Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study

Clinical Radiology xxx (2016) e1ee7

Contents lists available at ScienceDirect

Clinical Radiology journal homepage: www.clinicalradiologyonline.net

Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study d  q. Mazurkiewicz a, *, E. Or1owska-Baranowska b, J. Petryka c, M. Spiewak , M. Gawor e, B. Mi1osz-Wieczorek d, K. Werys d, q.A. Ma1ek f, M. Marczak d, J. Grzybowski e a

Department of Cardiomyopathies, CMR Unit, Institute of Cardiology, Warsaw, Poland Department of Acquired Cardiac Defects, Institute of Cardiology, Warsaw, Poland c Department of Coronary and Structural Heart Diseases, CMR Unit, Institute of Cardiology, Warsaw, Poland d CMR Unit, Institute of Cardiology, Warsaw, Poland e Department of Cardiomyopathies, Institute of Cardiology, Warsaw, Poland f Institute of Cardiology, Warsaw, Poland b

art icl e i nformat ion Article history: Received 28 March 2016 Received in revised form 18 August 2016 Accepted 10 October 2016

AIM: To investigate changes in myocardial tissue volume during the cardiac cycle to verify the hypothesis of non-compressibility of the myocardium in healthy individuals (HI) as well as in patients with hypertrophic cardiomyopathy (HCM), dilated cardiomyopathy (DCM), and aortic stenosis (AS). MATERIALS AND METHODS: The study group included 30 HI, and patients with HCM (n¼110), DCM (n¼89), and AS (n¼78). Left ventricular (LV) function, end-diastolic, and endsystolic volumes were calculated based on cardiac magnetic resonance imaging (CMR) for all participants. RESULTS: End-systolic myocardial volumes were higher than end-diastolic in both controls (91.226.6 versus 85.124.3 ml, p<0.001) and in all patient groups: HCM (214.381.6 versus 17664.2 ml, p<0.01), DCM (128.443.1 versus 115.442.9 ml, p<0.001) and AS (155.137.1 versus 129.434.6 ml, p<0.001). HCM and AS patients had significantly higher systolic volume gain than HI (21.58.3 versus 10.66.3%, p<0.01 and 18.35.7 versus 10.66.3% p¼0.013, respectively). Conversely, DCM patients had lesser increases in myocardial systolic volume than HCM patients (11.24.8% versus 21.58.3, p¼0.01) and AS patients (11.24.8% versus 18.35.7, p¼0.02). No differences were found in systolic volume gain between AS and HCM patients (p¼ns) or between DCM patients and HI (p¼ns). CONCLUSION: End-systolic myocardial volume was significantly higher than end-diastolic volume in all subsets of patients. The systolic volume gain was greater in individuals with hypertrophy than in those without. Ó 2016 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Introduction * Guarantor and correspondent: q. Mazurkiewicz, Department of Cardiomyopathies, CMR Unit, Institute of Cardiology, 42nd Alpejska Str, Warsaw 04-682, Poland. Tel.: þ48 501717527; fax: þ48 223434515. E-mail address: [email protected] (q. Mazurkiewicz).

Heart muscle morphology is usually altered in patients with cardiac disease.1e3 Different forms of hypertrophy are observed in patients with hypertrophic cardiomyopathy

http://dx.doi.org/10.1016/j.crad.2016.10.024 0009-9260/Ó 2016 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Mazurkiewicz q, et al., Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study, Clinical Radiology (2016), http://dx.doi.org/10.1016/j.crad.2016.10.024

e2

Ł. Mazurkiewicz et al. / Clinical Radiology xxx (2016) e1ee7

(HCM), hypertension, and valvular heart disease, such as aortic stenosis (AS), and it is also seen in athletes.4e9 In contrast, myocardial thinning with contractility impairment is seen in dilated cardiomyopathy (DCM;10,11). Histologically, hypertrophy can be distinguished by cardiomyocyte hypertrophy, fibre disarray, replacement fibrosis, and interstitial fibrosis.7,12,13 In DCM, myocyte apoptosis and diffuse fibrosis are typical.10,11 In the normal heart, myocardial deformation during the working cycle consists of shortening and thickening of the myocardium.14e16 It is currently thought that myocardial volume during systole and diastole is constant.17 This assumption was made based on echocardiography measurements of cardiac function; however, few data exist to support this hypothesis. The existing literature confirms that myocardial non-compressibility in healthy individuals (HI), using three-dimensional (3D), freehand echocardiography18 or computed tomography.19 Moreover, there are limited data on the changes of myocardial volume in other cardiac diseases. Cardiac magnetic resonance imaging (CMR) is the reference standard and offers reproducible analysis of left ventricular (LV) mass, volume, and geometry.20,21 This has been recognised in recent European Society of Cardiology guidelines, particularly with regards to tissue characterisation properties.22 The aim of the present study was to investigate the changes in myocardial tissue volume during the cardiac cycle, using CMR to verify the hypothesis that the myocardium in HI and patients with primary (HCM) and secondary AS forms of hypertrophy as well as in DCM.

Materials and methods The study was approved by the Institutional Ethics Committee and all patients provided a written informed consent before the study procedures.

Study cohort The patients were divided into four groups; Group A: the group of HI (n¼30; 20 males, mean age 23.23.1 years) with no significant medical history, normal physical examination, and normal 12-lead electrocardiography (ECG) results; group B: the HCM group comprised 110 patients with HCM who were diagnosed according to the standard criteria published in clinical guidelines.23 Patients with Fabry’s disease, Noonan’s syndrome, or a history of previous alcohol septal ablation were excluded from the study; group C: the AS group included 78 patients with severe aortic valve stenosis defined at echocardiography as a valve orifice area (AVA) <1 cm2, an indexed AVA <0.6 cm2/m2, a mean transvalvular gradient >40 mmHg, and a maximal velocity >4 m/s without significant aortic regurgitation or other concomitant cardiac disease24; group D: the DCM group comprised 89 patients with DCM who were diagnosed based on the World Health Organization (WHO)/European Society of Cardiology (ESC) recommendations, including increased LV volume and decreased ejection fraction (EF) of <40% measured at CMR.25 Patients with secondary or

reversible forms of cardiomyopathy caused by cardiotoxicity, human immunodeficiency virus (HIV) infection, neuromuscular diseases, tachyarrhythmias, or endocrine disorders were excluded. All patients except for controls underwent clinical and laboratory evaluation as well as echocardiography as a part of the routine evaluation. Coronary artery disease was excluded based on coronary angiography or computed tomography according to the Felker et al. criteria.26 Moreover, the presence of subendocardial late gadolinium enhancement, which is suggestive of myocardial infarction, was an exclusion criterion.

CMR CMR was performed in all patients using a 1.5 T system (Avanto, Siemens, Erlangen, Germany). A stack of short-axis breath-hold steady-state free precession images was used to calculate ventricular volumes and EF using dedicated software (MASS 6.2.1, Medis, Leiden, The Netherlands). The typical imaging parameters included: 2.2e3.6 ms repetition time, 1.2 ms echo time, 640e790 flip angle, 8 mm section thickness, and 2 mm gap. The volumetric analysis of the LV was performed according to the recommendations of the Society for Cardiovascular Magnetic Resonance Board of Trustees Task Force on Standardized Protocols.27,28 A shortaxis stack of cine images for ventriculography was planned by adjusting the section locations on four-chamber and LV two-chamber images in diastole (Fig 1). Both the axial and short-axis stacks were prescribed to ensure complete coverage of the LV. In the short-axis, the sections were oriented perpendicular to the ventricular septum on the four-chamber view, and care was taken to ensure precise positioning of the mitral valve plane for the accurate calculation of myocardial volume. The most basal short axis section was located immediately on the myocardial side of the atrioventricular junction at end-diastole prescribed from the previously acquired long axis cine images. Manual delineation of endocardial and epicardial contours was performed in the end-diastolic and end-systolic phases by three experienced observers (Fig 2). Using these data, the LV end-diastolic volume (LVEDV), LV end-systolic volume (LVESV), LV mass (LVM), LV ejection fraction (LVEF), and LV myocardial end-systolic (EDMV), and end-diastolic volumes (ESMV) were calculated. The maximal diastolic wall thickness (DWT) was recorded. The systolic wall thickness (SWT) was measured at the same point as the maximal diastolic wall thickness. The difference between SWT and DWT was absolute wall thickening (AWT;29). The ratio of AWT to DWT was the thickening gain (TG) and was expressed as a percentage. The average differences between ESMV and EDMV were expressed as absolute value and as a percentage of EDMV. The LVEDV, LVESV, and LVM were indexed for the body surface area (BSA). The papillary muscles were excluded from the LV mass calculation both in diastole and in systole. Close attention was paid to identifying the thickening papillary muscles in systole by comparing images from different phases of the cardiac cycle to exclude all trabecular tissue. All patients from the

Please cite this article in press as: Mazurkiewicz q, et al., Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study, Clinical Radiology (2016), http://dx.doi.org/10.1016/j.crad.2016.10.024

Ł. Mazurkiewicz et al. / Clinical Radiology xxx (2016) e1ee7

e3

Figure 1 Planning for ventriculography. A short-axis stack of cine images for ventriculography is planned by adjusting the section locations on four-chamber and LV two-chamber images in diastole. The axial and short-axis stacks are prescribed to ensure complete coverage of the left ventricle. The sections are oriented perpendicular to the ventricular septum on the four-chamber view, and care is taken to ensure that coverage includes all segments of left ventricle.

study group and controls underwent a full protocol CMR examination.

Statistical analysis All continuous variables were expressed as a mean  standard deviation or as a median and interquartile range. They were tested for normal distribution with the KolmogoroveSmirnov test. Comparisons between groups were performed with a two-sided Student’s t-test, WilcoxoneManneWhitney U-test, and chi-square or Fisher’s exact test for categorical variables as appropriate. The EDMV and

ESMV were compared with a two-sample paired t-test. Analysis of variance (ANOVA) was used to assess the significance of differences of myocardial volume and thickness gains between the groups. Post-hoc multiple comparisons (Bonferroni test) were performed to determine which gains were significantly different in cases of significant difference at ANOVA. For post-hoc analysis, six values of p, pHI/HCM, pHI/ AS, pHI/DCM, pHCM/AS, pHCM/DCM, pAS/DCM, were presented for significance between volume gains in the HI and HCM, HI and AS, HI and DCM, HCM and AS, HCM and DCM, AS and DCM groups, respectively. Correlation was tested by using the Pearson method. Intra-observer and interobserver

Figure 2 The examples of endomyocardial and epicardial contours in the end-diastolic and end-systolic phases in basal, mid-ventricular, and apical segments for all subsets of patients. All trabecular tissue was excluded in both diastole and systole. The volumetric analysis of left ventricle was based on ventriculography, which covered the whole left ventricle from base to apex. Please cite this article in press as: Mazurkiewicz q, et al., Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study, Clinical Radiology (2016), http://dx.doi.org/10.1016/j.crad.2016.10.024

Ł. Mazurkiewicz et al. / Clinical Radiology xxx (2016) e1ee7

e4 Table 1 Baseline clinical and CMR characteristics. HI No. 30 Age (years) 23.2 3.1 Male sex (n) 20 Heart rate (/min) 6512 Systolic BP (mmHg) 114.618.7 Diastolic BP (mmHg) 77.212.3 NYHA NA BSA (m2) 2.0 Magnetic resonance imaging data 87.427.2 LVEDVI (ml/m2) LVESVI (ml/m2) 32.425.1 LVEF (%) 62.97.2 LVMI (g/m2) 44.510.3 DWT (mm) 9.41.3 AWT (mm) 3.11.4

HCM

AS

DCM

110 34.1 4.1 68 7012 117.310.7 79.113.1 1.80.1 2.1

78 67.6 11.3 46 7811 125.112.9 84.113.8 1.60.1 2.1

89 32.8 7.1 51 8117 103.416.7 64.99.3 2.40.2 1.9

91.617.3 32.612.9 64.48.4 87.829.6 21.87.6 9.77.6

82.416.7 29.49.8 64.16.37 67.815.2 13.92.6 6.51.2

181.237.3 130.432.9 28.26.7 63.718.7 8.81.3 2.60.9

HI, healthy individuals; HCM, hypertrophic cardiomyopathy; AS, aortic stenosis; DCM, dilated cardiomyopathy; BP, blood pressure; BSA, body surface area; LVEDVI, left ventricle end diastolic volume index; LVESDI, left ventricle end systolic volume index; LVEF, left ventricle ejection fraction; LVMI, left ventricle mass index; DWT, diastolic wall thickness; AWT, absolute wall thickening.

variability for CMR measurements of LV volumes was assessed in 15 randomly selected patients in each group, using the BlandeAltman repeatability analysis method and interclass correlation coefficient. A two-sided p-value of <0.05 indicated statistical significance. The statistical analyses were performed using MedCalc 12.1.4.0 software (MedCalc, Mariakerke, Belgium).

Results There was a very good agreement for myocardial volume calculations between the two operators and for the repeated assessment of the same operator. For interobserver variability, the average difference in estimates was 1.33.1%, interclass correlation coefficient e0.99; for intraobserver variability the average difference was 0.52.5% with interclass correlation coefficient of 0.99. Baseline clinical and CMR characteristics are presented in Table 1. As expected, patients with AS were the oldest, and DCM patients were the youngest and had the largest LVEDVI and smallest LVEF. The HCM and AS patients had increased LV mass and unimpaired LV function. A comparison of ESMV and EDMV is shown in Table 2. In all study groups, the ESMV were higher than the EDMV. The average differences between ESMV and EDMV in the whole

Table 2 Comparison of end-systolic and end-diastolic myocardial volumes.

HI HCM AS DCM

EDMV ( ml)

ESMV ( ml)

p-Value

85.124.3 176.264.2 129.434.6 115.442.9

94.226.6 214.381.6 153.137.1 128.443.1

<0.001 <0.001 <0.001 <0.001

EDMV, left ventricle end diastolic myocardial volume; ESMV, left ventricle end systolic myocardial volume; HI, healthy individuals; HCM, hypertrophic cardiomyopathy; AS, aortic stenosis; DCM, dilated cardiomyopathy.

study group were 29.419.7 ml or 20.717.2% of the enddiastolic volume. Patients with HCM and AS had significantly higher systolic volume gain than HI (p<0.01 and p¼0.013, respectively). Conversely, DCM patients had lesser increases in myocardial systolic volume than HCM (p¼0.01) and AS (p¼0.02) patients. In addition, no differences were found in systolic volume gain between AS and HCM patients and between DCM patients and HI (Table 3). The mean TG was 38.3%. HCM and AS patients had significantly higher TGs than both HI (p¼0.01 and p¼0.02, respectively) and DCM individuals (p¼0.02 and p¼0.02, respectively); however, the differences in TG between AS and HCM patients as well as between DCM and HI were negligible (Table 3). Significant correlations both between TG and systolic myocardial volume gain (r¼0.79, p<0.01; Fig 3) as well as between diastolic myocardial volume and the increase in myocardial volume in systole (r¼0.71, p<0.01; Fig 4) were found.

Discussion ESMV was significantly higher than the EDMV in all study groups. Patients with HCM and AS had a significantly higher increase in myocardial systolic volume compared with DCM patients and HI. In addition, no difference in systolic volume gain was found neither between the groups of patients with hypertrophy (AS and HCM groups) nor between HI and DCM patients. Most biological tissues, including heart muscle, are considered to be incompressible, anisotropic, nonhomogeneous, and elastic.30 In humans, the contraction starts when the cytoplasmic calcium binds to troponin C, moving the tropomyosin complex off the actin binding site and allowing the myosin head to bind to the actin filament. Adenosine triphosphate (ATP) hydrolysis of the myosin head pulls the actin filament toward the centre of the sarcomere.31 Previous studies of LV myocardial volume variations in the cardiac cycle generally concluded that the volume is approximately constant, although the possibility of a small variation was not rejected because there was insufficient precision. The magnitude of single sarcomere shortening does not generally exceed 15%.32 Geometric consideration would suggest that this degree of shortening of a cylindrical fibre would result in the thickening by about 8%; however, thickening of the LV wall may reach 40% or higher, which is due to the specific structural morphology of the heart wall: myocardial fibres change the orientation from oblique at the epicardium through the circumferential orientation at the mid-wall to a reverse oblique direction at the end myocardium.33 In agreement with previous studies, systolic wall thickening gain was 38.3%. De Dumesnil et al.34 proposed that wall thickening is a direct reflection of the shortening that occurs in the circumferential and longitudinal directions. Rodrigues et al.29 demonstrated that an increased end-diastolic wall thickness consequently leads

Please cite this article in press as: Mazurkiewicz q, et al., Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study, Clinical Radiology (2016), http://dx.doi.org/10.1016/j.crad.2016.10.024

Ł. Mazurkiewicz et al. / Clinical Radiology xxx (2016) e1ee7

e5

Table 3 Comparisons of myocardial volume change between systole and diastole (percentage of end-diastolic myocardial volume) and thickening gain in all subset of patients.

Change of volume (%) TG (%)

HI

HCM

AS

DCM

p-Value (ANOVA between groups)a

Post hoc multiple comparisonsb pHI/HCM

pHI/AS

pHI/DCM

pHCM/AS

pHCM/DCM

pAS/DCM

10.66.3

21.58.3

18.35.7

11.24.8

0.02

<0.01

0.013

ns

ns

0.01

0.02

32.89.2

44.618.1

46.612.6

29.57.2

0.02

0.01

0.02

ns

ns

0.02

0.02

HI, healthy individuals; HCM, hypertrophic cardiomyopathy; AS, aortic stenosis; DCM, dilated cardiomyopathy; TG, thickening gain (AWT/DWT ratio); AWT, absolute wall thickness; DWT, diastolic wall thickness. a The significant deference between at least two of the subgroups. b pHI/HCM; pHI/AS; pHI/DCM; pHCM/AS; pHCM/DCM; pAS/DCM, indicates significance level between volume gains in HI and HCM; HI and AS; HI and DCM; HCM and AS; HCM and DCM; AS and DCM groups; respectively.

to an increase in wall thickness in end-systole. In fact, systolic wall thickness gain was greater in patients with hypertrophy. Moreover, a very good correlation was found between systolic wall thickening gain and the increase in myocardial volume. These findings might explain why change in myocardial volume was highest in hypertrophied hearts. Myocardial volume constancy is a fundamental principle in the measurement of cardiac function; however, data on the volume change analysis of the myocardium during the cardiac cycle remain controversial. Varied detailed analysis on animal models and humans were utilised to verify the hypothesis of non-compressibility of cardiac tissue. In the studies of Ashikaga et al.35 and Waldman et al.36 myocardial volume changes during systole and diastole were analysed based on cardiac deformations measured by implanted intramyocardial gold beads. Authors calculated a change of heart tissue only in 3.375 mm3 cubic of heart muscle. The authors reported 15% reduction of systolic volume. They also admitted that there seemed to be substantial regional and species variations in the systolic volume change. In sheep and beagles, the systolic decrease in volume was much smaller. Moreover, Rodriguez et al.37 measured the myocardial volume in a single mid-ventricular 1.5 mm thick slice of a beagle heart in an MRI tissue-tracking study. None

of these studies performed 3D volumetric analysis measuring the myocardial volume of a whole heart, as in the present study. In a view of these facts, the conclusions of these studies have limited application to the human heart. Abott et al.38 used piezoelectric methods to demonstrate changes in the volume of isolated frog and skeletal muscles during electric stimulation. This correlated with the pressure that developed inside the tissue during contraction. Ritman et al.39 used porcine hearts to calculate wall volumes through the heart cycle within 5% limits. Previously, Tsuiki et al.17 noticed that isolated canine LV muscle changes volume by 7% between systole and diastole. They both concluded that the variation in the calculated heart wall volume is influenced by the change in the myocardial blood flow to each phase of the cardiac cycle as well as by squeezing the part containing blood in the heart wall. The present results confirm that in HI, the change in myocardial volume is w10%. The higher increase in myocardial volume seen here is a result of the smaller sample size as well as the inclusion of other specimens and muscle types in the previous reports. There were also limitations in the measurement techniques available at that time. King et al.18 used 3D echocardiography to show that in healthy athletes, the differences between systolic and diastolic myocardial volumes were <2 ml or 1% of the diastolic

Figure 3 Correlation between myocardial volume gain and thickening gain (r¼0.79, p<0.001).

Figure 4 Correlation between the increase in myocardial volume in systole and myocardial diastolic volume (r¼0.71, p<0.001).

Please cite this article in press as: Mazurkiewicz q, et al., Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study, Clinical Radiology (2016), http://dx.doi.org/10.1016/j.crad.2016.10.024

e6

Ł. Mazurkiewicz et al. / Clinical Radiology xxx (2016) e1ee7

volume, which is far less than the values found in the present study. Freehand 3D echocardiography is a highly accurate and precise method for computing LV volume and mass compared with MRI, even in abnormal LVs; however, different imaging methods and the limitations of 3D echocardiography, such as slight underestimation of volume by the surface reconstruction algorithm and additional skills required for performing image acquisition, can be responsible for measurement discrepancy. Data regarding the heart volume in cardiac diseases are very limited. The aim of the present study was to include a large spectrum of cardiac diseases. Contrary to the present results, King et al.18 found no difference in myocardial volume throughout the heart cycle in patients with heart failure and preserved systolic function. A relatively small sample size and imaging method limitations might negatively affect the results. In the present study, the myocardial volume gain was significantly greater in patients with hypertrophy, which clearly demonstrates that an increased amount of myocardium provides additional volume generated during systole. The similar volume gains in both forms of hypertrophy (AS and HCM) suggest that the histological distinctness, such as fibre disarray and coronary microvascular dysfunction, found in HCM does not influence systolic volume gain. Conversely, loss of cardiomyocytes as a common cause of contractility compromise in DCM patients does not lead to the decrease of systolic volume gain compared to HI. That might be explained by an extensive workout of surviving myocytes as a part of the remodelling processes in the failing heart. Further analysis of myocardial volume gain may allow differentiation of the varied forms of hypertrophy and improve diagnostic accuracy of CMR in heart failure. In conclusion, MRI remains the reference standard for the measurement of cardiac volume and mass, and it is superior to other imaging methods. This study is first to reliably report statistical differences in myocardial volume during the cardiac cycle. ESMV was greater than EDMV, in both HI and patients with abnormal left ventricles. The magnitude of volume increase in systole was greater in individuals with hypertrophy than in patients without. No difference in systolic myocardial volume gain was found neither between AS and HCM patients nor between DCM patients and HI.

Acknowledgements The study was supported by a governmental grant from the Polish Ministry of Science and Higher Education (2011/ 03/B/NZ7/04870).

References 1. Takahashi M, Sasayama S, Kawai C, et al. Contractile performance of the hypertrophied ventricle in patients with systemic hypertension. Circulation 1980;62:116e26. 2. Hartford M, Wikstrand JCM, Wallentin I, et al. Left ventricular wall stress and systolic function in untreated primary hypertension. Hypertension 1985;7:97e104.

3. Bing OHL, Matsushsita S, Fanburg BL, et al. Mechanical properties of rat cardiac muscle during experimental hypertrophy. Circ Res 1971;28: 234e45. 4. Mann DL, Urabe Y, Kent RL, et al. Cellular versus myocardial basis for the contractile dysfunction of hypertrophied myocardium. Circ Res 1991;68:402e15. 5. Shimizu G, Hirota Y, Kita Y, et al. Left ventricular mid-wall mechanics in systemic arterial hypertension: myocardial function is depressed in pressure-overload hypertrophy. Circulation 1991;83:1676e84. 6. Zhang YD, Li M, Qi L, et al. Hypertrophic cardiomyopathy: cardiac structural and microvascular abnormalities as evaluated with multiparametric MRI. Eur J Radiol 2015;84(8):1480e6. 7. Briasoulis A, Mallikethi-Reddy S, Palla M, et al. Myocardial fibrosis on cardiac magnetic resonance and cardiac outcomes in hypertrophic cardiomyopathy: a meta-analysis. Heart 2015;101(17):1406e11. 8. Bahlmann E, Kuck KH, Nienaber CA. Athlete’s heart and hypertrophic cardiomyopathy: contribution on clinical and morphologic differentiation. J Am Coll Cardiol 1983;1(3):783e9. 9. Hess OM, Schneider J, Turina M, et al. Asymmetric septal hypertrophy in patients with aortic stenosis: an adaptive mechanism or a coexistence of hypertrophic cardiomyopathy? J Am Coll Cardiol 1983 Mar;1(3):783e9. € pe C. Endomyocardial biopsy and ul10. Savvatis K, Schultheiss HP, Tscho trastructural changes in dilated cardiomyopathy: taking a ‘deeper’ look into patients’ prognosis. Eur Heart J 2015;36(12):708e10. 11. Saito T, Asai K, Sato S, et al. Ultrastructural features of cardiomyocytes in dilated cardiomyopathy with initially decompensated heart failure as a predictor of prognosis. Eur Heart J 2015;36(12):724e32. 12. Bai F, Wang L, Kawai M. A study of tropomyosin’s role in cardiac function and disease using thin-filament reconstituted myocardium. J Muscle Res Cell Motil 2013;34(3e4):295e310. 13. Moravsky G, Ofek E, Rakowski H, et al. Myocardial fibrosis in hypertrophic cardiomyopathy: accurate reflection of histopathological findings by CMR. JACC Cardiovasc Imaging 2013;6(5):587e96. 14. Flitney FW, Hirst DG. Filament sliding and energy absorbed by the crossbridge in active muscle subjected to cyclical length changes. J Physiol 1978;276:467e79. 15. Bosco C, Tarkka I, Komi PV. Effect of elastic energy and myoelectrical potentiation of triceps surae during stretcheshortening cycle exercise. Int J Sports Med 1982;3(3):137e40. € din B, et al. Mechanical efficiency of positive work in 16. Ito A, Komi PV, Sjo running at different speeds. Med Sci Sports Exerc 1983;15(4):299e308. 17. Tsuiki K, Ritman EL, Donald DE, et al. Videometric determination of wall dynamics in a working isolated canine left ventricle. Physiologist 1973;16:473. 18. King DL, Coffin LE-K, Maurer MS. Non-compressibility of myocardium during systole using freehand three-dimensional echocardiography. J Am Soc Echocardiogr 2002;15:545. 19. Ritman EL. Temporospatial heterogeneity of myocardial perfusion and blood volume in the porcine heart wall. Ann Biomed Eng 1998;26: 519e25. 20. Nikitin NP, Loh PH, de Silva R, et al. Left ventricular morphology, global and longitudinal function in normal older individuals: a cardiac magnetic resonance study. Int J Cardiol 2006;108(1):76e83. 21. Grothues F, Moon JC, Bellenger NG, et al. Interstudy reproducibility of right ventricular volumes, function, and mass with cardiovascular magnetic resonance. Am Heart J 2004;147(2):218e23. 22. von Knobelsdorff-Brenkenhoff F, Schulz-Menger J. Role of cardiovascular magnetic resonance in the guidelines of the European Society of Cardiology. J Cardiovasc Magn Reson 2016;18(1):6. 23. Gersh BJ, Maron BJ, Bonow RO, et al. 2011 ACCF/AHA guideline for the diagnosis and treatment of hypertrophic cardiomyopathy: executive summary: a report of the American College of Cardiology Foundation/ American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2011;58:2703e38. 24. Vahanian A, Alfieri O, Andreotti F, et al. Guidelines on the management of valvular heart disease (version 2012): the Joint Task Force on the Management of Valvular Heart Disease of the European Society of Cardiology (ESC) and the European Association for Cardio-Thoracic Surgery (EACTS). Eur J Cardiothorac Surg 2012;42(4):S1e44. 25. Elliott P, Andersson B, Arbustini E, et al. Classification of the cardiomyopathies: a position statement from the European Society of Cardiology

Please cite this article in press as: Mazurkiewicz q, et al., Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study, Clinical Radiology (2016), http://dx.doi.org/10.1016/j.crad.2016.10.024

Ł. Mazurkiewicz et al. / Clinical Radiology xxx (2016) e1ee7

26.

27.

28.

29.

30.

31.

Working Group on Myocardial and Pericardial Diseases. Eur Heart J 2008;29:270e6. Felker GM, Shaw LK, O’Connor CM. A standardized definition of ischemic cardiomyopathy for use in clinical research. J Am Coll Cardiol 2002;39:210e8. Kramer CM, Barkhausen J, Flamm SD, et al. Cardiovascular magnetic resonance imaging (CMR) protocols, society for cardiovascular magnetic resonance: board of trustees task force on standardized protocols. J Cardiovasc Magn Reson 2008;10:35. http://dx.doi.org/10.1186/1532429X-10-35. Schulz-Menger J, von Knobelsdorff-Brenkenhoff F, Bluemke DA, et al. Standardized post processing in cardiovascular magnetic resonance. J Cardiovasc Magn Reson 2013;15:35. http://dx.doi.org/10.1186/1532429X-15-35. Rodrigues JC, Rohan S, Dastidar AG, et al. The relationship between left ventricular wall thickness, myocardial shortening, and ejection fraction in hypertensive heart disease: insights from cardiac magnetic resonance imaging. J Clin Hypertens (Greenwich) 2016 Jun 17, http://dx.doi.org/ 10.1111/jch.12849 [Epub ahead of print]. Mirsky I. Basic terminology and formulae for left ventricular wall stress. In: Mirsky I, Ghista DN, Sandler H, editors. Cardiac Mechanics. New York: John Wiley & Sons; 1974. p. 3e10. 5. Fabiato A. Calcium-induced calcium release from the cardiac sarcoplasmic reticulum. Am J Physiology 1983;245(1):C1e14.

e7

32. Sonnenblick EH, Ross Jr J, Covell JW, et al. The ultrastructure of the heart in systole and diastole. Circ Res 1967;21:423e31. 33. Rademakers FE, Rogers WJ, Guier WH, et al. Relation of regional crossfiber shortening to wall thickening in the intact heart. Threedimensional strain analysis by NMR tagging. Circulation 1994 Mar;89(3):1174e82. 34. Dumesnil JG, Shoucri RM, Laurenceau JL, et al. A mathematical model of the dynamic geometry of the intact left ventricle and its application to clinical data. Circulation 1979;59:1024e34. 35. Ashikaga H, Coppola BA, Yamazaki KG, et al. Changes in regional myocardial volume during the cardiac cycle: implications for transmural blood flow and cardiac structure. Am J Physiol Heart Circ Physiol 2008;295:H610e8. 36. Waldman LK, Fung YC, Covell JW. Transmural myocardial deformation in the canine left ventricle. Normal in vivo three-dimensional finite strains. Circulation Research 1985;57:152e63. 37. Rodriguez I, Ennis DB, Wen H. Noninvasive measurement of myocardial tissue volume change during systolic contraction and diastolic relaxation in the canine left ventricle. Magn Reson Med 2006 Mar;55(3):484e90. 38. Abott BC, Baskin RJ. Volume changes in frog muscle during contraction. J Physiol 1962;161:379e91. 2. 39. Ritman EL, Sturm RE, Wood EH. Comparison of volume of canine left ventricular casts and angiograms using biplane and monoplane Roentgen videometry. Physiologist 1970;13:294.

Please cite this article in press as: Mazurkiewicz q, et al., Systolic myocardial volume gain in dilated, hypertrophied and normal heart. CMR study, Clinical Radiology (2016), http://dx.doi.org/10.1016/j.crad.2016.10.024