This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Bogaert, J. Articles by Rademakers, F. E. Search for Related Content PubMed PubMed Citation Articles by Bogaert, J. Articles by Rademakers, F. E.

CLINICAL STUDIES

Remote myocardial dysfunction after acute anterior myocardial infarction: impact of left ventricular shape on regional function

A magnetic resonance myocardial tagging study

Jan Bogaert, MD^*, Hilde Bosmans, PhD^* , Alex Maes, MD^*, Paul Suetens, PhD, Guy Marchal, MD^* and Frank E. Rademakers, MD^*

^* Department of Nuclear Medicine, the Interdisciplinary Research Unit for Radiological Imaging, University Hospitals, Leuven, Belgium and
Department of Cardiology, Radiology, and the Interdisciplinary Research Unit for Radiological Imaging, University Hospitals, Leuven, Belgium

Manuscript received October 21, 1998; revised manuscript received December 3, 1999, accepted January 17, 2000.

Reprint requests and correspondence: Dr. Jan Bogaert, Department of Radiology, University Hospitals, Catholic University of Leuven, Herestraat 49, B-3000 Leuven, Belgium.
Jan.Bogaert{at}uz.kuleuven.ac.be

	Abstract

Top Abstract Methods Results Discussion References

 
OBJECTIVES

We sought to evaluate regional morphology and function in patients in their first week after having a reperfused anterior myocardial infarction (MI) using magnetic resonance (MR) myocardial tagging.

BACKGROUND

The mechanism of myocardial dysfunction in the remote, noninfarct-related regions is an unresolved issue to date.

METHODS

Sixteen patients with a first reperfused transmural anterior MI were studied with MR tagging at 5 ± 2 days after the event, and the results were compared with those of an age-matched control group regions. The left ventricle (LV) was divided into infarct, adjacent and remote regions. Magnetic resonance tagging provided information on the regional ventricular morphology and function.

RESULTS

Morphologically, an increase of the circumferential radius of curvature was found in the remote myocardium, whereas the longitudinal radius of curvature was increased in all regions of the LV. A significant increase in apical sphericity was also found. A significant reduction in strain and function was found not only in the infarct region, but also in the adjacent and remote myocardium. The loss in regional ejection fraction in the remote myocardium (61.4 ± 11.7% in patients vs. 68.7 ± 10.0% in control subjects, p < 0.0001) was related to a significant reduction of the longitudinal and circumferential strain, whereas systolic wall thickening was preserved.

CONCLUSIONS

Remote myocardial dysfunction contributes significantly to the loss in global ventricular function. This could be secondary to morphologic changes in the infarct region, leading to an increased systolic longitudinal wall stress without loss of intrinsic contractility in the remote regions.

Abbreviations and Acronyms   EF = ejection fraction   18FDG = 18-flurodeoxyglucose   LAD = left anterior descending coronary artery   LV = left ventricle or ventricular   MI = myocardial infarction   MR = magnetic resonance   13NH3 = nitrogen-13–ammonia   PET = positron emission tomography   TIMI = Thrombolysis in Myocardial Infarction trial

	Methods

Top Abstract Methods Results Discussion References

 
Study group.   Sixteen consecutive patients (13 men, 3 women; mean [±SD] age 58 ± 10 years [range 38 to 74]) with a first transmural anterior MI were studied. All patients presented with ST segment elevation 2 mm in two or more precordial leads (V₁ through V₆). All patients were successfully reperfused within 6 h after the onset of symptoms with a recombinant tissue-type plasminogen activator (n = 10), recombinant staphylokinase (n = 4) or primary angioplasty (n = 2). Nevertheless, all patients developed new Q waves in the anterior leads within 24 h and had positive cardiac enzymes (Table 1). At angiography, no significant lesions were found on coronary arteries other than the LAD. In two patients who received thrombolytic therapy, rescue angioplasty was performed at 90 min, whereas in seven other patients, elective angioplasty was performed at 1 ± 2 days after the acute event, so all patients were studied with an open infarct-related artery.

Study protocol.   All studies were performed according to the guidelines of the hospital’s Ethics Committee, and written, informed consent was obtained. All patients underwent coronary angiography, MR tagging and PET during the first week after their acute event. The MR tagging studies were performed at 5 ± 2 days (range 2 to 7) after the acute event.

Coronary angiography.   The patency of the infarct-related coronary artery was defined according to the Thrombolysis in Myocardial Infarction (TIMI) trial criteria for grading recanalization after MI (12). The severity of the residual stenosis was expressed as the percent reduction in the lumen diameter.

Positron emission tomography.   Myocardial blood flow was measured using nitrogen-13–ammonia (¹³NH₃) and myocardial metabolism using 18-flurodeoxyglucose (¹⁸FDG) (13). All patients were studied using the hyperinsulinemic euglycemic clamp technique (14). A three-dimensional delineation of the LV wall was used to construct a polar map (33 regions—one apical region and four rings of eight regions each) (13). A flow index was calculated as the ratio of ¹³NH₃ uptake in each region to the ¹³NH₃ uptake in the region with the highest uptake (reference region). The same anatomic region was used as the reference region for ¹⁸FDG. A metabolic index was defined as the ratio of glucose utilization in each region to that in the reference zone. Regions with a flow index >80% were considered to be normal. In the remaining regions, a flow-metabolism mismatch pattern was assumed if the ratio of metabolism to flow was >1.2, and a match pattern if this ratio was 1.2 (13).

Magnetic resonance tagging and data analysis.   Magnetic resonance tagging was used to calculate myocardial strains (15). All studies were obtained on a 1.0-tesla MR unit (Siemens, Erlangen, Germany). Tags are noninvasive markers placed on the myocardium by presaturating planes at end-diastole perpendicular to the subsequent imaging planes. They show up on the images as dark lines that move and deform with the myocardium on which they are inscribed. Five parallel short-axis planes and four radially oriented long-axis planes crossing the center of the LV were defined (Fig. 1). The gravitational centerline of the LV cavity was reached by the best fit connecting the center of the cavity at each of the different short-axis levels. Images were acquired at end-diastole and end-systole in all these planes, using the short-axis planes as tagging planes for the long-axis images and vice versa. By combining the short- and long-axis information, the entire LV wall, except for the apex, could be reconstructed into 32 small cuboids for which the three-dimensional coordinates of the node points were known. Myocardial strain and shear are defined as the difference between an end-systolic and end-diastolic dimension divided by a reference end-diastolic dimension and are, as such, dimensionless and presented as percent values. Strains are divided in normal and shear strains (Fig. 2). Normal strains are defined as displacements along a coordinate axis. Two adjacent node points can be projected on a coordinate axis, and the length of this projection can be measured. The length of this projection can change during the cardiac cycle, and the difference of these lengths divided by the total length at end-diastole defines the normal strains. Shear strains are similarly defined, but now the difference in projected length and the end-diastolic distance by which it is divided are on different axes. In a local coordinate system, three normal and three shear strains are obtained. Normal strains deform a cube into a beam; shear strains deform it into a parallellopiped. These strains were expressed in a local cardiac coordinate system for each epicardial and endocardial node point (Fig. 1). This local cardiac coordinate system is defined by three perpendicular axes (radial, circumferential and longitudinal). The circumferential axis is obtained in a plane tangential to the inner or outer LV surface and is directed in the short-axis direction. The longitudinal axis is obtained in a similar plane but is directed in the LV long-axis. Finally, the radial axis is obtained perpendicular to this tangential plane and is directed outward. Myocardial strains can be negative or positive. Positive radial strains represent wall thickening, whereas negative circumferential or longitudinal strains represent segment shortening.

View larger version (26K): [in this window] [in a new window]   Figure 1 Regional strain analysis with MR tagging. By means of MR tagging along the cardiac short and long axes, the LV wall is divided in 32 small cuboids (three-dimensional [3D] reconstruction). Each cuboid is defined by four epicardial and four endocardial node points. The strains are expressed in a local cardiac coordinate system for each epicardial and endocardial node point. The axes are radial (R), circumferential (C) and longitudinal (L).

View larger version (32K): [in this window] [in a new window]   Figure 2 Normal and shear strains. At the left, a "nondeformed" myocardial cube is shown at end-diastole. The deformation of the cube at end-systole, shown at the right, can be analyzed by means of a combination of three normal strains (left) and three shear strains (right). CL-shear = circumferential–longitudinal shear strain; CR-shear = circumferential–radial shear strain; EPI = epicardium; LR-shear = longitudinal–radial shear strain.

View larger version (27K): [in this window] [in a new window]   Figure 3 Regional ejection fraction.

Anatomic localization of the infarct, adjacent and remote myocardium.   The LV was divided into infarct, adjacent and remote regions. Regions presenting with decreased myocardial blood flow (i.e., a match or mismatch pattern on PET) were considered as being infarct-related. Matching PET and MR regions anatomically was feasible because both used a similar approach to divide the LV into small cuboids or regions that can be related to each other by the use of anatomic landmarks (16). Next, a single row of cuboids surrounding the infarct-related area was labeled as adjacent myocardium. All remaining cuboids were defined as remote myocardium. The anatomic location of the infarct-related myocardium corresponded very well with the expected location on the coronary angiogram. For comparison, in the control group, similar regions (infarcted, adjacent and remote) were defined, corresponding to the average extent and location in the patients with infarct-related myocardium.

Statistical analysis.   All data are expressed as the mean value ± SD. The simultaneous comparison of more than two mean values was performed with multiway analysis of variance, where both region (infarct, adjacent and remote) and population (control subjects vs. patients) were used as independent variables, and the Scheffé test was subsequently applied to identify the source of the difference. A p value <0.05 was considered to indicate statistical significance. Accuracy and reproducibility of MR tagging were reported previously (16).

	Results

Top Abstract Methods Results Discussion References

 
Patient characteristics and angiographic findings.   Age, gender, medical history, risk factors, angiographic findings, cardiac enzymes and medication at hospital discharge are listed in Table 1. Between the patient and control groups, no significant differences in blood pressure nor heart rate were found at the time of the MR study (146 ± 12/84 ± 7 mm Hg and 72 ± 13 beats/min in the patient group vs. 138 ± 15/80 ± 8 mm Hg and 73 ± 10 beats/min in the control group, p = NS). The culprit lesion of the LAD was located in the proximal segment in six patients, in the middle segment in nine patients and in the distal segment in one patient.

Global and regional morphology.   End-diastolic volumes were significantly larger in the infarct group than in the control group (99 ± 27 vs. 83 ± 16 ml, p = 0.03). In the patient group, end-diastolic wall thickness was also significantly larger in the infarct, adjacent and remote regions (Table 2). The increase in wall thickness, however, was more pronounced than the increase in diameter, indicating a moderate degree of concentric LV hypertrophy in the patient group (wall thickness to chamber diameter ratio in patients 0.266 ± 0.072 vs. control subjects 0.235 ± 0.047, p < 0.0001). A significant increase in the longitudinal radius of curvature was found throughout the LV in the patient group. A significant increase in the endocardial circumferential radius of curvature was shown in the remote myocardium. Epicardially, this radius was significantly larger in the infarct and remote myocardium. The apical sphericity was significantly larger in patients than in control subjects (radii 1.31 ± 0.2 vs. 0.71 ± 0.2 cm, p < 0.05) (Fig. 4).

View larger version (99K): [in this window] [in a new window]   Figure 4 Magnetic resonance tagging in a normal volunteer (A) and in a patient with an acute anterior MI (B), with corresponding PET study (C). A and B, Magnetic resonance tagging study. Horizontal long-axis view (top) and vertical long-axis view (bottom). Five tag lines are parallelly oriented in the short-axis direction and equally spread over the LV. Note the differences in apical sphericity between the control subjects and patients with an anterior MI. C, Positron emission tomographic study. Data are represented in bull’s eyes: 13NH3 map (left) and 18FDG map (right). The middle of the bull’s eye corresponds to the LV apex, whereas the periphery corresponds to the LV base. The anterior wall is above, the lateral wall to the right, the inferior wall below and the LV septum to the left of the bull’s eye. A reduction in flow or metabolism is represented as a dark area. Note the severe reduction in flow and metabolism in the anteroapical region extending to the septum.

View larger version (42K): [in this window] [in a new window]   Figure 5 Endocardial and epicardial longitudinal strain. *p < 0.0001. #p = 0.02.

View larger version (18K): [in this window] [in a new window]   Figure 6 Longitudinal–radial shear strain. Open bars = patients; hatched bars = control subjects. *p < 0.0001.

View larger version (36K): [in this window] [in a new window]   Figure 7 Endocardial (A) and epicardial (B) regional ejection fraction. Open bars = patients; hatched bars = control subjects. *p < 0.0001.

	Discussion

Top Abstract Methods Results Discussion References

Morphologic and functional changes in the infarct-related myocardium.   In the infarct-related myocardium, the functional loss is caused by a similar impairment in normal myocardial strains in the inner and outer layers. A combination of myocyte necrosis (mostly endocardial) and viable but dysfunctional (i.e., stunned) myocardium (17) (more epicardial) most likely contributes to this impairment. We previously reported a recovery in epicardial fiber shortening three months after reperfused MI representing recovery of stunned myocardium (16). The ventricular torsion (i.e., the circumferential–longitudinal shear strain) (18), however, was remarkably well preserved epicardially. Because the driving force for LV torsion is shortening of the oblique left-handed epicardial myofibers, counteracted by oblique right-handed endocardial fibers (19), epicardial torsion can be preserved in the infarct region when the modestly diminished epicardial fiber shortening is not or is minimally counteracted by severely reduced endocardial fiber shortening. The larger decrease in endocardial torsion is indicative of decreased tethering between layers, possibly due to an increased stiffness of the inner layers, resisting deformations. This finding also indicates that although all patients presented with transmural (i.e., Q wave) infarcts, residual viable tissue must be present in the outer layers in the infarct region. The increase in end-diastolic wall thickness in the infarct area can be explained by edema and inflammatory changes or by preexisting LV hypertrophy (e.g., arterial hypertension). Shape changes in the infarct-related myocardium include an increase in apical sphericity and a flattening of the anterior wall, as indicated by the increase in longitudinal radius of curvature (7,20).

Morphologic and functional changes in the adjacent and remote myocardium.   The issue of remote myocardial dysfunction or hyperfunction remains a matter of debate (21–23). Magnetic resonance tagging allows the quantification of the true myocardial strain, independent of any external reference system, so that the influence of gross cardiac motions, such as translation or rotation on the myocardial deformation, can be ruled out (15). The present study favors remote myocardial dysfunction, although early hyperfunction followed by late dysfunction cannot be ruled out, because the patients were studied two to seven days after the acute event. Although our study is in agreement with a recent study by Kramer et al. (2) showing a decrease in circumferential shortening in the remote myocardium, it also demonstrates a significant loss in longitudinal shortening, whereas wall thickening was not different from that in control subjects. This discrepancy is due to a significant impact on epicardial inward motion, resulting in preserved wall thickening in the presence of decreased endocardial inward motion. Morphologic findings in the remote myocardium include an increase in the circumferential and longitudinal radii of curvature and in wall thickness, a finding that was previously reported in chronic MIs with fibrous aneurysms (1). A possible mechanism for the increase in wall thickness is hypertrophy secondary to increased wall stress. However, preexisting differences in wall thickness between the patient group and control group before the MI cannot be ruled out.

Potential mechanisms of remote myocardial dysfunction.   It is well known that anteroapical MIs have a greater influence on LV function than do "similarly sized infarctions" in other regions of the LV (24). This is likely related to morphologic changes in the infarct-related myocardium, influencing the behavior of the remote myocardium. The present study may give a new view on the mechanism of remote myocardial dysfunction in patients with an anterior MI.

First, LV ejection is partially caused by longitudinal LV shortening (25), which mainly relies on the obliquely oriented endocardial and epicardial fibers. Impaired longitudinal shortening in the remote myocardium very likely relies on increased longitudinal wall stress secondary to morphologic changes in the infarct-related myocardium or to changes in LV shape and may represent a kind of longitudinal tethering (24). As shown in this study, wall expansion in the infarct area increases the longitudinal radius of curvature in the apex and exposes this wall segment to greater intramural tension (7,8). Subsequently, the longitudinal wall stress will increase in the remote areas and will lead to wall flattening (as shown by the increase in the longitudinal radius of curvature). This effect is more pronounced endocardially than epicardially, leading to greater endocardial longitudinal wall stress and a reversal of the longitudinal–radial shear strain. LeGrice (26) and Costa (27) and their colleagues stressed the importance of a normal longitudinal–radial shear strain in providing normal myocardial function. Although wall stress was not mathematically calculated, directional changes can be deduced reliably from alterations in the determinants of wall stress (i.e., radius of curvature) (28).

Second, although the increase in the circumferential radius of curvature in the remote myocardium could act as a compensatory mechanism to improve LV function by increasing the regional preload, this compensatory mechanism seems to be ineffective because the circumferential shortening decreases in the remote myocardium (2). Circumferential shortening is more affected epicardially than endocardially. The latter can explain the preserved apparent systolic wall thickening in the remote myocardium while the centripetal systolic wall motion is significantly reduced, thus contributing to a reduction of regional EF in this part of the ventricle.

Study limitations.   This study lacks preinfarct data on LV morphology and function in the patient group. Therefore, we compared the patient data with data from age-matched healthy control subjects. A second limitation is the absence of comparison with patients who did not receive reperfusion therapy or in whom reperfusion therapy failed. These groups can be expected to have more ventricular remodeling. Such a comparison would be interesting to evaluate the beneficial effects of reperfusion therapy on ventricular remodeling. All patients in this study presented with a first acute transmural anterior MI. Although we postulated that the noticed functional changes in the remote myocardium were directly related to changes in apical sphericity after an anterior MI, we cannot rule out that similar differences could be found after an MI in the posterior wall. Further research comparing the influence of an MI at different anatomic locations is therefore required. Also, preexisting LV hypertrophy in the patient group, as shown by the increase in wall thickness–chamber diameter ratio, may have an influence on the results. Although the blood pressures were slightly higher in the patient group than in the control group at the time of the MR study, the differences were not statistically significant. Analysis of medical history showed that at least three patients had a history of arterial hypertension and one patient had diabetes. Therefore, some degree of LV hypertrophy can be expected in the patient group. A significantly thicker end-diastolic LV wall was found in the patients with beta-blocker therapy.

Technical limitations include the exclusion of the LV apex from strain analysis, owing to the use of parallelly oriented tags in the long axis. To partially overcome this problem, the apical tag was located as near as possible to the apex. Another potential shortcoming of this study is the calculation of regional EF, because the intracavitary triangular volume described by each cuboid relies on the positioning of the LV center, which may be difficult to define in diseased ventricles, especially anteroapical infarctions. As mentioned in the Methods section, the gravitational center of the LV cavity was reached by the best fit through the center, determined for each of the different short-axis images. The impact on quantifying regional EF can be minimized by normalizing data to end-diastole.

Conclusions.   Impairment in LV function after an acute transmural anterior MI is related not only to myocardial tissue necrosis in the infarct-related myocardium, but also to remote myocardial dysfunction, and therefore may explain why an anterior MI often exhibits a larger functional loss than expected solely on the basis of the extent of myocardial necrosis. Remote myocardial dysfunction could be caused indirectly by morphologic changes in the infarct-related myocardium (i.e., increased apical sphericity), increasing the load on the remote myocardium.

	Footnotes

 
The study was supported in part by grant no. G 3132.94 from the Fonds voor Wetenschappelijk Onderzoek (FWO).

	References

Top Abstract Methods Results Discussion References

 

1. Lessick J, Sideman S, Azhari H, et al. Regional three-dimensional geometry and function of left ventricles with fibrous aneurysms: a cine-computed tomography study. Circulation. 1991;84:1072–1086[Abstract/Free Full Text]
2. 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]
3. Kramer CM, Lima JA, Reichek N, et al. Regional differences in function within noninfarcted myocardium during left ventricular remodeling. Circulation. 1993;88:1279–1288[Abstract/Free Full Text]
4. Weisman HF, Bush DE, Mannisi JA, Healy Bulkley B. Global cardiac remodeling after acute myocardial infarction: a study in the rat model. J Am Coll Cardiol. 1985;5:1355–1362[Abstract]
5. Mitchell GF, Lamas GA, Pfeffer MA. Ventricular remodeling after myocardial infarction. Sideman S, Beyar R. Interactive Phenomena in the Cardiac System. New York: Plenum Press; 1993. p. 265–276
6. Eaton LW, Weiss JL, Bulkley BH, et al. Regional cardiac dilatation after myocardial infarction. N Engl J Med. 1979;300:57–62[Abstract]
7. Jugdutt BI, Khan MI. Impact of increased infarct transmurality on remodeling and function during healing after anterior myocardial infarction in the dog. Can J Physiol Pharmacol. 1992;70:949–958[Medline]
8. Pirolo JS, Hutchins GM, Moore GW. Infarct expansion: pathologic analysis of 204 patients with a single myocardial infarct. J Am Coll Cardiol. 1986;7:349–354[Abstract]
9. Homans DC, Sublett E, Elsperger KJ, Schwartz JS. Mechanisms of remote myocardial dysfunction during coronary artery occlusion in the presence of multivessel disease. Circulation. 1986;74:588–596[Abstract/Free Full Text]
10. Olivetti G, Capasso JM, Sonnenblick EH, Anversa P. Side-to-side slippage of myocytes participates in ventricular wall remodeling acutely after myocardial infarction in rats. Circ Res. 1990;67:23–34[Abstract/Free Full Text]
11. Ginzton LE, Conant R, Rodrigues DM, Laks MM. Functional significance of hypertrophy of the noninfarcted myocardium after myocardial infarction in humans. Circulation. 1989;80:816–822[Abstract/Free Full Text]
12. TIMI Study Group. The Thrombolysis in Myocardial Infarction (TIMI) trial: phase I findings. N Engl J Med. 1985;312:932–936[Medline]
13. Maes A, Flameng W, Nuyts J, et al. Histological alterations in chronically hypoperfused myocardium: correlation with PET findings. Circulation. 1994;90:735–745[Abstract/Free Full Text]
14. Knuuti JM, Nuutila P, Ruotsalainen U, et al. Euglycemic hyperinsulinemic clamp and oral glucose load in stimulating myocardial glucose utilization during positron emission tomography. J Nucl Med. 1992;33:1255–1262[Abstract/Free Full Text]
15. Zerhouni EA, Parish DM, Rogers WJ, et al. Human heart: tagging with MR imaging—a new method for noninvasive assessment of myocardial motion. Radiology. 1988;169:59–63[Abstract/Free Full Text]
16. Bogaert J, Maes A, Van de Werf F, et al. Functional recovery of subepicardial myocardial tissue in transmural myocardial infarction after successful reperfusion. Circulation. 1999;99:36–43[Abstract/Free Full Text]
17. Braunwald F, Kloner RA. The stunned myocardium: prolonged, postischemic ventricular dysfunction. Circulation. 1982;66:1146–1149[Abstract/Free Full Text]
18. 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]
19. Arts T, Meerbaum S, Reneman RS, Corday E. Torsion of the left ventricle during the ejection phase in the intact dog. Cardiovasc Res. 1984;18:183–193[Medline]
20. Fantini F, Barletta GA, Baroni M, et al. Quantitative evaluation of left ventricular shape in anterior aneurysm. Cathet Cardiovasc Diagn. 1993;28:295–300[Medline]
21. Smalling RW, Ekas RD, Felli PR, et al. Reciprocal functional interaction of adjacent myocardial segments during regional ischemia: an intraventricular loading phenomenon affecting apparent regional contractile function in the intact heart. J Am Coll Cardiol. 1986;7:1335–1346[Abstract]
22. Lew WYW, Chen Z, Guth B, Covell JW. Mechanisms of augmented segment shortening in nonischemic areas during acute ischemia of the canine left ventricle. Circ Res. 1985;56:352–358
23. Goto Y, Igarashi Y, Yamada O, et al. Hyperkinesis without the Frank-Starling mechanisms in a nonischemic region of acutely ischemic excised canine heart. Circulation. 1988;77:468–477[Abstract/Free Full Text]
24. Marino PN, Kass DA, Becker LC, et al. Influence of site of regional ischemia on nonischemic thickening in anesthetized dogs. Am J Physiol. 1989;25:H1417–H1425
25. Rogers WJ, Shapiro EP, Weiss JL, Buchalter MB, 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]
26. LeGrice IJ, Takayama Y, Covell JW. Transverse shear along myocardial cleavage planes provides a mechanism for normal systolic wall thickening. Circ Res. 1995;77:182–193[Abstract/Free Full Text]
27. Costa KD, Takayama Y, McCulloch AD, Covell AD. Laminar fiber architecture and three-dimensional systolic mechanisms in canine ventricular myocardium. Am J Physiol. 1999;76:H595–H607
28. Janz RF. Estimation of local myocardial stress. Am J Physiol. 1982;242:H875–H881

This article has been cited by other articles:

				G. D. Buckberg Congestive heart failure: Treat the disease, not the symptom Return to normalcy/Part II-The experimental approach. J. Thorac. Cardiovasc. Surg., October 1, 2007; 134(4): 844 - 849. [Full Text] [PDF]

				A. Jacquier, C. B. Higgins, A. J. Martin, L. Do, D. Saloner, and M. Saeed Injection of Adeno-associated Viral Vector Encoding Vascular Endothelial Growth Factor Gene in Infarcted Swine Myocardium: MR Measurements of Left Ventricular Function and Strain Radiology, October 1, 2007; 245(1): 196 - 205. [Abstract] [Full Text] [PDF]

				V. S. Rao, L. R. La Bonte, Y. Xu, Z. Yang, B. A. French, and W. H. Guilford Alterations to myofibrillar protein function in nonischemic regions of the heart early after myocardial infarction Am J Physiol Heart Circ Physiol, July 1, 2007; 293(1): H654 - H659. [Abstract] [Full Text] [PDF]

				Z. B. Popovic, C. Benejam, J. Bian, N. Mal, J. Drinko, K. Lee, F. Forudi, R. Reeg, N. L. Greenberg, J. D. Thomas, et al. Speckle-tracking echocardiography correctly identifies segmental left ventricular dysfunction induced by scarring in a rat model of myocardial infarction Am J Physiol Heart Circ Physiol, June 1, 2007; 292(6): H2809 - H2816. [Abstract] [Full Text] [PDF]

				I. George, Y. Cheng, G.-H. Yi, K.-L. He, X. Li, M. C. Oz, J. Holmes, and J. Wang Effect of passive cardiac containment on ventricular synchrony and cardiac function in awake dogs Eur. J. Cardiothorac. Surg., January 1, 2007; 31(1): 55 - 64. [Abstract] [Full Text] [PDF]

				B. B. Carmichael, R. M. Setser, A. E. Stillman, M. L. Lieber, N. G. Smedira, P. M. McCarthy, R. C. Starling, J. B. Young, J. A. Weaver, A. G. Lawrence, et al. Effects of Surgical Ventricular Restoration on Left Ventricular Function: Dynamic MR Imaging Radiology, December 1, 2006; 241(3): 710 - 717. [Abstract] [Full Text] [PDF]

				A. N. Mazzadi, X. Andre-Fouet, N. Costes, P. Croisille, D. Revel, and M. F. Janier Mechanisms leading to reversible mechanical dysfunction in severe CAD: alternatives to myocardial stunning Am J Physiol Heart Circ Physiol, December 1, 2006; 291(6): H2570 - H2582. [Abstract] [Full Text] [PDF]

				S. A.F. Tulner, P. Steendijk, R. J.M. Klautz, J. J. Bax, M. J. Schalij, E. E. van der Wall, and R. A.E. Dion Surgical ventricular restoration in patients with ischemic dilated cardiomyopathy: Evaluation of systolic and diastolic ventricular function, wall stress, dyssynchrony, and mechanical efficiency by pressure-volume loops. J. Thorac. Cardiovasc. Surg., September 1, 2006; 132(3): 610 - 620. [Abstract] [Full Text] [PDF]

				S. G. Lloyd, G. D. Buckberg, and the RESTORE Group Use of cardiac magnetic resonance imaging in surgical ventricular restoration Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S216 - S224. [Abstract] [Full Text] [PDF]

				M.-C. Toufektsian, Z. Yang, K. M. Prasad, L. Overbergh, S. I. Ramos, C. Mathieu, J. Linden, and B. A. French Stimulation of A2A-adenosine receptors after myocardial infarction suppresses inflammatory activation and attenuates contractile dysfunction in the remote left ventricle Am J Physiol Heart Circ Physiol, April 1, 2006; 290(4): H1410 - H1418. [Abstract] [Full Text] [PDF]

				T. Edvardsen, R. Detrano, B. D. Rosen, J. J. Carr, K. Liu, S. Lai, S. Shea, L. Pan, D. A. Bluemke, and J. A.C. Lima Coronary Artery Atherosclerosis Is Related to Reduced Regional Left Ventricular Function in Individuals Without History of Clinical Cardiovascular Disease: The Multiethnic Study of Atherosclerosis Arterioscler. Thromb. Vasc. Biol., January 1, 2006; 26(1): 206 - 211. [Abstract] [Full Text] [PDF]

				D. R. Messroghli, G. J. Bainbridge, K. Alfakih, T. R. Jones, S. Plein, J. P. Ridgway, and M. U. Sivananthan Assessment of Regional Left Ventricular Function: Accuracy and Reproducibility of Positioning Standard Short-Axis Sections in Cardiac MR Imaging Radiology, April 1, 2005; 235(1): 229 - 236. [Abstract] [Full Text] [PDF]

				J. C. Silva, C. E. Rochitte, J. S. Junior, J. Tsutsui, J. Andrade, E. E. Martinez, P. J. Moffa, J. C. Menegheti, R. Kalil-Filho, J. F. Ramires, et al. Late coronary artery recanalization effects on left ventricular remodelling and contractility by magnetic resonance imaging Eur. Heart J., January 1, 2005; 26(1): 36 - 43. [Abstract] [Full Text] [PDF]

				S. D. Zimmerman, J. Criscione, and J. W. Covell Remodeling in myocardium adjacent to an infarction in the pig left ventricle Am J Physiol Heart Circ Physiol, December 1, 2004; 287(6): H2697 - H2704. [Abstract] [Full Text] [PDF]

				C. L. Athanasuleas, G. D. Buckberg, A. W.H. Stanley, W. Siler, V. Dor, M. Di Donato, L. Menicanti, S. Almeida de Oliveira, F. Beyersdorf, I. L. Kron, et al. Surgical ventricular restoration in the treatment of congestive heart failure due to post-infarction ventricular dilation J. Am. Coll. Cardiol., October 6, 2004; 44(7): 1439 - 1445. [Abstract] [Full Text] [PDF]

				H. S. Maniar, B. P. Cupps, D. D. Potter, P. Moustakidis, C. J. Camillo, C. M. Chu, M. K. Pasque, and T. M. Sundt III Ventricular function after coronary artery bypass grafting: Evaluation by magnetic resonance imaging and myocardial strain analysis J. Thorac. Cardiovasc. Surg., July 1, 2004; 128(1): 76 - 82. [Abstract] [Full Text] [PDF]

				G. D. Buckberg Congestive heart failure: Treat the disease, not the symptom--return to normalcy J. Thorac. Cardiovasc. Surg., March 1, 2003; 125(90030): S41 - 49. [Full Text] [PDF]

				C. Pislaru, P. C. Anagnostopoulos, J. B. Seward, J. F. Greenleaf, and M. Belohlavek Higher myocardial strain rates duringisovolumic relaxation phase than duringejection characterize acutely ischemic myocardium J. Am. Coll. Cardiol., October 16, 2002; 40(8): 1487 - 1494. [Abstract] [Full Text] [PDF]

M. Saeed, N. Watzinger, G. A. Krombach, G. K. Lund, M. F. Wendland, M. Chujo, and C. B. Higgins Left Ventricular Remodeling after Infarction: Sequential MR Imaging with Oral Nicorandil Therapy in Rat Model Radiology, September 1, 2002; 224(3): 830 - 837. [Abstract] [Full Text] [PDF]