Ann Thorac Surg 2005;80:2186-2192
© 2005 The Society of Thoracic Surgeons
Original article: Cardiovascular
Myocardial Systolic Strain is Decreased After Aortic Valve Replacement in Patients With Aortic Insufficiency
Benjamin J. Pomerantz, MD
a
,
Jason R. Wollmuth, MD
a
,
Marc D. Krock, MD
a
,
Brian P. Cupps, PhD
a
,
Pavlos Moustakidis, MD
a
,
Nicholas T. Kouchoukos, MD
b
,
Victor G. Davila-Roman, MD
a
,
Michael K. Pasque, MD
a
,
*
a Department of Surgery, Division of Cardiothoracic Surgery, Washington University in St. Louis, St. Louis, Missouri
b Missouri Baptist Medical Center, St. Louis, Missouri
Accepted for publication May 27, 2005.
* Address correspondence to Dr Pasque, Washington University in St. Louis, One Barnes-Jewish Hospital Plaza, Suite 3103 Queeny Tower, St. Louis, MO 63110-1013 (Email: pasquem{at}msnotes.wustl.edu).
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Abstract
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BACKGROUND: Left ventricular three-dimensional nonlinear systolic strain determinations have potential to detect small decrements in ventricular function in patients with aortic insufficiency before and after aortic valve replacement.
METHODS: Magnetic resonance imaging with tissue-tagging was performed on 42 normal volunteers and 14 patients with chronic aortic insufficiency both before and 28 ± 11 months after aortic valve replacement. Preoperative and postoperative left ventricular volume, dimensions and ejection fraction were determined for all subjects. Left ventricular systolic radial, circumferential, longitudinal, and minimum principal strain were calculated for six left ventricular regions.
RESULTS: After aortic valve replacement, left ventricular volume and dimensions decreased significantly (p < 0.001) and ejection fraction increased nonsignificantly (p = 0.096). Strain values in preoperative aortic insufficiency patients did not differ significantly from controls. At an average of 28 ± 11 months postoperatively, however, regional three-dimensional minimum principal and longitudinal strain was decreased in all six ventricular regions as well as globally (p < 0.03) compared with normal control values. Circumferential strain was significantly decreased globally and in all but two regions (p < 0.03).
CONCLUSIONS: These magnetic resonance imaging–based techniques are sensitive enough to detect a previously unrecognized, significant decrease in both global and regional three-dimensional left ventricular systolic strain 2 years after aortic valve replacement for minimally symptomatic chronic aortic insufficiency despite improvement in ejection fraction and a decrease in left ventricular size. The reasons for a significant decline in left ventricular systolic strain after successful aortic valve replacement in minimally symptomatic chronic aortic insufficiency patients are not clear and warrant further investigation.
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Introduction
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The ultimate goal of clinicians who follow up patients with chronic aortic insufficiency (AI) is the timely detection of the onset of an irreversible decrement in ventricular function that has the potential to impact either quality or length of life. The achievement of this goal requires the availability of highly accurate, clinically applicable indices that are sensitive enough to detect small changes in myocardial function early in the course of the ventricular remodeling process.
Magnetic resonance imaging (MRI), combined with radiofrequency tissue-tagging techniques [1], can accurately characterize patient-specific, three-dimensional ventricular wall geometry. These techniques also allow the three-dimensional tracking of transmural, regionally varying myocardial point displacements and calculation of myocardial strain that has been shown to agree with previous results of three-dimensional studies involving implantation of radiopaque beads in the canine model [2]. In addition, these techniques are very sensitive in detecting subtle wall motion abnormalities in ischemic heart disease and hypertrophic cardiomyopathy [3, 4]. The exceptional accuracy of these techniques suggests that they may have potential for the more sensitive detection of myocardial injury before and after aortic valve replacement for chronic aortic insufficiency.
Our group has previously documented regional changes in two-dimensional circumferential shortening in a small group of AI patients studied 5 months after aortic valve replacement [5]. In this study, we used MRI with radiofrequency tissue-tagging to characterize the three-dimensional left ventricular global and regional systolic strain patterns in a larger group of patients with chronic aortic insufficiency studied before and several years after aortic valve replacement.
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Patients and Methods
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Patients
This study was approved by the Human Studies Committee at Washington University, St. Louis, Missouri. Informed written consent was obtained from all patients and control subjects. All patients referred to the Washington University Medical Center for aortic valve replacement were screened for eligibility. Patients with pacemakers, claustrophobia, or a history of ventricular tachycardia, atrial fibrillation, or other arrhythmias were excluded from the study. Patients with coronary artery disease, history of myocardial infarction, unstable angina, or coexisting aortic stenosis or mitral valvular disease were also excluded from the study. Follow-up scans were scheduled to be performed 2 years after surgery. Three patients enrolled into the study had preoperative scans but were lost to follow-up and were not included in this analysis. In addition, 1 patient was not included because of significant ectopy resulting in poor image quality.
The study group consisted of 14 patients (12 men and 2 women) with a mean age of 44.7 ± 15.9 years. Seven patients were New York Heart Association class I, 6 patients were class II, and 1 patient was class III. All patients underwent evaluation of their left ventricular function by echocardiography or left ventriculography as part of their routine AI evaluation. The etiology of the AI was secondary to a bicuspid aortic valve (8 patients), rheumatic disease (3 patients), and aortic root dilation/aneurysm (3 patients). Four patients underwent a Ross procedure whereas 5 patients each had aortic valve replacement with mechanical and bioprosthetic valves. Forty-two healthy volunteers (18 men and 24 women) served as a control group, mean age 32.8 ± 13.1 years. All control patients had normal ventricular diameter and normal systolic function. Control subjects had normal physical and electrocardiographic findings and no history of any heart disease.
Data Acquisition
Imaging was performed with the subjects at rest in a 1.5 Tesla MR scanner (Magnetom Vision; Siemens Medical Systems, Iselin, New Jersey). A series of scout images were obtained to locate the heart and establish the long- and short-axis imaging planes. Subsequently, a set of parallel short-axis imaging planes were obtained at 8mm intervals beginning at the level of the mitral valve and ending at a short-axis imaging plane that contained only apical myocardium and no left or right ventricular endocardium. An additional set of four long-axis imaging planes were obtained according to the following criteria: (1) orthogonal to the short-axis imaging planes, (2) intersecting the centroid of the left ventricle, and (3) oriented in a radial fashion with 45-degree separation between long-axis imaging planes (Fig 1).
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Fig 1. Left ventricular imaging planes. (A) Location of the five short-axis imaging planes used in the analysis as illustrated on a long-axis image. (B) Location of the four long-axis imaging planes as illustrated on a midventricular short-axis image.
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Image acquisition was synchronized with real-time electrocardiogram at the time of the MRI scanning. The R wave of the electrocardiogram signal was used to trigger MRI scan acquisition. During the actual imaging, the subjects were instructed to hold their breath at midexpiration and a series of images was acquired at 29-ms intervals until the approximate completion of the entire cardiac cycle at each imaging plane. Each cine sequence of images consisted of 12 to 18 images acquired over a period of 25 to 30 seconds during a single breath hold. For each subject, the end-diastolic image was chosen as the first image in sequence (Fig 2A and C) and the end-systolic image was determined by choosing the smallest ventricular size in sequence (Fig 2B and D). Total MRI data acquisition time was approximately 60 minutes. For each selected imaging plane, a single-slice MR tagged image was collected with a sequence consisting of a spatial modulation of magnetization [6] radiofrequency tissue-tagging preparation followed by a two-dimensional fast low flip angle shot cine image acquisition. Imaging parameters were a repetition time (TR) of 58 ms per cine segment, an echo time (TE) of 2.9 ms, an excitation angle (
) of 30 degrees, a slice thickness of 8 mm, and an acquisition matrix of 256 x 256. The field of view was set to 300 x 300 mm2 and 400 x 400 mm2 for the short- and long-axis images, respectively.
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Fig 2. Representative images from a patient with chronic aortic insufficiency. Short-axis end-diastolic image (A) and end-systolic image (B). Long-axis end-diastolic image (C) and end-systolic image (D) as determined by choosing the largest and smallest ventricular size in the systolic cycle.
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Finite Element Model Construction—Strain Analysis
Five midventricular short-axis image sets and four radially oriented long-axis image sets were used in each analysis. The image sets were analyzed in the following manner. Raw images were analyzed using a personal computer with the Linux operating system using custom-designed analysis software. Each of the short-axis imaging planes was illustrated on a four-chamber long-axis end-diastolic image. The line between the apex and the base (middle of the mitral valve) of the heart was drawn, and the distance was measured. The short-axis imaging plane that was closest to the midpoint of that line was selected as the middle of the five short-axis image sets that were used for the analysis in all subjects. The middle short-axis image was used to measure the end-systolic and end-diastolic diameter. Endocardial and epicardial boundaries were manually identified on each of the short- and long-axis image sets. An initial spline representation of the tag lines on the end-diastolic images was constructed based on the spacing between adjacent tag lines. Tag lines were located on successive images using a semiautomatic algorithm. The algorithm that we used was based on a method reported by McVeigh and Zerhouni [7]. With this method, an initial approximation for each tag line was adjusted based on the local pixel density function. Spline curves from corresponding tag lines were used to construct a spline surface representation of the tag surfaces. Three-dimensional systolic displacements were computed along the intersection curves of individual short- and long-axis tag surfaces (Fig 3) using a previously described and validated method [8]. Analysis of the displacement data was carried out using the finite element software package, StressCheck (ESRD, St. Louis, Missouri), utilizing features that were specifically implemented for our laboratory. A finite element mesh of a three-dimensional midventricular slab of the left ventricle was constructed as follows: endocardial and epicardial contours from each of the short-axis images at end diastole were used to construct a spline surface representation of the endocardial and epicardial surfaces. A mesh for each model was manually created consisting of six hexahedral elements corresponding to the anteroseptal, anterior, anterolateral, posterolateral, posterior and posteroseptal walls. Classification and nomenclature for these elements follows the recommendations of the American Society of Echocardiography Committee on Standards [9] (Fig 4). Predicted displacements at any point within the domain of the model were obtained from a least squares fitting of the measured displacement data using the finite element basis functions [10]. Average regional values of the minimum principal strain (e
3) were computed from the results of this fitting. The minimum principal strain is the smallest eigenvalue of the strain tensor and is associated with the maximum contraction that occurs at a given material point. In addition, circumferential (e
cc), radial (e
rr), and longitudinal (e
ll) strain values were also calculated. The Almansi strain tensor was used for all calculations [11].
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Fig 4. A finite element mesh of a three-dimensional midventricular slab of the left ventricle. A mesh for the model was manually created consisting of six hexahedral elements corresponding to the anteroseptal (AS), anterior (A), anterolateral (AL), posterolateral (PL), posterior (P), and posteroseptal (PS) walls. The model was defined in a Cartesian coordinate system (X, Y and Z).
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Statistical Analysis
Statistical analysis was carried out using SPSS software (SPSS, Chicago, Illinois). Hemodynamic parameters and ventricular dimensions were compared using a paired Student t test. Regional strain values were compared using analysis of variance with post-hoc testing using Fisher's least significant difference test. In all cases a p value less than 0.05 was considered significant.
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Results
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Hemodynamic Measurements
As expected in patients with severe AI, diastolic blood pressure significantly increased after surgery from 66.9 ± 9.8 mm Hg to 82.7 ± 8.9 mm Hg (p < 0.002). There was no significant difference in systolic blood pressure (p = 0.11) or in heart rate (p = 0.39) before and after surgery. Compared with control group, the AI patients had significantly higher preoperative systolic blood pressure (135.5 ± 20.8 mm Hg versus 121.5 ± 13.5 mm Hg, p = 0.04) and postoperative diastolic blood pressure (82.7 ± 8.9 mm Hg versus 72.2 ± 10.7 mm Hg, p = 0.002). All other hemodynamic parameters were not significantly different between the two groups.
Left Ventricular Measurements
Preoperatively, patients with AI had an average echocardiographic ejection fraction of 54.1% ± 8.4% and an average left ventricular end-diastolic diameter of 6.6 ± 1.0 cm. Preoperative MRI-obtained end-systolic and end-diastolic diameters were 4.1 ± 0.7 cm and 6.0 ± 0.6 cm, respectively. Ejection fraction was also calculated for the AI patients using MRI-obtained end-diastolic and end-systolic volumes. Preoperatively, the AI patients had an average ejection fraction of 56.0% ± 7.0%, which was not significantly different than preoperative echo values (p = 0.54). As expected, left ventricle size decreased significantly after surgery. End-systolic and end-diastolic diameters decreased to 3.0 ± 0.6 cm and 4.5 ± 0.7 cm postoperatively (p < 0.0001 for both). The MRI-generated end-diastolic volume decreased from 200 ± 77 mL preoperatively to 90 ± 33 mL postoperatively (p < 0.0001). In addition, a nonsignificant increase in the MRI-generated ejection fraction to 60.7% ± 7.6% (p = 0.09) was seen after surgery.
Left Ventricular Strain Analysis
Left ventricular strain determinations in 42 normal volunteers demonstrated consistent and uniform values with reasonably tight standard deviations as demonstrated in Figure 5. There were no differences in minimum principal strain (e
3) between men and women. There was no difference in average e
3 values when preoperative AI patients were compared (regionally or globally) with normal control subjects (Fig 5). When postoperative e
3 was compared with preoperative values, a significant decrease in e
3 is clearly evident in all but one region (p 
0.036) and in the global average of all six regions (p = 0.005). Furthermore, postoperative values are significantly reduced in all regions (p 0.032) and globally (p < 0.001) when compared with normal control group values (Fig 5). Similar findings were seen with longitudinal (e
ll) strain (Fig 6). There was no difference in e
ll between the control subjects and preoperative AI patients but there was significant differences (p 0.003) between normal and AI patients postoperatively in all regions and globally. Additionally, there were significant differences (p 0.028) in circumferential strain (e
cc) between control subjects and AI patients postoperatively in four regions and globally (Fig 7). There were no significant differences between any of the groups in radial strain (e
rr). There was no significant difference in e
3 between the AI patients that were asymptomatic versus those with symptoms, either preoperatively or postoperatively. Neither preoperative nor postoperative global strain values were predictive of postoperative ejection fraction, end-diastolic diameter, or left ventricle volume.
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Fig 5. Left ventricular minimum principal strain (e
3
). The e
3
was not significantly different from normal control group values, in any region or globally, before surgical intervention in the cohort of chronic aortic insufficiency (AI) patients referred for aortic valve replacement. Postoperatively, however, average left ventricle e
3
reduced to levels below the normal control group values uniformly in all regions and globally. *p < 0.05 versus normal.  p < 0.05 versus AI preoperative. (Solid bars = normal; striped bars = AI preoperative; open bars = AI postoperative; Ant = anterior; Lat = lateral; Post = posterior; Sept = septal.)
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Fig 6. Left ventricular longitudinal strain (e
ll
). Postoperatively, e
ll
was significantly decreased in all regions and globally compared with normal subjects. Also, e
ll
was significantly decreased in three regions and globally compared with preoperative values. *p < 0.05 versus normal. p < 0.05 versus aortic insufficiency (AI) preoperative. (Solid bars = normal; striped bars = AI preoperative; open bars = AI postoperative; Ant = anterior; Lat = lateral; Post = posterior; Sept = septal.)
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Fig 7. Left ventricular circumferential strain (e
cc
). Global postoperative e
cc
was significantly decreased compared with both normal subjects and aortic insufficiency (AI) patients' preoperative global e
cc
values. Regional comparison reveals signicantly decreased postoperative e
cc
in two regions versus preoperative values and in four regions versus normal subjects. *p < 0.05 versus normal. p < 0.05 versus AI preoperative. (Solid bars = normal; striped bars = AI preoperative; open bars = AI postoperative; Ant = anterior; Lat = lateral; Post = posterior; Sept = septal.)
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Comment
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Criteria for referral for aortic valve replacement in symptomatic patients with chronic AI are well established and accepted by clinicians [12]. The timing of aortic valve replacement in asymptomatic or minimally symptomatic patients, however, continues to present a clinical challenge [13]. A consistently accurate, objective, clinically applicable measure of myocardial function that is sensitive enough to detect the early onset of myocardial injury, before the establishment of significant irreversible damage, is a prerequisite for the accurate determination of the timing of surgical intervention. Highly accurate strain indices based upon MRI-generated geometry datasets have clear potential in this regard. Before they can be tested as to their utility in heralding the onset of irreversible injury of the myocardium, however, their ability to detect incrementally small changes in ventricular function and their direct applicability to the clinical setting must be confirmed. It is exactly this confirmation that we sought in this investigation.
Currently, numerous modalities are used to assess myocardial function in patients with aortic insufficiency. Transthoracic and transesophageal echocardiography, contrast radiographic ventriculography, and radionuclide ventriculography are currently the clinical standards for evaluation of patients with valvular heart disease [14]. The well-established advantages of echocardiography include its ease of clinical application, as well as its speed, availability, and minimal expense in most clinical settings. Nonetheless, it shares many disadvantages with the other modalities including its relative dependence upon operator skill, subjectivity of its interpretation, limited visualization of regional cardiac anatomy in some patient populations, as well as the qualitative nature of many of its observations. In addition, strain measurements using Doppler echocardiography are dependent on the direction of the Doppler angle of incidence in relation to the direction of myocardial motion [15], thus making precise measurements of strain more difficult.
It is in this setting that the findings of this study gain physiological significance with possible clinical implications. In a cohort of AI patients referred for surgical intervention, we have demonstrated the clinical application of an accurate index of myocardial function that nearly uniformly is impaired at an average of more than 2 years after aortic valve replacement for AI. This sensitive, regionally accurate index is the result of the clinical application of advanced mathematical modeling and analysis of the computer-assisted, intramural three-dimensional tracking of ventricular wall movement by MRI utilizing radiofrequency tissue-tagging. The mathematical description of the tag-line displacement information obtained from this relatively easily applied clinical tool can be transformed by a polynomial fitting, developed in our laboratory, into highly accurate, fully three-dimensional, nonlinear strain maps of the ventricular myocardium. Strain is a nondimensional quantity that is the measurement of the deformation of an object that is not dependent on visual analysis of wall thickening and motion. Strain gives a quantitative analysis of myocardial function that is not affected by cardiac motion and rotation or the function of adjacent segments. This property is particularly useful in the postsurgical patient where pericardial adhesions and paradoxical septal motion are common. The result of the application of these advanced methodologies, therefore, is the construction and clinical utilization of a new mathematical tool that enables the accurate regional and transmural assessment of myocardial fiber contractile function.
The data presented demonstrate a consistent and significant decrease in systolic circumferential, longitudinal, and minimum principal strain after aortic valve replacement for chronic severe AI. There was no significant difference in radial strains between the three groups. This finding is likely secondary to greater variability in e
rr measurements due to a lack of data points across the myocardium in the radial direction. Other investigators have likewise shown that e
rr obtained from MRI tissue-tagging techniques is less reliable than e
3, e
cc, and e
ll [16]. Given that symptomatic patients with severe AI often have a suboptimal response to surgery, it is not surprising that these patients had postoperative myocardial abnormalities. However, similar results were seen when the patients were asymptomatic. This decrement in strain is documented at 2 years after surgical intervention. Any transient effects on strain associated with the surgical procedure itself would quite reasonably be expected to have resolved at this postoperative interval. In a similar fashion, any anticipated reversal of the chronic AI remodeling process has most likely occurred at this moderate follow-up interval. We can, therefore, predict that this decrement in this patient subgroup will most likely not further improve. Whether it is a harbinger of a progressive decline in selected patients deserves further follow-up investigation.
One possible explanation for the consistent, uniformly documented reduction in minimum principal strain is an increase in ventricular afterload caused by the valve prosthesis. The consistent reduction in ventricular volume and left ventricle mass after aortic valve replacement, as well as a previously documented decrease in left ventricle end-systolic stress [17], suggests that a significant increase in afterload did not occur. Also, follow-up echocardiograms in 6 of our AI patients revealed no evidence of stenosis, patient-prosthesis mismatch, or regurgitation. In addition, the low gradients documented across the currently utilized mechanical and bioprosthetic valves—and certainly documented after the Ross procedure—do not support this hypothesis. Studies of hemodynamic performance after the Ross procedure by da Costa and colleagues [18] support the absence of significant transvalvular gradient. Another possible explanation for the consistent reduction in systolic strain seen in our patient population is the presence of myocardial fibrosis from the chronic effects of left ventricle volume overload and the associated remodeling process. Strain abnormalities have been seen in other myocardial disease processes that involve the development of myocardial fibrosis, such as myocardial infarction and hypertrophic cardiomyopathy [3, 4]. In addition, biopsy studies have shown that patients with chronic aortic insufficiency undergoing aortic valve replacement have shown increased myocardial fibrosis [19, 20]. Animal studies have shown that the fibrosis precedes the development of congestive heart failure and is greater after the development of congestive heart failure [21]. Further investigation will be needed to assess whether progressive myocardial fibrosis coincides with a reduction in systolic strain at various stages of disease progression.
We encountered several limitations in the performance of this study, including the inclusion of data from a large midventricular slab in the geometrical data-set, thereby not fully utilizing information from the base and distal apex of the left ventricle. The advantage of this approach is the semiautomatic nature of the strain analysis that could be performed, thereby limiting investigator bias. Efforts are currently under way to allow for automated strain model construction of the entire ventricle. Other criticisms of cardiac MRI in general include the long scan time and the difficult breath holds required for scan data acquisition. In our experience, however, even patients with significant cardiac disease usually tolerate the procedures well. Furthermore, with advances in MRI technology, such as real time MRI, the scans would become increasingly quicker and hence more adaptable to sicker patients [22, 23]. Finally, while this study clearly demonstrates a significant decrease in systolic strain at an average of 2 years after aortic valve replacement, it lacks a true longitudinal clinical comparison of strain values over a more complete spectrum of AI patients. We are currently targeting patients who are earlier in the natural history of this disease process in an attempt to more accurately define the natural history of strain in patients with severe AI.
The clinical implementation of strain indices in this study demonstrates the ease of application of these methodologies. It also clearly establishes that consistent and uniform strain data can be obtained in both normal volunteers and patients with chronic aortic insufficiency before and after surgical intervention. Our results also suggest that advanced MRI-based strain methodologies may be capable of a new level of sensitivity in the assessment of regional ventricular function that may be applicable to any number of patient subsets, including patients with valvular, ischemic, or cardiomyopathic processes.
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Acknowledgments
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We would like to thank Richard Scheussler, PhD, for his assistance with the statistical analysis and Glenn Foster, RRT, Rich Nagel, RRT, and Marci Bailey, RN, for their assistance in acquiring the data used in this manuscript. This work was supported by NIH Grant RO1 HL64869.
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Top
Abstract
Introduction
