Rigid, Complete Annuloplasty Rings Increase Anterior Mitral Leaflet Strains in the Normal Beating Ovine Heart
Background—Annuloplasty ring or band implantation during surgical mitral valve repair perturbs mitral annular dimensions, dynamics, and shape, which have been associated with changes in anterior mitral leaflet (AML) strain patterns and suboptimal long-term repair durability. We hypothesized that rigid rings with nonphysiological three-dimensional shapes, but not saddle-shaped rigid rings or flexible bands, increase AML strains.
Methods and Results—Sheep had 23 radiopaque markers inserted: 7 along the anterior mitral annulus and 16 equally spaced on the AML. True-sized Cosgrove-Edwards flexible, partial band (n=12), rigid, complete St Jude Medical rigid saddle-shaped (n=12), Carpentier-Edwards Physio (n=12), Edwards IMR ETlogix (n=11), and Edwards GeoForm (n=12) annuloplasty rings were implanted in a releasable fashion. Under acute open-chest conditions, 4-dimensional marker coordinates were obtained using biplane videofluoroscopy along with hemodynamic parameters with the ring inserted and after release. Marker coordinates were triangulated, and the largest maximum principal AML strains were determined during isovolumetric relaxation. No relevant changes in hemodynamics occurred. Compared with the respective control state, strains increased significantly with rigid saddle-shaped annuloplasty ring, Carpentier-Edwards Physio, Edwards IMR ETlogix, and Edwards GeoForm (0.14±0.05 versus 0.16±0.05, P=0.024, 0.15±0.03 versus 0.18±0.04, P=0.020, 0.11±0.05 versus 0.14±0.05, P=0.042, and 0.13±0.05 versus 0.16±0.05, P=0.009), but not with Cosgrove-Edwards band (0.15±0.05 versus 0.15±0.04, P=0.973).
Conclusions—Regardless of three-dimensional shape, rigid, complete annuloplasty rings, but not a flexible, partial band, increased AML strains in the normal beating ovine heart. Clinical studies are needed to determine whether annuloplasty rings affect AML strains in patients, and, if so, whether ring-induced perturbations in leaflet strain states are linked to repair failure.
Surgical mitral valve repair most commonly includes the insertion of an annuloplasty band or ring. Whereas bands are flexible devices that spare the anterior, fibrous portion of the mitral annulus, rings encircle the entire annulus and may be flexible, semirigid, or rigid. Rigid rings are available in various shapes. The most commonly used ring (Carpentier-Edwards Physio [PHYSIO]) is flat, semirigid, and D-shaped. Recently, saddle-shaped, rigid, complete annuloplasty rings have been introduced (eg, Saint Jude Medical rigid saddle-shaped annuloplasty ring [RSAR], Medtronic Profile 3-D, and PHYSIO II) to account for the physiological three-dimensional (3D) shape of the mitral annulus.1,2 Furthermore, rigid rings with nonphysiological shapes and dimensions have been designed specifically for patients with functional/ischemic mitral regurgitation (eg, Edwards GeoForm [GEO] and IMR ETlogix [ETL]). These rings aim to counteract the main determinants of functional/ischemic mitral regurgitation (ie, mitral annular dilatation, left ventricular dilatation and papillary muscle displacement) on an annular level via their specific designs, all of which include disproportionate annular septal-lateral (S-L) downsizing.3 Although some studies demonstrate that such rings may reduce mitral leaflet strains in the diseased heart,4 other studies suggest that, by perturbing the natural saddle-shaped mitral annulus, disease-specific or nonphysiologically shaped rings may increase leaflet strains in the normal heart.5–7 Because of these results from in vitro measurements, it has been speculated that such perturbations in mitral leaflet strain patterns could be associated with impaired long-term results after mitral valve repair.5–7 Our goal, therefore, was to assess the effects of 1 flexible, partial band and 4 different complete annuloplasty rings on anterior mitral leaflet (AML) strains in healthy, beating ovine hearts. We tested the hypothesis that rigid, complete rings with nonphysiological 3D shapes, but not saddle-shaped rigid rings or flexible, partial bands, increase maximum principal strains across the AML.
All animals received humane care in compliance with the Principles of Laboratory Animal Care formulated by the National Society for Medical Research and the Guide for Care and Use of Laboratory Animals prepared by the National Academy of Sciences and published by the National Institutes of Health (Department of Health Education and Welfare Publication 85-23, revised 1985). This study was approved by the Stanford Medical Center Laboratory Research Animal Review Committee and was conducted according to Stanford Universitypolicy.
Fifty-nine adult, Dorsett-hybrid, male sheep (49±5 kg) were premedicated with ketamine (25 mg/kg intramuscularly), anesthetized with sodium thiopental (6.8 mg/kg intravenously), intubated, and mechanically ventilated with inhalational isoflurane (1.0% to 2.5%). A left thoracotomy was performed, and the heart was suspended in a pericardial cradle. Thirteen miniature radiopaque tantalum markers were surgically implanted into the subepicardium to silhouette the left ventricular chamber at the intersections of 2 longitudinal and 3 crosswise meridians, as shown in Figure 1A. Using cardiopulmonary bypass and cardioplegic arrest, a total of 33 radiopaque tantalum markers were sewn to the following sites (Figure 1B): 16 around the mitral annulus (markers 17 to 32, Figure 2A and 2B), 16 equally spaced on the atrial aspect of the AML (markers 1 to 16, Figure 2B), and 1 on the central edge of the middle scallop of the posterior mitral leaflet (marker 33, Figure 2B). A single tantalum loop (0.6 mm inner diameter, 1.1 mm outer diameter, 3.2 mg) was used for each leaflet marker.
After marker placement, 5 different annuloplasty ring models, the Cosgrove-Edwards band (COS) (Edwards Lifesciences, Irvine, CA, USA, n=12), RSAR (St. Jude Medical Inc, St. Paul, MN, n=12), PHYSIO (n=12), Edwards IMR ETL (n=11), and Edwards GeoForm (GEO, n=12, all three Edwards Lifesciences, Irvine, CA) were implanted in a releasable fashion as described earlier.8 In brief, the annuloplasty devices were prepared before the operation in the following manner: the middle parts of 8 double-armed polyester braided sutures were stitched evenly spaced around the ring or band from the bottom to the top side using a “spring eye” needle. The resulting loops were “locked” with 2 polypropylene sutures. The polyester sutures were stitched equidistantly in a perpendicular direction from the ventricular to the atrial side through the mitral annulus. The annuloplasty devices were secured to the mitral annulus by tying these sutures. The locking sutures (polypropylene) and the drawstrings were exteriorized before the atrium was closed. Ring and band sizes were determined by assessing the entire area of the AML using a sizer from Edwards Lifesciences. All annuloplasty devices were true-sized (as all animals had similarly sized leaflets, each received size 28 rings or bands). The left atrium was closed, and the left circumflex artery was encircled with a vessel loop for a parallel study.9 Data from mitral annular and leaflet geometry using this data set have been published earlier.8–11 The animals were then transferred to the experimental catheterization laboratory for data acquisition under acute open-chest conditions.
Videofluoroscopic images (60 frames/s) of all radiopaque markers were acquired using biplane videofluoroscopy (Philips Medical Systems, Pleasanton, CA). First, images were acquired under baseline conditions with the ring inserted (COS, RSAR, PHYSIO, ETL, GEO). Following the data acquisition under baseline conditions, 90 seconds of ischemia was induced, for a parallel study, by tightening the encircling left circumflex artery vessel loop with a tourniquet. Thereafter, the locking sutures were pulled out, and the ring was lifted away from the mitral annulus toward the left atrial roof using the drawstrings. After hemodynamic values returned to baseline, a third data acquisition was performed, and images were acquired under baseline conditions with the ring released (COS-control [CTRL], RSAR-CTRL, PHYSIO-CTRL, ETL-CTRL, GEO-CTRL). Marker coordinates from 2 consecutive sinus rhythm heart beats from each of the biplane views were then digitized and merged to yield the 3D coordinates of each marker centroid in each frame using semiautomated image processing and digitization software.12 Simultaneously, analog left ventricular pressures (LVP), as well as ECG signals, were recorded in real time on the video images during data acquisition.
Hemodynamic Parameters and Cardiac Cycle Timing
For each beat, the end-diastolic videofluoroscopic frame was defined as the frame that coincided with the peak of the R-wave on the ECG. To calculate leaflet strains, a reference configuration during diastole and a deformed configuration during peak systole were determined for each beat (t0 and tn, respectively,Figure 2). When defining these configurations, the goal was to quantify strains with the mitral valve closed in both configurations and maximize the LVP difference between the 2 time points. To identify the reference configuration, the distance between AML central edge (marker 4,Figure 1B) and posterior mitral leaflet edge marker (marker 33,Figure 1B) was plotted throughout the cardiac cycle for each animal. For each heartbeat, the time point of leaflet opening was defined as the time point immediately before the AML and posterior mitral leaflet started to separate (Figure 2), thereby defining the reference state for beat 1 (t01,Figure 2) and beat 2 (t02,Figure 2). To identify the deformed configuration, LVP curves were plotted throughout the cardiac cycle. The time point of maximum LVP for each heartbeat was defined as the deformed state (tn1 and tn2, respectively,Figure 2). The embedded period between these 2 states closely reflects the period of isovolumetric relaxation (Figure 2). Maximum systolic dP/dt (dP/dtmax) was calculated for each beat for each animal. Left ventricular volumes (LVV) were calculated from space-filling tetrahedral fit between all left ventricular markers at each beat at end-diastole (left ventricular end-diastolic volume), tn1, tn2, t01, and t02 (see Moon et al13 for details). Changes in LVP and LVV (ΔLVP and ΔLVV, respectively) from t01 to tn1 and from t02 to tn2 were calculated as LVPtn1−LVPt01 and LVPtn2−LVPt02 and as LVVtn1−LVVt01 and LVVtn2−LVVt02, respectively.
Mitral Annular Dimensions
At tn1, tn2, t01, and t02, distances between markers 20 and 28 and distances between markers 32 and 24 (Figure 1B) were calculated to determine S-L and commissure-commissure (C-C) annular dimensions, respectively. Changes in mitral annular S-L and C-C dimensions (ΔS-L and ΔC-C, respectively) from t01 to tn1 and from t02 to tn2 were calculated as tn1−t01 and tn2−t02.
Global Maximum Principal, Radial, and Circumferential Strains
To determine the largest (global) maximum principal, radial and circumferential strains across the entire leaflet, the 16 AML mitral leaflet markers (markers 1 to 16, Figure 1B) and the 7 mitral annular markers (markers 17 to 23, Figure 1B) were triangulated, and 30 triangular membrane elements were generated. For each triangle, the co- and contravariant base vectors at time points t01, tn1, t02, and tn2 were calculated to determine the corresponding metric tensors and the resulting Euler-Almansi strain tensors for beats 1 and 2. The direction defined by the belly markers 9 and 11 (Figure 1B) in the deformed configuration, ie, at times tn1 and tn2 for beat 1 and beat 2, respectively, was interpreted as the circumferential direction. The radial direction was defined orthogonal to the circumferential axis, passing through belly marker 10 (see Figure 1B). The largest projections of the Euler-Almansi strain tensor onto the circumferential and radial directions were defined as global maximum circumferential strain (global εcir) and global maximum radial strain (global εrad), respectively. These values were determined for 2 beats in each animal and each state (with and without annuloplasty device implanted). The animal global maximum principal strain (global εmax) was calculated as the 2-beat average for each animal and each state by solving the eigenvalue problem for the Euler-Almansi strain tensor.
Maximum Principal (εmax,), Radial (εrad), and Circumferential (εcir) Strains Across the Entire AML
To provide a qualitative description of changes in strain patterns across the entire AML with and without annuloplasty device implanted, the 2-beat averages of εmax, εrad, and εcir values of each triangular element were calculated for each animal in each state. These values were averaged for all animals (by extrapolating constant average element strains to the individual marker positions using superconvergent patch recovery to obtain smoothly varying strain profiles) and plotted onto color-mapped schematics.
Average values of all animals in the respective groups were reported as mean±1 SD. All data reported for individual animals and all data used for quantitative statistical comparisons are 2-beat averages. Data with and without annuloplasty ring (or band) were compared using 1-way repeated-measures analysis of variance with a Holm-Sidak post hoc test (Sigmaplot 11.0, Systat Software Inc). To look at strain differences between the ring groups, maximum principal (εmax,), radial (εrad), and circumferential (εcir) strains with rings (COS, RSAR, PHYSIO, ETL, and GEO) were compared using 1-way analysis of variance. A probability value of less than 0.05 was considered statistically significant.
Heart Rate, Left Ventricular End-Diastolic Volume, and dP/dtmax
Group mean heart rates, left ventricular end-diastolic volumes, and dP/dtmax are shown in Table 1. No significant differences were found between ring and control states in all 5 groups (except for Cosgrove, where dP/dtmax was slightly higher compared with control).
Left Ventricular Pressures and Volumes at Reference State (t0) and Deformed State (tn)
Table 2 shows LVPs and LVVs at t0 and tn, as well as ΔLVP and ΔLVV. ΔLVP and ΔLVV are also graphically depicted in Figure 3(top row). A significant increase in LVPs by approximately 80mmHg (note that changes in LVP and LVV (ΔLVP and ΔLVV) are described from t0 to tn, ie, backward in time) occurred in both ring and control states from t0 to tn, whereas no relevant LVV changes were observed.
Mitral Annular Dimensions at Reference State (t0) and Deformed State (tn)
Table 3 shows the mitral annular S-L and C-C dimensions at tn and t0, as well as ΔS-L and ΔC-C. ΔS-L and ΔC-C are also graphically depicted in Figure 3 (middle row). Again, note that ΔS-L and ΔC-C are described from t0 to tn, ie, backward in time. Consequently, negative ΔS-L and ΔC-C represent an increase, whereas positive ΔS-L and ΔC-C represent a decrease in the respective dimension during the regular cardiac cycle. Relative to control, implantation of either complete, rigid rings (RSAR, PHYSIO, ETL, or GEO) or the flexible band (COS) resulted in significantly smaller mitral annular S-L and C-C dimensions. Decreases in S-L and C-C diameters from t0 to tn (negative ΔS-L and ΔC-C, Table 3) were observed for the control cases (all groups). With the annuloplasty device implanted, the S-L dimension became slightly smaller from t0 to tn with COS (ΔS-L: −0.9±0.5 mm, Table 3 and Figure 3, middle row), whereas no relevant decreases in S-L and C-C diameters from t0 to tn were found with RSAR, PHYSIO, ETL, or GEO.
Global Maximum Principal (Global εmax), Radial (global εrad), and Circumferential (Global εcir) Strains
Table 4 shows global εmax, εrad, and εcir for all 5 groups with and without annuloplasty devices implanted. Global εmax, εrad, and εcir (average from all animals) are also graphically displayed in Figure 3 (bottom row). Compared with the respective control state, strains increased significantly with RSAR, PHYSIO, ETL, and GEO (0.14±0.05 versus 0.16±0.05, P=0.024; 0.15±0.03 versus 0.18±0.04, P=0.020; 0.11±0.05 versus 0.14±0.05, P=0.042; and 0.13±0.05 versus 0.16±0.05, P=0.009, respectively; all P<0.05), but not with COS (0.15±0.05 versus 0.15±0.04, not significant, P=0.973). Global εrad increased significantly compared with the control state only with RSAR, whereas greater global εcir values were found with RSAR, PHYSIO, ETL, and GEO (however, they were insignificant for GEO; Table 4). No significant changes in global εrad or εcir were found with COS compared with the control state. With no annuloplasty device implanted, global εrad was greater than global εcir in all 5 groups (COS-CTRL, RSAR-CTRL, PHYSIO-CTRL, ETL-CTRL, GEO-CTRL; Table 4 and Figure 3, bottom row). With the annuloplasty device implanted, global εrad values were either greater than global εcir (COS, RSAR), smaller (PHYSIO), or similar (ETL, GEO; Table 4 and Figure 3, bottom row). No differences in εmax (P=0.331, F=1.178), εrad (P=0.188, F=1.598), or εcir (P=0.160, F=1.716) with rings implanted were found between the groups (COS, RSAR, PHYSIO, ETL, and GEO).
Maximum Principal, Radial, and Circumferential Strains Across the Entire AML
Figure 4 shows maximum principal (εmax), radial (εrad), and circumferential (εcir) strains across the entire AML for both states, with and without annuloplasty device implanted in all 5 groups. Increases in εmax can be appreciated with RSAR, PHYSIO, ETL, and GEO compared with the respective control state and predominantly occur in the belly and edge region of the AML. No major changes in strain patterns (εmax, εrad, or εcir) were observed with COS. εmax values across the AML of the respective control states were slightly different between groups, with COS-CTRL, RSAR-CTRL, and PHYSIO-CTRL being more strained than GEO-CTRL and ETL-CTRL.
The principal finding of this study was that with no relevant changes in hemodynamics, implantation of rigid, complete annuloplasty rings (RSAR, PHYSIO, ETL, and GEO), but not of the flexible, partial band (COS), increased global maximum principal strains of the AML. These changes occurred predominantly in the region of the AML belly and edge.
Several studies have determined mitral leaflet strains and stretches using a variety of different techniques.4–7,14–19 In vitro studies have been used to characterize dynamic stretches on the anterior and posterior leaflet of excised porcine mitral valves using a left heart simulator.6,14–17 In vivo studies, using sonomicrometer technology, quantified AML strains in the beating ovine heart,16 and lastly, finite element studies investigated strain patterns across the AML.4,5,18,19
Salgo et al demonstrated in a numeric simulation that the native mitral annular shape is important to minimize stresses acting on the leaflet.5 In a previous analysis from the same data set, we demonstrated that implantation of the PHYSIO, IMR ETL, and GEO, but not RSAR, perturbed the physiological saddle shape of the mitral annulus.11 The increased maximum principal leaflet strains observed with these 3 rings are therefore consistent with engineering intuition quantified through the results of Salgo et al.5 However, to our surprise, the supposedly physiologically shaped RSAR also led to an increase in maximum principal leaflet strains. Assuming that the shape of this ring is physiological, it could be speculated that the dynamic motion of the mitral annulus, rather than its 3D shape, is of major importance to preserve AML strain distribution. This hypothesis, however, is contrary to previous studies that suggested changes in the physiological mitral annular 3D saddle shape lead to increases in leaflet strains.6 It may therefore also be speculated that the shape of the RSAR does not fully represent the natural 3D annular shape and that, as discussed earlier,6 increased strains are also a result of a nonphysiological annular shape.
The partial, flexible band (COS) has been found to preserve the mitral annular saddle shape11 and allow minimal mitral annular S-L dynamics (Figure 3, middle row) during the observed time period (from t0 to tn). However, COS significantly reduced mitral annular dimensions compared with the control state (Table 3 and Bothe et al11). Because COS did not affect AML strains (Figure 3, bottom row), we speculate that preserving physiological mitral annular dynamics and shape rather than absolute mitral annular dimensions are the key components to maintaining a physiological strain distribution across the AML.
To our knowledge, Votta et al are the only group that has quantified the effects of annuloplasty rings (GEO and PHYSIO) on mitral leaflet strains and stresses.4 The group used a finite element model and demonstrated that the GEO, but not the PHYSIO, reduced maximum principal mitral leaflet stresses during simulated functional mitral regurgitation.4 In our study, we found that all rigid rings (RSAR, PHYSIO, ETL, and GEO) increased maximum principal AML strains, irrespective of their 3D shape. However, unlike Votta et al, we used an in vivo model of the normal, beating heart. We therefore cannot comment on the potential effects of rings designed to treat functional or ischemic mitral regurgitation (ie, GEO, ETL) in the diseased state, and it is possible that these rings restore a physiological strain distribution in hearts with dilated left ventricles.
In this study, we report the effect of different annuloplasty devices on radial and circumferential strains. Whereas global εrad was only greater with RSAR, global εcir was greater with all rigid, complete rings (RSAR, PHYSIO, ETL, and GEO;Table 4) compared with the control state (insignificantly, however, for GEO), suggesting that rigid, complete annuloplasty devices affect circumferential strains more than radial strains. The reason for the insignificant increase in global εcir observed with GEO could be a result of the larger commissure to commissure dimension of this ring compared with RSAR, PHYSIO, or ETL,3 suggesting that the physiological circumferential AML strain distribution is sensitive to the amount of mitral annular C-C decrease.
Several limitations should be addressed to allow a better interpretation of these data. First, the data were acquired from open-chest, anesthetized ovine hearts with normal preoperative anatomy. Considerable caution must therefore be exercised when extrapolating these findings to the human heart. This is especially true for the GEO and IMR ETL rings, which were designed for patients with ischemic or functional mitral regurgitation (with distorted annular, leaflet, and ventricular geometry and function). As mentioned above, if these rings are implanted in the setting of functional or ischemic mitral regurgitation, it could well be that they reduce (or restore physiological) leaflet strains, as demonstrated by Votta et al in a computer simulation.4 In future analyses, we aim to use our experimental in vivo data to determine whether these 2 rings designed to treat functional or ischemic mitral regurgitation (GEO and ETL) are more efficient than conventional rings in terms of reducing leaflet strains during acute myocardial ischemia. Second, AML strains were quantified for only the isovolumetric relaxation phase of the cardiac cycle, and it could be that the rings affect strain patterns differently in other phases of the cardiac cycle.20 Third, although perturbed leaflet strains have been associated with impaired mitral valve repair durability,6,7 currently no study exists that proves causation. Consequently, it remains to be determined whether perturbations in AML strains impair long-term function of the mitral valve after repair. Fourth, when radial and circumferential strains were plotted onto color-mapped schematics (Figure 4), we observed not only tensile but also compressive strains in both control states and with rings implanted (green and blue areas,Figure 4). Compressive strains do not occur, eg, in purely computational models that use simplified AML shapes with the leaflet being entirely convex to the left ventricle4 and thus may be a result of the complex AML shape21 that was included in our analyses. The finding of compressive strains warrants further investigation; however, in this study, we focused on the tensile aspects of strain and did not perform detailed analyses of compressive strain patterns. Fifth, no statistically significant differences in strains were found between the different ring types. We therefore cannot draw any conclusions from these data whether any ring design is superior to another; however, this study was not adequately powered to demonstrate differences between the different ring types. Sixth, we studied only a partial, flexible band. Because no complete, flexible ring was examined in this experiment, it is not possible to distinguish whether the observed lack of increase in AML strains with a partial band is due to its partial design, its flexibility, or a combination of the 2. Lastly, strain patterns may change with varying annuloplasty device sizes.4 Because only 28-mm annuloplasty rings were used in this study, we are unable to draw any conclusions about the impact of ring or band size on leaflet strains.
In conclusion, regardless of their 3-dimensional shape, rigid, complete annuloplasty rings (RSAR, PHYSIO, ETL, GEO), but not a partial, flexible band (COS), increased maximum principal AML strains predominantly in the belly and edge regions in the normal beating ovine heart. Large, randomized clinical trials are needed to answer the question of whether the observed ring-induced alterations in mitral leaflet strain states exist in human patients, and if so, whether they adversely affect long-term mitral valve repair durability.
Sources of Funding
This study was funded by Research Grants R01-HL29589 (1982–2008) and R01-HL67025 (2001–2010), National Heart, Lung, and Blood Institute, National Institutes of Health (to D.C.M.); Research Grant S/06/07, Deutsche Herzstiftung, Frankfurt, Germany (to W.B.); National Science Foundation Career Award CMMI-0952021 (to E.K.); US-Norway Fulbright Foundation, the Swedish Heart-Lung Foundation, and the Swedish Society for Medical Research. (to J.-P.E.K.); and a Western States Affiliate American Heart Association Postdoctoral Fellowship (to J.C.S.).
Dr Miller is a consultant for Medtronic CardioVascular Division, St. Jude Medical, Inc, and Abbott Vascular (MitraClip) and a partner of the US Pivotal Trial Executive Committee and Edwards Lifesciences (uncompensated).
The authors gratefully acknowledge the expert technical assistance of Paul Chang, Maggie Brophy, Sigurd Hartnett, Erin Schultz, and George T. Daughters, as well as the inspiring suggestions of Frank Langer.
- © 2011 American Heart Association, Inc.
- Salgo IS,
- Gorman JH III.,
- Gorman RC,
- Jackson BM,
- Bowen FW,
- Plappert T,
- St John Sutton MG,
- Edmunds LH Jr.
- Bothe W,
- Chang PA,
- Swanson JC,
- Itoh A,
- Arata K,
- Ingels NB,
- Miller DC
- Bothe W,
- Kvitting JP,
- Swanson JC,
- Goktepe S,
- Vo KN,
- Ingels NB,
- Miller DC
- Bothe W,
- Kvitting JP,
- Swanson JC,
- Hartnett S,
- Ingels NB Jr.,
- Miller DC
- Itoh A,
- Krishnamurthy G,
- Swanson JC,
- Ennis DB,
- Bothe W,
- Kuhl E,
- Karlsson M,
- Davis LR,
- Miller DC,
- Ingels NB Jr.