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Ann Thorac Surg 2012;93:1188-1193. doi:10.1016/j.athoracsur.2011.12.066
© 2012 The Society of Thoracic Surgeons
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Original Articles: Adult Cardiac

First Evidence of Depressed Contractility in the Border Zone of a Human Myocardial Infarction

Jonathan F. Wenk, PhDa,b, Doron Klepach, PhDc,d, Lik Chuan Lee, PhDc,d, Zhihong Zhang, MSc, Liang Ge, PhDc,d, Elaine E. Tseng, MDc, Alastair Martin, PhDe, Sebastian Kozerke, PhDf, Joseph H. Gorman, III, MDg, Robert C. Gorman, MDg, Julius M. Guccione, PhDc,d,*

a Department of Mechanical Engineering, University of Kentucky, Lexington, Kentucky
b Department of Surgery, University of Kentucky, Lexington, Kentucky
c Department of Surgery, University of California, San Francisco, California
d Department of Bioengineering, University of California, San Francisco, California
e Department of Radiology and Biomedical Imaging, University of California, San Francisco, California
f Institute for Biomedical Engineering, University and ETH Zurich, Zurich, Switzerland
g Gorman Cardiovascular Research Group, University of Pennsylvania, Philadelphia, Pennsylvania

Accepted for publication December 19, 2011.

Abbreviations and Acronyms BZ = border zone; ED = end-diastolic; ES = end-systolic; FE = finite element; LV = left ventricle left ventricular; MI = myocardial infarction; MRI = magnetic resonance imaging; MSE = mean squared error

* Address correspondence to Dr Guccione, UCSF/VA Medical Center (112D), 4150 Clement St, San Francisco, CA 94121 (Email: guccionej{at}surgery.ucsf.edu).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background: The temporal progression in extent and severity of regional myofiber contractile dysfunction in normally perfused border zone (BZ) myocardium adjacent to a myocardial infarction (MI) has been shown to be an important pathophysiologic feature of the adverse remodeling process in large animal models. We sought, for the first time, to document the presence of impaired contractility of the myofibers in the human BZ myocardium.

Methods: A 62-year-old man who experienced an MI in 1985 and had recently had complete revascularization was studied. Myofiber systolic contractile stress developed in the normally perfused BZ adjacent to the MI (T max_B) and that developed in regions remote from the MI (T max_R) were quantified using cardiac catheterization, magnetic resonance imaging, and mathematical modeling.

Results: The resulting finite element model of the patient's beating left ventricle was able to simulate the reduced systolic strains measured using magnetic resonance imaging at matching left ventricular pressures and volumes. The T max_B (73.1 kPa) was found to be greatly reduced relative to T max_R (109.5 kPa). These results were found to be independent of assumptions relating to BZ myofiber orientation.

Conclusions: The results of this study document the presence of impaired contractility of the myofibers in the BZ myocardium and support its role in the post-MI remodeling process in patients. To fully establish this important conclusion serial evaluations beginning at the time of the index MI will need to be performed in a cohort of patients. The current study supports the importance and demonstrates the feasibility of larger and longer-term studies.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Adverse left ventricular (LV) remodeling after myocardial infarction (MI) is responsible for nearly 70% of heart failure cases. Previous studies in clinically relevant large animal preparations using state-of-the-art magnetic resonance imaging (MRI) tissue tagging and finite element (FE) modeling algorithms have demonstrated that a spatially progressive loss of contractile function in perfused myocardium outside the infarct zone is central to the mechanism by which an initially well-tolerated acute myocardial loss progressively leads to chronic symptomatic heart failure [1–4]. These animal studies have established that loss of contractile function occurs initially and is most severe in the perfused border zone (BZ) adjacent to the infarct. In this report we present a fully validated tissue tagging and analytic modeling technique to assess regional contractile function in the remodeled human heart.

An important feature of this investigation is the combined use of three-dimensional complementary spatial modulation of magnetization for measuring regional myocardial deformation and a realistic mathematical (FE) model of the infarcted LV for computing regional myocardial force development. The technique has been previously validated by direct ex vivo active force measurements in skinned fiber preparations [5]. Direct measurement of such forces in an intact LV has been unreliable in animals and is not possible in patients.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
This study was approved by the Committee on Human Research at the University of California at San Francisco Medical Center and the Institutional Review Board of the San Francisco Veterans Affairs Medical Center. Informed consent for MRI was obtained from the patient who had no contraindication to the procedure.

Experimental Measurements
A 62-year-old man experienced an MI in 1985. In 2010, he underwent coronary artery bypass grafting. Before coronary artery bypass grafting, persantine thallium stress testing demonstrated reversible defects that were all amenable to surgical revascularization. The patient underwent three-dimensional complementary spatial modulation of magnetization (Fig 1 A) 6 weeks after coronary artery bypass grafting, at which time there was no evidence of ongoing ischemia. In addition, the patient underwent magnetic resonance delayed hyperenhancement to precisely delineate the infarct region. Left ventricular pressure was continuously measured by means of cardiac catheterization. The endocardial and epicardial LV surfaces were contoured from the magnetic resonance images, and the systolic tags were segmented to compute the systolic myocardial strain at the midwall of the LV [5, 6].


Figure 1
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  		Fig 1. (A) Short-axis view from three-dimensional complementary spatial modulation of magnetization image of patient left ventricle, with the posterior region circled in blue, and (B) finite element model reconstructed from the magnetic resonance images, showing the remote (red), border zone (green), and infarct (tan) regions.

 
Finite Element Model
The images used to build the model were from the last MRI time step before mitral valve opening. This point was during the latter part of isovolumic relaxation, and was selected because the stress is at a minimum in the LV. A customized version of the MRI postprocessing software, FindTags (Laboratory of Cardiac Energetics, National Institutes of Health, Bethesda, MD), was used to contour the endocardial and epicardial LV surfaces. An FE model was then projected to the LV wall surfaces (Truegrid, XYZ Scientific Applications, Inc, Livermore, CA). The geometry was meshed with eight-node trilinear brick elements, for a total of 2,400 elements, using a single integration point for computational efficiency. The transmural mesh density was adjusted until the ventricular volume changed by less than 5% for a given load. It was found that three elements are sufficient for accurate ventricular volume calculations [5]. Each region (remote, BZ, and infarct) was assigned different material properties [5]. Cardiac myofiber angles were assigned to vary transmurally from –60 degrees to 60 degrees (epicardium to endocardium), relative to the circumferential direction, in all regions [7].

Boundary and Loading Conditions
The boundary conditions of the LV were assigned to fully constrain the displacement at the epicardial-basal edge, while allowing the remaining nodes at the base to move in the circumferential-radial plane. The inner endocardial wall of the LV was loaded with the clinically measured pressures to simulate the end-diastolic (ED) and end-systolic (ES) states. It should be noted that the pressure boundary conditions were applied by quickly ramping the load to the measured value and then holding the load constant as the simulation reached a steady-state solution at ED and ES.

Material Properties of the Heart
Nearly incompressible, transversely isotropic, hyperelastic constitutive laws for passive [8] and active myocardium [9] were modeled with a user-defined material subroutine in the explicit FE solver, LS-DYNA (Livermore Software Technology Corporation, Livermore, CA). Passive material properties were represented by the strain energy function:


Formula 1

(1)

where E 11 is fiber strain, E 22 is cross-fiber strain, E 33 is radial strain, E 23 is shear strain in the transverse plane, and E 12 and E 13 are shear strain in the fiber-cross fiber and fiber-radial planes, respectively. Values for the material constants b f , b t , and b fs were chosen as 24.63, 9.63, and 8.92, respectively, which were scaled (ie, a value of 6 was added to each exponential material constant) from previous studies of canine myocardium [8]. To validate the models, the material constant C was adjusted until the LV ED volumes matched the experimentally measured values. As was the case in our previous FE models of the infarcted ovine LV [2, 5, 6], we assume that C has the same value in the BZ and remote myocardium but is 10 times stiffer in the infarct.

Active contraction was modeled by defining total stress as the sum of the passive stress derived from the strain energy function and an active fiber directional component, T 0, which is a function of time, t, peak intracellular calcium concentration, Ca 0, sarcomere length, l, and maximal isometric tension achieved at the longest sarcomere length, T max [5]:


Formula 2

(2)

where S is the second Piola-Kirchoff stress tensor, p is the hydrostatic pressure introduced as the Lagrange multiplier needed to ensure incompressibility, J is the Jacobian of the deformation gradient tensor, C is the right Cauchy-Green deformation tensor, Dev is the deviatoric projection operator:


Formula 3

(3)

and Formula is the deviatoric contribution of the strain energy function, Formula (Eq 1). The assumption of near incompressibility of the myocardium requires the decoupling of the strain energy function into dilational and deviatoric components:


Formula 4

(4)

where U is the dilatational (volumetric) contribution [10].

The active fiber-directed stress component is defined by a time-varying elastance model, which at end-systole, is reduced to [11]:


Formula 5

(5)

with m and b as constants, and the length-dependent calcium sensitivity, ECa 50, is given by:


Formula 6

(6)

where B is a constant, (Ca 0)max is the maximal peak intracellular calcium concentration, l 0 is the sarcomere length at which no active tension develops, and l R is the stress-free sarcomere length. The material constants for active contraction were taken to be [12] Ca 0, 4.35 μmol/L; (Ca 0)max, 4.35 μmol/L; B, 4.75 μm–1; l 0, 1.58 μm; m, 1.0489 s/μm; b, –1.429 seconds, and l R was set at 1.85 μm, the sarcomere length in the unloaded reference configuration. On the basis of biaxial stretching experiments [13] and FE analyses [14, 15], cross-fiber, in-plane stress equivalent to 40% of that along the myocardial fiber direction was added. To further validate the models, the parameter T max was formally optimized.

Material Parameter Optimization
The objective function for the optimization was taken to be the mean squared error (MSE) [1]. The passive material parameters were determined such that the FE model-predicted LV ED volume matched the patient-specific in vivo measured value. The systolic material parameters in the remote (T max_R) and BZ (T max_B) regions were estimated by minimizing the errors between FE model-predicted and in vivo measured systolic strains and LV ES volume. The goal of the optimization is to minimize the MSE:


Formula 7

(7)

where n is the in vivo strain point, N is the total number of in vivo strain points, Formula is the computed FE strain at each strain point, and V ED and V ES are the computed FE LV ED and ES volumes, respectively. The overbar represents the experimental in vivo measurements.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
The LV ED and ES pressures were measured with cardiac catheterization, and found to be 10 mm Hg and 107 mm Hg, respectively. These values were applied to the endocardial wall of the FE model as a patient-specific boundary condition. The measured ED and ES volumes were found to be 60.3 mL and 35.3 mL, respectively. The computed ED and ES volumes from the optimization were 60.3 mL and 37.05 mL, respectively, which are within 5% of the measured values.

The optimization displayed good convergence, with a 90% confidence interval of 18%, which only took 10 iterations to reach (Fig 2). However, the optimization procedure was allowed to run 5 extra iterations to ensure convergence. The final MSE value of 8.53 was calculated using 816 strain components and two volumes. The MSE value indicates generally good agreement between the FE model-predicted systolic strains and the patient-specific in vivo measured strains, and is similar in magnitude to our previous studies, which were validated with infarcted ovine hearts [5, 6].


Figure 2
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  		Fig 2. Convergence plots of (A) maximal isometric tension achieved at the longest sarcomere length in the remote region (Tmax_R) and (B) maximal isometric tension achieved at the longest sarcomere length in the border zone region (Tmax_B) during the numerical optimization process. Note that the solution was stable after roughly 10 iterations.

 
The passive material parameter was found to be C = 0.195 kPa, which allowed the FE model LV volume to match the experimental value within 2%. The optimized contractility parameters for this patient are given in Table 1, and were found to be T max_R = 109.5 kPa and T max_B = 73.1 kPa. This shows a 33% decrease in contractile function in the BZ compared with the remote region. To assess the influence of varying BZ helix fiber angles, a sensitivity study was conducted in which the BZ fiber angles were rotated. Table 1 shows the effect of helix angles in remote (HA _R), BZ (HA _B), and infarct (HA _I) regions on the optimized parameters T max_R and T max_B. A helix angle is the angle (in degrees) that the local myofiber direction makes with the circumferential direction (eg, a helix angle of 0 means the myofiber direction is circumferential, whereas a helix angle of 90 degrees means the myofiber direction is longitudinal). A 20-degree "leftward" shift in HA _B and HA _I (case 2 versus 1) results in only a 2.1% decrease and 9.5% increase in T max_R and T max_B, respectively.


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  		Table 1 Contractility Parameter, Based on Myofiber Helix Angle
 
It can be seen in Figure 3 that the systolic myofiber strain in the remote region of the FE model is negative, which implies the myofibers are shortening during contraction. In addition, the strain in the BZ is elevated (ie, less negative) relative to the remote region, indicating that the myofibers are being stretched during systole. The infarct region demonstrates positive strain, indicating that this region is noncontractile and dyskinetic. It can be seen in the three-dimensional complementary spatial modulation of magnetization image (Fig 1A) that the posterior wall has virtually no contractility during the systolic phase (region in the blue circle). This confirms the presence of the MI, which was assumed to have T max_I = 0 kPa.


Figure 3
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  		Fig 3. End-systolic myofiber strain distribution. (A) View of epicardial surface with infarct and border zone regions outlined. (B) Interior view of posterior endocardial wall with infarct and border zone regions outlined. (C) Midventricular slice through remote, border zone, and infarct regions. Note the elevated strain in the border zone.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
These studies provide evidence that myocardial contractility in the BZ region of a human MI is substantially less (25% to 33% depending on regional myofiber orientation) than that in regions remote from the MI. The temporal progression in extent and severity of regional contractile dysfunction in normally perfused myocardium adjacent to the infarct has been shown to be an important pathophysiologic feature of the adverse remodeling process in large animal models [16]. The results reported here support that the process demonstrated in large animal models likely occurs in patients.

Myocardial tissue tagging using complementary spatial modulation of magnetization allows detailed assessment of myocardial motion. To capture the complex three-dimensional cardiac motion pattern, multiple two-dimensional tagged slices are usually acquired in different orientations. These approaches are prone to slice misregistration and associated with long acquisition times. In this work, we applied the accelerated three-dimensional tagging acquisition method of Rutz and coworkers [17], which enabled assessment of three-dimensional motion information with whole heart coverage in three short breathholds. They found hypokinetic regions in patients with an MI corresponded well with regions exhibiting hyperenhancement after contrast injection. However, Rutz and colleagues did not attempt to quantify the forces or stresses responsible for that hypokinesis.

Using an MRI-based FE stress analysis of a clinically relevant large animal preparation, Guccione and associates [2] suggested that the mechanism underlying mechanical dysfunction in the BZ of LV aneurysm is primarily the result of myocardial contractile dysfunction rather than increased wall stress in this region. Then, Walker and coworkers [15, 18] used a fixed ratio of 2:1 in remote versus BZ region contractility to compute regional myocardial material properties and stress in 6 animals [18] after linear repair of LV aneurysm and in 5 animals that underwent a sham operation [15]. More recently, Sun and colleagues [5] developed a computationally efficient formal optimization that allows regional myocardial contractility to be quantified without enforcing the fixed ratio mentioned above. Moreover, in vivo estimates of regional myocardial contractility were validated using ex vivo direct force measurements in skinned fiber preparations. Then, that formal optimization was applied in 6 animals 2 weeks before and 2 and 6 weeks after patch repair of LV aneurysm [16], as well as in an animal with posterobasal MI [6]. Most important, in every single animal and time included in those previous studies (32 instances), myocardial contractility in the BZ of the MI was significantly less than that in regions remote from the MI.

In this paper we present two distinct values for the contractility parameters for BZ (T max_B) and remote myocardium (T max_R). In a recent study of an ovine model of LV aneurysm [19], we found that our corresponding FE model was better able to reproduce the experimental LV pressure versus myocardial strain data when we allowed T max_B to have values that vary linearly from 0 at the boundary between the aneurysm and BZ to T max_R at the boundary between the BZ and remote myocardium. We expect a similar gradient in T max_B to exist in the BZ of other types of MIs, including the MI of the patient in the present study.

At present, the greatest challenge in quantifying regional myocardial contractility in patients is the very sophisticated MRI hardware required to quantify regional myofiber orientation in vivo. The diffusion imaging approach proposed by Gamper and associates [20] appears to be the state of the art, but it requires an MRI scanner with uniquely large gradients (of at least 80 mT/m). Because we did not have access to such a scanner, we instead repeated our quantification of regional myocardial contractility in a patient with an MI using a range of myofiber angle distributions. Case 2 of the fiber angle sensitivity study corresponds to the in vivo diffusion MRI data of Wu and coworkers [21, 22] concerning patients with an MI in which the percentage of left-handed helical fibers (negative subepicardial helix angles) increased from the remote zone to the BZ and infarct zone, and the percentage of right-handed helical fibers (positive subendocardial helix angles) decreased from the remote zone to the BZ and infarct zone. The findings of Wu and colleagues [21, 22] are at variance with the ex vivo observations of Chen and associates [23]. Recent ex vivo diffusion MRI data from infarcted rat hearts indicate that BZ helix angles are preserved [24, 25].

This investigation demonstrates the substantial depression of myocardial contractility in the BZ of a human MI relative to that in regions remote from the MI. The current study evaluates one patient at one time very remote from the index MI; however, the results of this study support the central role of the BZ myocardium in the post-MI remodeling process in patients that has been demonstrated in large animal infarct models. To fully establish this important conclusion, serial evaluations beginning at the time of the index MI will need to be performed in a large cohort of patients. The current study supports the importance and demonstrates the feasibility of such large and long-term studies.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was supported by NIH grants R01-HL063954 (RCG), R01-HL103723 (RCG), R01-HL073021 (JHG), R01-HL077921 (JMG), and R01-HL086400 (JMG). This support is gratefully acknowledged. Doctors R.C. Gorman and J.H. Gorman are supported by individual American Heart Association Established Investigator Awards.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Gorman RC, Gorman III JH. Mechanism underlying mechanical dysfunction in the border zone left ventricular aneurysm. A finite element model study. Invited commentary. Ann Thorac Surg 2001;71:662.[Free Full Text]
  2. Guccione JM, Moonly SM, Moustakidis P, et al. Mechanism underlying mechanical dysfunction in the border zone of left ventricular aneurysm: a finite element model study Ann Thorac Surg 2001;71:654-662.[Abstract/Free Full Text]
  3. Jackson BM, Gorman JH, Moainie SL, et al. Extension of borderzone myocardium in postinfarction dilated cardiomyopathy J Am Coll Cardiol 2002;40:1160-1167.[Medline]
  4. Ratcliffe MB. Non-ischemic infarct extension: a new type of infarct enlargement and a potential therapeutic target [invited commentary] J Am Coll Cardiol 2002;40:1168-1171.
  5. Sun K, Stander N, Jhun C-S, et al. A computationally efficient formal optimization of regional myocardial contractility in a sheep with left ventricular aneurysm J Biomech Eng 2009;131:111001.[Medline]
  6. Wenk J, Sun K, Zhang Z, et al. Regional left ventricular myocardial contractility and stress in a finite element model of posterobasal myocardial infarction J Biomech Eng 2011;133:044501.[Medline]
  7. Streeter Jr DD, Spotnitz HM, Patel DP, Ross Jr J, Sonnenblick EH. Fiber orientation in the canine left ventricle during diastole and systole Circ Res 1969;24:339-347.[Abstract/Free Full Text]
  8. Guccione JM, McCulloch AD, Waldman LK. Passive material properties of intact ventricular myocardium determined from a cylindrical model J Biomech Eng 1991;113:42-55.[Medline]
  9. Guccione JM, Waldman LK, McCulloch AD. Mechanics of active contraction in cardiac muscle: part II—Cylindrical models of the systolic left ventricle J Biomech Eng 1993;115:82-90.[Medline]
  10. Wenk JF, Papadopoulos P, Zohdi TI. Numerical modeling of stress in stenotic arteries with microcalcifications: a micromechanical approximation J Biomech Eng 2010;132:091011.[Medline]
  11. Tözeren A. Continuum rheology of muscle contraction and its application to cardiac contractility Biophys J 1985;47:303-309.[Medline]
  12. Guccione JM, Costa KD, McCulloch AD. Finite element stress analysis of left ventricular mechanics in the beating dog heart J Biomech 1995;28:1167-1177.[Medline]
  13. Lin DH, Yin FC. A multiaxial constitutive law for mammalian left ventricular myocardium in steady-state barium contracture or tetanus J Biomech Eng 1998;120:504-517.[Medline]
  14. Usyk TP, Mazhari R, McCulloch AD. Effect of laminar orthotropic myofiber architecture on regional stress and strain in the canine left ventricle J Elast 2000;61:143-164.
  15. Walker JC, Ratcliffe MB, Zhang P, et al. MRI-based finite-element analysis of left ventricular aneurysm Am J Physiol Heart Circ Physiol 2005;289:H692-H700.[Abstract/Free Full Text]
  16. Sun K, Zhang Z, Suzuki T, et al. Dor procedure for dyskinetic anteroapical left ventricular aneurysm fails to improve myocardial contractility in the border zone J Thorac Cardiovasc Surg 2010;140:233-239.[Abstract/Free Full Text]
  17. Rutz AK, Ryf S, Plein S, Boesiger P, Kozerke S. Accelerated whole-heart 3D CSPAMM for myocardial motion quantification Magn Reson Med 2008;59:755-763.[Medline]
  18. Walker JC, Ratcliffe MB, Zhang P, et al. Magnetic resonance imaging-based finite element stress analysis after linear repair of left ventricular aneurysm J Thorac Cardiovasc Surg 2008;135:1094-1102.[Abstract/Free Full Text]
  19. Lee LC, Wenk JF, Klepach D, et al. A novel method for quantifying in-vivo regional left ventricular myocardial contractility in the border zone of a myocardial infarction J Biomech Eng 2011;133:094506.[Medline]
  20. Gamper U, Boesiger P, Kozerke S. Diffusion imaging of the in vivo heart using spin echoes—considerations on bulk motion sensitivity Magn Reson Med 2007;57:331-337.[Medline]
  21. Wu MT, Su MYM, Huang YL, et al. Sequential changes of myocardial microstructure in patients postmyocardial infarction by diffusion-tensor cardiac MR correlation with left ventricular structure and function Circ Cardiovasc Imaging 2009;2:32-40.[Abstract/Free Full Text]
  22. Wu MT, Tseng WYI, Su MYM, et al. Diffusion tensor magnetic resonance imaging mapping the fiber architecture remodeling in human myocardium after infarction: correlation with viability and wall motion Circulation 2006;114:1036-1045.[Abstract/Free Full Text]
  23. Chen J, Song SK, Liu W, et al. Remodeling of cardiac fiber structure after infarction in rats quantified with diffusion tensor MRI Am J Physiol Heart Circ Physiol 2003;285:H946-H954.[Abstract/Free Full Text]
  24. Sosnovik DE, Wang R, Dai G, Reese TG, Wedeen VJ. Diffusion MR tractography of the heart J Cardiovasc Magn Reson 2009;11:47.[Medline]
  25. Sosnovik DE, Wang RP, Dai GP, et al. Diffusion spectrum MRI tractography reveals the presence of a complex network of residual myofibers in infarcted myocardium Circ Cardiovasc Imaging 2009;2:206-212.[Abstract/Free Full Text]

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Invited Commentary
Jerry Braun
Ann. Thorac. Surg. 2012 93: 1193-1194. [Extract] [Full Text] [PDF]



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