.89, P < 0.01). Receiver operating characteristic (ROC) curves identified systolic SR as the most accurate parameter to predict TEI. In conclusion, in a murine model of MI, SR imaging is superior to conventional echocardiography to predict TEI early after MI.

echocardiography; murine model

WITH THE DEVELOPMENT of genetically modified mice, murine models of myocardial infarction (MI) are increasingly used, in particular to explore the molecular pathways involved in left ventricular (LV) remodeling (3, 7, 19, 35) and to assess the effect of innovative cardioprotection therapies on infarct size (10, 23, 35).

After MI, the alteration of global and regional LV function and the presence of myocardial viability depend on both the infarct size and the transmural extension of necrosis in relation to the duration of ischemia (4, 5, 29). In addition, infarct size is a major determinant of mortality (26, 27), justifying the development of new therapeutic strategies to reduce infarct size (15, 26, 27, 37). Therefore, accurate assessment of the infarct size and differentiation between transmural and nontransmural infarction are crucial in the prediction of prognosis.

Triphenyltetrazolium chloride (TTC) staining is the reference method to assess the transmural extension of necrosis but has the disadvantage of being an experimental postmortem technique (41). Cardiac imaging modalities such as nuclear scintigraphy (44), magnetic resonance imaging (18), and contrast echocardiography (12, 34) have been adapted to enable the imaging of small animals and have attempted to quantify myocardial extension of necrosis. However, these techniques are not widely available and are relatively invasive, and their spatial and temporal resolutions are limited.

The small size and rapid heart rate of mice challenge the accuracy of echographic studies of cardiac structure and function, but the introduction of high-frequency ultrasound transducers has overcome these limitations (33). However, conventional echocardiography cannot differentiate between ischemic, stunned, and infarcted myocardium (9). In contrast, strain rate (SR) imaging reliably measures myocardial deformation (39) and can accurately identify ischemic myocardial dysfunction (1, 16, 42) and differentiate transmural from nontransmural necrotic myocardial segments in large animals or humans (8, 28, 43, 46). The use of SR was recently validated in mice versus sonomicrometry (36) but has not yet been assessed to explore transmural extension of necrosis in a murine model of MI.

The objective of this study was to assess whether SR imaging is able to evaluate the transmural extension of necrosis in a murine model of acute MI induced by various durations of ischemia followed by 24 h of reperfusion.


   METHODS
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 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This study conformed to the Guide for the Care and Use of Laboratory Animals and was approved by our Institutional Animal Care and Use Committee.

Surgical preparation. Mice (C57BL/6; 2 mo old, weight 26 ± 1 g) were anesthetized by intraperitoneal injection of 0.3 ml/10 g body wt of a 1:1 mixture of fentanyl citrate (0.011 mg/ml) and midazolam (0.4 mg/ml), as previously described (13). The animals were orally intubated with a 22-gauge vinyl catheter and ventilated via a rodent ventilator (model 687, Harvard Apparatus) with a tidal volume of 0.2 ml and a breath rate of 160 breaths/min. The heart was exposed after a left thoracotomy, and a left coronary artery (LCA) occlusion was performed by tightening an 8-0 polypropylene silk suture mounted on a tapered needle ~2 mm distal to the border of the left atrial appendage, around a 1-mm piece of PE-10 tubing, forming a loose snare around the LCA. To release the ligature, the silk snare was loosened, and reperfusion was confirmed by visual inspection and reduction of the ST segment shift on the ECG. The suture material was left in place to allow subsequent documentation of precisely the same risk territory. ECG was recorded throughout the surgical preparation. Body temperature was monitored by a rectal thermometer and maintained at 36–37°C with a heating pad. After surgery mice were allowed to recover from anesthesia, and the endotracheal tube was removed once spontaneous breathing resumed.

Experimental protocol. We divided 58 mice into four groups according to the duration of the LCA occlusion (coronary occlusion, CO): 0 min (Sham group; n = 10), 30 min (30-CO group, n = 16), 60 min (60-CO group; n = 17), and 90 min (90-CO group; n = 15).

In all groups, CO was followed by 24 h of reperfusion. Echocardiography was performed in all mice at baseline and 24 h after reperfusion, immediately before euthanasia.

Echocardiography. Echocardiography was performed under light anesthesia (ketamine 80 mg/kg ip). Images were acquired with a 13-MHz linear-array transducer with a digital ultrasound system (Vivid 7, GE Medical Systems).

Conventional measurements [LV diameters, anterior wall (AW) and posterior wall (PW) thickness and thickening] were obtained from grayscale M-mode tracings at the level of the papillary muscles. LV end-systolic and end-diastolic volumes and LV ejection fraction (LVEF) were measured by Simpson's method from two-dimensional parasternal long- and short-axis (basal, mid, and apical level) views, as previously described (35).

SR images (SRI) were obtained from the parasternal short-axis views at the midventricular level, at a frame rate of 450 frames/s and a depth of 1 cm (36). SRI analysis was performed off-line by an observer (H. Thibault) blinded to the TTC results (EchoPac Software, GE Medical). Radial systolic SR was measured over an axial distance of 0.6 mm. The temporal smoothing filters were turned off for all measurements. Peak systolic SR was averaged over five consecutive cardiac cycles. Intra- and interobserver variability of systolic SR were measured within the anterior wall in 10 normal mice by 2 independent observers (H. Thibault and G. Derumeaux).

Area at risk and infarct size determination. At the end of the 24 h of reperfusion, the LCA was briefly reoccluded and 0.5 mg/kg of Unisperse blue pigment (Ciba-Geigy, Hawthorne, NY) was injected intravenously to delineate the in vivo area at risk (AR), as previously described (13).

The heart was excised and cut into four transverse slices, parallel to the atrioventricular groove. After right ventricular tissue was removed, each heart slice was weighed. The basal surface of each slice was photographed for later measurement of the AR. Each slice was then incubated for 30 min in a 1% solution of TTC at 37°C to differentiate infarcted (pale) from viable (brick red) myocardial area (41). The slices were then rephotographed. Enlarged projections of these slices were traced for determination of the boundaries of the AR and the area of necrosis (AN). The extent of the AR and the AN was quantified by computerized planimetry and corrected for the weight of the tissue slices. Total weights of the AR and AN were then calculated and expressed in grams and as percentages of total LV or AR weight, respectively.

In addition, at the papillary muscle level, LV short-axis images were segmented into four equal quadrants corresponding to the following myocardial segments: anterior, posterior, lateral, and septal. The degree of transmural extension of infarction (TEI) from the epicardium toward the endocardium (TTC-negative areas, expressed in % of wall thickness) was assessed within the anterior segments (Fig. 1) in order to be compared with the SR values, as previously described (8). TEI was measured by two independent observers blinded to the echocardiography results (L. Gomez, E. Donal). A transmural MI was arbitrarily defined as an extension over 75% of the AW thickness (4).


Figure 1
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  		Fig. 1. Examples of determination of transmural extension of infarction (TEI), as % of anterior wall (AW) thickness, at the mid-left ventricular level after triphenyltetrazolium chloride staining. A: example of a Sham group animal. B: example of a 60-min ischemic animal. PW, posterior wall; LW, lateral wall.

 
Statistics. In this study, TTC staining was the "gold standard" for measuring the transmural extent of MI. StatView 5.0 (Abacus Concepts, Berkeley, CA) statistical software was used. Values are expressed as means ± SE. Comparison between groups was performed by one-way ANOVA and Bonferonni test. After the testing for inequality of variances, the difference between echocardiographic variables before and after surgery was tested by ANOVA for repeated measurements. A P value <0.05 was considered as indicative of a statistically significant difference. Receiver operating characteristic (ROC) were analyzed for echographic and SRI parameters to determine the best imaging parameter in identifying transmural MI (i.e., TEI ≥75%). Sensitivities and specificities were calculated for wall thickening and systolic SR. Interobserver and intraobserver variability were calculated as the difference ± SD between the two observations and expressed as percentages.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Mortality and exclusions. In the ischemia-reperfusion groups, 18 mice died before completion of the experiment. There was no death in the Sham group. Echographic, SR, and colorimetric measurements were interpretable in the 40 animals that completed the whole protocol (n = 10 in Sham group, n = 11 in 30-CO group, n = 10 in 60-CO group, n = 9 in 90-CO group).

Area at risk and infarct size. AR involved the apical, midposterior, and midanterior segments and was comparable among the three groups [38 ± 2% vs. 37 ± 2% vs. 39 ± 1% of LV in 30-, 60-, and 90-CO groups, respectively; P = not significant]. AN significantly increased with the duration of the LCA occlusion (25 ± 2% vs. 56 ± 5% vs. 71 ± 6% of AR in 30-, 60-, and 90-CO groups, respectively; P < 0.05) (Fig. 2). TEI in the AW significantly increased with the duration of CO from 40 ± 25% (30-CO) to 80 ± 18% (60-CO) and 99 ± 2% (90-CO) (P < 0.01). The Sham group had no necrosis (TEI = 0%).


Figure 2
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  		Fig. 2. Area at risk and infarct size. A: area at risk (AR; left) and infarct size (area of necrosis, AN; right) obtained in 3 groups of animals according to the duration of the coronary occlusion (CO; 30, 60, and 90 min, respectively). AR was similar among the 3 groups. AN significantly increased with duration of ischemia. *P < 0.05. B: infarct size as a function of AR. The increase in AN with duration of CO is not related to the increase in AR.

 
Conventional echocardiographic parameters. At baseline, all conventional parameters were comparable among the Sham group and the three ischemia-reperfusion groups (Table 1).


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  		Table 1. Echocardiographic measurements at baseline

 
After 24 h of reperfusion (Table 2), LV volumes significantly increased and LVEF and AW thickening decreased in the three ischemia-reperfusion groups compared with baseline values (ANOVA, P < 0.01). The mean decrease in AW thickening was similar in the three CO groups: 39 ± 20% in the 30-CO group, 45 ± 14% in the 60-CO group, and 55 ± 15% in the 90-CO group (Table 2, Fig. 3A). PW thickening significantly decreased only in the 90-CO group but was unchanged in the 30-CO and 60-CO groups compared with baseline values. In addition, the duration of CO led to a significant increase in LV end-diastolic diameter and volumes and decrease in LVEF. Sham group parameters were comparable at baseline and 24 h after surgery.


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  		Table 2. Echocardiographic measurements at 24 h of reperfusion

 

Figure 3
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  		Fig. 3. Wall thickening and strain rate (SR) at baseline and at 24 h of reperfusion for the 4 groups of animals. A: wall thickening. B: peak systolic SR. *P < 0.05 vs. baseline.

 
Strain rate. Interobserver and intraobserver variability of SR measurements were 7.2 ± 3.8% and 8.0 ± 4.6%, respectively. At baseline, SR values did not differ among the Sham group and the three ischemia-reperfusion groups and within the AW and the PW (Table 1).

After 24 h of reperfusion (Table 2, Fig. 3B), systolic SR significantly decreased in the three ischemia-reperfusion groups both within the AW (Fig. 4) and, to a lesser extent, within the PW compared with baseline values. In addition, AW systolic SR significantly decreased with the duration of CO by 51 ± 33% in the 30-CO group, 83 ± 11% in the 60-CO group, and 106 ± 19% in the 90-CO group (P < 0.05; Table 2). Sham group parameters remained unchanged between baseline and 24 h after surgery.


Figure 4
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  		Fig. 4. AW SR curves obtained at baseline and at 24 h of reperfusion in a mouse from the 60-CO group. After ischemia-reperfusion, SR decreased in the infarcted area compared with baseline. Arrows indicate the peak systolic SR.

 
Assessment of infarct transmural extension. Both AW thickening and systolic SR were significantly correlated with TEI within the AW (Fig. 5A). By ROC analysis, systolic SR was the best parameter to identify transmural MI as defined by TEI ≥ 75% (area under the curve: 97; P < 0.05) (Fig. 5B). A systolic SR cutoff of 7 s–1 identified transmural myocardial infarcted segments with a sensitivity and a specificity of 90% (95% confidence interval: 87–99%), whereas an AW thickening cutoff of 33% identified transmural myocardial infarcted segments with a sensitivity and a specificity of 72% (95% confidence interval: 64–91%).


Figure 5
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  		Fig. 5. Determination of TEI. A: AW thickening (%; left) and peak systolic SR (s–1; right) values measured at 24 h of reperfusion according to TEI determined by TTC. B: receiver operating characteristic curves for identification of segmental myocardial TEI. Area under curve (AUC) is given for AW thickening and peak systolic SR.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In this murine model of acute MI, our study identifies an important role for noninvasive echocardiography and particularly SR imaging in quantifying the TEI induced by various durations of coronary artery occlusion. This is to our knowledge the first report showing the graded decrease of SR imaging associated with the increase in transmurality of acute MI in mice.

Transmural MI is associated with a poorer prognosis, a lack of myocardial viability, and further enlargement and remodeling of the LV (2). Therefore, the early differentiation of transmural from nontransmural MI is particularly important.

Since infarct size and transmurality increase with the duration of ischemia (4, 5, 29), we used different durations of LCA occlusion (30, 60, and 90 min) to obtain various values of MI transmurality (22) as opposed to permanent coronary artery ligation or cryoinjury leading to transmural MI (40). Mortality (31%) was similar to that reported in previously described murine ischemia-reperfusion models (30).

Our results are important in regard to the growing use of murine MI models in the experimental area. The development of murine models of altered cardiac function (14, 24, 38) and ischemia (45) has led to the need for dedicated instruments to reliably assess in vivo cardiac alterations and to replace ex vivo techniques. The primary challenge in developing cardiovascular imaging for mice is attaining an adequate spatial and temporal resolution to resolve the millimeter-thick murine myocardium and the high heart rate. High-frequency echocardiography and high-field magnetic resonance imaging are currently the most prominent methods for imaging the heart in small animals (6, 31). They provide cardiac images with excellent temporal and spatial resolution, permitting measurement of ventricular volume and mass as well as functional parameters, such as LVEF (6, 17). However, magnetic resonance imaging remains costly and of limited availability, whereas echocardiography is increasingly used in small animal studies. Radionuclide techniques, such as positron emission tomography and single-photon emission computed tomography, have been applied recently to produce functional cardiac images, but they cannot approach the spatial resolution of the anatomic imaging modalities (44).

In the setting of ischemia-reperfusion experiments, cardiac ultrasound imaging therefore has a key role in assessing the consequences of the extent of MI on both the global and the regional myocardial function. Whereas LV fractional shortening and volumes aim to assess the consequences of MI on global LV systolic function and remodeling, SR imaging specifically analyzes regional myocardial function. Recent experimental studies in large animals (8, 28, 43) and clinical studies (32, 46) have demonstrated that assessment of regional deformation by SR imaging is superior to wall thickening in differentiating viable from infarcted myocardium and in assessing the severity of MI transmurality.

Recently, SR imaging was validated versus sonomicrometry in mice by Sebag et al. (36), and the same group showed the potential of this technique to detect subtle alterations in myocardial function early in a murine model of doxorubicin-induced cardiac injury (24). In the present mouse model of ischemia-reperfusion, we demonstrated that the measurement of regional deformation by systolic SR can accurately differentiate between transmural and nontransmural MI.

After 24 h of reperfusion, wall thickening and systolic SR significantly decreased in the infarcted area (AW). Both SR and wall thickening were correlated with TEI within the AW. However, ROC analysis demonstrated the superiority of systolic SR over wall thickening in differentiating nontransmural from transmural MI as defined as a percentage of necrosis ≥75% of the AW thickness by TTC.

Our results in this murine model of MI are in concordance with previous clinical and experimental studies in large animals. Regional wall thickening has been shown to become abnormal only when MI affects 30–50% of myocardium (20, 21, 25). This underestimation of the MI transmurality by wall thickening may be explained by the presence of normally contracting neighboring segments and by the fact that wall thickening mainly depends on subendocardial contraction, whereas MIs are mostly subepicardial in this murine model. The value of regional deformation in the quantification of MI transmurality was initially demonstrated in an acute infarct model in dogs using the radial transmural velocity gradient (8) and then in a chronic MI model in pigs using SR imaging (43). More recently, some clinical studies have confirmed the value of SR imaging for assessing the transmural extent of MI and predicting viability, using magnetic resonance imaging as a reference method for quantifying the transmural extent of infarct (32, 46). The implications of this technique in murine models of MI are important when it is applied in new therapeutic strategies to reduce infarct size such as pre- and postconditioning, cell transplantation, or gene therapy (10, 11, 23, 35). SR imaging might help in identifying a subtle improvement in regional myocardial function, not otherwise detectable with conventional techniques.

Limitations.

We focused our analysis on radial function since apical views are difficult to obtain and poorly reproducible in small rodents, precluding the reliable analysis of longitudinal velocities and SR. Evaluation of TEI was done at midventricular level using only one pathological slice and one echocardiographic view for M-mode tracing and SR measurement.

Conclusions.

SR decreased early after MI and was able to predict TEI early with excellent sensitivity and specificity. SR imaging has the potential to be used to evaluate the efficiency of new therapeutic strategies, developed on murine MI models, to reduce infarct size.


   ACKNOWLEDGMENTS
 
H. Thibault was a recipient of a grant from the Académie Nationale de Médecine.


   FOOTNOTES
 

Address for reprint requests and other correspondence: G. Derumeaux, Faculté de Médecine Lyon Nord, INSERM E 0226, 8, Ave. Rockefeller, 69373 Lyon cedex 8; France (e-mail: genevieve.derumeaux{at}chu-lyon.fr)

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.

* H. Thibault and L. Gomez contributed equally to this work. Back


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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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