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Circulation: Cardiovascular Imaging. 2008;1:141-147
Published online before print July 30, 2008, doi: 10.1161/CIRCIMAGING.108.783795
CLINICAL PERSPECTIVE
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Original Articles

Functional Analysis of the Components of the Right Ventricle in the Setting of Tetralogy of Fallot

Narendra K. Bodhey, MD, DNB; Philipp Beerbaum, MD; Samir Sarikouch, MD; Siegfried Kropf, PhD; Peter Lange, MD; Felix Berger, MD; Robert H. Anderson, MD, PhD, DSc, BS, FRCPath and Titus Kuehne, MD

From the Department of Congenital Heart Disease and Paediatric Cardiology (N.K.B., P.L., F.B., T.K.), Deutsches Herzzentrum Berlin, Berlin, Germany; Department of Imaging Sciences (P.B.), King’s College London, London, United Kingdom; Department of Heart- Thorax- and Transplantation Medicine (S.S.), Medical University Hannover, Hannover, Germany; Institute of Biostatistics (S.K.), University of Magdeburg, Magdeburg, Germany; Institute of Child Health (R.H.A.), Cardiac Unit, University College London, London, United Kingdom.

Correspondence to Titus Kuehne, MD, Department of Congenital Heart Disease and Pediatric Cardiology, Deutsches Herzzentrum Berlin, Berlin, Germany. E-mail kuehne{at}dhzb.de

Received April 2, 2008; accepted July 22, 2008.


    Abstract
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
Background— Anatomic and functional observations suggest that the right ventricle (RV) can be analyzed in terms of its inlet, apical trabecular, and outlet components. Our study was designed to evaluate the regional adaptation of these components to different conditions of loading, with additional analysis of the surgical techniques used for primary repair.

Methods and Results— We studied prospectively 45 patients with tetralogy of Fallot (age, 20.5±8.1 years) and 24 control subjects (age, 20.1±5.8 years). All subjects were studied by using cardiac MRI. End-diastolic (EDV), end-systolic (ESV), stroke volumes (SV), and ejection fraction (EF) were determined for the overall RV and separately for its inlet, apical trabecular, and outlet components. The patients had pulmonary regurgitant fractions of 33.2±11.1%, and RV peak-systolic pressures of 40.7±16.1 mm Hg. In controls, the apical trabecular component EDV was 51.5±11.1 mL/m2 (54.3±6.8% of the total RV EDV), ESV was 19.2±6.3 mL/m2 (47.6±10.5% of RV ESV), and SV was 32.3±6.9 mL/m2 (58.9±6.6% of RV SV), resulting in an EF of 63.1±7.7%. When considering all patients, the apical trabecular component took up the greatest part of the overload, having an EDV of 76.5±18.1 mL/m2, and an ESV of 31.6±12.8 mL/m2, reflecting an increase of 49 and 67% over controls, respectively (P<0.001). EF was 59.7±10.7%, and was maintained at control levels (P=0.132). In controls, the outlet had considerable ejecting force, with an EF of 54.8±9.1%, whereas it was decreased in the patients with tetralogy (EF=28.5±11.9%). There was significant increase of ESV (P<0.001), but not of EDV, with EF decreased by 45% (P<0.001). The inlet was not significantly affected by overload. The surgical technique did not significantly affect any measured parameter for any component.

Conclusions— In patients with tetralogy of Fallot, subsequent to surgical correction, the individual components of the RV respond in characteristic fashion to RV overload.

Key Words: magentic resonance imaging • tetralogy of Fallot • heart defects, congenital


    Introduction
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
In the light of the favorable outcomes now expected after surgical correction, recent work, often involving patients with tetralogy of Fallot, has begun to show the functional significance of the right ventricle (RV).1–5 Despite the success of surgical correction, many patients postoperatively experience progressive RV enlargement, or ventricular dysfunction, as a result of varying degrees of regurgitation or obstruction across the reconstructed subpulmonary outflow tract.6,7 It is now accepted that such patients should be followed with great care. The adaptive response of the RV to chronic overload, however, remains incompletely understood. In particular, provision of reliable cutoff points for timing of reintervention, notably with regard to replacement of the pulmonary valve, remains challenging.8,9

Clinical Perspective p 147

In the majority of studies conducted thus far, the RV has been analyzed as an entity, or else regional findings have been extrapolated to provide global analysis of function.1–4,7–9 There is evidence, nonetheless, that the functional parameters of the global RV do not necessarily reflect the true picture of this complex cardiac chamber. Both anatomic and functional observations suggest that the chamber, functioning as the pump to the pulmonary circulation, can best be considered to possess inlet and outlet components, with a third component, the apical trabecular part, providing the driving force.10 With this concept of tripartite ventricular composition in mind, we designed this study to establish the relative contributions of these component parts to global ventricular function, comparing findings in healthy volunteers to patients who had undergone surgical correction of tetralogy of Fallot.


    Methods
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
Patients
During the year 2007, we performed magnetic resonance imaging (MRI) prospectively in 45 patients (21 males and 24 females) with tetralogy of Fallot, comparing the findings in 24 age-matched healthy controls (11 males and 13 females), all of them being of Caucasian origin. To minimize age-dependent variations in ventricular size, we studied only youths and young adults. Other criteria for inclusion were clinical state, the substrate for ventricular overload, and the type of, and age at, primary corrective surgery.

For analysis of cofactors that influence RV function, we divided the patients according to the conditions of overload, comparing overload produced by volume in isolation with loading produced by combined pressure and volume. Peak-systolic pressures in the RV were estimated with Doppler echocardiography, quantifying pulmonary regurgitation, and ventricular volumes with MRI.

Isolated Volume Overload
Patients in this group had pulmonary regurgitant fractions of >35% and peak-systolic pressures in the RV of <30 mm Hg, or a pressure gradient across the RV outflow tract of <15 mm Hg.

Combined Pressure and Volume Overload
Patients forming this group had regurgitant fractions ranging between 20% and 25%, peak-systolic RV pressures of >45 mm Hg, or a pressure gradient across the RV outflow tract of >30 mm Hg.

We also segregated the patients on the basis of the surgical procedure performed during the initial operation, comparing those undergoing primary relief of the obstructed RV outflow tract with or without insertion of a patch across the infundibulo-arterial junction. Their hemodynamic data are shown in Table 1. Patients with large aneurysms of the RV outflow tract were not included in our study.


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Table 1. Baseline Characteristics
 
We also analyzed, as a separate group, those patients in whom recent investigations provided indications for replacement of the pulmonary valve.8,9

Indications for Replacement of the pulmonary Valve
The decision for reintervention was based, among other considerations, on an increased end-diastolic volume (EDV) (namely >150 mL/m2 of the total RV volume8) in conjunction with recognized impairment of the physical capacity for work. Reintervention included replacement of the pulmonary valve either surgically or by transcatheter implantation of a valved pulmonary stent. All subjects studied gave informed consent.

Protocol for MRI
Studies were performed on a 1.5-T system (Intera, Philips Medical Systems, Best, The Netherlands) using a cardiac surface array coil. Volumetric analysis of the ventricles was done with multislice, multiphase steady-state free precision MRI in an axial plane. Imaging was performed in an axial plane to permit better recognition of the anatomic landmarks required to segregate the RV compartments.11 We used sequence parameters of 6 mm slice thickness, with the values set at gap=–0.5 mm; TR/TE=shortest; matrix 160 to 256x140 to 212 mm; field of view 280 to 400x220 to 320 mm (approximate in plane resolution of 1.4x1.4x6 mm); 35 phases per cardiac cycle. Pulmonary regurgitant fraction was measured using through-plane velocity-encoded images. Sequence parameters were TR/TE=5.1/3.0 ms; flip angle of 15° encoding velocity of 200 cm/s.

General Analysis
Postacquisition analysis was performed with the software View Forum (release 6.1, Philips Medical Systems, Best, The Netherlands). We computed volumes of the left ventricle, the RV, and then the component parts of the RV. For the RV, this was achieved by tracing the endocardial borders of the ventricles, along with those of the component parts, measuring both EDV and end-systolic volume (ESV). Stroke volume (SV) was calculated as the difference between the diastolic and systolic volumes. Ejection fraction (EF), expressed as a percentage, was calculated as the ratio of SV to EDV. The volumes were indexed by dividing them with the body surface area. Pulmonary flow and regurgitation fraction were measured as described elsewhere.12

Analysis of the RV Components
We used anatomic landmarks to trace the boundaries of the inlet, apical trabecular, and outlet portions of the RV (Figure 1).10 The inlet component was deemed to extend from the atrioventricular junction to the attachments of the tension apparatus of the tricuspid valve, with the apical trabecular component extending beyond the attachments of the tricuspid valvar tension apparatus to the mouth of the outlet part. The outlet part was then considered to extend from this distal border of the apical part to the attachments of the leaflets of the pulmonary valve.


Figure 1783795
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Figure 1. Representative cine MR images (upper panel) showing the anatomic landmarks as used for distinction of the components of the RV. The components are then illustrated in a three-dimensional reconstruction of the tomographic MR images (lower panel, seen in a front view, left and back view, right). TA indicates tension apparatus of the tricuspid valve; CT, coarse trabeculation; AJ, upper rim of the atrioventricular junction; PA, attachment of pulmonary valvar leaflets. 1=inlet, 2=apical trabecular; 3=outlet component.

 
Statistical Analysis
We compared EDV, ESV, SV and the EF between controls and patients, as well as for the defined subgroups of patients. Significance levels were first evaluated using global ANOVA and post hoc test (LSD and Tukey’s HSD) for all groups and pair-wise comparison of subgroups. Patients and probands have been matched for sex and age at a group level, so that both groups have similar percentages of males and females and similar distributions of age. A probability value of <0.05 was considered as significant. Correlation after Pearson and canonical correlation was determined for volumetric MRI measurements, pulmonary regurgitant fraction, and RV peak-systolic pressures. All MRI data were analyzed by 2 independent observers. From these 2 measurements per patient or proband, the coefficient of variation (quotient of standard deviation and mean) has been computed, and the median over the groups has been determined together with 95% confidence intervals.


    Results
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
All patients and control subjects showed good compliance during MRI. Our patients and their age-matched controls ranged in age from 15 to 36 years and 16 to 35 years, respectively. All patients had undergone primary correction in their early childhood and at the time of the study were classified in New York Heart Association class I or II. None had additional congenital cardiac malformations, ischemic heart disease, or arrhythmias. All patients who participated in the study had mild tricuspid valvar insufficiency. Their baseline characteristics are given in Table 1.

According to the findings, we placed 23 patients in the group having isolated volume overload, and 22 in the group with combined pressure and volume overload. For surgical correction, 17 patients had undergone an infundibulectomy alone, whereas an additional patch was inserted across the infundibulo-arterial junction in 28 (Table 1). Replacement of the pulmonary valve, either surgically or by transcatheter implantation of a valved pulmonary stent, was considered desirable in 11 patients.8

Analysis of the Right and Left Ventricular Volumes
All patients showed significant increases in EDV and ESVs of the RV, along with the SV (P<0.01), and EFs decreased slightly but significantly (P<0.05). The functional parameters for the left ventricle were at control levels.

Analysis of the RV Components
Inlet Portion
In the control subjects, the inlet portion accounted for 19.5±5.1% of the end-diastolic RV volume. With an EF of 47.2±6.1%, it provided 16±5.1% of the ejected RV volume (Table 2). In the patients, the inlet was the least affected of the 3 RV components, with no significant change found either in volumes or in EF when compared with controls (Table 2 and Figure 2). We found no significant correlations for any measured parameter between the inlet and the global RV or with the outlet or apical trabecular components.


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Table 2. Parameters of Function of the Component Parts of the Right Ventricle
 

Figure 2783795
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Figure 2. The graph illustrates mean differences of parameters between patients and controls, expressed as percentage with respect to the mean of controls. The whiskers display 95% confidence intervals calculated according to Fieller’s theorem. EDV indicates end-diastolic volume; ESV, end-systolic volume; SV, stroke volume; EF, ejection fraction.

 
Apical Trabecular Portion
The apical trabecular portion in the control subjects accounted for the largest volume, and provided the greatest ejectile momentum (Table 2). With an EDV of 51.5±11.1 mL/m2, it accounted for 54.3±6.8% of the total RV EDV (86.6±7.2 mL/m2). Driven by an EF of 63.1±7.7%, it provided 58.9±6.6% of the ventricular total SV. In normal subjects, the EF of this portion was significantly higher than the inlet and the outlet portions (P<0.01). In the patients, this component took up most of the volume load on the RV. In turn, the EDV (76.5±18.1 mL/m2) increased significantly to 64±6.7% of the total RV EDV (121.0±25.3 mL/m2; P<0.01), reflecting a proportional increase of 49% compared with control values (Figure 2). Because both EDV and ESVs augmented to similar levels, the EF was not reduced significantly. We found a close correlation between the apical trabecular component and the global RV in terms of EDV and ESVs, and also for EF (r2=0.78, r2=0.71, r2=0.69, respectively).

Outlet Portion
The parameters for the outlet component in the control subjects were similar to those of the inlet portion, with the outlet accounting for 26.3±6% of the RV EDV. With an EF of 54.8±9.1%, the outlet provided 25.1±7.1% of the ejected volume (Table 2). Significant changes were observed in the patients. Notably, although EDV did not increase significantly, ESV increased by 69% compared with control values (Table 2 and Figure 2). In turn, there was a significant decrease in EF (to 28.5±11.9%), representing a decrease of 48% compared with control values. We found no correlation, however, between the changes observed in the outlet and the overall RV or its inlet or apical trabecular components.

Analysis of Subgroups
Overload Produced by Volume Compared With Combined Pressure and Volume
As expected, the patients with overload produced exclusively by volume had larger global RV volumes (P<0.01) with only slightly but significantly reduced ejections fractions (P=0.045). In these patients, there was significantly larger volume for both the apical trabecular and outlet components when compared with the total group of patients (P<0.05), in conjunction with maintenance of the EF (Table 2). In contrast, in the patients with pressure overload due to obstruction of the outlet, there was a marked decrease in EF for the outlet but unchanged fractions for the apical trabecular and inlet components. The overall RV EF, therefore, was only slightly reduced (Tables 2 and 3Go).


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Table 3. Parameters of Function of the Left and Right Ventricles Analyzed in Their Entirety
 
Patients With Indications for Replacement of Pulmonary Valves
The variables for these patients are summarized in Table 4. Of the 11 patients, 6 had an isolated volume load, and 5 an overload produced by the combination of pressure and volume. Compared with the other patients, the degree of pulmonary regurgitant fraction was slightly but significantly larger (Table 4). This subgroup of patients had, by definition, substantially enlarged RV volumes. Even in this setting, the increase in volume took place primarily in the apical trabecular compartment.


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Table 4. Comparison of Patients With and Without Indication for Pulmonary Valve Replacement
 
Patch Versus No Patch
The type of surgery had no statistically significant effect on any measured parameter for any of the RV components. There was no significant correlation between the fraction of pulmonary regurgitation or RV peak-systolic pressures and the type of surgery.

Interobserver Variability
Data of interobserver variability is shown as percentages, with the confidence intervals included in parentheses. Measurements for the global RV indexed to body surface area were for RV EDVs 5.4% (4.8 to 6.7). Computations of the RV components for the outlet were 5.6% (4.2 to 6.8); for the inlet, 6.4% (5.6 to 8.3); and for the trabecular component, 7.1% (5.8 to 8.8).


    Discussion
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
The tripartite approach for the analysis of the morphologically RV in terms of its inlet, apical trabecular, and outlet components has great utility in the study of congenitally malformed hearts with univentricular atrioventricular connections, because analysis in terms only of the "sinus" and "conus" does not permit recognition and appropriate description of those ventricles lacking only their inlet components.10,13,14 Our study now provides evidence that such tripartite analysis is also of value in the setting of hearts with biventricular atrioventricular connections, because the 3 components of the morphological RV show variable adaptive responses to overload produced by volume in isolation as opposed to pressure combined with volume. As might be expected, the apical trabecular component provides the major ejectile momentum of the ventricle, this function being maintained in patients with slight-to-moderate ventricular dysfunction. The apical component, however, also takes up the greater part of a volume load as a response to pulmonary regurgitation or RV pressure load. The outlet part, in contrast, shows a consistently and markedly decreased EF that does not seem to be part of a true adaptive response to chronic RV overload. Furthermore, the inlet component is also limited in its response to overload. These adaptive responses showed no correlation with the techniques used for surgical correction.

As did Lytrivi et al,15 we observed significant ejectile forces provided by the outlet components of our healthy controls. The EF of the outlet, however, was significantly reduced in all our patients, irrespective of the nature of the overload they experienced, or the surgical technique used for correction. It was an exaggerated ESV that reduced the EF, because the EDV remained at control levels, and this was relatively consistent for all the patients. Only in the patients with combined pressure and volume overload did we find slight diminutions of the EF, along with the end-diastolic volumes. This observation might reflect diminished diastolic compliance in the obstructed RV outflow tract compared to the patients with isolated volume load. Lytrivi et al included patients with wide-ranging ages in their study.15 The consistency of our observations with theirs, therefore, suggests that there is only limited impact of age, as well as of the degree or kind of overload. We can presume that the outlet, in contrast to the apical trabecular portion, does not take part in the adaptive response of the RV. Changes of the outlet seem to be predetermined by postsurgical scarring, which induces reduced contractile function, as manifested by the increased ESV, as well as mitigating dilation of the outlet part, shown by the retained EDV. This point of view would be in concordance with the findings of Oosterhof at al.16, who observed the presence of fibroses in conjunction with enlarged diameters of the right ventricular outflow tract. When interpreting our findings it should be noted that, before surgical correction, part of the subaortic outlet arises from the morphologically RV, albeit that this is given to the morphologically left ventricle after the surgical procedure. The combination of tissue affiliation, fibrosis and dilation, particularly during systoly, might be one of the factors that exaggerate the role of the outlet as a source of malignant arrhythmias.17

Clinical Implication of the Study
Clear cutoff values for replacement of the pulmonary valve have still not been defined. Some investigators have noted that the RV fails to normalize in terms of size after corrective surgery when its EDV exceeded cutoff values of 150 mL/m2, or 170 mL/m2, respectively.8,9 Oosterhof et al18 noted substantial decrease of RV size postoperatively in RV that were dilated to an even greater extent. In our study, we found that the volumes of the inlet and outlet components, unlike those of the apical trabecular component, were not substantially affected by the conditions and extent of loading. The proportional enlargement of the apical trabecular component, therefore, is much greater than that of the entire RV. These differences in distension might be explained, in addition to consideration of postsurgical scarring, by the simple fact that the inlet and outlet parts have a narrow geometric configuration. Because of this, when applying the law of Laplace, they are less affected by mural stress than the apical trabecular portion. It may be significant, however, that no patients with major tricuspid insufficiency were included in our study. In such patients, distension of the tricuspid valvar annulus might potentially enlarge the volumes of the inlet components.19 We speculate, therefore, that the assessment of the apical trabecular component, with its pronounced changes in size, might be of value in the follow-up of patients. Our study has shown unequivocally that it is the apical trabecular component that provides the major driving force of the RV, accounting for three fifths of this force in the control subjects. This contribution was accentuated in the face of loading, with the prorated systolic volume produced by the apical part increasing to three-quarters, whereas that generated by the inlet and outlet parts was even slightly diminished. The workload, though not directly measured in our study, is thought to be augmented considerably in the apical trabecular component. This should be kept in mind when defining new cutoff values for pulmonary valvar replacement, or other reintervention involving the RV.

Implication of the Imaging Technique Beyond Tetralogy of Fallot
Our method relied only on the specific anatomic landmarks seen reproducibly in the MR images and therefore yielded reasonably low variations among different observers. Besides evaluating the differential function of the component parts of the RV in patients with tetralogy of Fallot, the technique might be applied more universally. This would include questions devolving on RV function in general, no matter if in acquired or congenital cardiac diseases. In addition, the technique could be applied in a variety of patients with more complex congenitally malformed hearts. Meaningful studies might be performed of the dominant left ventricle in double inlet left ventricle, which has 2 inlets, as opposed to the dominant left ventricle in tricuspid atresia. Similar considerations relate to double outlet RV, and so on.

Limitation of the Study
To avoid large bias in the data, we compared findings in healthy volunteers with those from patients with tetralogy of Fallot, keeping the criteria for inclusion restrictive in terms of age, degrees of loading, functional performance, and presence of tricuspid valvar insufficiency, as well as taking note of the current clinical state of the patients. Because of these tight criteria for selection, we failed to account for several additional clinical situations, and thus, it is inappropriate to extrapolate further from our results, particularly when defining prognostic indicators. This will require further study. This takes also into account that, in the current study, patients with large aneurysms of the right ventricular outflow tract were not included to avoid the influence of additionally increased end-systolic volumes on the measurements made of the outlet. In addition, patients included in our study had undergone their surgical corrections about 20 years ago. In the intervening period, surgical techniques have been refined, and corrective surgery is generally performed at an earlier age. This will have an impact, in particular on the function of the outlet component.


    Conclusions
 Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
The method we have used allows accurate assessment of the components of the RV. In the setting of tetralogy of Fallot, these components show a differential response to overload. It is the apical trabecular component that yields the major adaptive response. This compartment, therefore, should be in focus of future studies that seek to provide prognostic criteria for preventing RV failure.


    Acknowledgments
 
We acknowledge the support of I. Wolf, Department of Medical Informatics, Deutsches Krebsforschungszentrum, Heidelberg, Germany.

Sources of Funding

This work was supported by the Kompetenznetz Angeborene Herzfehler (Competence Network for Congenital Heart Defects) funded by the Federal Ministry of Education and Research (BMBF), FKZ 01G10210. Dr N.K. Bodhey, Department of Imaging Sciences and Interventional Radiology, Sree Chitra Tirunal Institute of Science and Technology, Trivandrum, was funded by the Ministry of Science and Technology, Government of India.

Disclosures

None.


    References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusions
 References
 
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CLINICAL PERSPECTIVE

Predicting the transition from compensated to irreversible and decompensated insufficiency of the right ventricle in the clinical setting is complicated by its complex morphology and function. In turn, reliable timing of catheter-based or surgical reintervention in the setting of Tetralogy of Fallot, or other pathologies involving the right ventricle, remains challenging. Assessment of the "total" right ventricle by MRI provides valuable information that supports medical decision making by defining cutoff values for global right ventricular volumes. However, from a functional and morphological perspective, the right ventricle should not be analyzed as a single entity. Initial clinical studies identified the right ventricular outlet as a major source of arrhythmias. In our study we observed an important role for the apical trabecular component. In healthy individuals, this component provides the major ventricular contractile force. In the pressure and/or volume loaded right ventricle, this compartment takes up by far the greater part of the adaptive response. In contrast, the inlet, along with the outlet, responds substantially less in functional terms to loading. This specific adaptive response concentrates the augmented ventricular workload to the apical trabecular region. This observation might have significant clinical importance, because attention to specific assessment of the apical trabecular component might better demonstrate the initial signs of ventricular insufficiency, rather than evaluating the right ventricle as a global entity. Imaging the ventricle with magnetic resonance allowed for reproducible assessment of the individual right ventricular compartments, and therefore appears suited for use in the clinical context.




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A. J. Teske, N. H. Prakken, B. W. De Boeck, B. K. Velthuis, E. P. Martens, P. A. Doevendans, and M. J. Cramer
Echocardiographic tissue deformation imaging of right ventricular systolic function in endurance athletes
Eur. Heart J., April 2, 2009; 30(8): 969 - 977.
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