DOI: 10.1002/pd.4461
ORIGINAL ARTICLE
Speckle tracking echocardiography in fetuses diagnosed with congenital diaphragmatic hernia Philip DeKoninck1,2, Jan D’hooge3, Tim Van Mieghem1,2, Jute Richter1,2 and Jan Deprest1,2* 1
Fetal Medicine Unit, Department of Obstetrics and Gynecology, University Hospitals Leuven, Leuven, Belgium Cluster Organ Systems, Department of Development and Regeneration, KU Leuven, Leuven, Belgium 3 Laboratory for Cardiovascular Imaging and Dynamics, Department of Cardiovascular Sciences, KU Leuven, Leuven, Belgium *Correspondence to: Jan Deprest. E-mail: [email protected] 2
ABSTRACT Objective The aim of this study is to evaluate cardiac function in fetuses with congenital diaphragmatic hernia (CDH) using speckle tracking. Method Case-control study assessed cardiac contractility in consecutive fetuses with CDH. Controls were anatomically normal fetuses, adjusted for gestational age. Speckle tracking software calculated ventricular peak longitudinal velocity, displacement and strain. Pulmonary hypoplasia was assessed using observed/expected lung-to-head ratio (O/E LHR).
Results Thirty-eight fetuses with CDH (29 left and nine right) were evaluated at a mean gestational age of 26.9 ± 2.5 weeks. In six fetuses, the acquired images were of insufficient quality (feasibility 83%). Velocity and displacement showed regional differences, as well as significant differences between the ventricular walls, similar to control fetuses. Strain measurements also demonstrated regional differences yet less uniformly arranged. In left CDH, we observed increased strain values in the left ventricle compared with controls ( 18.7 ± 7.2 vs 15.1 ± 4.9). There was no correlation between strain values in the left ventricle and O/E LHR. In fetuses with right CDH, deformation analysis was not different from controls.
Conclusions In fetuses with CDH, no cardiac dysfunction could be detected despite the often concurrent hypoplasia of ipsilateral cardiac structures. In fetuses with left CDH, the decrease in ventricular size coincides with increased strain values in the free left ventricular wall. © 2014 John Wiley & Sons, Ltd.
Funding sources: This work has been supported by the Fonds voor Wetenschappelijk Onderzoek Vlaanderen (1.8.012.07.N.02; J. D. P.), the Instituut voor Wetenschap en Technologie (IWT/070715), the European Commission (Industria-Academia Partnership via www.endovv.com; PIAP-GA-2009-251356; P. D. K. and J. R.) and the Klinische onderzoeks- en opleidingsraad fonds of the University Hospitals Leuven (T. V. M.). Conflicts of interest: None declared
INTRODUCTION Congenital diaphragmatic hernia (CDH) is a rare congenital malformation affecting approximately 1 to 4 per 10 000 live births.1 The condition arises in the embryonic stage when the diaphragm fails to close. Abdominal organs herniate through this defect into the thoracic cavity. This results in mediastinal shift and compromised lung development. At birth, the lungs of these neonates are hypoplastic; that is, they are smaller and have fewer bronchi and alveoli as well as abnormally developed pulmonary vasculature. CDH also has an impact on the size of the ipsilateral cardiac structures.2,3 In fetuses with left-sided CDH (LCDH), which are more frequent and thus better documented, ventricular dimensions are smaller both on prenatal ultrasound3,4 and in autopsy specimens.5 In a recent report, we described similar changes in fetuses with right-sided CDH (RCDH).6 Experimental data in sheep have shown that there is true hypoplasia of the ventricle rather than
Prenatal Diagnosis 2014, 34, 1262–1267
atrophy, as the DNA/protein ratio remains unchanged compared with normal controls.7,8 The underlying etiology resulting in the smaller cardiac size is likely a combination of several factors. Because of the herniated organs, there is compression of the cardiac structures and an altered cardiac axis leading to a distorted orientation between the foramen ovale and inferior caval vein.2,9,10 As a consequence, the venous return from the inferior vena cava is inadequately streamed into the right rather than the left ventricle. In combination with an increased pulmonary vascular resistance and, hence, reduced pulmonary flow, this leads to decreased left ventricular preloading and poorer growth.10 Despite the significant reduction in cardiac size, the functional impact of this ventricular smallness is questionable. Indeed, in most CDH fetuses, biventricular circulation can be achieved after birth, and true aortic coarctation is rare.4
© 2014 John Wiley & Sons, Ltd.
Speckle tracking echocardiography in congenital diaphragmatic hernia
1263
Deformation analysis with speckle tracking or velocity vector imaging (VVI) is a recent method to evaluate the fetal ventricular function. The technique makes use of speckles that are natural acoustic markers present in a 2D ultrasound image. These speckles are equally distributed throughout the myocardium and can be identified by purpose-designed software. Tracking of these markers during the cardiac cycle yields information on tissue movement, thereby generating velocity vectors.11 The acquired vectors allow the determination of myocardial displacement, velocity and deformation (strain and strain rate). The use of speckle tracking in the prenatal period has been shown feasible in healthy fetuses as well as fetuses with pathologic fetal hearts.11–14 We aimed to apply this technology to evaluate cardiac function in fetuses with CDH to document potential implications of this condition of ventricular deformation. Given the abnormal position and morphologic appearance of the heart, we also wanted to evaluate its feasibility.
analyzed in the same way as we described earlier to allow comparison between the two data sets.20 The timing of the onset of the cardiac cycle was defined on the basis of mitral valve opening on a concomitantly generated M-mode tracing of the mitral valve. The endocardium was manually traced for both the left and the right cardiac ventricles on a still frame in mid to end systole. The ventricle was traced starting just below the valve annulus of the atrioventricular valve, over the ventricular free wall to the apex and then returning to the cardiac base over the septum. The software then automatically generates velocity vectors using speckle tracking and border recognition. The accuracy of tracking was subjectively verified, and border delineation with subsequent tracking was repeated when necessary (Figure 1). For each segment (base, mid and apex) of each ventricular wall (left free wall, right wall and septum), we obtained peak longitudinal cardiac velocity, displacement and strain values (Figure 1). The software also provides a so-called global result for each parameter, being the averaged regional values for each ventricular wall. Regarding the septum, we only used the data obtained while analyzing the left ventricle, as both left and right sides of the septum are reflections of the same muscular region. As controls, we used the raw data of measurements in 59 uncomplicated singleton fetuses between 16 and 36 weeks, which were part of an earlier normative study.20
MATERIALS AND METHODS This is a prospective single-center observational study performed at the University Hospitals Leuven. We included consecutive fetuses diagnosed with isolated CDH and confirmed normal karyotype between November 2010 and December 2011. Each fetus was included only once, that is, at first assessment in our unit, before any fetal intervention was performed. Maternal, delivery and neonatal records were reviewed to confirm the isolated character of the defect and to exclude congenital cardiac malformations interfering with fetal cardiac function. Lung size was assessed using the lung-to-head ratio (LHR)15 expressed as a ratio of what is normally expected for that gestational age,16 to obtain a gestational independent measurement (observed/ expected or O/E LHR).17,18 The intrathoracic part of the liver was expressed as a ratio to the thoracic cavity volume (LiTR) as was described previously.19 The prenatal program for in utero management of CDH, including the evaluation of parameters predicting outcome, as well as a randomized trial comparing fetal treatment with expectant management during pregnancy, have been approved by the Ethics Committee of the University Hospitals Leuven.
Cardiac ultrasound All ultrasound images were acquired on a Voluson E8 or 730 Expert ultrasound machine (GE Medical Systems, Kretztechnik, Zipf, Austria), using a curved 4- to 8-MHz linear array volumetric 3D probe. Image settings were optimized as previously described: speckle reduction imaging was turned off, and the contrast and gain were adapted to clearly visualize the delineation of the ventricular wall.20 All images were acquired at the level of the fetal four-chamber view and with optimal magnification to include only the fetal heart. Image acquisition was performed during a period of fetal inactivity. For each fetus, a cine-loop sequence including at least three complete cardiac cycles was obtained and stored for offline analysis. Images were stored in digital imaging and communications in medicine (DICOM) format and were exported to an external workstation for processing, using purposely designed software (Siemens VVI, version 3.0.0.428, Erlangen, Germany). The images were Prenatal Diagnosis 2014, 34, 1262–1267
Statistical analysis Data were analyzed with Prism for Mac version 6.0b (GraphPad Software, San Diego, CA, USA). Continuous data were expressed as means and standard deviation or median and interquartile range if appropriate. The data from fetuses with RCDH and LCDH were analyzed separately. In the CDH groups, we evaluated regional differences within the examined ventricles using a two-way analysis of variance with Bonferroni’s post-hoc test. Subsequently, global ventricular wall (left ventricle, right ventricle and septum) control values were compared with measurements in fetuses with CDH using multivariate analysis of covariance (MANCOVA) testing with gestational age as covariate, followed by simple contrast analysis. We also evaluated the correlation between O/E LHR, LiTR and strain values in the left ventricle in fetuses with LCDH. A p value < 0.05 was considered statistically significant.
RESULTS Thirty-eight consecutive fetuses with CDH were examined with a mean gestational age of 26.9 ± 2.5 weeks (range 20.9–31.6 weeks). In the majority of cases, the defect was located on the left side (n = 29), whereas nine fetuses had an RCDH. Median O/E LHR was 29.0% (21.5–37.5%) and 35.5% (29.4–56.4%) in LCDH and RCDH, respectively. In 79% of the LCDH cases, there was a partial herniation of liver [median LiTR: 9.7% (3.3–15.4%)] into the thorax, and as expected, all cases with RCDH had liver herniation. In six (16%) fetuses (five LCDH and one RCDH), the obtained images were of insufficient quality for further analysis, because of either fetal position or maternal obesity. In the remaining 32 fetuses, all six segments of the ventricle could be adequately tracked. The results for peak longitudinal velocity, displacement and strain measurements are presented in Tables 1 and 2. The © 2014 John Wiley & Sons, Ltd.
P. DeKoninck et al.
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Figure 1 Longitudinal strain waveforms with 2D speckle tracking. Top: left ventricle in LCDH. Bottom: right ventricle in RCDH median fetal heart rate was 143 (136–149) bpm, and the frame rates (FRs) ranged between 38 and 62 Hz (average 44 Hz). This means that about 18 image frames were obtained per cardiac cycle. In fetuses with LCDH, velocity and displacement showed a significant increase from apex to base in all three ventricular walls (Table 1). There were also significant regional differences for strain with higher values in the apex, compared with the mid and basal regions in the left ventricular wall and septum (p < 0.01). Comparing the three ventricular walls, velocity and displacement were significantly higher in the right ventricular wall as compared with the septum and the left free wall, which is similar to observations in controls (p < 0.001). We did not observe significant differences in strain values between the ventricular walls in LCDH. In RCDH cases, we observed a similar increase from apex to base for velocity and displacement values in the right and left ventricular walls. Comparing the separate walls, we only observed higher velocity and displacement measurements in the basal region of the right ventricle compared with the left wall and septum. Strain values were not different between the different ventricular walls. Evaluating the global ventricular function of the ventricular walls using MANCOVA testing with GA as a covariate, we observed significant differences in measurements in the left ventricle and septum in fetuses with LCDH compared with controls (p < 0.0001). Table 2a displays the differences between LCDH and controls. In the left ventricle, the most interesting observation was an increase in strain values in the cases compared with normal controls. Conversely, in the septum, the differences were mainly caused by differences in Prenatal Diagnosis 2014, 34, 1262–1267
myocardial motion (velocity and displacement). In the right ventricle, there were no significant differences from controls. In the RCDH group, there were no significant differences between cases and normal controls; these data are displayed in Table 2b. There was no significant correlation between the pulmonary size, assessed by O/E LHR and liver herniation (LiTR), and the observed strain values in both CDH groups.
DISCUSSION In this study, we evaluated the use of velocity vector imaging in fetuses with isolated CDH. Using this method, we have found no evidence for ventricular dysfunction in these fetuses. As the base of the heart moves toward the apex, velocity and displacement values are normally increasing from the apex to the base.11 In fetuses with CDH, we observed the same regional differences. In LCDH, we observed higher longitudinal strain values in apex compared with the mid and basal regions, which could be the result of an altered distribution of wall stress within the left ventricle due to geometrical changes. Alternatively, higher apical strain values could be measured because of foreshortening that could be more pronounced during abnormal ventricular (out of plane) motion as a result of the hernia. Furthermore, the higher global strain values in the left ventricular free wall, in comparison with normal controls, are most likely the mechanical expression of well-documented anatomical changes. Indeed, in an attempt to maintain normal cardiac output values, a small ventricle will undergo more deformation21 and as such could explain the increased strain values observed in the left ventricular free wall. Nevertheless, © 2014 John Wiley & Sons, Ltd.
0.04
ORIGINAL ARTICLE
Speckle tracking echocardiography in fetuses diagnosed with congenital diaphragmatic hernia Philip DeKoninck1,2, Jan D’hooge3, Tim Van Mieghem1,2, Jute Richter1,2 and Jan Deprest1,2* 1
Fetal Medicine Unit, Department of Obstetrics and Gynecology, University Hospitals Leuven, Leuven, Belgium Cluster Organ Systems, Department of Development and Regeneration, KU Leuven, Leuven, Belgium 3 Laboratory for Cardiovascular Imaging and Dynamics, Department of Cardiovascular Sciences, KU Leuven, Leuven, Belgium *Correspondence to: Jan Deprest. E-mail: [email protected] 2
ABSTRACT Objective The aim of this study is to evaluate cardiac function in fetuses with congenital diaphragmatic hernia (CDH) using speckle tracking. Method Case-control study assessed cardiac contractility in consecutive fetuses with CDH. Controls were anatomically normal fetuses, adjusted for gestational age. Speckle tracking software calculated ventricular peak longitudinal velocity, displacement and strain. Pulmonary hypoplasia was assessed using observed/expected lung-to-head ratio (O/E LHR).
Results Thirty-eight fetuses with CDH (29 left and nine right) were evaluated at a mean gestational age of 26.9 ± 2.5 weeks. In six fetuses, the acquired images were of insufficient quality (feasibility 83%). Velocity and displacement showed regional differences, as well as significant differences between the ventricular walls, similar to control fetuses. Strain measurements also demonstrated regional differences yet less uniformly arranged. In left CDH, we observed increased strain values in the left ventricle compared with controls ( 18.7 ± 7.2 vs 15.1 ± 4.9). There was no correlation between strain values in the left ventricle and O/E LHR. In fetuses with right CDH, deformation analysis was not different from controls.
Conclusions In fetuses with CDH, no cardiac dysfunction could be detected despite the often concurrent hypoplasia of ipsilateral cardiac structures. In fetuses with left CDH, the decrease in ventricular size coincides with increased strain values in the free left ventricular wall. © 2014 John Wiley & Sons, Ltd.
Funding sources: This work has been supported by the Fonds voor Wetenschappelijk Onderzoek Vlaanderen (1.8.012.07.N.02; J. D. P.), the Instituut voor Wetenschap en Technologie (IWT/070715), the European Commission (Industria-Academia Partnership via www.endovv.com; PIAP-GA-2009-251356; P. D. K. and J. R.) and the Klinische onderzoeks- en opleidingsraad fonds of the University Hospitals Leuven (T. V. M.). Conflicts of interest: None declared
INTRODUCTION Congenital diaphragmatic hernia (CDH) is a rare congenital malformation affecting approximately 1 to 4 per 10 000 live births.1 The condition arises in the embryonic stage when the diaphragm fails to close. Abdominal organs herniate through this defect into the thoracic cavity. This results in mediastinal shift and compromised lung development. At birth, the lungs of these neonates are hypoplastic; that is, they are smaller and have fewer bronchi and alveoli as well as abnormally developed pulmonary vasculature. CDH also has an impact on the size of the ipsilateral cardiac structures.2,3 In fetuses with left-sided CDH (LCDH), which are more frequent and thus better documented, ventricular dimensions are smaller both on prenatal ultrasound3,4 and in autopsy specimens.5 In a recent report, we described similar changes in fetuses with right-sided CDH (RCDH).6 Experimental data in sheep have shown that there is true hypoplasia of the ventricle rather than
Prenatal Diagnosis 2014, 34, 1262–1267
atrophy, as the DNA/protein ratio remains unchanged compared with normal controls.7,8 The underlying etiology resulting in the smaller cardiac size is likely a combination of several factors. Because of the herniated organs, there is compression of the cardiac structures and an altered cardiac axis leading to a distorted orientation between the foramen ovale and inferior caval vein.2,9,10 As a consequence, the venous return from the inferior vena cava is inadequately streamed into the right rather than the left ventricle. In combination with an increased pulmonary vascular resistance and, hence, reduced pulmonary flow, this leads to decreased left ventricular preloading and poorer growth.10 Despite the significant reduction in cardiac size, the functional impact of this ventricular smallness is questionable. Indeed, in most CDH fetuses, biventricular circulation can be achieved after birth, and true aortic coarctation is rare.4
© 2014 John Wiley & Sons, Ltd.
Speckle tracking echocardiography in congenital diaphragmatic hernia
1263
Deformation analysis with speckle tracking or velocity vector imaging (VVI) is a recent method to evaluate the fetal ventricular function. The technique makes use of speckles that are natural acoustic markers present in a 2D ultrasound image. These speckles are equally distributed throughout the myocardium and can be identified by purpose-designed software. Tracking of these markers during the cardiac cycle yields information on tissue movement, thereby generating velocity vectors.11 The acquired vectors allow the determination of myocardial displacement, velocity and deformation (strain and strain rate). The use of speckle tracking in the prenatal period has been shown feasible in healthy fetuses as well as fetuses with pathologic fetal hearts.11–14 We aimed to apply this technology to evaluate cardiac function in fetuses with CDH to document potential implications of this condition of ventricular deformation. Given the abnormal position and morphologic appearance of the heart, we also wanted to evaluate its feasibility.
analyzed in the same way as we described earlier to allow comparison between the two data sets.20 The timing of the onset of the cardiac cycle was defined on the basis of mitral valve opening on a concomitantly generated M-mode tracing of the mitral valve. The endocardium was manually traced for both the left and the right cardiac ventricles on a still frame in mid to end systole. The ventricle was traced starting just below the valve annulus of the atrioventricular valve, over the ventricular free wall to the apex and then returning to the cardiac base over the septum. The software then automatically generates velocity vectors using speckle tracking and border recognition. The accuracy of tracking was subjectively verified, and border delineation with subsequent tracking was repeated when necessary (Figure 1). For each segment (base, mid and apex) of each ventricular wall (left free wall, right wall and septum), we obtained peak longitudinal cardiac velocity, displacement and strain values (Figure 1). The software also provides a so-called global result for each parameter, being the averaged regional values for each ventricular wall. Regarding the septum, we only used the data obtained while analyzing the left ventricle, as both left and right sides of the septum are reflections of the same muscular region. As controls, we used the raw data of measurements in 59 uncomplicated singleton fetuses between 16 and 36 weeks, which were part of an earlier normative study.20
MATERIALS AND METHODS This is a prospective single-center observational study performed at the University Hospitals Leuven. We included consecutive fetuses diagnosed with isolated CDH and confirmed normal karyotype between November 2010 and December 2011. Each fetus was included only once, that is, at first assessment in our unit, before any fetal intervention was performed. Maternal, delivery and neonatal records were reviewed to confirm the isolated character of the defect and to exclude congenital cardiac malformations interfering with fetal cardiac function. Lung size was assessed using the lung-to-head ratio (LHR)15 expressed as a ratio of what is normally expected for that gestational age,16 to obtain a gestational independent measurement (observed/ expected or O/E LHR).17,18 The intrathoracic part of the liver was expressed as a ratio to the thoracic cavity volume (LiTR) as was described previously.19 The prenatal program for in utero management of CDH, including the evaluation of parameters predicting outcome, as well as a randomized trial comparing fetal treatment with expectant management during pregnancy, have been approved by the Ethics Committee of the University Hospitals Leuven.
Cardiac ultrasound All ultrasound images were acquired on a Voluson E8 or 730 Expert ultrasound machine (GE Medical Systems, Kretztechnik, Zipf, Austria), using a curved 4- to 8-MHz linear array volumetric 3D probe. Image settings were optimized as previously described: speckle reduction imaging was turned off, and the contrast and gain were adapted to clearly visualize the delineation of the ventricular wall.20 All images were acquired at the level of the fetal four-chamber view and with optimal magnification to include only the fetal heart. Image acquisition was performed during a period of fetal inactivity. For each fetus, a cine-loop sequence including at least three complete cardiac cycles was obtained and stored for offline analysis. Images were stored in digital imaging and communications in medicine (DICOM) format and were exported to an external workstation for processing, using purposely designed software (Siemens VVI, version 3.0.0.428, Erlangen, Germany). The images were Prenatal Diagnosis 2014, 34, 1262–1267
Statistical analysis Data were analyzed with Prism for Mac version 6.0b (GraphPad Software, San Diego, CA, USA). Continuous data were expressed as means and standard deviation or median and interquartile range if appropriate. The data from fetuses with RCDH and LCDH were analyzed separately. In the CDH groups, we evaluated regional differences within the examined ventricles using a two-way analysis of variance with Bonferroni’s post-hoc test. Subsequently, global ventricular wall (left ventricle, right ventricle and septum) control values were compared with measurements in fetuses with CDH using multivariate analysis of covariance (MANCOVA) testing with gestational age as covariate, followed by simple contrast analysis. We also evaluated the correlation between O/E LHR, LiTR and strain values in the left ventricle in fetuses with LCDH. A p value < 0.05 was considered statistically significant.
RESULTS Thirty-eight consecutive fetuses with CDH were examined with a mean gestational age of 26.9 ± 2.5 weeks (range 20.9–31.6 weeks). In the majority of cases, the defect was located on the left side (n = 29), whereas nine fetuses had an RCDH. Median O/E LHR was 29.0% (21.5–37.5%) and 35.5% (29.4–56.4%) in LCDH and RCDH, respectively. In 79% of the LCDH cases, there was a partial herniation of liver [median LiTR: 9.7% (3.3–15.4%)] into the thorax, and as expected, all cases with RCDH had liver herniation. In six (16%) fetuses (five LCDH and one RCDH), the obtained images were of insufficient quality for further analysis, because of either fetal position or maternal obesity. In the remaining 32 fetuses, all six segments of the ventricle could be adequately tracked. The results for peak longitudinal velocity, displacement and strain measurements are presented in Tables 1 and 2. The © 2014 John Wiley & Sons, Ltd.
P. DeKoninck et al.
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Figure 1 Longitudinal strain waveforms with 2D speckle tracking. Top: left ventricle in LCDH. Bottom: right ventricle in RCDH median fetal heart rate was 143 (136–149) bpm, and the frame rates (FRs) ranged between 38 and 62 Hz (average 44 Hz). This means that about 18 image frames were obtained per cardiac cycle. In fetuses with LCDH, velocity and displacement showed a significant increase from apex to base in all three ventricular walls (Table 1). There were also significant regional differences for strain with higher values in the apex, compared with the mid and basal regions in the left ventricular wall and septum (p < 0.01). Comparing the three ventricular walls, velocity and displacement were significantly higher in the right ventricular wall as compared with the septum and the left free wall, which is similar to observations in controls (p < 0.001). We did not observe significant differences in strain values between the ventricular walls in LCDH. In RCDH cases, we observed a similar increase from apex to base for velocity and displacement values in the right and left ventricular walls. Comparing the separate walls, we only observed higher velocity and displacement measurements in the basal region of the right ventricle compared with the left wall and septum. Strain values were not different between the different ventricular walls. Evaluating the global ventricular function of the ventricular walls using MANCOVA testing with GA as a covariate, we observed significant differences in measurements in the left ventricle and septum in fetuses with LCDH compared with controls (p < 0.0001). Table 2a displays the differences between LCDH and controls. In the left ventricle, the most interesting observation was an increase in strain values in the cases compared with normal controls. Conversely, in the septum, the differences were mainly caused by differences in Prenatal Diagnosis 2014, 34, 1262–1267
myocardial motion (velocity and displacement). In the right ventricle, there were no significant differences from controls. In the RCDH group, there were no significant differences between cases and normal controls; these data are displayed in Table 2b. There was no significant correlation between the pulmonary size, assessed by O/E LHR and liver herniation (LiTR), and the observed strain values in both CDH groups.
DISCUSSION In this study, we evaluated the use of velocity vector imaging in fetuses with isolated CDH. Using this method, we have found no evidence for ventricular dysfunction in these fetuses. As the base of the heart moves toward the apex, velocity and displacement values are normally increasing from the apex to the base.11 In fetuses with CDH, we observed the same regional differences. In LCDH, we observed higher longitudinal strain values in apex compared with the mid and basal regions, which could be the result of an altered distribution of wall stress within the left ventricle due to geometrical changes. Alternatively, higher apical strain values could be measured because of foreshortening that could be more pronounced during abnormal ventricular (out of plane) motion as a result of the hernia. Furthermore, the higher global strain values in the left ventricular free wall, in comparison with normal controls, are most likely the mechanical expression of well-documented anatomical changes. Indeed, in an attempt to maintain normal cardiac output values, a small ventricle will undergo more deformation21 and as such could explain the increased strain values observed in the left ventricular free wall. Nevertheless, © 2014 John Wiley & Sons, Ltd.
0.04
