Author + information
- Received October 29, 2007
- Revision received December 17, 2007
- Accepted January 26, 2008
- Published online July 1, 2008.
- Gösta B. Pettersson, MD, PhD⁎,⁎ (, )
- Adrian C. Crucean, MD⁎,
- Robert Savage, MD, FACC†,
- Carmel M. Halley, MD‡,
- Richard A. Grimm, DO, FACC‡,
- Lars G. Svensson, MD, PhD, FACC⁎,
- Sepehre Naficy, MD⁎,
- A. Marc Gillinov, MD, FACC⁎,
- Jingyuan Feng, MS§ and
- Eugene H. Blackstone, MD, FACC⁎,§
- ↵⁎Reprint requests and correspondence:
Dr. Gösta B. Pettersson, Department of Thoracic and Cardiovascular Surgery, Cleveland Clinic, 9500 Euclid Avenue/Desk F24, Cleveland, Ohio 44195.
Objectives Our purpose was to investigate a new approach to bicommissural repair of regurgitant aortic valves.
Background Repair of regurgitant aortic valves is not widely accepted, but interest is increasing, particularly for bicuspid valves. We hypothesize that a systematic, segmental approach to morphology and corresponding morphology-directed repair will improve decision making and success.
Methods From December 2001 to July 2007, a systematic surgical approach to valve analysis and bicommissural repair was applied prospectively to 63 consecutive patients with pure aortic valve regurgitation, mean age 40 ± 12 years. Cusp, commissure, and root morphologies were analyzed sequentially by direct inspection. Each abnormality was corrected by corresponding morphology-directed repair procedures. Retrospectively, 2 echocardiographic indexes—of tissue pliability (change in systolic to diastolic area) and coaptation deficiency (conjoint and reference cusp heights vs. “annulus” diameter)—were developed to evaluate repairability.
Results Forty-two (67%) valves were repaired and 21 (33%) replaced. Regurgitation was related primarily to cusp (prolapse, restriction) and commissure (splaying) morphology; root pathology was less important. Morphology-directed repair included cusp maneuvers in all, commissural maneuvers in 71%, and root procedures in 33%. Restriction and cusp tissue deficiency limited repairability. Echocardiography reflected this in greater tissue pliability of successfully repaired valves compared with replaced ones (conjoint cusp 61 ± 16% vs. 34 ± 17%; reference cusp 65 ± 16% vs. 42 ± 16%; p = 0.0001) and less coaptation deficiency (1.06 ± 0.24 for repaired and 1.27 ± 0.19 for replaced valves; p = 0.002).
Conclusions Systematic segmental analysis of morphology and a logical morphology-directed surgical approach facilitate aortic valve repair. Initial application of this paradigm suggests sufficient mobile cusp tissue is a key determinant of repairability.
Fifteen percent to 20% of patients with bicuspid aortic valves present as young or middle-aged adults with important aortic regurgitation (AR) (1,2). Unattractiveness of aortic valve replacement has stimulated interest in repairing such valves (3–10). However, little information is available about repairability, durability, and post-repair gradients. Further, focus has centered on repairing “prolapsing” cusps (11), but the concept of prolapse does not fully cover the morphologic complexity associated with AR.
Although aortic valves are morphologically classified by number of cusps, they could be equally well or better defined by number of open commissures. Unicuspid and bicuspid morphology (1 or 2 open commissures, respectively) is less optimal than tricuspid morphology (3 open commissures) (12–14), but the majority of bicuspid valves function well for life (1,2,15). This natural history indicates their potential for durability and justifies bicommissural repair.
Recently, we described important echocardiographic clues regarding bicuspid valve repairability (16); yet, in that study, only 57% of valves were successfully repaired. Therefore, a segmental morphology-specific approach to bicommissural aortic valve repair was devised and applied prospectively to unicuspid and bicuspid aortic valves. Our objectives were to describe in a systematic way the surgical morphology encountered and corresponding morphology-directed repairs, judge repairability and success of repair, and assess repair quality and durability. By retrospectively reviewing morphologic-echocardiographic correlations of successful repair, we hoped to identify new predictors of repairability.
Aortic valve morphology: concepts and definitions
Typical unicuspid valves have an eccentric opening and a common horseshoe-shaped cusp with 1 open commissure and 2 fused remnants of commissures with or without raphes, and a rudimentary cusp in between (Table 1). A few have only a central opening and no well-defined open commissure (17–19).
Bicuspid valves may have 2 symmetric cusps separated by 2 normal commissures, with horizontal orientation the most frequent; these are considered herein as true bicuspid valves. Most often, however, the 2 cusps have different morphology: the first is normal looking, herein referred to as the reference cusp; the second is seemingly made up of 2 cusps separated by a partially or completely fused commissure (most often right and left cusp fusion), herein referred to as the conjoint cusp. A bicuspid valve has 2 open commissures, justifying the concept of a bicommissural valve. If not a true bicuspid valve, the third fused commissure is marked by a raphe of varying development and a cleft if fusion is incomplete. The second cusp can be any size relative to the reference cusp, ranging from close to 1:1 for good, true bicuspid valves to 2:1 when a conjoint cusp is seemingly composed of 2 normal-sized cusps.
Prolapse is an important concept used in describing morphology of regurgitant valves, particularly repairable cusps (20). It means that a cusp's free margin falls below the line of coaptation, preventing diastolic closure. Effective height, a relative measure of prolapse, is a recently introduced concept (21). The opposite of prolapse is restriction. When describing a partially fused conjoint cusp, however, prolapse and restriction are difficult to define. In this study, prolapse and restriction were defined in relation to tissue availability for repair as excess or deficient cusp tissue, respectively, in any dimension or part of a cusp.
Surgical approach, reading valve morphology, and repair techniques
Surgical approach included mini or full median sternotomy, direct aortic and atrial cannulation, and cardiopulmonary bypass. Aortic valve repair began with careful review of the intraoperative transesophageal echocardiogram (TEE). Number and direction of regurgitant jets, available cusp tissue, valve area, and gradients were evaluated and correlated with surgical findings. The heart was then arrested using blood cardioplegia.
Reading Valve Morphology
Valve morphology was systematically evaluated, read, and recorded segment by segment: cusps, commissures, and root (Online Appendix). Cusps: Normality of the reference cusp was evaluated for integrity, thickness, mobility, size, and shape. Each was graded as normal, moderately abnormal (potentially correctable), or severely abnormal (probably not correctable). Next, the second or conjoint cusp was evaluated for the same qualities using the reference cusp as a benchmark. The regurgitant orifice, delineated by free-margin cusp thickening, was identified (6,22,23). Commissural abnormalities recorded included splaying, alignment, and attachment. The root and ascending aorta were examined for shape and dimensions, absolute and in relation to the cusps (primarily the reference cusp), and related to patient size. If any severe abnormality of any segment was considered uncorrectable, the valve was replaced.
The primary repair principle was to transform the valve into a good bicommissural valve (Online Appendix). Based on anatomy, a morphology-specific repair plan, segment-by-segment and abnormality-by-abnormality, was chosen. First, the cusps were repaired (Table 2,Fig. 1). Closing tears and perforations by direct suture or autologous pericardial patching restored integrity. Shaving the free margins was performed cautiously; occasionally, the free margin was reinforced. Lengths of the free margins of the 2 cusps were then equalized. Good parts of free margins of the prolapsing or conjoint cusp were aligned and fixed to the free margin of the reference cusp with fine stay sutures (7-0 monofilament). This lineup revealed: 1) excess tissue and true prolapse; 2) 2 cusps well aligned; or 3) cusp restriction and tissue deficiency. Excess tissue was addressed by triangular resection, if redundant, or simple cusp plication, if less prominent. Well-aligned cusps with adequate tissue invited closing of the cleft. Tissue deficiency was addressed by overcorrecting the free margin of the conjoint cusp to a length shorter than that of the free margin of the reference cusp, resecting the raphe, and performing a “low” commissuroplasty (Cabrol stitch annuloplasty) or other manipulation to reduce the “annulus.” Second, commissures were resuspended, realigned, and approximated as needed (Table 3,Fig. 2).Third, root maneuvers were performed, including reduction aortoplasty or ascending aorta replacement. Result of repair was evaluated immediately by post-pump TEE. Acceptable repair was defined as AR ≤1+, mean gradient ≤15 mm Hg, or peak gradient ≤30 mm Hg. Post-repair AR >1+ was immediately addressed with additional repair maneuvers; no patient left the operating room with AR >1+. Slightly higher gradients were accepted in several cases.
From December 2001 to July 2007, 63 consecutive patients with unicuspid (n = 4) or bicuspid (n = 59) aortic valves underwent surgery for at least moderate (≥2+) pure AR by one surgeon (G.B.P.) at Cleveland Clinic. Mean age was 40 ± 12 years. Patients with aortic stenosis were excluded, as were those with aortic dissection. Primary indication for surgery was isolated AR in 48 patients and AR associated with proximal aortic aneurysm in 15 patients. Thirteen had aortic valve endocarditis, acute or remote, with pathology confined to the cusps. Five had undergone previous aortic valve operations: repair in 1; aortic valvotomy in 2; or balloon dilation for stenosis during childhood in 2. Aortic valve repair was considered in all patients; reason for not attempting repair was recorded in the operative note.
Clinical and operative data collection
Clinical and additional operative data were obtained from Cleveland Clinic's Cardiovascular Information Registry and review of patients' clinical records. Use of these data for research was approved by the institutional review board, with patient consent waived.
Retrospective echocardiographic review
Retrospectively, all intraoperative pre- and post-pump TEEs were reviewed, analyzed, and compared with pre- and post-operative transthoracic echocardiograms (TTEs). From the aortic valve short-axis view, reference and conjoint cusps were identified. At the short-axis level of the left main coronary artery, diastolic and systolic areas of conjoint and reference cusps were planimetered and recorded using Prosolv 3.5 (Problem Solving Concepts, Inc., Indianapolis, Indiana). Pliability of each cusp was estimated as apparent change in its area from systole to diastole and was called the tissue normality index (TNI): TNI = (diastolic cusp area − systolic cusp area)/diastolic cusp area
Adequacy of cusp tissue for coaptation was estimated by measuring the curvilinear height of anterior and posterior cusps in a plane parallel to the aortic orifice. A coaptation deficiency index (CDI) was calculated using the formula: CDI = (conjoint cusp height + reference cusp height)/diastolic aortic “annulus” diameter
When comparing echocardiographic features of repaired and replaced valves, valves replaced for reasons other than morphology were excluded.
Follow-up was by telephone interview using an institutional review board-approved protocol in July and August 2007 and was 97% complete. One foreign patient was not contacted after discharge. Follow-up included review of all available echocardiograms; 1 patient had no post-discharge echocardiogram. Median follow-up was 13 months, with 25% followed beyond 34 months (range 2 to 70 months).
Categorical variables are summarized by frequencies and percentages, and continuous variables by means and standard deviations and nonparametric box plots. Wilcoxon rank-sum tests were used to compare differences. The association of reference and conjoint cusp TNI and of CDI to aortic valve replacement was explored using multivariable logistic regression. Linearizing transformations of scale were used to meet the logit assumption.
Segmental structure and morphology-directed repair
One of 4 unicuspid and 41 of 59 (69%) bicuspid valves were repaired (Fig. 3).
One unicuspid valve had 1 good commissure and 2 good, mildly thickened cusps joined by a rudimentary third cusp mimicking a detached commissure (Table 2). Repair was by resuspension, creating a second commissure, combined with approximating the new commissure with a figure-of-8 stitch. Cusp thickening was shaved. The other 3 unicuspid valves had a highly thickened cusp with reduced mobility and were judged unrepairable.
Fifteen of 59 bicuspid valves (25%) were true bicuspid valves with horizontal commissure orientation. Forty-four valves (69%) had partial or incomplete fusion of the conjoint cusp and a raphe. Thirty-eight of the 44 (86%) had right-left cusp fusion. Area of the conjoint cusp appeared larger than that of the reference cusp, with relative size closer to 2:1 than 1:1. The main cause of AR was almost uniformly related to incomplete fusion of the conjoint cusps, whether true prolapse, central restriction, or the cleft itself. The regurgitant orifice was always delineated by thickened margins of the cleft and opposing central portion of the reference cusp. In 16 cases, cusp tears or perforations caused AR.
Forty-one of these bicuspid valves (69%) were repaired, with cusp procedures directed at corresponding cusp morphology required in all. Overcorrection of the conjoint cusp was employed in 5 instances. Ten repairs (24%) required more than 1 pump run. In 1 additional patient, repair failed (repair was unsatisfactory after 2 pump runs), possibly contributed to by choice of an undersized ascending aorta graft; this patient has been counted as undergoing valve replacement.
After evaluating and recording morphology, 18 bicuspid valves (31%) were replaced, 4 for nonmorphologic reasons (old age, multiple comorbidities) and 14 for unfavorable cusp morphology. Unfavorable morphology was dominated by conjoint cusp tissue deficiency and restriction (8 of 14), combined with cusp thickening (11 of 14) and calcification (6 of 14), and important reference cusp pathology. Reduced cusp pliability and tissue deficiency, identified retrospectively by echocardiography, was associated with limited repairability; TNI (Fig. 4) of replaced valves was lower (conjoint cusp 34 ± 17% vs. 61 ± 16%, p < 0.0001; reference cusp 42 ± 16% vs. 65 ± 16%, p < 0.0001) and CDI (Fig. 5) greater (1.27 ± 0.19 for replaced vs. 1.06 ± 0.24 for repaired valves; p < 0.002) than for repaired valves (Fig. 6). Of these echocardiographic measurements, TNI of the reference cusp was the most informative of inability to repair the valve (univariable p < 0.0004; C = 0.83); however, CDI ≥1 was also independently associated with valve replacement (bivariable p < 0.01; C = 0.88). The TNI and CDI reflect different and noninteracting (p = 0.5) cusp properties as demonstrated by their weak correlations (r = −0.26 for conjoint and r = −0.27 for reference cusps) that together may be useful in predicting aortic valve repairability (Online Table E1).
Commissural splaying, malalignment, and detachment caused or contributed to AR in 31 (53%) of the 59 bicuspid valve patients (Table 3). Of the 41 repaired, 29 (71%) had commissural procedures, including 6 commissurotomies for fusion. Sixteen of 42 repairs included Cabrol or Cabrol-like stitches; 3 were high commissural and 13 low.
Root and Ascending Aorta
Aortic root and ascending aorta abnormalities included dilation of the “annulus” in 24 of the 63 patients (38%), dilated sinus in 25 (40%), dilation of the sinotubular junction in 23 (37%), proximal aortic aneurysm in 16 (25%), and dilation of the ascending aorta in 22 (35%). Root and ascending aorta procedures were performed in 13 of 42 patients (31%) undergoing valve repair: 1 unicuspid and 12 bicuspid.
Of the 4 unicuspid valve patients, the 1 undergoing repair had supracoronary ascending aorta replacement. The other 3 had composite graft root replacements, with ascending aorta in 2 and ascending aorta and hemiarch in the third.
Of the 41 patients undergoing bicuspid valve repair, 3 had a wedge ascending aortoplasty (in 1 extended down into the sinus), and 5 had supracoronary ascending replacement (in 1 combined with sinus wedge aortoplasty). Of the 18 undergoing bicuspid valve replacement, 4 had allograft root replacement (3 with ascending aorta and hemiarch replacement), 1 had a Ross procedure combined with ascending wedge aortoplasty, and 5 had ascending aorta and hemiarch replacement.
In addition, 16 of 42 repairs included Cabrol or Cabrol-like stitches, not only to address the commissural issues noted previously, but also to reduce “annulus,” sinuses, or sinotubular junction.
Transthoracic echocardiography was performed on post-operative day 3 or 4. Mean and peak transvalvar gradients were 11 ± 4.3 mm Hg and 19 ± 8.7 mm Hg, respectively. For the 5 overcorrected valves, gradients were 17 ± 12 mm Hg and 27 ± 17.5 mm Hg, respectively. Gradients higher than our criteria for “acceptable repair” (defined as <15/30 mm Hg mean/peak pressures) were found in 8 patients.
Three patients developed recurrent AR ≥3+ before discharge and underwent reoperation. No repair patient left the hospital with residual AR ≥1+.
Repair Failures and Reoperations
To date, excluding the intraoperative failure mentioned in the preceding text, 4 patients have undergone reoperation for recurrent ≥3+ AR, including the 3 mentioned under “Pre-discharge TTE.” The commissural realignment had dehisced in 1 patient and was rerepaired with commissural realignment. In 2, cusp plication suture lines were torn after overcorrection, and both valves were replaced. The fourth patient developed symptoms from severe AR at 6 months; at 8 months, the valve was replaced; at reoperation, rupture of suture repair of a conjoint cusp perforation, which primarily occurred when the raphe was resected, was found.
Mortality and Morbidity
One patient ready for discharge exsanguinated on post-operative day 6 from rupture of the aortotomy suture. At last follow-up, there were no post-discharge deaths or episodes of thromboembolism or endocarditis.
Causes and mechanisms of regurgitation
This study includes all consecutive patients with regurgitant unicuspid or bicuspid aortic valves referred for surgery to a single surgeon, irrespective of cause or mechanism. The main cause of AR was cusp related. Commissural issues were also important contributors to AR. Root geometry or dilation was not the primary cause of AR, judged by need for correction to accomplish valve competence.
Contribution of echocardiography to aortic valve repair
Echocardiography already plays an important role in patient selection and in predicting repairability (16). In the operating room, it plays an important role in guiding repair and judging results. Primary interest is in number and location of jets and whether these are deflected. Jet deflection is a surrogate for cusp tissue redundancy and prolapse (16). Central nondeflected jet suggests restriction and cusp tissue deficiency relative to the root. Retrospective review and analyses of the echocardiograms included in this study resulted in development of 2 new indexes related to tissue normality (TNI) and availability (CDI), the most important of which is reference cusp TNI; these may importantly enhance our ability to predict repairability.
Sequential structure and morphology-directed repair
Morphology-directed repair means that every surgical maneuver confirmed, quantified, and addressed the perceived importance of a corresponding pathology.
We perceive optimal bicuspid valves as perfectly competent, but still having a mildly restrictive opening in systole that causes turbulence and a measurable gradient. The gradient is determined by valve opening area and degree of doming of 1 or both cusps. Regurgitation can be caused by either excess tissue and prolapse or tissue deficiency and restriction, preventing coaptation.
Most regurgitant bicuspid valves in this series were asymmetric. All repaired valves had a good or normal-looking reference cusp, the main exception being perforations in the cusp belly caused by endocarditis. When, during attempted repair, good portions of the conjoint cusp lined up against the reference cusp, the tricuspid configuration was recreated. Parts of the conjoint cusp facing the reference cusp closest to the open commissures often looked normal and thin (implying low stress and coaptation), whereas parts closest to the raphe were thickened and delineated the regurgitant orifice. The “line up” invited direct closure of the regurgitant orifice or plication or triangular resection to correct prolapse and redundant tissue.
Residual noncommissural regurgitation after equalizing length of the 2 cusps was interpreted as tissue deficiency. Restriction was not always centered on the raphe. Resection of the raphe was seldom sufficient, nor was shortening of the “annulus” by a low commissuroplasty suture (low Cabrol stitch) or plication stitch beneath the restricted portion of a cusp. Shortening the free margin (overcorrection) reduced regurgitation at the expense of increased doming, reduced valve area, and higher post-repair gradient (Fig. 7); 2 of 5 failures were related to overcorrection. Post-repair doming of the conjoint cusp is obligatory when this cusp is larger than the reference cusp, and not exclusively a consequence of overcorrection. Cusp extension with autologous pericardium or fascia has been attempted by others to correct tissue deficiency, but results have been less than satisfactory (24,25).
Commissural issues were frequent but easy to identify and deal with. The figure-of-8 suture to ensure perfect alignment has been our technique of choice to handle this, replacing the classic Cabrol stitch (26). Most likely we placed more figure-of-8 sutures than necessary. Cabrol-like stitches were also used to manipulate commissural alignment and to reduce the annulus locally to oppose cusp restriction. A Cabrol stitch often provokes splaying, which requires a compensatory figure-of-8 suture.
Root and Ascending Aorta
Aortic dilation is an important aspect of bicuspid valve disease, but not necessarily the cause of regurgitation. Some of the commissural Cabrol stitches could rightly also be claimed to address root dilation, but besides these, root procedures were directed against the root and aortic dilation rather than being part of the valve repair. We, as others, are increasingly liberal with reduction aortoplasty or aortic replacement, but to address dilation and aneurysm rather than as part of the valve repair. The question is, how aggressive should one be? Borger et al. (27) suggest that an aortic diameter of ≥4.5 cm should be addressed. Combined bicuspid valve repair with aortic replacement by a supracoronary graft has been our most common approach, as well as that of Veldtman et al. (28). Asymmetric configuration of a dilated aorta invites reduction aortoplasty (29,30). Interestingly, the Toronto group has reported higher freedom from recurrent AR after bicuspid aortic valve repair associated with reimplantation than after valve repair alone (31). Repair associated with remodeling has also produced good results (32).
Short- and long-term repair durability is related to different phenomena. Our early failures were related to tissue quality and fragility.
A previous study from our institution showed that post-operative AR >1+ was associated with repair failure and reoperation (5). We have found no studies of post-repair gradients and their relationship to durability, repair failure, and reoperation; we anticipate that high post-repair gradients will be associated with higher risk of developing severe stenosis requiring reoperation (13,33).
Feasibility of repair
When repair was considered infeasible for morphologic reasons, the dominant reason was cusp pathology. Important reference cusp pathology also limited repair.
Sutures in normally thin cusp tissue are prone to tearing, a contributing factor in all 4 repair failures. Cusp defects and perforations may be repaired with autologous pericardium as long as contour, size, and shape of the cusp remain well defined. Edges of cusp defects always have some thickening and fibrosis, allowing suturing. Repair intuitively becomes less attractive when cusps are already thickened and calcification has begun. Our findings corroborate previous reports in which thickened and immobile cusps were less amenable to repair (6,7).
We have not identified any specific commissural or root morphology that precludes successful bicuspid aortic valve repair.
This is a prospective series, but the number of patients is small and limited to one surgeon, restricting general applicability of the findings and concepts. Although many aspects of “reading” aortic valve pathology are dichotomous and objective (calcification, integrity, folding, attachment, dilation, aneurysm, subvalvar pathology), others that relate to degree of severity are only semiquantitative (thickness, mobility, fusion, splaying, size). Our systematic sequential approach to analysis and repair of the valve was intended to reduce this subjectivity, as was the development of quantitative echocardiographic indexes for estimating repairability. Three-dimensional echocardiography and gated high-resolution computed tomography are technologies that promise to improve aortic valve imaging and reduce even further this subjectivity.
This was a feasibility study to identify which morphologic findings of regurgitant unicuspid and bicuspid aortic valves and surgical details were important for successful repair. Learning the art of reading and interpreting surgical findings is an ongoing effort (22,34–37). The systematic segmental approach to morphology and correlation of morphologic features to repair of bicuspid aortic valves refined our choices of repair maneuvers and resulted in repair of a high percentage of regurgitant valves. Our results emphasize that redundant or sufficient cusp tissue offers greater potential for valve repair than restricted cusps with deficient tissue. The importance of echocardiography to patient selection for repair is emphasized by development of new indexes illustrating normal cusp tissue availability.
The authors thank Peter Kisuule for data management, Ross Papalardo and Brian Kohlbacher for medical illustrations, and Tess Parry for editorial assistance.
For the morphology, pathology, and repair data collection and correlation information, please see the online version of this article.
Toward Predictable Repair of Regurgitant Aortic Valves: A Systematic Morphology-Directed Approach to Bicommissural Repair
This study was supported, in part, by the Peter and Elizabeth C. Tower and Family Endowed Chair in Cardiothoracic Research, James and Sharon Kennedy, the Slosburg Family Charitable Trust, and Stephen and Saundra Spencer (to Dr. Pettersson), and the Kenneth Gee and Paula Shaw, PhD, Chair in Heart Research (to Dr. Blackstone).
- Abbreviations and Acronyms
- aortic regurgitation
- coaptation deficiency index
- transesophageal echocardiogram
- tissue normality index
- transthoracic echocardiogram
- Received October 29, 2007.
- Revision received December 17, 2007.
- Accepted January 26, 2008.
- American College of Cardiology Foundation
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