EXPERIMENTAL STUDY
Validation of in vivo myocardial strain measurement by magnetic resonance tagging with sonomicrometry
Susan B. Yeon, MD, FACC*,
Nathaniel Reichek, MD, FACC ,
Barbara A. Tallant, VMD ,
João A. C. Lima, MD, FACC ,
Linda P. Calhoun, MD, FACC,
Neil R. Clark, MD, FACC,
Eric A. Hoffman, PhD||,
Kalon K. L. Ho, MD, MSc, FACC* and
Leon Axel, PhD, MD ¶
* Cardiovascular Division, Department of Medicine, Beth Israel Deaconess Medical Center, Boston, Massachusetts, USA
Division of Cardiology, Department of Medicine, Allegheny General Hospital, Pittsburgh, Pennsylvania, USA
Cardiovascular Division, Department of Medicine, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania, USA
Cardiology Division, Department of Medicine, Johns Hopkins University, Baltimore, Maryland, USA
|| Department of Radiology, University of Iowa College of Medicine, Iowa City, Iowa, USA
¶ the Devon Imaging Center and Pendergrass Laboratory, Department of Radiology, University of Pennsylvania, Philadelphia, Pennsylvania, USA
Manuscript received November 7, 2000;
revised manuscript received March 9, 2001,
accepted April 25, 2001.
Reprint requests and correspondence: Dr. Susan B. Yeon, Cardiovascular Division, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston, Massachusetts 02215
syeon{at}caregroup.harvard.edu
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Abstract
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OBJECTIVES
This study was designed to validate strain measurements obtained using magnetic resonance tagging with spatial modulation of magnetization (SPAMM). We compared circumferential segment shortening measurements (%S) obtained using SPAMM to sonomicrometry %S in a canine model with (n = 28) and without (n = 3) coronary artery ligation.
BACKGROUND
Magnetic resonance tagging enables noninvasive measurement of myocardial strain, but such strain measurements have not yet been validated in vivo.
METHODS
Circumferential sonomicrometry crystal pairs were placed in apical myocardium at ischemic risk in ligation studies and in adjacent and remote myocardium. The %S was obtained from closely juxtaposed sonomicrometry and SPAMM sites.
RESULTS
Paired data were available from 19 of 31 studies. Both methods distinguished remote from ischemic function effectively (p = 0.014 for SPAMM and p = 0.002 for sonomicrometry). SPAMM %S was similar to sonomicrometry %S in ischemic myocardium (2 ± 3 vs. 0 ± 3, p = 0.067) but was slightly higher than sonomicrometry %S in remote myocardium (11 ± 10 vs. 7 ± 5, p = 0.033). End-systolic (n = 30) and late systolic (n = 34) SPAMM %S correlated well with sonomicrometry %S (r = 0.84, p < 0.0001 and r = 0.88, p < 0.0001).
CONCLUSIONS
Magnetic resonance tagging using SPAMM can quantitate myocardial strain in ischemic and remote myocardium. This study validates its application in scientific investigation and clinical assessment of patients with myocardial ischemia.
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Abbreviations and Acronyms
| | %S | = circumferential shortening measurement | | ED | = end-diastolic | | ES | = end-systolic | | LS | = late-systolic | | MRI | = magnetic resonance imaging | | SPAMM | = spatial modulation of magnetization |
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Myocardial mechanical function can be imaged by silhouette techniques, such as contrast and radionuclide ventriculography, and tomographic techniques such as echocardiography, fast computed tomography and cardiac magnetic resonance imaging (MRI). With these methods, regional contraction can be assessed by measurement of endocardial excursion (1–4). However, endocardial excursion is not a direct measure of intramural myocardial shortening (5). Tomographic techniques are also commonly used to assess wall thickening, a more direct index of intramural function (6). However, assessment of wall thickening is affected by in-plane and through-plane myocardial motion (7,8). In addition, transmural gradients in function in normal and ischemic myocardium cannot be resolved by wall thickening analysis (9–11). Therefore, myocardial point tracking is required for spatially detailed characterization of function including assessment of transmural heterogeneity. Such material point tracking cannot be performed by conventional imaging techniques. Experimental methods used to measure myocardial strain are sonomicrometry and cineroentgenographic tracking of radio-opaque intramyocardial markers (10–13). Limitations in the applicability of these techniques include their invasive nature, the relatively limited sampling of myocardium they permit and potential tethering and myocardial injury produced by crystal or marker implantation. Magnetic resonance tagging techniques enable noninvasive demonstration of segmental myocardial shortening (14,15). Spatial modulation of magnetization (SPAMM) is one such technique, which produces grids of stripes on two-dimensional images (15,16). The stripes deform with myocardial motion, thus providing detailed noninvasive tracking of myocardial motion.
In vitro strain estimation using SPAMM has been validated using a deformable silicone gel phantom (17). Magnetic resonance tagging has been used to measure strains and torsional deformation of the heart in normal subjects (8,18–20) and athletes (19); in patients with myocardial infarction (18), dilated cardiomyopathy (20), hypertrophic cardiomyopathy (21,22) and aortic stenosis (19); and in experimental animals during myocardial ischemia (23) and infarction (24) and with pacing (25). Systolic circumferential myocardial segment shortening has been measured using SPAMM in normal human subjects (26), in subjects with left ventricular hypertrophy (27), in subjects with hypertrophic cardiomyopathy (28) and in subjects and experimental models with myocardial infarction (29,30).
Despite its widespread use in cardiovascular investigation during the past decade, the application of magnetic resonance tagging to measure myocardial strain has not yet been validated in vivo. In order to compare measurements of strain by SPAMM and by sonomicrometry, we studied myocardial systolic function in a canine coronary artery ligation model using these two techniques.
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Methods
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Experimental model.
Thirty-one purpose-bred mongrel dogs, each weighing approximately 20 kg, were studied in accordance with the Position of the American Heart Association on Research Animal Use adopted on November 15, 1984. Following induction of anesthesia with morphine and pentobarbital, each animal was intubated and placed on a respirator. In 28 studies, after left thoracotomy, pericardiotomy and isolation of the mid left anterior descending coronary artery, one pair of piezoelectric cylindrical segment-length sonomicrometry crystals (Physiological Monitoring Systems, Durham, North Carolina, and Triton Technology, Inc., San Diego, California) was implanted in the area to be rendered ischemic and a second pair was placed remotely in the basal myocardium. In four of these animals, a third pair of crystals was implanted in the myocardium adjacent to the area at risk. In three studies, no coronary artery dissection was performed, but crystal pairs were placed at apical, basal and midventricular levels. Each crystal pair was oriented along the circumference of the short axis of the left ventricle. Epicardial copper sulfate-filled markers that were bright on SPAMM images were attached to each securing suture to aid in crystal identification on magnetic resonance images. In 28 studies, the left anterior descending coronary artery was ligated (along with additional arterial branches as needed) to produce development of persistent apical dysfunction documented by surface inspection and sonomicrometry. The chest was closed and the left lung was reinflated.
MRI.
Magnetic resonance imaging was performed on a 1.5 T scanner (Signa, General Electric Co., Milwaukee, Wisconsin) beginning 3 h after coronary artery ligation. Following scout spin-echo coronal imaging, a single-phase multislice short-axis SPAMM series was acquired to verify alignment and determine the duration of stripe persistence. A single-slice axial cine MRI sequence (frame duration 25 ms) through the left ventricle was used to determine the timing of end-systole, defined as time of minimal left ventricular cavity size. One or two series of short-axis multiplane, multiphase SPAMM images were obtained for analysis of segmental function. Imaging parameters were 24 cm field of view, 128 x 256 matrix, pixel size 1.875 x 0.938 mm interpolated to 0.938 x 0.938 mm, TR = R-R interval, TE = 30 ms, four to five slices at four to five time points per series, from 13 ms after the R-wave peak to end-systole, two to four signal acquisitions with stripes having 7 to 10 mm center-to-center spacing.
Sonomicrometry recordings.
Sonomicrometry recordings were made using a SONO-1-4D sonomicrometer (Physiological Monitoring Systems) at 50 and 100 mm/s paper speed with electrocardiogram reference. Recordings were obtained at baseline, after coronary ligation and before and after the multiphase SPAMM series. Following completion of imaging, diastolic arrest was induced with cadmium chloride (31) under deep barbiturate anesthesia and the heart was removed. Locations, alignment and transmural depths of crystals were verified by mapping the positions of crystal pairs with respect to surface cardiac landmarks and by determining the depths of implantation by transecting the myocardium adjacent to each crystal site without disturbing securing sutures.
Data analysis.
Stripe separations on SPAMM images were measured on a Sun workstation using the Region of Interest module in the Volumetric Image Display and Analysis (VIDATM) (32), a comprehensive cardiopulmonary image analysis package developed by the Cardiothoracic Imaging Research Center at the University of Pennsylvania. Locations of sonomicrometry crystal pairs were found on images using crystal artifacts and epicardial copper sulfate tags, and the closest adjacent SPAMM measurement sites were selected. Measurements of circumferential shortening by MRI tissue tagging have been performed extensively by our group and other investigators (26–28) and have been previously described in detail (26). In brief, measurements were performed in one of two ways depending upon the orientation of the stripes adjacent to each crystal pair (Fig. 1). At sites where stripes were normal to the endocardium at end-diastole, interstripe distance was measured perpendicular to these stripes or parallel to the endocardium (Fig. 1). Where stripes were oriented at 45° to the endocardial surface, the distance between pairs of stripe intersections defining a segment parallel to the endocardium was measured (26). We have previously shown that both interobserver and intraobserver reproducibility with this method are good (r = 0.92 for both) (26,27). Stripe separation was measured at late-systole (the last image before end-systole typically 60 to 70 ms before, depending on heart rate) and, when stripe persistence permitted, at end-systole. Sonomicrometry segment length was measured with calipers on three to five cycles at R-wave peak, at end-systole and late systole. Measurements were performed by an investigator blind to the SPAMM results except for the timing of late and end-systolic (ES) measurements. Timing during the cardiac cycle of sonomicrometry measurement was matched with that of the SPAMM measurement. Circumferential shortening (%S) by SPAMM and by sonomicrometry was calculated using end-diastolic (ED) measurements and late systolic (LS) or ES measurements with %S = (ED – LS)/ED x 100% or (ED – ES)/ED x 100%.
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Figure 1 Diagram of a short-axis image of left ventricle tagged with spatial modulation of magnetization (SPAMM). (A) At sites where SPAMM stripes were perpendicular to the endocardium at end-diastole, interstripe distance was measured normal to these stripes or parallel to the endocardium. (B) At sites where adjacent stripes were oriented at 45° to the endocardial surface, the interstripe distance was measured at stripe intersections aligned parallel to the endocardium.
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Statistical methods.
Correlation analysis was used to determine the linear relationship between SPAMM and sonomicrometry %S for both ES and LS time points. Linear regression analysis and Bland-Altman plots were used to compare methods. A paired t test was used to compare %S by sonomicrometry and SPAMM in ischemic regions and in normal regions; an unpaired t test was used to compare ischemic and normal regions by each technique.
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Results
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Spatial modulation of magnetization images basal to the level of coronary ligation generally revealed the expected systolic reduction in spacing of stripes oriented perpendicular to the endocardium, with convergence of stripes at the endocardium at end-systole (Fig. 2). This pattern is characteristic of normal circumferential segment shortening with a normal transmural gradient in function, as previously described (26). Spatial modulation of magnetization images apical to the level of coronary ligation demonstrated segmental dysfunction, seen as lack of normal stripe deformation and lack of normal wall thickening (Fig. 3). Of note, immediately adjacent to some basal crystal sites in normal myocardium (4 of 14 overall) locally diminished stripe deformation was observed (Fig. 2).
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Figure 2 End-diastolic (A) and end-systolic (B) short-axis spatial modulation of magnetization images of canine left ventricle in a basal location remote from ischemia demonstrating characteristic normal systolic stripe deformation. Note the presence of derangement in normal pattern of contraction immediately adjacent to the crystal associated artifact (arrow).
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Figure 3 End-diastolic (A) and end-systolic (B) spatial modulation of magnetization images of canine left ventricle in an apical location in the region of ischemia. Loss of contraction is demonstrated in a region of diastolic wall thinning (arrow) as well as in an adjacent region with normal diastolic thickness (arrowhead) by lack of normal systolic wall thickening and lack of normal stripe deformation.
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Spatial modulation of magnetization and sonomicrometry measurements were obtained at closely juxtaposed but not identical myocardial sites. Spatial modulation of magnetization data were obtained from the closest stripe pair or intersection pair adjacent to the segments at which sonomicrometry data were obtained. When crystal artifacts (about 3 mm in diameter) were identified, a SPAMM measurement site was chosen immediately adjacent to but not distorted by artifact because the presence of a hypointense artifact abutting a dark SPAMM stripe could make the location of stripe position ambiguous. In all instances, distance from the SPAMM measurement site to the nearest crystal was <2 stripe pairs, or 14 mm at end-diastole. Spatially and temporally matched data suitable for comparison of SPAMM and sonomicrometry results were obtained in 19 of 31 studies. Data were not obtained in four studies because of cardiac arrest before protocol completion, in three studies because of instability (ventricular tachycardia, ventricular fibrillation and cardiogenic shock), in three other studies because of inadequate sonomicrometric recordings and in two studies because of inadequate SPAMM images. Among the 19 analyzable studies, 36 out of 45 crystal sites could be matched and evaluated by both sonomicrometry and SPAMM techniques. At 28 sites, %S was determined at both late and end-systole. At six sites, %S was determined only at late systole (mean 65 ms before end-systole) because of difficulty in discerning stripe locations on ES images with certainty. At two sites, %S was determined only at end-systole because an appropriately timed LS image was not available. Transmural depths of SPAMM measurement sites were matched to the positions of corresponding sonomicrometry crystals with 11 sites adjacent to the endocardium, 19 midwall and 6 adjacent to the epicardium. Circumferential shortening at end-systole as determined by SPAMM (n = 30) correlated well with that measured by sonomicrometry, with a correlation coefficient of 0.84 (p < 0.0001) (Fig. 4A). A similar relationship was found at late systole (Fig. 4B) with %S as determined by SPAMM (n = 18) correlating well with that measured by sonomicrometry (r = 0.88, p < 0.0001). The slope of the linear regression for %S by SPAMM versus %S by sonomicrometry was 1.2 at end-systole (not significantly different from 1, p = 0.14) and 1.3 at late-systole (significantly >1, p = 0.037). Bland-Altman plots of measurements by SPAMM and sonomicrometry revealed a bias with an increase in difference between SPAMM %S and sonomicrometry %S with increase in average %S. Therefore, transformed Bland-Altman plots were constructed plotting the ratio of SPAMM %S to sonomicrometry %S versus average %S (Fig. 5). However, the 95% limits of agreement for these plots are wide, reflecting nonsystematic differences between the methods and fairly small sample size. Both SPAMM and sonomicrometry distinguished between remote normal and ischemic sites effectively (Table 1). Mean %S by SPAMM was 11% ± 10% at remote normal sites versus 2 ± 3% at ischemic sites (p = 0.014). Similarly, using sonomicrometry, remote normal %S was 7 ± 5% versus 0 ± 3% at ischemic sites (p = 0.002). However, at normal sites, %S by sonomicrometry was significantly lower than that obtained using SPAMM (7 ± 5% vs. 11 ± 10%, p = 0.033). In contrast, at ischemic sites no significant difference between sonomicrometry and SPAMM measurements was found (0 ± 3% vs. 2 ± 3%, p = 0.07).
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Figure 4 Plot of relation between percent circumferential shortening (%S) as determined by sonomicrometry and %S determined by spatial modulation of magnetization at (A) end-systole (n = 30) and (B) at late systole (n = 34). SPAMM = spatial modulation of magnetization.
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Figure 5 Bland-Altman plots for comparison of percent circumferential shortening (%S) comparing the ratio of spatial modulation of magnetization (SPAMM) %S and sonomicrometry (sono) %S at (A) end-systole and (B) end-diastole to average %S (0.01 was added to end-diastolic %S for this plot to avoid division by 0).
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Discussion
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To our knowledge, this is the first study to validate measurements of myocardial circumferential shortening by MRI tissue tagging in vivo. These results are particularly important given the extensive use of this technique in cardiovascular research and its applicability to routine clinical diagnostic cardiology (18). Previous studies have used MRI tagging to construct three-dimensional volume elements from which measurements of systolic wall thickening were compared to thickening from sonomicrometry crystals implanted along the radial direction (33). Those studies did not validate direct measurements of alterations in interstripe distance as reported in this study.
Both SPAMM and sonomicrometry effectively distinguished shortening in normal regions from that found in regions of ischemic dysfunction. However, shortening in remote regions tended to be slightly higher by SPAMM compared with sonomicrometry (Table 1). Spatial modulation of magnetization and sonomicrometry shortening values were similar in ischemic regions; SPAMM and sonomicrometry measurements of circumferential fractional shortening correlated well. These results indicate that SPAMM is a reliable method for assessment of segmental myocardial dysfunction due to ischemia.
Limitations of SPAMM measurements.
Myocardium imaged at end-systole was not identical to that imaged at end-diastole because of long-axis cardiac translation through short-axis imaging planes. However, systolic segment shortening could be accurately measured because stripe spacing at end-diastole is identical in all short-axis planes. Hence, the initial ED stripe separation in myocardium imaged at end-systole is known, even when that myocardium is not imaged at end-diastole. Therefore, segment shortening can be calculated using the known uniform ED stripe separation and measured ES stripe separations. Spatial modulation of magnetization images represented temporally averaged data acquired over hundreds of cardiac cycles. Such averaging can cause significant image degradation under unstable conditions associated with significant heart rate and respiratory variation during imaging. However, good image quality was obtained in the majority of studies. Faster gradient echo tagging methods can shorten data acquisition times by a factor of 7 to 10 (34).
Correspondence between SPAMM and sonomicrometry.
Spatial modulation of magnetization and sonomicrometry measurements were made at closely juxtaposed but not identical locations. However, imperfect matching of SPAMM and sonomicrometry sites likely contributed to the variation between methods demonstrated on the Bland-Altman plots. Subsequent to completion of this study, repeated efforts using alternative crystal designs, lead materials, crystal spacing and imaging methods have not yielded an approach permitting closer correspondence of sonomicrometry and SPAMM measurement sites. Spatial modulation of magnetization and sonomicrometry data could not be collected simultaneously owing to the effects of radiofrequency pulses and magnetic field gradients on the sonomicrometry system. However, sonomicrometry data were obtained immediately before and after each SPAMM series used for data analysis.
Circumferential shortening measurements by sonomicrometry and SPAMM in remote myocardium were generally similar to those reported in the sonomicrometry literature (9,10,35,36). However, as reflected in Table 1, shortening at some remote sites was impaired. Depression of systolic function at sites remote from myocardial ischemia has been observed within minutes to days following coronary occlusion (29,37,38). Factors that may have contributed to the depression of remote shortening in this study include the length of the experiments (with sonomicrometry and SPAMM measurements occurring at least 3 h following coronary occlusion), the severity of ischemic insult and potential local effects of sonomicrometry crystals. Bland-Altman plots demonstrated greater absolute differences in SPAMM %S versus sonomicrometry %S at greater average %S. Differences between SPAMM and sonomicrometry measurements may have been due to reduced function immediately around and between sonomicrometry crystal loci because of local trauma or tethering by either the sonomicrometry leads or securing sutures. Such dysfunction would likely be maximal between crystals and have less effect on function in the adjacent myocardium assessed using SPAMM. In support of this explanation were observations (Fig. 2) of disruptions in systolic SPAMM stripe deformation immediately adjacent to crystals. Sonomicrometry and SPAMM results may correspond more closely in ischemic myocardium because sonomicrometry crystal insertion did not significantly alter function that was already markedly depressed.
Conclusions.
We conclude that magnetic resonance tagging with SPAMM is an effective noninvasive means of measuring segmental myocardial function that can quantitate segment shortening in normal and ischemic myocardium. Results are consistent with those obtained by sonomicrometry and effectively distinguish normal function from ischemic dysfunction. Magnetic resonance tagging methods such as SPAMM permit extensive noninvasive, readily repeatable transmural topographic analysis of segmental function in experimental models and in human subjects. In addition, tagged images can be spatially correlated with magnetic resonance contrast enhancement patterns that identify infarction, viability and microvascular obstruction (24,39). Such methods should prove particularly helpful in further characterizing the topography of segment function over time in experimental and clinical studies of ischemic heart disease.
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Footnotes
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This study was supported by research fellowship grants HL 42958, HL43014, HL28438 and HL29886 to Dr. Yeon from the American Heart Association, Southeastern Pennsylvania Affiliate, and a Commonwealth of Pennsylvania Health Services Contract for Cardiovascular Research.
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References
|
|---|
1. Dodge HT, Sheehan FH. Quantitative contrast angiography for assessment of ventricular performance in heart disease. J Am Coll Cardiol. 1983;1:73–81[Abstract]
2. Marshall RC, Berger HJ, Costin JC, et al. Assessment of cardiac performance with quantitative radionuclide angiography: sequential left ventricular ejection fraction, normalized left ventricular ejection rate, and regional wall motion. Circulation. 1977;56:820–829[Free Full Text]
3. Lipton MJ, Higgins CB, Farmer D, Boyd DP. Cardiac imaging with a high-speed cine-CT scanner: preliminary results. Radiology. 1984;152:579–582[Abstract/Free Full Text]
4. Pflugfelder PW, Sechtem UP, White RD, Higgins CB. Quantification of regional myocardial function by rapid cine MR imaging. Am J Roentgenol. 1988;150:523–529[Abstract/Free Full Text]
5. Chappuis F, Widmann T, Guth B, et al. Quantitative assessment of regional left ventricular function by densitometric analysis of digital-subtraction ventriculograms: correlation with myocardial systolic shortening in dogs. Circulation. 1988;77:457–467[Abstract/Free Full Text]
6. Weiss JL, Bulkley BH, Hutchins GM, Mason SJ. Two-dimensional echocardiographic recognition of myocardial injury in man: comparison with postmortem studies. Circulation. 1981;63:401–408[Free Full Text]
7. Rogers WJ, Shapiro EP, Weiss JL, et al. Quantification of and correction for left ventricular systolic long-axis shortening by magnetic resonance tissue tagging and slice isolation. Circulation. 1991;84:721–731[Abstract/Free Full Text]
8. Buchalter MB, Weiss JL, Rogers WJ, et al. Noninvasive quantification of left ventricular rotational deformation in normal humans using magnetic resonance imaging myocardial tagging. Circulation. 1990;81:1236–1244[Abstract/Free Full Text]
9. Weintraub WS, Hattori S, Agarwal JB, et al. The relationship between myocardial blood flow and contraction by myocardial layer in the canine left ventricle during ischemia. Circ Res. 1981;48:430–438[Abstract/Free Full Text]
10. Gallagher KP, Stirling MC, Choy M, et al. Dissociation between epicardial and transmural function during acute myocardial ischemia. Circulation. 1985;71:1279–1291[Abstract/Free Full Text]
11. Holmes JW, Yamashita H, Waldman LK, Covell JW. Scar remodeling and transmural deformation after infarction in the pig. Circulation. 1994;90:411–420[Abstract/Free Full Text]
12. Ingels NB Jr, Daughters GT 2nd, Stinson EB, Alderman EL. Evaluation of methods for quantitating left ventricular segmental wall motion in man using myocardial markers as a standard. Circulation. 1980;62:966–972
13. Waldman LK, Fung YC, Covell JW. Transmural myocardial deformation in the canine left ventricle: normal in vivo three-dimensional finite strains. Circ Res. 1985;57:152–163[Abstract/Free Full Text]
14. Zerhouni EA, Parish DM, Rogers WJ, et al. Human heart: tagging with MR imaging—a method for noninvasive assessment of myocardial motion. Radiology. 1988;169:59–63[Abstract/Free Full Text]
15. Axel L, Dougherty L. MR imaging of motion with spatial modulation of magnetization. Radiology. 1989;171:841–845[Abstract/Free Full Text]
16. Axel L, Dougherty L. Heart wall motion: improved method of spatial modulation of magnetization for MR imaging. Radiology. 1989;172:349–350[Abstract/Free Full Text]
17. Young AA, Axel L, Dougherty L, et al. Validation of tagging with MR imaging to estimate material deformation. Radiology. 1993;188:101–108[Abstract/Free Full Text]
18. Garot J, Bluemke DA, Osman NF, et al. Fast determination of regional myocardial strain fields from tagged cardiac images using harmonic phase MRI. Circulation. 2000;101:981–988[Abstract/Free Full Text]
19. Stuber M, Scheidegger MB, Fischer SE, et al. Alterations in the local myocardial motion pattern in patients suffering from pressure overload due to aortic stenosis. Circulation. 1999;100:361–368[Abstract/Free Full Text]
20. MacGowan GA, Shapiro EP, Azhari H, et al. Noninvasive measurement of shortening in the fiber and cross-fiber directions in the normal human left ventricle and in idiopathic dilated cardiomyopathy. Circulation. 1997;96:535–541[Abstract/Free Full Text]
21. Maier SE, Fischer SE, McKinnon GC, et al. Evaluation of left ventricular segmental wall motion in hypertrophic cardiomyopathy with myocardial tagging. Circulation. 1992;86:1919–1928[Abstract/Free Full Text]
22. Young AA, Kramer CM, Ferrari VA, et al. Three-dimensional left ventricular deformation in hypertrophic cardiomyopathy. Circulation. 1994;90:854–867[Abstract/Free Full Text]
23. Azhari H, Weiss JL, Rogers WJ, et al. A noninvasive comparative study of myocardial strains in ischemic canine hearts using tagged MRI in 3-D. Am J Physiol. 1995;268:H1918–H1926
24. Lima JAC, Ferrari VA, Reichek N, et al. Segmental motion and deformation of transmurally infarcted myocardium in acute postinfarct period. Am J Physiol. 1995;268:H1304–H1312
25. Prinzen FW, Hunter WC, Wyman BT, McVeigh ER. Mapping of regional myocardial strain and work during ventricular pacing: experimental study using magnetic resonance imaging tagging. J Am Coll Cardiol. 1999;33:1735–1742[Abstract/Free Full Text]
26. Clark NR, Reichek N, Bergey P, et al. Circumferential myocardial shortening in the normal human left ventricle: assessment by magnetic resonance imaging using spatial modulation of magnetization. Circulation. 1991;84:67–74[Abstract/Free Full Text]
27. Palmon LC, Reichek N, Yeon SB, et al. Intramural myocardial shortening in hypertensive left ventricular hypertrophy with normal pump function. Circulation. 1994;89:122–131[Abstract/Free Full Text]
28. Kramer CM, Reichek N, Ferrari VA, et al. Regional heterogeneity of function in hypertrophic cardiomyopathy. Circulation. 1994;90:186–194[Abstract/Free Full Text]
29. Kramer CM, Rogers WJ, Theobald TM, et al. Remote noninfarcted region dysfunction soon after first anterior myocardial infarction: a magnetic resonance tagging study. Circulation. 1996;94:660–666[Abstract/Free Full Text]
30. Rogers WJ, Kramer CM, Geskin G, et al. Early contrast-enhanced MRI predicts late functional recovery after reperfused myocardial infarction. Circulation. 1999;99:744–750[Abstract/Free Full Text]
31. Weber KT, Janicki JS, Shroff SG, et al. Collagen remodeling of the pressure-overloaded, hypertrophied, nonhuman primate myocardium. Circ Res. 1988;62:757–765[Abstract/Free Full Text]
32. Hoffman EA, Gnanaprakasam D, Gupta KB, et al. VIDA: an environment for multidimensional image display and analysis. SPIE Proc. 1992;1660:694–711[CrossRef]
33. Lima JAC, Jeremy R, Guier W, et al. Accurate systolic wall thickening by nuclear magnetic resonance imaging with tissue tagging: correlation with sonomicrometers in normal and ischemic myocardium. J Am Coll Cardiol. 1993;21:1741–1751[Abstract]
34. McVeigh ER, Atalar E. Cardiac tagging with breath-hold cine MRI. Magn Reson Med. 1992;28:318–327[Medline]
35. Ross J, Franklin D. Analysis of regional myocardial function, dimensions, and wall thickness in the characterization of myocardial ischemia and infarction. Circulation. 1976;53(Suppl I):I88–I92
36. Homans DC, Asinger R, Elsperger KJ, et al. Regional function and perfusion at the lateral border of ischemic myocardium. Circulation. 1985;71:1038–1047[Abstract/Free Full Text]
37. Meyer TE, Perlini S, Foex P. Regional nonischemic performance as assessed by end-systolic measures of shortening and thickening. J Am Coll Cardiol. 1994;24:1797–1805[Abstract]
38. Wyatt HL, Forrester JS, da Luz PL, et al. Functional abnormalities in nonoccluded regions of myocardium after experimental coronary occlusion. Am J Cardiol. 1976;37:366–372[CrossRef][Medline]
39. Lima JAC, Judd RM, Bazille A, et al. Regional heterogeneity of human myocardial infarcts demonstrated by contrast-enhanced MRI. Circulation. 1995;92:1117–1125[Abstract/Free Full Text]
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J. Am. Coll. Cardiol.,
November 5, 2003;
42(9):
1574 - 1583.
[Abstract]
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R. M. Setser, R. D. White, B. Sturm, P. M. McCarthy, R. C. Starling, J. B. Young, J. Kasper, T. Buda, N. Obuchowski, and M. L. Lieber
Noninvasive assessment of cardiac mechanics and clinical outcome after partial left ventriculectomy
Ann. Thorac. Surg.,
November 1, 2003;
76(5):
1576 - 1585.
[Abstract]
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J. M. Guccione and M. B. Ratcliffe
Invited commentary
Ann. Thorac. Surg.,
November 1, 2003;
76(5):
1585 - 1586.
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Abstract
Methods