Left ventricular solid body rotation in non-compaction cardiomyopathy: A potential new objective and quantitative functional diagnostic criterion?

ure 10 (2008) 1088–1093www.elsevier.com/locate/ejheart

European Journal of Heart Fail

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Left ventricular solid body rotation in non-compaction cardiomyopathy:A potential new objective and quantitative functional diagnostic criterion?

Bas M. van Dalen, Kadir Caliskan, Osama I.I. Soliman, Attila Nemes,Wim B. Vletter, Folkert J. ten Cate, Marcel L. Geleijnse ⁎

Department of Cardiology, Thoraxcenter, Erasmus University Medical Center, Rotterdam, The Netherlands

Received 2 May 2008; received in revised form 4 July 2008; accepted 20 August 2008Available online 24 September 2008

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Abstract

Background: Left ventricular (LV) twist originates from the interaction between myocardial fibre helices that are formed during the formationof compact myocardium in the final stages of the development of myocardial architecture. Since non-compaction cardiomyopathy (NCCM)is probably caused by intrauterine arrest of this final stage, it may be anticipated that LV twist characteristics are altered in NCCM patients,beyond that seen in patients with impaired LV function and normal compaction.Aims: The purpose of this study was to assess LV twist characteristics in NCCM patients compared to patients with non-ischaemic dilatedcardiomyopathy (DCM) and normal subjects.Methods and results: The study population consisted of 10 patients with NCCM, 10 patients with DCM, and 10 healthy controls. LV twistwas determined by speckle tracking echocardiography. In all controls and DCM patients, rotation was clockwise at the basal level andcounterclockwise at the apical level. In contrast, in all NCCM patients the LV base and apex rotated in the same direction.Conclusions: These findings suggest that ‘LV solid body rotation’, with near absent LV twist, may be a new sensitive and specific, objectiveand quantitative, functional diagnostic criterion for NCCM.© 2008 European Society of Cardiology. Published by Elsevier B.V. All rights reserved.

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Keywords: Speckle tracking echocardiography; Non-compaction cardiomyopathy; Left ventricular rotation

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1. Introduction

Left ventricular (LV) twist, defined as the wringingmotion of the heart as the apex rotates with respect to thebase around the LV long-axis, has an important role in LVejection and filling [1,2]. The final stage of the developmentof myocardial architecture is characterized by the formationof compact myocardium and development of oppositelywound epicardial and endocardial myocardial fibre helices

Abbreviations: LV, Left ventricle (or ventricular); NCCM, Non-compac-tion cardiomyopathy; STE, speckle tracking echocardiography; DCM, Dilatedcardiomyopathy.⁎ Corresponding author. Department of Cardiology, Thoraxcenter, Erasmus

University Medical Center Rotterdam, 's-Gravendijkwal 230, 3015 CE, RoomBa304,Rotterdam, TheNetherlands. Tel.: +31104633533; fax: +3110 4635498.

E-mail address: [email protected] (M.L. Geleijnse).

1388-9842/$ - see front matter © 2008 European Society of Cardiology. Publishdoi:10.1016/j.ejheart.2008.08.006

[3,4]. LV twist originates from the dynamic interactionbetween these helices. Non-compaction cardiomyopathy(NCCM) is a heterogeneous disorder probably caused byintrauterine arrest of the final stage of cardiac embryogenesis[5]. It may be anticipated that LV twist characteristics arealtered in NCCM patients, beyond that seen in patients withimpaired LV function and normal compaction.

Recently, speckle tracking echocardiography (STE) hasbeen introduced as a new method for angle-independentquantification of LV twist [6]. Speckles are natural acousticmarkers that occur as small and bright elements inconventional grayscale ultrasound images. The specklesare the result of constructive and destructive interference ofultrasound, back-scattered from structures smaller than awavelength of ultrasound [7]. This gives each small area arather unique speckle pattern that remains relatively constantfrom one frame to the next. Therefore, a suitable pattern-

ed by Elsevier B.V. All rights reserved.

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matching algorithm can identify the frame-to-frame dis-placement of a speckle pattern, allowing myocardial motionto be followed in two dimensions.

This study sought to assess LV twist characteristics by STEin NCCM patients compared to patients with non-ischaemicdilated cardiomyopathy (DCM) and normal subjects.

2. Methods

2.1. Study participants

The study population consisted of 10 patients withNCCM (mean age 41±16 years, 6 men), 10 patients withDCM (mean age 47±13 years, 5 men), and 10 healthycontrols (mean age 43±8 years, 5 men) without hypertensionor diabetes, and with normal left atrial dimensions, LVdimensions, and LV function. Only subjects in sinus rhythmwith good two-dimensional image quality were enrolled.Informed consent was obtained from all subjects and theinstitutional review board approved the study.

2.2. Diagnostic criteria for NCCM and non-ischaemic DCM

NCCM patients strictly fulfilled all 4 echocardiographicdiagnostic criteria for NCCM according to Jenni et al. [8]:[1] absence of co-existing cardiac abnormalities (includingcoronary stenoses); [2] a 2-layered structure of the LV wall,with the end-systolic ratio of non-compacted to compactedlayer N2; [3] finding this structure predominantly in theapical and mid-ventricular areas; and [4] blood flow directlyfrom the ventricular cavity into the deep intertrabecularrecesses as assessed by Doppler and contrast echocardio-graphy [9]. Hypertensive heart disease was excluded byclinical and echocardiographic examinations (septal thick-ness b13 mm). DCM was characterized by ventricularchamber enlargement and systolic dysfunction, based oncurrent guidelines [10]. All NCCM and DCM patients hadundergone coronary angiography to exclude coronary arterydisease.

2.3. Echocardiography

Two-dimensional grayscale harmonic images at a framerate of 60 to 80 frames/s were obtained in the left lateraldecubitus position using a commercially available ultra-sound system (iE33, Philips, Best, The Netherlands),equipped with a broadband (1–5 MHz) S5-1 transducer(frequency transmitted 1.7 MHz, received 3.4 MHz).Measurements of LV dimensions, volumes, fractional short-ening, and ejection fraction were obtained in accordancewith the recommendations of the American Society ofEchocardiography [11]. According to the recommendationsof the American Heart Association on standardized myo-cardial segmentation and nomenclature for tomographicimaging of the heart, a 17-segment model was used for theassessment of regional LV wall motion [12]. Parasternal

short-axis images at the basal level (showing the tips of themitral valve leaflets), with the cross section as circular aspossible, were obtained from the standard parasternalwindow, in which the LV and aorta were most in-line withthe mitral valve tips in the middle of the sector. To obtain ashort-axis image at the apical level (just proximal to the levelwith LV luminal obliteration at the end-systolic period) thetransducer was positioned 1 or 2 intercostal spaces morecaudal as previously described by us [13]. From each short-axis image, three consecutive end-expiratory cardiac cycleswere acquired and transferred to a QLAB workstation(Philips, Best, The Netherlands) for off-line analysis.

2.4. Data analysis

Analysis of the datasets was performed using QLABAdvanced Quantification Software (version 6.0, Philips,Best, The Netherlands) that was recently validated againstMRI for assessment of LV twist by speckle tracking [14]. Toassess LV rotation, six tracking points were placed manually(after gain correction) on an end-diastolic frame in eachparasternal short-axis image on the midmyocardium. InNCCM patients the tracking points were placed in the innerto midsection of the compacted part of the muscle. Trackingpoints were separated about 60° from each other and placedon 1 (anteroseptal insertion into the LVof the right ventricle),3, 5, 7, 9 (inferoseptal insertion into the LV of the rightventricle) and 11 o'clock to fit the total LV circumference.LV rotation was estimated as the average angular displace-ment of all six tracking points relative to the center of a best-fit circle through the same tracking points. Rotation datawere exported to a spreadsheet program (Excel, MicrosoftCorporation, Redmond, WA) to determine LV peak rotationand time-to-peak LV rotation at the different short-axisplanes, instantaneous peak LV twist (apical LV peakrotation–basal LV peak rotation), and time-to-peak LVtwist. Counterclockwise rotation and twist as viewed fromthe apex was expressed as a positive value, clockwiserotation and twist was expressed as a negative value. Toadjust for intersubject differences in heart rate, the timesequence was normalized to a percentage of systolicduration. The end of systole was defined as the point ofaortic valve closure.

2.5. Statistical analysis

Continuous variables were presented as mean±SD, andtested for normality. Categorical data were expressed aspercentages. Variables were compared using the Student'st test, the Chi-square test or ANOVAwhen appropriate. A Pvalue b0.05 was considered statistically significant. To testthe intraobserver variability, measurements were repeated4 weeks apart by the same observer (BVD) on the sameechocardiographic loop for 10 randomly selected subjects.To test inter-observer variability, a second observer (MLG)who was unaware of the results of the first measurements,

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performed repeated measurements on the same randomlyselected subjects. Variability was calculated as the meanpercent error, derived as the absolute difference between thetwo sets of measurements, divided by the mean of themeasurements. Intra- and inter-observer variability for allparameters varied from 2.1% to 6.3% and 4.2% to 8.7%respectively.

3. Results

3.1. Subject characteristics

All clinical and traditional echocardiographic character-istics in controls, DCM and NCCM patients are shown inTable 1. Controls had a significantly shorter QRS duration,smaller LV dimensions and volumes, and higher LVfractional shortening and ejection fraction compared toNCCM and DCM patients. Regional wall motion wasnormal in all segments in controls (Pb0.001 vs. DCM andNCCM), none of the segments in DCM patients (Pb0.001vs. NCCM), and in 27% of the compacted, and 11% of thenon-compacted segments in patients with NCCM.

3.2. LV rotation in NCCM

In all controls and DCM patients, LV rotation wasclockwise at the basal level and counterclockwise at theapical level. In contrast, in all NCCM patients the LV base and

Table 1Characteristics of NCCM and DCM patients, and controls

NCCM DCM Controls

(n=10) (n=10) (n=10)

Clinical dataAge, years 41±16 47±13 43±8Men, n (%) 6 (60) 5 (50) 5 (50)QRS duration, ms 116±38 117±34 89±8*Bundle branch block(left/right/aspecific), n

2/0/1 3/0/0 0/0/0

Echocardiographic dataLV-EDD, mm 56±8 67±12 50±6*LV-ESD, mm 44±9 55±14 34±6*LV fractionalshortening, %

23±6 18±9 32±7*

LV-EDV, ml 152±52 167±55 115±23*LV-ESV, ml 92±43 117±44 44±15 †LV ejectionfraction, %

38±13 30±9 62±7 †

Regional wall motion Compacted Non-compactedSegments, n (%) 94 (55) 76 (45) 170 (100) 170 (100)Normal, n (%) 25 (27) †† 8 (11) †† 0 (0) 170 (100) ‡Hypokinesis, n (%) 49 (52) 46 (61) 100 (59) 0 (0) ‡Akinesis, n (%) 20 (21)** 18 (24)** 64 (38) 0 (0) ‡Dyskinesis, n (%) 0 (0) 4 (5) 6 (3) 0 (0)

Data are presented as mean±SD. NCCM=non-compaction cardiomyo-pathy, DCM=dilated cardiomyopathy, LV=left ventricular, EDD=end-diastolic dimension, ESD=end-systolic dimension, EDV=end-diastolicvolume, ESV=end-systolic volume. *Pb0.05, †Pb0.01, ‡Pb0.001 vs.NCCM and DCM, **Pb0.05, ††Pb0.001 vs. DCM.

Fig. 1. Basal and apical left ventricular rotation in controls (upper), dilatedcardiomyopathy (middle), and non-compaction cardiomyopathy (lower).

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apex rotated in the same direction. The LV rotated as a solidbody in a clockwise direction in 7 NCCM patients, and in acounterclockwise direction in 3 NCCM patients (Fig. 1). LVbasal rotation (−2.7°±1.1° vs. −3.6°±2.0° vs. −3.5°±1.0°,P=NS) was comparable in controls, DCM patients, and the7 NCCM patients with clockwise solid body rotation. In the 3NCCM patients with counterclockwise solid body rotation,LV basal rotation (3.4°±1.8°) was significantly different fromLV basal rotation in controls and DCM patients (bothPb0.001). LV apical rotation was significantly lower in bothNCCM patients with clockwise (−2.5°±1.1°, Pb0.001) andcounterclockwise (4.2°±1.0°, Pb0.05) solid body rotation,

Table 2Left ventricular rotation and twist in NCCM and DCM patients, and controls

NCCM (n=10) DCM (n=10) Controls (n=10)

Clockwise Counterclockwise

LV rotation n nBasal, degrees −3.5±1.0 7 3.4±1.8††‡ 3 −3.6±2.0 −2.7±1.1Apical, degrees −2.5±1.1††‡ 7 4.2±1.0** 3 2.6±1.4‡ 7.2±2.0

LV twist, degrees −2.0±0.9*† 2 2.5±1.0*‡ 8 5.4±2.5** 9.4±3.7Time-to-peak LV rotation

Basal, % 82±28 83±30 91±18 89±19Apical, % 93±29 93±30 89±23 94±8

Time-to-peak LV twist, % 94±12 97±15 93±17 93±5

Data presented as mean±SD. Time-to-peak LV rotation and time-to-peak LV twist as a percentage of duration of systole. Abbreviations are as in Table 1.*Pb0.01, ††Pb0.001 vs. DCM, **Pb0.05, †Pb0.01, ‡Pb0.001 vs. controls.

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and DCM patients (2.6°±1.4°, Pb0.001) as compared tocontrols (7.2°±2.0°). There were no differences in basal andapical time-to-peak rotation between controls, DCM, andNCCM (Table 2). Typical examples of rotation–time curves incontrols, DCM and NCCM are shown in Fig. 2.

3.3. LV twist in NCCM

Even though rotation at the basal and apical level was inthe same direction in NCCM, there was still a smallinstantaneous LV twist because of differences in the degreeand timing of peak rotation at the LV basal and apical level.Nevertheless, LV twist in both the NCCM patients withclockwise (−2.0°±0.9°) and counterclockwise solid bodyrotation (2.5°±1.0°) was significantly lower compared toDCM patients (5.4°±2.5°, both Pb0.01) and controls(9.4°±3.7°, Pb0.001 and b0.01, respectively).

3.4. Counterclockwise vs. clockwise rotation in NCCM

No significant differences in clinical or traditionalechocardiographic data between NCCM patients with LVrotation in a clockwise or counterclockwise direction couldbe identified, although patients with counterclockwise LVrotation tended to have a shorter QRS duration (90±12ms vs.127±41 ms). In both NCCM patients with a left bundlebranch block and the NCCM patient with aspecificintraventricular conduction delay, solid body rotation wasin a clockwise direction.

4. Discussion

The main findings of our study are 1) in patients withDCM LV basal rotation is clockwise and LVapical rotation iscounterclockwise as in normal controls but LVapical rotationis of a lesser magnitude (LV twist is less), and 2) in NCCMpatients LVapical rotation is also of a lesser magnitude but incontrast to normal controls and DCM, LV basal and LVapical rotation are in the same direction (‘LV solid bodyrotation’). The development of the myocardial architectureof the heart wall passes through several distinct steps [15]. Inthe early tubular heart, the myocardium has an epithelial

nature with just a few layers of cells. The next step is thecavity-specific formation of sheet-like myocardial protru-sions into the lumen, so-called trabeculations. These earlytrabeculations effectively increase the myocardial surfacearea, enabling the myocardial mass to increase in the absenceof a coronary circulation. Currently, there is no consensus onwhat happens to this trabecular layer. Although some statethat the trabeculations become compacted to form thecompact wall of the ventricular mass [15], others claimthat this is most unlikely [16], supported by a lack of prooffor the former theory. Anyway, the final stage of thedevelopment of myocardial architecture is characterized bythe development of a multilayered spiral system in the compactmyocardium, coinciding with invasion of the coronaryvascular system from the epicardium [3,4]. The differentlayers of the spiral system can be revealed by the techniqueof peeling. It can be seen that there is an ordered structurefor the ventricular mass, albeit that the aggregated myocytesdo not form clearly separable fibres, nor are the layersisolated by supporting scaffolds of connective tissue [17].In the matured heart, the ventricular mass is arranged inthe form of a modified blood vessel, with each myocyteanchored to its neighbor within a three-dimensionalmyocardial mesh [18]. Streeter et al. [19] introduced themyocyte helix angle, representing the angle betweenthe myocytes, as projected onto the circumferential–longitudinal plane, and the circumferential axis. Themyocyte helix angle changes continuously from thesubendocardium to the subepicardium, typically rangingfrom +60° at the subendocardium to −60° at thesubepicardium [20]. LV twist originates from the dynamicinteraction between the oppositely wound subepicardial andsubendocardial myocyte helices [21]. Furthermore, trans-mural oriented myocytes may be necessary to ensurestability of the shape of the ventricular walls throughoutthis twisting deformation [17]. The direction of LV twist isgoverned by the epicardial myocytes, mainly owing to theirlonger arm of movement [22]. Mathematical models haveshown that this counterdirectional helical arrangement ofmuscle fibres in the heart is energetically efficient and isimportant for equal redistribution of stresses and strain inthe heart [23]. NCCM is a heterogeneous disorder probably

Fig. 2. Typical examples of rotation–time curves during one completecardiac cycle in controls (upper), dilated cardiomyopathy (middle), and non-compaction cardiomyopathy (lower).

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caused by intra-uterine arrest of compaction of themyocardialfibres during embryogenesis [5]. Due to this arrest ofmyocardial compaction it may be anticipated that the

characteristic spiral helix will also not develop. Absence ofthe endocardial helix would lead to increased clockwise basaland counterclockwise apical LV rotation, due to loss of thecounteracting activity. On the other hand, absence of theepicardial helix would lead to counterclockwise basal andclockwise apical LV rotation. Therefore, based on our results,the assumption has to be made that both helices must beinvolved to a similar extent in NCCM. LV solid body rotationwith near absent LV twist may be one of themainmechanismsof impaired LV function in NCCM patients. In healthyneonates with an immature heart LV solid body rotation hasalso been described with basal and apical rotation being in acounterclockwise direction [24]. Why some of our patientsshow clockwise and others counterclockwise LV solid bodyrotation remains unclear at this moment. Nevertheless, it isstriking that all patients who showed the neonatal form of LVsolid body (counterclockwise) rotation had no evidence forabnormal LV conduction, evidenced by a normal QRSduration. At present, there is no consensus on how to preciselydefine NCCM. Recently, Kohli et al. [25] studied 199 patientsreferred to a dedicated heart failure clinic. There was anunexpectedly high percentage of patients that could beidentified as having NCCM: 23.6% of the patients fulfilledone or more of the echocardiographic criteria currentlyused for the identification of NCCM [8,26,27]. This highpercentage suggests that current diagnostic criteria may be toosensitive. Furthermore, there was a poor correlation betweenthe echocardiographic definitions, with only 29.8% of theidentified NCCM patients fulfilling all three criteria. Wepropose ‘LV solid body rotation’ as a new sensitive andspecific, objective and quantitative, functional criterion,supplementing the classic subjective morphologic NCCMcriteria [8,26,27]. It should be noticed that others, in contrastto our findings, have occasionally described LV solid bodyrotation in DCM patients [28]. Although it cannot beexcluded that in these patients the diagnosis NCCM wasoverlooked, the true specificity of LV solid body rotation forthe diagnosis of NCCM may be lower than that in our study.Other studies should confirm our data before this newcriterion should be used clinically.

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