| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Eur J Cardiothorac Surg 2006;29:S165-S177
© 2006 Elsevier Science NL
a Option on Bioengineering, California Institute of Technology, Pasadena, CA, USA
b Department of Anesthesiology, David Geffen School of Medicine at UCLA, Los Angeles, CA, USA
c Department of Surgery, Division of Cardiothoracic Surgery, David Geffen School of Medicine at UCLA, 10833 Le Conte Avenue, 62-258 CHS, Los Angeles, CA 90095-1741, USA
d Department of Diagnostic Radiology, University Hospital Freiburg, Germany
e Hospital de Mataro, Barcelona, Spain
Received 22 February 2006; accepted 27 February 2006.
* Corresponding author. Tel.: +1 310 206 1027; fax: +1 310 825 5895. (Email: gbuckberg{at}mednet.ucla.edu).
 |
Abstract |
|---|
 Top Abstract 1. Introduction2. Methods3. Results4. Discussion5. ConclusionsAppendix AReferences |
|---|
Key Words: MRI myocardial motion • Fiber tracking • Helical ventricular myocardial band • Echocardiography • Sonomicrometer crystals • Radionuclide ventriculography • Corrosion casts • Isovolumic contraction
|
1. Introduction |
|---|
|
TopAbstract1. Introduction2. Methods3. Results4. Discussion5. ConclusionsAppendix AReferences |
|---|
The dynamics of cardiac action become evident from MRI recordings [2], a tool that also implies structural fiber orientation by generating acceleration fiber tracking [3]. These MRI recordings demonstrate the rotational motions of twisting and longitudinal motion that underlie the narrowing, shortening, lengthening, and widening motions performed by the normal ventricular chamber [4]. Each dominant motion component responsible for cardiac mechanics during isometric contraction, systole during ejection, the isovolumetric phase for rapid filling, and diastole must evolve myocardial fiber orientation exerts its dynamic action on left ventricular performance. There must be a clear structural basis for what we see, thereby creating the structure/function relationship.
This report will define results from analysis of normal myocardial motion by means of functional magnetic resonance imaging (MRI) in the context of dominate motion components during different phases of the cardiac cycle and myocardial fiber tracking, and compare these findings with other phasic measurements of cardiac activity made by ultrasonic sonomicrometer crystals [5], echocardiography, radionuclide ventriculography tracings [6], and determine if a structure/function relationship can be linked to spatial orientation of the helical ventricular myocardial band [7].
These results will demonstrate a close relationship between MRI resolution of myocardial motion and fiber tracking with these other technologies during each phase of the cardiac cycle. The integration of these techniques with the helical heart ventricular band model identifies structural reasons for the sequential dynamics responsible for global functional events, that include (a) ‘cocking’ of the heart during isometric contraction, (b) ‘co-contraction’ during shortening during ejection, and (c) a muscular reason for reciprocal twisting and lengthening during the isovolumetric contraction (IVC) during rapid ventricular filling, a phase previously thought of as IVR or isovolumetric relaxation.
The close agreement amongst a spectrum of imaging studies provides a very powerful integration that transcends a single look by any one imaging modality, since each component of global technology sees the same thing. These findings imply that the helical ventricular band is the infrastructure for the global functional changes observed by MRI and other technologies.
|
2. Methods |
|---|
|
TopAbstract1. Introduction2. Methods3. Results4. Discussion5. ConclusionsAppendix AReferences |
|---|
The spatial structure of the helical ventricular myocardial band was employed to determine if the MRI and the other functional tests had correlation to this configuration (Fig. 1 ). Unfolding of this band configuration shows that the heart comprises two loops that include a wrap around basal loop composed of a right and left ventricular segment that contains transverse fibers and acts like a buttress that surrounds the underlying oblique apical loop. The apical loop has a helical configuration and is constructed from the oblique fibers of the descending and ascending segments that have a crisscross fiber orientation arrangement that forms a vortex at the left ventricular apex.
|
We systematically describe our observations of cardiac motion using transesophageal echocardiography (TEE) in humans. Various imaging modes including strain-, tissue velocity-, m-mode and two-dimensional echocardiography have been utilized in standard TEE views to validate the motion in the helical heart. Left ventricular velocities and motion are measured in reference to transducer at the apex of the sector scan.
This echocardiographic approach defined the four phases of motion including narrowing, shortening, lengthening, and widening during the cardiac cycle, to complement information gained from other imaging techniques like MRI (twisting), radionuclide ventriculography (endocardial motion on ventricular blood pool), and sonomicrometer crystals that show only regional shortening between pairs of crystals, but cannot distinguish quantify twisting, transmural thickening, shortening or lengthening of the chamber. The interaction of this broad spectrum of imaging methods may improve understanding of how the underlying model of cardiac structure determines the sequences of cardiac motion they measure.
|
3. Results |
|---|
|
TopAbstract1. Introduction2. Methods3. Results4. Discussion5. ConclusionsAppendix AReferences |
|---|
|
320 ms, and this interval is used to describe the end point from normalized data to provide a clearer time frame, rather than using the 13.8 ms intervals. Before evaluation of these three slice motions, Fig. 4
a–c define each of the three individual motions of radial velocity of contraction/expansion, tangential velocity of rotation (twisting), and longitudinal velocity of motion (shortening/lengthening) evaluated within these three slices.
|
|
Tangential motion (twisting) is displayed in Fig. 4b, and shows that initially, all segments move counter-clockwise during the isometric phase. However, throughout systole (the time frame the radial tracing velocities are above the zero line), the basal slice develops a clockwise motion, while the apex continues a counter-clockwise motion. These MRI components thereby compliment the twisting motion seen in Video 1 in http://www.ejcts.ctsnetjournals.org/cgi/content/full/27/2/202/DC1 and Fig. 2. Apical and mid-wall regions’ tangential motion begins to reverse direction during the later phases of systole at the isovolumic interval just before rapid filling. Consequently, there was initiation of a reversal toward a clockwise motion during the ongoing thickening that is evident by contraction shown in Fig. 4a, demonstrating values above the zero line.
The longitudinal velocity of shortening exists in the base and mid-wall, as values are above the zero line, during this systolic phase that extends to 320 ms. There is negligible apical motion during this systolic time frame, thus codifying movement of the base toward the apex during systole. This downward motion of the base toward the apex is further amplified by the echo tracings described below.
Mean radial velocity of expansion (lack of contraction) occurs after the 320 ms time frame, accompanied by a reversal of the tangential (twisting) velocity, so that the base proceeds clockwise and apex counter-clockwise, and the longitudinal velocities display lengthening (values below the zero baseline), with two distinct peaks appearing during subsequent diastole. Fig. 5 displays the radial velocity of thickening owing to contraction, and documents ongoing thickness during and just beyond the isovolumetric phase at the end of systole. The temporal axis was normalized to end systole in order to avoid temporal jitter owing to different heart rates.
|
Fig. 6 shows three-dimensional identification of acceleration tracks at these four different cardiac frames, and displays a smooth coverage of the entire LV for the cardiac frame during isovolumetric contraction (IVC) (a). The oblique angulation, from base to apex, shown during mid-systole (b) conforms to the oblique fiber orientation of the descending segment of the helical myocardial band (Fig. 7 ), the angulation of the ultrasonic crystals used previously to show maximum force of shortening during ejection (Fig. 8 ), and the spiral trabeculae that compress blood within the LV cavity in corrosion casts, prepared by Gorodkov et al. [8] (Fig. 9 ).
|
|
|
|
|
|
|
|
|
|
|
|
|
4. Discussion |
|---|
|
TopAbstract1. Introduction2. Methods3. Results4. Discussion5. ConclusionsAppendix AReferences |
|---|
The characteristic global movements documented by TPM velocity recordings during the cardiac cycle have traditionally been evident by echocardiography and ventriculogram, and include narrowing during the isometric phase of contraction, shortening during ejection, lengthening during the isovolumetric phase of rapid lengthening in preparation for rapid filling, and widening as passive ventricular filling occurs. Patterning of these findings with other imaging modalities, by using the model of the helical ventricular myocardial band gave insight into the structural reasons for global and regional motion dynamics defined by these imaging tools.
The tangential motions of twisting during TPM velocity recordings with also evident in the whole heart in Video 1 in http://www.ejcts.ctsnetjournals.org/cgi/content/full/27/2/202/DC1 and have been observed by tagging MRI studies [4]. The movements include counter-clockwise twisting during the isometric phase, torsion during ejection characterized by clockwise twisting of the base and counter-clockwise twisting of the apex, a reversal of this pattern in the apex during the isovolumetric phase before rapid ventricular filling, and continuance of this into early diastole. Similar reciprocal twisting of the walls was also previously reported by the DENSE studies of MRI motion obtained at the NIH by Wen (see Video 2 in http://www.ejcts.ctsnetjournals.org/cgi/content/full/27/2/202/DC1). These motions are related to actions of the underlying muscle, and correlation between these MRI measurements and motion by other collective imaging modalities was closely interfaced with the spatial structure of the myocardial band.
Isolated focus was not the purpose of this study although clear correlation of phases of individual TPM measurements with DTI measurements was evident, such as the brief small biphasic wave during isovolumetric relaxation. Rather, the intent was to try to match sequential TPM measurements and myocardial fiber tracking during the aforementioned four phases of cardiac movement during the cardiac cycle, together with associated twisting movements to determine if a structure/function relationship existed in relationship to the myocardial band.
4.1 Isometric contraction
The counter-clockwise twisting during the early isovolumetric phase of systole was reported by Lorenz et al. [4], and the correlation with other functional measurements defined a muscular cause of this movement. Narrowing of the chamber was evident by the TMP radial velocities of thickening, as well as by constriction of the mitral ring by echocardiogram [14]. This phase exists before ejection has been termed as ‘cocking’ of the chamber and before the downward motion during ventricular systole [15].
The mechanisms of this ‘cocking’ action are suggested by (a) a sequential shortening of the right, then the left segments of the basal loop by ultrasonic crystals, and (b) evidence of endocardial motion by radionuclide ventriculography that begins in the right segment and proceeds to the left segment of the basal loop of the myocardial band [6,16]. These motions suggest that the heart is pulled in a counter-clockwise direction by the right to left sequence of movement. A similar motion of the base, whereby the right segment pulled the left in a counter-clockwise movement was also reported in 1961 [17] by Coghlan who used simultaneous pressure derivative analysis of all chambers and great vessels. Furthermore, preliminary strain recordings by DENSE MRI methodology (see Video 4 in http://www.ejcts.ctsnetjournals.org/cgi/content/full/27/2/202/DC1) show sequential development of strain in the base of the heart before a spiral motion toward the apex. The counter-clockwise twisting, coupled with simultaneous narrowing of the mitral annulus during the isometric phase provided a muscular cause that is related to sequential movement of the basal loop. This motion explains the 28% compression of the mitral annulus in man during the pre-ejection phase on two-dimensional echocardiography previously reported by Ormiston et al. [14].
There is no longitudinal motion of ventricular shortening during this isometric interval, as the septum and lateral wall do not move downward toward the apex, so that the recorded endocardial shortening by sonomicrometer crystals does not contain the transmural component needed to generate global shortening. This longitudinal motion would be evident by echocardiogram and MRI but did not occur. Simultaneously, demonstration of positive strain in the septum by echocardiography, clarified the validity of endocardial shortening findings by sonomicrometer crystals.
The m-mode echocardiogram showed the septum slightly lengthened during this isometric phase. The upward motion of the septum during isometric contraction seems, at first, to reflect a paradoxical movement because the endocardium of the apical loop is simultaneously contracting and would be expected to shorten. However, the absence of shortening by echocardiogram and ongoing circumferential compression by the contracting basal loop implies that only the endocardial region of the septum is shortening, rather than the full wall. The apical loop narrows during its compression by a basal loop contraction, signifying that the basal loop is the dominant force, despite sonomicrometer evidence of descending segment (endocardial) contraction in the septum and the free wall and septum. The incompletely contracting septum is raised cephalad during the isometric phase of systole, and is associated with billowing of the closed mitral valve into the atrium.
4.2 Ejection
The phase of ejection is documented by thickening and shortening by TMP measurement and was accompanied by clockwise twisting of the base and counter-clockwise twisting of the apex. Longitudinal shortening was documented by echocardiogram and co-contraction of both the descending and ascending segments of the apical loop of the ventricular band was confirmed by ultrasonic crystal recordings.
The crystals were placed in a crisscross manner to obtain the maximal force of shortening, and the change of the slope during ejection implies that the counterforce of ascending shortening in a different or upward direction during co-contraction may explain the less steep slope of the sonomicrometer crystal tracing during this phase of ejection, as seen in Fig. 8.
Reciprocal twisting of the ventricle occurs during longitudinal shortening during ejection, and co-contraction of the ascending and descending segments of the apical segment of the myocardial band maximize the rate of shortening. Studies by Gorodkov et al. [8] document how the oblique spiral architecture compresses the corrosion cast (reflecting blood within the LV cavity), and we suspect the predominant power resides in the descending segment (Fig. 7) which becomes dominant during this ejection time period, despite epicardial ascending segment shortening and thickening.
4.3 Isovolumetric phase before rapid filling
The isovolumetric phase initiates before rapid filling (preciously considered isovolumic relaxation (IVR)), and the apex performs a clockwise rotation, whereas basal and mid-ventricular locations show early expansion in the anteroseptal and anterior regions with simultaneous (mild) clockwise rotation. The initiation of these clockwise movements occurs while radial velocity demonstrates ongoing contraction (Fig. 4a–c), so that the beginning of clockwise motion precedes the start of the lengthening motion. The descending segment stops shortening, but ascending segment shortening continues (Fig. 8).
Contraction itself seems to be responsible for this twisting motion, because systole exists and strain is observed in the septum and lateral wall by echocardiogram during the lengthening motion that occurs prior to rapid ventricular filling. The concept of systolic ventricular filling was previously suggested [18,7,19] and differs from prior suggestions that stored potential energy [20] from preceding systole (which is still occurring), collagen [21,22], of titin [22] can explain the tangential twisting motion that exists before rapid filling. The mitral valve opens during this lengthening time frame that the heart undergoes reciprocal twisting [13], and perhaps the active rapid reciprocal twisting of the apex will uncross the papillary muscles to open the valve leaflets.
The reciprocal clockwise shortening and twisting of the ascending segment [18] produces an upward cardiac lengthening on echocardiography (that also shows strain during this phase), and reflects the epicardial ascending segments predominating action during ongoing lengthening; no contraction occurs in the endocardium (descending segment) or basal loop segments during this interval. The unbridled ascending segment reciprocally twists to set the frame work for suction as LV pressure falls below atrial pressure to allow rapid filling.
There is no counterforce or co-shortening from the descending segment during this time interval of reciprocal twisting. Simultaneous widening of the base of the heart is evident by expansion on TMP velocity recordings, and greater distance between paired sonomicrometer crystals in the basal segments [5,2]. Such expansion prepares the ventricular cavity for rapid filling that occurs when suction is generated by the twisting ascending segment muscular contractile effort.
We had suspected [18,23] that although the active contraction of the descending segment has ceased, this region maintains muscular tone to retain its action as a fulcrum during the lengthening following the clockwise rotation and twist from the ascending segment; this concept is supported by persistent thickness observed by MRI imaging. Left ventricular chamber filling becomes passive after active shortening (crystals) or thickening (MRI) stops in all segments.
These findings of motion by echocardiography, MRI, and sonomicrometer crystals imply that the term isovolumic contraction (IVC) should replace isovolumic relaxation, because thickening, active shortening, and strain occur at a time phase previously thought of as relaxation. These observations thus challenge the concept of systole as contraction and diastole as relaxation, which is considered to begin at the junction of the dichrotic notch of the aortic and left ventricular pressure curves.
Our findings show that a longer systolic interval exits during the period previously called isovolumetric relaxation, and results from ascending segment shortening and twisting motion. The MRI velocity analysis (Fig. 4a–c) indicates a period of ongoing muscular contraction and ventricular compression exists as the twisting for rapid filling develops. Consequently, this muscular phase of prolonged systole, or ventricular systolic filling [19,18] underscores the mechanisms for the deceleration of the LV pressure, negative dP/dt and contractile component of rapid filling, and might expand the understanding of diastolic dysfunction and its potential treatment.
4.4 Diastole
Active contraction by radial velocity has stopped, and longitudinal lengthening is evident by TMP measurement, as well as by echocardiography. However, there is a biphasic wave observed, as with TDI recordings (Fig. 16), as well as an early continuation of the clockwise twisting of the apex and reciprocal twisting of the base to continue torsion. These movements are an active muscular phenomena that augments suction for rapid filling when ventricular pressure falls below atrial pressure. Passive filling from differences in pressures between the atrium and ventricle develops later during the diastolic interval. Shapiro et al. [24] and Rademakers et al. [25] used tagging MRI studies to demonstrate that rapid reciprocal twisting is responsible for 50% of diastolic filling in the normal heart, and becomes augmented to 60% by inotropic drugs to emphasize the muscular aspect of the suction process.
4.5 Fiber orientation
These composite observations from several imaging sources imply that the acquisition of three-directional velocity data over the entire left ventricle provide velocity fields must be related to the myocardial fiber structure. While measured velocity direction may deviate from the structural fiber orientation, this velocity is thought to relate to structural fiber orientation [3]. The implication that more diagonal arrangement of muscle fibers may lead to more efficient cardiac output, is supported by sonomicrometer crystals studies that show the dominant fiber direction of the ascending and descending segments of the ventricular myocardial band exist in this fashion, as shown in Figs. 9 and 10. However, focal crystals are placed upon only the muscle surface, but their motions were considered to reflect movement generated by the overlying cross-striated fibers [5]; the TPM dataset demonstrates this net effect by velocity measurements.
Comparison of velocity-based evaluation with postmortem structural evaluation is needed to determine how generated velocity fibers conform with the structural fiber orientation. An aspect of this interaction is shown in Figs. 9–11, whereby the velocity-based evaluation during both mid-systole, isovolumic phase before rapid filling and mid-diastole show close correlation with corrosion casts used to substitute for cavity blood [8] or helical ventricular myocardial band anatomy. There is similarity between accelerated velocity by MRI, spiral trabeculae of endocardial muscle and myocardial band.
The constraint of deriving structural fiber information from dynamic velocity data is due to limitations from observing that only net effects within each voxel, so that sophisticated dynamic modelling is needed. These data cannot detect resultant force direction from interwoven fiber pathways of different orientation because this velocity acceleration cannot identify such crisscross tissue types that impact this force. This concept of resultant force is, however, also implied by prior ultrasonic crystal measurements [5], whereby the crystals are placed into the angulation of the presumed functional units of the descending and ascending segments of the apical loop of the helical ventricular myocardial band. Correlation of anatomic fiber orientation and the motion characteristics during MRI examination may exist, as suggested in Fig. 8 (ultrasonic crystals) and from Figs. 9 and 10 that correlate TPM velocity acceleration tracts of fiber orientation during systole when the chamber shortens during ejection and lengthens during the isovolumetric phase before rapid filling.
The close interaction of these surrogate MRI parameters during the four phases of motion during the cardiac cycle, together with acceleration velocities for myocardial fiber tracking suggests that these MRI measurements may link with cardiac structure of models like the helical ventricular myocardial band. The correlation of these presumptions with evidence of how the spiral endocardial fibers impacts intracavitary blood by the corrosion cast method [26] expands this interaction, together with support by other imaging modalities like ultrasonic crystals, echocardiography, and radionuclide ventriculography studies.
|
5. Conclusions |
|---|
|
TopAbstract1. Introduction2. Methods3. Results4. Discussion5. ConclusionsAppendix AReferences |
|---|
Of greater importance, the close agreement amongst a spectrum of imaging studies provides a very powerful integration that transcends a single look by any one imaging modality. The integrated global technology of function sees the same thing that evolves from underlying spatial architecture. The collaboration of these different imaging methods provides novel explanations to answer questions posed and unanswered by individual imaging tools. These pooled imaging findings imply that the helical ventricular band is the structural basis for the global functional changes observed by MRI and other technologies.
|
Appendix A |
|---|
|
TopAbstract1. Introduction2. Methods3. Results4. Discussion5. ConclusionsAppendix AReferences |
|---|
Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.ejcts.2006.02.064.
|
References |
|---|
|
TopAbstract1. Introduction2. Methods3. Results4. Discussion5. ConclusionsAppendix AReferences |
|---|
This article has been cited by other articles:
|
|
 |
|
  J.-O. Choi, S. W. Cho, Y. B. Song, S. J. Cho, B. G. Song, S.-C. Lee, and S. W. Park Longitudinal 2D strain at rest predicts the presence of left main and three vessel coronary artery disease in patients without regional wall motion abnormality Eur J Echocardiogr, July 1, 2009; 10(5): 695 - 701. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H.-Y. Yu, Y.-S. Chen, W.-Y. Tseng, N.-S. Chi, C.-H. Wang, S.-S. Wang, and F.-Y. Lin Why is the surgical ventricular restoration operation effective for ischemic cardiomyopathy? Geometric analysis with magnetic resonance imaging of changes in regional ventricular function after surgical ventricular restoration J. Thorac. Cardiovasc. Surg., April 1, 2009; 137(4): 887 - 894. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. Buckberg, J. I.E. Hoffman, A. Mahajan, S. Saleh, and C. Coghlan Cardiac Mechanics Revisited: The Relationship of Cardiac Architecture to Ventricular Function Circulation, December 9, 2008; 118(24): 2571 - 2587. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. E. Stelzer, H. S. Norman, P. P. Chen, J. R. Patel, and R. L. Moss Transmural variation in myosin heavy chain isoform expression modulates the timing of myocardial force generation in porcine left ventricle J. Physiol., November 1, 2008; 586(21): 5203 - 5214. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. E. Stelzer, J. R. Patel, J. W. Walker, and R. L. Moss Differential Roles of Cardiac Myosin-Binding Protein C and Cardiac Troponin I in the Myofibrillar Force Responses to Protein Kinase A Phosphorylation Circ. Res., August 31, 2007; 101(5): 503 - 511. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Carlsson, M. Ugander, H. Mosen, T. Buhre, and H. Arheden Atrioventricular plane displacement is the major contributor to left ventricular pumping in healthy adults, athletes, and patients with dilated cardiomyopathy Am J Physiol Heart Circ Physiol, March 1, 2007; 292(3): H1452 - H1459. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E. Stelzer, S. L. Brickson, M. R. Locher, and R. L. Moss Role of myosin heavy chain composition in the stretch activation response of rat myocardium J. Physiol., February 15, 2007; 579(1): 161 - 173. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E. Stelzer, J. R. Patel, and R. L. Moss Protein Kinase A-Mediated Acceleration of the Stretch Activation Response in Murine Skinned Myocardium Is Eliminated by Ablation of cMyBP-C Circ. Res., October 13, 2006; 99(8): 884 - 890. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. E. Stelzer and R. L. Moss Contributions of Stretch Activation to Length-dependent Contraction in Murine Myocardium J. Gen. Physiol., October 1, 2006; 128(4): 461 - 471. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E. Stelzer, J. R. Patel, and R. L. Moss Acceleration of Stretch Activation in Murine Myocardium due to Phosphorylation of Myosin Regulatory Light Chain J. Gen. Physiol., August 28, 2006; 128(3): 261 - 272. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. D. Buckberg, M. Castella, M. Gharib, and S. Saleh Active myocyte shortening during the 'isovolumetric relaxation' phase of diastole is responsible for ventricular suction; 'systolic ventricular filling' Eur. J. Cardiothorac. Surg., April 1, 2006; 29(Suppl_1): S98 - S106. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ANN THORAC SURG | ASIAN CARDIOVASC THORAC ANN | EUR J CARDIOTHORAC SURG |
| J THORAC CARDIOVASC SURG | ICVTS | ALL CTSNet JOURNALS |
