Transapical off-pump removal of the native aortic valve: A proof-of-concept animal study
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1 Transapical off-pump removal of the native aortic valve: A proof-of-concept animal study Stefano Salizzoni, MD, a Pietro Bajona, MD, a Kenton J. Zehr, MD, a William D. Anderson, MD, b Stijn Vandenberghe, PhD, a and Giovanni Speziali, MD a Objective: This study evaluates the feasibility of off-pump native aortic valve removal in preparation for transapical aortic valve replacement. Off-pump aortic valve replacement is performed by balloon predilatation of the native valve followed by insertion of a stented prosthesis. In patients with calcified annuli and cusps, particulate embolization, suboptimal prosthesis sizing, and perivalvular leaks may occur. Therefore, native valve removal may improve outcomes after transapical aortic valve replacement. Methods: The aortic cusps were sequentially removed from 10 pigs in an off-pump procedure. A temporary valve was inserted percutaneously into the ascending aorta to prevent aortic regurgitation. The electrocardiogram, coronary blood flow, and arterial, left atrial, and ventricular pressures were continuously monitored. Results: Removal of the aortic cusps caused a drop in diastolic arterial pressure and its equalization with left ventricular diastolic pressure. Systolic pressure decreased by 13.5%. Left atrial pressure increased by 86.0%. Coronary blood flow decreased by 39.9% and its pattern changed from mostly diastolic to mostly systolic. Electrocardiographic signs of ischemia appeared almost immediately. Percutaneous insertion of a temporary valve in the ascending aorta increased diastolic pressure and caused a tendency toward echocardiographic normalization. Conclusions: Aortic valve removal in a healthy beating heart causes acute massive aortic regurgitation, hemodynamic instability, and the rapid onset of myocardial ischemia. Reduction of left ventricular volume overload, by placement of a temporary valve in the ascending aorta, mitigates myocardial distress, helps stabilize hemodynamic parameters, and may be a useful tool to allow surgical manipulations of the aortic valve and annulus during transapical aortic valve replacement procedures. Aortic valve stenosis is one of the most common types of acquired valve disease, 1 and it is conventionally treated with aortic valve replacement (AVR) during open cardiac operations with cardiopulmonary bypass and cardioplegic arrest of the heart. Minimally invasive approaches aim to improve the life expectancy and quality of life in patients who cannot currently benefit from conventional surgical procedures. New technologies have led progressively toward less invasive cardiac procedures, and minimally invasive replacement, reconstruction, and implantation of heart valves are currently important focuses of cardiac research. 2,3 The first attempts to treat aortic stenosis in a nonsurgical way began with balloon aortic valvuloplasty in This procedure was gradually abandoned because of suboptimal From the Division of Cardiothoracic Surgery Heart, Lung and Esophageal Surgery Institute, a and Department of Cardiology, b University of Pittsburgh Medical Center, Pittsburgh, Pa. Funded by the Division of Cardiothoracic Surgery, University of Pittsburgh Medical Center. Received for publication Jan 16, 2009; revisions received March 5, 2009; accepted for publication March 13, 2009; available ahead of print June 1, Address for reprints: Giovanni Speziali, MD, Department of Cardiac Surgery, University of Pittsburgh Medical Center, 200 Lothrop St, Pittsburgh PA ( spezialig@upmc.edu). J Thorac Cardiovasc Surg 2009;138: /$36.00 Copyright Ó 2009 by The American Association for Thoracic Surgery doi: /j.jtcvs results. 4-6 Since 1992, bioprosthetic heart valves have been sutured onto balloon-expandable stents for catheter-based deployment. 7 These stented valves opened new frontiers in aortic valve implantation. In 2002, Cribier and associates 8 used this technique for the treatment of calcified aortic stenosis in a patient whose condition was considered inoperable by conventional methods. In the following years, antegrade/transapical, retrograde/percutaneous, and valve-invalve variations of this technique were reported. 9,10 Continued development and improvements in valve replacement by both percutaneous and transapical approaches have expanded the clinical indications for minimally invasive AVR, especially in the treatment of elderly and highrisk patients However, neither technique removes the native cusps or decalcifies the annulus, important steps during open AVR. 15 Instead, simple balloon predilatation is used to prepare the annulus for the implantation of the prosthesis. 10 Patient prosthesis mismatch, embolization of calcium debris, coronary flow (CF) obstruction, and onset of perivalvular leaks have been reported after aortic valve implantation with these techniques Resection of the native calcified aortic valves before transapical or percutaneous AVR may improve outcomes. 19,20 However, removing the aortic valve in an offpump procedure leads to acute, severe aortic regurgitation. This study was undertaken to determine the technical 468 The Journal of Thoracic and Cardiovascular Surgery c August 2009
2 Abbreviations and Acronyms AP ¼ arterial pressure AVR ¼ aortic valve replacement CF ¼ coronary flow ECG ¼ electrocardiogram LAP ¼ left atrial pressure LV ¼ left ventricle (ventricular) feasibility of beating heart, off-pump, aortic valve removal in preparation for transapical or percutaneous AVR. We evaluated the hemodynamic effects and physiologic response of the heart to transapical removal of aortic cusps in an off-pump procedure in swine and the protective effects of placing a temporary valve in the ascending aorta to minimize hemodynamic instability during the procedure. METHODS Surgical Procedure After we had obtained institutional approval, 8 domestic cross pigs (average weight 96.4 kg, range kg) were anesthetized, intubated, and mechanically ventilated. Arterial pressure (AP), left atrial pressure (LAP), and left ventricular (LV) pressure were continuously monitored and recorded. The left anterior descending artery was isolated and a 2-mm flow probe was positioned around it to continuously monitor CF. A cutting device was inserted into the LV through the apex and the three aortic cusps were sequentially removed by rotating the tool 120 to cut each cusp (Figure 1). At most, two attempts were needed to grab and cut each cusp, and the removal of all three cusps took less than 4 minutes in all cases. The procedure was performed under real-time epicardial echocardiographic guidance with a transesophageal probe resting on the lateral surface of the heart at the level of the right atrium (Figure 2, A and B). Finally, a temporary valve was inserted, in a retrograde fashion, through the right carotid artery and advanced into the ascending aorta, first to a supracoronary position and then at the level of the aortic annulus, in the orthotopic position. As before, pressures, CF, and the electrocardiogram (ECG) were monitored and recorded. At the end of the procedure, the animals were humanely killed and the hearts were harvested for necroscopic inspection. All data were collected with DataQ software and hardware DI 510 (DataQ Instruments, Akron, Ohio). Cutting Device and Temporary Valve The cutting device was manufactured from two pieces of hypodermic seamless tubing (Figure 3). One extremity of the smaller diameter tube was sharpened to a knife edge for cutting and slid freely inside the larger diameter tube, which had a sharpened notched section close to the distal end. When the cusp was captured in the notch of the larger tube, the smaller tube was moved forward to cut the cusp, which remained trapped inside the device and was removed (Figure 1). The temporary valve was mounted on a wire and consisted of a conical membrane with chordae, thereby resembling a parachute. It was previously described by Vandenberghe and colleagues. 21 Figure 4 shows the final assembly. Statistical Analysis Continuous variables are presented as mean over 10 consecutive beats standard deviation. Data were processed with Statistical Package for Social Sciences 13.0 software (SPSS Inc, Chicago, Ill). One-way analysis of variance was performed to compare parameters under different conditions, followed by a multiple pairwise comparison procedure (Tukey test). Assumptions of normality were checked and met. The Holm Sidak method was used to increase the power of the analysis. The Pearson product moment r coefficient was calculated to evaluate correlations. RESULTS Hemodynamic Effects of Removing the Aortic Cusps Removal of the three aortic cusps caused a dramatic and immediate drop in diastolic AP (P<.001) and its equalization with LV end-diastolic pressure 22 (Figure 5 and Table 1). Systolic AP decreased by 13.5% (P <.001) and LAP increased by 86.0% (P <.05). Average CF decreased by 49.9% (P <.05), and its pattern changed from mostly diastolic to mostly systolic (Figure 5). ECG changes (T-wave inversion) appeared an average of 30.8 seconds (range: seconds) after introduction of the cutting device into the LV apex. Massive regurgitation was seen by echocardiographic imaging (Figure 2, B). Thus, as expected, removal of the aortic cusps from the beating heart significantly altered CF and pressures. However, these changes were not immediately lethal and were tolerated for up to 30 minutes, despite the early onset of ECG ischemic changes. FIGURE 1. The procedure for transapical removal of the aortic cusps. A, Insertion of the cutting device into the left ventricle through the apex. B, Capturing and cutting the cusp. C, Removing the cutting device and captured cusp from the left ventricle. This procedure was done for each cusp by simply rotating the cutting device 120 counterclockwise. The Journal of Thoracic and Cardiovascular Surgery c Volume 138, Number 2 469
3 FIGURE 3. The cutting device. Inner tube (1). Outer tube (2). A Temporary Valve Restores Hemodynamic Stability To test whether a temporary device could reduce regurgitation and acute LV volume overload during debridement before transapical AVR, we inserted a temporary valve with a parachute-like design into the ascending aorta after removal of the aortic cusps (Figure 6). We previously tested this valve in a mechanical cardiovascular simulator and found that the valve increased output and decreased regurgitation. 21 After placement of the temporary valve in the supracoronary position, diastolic AP increased (P <.001) and a tendency toward T-wave normalization was noted (Figure 5). Unexpectedly, absolute CF decreased further compared with the no-cusp situation, although the difference was not statistically different (Table 1). When the temporary valve was pushed down into the orthotopic position, CF significantly improved (P <.05), although the other hemodynamic parameters (LAP, diastolic AP, and systolic AP) did not change in a significant manner. In conclusion, placing the temporary valve in the supracoronary position only caused a tendency toward normalization of the diastolic AP, whereas pushing the temporary valve into the orthotopic position also significantly improved the CF. Systolic AP and LAP were not affected in either case. After all procedures were completed, the hearts were harvested for necroscopic inspection. In all cases, cusp removal and insertion of the temporary valve caused neither anatomic abnormalities nor damage to the mitral subvalvular apparatus, aortic root and annulus, or aortic wall (Figure 7). FIGURE 2. Echocardiographic monitoring of cusp removal and aortic regurgitation. A, Epicardial long-axis echocardiogram showing the cutting device (CD) inserted through the left ventricle (LV) grabbing the noncoronary cusp (NCC). The left main coronary artery (LCA) and left atrium (LA) are also visible. B, Massive aortic regurgitation (AR) immediately after the removal of the aortic valve. VP, Valve plane. DISCUSSION Between 30% and 60% of patients affected by severe aortic stenosis are not treated surgically, usually owing to advanced age and comorbidities. 24 A feasibility study, approved by the Food and Drug Administration, of a less invasive transcatheter/transapical approach to AVR in high-risk, elderly patients was initiated in several centers. The procedure was found to be feasible but carried considerable risk. Early experience showed an in-hospital/30-day mortality of 22.5%, with a total mortality of 37.5% at 1 year, 25 although other more recent publications have shown lower mortality and a low risk of embolization. 26 In this study, we investigated the feasibility of performing a complete FIGURE 4. The assembled temporary valve. PU, Polyurethane; eptfe, expanded polytetrafluoroethylene. 470 The Journal of Thoracic and Cardiovascular Surgery c August 2009
4 FIGURE 5. Electrical activity and hemodynamics after aortic cusp removal and temporary valve placement. Two-second recordings of electrical activity, arterial, atrial, and ventricular pressures, and coronary flow during the four experimental conditions tested. A representative experiment (pig 8) is shown. AP, Arterial pressure (plotted in black); LVP, left ventricular pressure (plotted in gray). LAP, left atrial pressure; CF, coronary flow. In the plots for CF, the horizontal gray lines represent zero. EKG, Electrocardiogram. aortic valve cusp removal in an off-pump, beating-heart situation. The rationale underlying this approach is that cusp removal and annular cleanup before transapical or transfemoral AVR might yield improved procedural results. In this study, the sudden onset of severe aortic regurgitation after off-pump removal of the aortic cusps in a normal beating heart caused profound changes in AP, CF, and LAP. This is consistent with the results of others, although, in these prior studies, the aortic valve was damaged but not completely removed In our experiments, all three aortic cusps were completely removed. The LV tolerated these acute changes for some time, but myocardial ischemia appeared soon thereafter. Placement of a temporary valve in the ascending aorta reduced LV volume overload and mitigated myocardial distress. An immediate consequence of aortic cusp removal was a significant decrease in CF ( 39.9% from baseline), with subsequent appearance of ECG indications of ischemia. After placement of a temporary valve in the supracoronary position, CF decreased by an additional 24.8%, most likely as a consequence of the almost total loss of the diastolic component to blood flow. Pushing the catheter-based temporary valve deeper into the LV outflow tract (orthotopic, subcoronary position) caused the CF to return to a near physiologic level, with a difference of only 14.0% compared with the baseline situation. This small difference may be due simply to a suboptimal valve design or to the fact that it is quite difficult to place and retain the temporary valve in the exact location of the native valve. LAP increased dramatically after the removal of the cusps, and the temporary valve was unable to alleviate this in either the orthotopic or supracoronary position. Perhaps LAP did not recover because the experiment was not continued for enough time to allow complete myocardial recovery. TABLE 1. In vivo hemodynamic measurements Hemodynamic measurements Baseline No cusps Supracoronary Orthotopic Diastolic AP * *y *y (mm Hg) Systolic AP * y (mm Hg) LAP (mm Hg) * * CF (ml/min) * * z AP, Arterial pressure; LAP, left atrial pressure; CF, coronary flow. *Differs from baseline; P<.05. ydiffers from no cusps; P<.05. zdiffers from supracoronary; P<.05. The Journal of Thoracic and Cardiovascular Surgery c Volume 138, Number 2 471
5 FIGURE 6. Behavior of the temporary valve in ascending aorta, A and B, Schematic design. C and D, Echocardiographic images. A and C, Temporary valve closed during systole to permit blood flow into the ascending aorta. B and D, Open in diastole to prevent aortic regurgitation. PU, Polyurethane leaflets; W, guidewire. We also observed that the young healthy hearts in these pigs could maintain adequate hemodynamics as long as 30 minutes after induction of massive aortic regurgitation. Implantation of a temporary valve in the ascending aorta limits LV volume overload and has the potential to prolong this period of hemodynamic stability. Eventually, though, myocardial ischemia ensues owing to reduction in CF, and hemodynamic deterioration follows. In theory, the addition of a percutaneous (transfemoral) system allowing direct cannulation of the coronary ostia and coronary perfusion at a physiologic pressure and flow should allow longer periods of hemodynamic stability. Further investigation is needed to determine whether this additional step is feasible and has the potential to increase safety in a hybrid approach to transapical AVR. In these experiments, we accessed the heart via a sternotomy and then inserted the cutting device into the LV apex. We chose the direct LV apical approach instead of the peripheral retrograde approach because transfemoral access limits the size of the surgical devices and decreases the precision of the surgical manipulations. 30 Although these experiments were performed via sternotomy, the procedure could be easily done in a minimally invasive manner through a left minithoracotomy or a subxiphoidal incision. A peripheral, retrograde approach may also be possible with differently designed instruments. Limitations The most difficult limitation to resolve is the absence of calcific aortic stenosis in our animal model. However, we are not aware of any animal model for this condition. With a healthy aortic valve, it is easy to cut the cusps, but it will undoubtedly be more difficult to remove the cusps and debride the aortic annulus when calcifications are present. Additionally, in this pilot study, we did not attempt to prevent embolic events caused by the procedure. Future experiments are planned with a new temporary valve that incorporates a net in the distal portion to capture solid emboli. Finally, we learned that a normal heart is able to tolerate acute severe aortic regurgitation for short time periods; however, we do not know whether a hypertrophic heart, as in a patient with aortic valve stenosis, would behave similarly. In summary, this study was undertaken to determine the technical feasibility of removing the aortic cusps in an offpump, beating-heart model and to evaluate the effects of the insertion of a temporary valve in the ascending aorta to minimize hemodynamic instability during the procedure. Although further testing is needed and modifications in the instrumentation may be necessary, this study clearly FIGURE 7. The aortic root and cusps after the procedure. A, The aortic root at the end of the experiment. RCA, Right coronary artery ostium; LCA, left coronary artery ostium; NCC, cut noncoronary cusp; IVS, interventricular septum, which in pigs is thicker than in humans. 23 B, Removed aortic cusps. 472 The Journal of Thoracic and Cardiovascular Surgery c August 2009
6 demonstrates the feasibility of endovascular resection of the aortic cusps as a possible component of future transapical, off-pump AVR operations. We thank Shannon Wyszomierski, PhD, for her assistance in editing this manuscript, Brian Frankowski for his help in manufacturing the temporary valve, and Mazen Zenati, MD, MPh, PhD, for his assistance in the statistical analysis. References 1. Iung B, Baron G, Butchart EG, Delahaye F, Gohlke-Bärwolf C, Levang OW, et al. A prospective survey of patients with valvular heart disease in Europe: The Euro Heart Survey on Valvular Heart Disease. Eur Heart J. 2003;24: Kim BS, Soltesz EG, Cohn LH. Minimally invasive approaches to aortic valve surgery: Brigham experience. Semin Thorac Cardiovasc Surg. 2006;18: Tabata M, Umakanthan R, Cohn LH, Bolman RM III, Shekar PS, Chen FY, et al. Early and late outcomes of 1000 minimally invasive aortic valve operations. Eur J Cardiothorac Surg. 2008;33: Cribier A, Savin T, Saoudi N, Rocha P, Berland J, Letac B. Percutaneous transluminal valvuloplasty of acquired aortic stenosis in elderly patients: an alternative to valve replacement? Lancet. 1986;1: Letac B, Cribier A, Eltchaninoff H, Koning R, Derumeaux G. Evaluation of restenosis after balloon dilatation in adult aortic stenosis by repeat catheterization. Am Heart J. 1991;122: Klein A, Lee K, Gera A, Ports TA, Michaels AD. Long-term mortality, cause of death, and temporal trends in complications after percutaneous aortic balloon valvuloplasty for calcific aortic stenosis. J Interv Cardiol. 2006;19: Andersen HR, Knudsen LL, Hasenkam JM. Transluminal implantation of artificial heart valves. Description of a new expandable aortic valve and initial results with implantation by catheter technique in closed chest pigs. Eur Heart J. 1992; 13: Cribier A, Eltchaninoff H, Bash A, Borenstein N, Tron C, Bauer F, et al. Percutaneous transcatheter implantation of aortic valve prosthesis for calcific aortic stenosis: first human case description. Circulation. 2002;106: Wenaweser P, Buellesfeld L, Gerckens U, Grube E. Percutaneous aortic valve replacement for severe aortic regurgitation in degenerated bioprosthesis: the first valve in valve procedure using the Corevalve Revalving system. Catheter Cardiovasc Interven. 2007;70: Walther T, Simon P, Dewey T, Wimmer-Greinecker G, Falk V, Kasimir MT, et al. Transapical minimally invasive aortic valve implantation. Multicenter experience Circulation. 2007;116(Suppl I):I Cribier A, Eltchaninoff H, Tron C, Bauer F, Agatiello C, Nercolini D, et al. Treatment of calcific aortic stenosis with the percutaneous heart valve. Mid-term follow-up from the initial feasibility studies. The French experience. J Am Coll Cardiol. 2006;47: Marcheix B, Lamarche Y, Berry C, Asgar A, Laborde JC, Basmadjian A, et al. Surgical aspects of endovascular retrograde implantation of the aortic CoreValve bioprosthesis in high-risk older patients with severe symptomatic aortic stenosis. J Thorac Cardiovasc Surg. 2007;134: Grube E, Laborde JC, Gerckens U, Felderhoff T, Sauren B, Buellesfeld L, et al. Percutaneous implantation of the CoreValve self-expanding valve prosthesis in high-risk patients with aortic valve disease. Circulation. 2006;114: Vahanian A, Alfieri OR, Al-Attar N, Antunes MJ, Bax J, Cormier B, et al. Transcatheter valve implantation for patients with aortic stenosis: a position statement from the European Association of Cardio-Thoracic Surgery (EACTS) and the European Society of Cardiology (ESC), in collaboration with the European Association of Percutaneous Cardiovascular Interventions (EAPCI). Eur J Cardiothorac Surg. 2008;34: Kouchouks NT, Blackstone EH, Doty DB, Hanley FL, Karp RB. Aortic valve disease. In: Kirklin JW, Barratt-Boyes BG, editors. Cardiac surgery. 3rd ed. Vol 1. New York: Churchill Livingstone; p Rao V, Jamieson E, Ivanonv J, Armstrong S, David TE. Prosthesis patient mismatch affects survival after aortic valve replacement. Circulation. 2000; 102(Suppl III):III Flecher EM, Curry JW, Joudinaud TM, Kegel CL, Weber PA, Duran CMG. Coronary flow obstruction in percutaneous aortic valve replacement. An in vitro study. Eur J Cardiothorac Surg. 2007;32: Hanzel GS, O Neill WW. Complications of percutaneous aortic valve replacement: experience with the Cribier-EdwardsÔ percutaneous heart valve. Eurointervention Suppl. 2006;1(Suppl A):A Quaden R, Attmann T, Boening A, Cremer J, Lutter G. Percutaneous aortic valve replacement: resection before implantation. Eur J Cardiothorac Surg. 2005;27: Quaden R, Attmann T, Schünke M, Theisen-Kunde D, Cramer J, Lutter G. Percutaneous aortic valve replacement: endovascular resection of human aortic valve in situ. J Thorac Cardiovasc Surg. 2008;135: Vandenberghe S, Salizzoni S, Bajona P, Zehr KJ, Speziali G. In vitro testing of a temporary catheter-based aortic parachute valve. ASAIO J. 2008;54: Stouffer GA, Uretsky BF. Hemodynamic changes of aortic regurgitation. Am J Med Sci. 1997;314: Crick SJ, Sheppard MN, Ho SY, Gebstein L, Anderson RH. Anatomy of the pig heart: comparison with normal human cardiac structure. J Anat. 1998;193: Pai RG, Kapoor N, Bansal RC, Varadarajan P. Malignant natural history of asymptomatic severe aortic stenosis: benefit of aortic valve replacement. Ann Thorac Surg. 2006;82: Svensson LG, Dewey T, Kapadia S, Roselli EE, Stewart A, Williams M, et al. United States feasibility study of transcatheter insertion of a stented aortic valve by the left ventricular apex. Ann Thorac Surg. 2008;86: Walther T, Falk V, Kempfert J, Borger MA, Fassl J, Chu MWA, et al. Transapical minimally invasive aortic valve implantation; the initial 50 patients. Ann Thorac Surg. 2008;86: Ardehali A, Segal J, Cheitlin MD. Coronary blood flow reserve in acute aortic regurgitation. 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2 Brigham and Women s Hospital, Boston, MA.
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