Regional Myocardial Three-Dimensional Principal Strains During Post-Infarction Remodeling

James J Pilla; Kevin J Koomalsingh; Jeremy R McGarvey; Walter RT Witschey; Larry Dougherty; Joseph H Gorman, III; Robert C Gorman

doi:10.1016/j.athoracsur.2014.10.067

. Author manuscript; available in PMC: 2016 Mar 1.

Published in final edited form as: Ann Thorac Surg. 2015 Jan 23;99(3):770–778. doi: 10.1016/j.athoracsur.2014.10.067

Regional Myocardial Three-Dimensional Principal Strains During Post-Infarction Remodeling

James J Pilla ^1,², Kevin J Koomalsingh ², Jeremy R McGarvey ², Walter RT Witschey ^1,², Larry Dougherty ¹, Joseph H Gorman III ², Robert C Gorman ²

PMCID: PMC4352409 NIHMSID: NIHMS658420 PMID: 25620591

Abstract

Background

The purpose of this study was to quantify myocardial 3D principal strains as the left ventricle (LV) remodels after myocardial infarction (MI). Serial quantification of myocardial strains is important for understanding the mechanical response of the LV to MI. Principal strains convert the 3D LV wall-based strain matrix with 3 normal and 3 shear elements, to a matrix with three non-zero normal elements, thereby eliminating the shear elements which are difficult to physically interpret.

Methods

The study was designed to measure principal strains of the remote, BZ and infarct regions in a porcine model of post- MI LV remodeling. MRI was used to measure function and strain at baseline, one-week, and four-week post-infarct. Principal strain was measured using 3D acquisition and optical flow method (OFM) for displacement tracking.

Results

Principal strains where altered as the LV remodeled. Maximum principal strain magnitude decreased in all regions including the non-infarcted remote while maximum principal strain angles rotated away from the radial direction in the BZ and infarct. Minimum principal strain magnitude followed a similar pattern however strain angles where altered in all regions. Evolution of principal strains correlated with adverse LV remodeling..

Conclusions

Using a state-of-the-art Imaging and OFM technique 3D principal strains can be measured serially after MI in Pigs. Results are consistent with progressive infarct stretching as well as decreased contractile function in the BZ and remote myocardial regions.

Keywords: Remodeling, Principal Strain, MR

Introduction

After a myocardial infarction (MI), the left ventricle (LV) is at risk for remodeling. Infarct expansion has been implicated in sustaining LV remodeling after MI [1]. Immediately after ischemia, the infarct region ceases to contract and is subjected to mechanical loads produced by cavity pressure and the non-infarcted remainder of the ventricle. This abnormal loading results in stretching of the infarct and increased stress in the borderzone (BZ) region adjacent to the infarct [2]. This dysfunctional BZ becomes more hypocontractile and progresses to involve additional perfused myocardium as remodeling continues.

Tagged MRI is a method of tracking the myocardial displacement using noninvasive markers [3]. The development of 3D tagging in a single acquisition makes regional LV measurements of the 3D strain possible [4,5]. Principal strains derived from the strain tensor provide information on the magnitude and direction of the deformation that are more amenable to physical interpretation than LV wall-based strains. For LV wall-based strains the strain matrix is oriented with respect to the left ventricular geometry. The coordinate system is rotated so that the x, y, and z direction align with the radial, circumferential, and longitudinal direction of the LV respectively. Components of the normal and shear strains are expressed as magnitudes values in the given wall-based direction. Changes in cardiac strain during remodeling are reported as normal and shear values with constant orientation. Normal strains are easily interpreted while shear strains are more difficult to comprehend because of their definition and complex orientation (Appendix 1).

Studies using invasive methods and tagging have suggested that mechanical changes in the BZ and infarct regions are associated with remodeling [6–8]. These studies have shown that wall-based circumferential and longitudinal strain magnitudes are altered in the infarct and BZ regions. However, a complete understanding of the mechanical alterations in these regions has been limited by the inability to measure 3D strains during remodeling.

The purpose of this study was to serially quantify myocardial 3D principal strains after MI to better understand the mechanism of post MI remodeling.

Material and Methods

The study was designed to quantify the changes in regional principal strains in a porcine model of post-MI remodeling. Animals were treated under an experimental protocol in compliance with NIH “Guide for the Care and Use of Laboratory Animals” (NIH publication 85–23, revised 1996) and approved by the University of Pennsylvania Institutional Animal Care and Use Committee. Five animals received a baseline MRI to access LV volume and regional principal strains prior to infarction. Subsequently, a posterolateral infarct was created by ligating the left circumflex artery distal to the first obtuse marginal artery branch and markers where placed along the boundary of the infarct. The animals were recovered and an MRI was performed at one and four week post-infarction.

MRI was used to measure LV end systolic and end diastolic volume (ESV, EDV), and regional principal strain at baseline, one, and four week after MI using a 3T Scanner (Siemens, Inc. Malvern, PA). LV volume imaging consisted of a CINE cardiac acquisition followed by strain imaging using a 3D tag sequence [4].

Data Analysis

LV volume data were obtained from the CINE MR images. The endocardial contours were drawn for each slice and phase then imported into a custom program to calculate volumes. Systolic LV regional strain was assessed from tagged images using a method previously described and validated [7]. An optimized 3D optical flow mapping (OFM) algorithm tracked the myocardium motion and produced displacement fields in the x, y, and z direction (Appendix 2). The Lagrangian Green’s strain tensor was calculated from the displacement fields between the initial state of ED and the deformed state of ESand principal strains where determined from the strain tensor by solving the eigenvalue problem. Principal strains represent the magnitude (eigenvalue) and direction (eigenvector) of the maximum stretch (E₁), maximum shortening (E₃), and mutually orthogonal difference of the stretch and shortening (E₂) of the myocardium. They differ from wall-based strains by providing a means for tracking not only strain magnitude but strain orientation as the heart remodels. (Appendix 1)

A local wall-based coordinate system was established for eigenvector orientation [9]. The circumferential (c) direction was defined by a vector tangent to epicardial contour. Radial direction (r) was defined by a vector inward and normal to the local epicardial wall. The longitudinal direction (l) was defined to be in the direction of the vector cross product of c and r, tangent to the epicardial surface. (Figure 1)

Radial-circumferential angle (θ_RC) is the principal strain vector projected on the radial/circumferential plane (A). Analogous descriptions are used for the radiallongitudinal (θ_RL) (B) and longitudinal-circumferential (θ_CL) planes (C). (**Long**: longitudinal, **Circ**: circumferential)

Three mid-ventricular slices were selected for quantitative analysis for each animal. To investigate alteration of the principal strains during post-infarction ventricular remodeling, each slice was divided into three segments: infarct, BZ, and remote. Infarct regions were delineated using the markers. The BZ region was determined to be the myocardium encompassed by a 20° arc between the marker and the remote region [10].

Statistics

Data are presented as mean ± SEM. LV volume data were assessed using one-way repeated measures ANOVA with Tukey post-hoc evaluation. Two-way repeated measures ANOVA with Tukey multiple comparisons was used to analyze the principal strain for differences between regions and time points. Pearson and Spearman’s ranked-order correlation where used to analyze the relationship between the change in regional strain and LV volume. Strain magnitudes and directions in each segment were compared by paired Student’s t-test. P < 0.05 was considered statistically significant for all comparisons.

Results

Global LV Remodeling

Global LV remodeling occurred in all animals throughout the study period. Statistically significant and progressive increases in EDV and ESV were documented as was a concurrent decrease in EF. (Table 1)

Table 1.

Change LV function with remodeling

	Baseline	1-week	4-weeks
EDV (ml)	61.4±4.7	90.4±8.7^*	119.9±11.8^†
ESV (ml)	34.7±3.6	58.9±5.1^*	84.1±8.3^†
EF (%)	43.3±2.5	34.7±1.4^*	29.7±3.2^†

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Mean ± SEM

p<0.05 vs. baseline,

^†

p<0.05 vs. 1-week.

Principal Strains

Representative 3D tagged images are shown in Figure 2. Altered deformation of the tags in the infarct and BZ regions is evident at ES. Maximum, minimum, and intermediate principal strains are presented below for each region and time point.

Short-axis mid-ventricular images acquired at baseline (left), 1-week (middle), and 4-weeks (right) after infarct. End-diastolic (ED) images (top row) show the change in LV size and geometry with infarct progression. Regional tag deformation at end-systole (ES) are shown for the three time points in the bottom row. Infarct region is delineated using markers which create signal voids (arrows).

Maximum Principal Strain

The magnitude (eigenvalue – E₁Mag) and direction (eigenvectors – E₁θ_RC, E₁θ_RL, E₁θ_CL) of the maximum principal strain (E₁) for the cohort of animals are presented in Figure 3. At baseline, the magnitude of the E₁ is similar in all regions (Figure 3A). E₁θ_RC (Figure 3B) and E₁θ_RL (Figure 3C) measure the angles between local radial direction and the projection of E₁ on to transverse and longitudinal plane, respectively. Both E₁θ_RC (Figure 3B) and E₁θ_RL (Figure 3C) before infarction are less than 10° while E ₁θ_CL is near 45° (Figure 3D) for all regions, demonstrating that before infarction E₁ is directed predominately in the radial direction indicative of normal wall thickening.

One and 4 weeks post-MI the magnitude of E₁ (i.e. E₁Mag) is significantly reduced in all myocardial regions (Figure 3A). Interpretation of this reduced magnitude is highly dependent on the associated changes in eigenvector directions: E₁θ_RC, E₁θ_RL and E₁θ_CL. Reduction in E₁Mag can be interpreted as a decrease in radial wall thickening if the associated eigenvector directions angles are not significantly changed from the baseline values (i.e. E₁θ_RC, and E₁θ_RL near zero; E₁θ_CL near 45°).However, changes in the associated eigen vector directions, especially increases in E₁θ_RC and E₁θ_RL, are indicative of some degree regional myocardial stretching.

One-week post-MI, the eigenvector of E₁ in the BZ and infarct regions deviate from the original radial direction, resulting in significant increase in E₁θ_RC with the infarct having the largest change. E₁θ_CL decreases in both the BZ and infarct regions. These changes are consistent with a shift from radial thickening to circumferential stretching. E₁θ_RL is unchanged in BZ but increases in the infarct indicating a shift from radial thickening to longitudinal stretch in this region. All angles in the remote region are unchanged at 1 week after MI; however, E₁Mag in this region is significantly reduced indicating reduced wall thickening.

Four weeks after MI, the eigenvector for E₁ in the infarct continues to deviate from the radial direction as indicated by the continued increases in E₁θ_RC and E₁θ_RL. These data are consistent with progressive circumferential and longitudinal infarct stretching as well as complete loss of wall thickening in the infarct region. In the BZ E₁Mag remains decreased and all three angles are increased, which is consistent with decreased wall thickening and increased circumferential and longitudinal stretching. In the remote region all angles remain preserved, but there is a persistent reduction in E₁Mag indicating that remote wall thickening remains impaired at 4 weeks after MI.

Minimum Principal Strain

The magnitude (eigenvalue – E₃Mag) and direction (eigenvectors - E₃θ_RC, E₃θ_RL and E₃θ_CL) of the minimum principal strain (E₃) for the cohort of animals are presented in Figure 4. Before infarction E₃Mag is similar in all regions. E₃θ_RC and E₃θ_RL approach 90° at baseline while E₃θ_CL is near 45° (Figure 4B, 4C and 4D). These eigenvec tors indicate that the majority of myocardial shortening occurs in the circumferential and longitudinal directions. The orientation of E₃θ_CL is also indicative of a spiraling or torsional contraction from apex to base (Figure 4D). The physical interpretation of these findings is that before infarction the minimum principal strain (E₃) represents the maximum shortening or contraction in the LV wall. During systole the normal LV simultaneously shortens in both the longitudinal and circumferential directions which contribute to the well-described torsional movements of the LV. [11, 12].

One week after MI all regions demonstrate decreased E₃, with the infarct region having the lowest strain (Figure 4A). The infarct region also exhibits a significant decrease in E₃θ_RC indicating a shifting from circumferential shortening to radial shortening. E₃θ_RL is significantly reduced in all regions due to a change in shortening orientation away from the longitudinal direction. At 4 weeks after MI, E₃Mag in all regions increases relative to 1 week, but fails to reach pre-infarction levels. The increased E₃Mag in the remote region may be jointly attributed to contractile compensation as well as increased infarct compliance which theoretically could decrease initial resistance to contraction. Whereas in the infarct the increase in E₃Mag is indicative of increased stretch and in the BZ it is likely a combination of both contractile compensation and increased stretch. Additionally, at 4-weeks E₃θ_RC and E₃θ_RL in the infarct remain significantly reduced relative to pre-infarction which is indicative of persistent atypical shortening in the radial direction (i.e. continued infarct systolic thinning). BZ region continued to have altered strain in both E₃θ_RL and E₃θ_CL. The remote region returned to baseline E₃θ_RL values while, E₃θ_CL continued to be elevated signifying altered torsion.

Bulls-eye plots of the minimum and maximum principal strain eigenvalues and eigenvector components for a representative animal are shown in figure [5A and 5B].

Intermediate Principal Strains

The physical interpretation of intermediate principal strain (E₂) is more difficult to determine. While E₁ and E₃ represent the thickening and shortening respectively, E₂ is the mutually perpendicular strain to E₁ and E₃. Following infarction significant changes occur in E₂ (Figure 6A). E₂θ_RC is altered at 4 weeks after infarction with little change in the remote and BZ (Figure 6B). E₂θ_RL is decreased at one week and four weeks after MI (Figure 6C).

Contrasting E₁Mag and E₃Mag, the regional magnitude of E₂ (E₂Mag) varies significantly with location before infarction. Following infarction E₂θ_RC is altered at 4 weeks with little change in the remote (REM) and borderzone (BZ). E₂θ_RL is decreased at one week and four weeks after MI. (+ p<0.05 vs baseline, *p<0.05 vs REM, • <0.05 vs BZ)

Correlation of Principal Strain with LV Remodeling

One-week post-MI the change in EDV from baseline was correlated with changes in several of the principal strain components. E₁ components in both the remote and infarct regions where highly correlated while components in the BZ and infarct where better correlated for E₃. ESV change was also correlated to components of both E₁ and E₃ (Table 2).

Table 2.

Correlation between function and principal strain at one-week

	Principal Strain	R value	p
EDV	E₁θ_RCremote	0.85	0.06
	E₁θ_RCinfarct	0.90	0.03
	E₃BZ	0.82	0.08
	E₃θ_RCBZ	−1	0.01
	E₃ θ_CLinfarct	−1	0.01
ESV	E₁θ_RCremote	0.81	0.09
	E₁θ_RCinfarct	−0.86	0.05
	E₁BZ	0.92	0.02
	E₃BZ	0.90	0.08
	E₃θ_RCBZ	−1	0.01

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E₃ was the only principal strain correlated with remodeling at four weeks post infarct (Table 3). EDV was correlated with eigenvector angles for both the remote and BZ while changes in ESV where associated with angles in the infarct and BZ regions.

Table 3.

Correlation between function and principal strain at four-week

	Principal Strain	R value	p
EDV	E₃θ_RLremote	0.90	0.08
	E₃θ_CLBZ	−0.90	0.08
ESC	E₃θ_RLBZ	0.85	0.07
	E₃θ_CLBZ	−0.81	0.09
	E₃θ_RLinfarct	0.90	0.08
	E₃θ_CLinfarct	−0.84	0.07

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Principal strains at one-week where compared to the change in LV remodeling from one-week to four-weeks as a potential predictor of remodeling (Table 4). E₃ infarct had a strong positive correlation with increasing EDV as the LV continued to remodel. Angular components of E₁ in the remote region also demonstrated an influence on dilatation. ESV dilatation was strongly negatively correlated to E₂ infarct and E₁ remote and positively correlated a maximum principal strain angle in the infarct region. Ejection fraction was correlated to the magnitudes of E₁ in the BZ and E₂ in the remote region as well as an angular component of E₁ infarct.

Table 4.

Correlation between principal strain at one-week and function from one-week to four-week

	Principal Strain	R value	p
EDV	E₁θ_RLremote	−0.88	0.04
	E₁θ_CLremote	−0.81	0.09
	E₃infarct	0.92	0.02
ESV	E₁remote	−0.94	0.01
	E₁θ_CLinfarct	0.94	0.01
	E₂infarct	−0.98	0.003
EF	E₁BZ	0.83	0.08
	E₁θ_RLinfarct	−0.86	0.06
	E₂remote	−0.90	0.02

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Comment

In this study we employed an optical flow method (OFM) [4] as well as an acquisition scheme that enables direct measurement of 3D myocardial displacement before and after a posterolateral MI in pigs. Using this combined acquisition and tracking method we quantified the temporal changes in the 3D strain tensor to gain an improved understanding of the evolution of post-infarct remodeling.

Our results indicated that during LV remodeling strain was altered in all regions and at all time-points after MI with the most pronounced changes occurring in the BZ and infarct regions. Previous ex vivo tissue experiments have demonstrated that infarct passive mechanical stiffness is greatest at 1-week after coronary occlusion and decreases progressively with time leading to increased tissue stretch [13]. This temporal change in infarct material properties is confirmed by the magnitude and orientation of the eigenvectors presented in this study. One week after MI, the orientation of the E₁ eigenvectors demonstrate that the infarct is stretching in the longitudinal and circumferential direction rather than thickening in the radial direction. Four weeks after MI, the orientation of the E₁ eigenvectors indicate progressive stretch in longitudinal and circumferential directions consistent with a continued decrease in infarct stiffness. Concomitant post-infarction changes in the orientation of the E₃ eigenvectors are indicative of progressive systolic wall thinning and confirm progressive loss of infarct stiffness during post-MI LV remodeling.

The changes in principal strain magnitude and angles over time are indicative of the active role the infarct mechanical properties play in LV remodeling and function. Rapid loss of contractile function after coronary occlusion immediately reduces the systolic compliance of the infarct. Over time the infarct stiffness decreases further, which increases infarct strain (stretching) and wall stress as the infarct becomes more compliant. Progressive infarct compliance increases the workload of the remote myocardium by increasing the work lost to stretching in the infarct region [14]. Increased LV wall stress has also been associated with maladaptive biologic sequelae particularly matrix metalloproteinase activation. [15]

BZ which is classified as the hypokinetic region adjacent to the infarct is under unique stress due to its position between the normally contracting remote myocardium and the non-contractile infarct [2]. This region undergoes a comparable temporal evolution of strain magnitude and angles as the infarct region even though it is not part of the initial ischemic insult. E₁Mag decreases early and remains depressed at the late time point. Angles are rotated away from the pre-infarct radial direction but to a lesser degrees than the infarct region suggesting there is a component of BZ thickening in the radial direction and a portion is stretching in both the longitudinal and circumferential directions. These observed temporal changes in BZ strain can be attributed to the altered stress distribution due the adjacent infarct region and are potentially a stimulus for continued remodeling [16, 17].

Remote principal strain magnitudes decreased at one week after MI, and then subsequently increased at 4-weeks. Improved strain in the remote region may be jointly attributed to contractile compensation and increased infarct compliance. Infarct stretch lessens initial contractile load increasing the remote strain; however, this results in increased LV workload for a given stroke volume [14].

The orientation E₁ eigenvectors (E₁θ_RC, E₁θ_RL and E₁θ_CL) in the remote region changed little after MI indicating myocardial thickening continued to be predominantly in the radial direction. Minimum principal strain angles where altered in the remote with remodeling, signifying that shortening had rotated away from the longitudinal direction to more circumferential orientation. This rotation was likely a consequence of reduced LV torsion [18, 19]. Decreased torsion due to the non-contracting infarct region would impair the LV’s ability to shorten in the longitudinal direction altering the longitudinal components (θ_RL and θ_CL) of E₃. This decreased shortening would increase myocardial stress and oxygen demand by increasing LV workload and could contribute to continue remodeling and decreased function [14, 20].

An appreciation of the temporal changes in LV wall principal strains after MI is crucial to understanding the mechanism of LV remodeling as well as to developing new strategies to halt or reverse the process. Altering the principal strains in the infarct and BZ has become a potential therapeutic target to prevent the progression of LV remodeling after MI. Mechanical and biological methods of modifying stress/strains in the infarct have been proposed. These include restraint devices [21, 22] placed over the infarct and stiffening agents injected [23, 24] into the infarct tissue. The successful application of these novel therapeutic approaches will be dependent on a better understanding of the time-dependent changes that occur in healing and mature MI

This study also examined the prognostic value of principal strains in predicting remodeling. Correlation studies between the evolution of principal strain and adverse LV remodeling demonstrate that regional magnitude and angles have prognostic significance indicating that principal strain changes precede ventricular dilatation and performance decline. Previous studies using 2D echo measuring normal strains have concluded that global circumferential and longitudinal strains were predictive of adverse remodeling after MI [25–27]. These global strain changes are a consequence of the regional alterations. Infarct and BZ principal strains will influence the strains over the entire LV by modifying systolic and diastolic stress distribution and blood flow patterns. Regional principal strain may be a more powerful predictor since remodeling post-MI likely begins on the regional level then affects the ventricle globally.

Principal strain orientation maybe less affected by preload and afterload especially in the infarct and BZ regions. Strain orientation in these regions is more a function of material properties than contractile load. Accordingly, regional principal strains maybe a better predictor of which patients will benefit from emerging infarct modification therapies as well as determining the optimal timing for such interventions.

Supplementary Material

NIHMS658420-supplement-1.pdf^{(129.9KB, pdf)}

NIHMS658420-supplement-2.pdf^{(86.8KB, pdf)}

Plots display three mid-ventricular slices from apex (inner) to base (outer) for remote (REM), border zone (BZ), and infarct (INF) regions. E₁ magnitude (E₁Mag) decreases in all regions at 1-Wk but increases at 4-wks in the infarct. Infarct E₁ vectors (E₁θ_RC, E₁θ_RL) shift from radial direction at baseline to more circumferential/longitudinal signifying decreased wall thickening and increased tissue stretch. Circumferential shortening (E₃Mag) decreases in all regions as the LV remodels while infarct E₃ vectors shifts (E₃θ_RC, E₃θ_RL) from circumferential/longitudinal to a more radial direction indicating tissue stretch.

Footnotes

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

NIHMS658420-supplement-1.pdf^{(129.9KB, pdf)}

NIHMS658420-supplement-2.pdf^{(86.8KB, pdf)}

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PERMALINK

Regional Myocardial Three-Dimensional Principal Strains During Post-Infarction Remodeling

James J Pilla, PhD

Kevin J Koomalsingh, MD

Jeremy R McGarvey, MD

Walter RT Witschey, PhD

Larry Dougherty, PhD

Joseph H Gorman III, MD

Robert C Gorman, MD

Abstract

Background

Methods

Results

Conclusions

Introduction

Material and Methods

Data Analysis

Figure 1. Coordinate System of Principal Strain Vectors.

Statistics

Results

Global LV Remodeling

Table 1.

Principal Strains

Figure 2. Tagged images of left ventricular (LV) remodeling following MI.

Maximum Principal Strain

Figure 3. Regional maximum principal strain magnitude and angles during LV remodeling.

Minimum Principal Strain

Figure 4. Regional minimum principal strain magnitude and angles during LV remodeling.

Intermediate Principal Strains

Figure 6. Regional intermediate principal strain magnitude and angles during LV remodeling.

Correlation of Principal Strain with LV Remodeling

Table 2.

Table 3.

Table 4.

Comment

Supplementary Material

Figure 5. Bulls-eye plots of maximum (E1) (A) and minimum (E3) (B) principal strain at baseline, one week (1-Wk) and four week (4-Wk) post-infarct for a representative animal.

Footnotes

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

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Links to NCBI Databases

Figure 5. Bulls-eye plots of maximum (E₁) (A) and minimum (E₃) (B) principal strain at baseline, one week (1-Wk) and four week (4-Wk) post-infarct for a representative animal.