Degenerative aortic valve (AV) stenosis is the most
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1 Crimping May Affect the Durability of Transcatheter Valves: An Experimental Analysis ADULT CARDIAC Philipp Kiefer, MD, Felix Gruenwald, Joerg Kempfert, MD, Heike Aupperle, PhD, Joerg Seeburger, MD, Friedrich Wilhelm Mohr, MD, PhD, and Thomas Walther, MD, PhD Department of Cardiac Surgery, Heart Center and Institute of Pathology, Faculty of Veterinary Medicine, University of Leipzig, Leipzig, Germany Background. Transcatheter aortic valve implantation has gained widespread acceptance to treat elderly high-risk patients with aortic stenosis. We used a subcutaneous rat model to evaluate whether crimping may affect valve longterm durability. Methods. Standard Sapien transcatheter valves (Edwards Lifesciences, Irvine, CA) were crimped for different durations (1 hour, 1 day, 1 month) and uncrimped, and leaflet pieces as well as control tissue (Perimount Magna, Edwards) were then implanted subcutaneously in 15 male weanling Sprague-Dawley rats for 12 weeks. Grade of calcification was measured by freeze-dried mass and van Kossa staining. Histologic and electron microscopic examination were performed to investigate potential leafletfragmentation caused by crimping. Results. There were no differences in calcification among the groups. The calcium carbonate concentrations in all samples ranged from 0.1 to 100 mg/g dry weight. Leaflet morphology, however, differed from no fragmentation (control group) to highly fragmented tissue (1-month crimped). These differences reached statistical significance between crimped and non-crimped leaflets (p < 0.003). Conclusions. Transcatheter valve crimping does not necessarily affect leaflet calcification. However, the structural changes of the leaflets that were caused by crimping may have clinical significance. Duration of crimping should be as short as possible, and very tight crimping to small diameters should be avoided. (Ann Thorac Surg 2011;92:155 60) 2011 by The Society of Thoracic Surgeons Degenerative aortic valve (AV) stenosis is the most common heart valve disease in Western countries. Untreated, the outcome is poor, and progression will lead to heart failure and death [1]. AV replacement represents the current standard care, with excellent operative and long-term results [2 4]. However, comorbidities in elderly patients lead to a higher perioperative risk; therefore, transcatheter techniques, such as the transfemoral or transapical procedures for AV implantation (AVI), have recently been established [5, 6]. The value of these procedures is the decrease in complications related to cardiopulmonary bypass, including stroke and organ failure, and also the reduction of procedure time and hospital stay. The balloon-expandable Edwards-Sapien prosthesis (Edwards Lifesciences, Irvine, CA) is a frequently used biologic stent prosthesis that can be implanted through transapical and transfemoral access. In case of malfunction or incorrect positioning with subsequent rapid hemodynamic deterioration, however, rescue implantation of a second prosthesis after the valve-in-valve concept [7, 8] may be necessary. Because in current practice the additional prosthesis has to be prepared on the shelf, which requires a certain amount of time, a precrimped Accepted for publication March 9, Address correspondence to Dr Kiefer, Heart Center, Leipzig University, Struempelstrasse 39, Leipzig, Germany; p.kiefer@med. uni-leipzig.de. valve would facilitate the immediate availability of the second prosthesis; however, use of a precrimped Sapien valve has not been reported. We therefore used a subcutaneous rat model to evaluate the influence of precrimping on bovine tissue structure and valve short-term durability. Material and Methods The Sapien Valve The Edwards Sapien bioprosthesis is made of bovine pericardium and is fixed on a stainless steel stent. For anticalcific treatment, the leaflets are treated with the Thermafix procedure (Edwards Lifesciences). This method combines glutaraldehyde fixation for structural stabilization, the XenoLogiX (Edwards Lifesciences) treatment for extraction of phospholipids, and a new, mild heat treatment that removes unstable glutaraldehyde moieties. The prosthesis is available in sizes of 23 and 26 mm as well as 29 mm for experimental analysis. In a standard implantation procedure, each valve is crimped with its individual size-specific crimper (Fig 1)to be implanted through a 24F sheath [9, 10]. The 26-mm prostheses were used in this study. Before implantation into the rat model, 20 prostheses were divided in four groups and individually crimped for a defined duration: group 1, uncrimped; group 2, 1 hour; group 3, 1 day; and group 4, 1 month. This was followed 2011 by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur
2 ADULT CARDIAC 156 KIEFER ET AL Ann Thorac Surg CRIMPING AFFECTS TRANSCATHETER VALVES 2011;92: Fig 1. Standardized crimping procedure for the Sapien valve in three steps: (A) the Sapien valve with natrium chloride (0.9%), (B) the Sapien valve crimped on a balloon catheter, and (C) the valve is placed in a loader for implantation through a 24F sheath. by resection of 60 valve leaflets from the prosthesis. All leaflets were rinsed with sterile water and subcutaneously implanted in the animal model. The control was the Perimount Magna prosthesis (Edwards Lifesciences), which is used for conventional operations and is made of the same components as the Sapien prosthesis (Fig 2). Animal Model A standard subcutaneous rat model using 15 weanling male Sprague-Dawley rats (21 days old) was used. This standard animal model for analysis of calcification is equivalent to a long term of in vivo implantation [11 19]. As required by the current regulations on the protection of animals, consent was obtained from the German governmental offices after outlining the study protocol in detail. Animals received humane care in compliance with the Guide for the Care and Use of Laboratory Animals (National Institutes of Health publication 85-23, revised 1985). Surgical Procedure The implantation and explantation operations were performed under sterile conditions using inhalation anesthesia (4% isoflurane for induction, and 2% to 3% isoflurane during the operation). Five dorsal horizontal 1.5-cmlong incisions were made and separate subcutaneous pouches prepared. Five leaflets, 1 from each group, were implanted in every animal. The implantation was done without folding or distortion of the samples. The skin was sutured with 4-0 Prolene (Ethicon, Somerville, NJ) and covered with medical aerosol glue. After 12 weeks, the leaflets were explanted, and each leaflet was cut in 3 slices and underwent histologic, electron microscopic, and calcium-level analysis. Tissue Analysis Mass measurements of freeze-dried samples were used to quantify the grade of calcification in milligrams/gram dry weight related to blood calcium levels. Additional histologic and electron microscopic examinations were performed to investigate potential leaflet fragmentation. Material for histologic investigations was fixed in formalin, embedded in paraplast, and slides were stained with hematoxylin and eosin (HE), picrosirius red, and van Kossa staining. The samples were blinded, and the area of calcification was measured with light microscopy using an interactive digital image analysis system (Olympus DP-soft, Olympus Europa GmbH, Hamburg, Ger- Fig 2. Schematic description shows the study design.
3 Ann Thorac Surg KIEFER ET AL 2011;92: CRIMPING AFFECTS TRANSCATHETER VALVES Table 1. Calcium Levels for Bovine Pericardial Leaflets a Group (n 15) Crimp Time Ca 2 Levels b (mg/g dry weight) Magna p Value vs 157 Uncrimped ADULT CARDIAC Magna Uncrimped Sapien Uncrimped hour day mon a After 12 weeks of implantation highest calcium levels are shown in the uncrimped Sapien valve. mean. b Data are presented with the standard error of the many). The degree of fragmentation was graded as no fragmentation; mild: multifocally single discontinuous collagen bundles; moderate: multifocally extended areas of discontinuous collagen bundles and elastic fibers; marked: the whole tissue is destructed and only short fragments are seen. For ultrastructural examinations, the glutaraldehyde-fixed leaflets were embedded in Epon 120 and contrasted by uranyl acetate and tannin. Statistical analysis was performed using SPSS software (SPSS Inc, Chicago, IL). Results are given as mean standard deviation. The Wilcoxon test was applied to assess the difference between crimped leaflets and noncrimped leaflets as well as the time-dependent variations within the leaflets. Results No infection was evident at explantation. All samples were explanted, and there were no associated difficulties. Calcification of Specimen After 12 weeks of implantation, all samples showed similar levels of calcification. The calcium carbonate levels differed from 0.1 to 100 mg/g freeze-dried weight (Table 1). Calcium levels were higher in the uncrimped and 1-month group than in the 1-hour and 1-day crimped group; however, this was not statistically significant. Even comparisons with the control group showed no statistical significance. Furthermore, the serum levels of calcium were in the normal range in all animals. Light microscopy (Van Kossa) staining showed similar results. Plaque-like or diffuse calcification patterns were seen. These areas were measured digitally, and the calcification area was determined. Overall, the area of calcification was not significantly different among the groups. Specimen Fragmentation The degree of fragmentation was different among the leaflets crimped for 1 month compared with 1 day and uncrimped (Table 2, Figs 3 to 7). All samples were covered with a thin layer of fibroangioblastic granulation tissue. All of the uncrimped Magna samples (Fig 3) were well preserved, and the collagen fibers were regularly structured. A moderate invasion of macrophages and giant cells was detected, along with signs of phagocytosis. Granulomas were present multifocally, and there was evidence of intralesional craze. Signs of calcification were seen in 7 of 15 samples. The uncrimped Sapien (Fig 4) implants showed small fragmentations of the collagen fibers and the structure appeared low-graded irregular. Moderate invasion of macrophages and giant cells was detected along with signs of phagocytosis. Granulomas were seen multifocally and intralesional craze. Signs of calcification were seen in 7 of 15 samples. The 1-hour crimped Sapien (Fig 5) implants showed small fragmentations of the collagen fibers, and the structure appeared mildly irregular. Moderate invasion of macrophages, giant cells, and signs of phagocytosis could be detected. Signs of calcification were found in 5 of 15 samples. The 1-day crimped Sapien (Fig 6) implants showed moderate fragmentations of the collagen fibers, and the Table 2. Degrees of Fragmentation and Irregularity of the Leaflet Collagen Fibers a Irregular, No. Group Crimp Time Regular No. Mildly Moderately Markedly Magna (uncrimped) 13 2 Sapien (uncrimped) hour day mon a Data are for 15 leaflets.
4 ADULT CARDIAC 158 KIEFER ET AL Ann Thorac Surg CRIMPING AFFECTS TRANSCATHETER VALVES 2011;92: Fig 3. Samples of pericardium leaflets from the Magna control valve. (A) Typical structure of bovine pericardium mainly composed of regularly structured collagen (red), a few elastic fibers (purple), and single small vessels (picrosirius red stain). (B) Regular structure of collagen fiber bundles (c) and single elastic fibers (e) are visible with electron microscopy (tannin contrast). structure appeared moderately irregular. As well, a moderate invasion of macrophages, giant cells and signs of phagocytosis could be detected. Signs of calcification were found in 5 of 15 samples. The 1-month crimped Sapien (Fig 7) implants showed marked fragmentations of the collagen fibers, and the structure appeared high-graded irregular. Signs of calcification were found in 5 of 15 samples. Alterations of the leaflet structure and its connective tissue were seen by light microscopy as well as in the ultrastructural investigations. The collagen fibers in the leaflets of the Magna valve (control) and the uncrimped Sapien valve were arranged in long straight bundles, with some deposits of elastin in between. Fibrocytes were seen only rarely, and mesothelial cells were absent. After short time of crimping (1 hour), the collagen bundles appeared to be wavy, but only rare fragmentations were seen. With increasing crimp-time, the number of fragmented collagen fibers increased (Figs 3 to 7). Comment Aortic valve replacement is the standard treatment for aortic stenosis and is associated with excellent results [1 4]. Recently, two additional procedures have been evaluated in clinical practice: the transcatheter approach through the femoral arteries or the apex of the heart. These techniques are used for the implantation of biologic prostheses. During the procedure, however, complications such as malfunction can occur [7, 8]; therefore, rapid implantation of a second prepared prosthesis is compulsory to ensure hemodynamic stable conditions and to avoid using the heart-lung machine. Fig 4. Samples of uncrimped pericardium Sapien leaflets. (A) Typical structure of bovine pericardium mainly composed of regularly structured collagen (red), a few elastic fibers, (purple), and single small vessels (picrosirius red stain) (B) Regular structure of collagen fiber bundles are visible with electron microscopy (tannin contrast). Fig 5. Samples of 1-hour crimped pericardium Sapien leaflets. (A) Wavy arrangement and single fragmentations of the collagen and elastic fibers (arrows; picrosirius red stain), (B) Wavy arrangement and focal fragmentation (arrows) of collagen fibers (c) and single elastic fibers (e) are visible with electron microscopy (tannin contrast).
5 Ann Thorac Surg KIEFER ET AL 2011;92: CRIMPING AFFECTS TRANSCATHETER VALVES 159 Fig 6. Samples of 1-day crimped pericardium Sapien leaflets. (A) Multiple fragmentations of the collagen and elastic fibers (arrows; picrosirius red stain). (B) Multiple fragmentations (arrows) of collagen fibers (c) and single elastic fibers (e) are visible with electron microscopy (tannin contrast). ADULT CARDIAC In contrast to the no-touch technique in conventional valve operations, the preoperative crimping process may harm transcatheter valves. Crimping, however, is inevitable in order to be able to insert transcatheter valves through small-diameter sheaths. The potential effect of crimping on the calcification, strength, and durability of the prosthesis, however, has never been evaluated systematically. We sought to analyze the effect of crimping on the Sapien valve in a short-term rat model. The experimental subcutaneous rat model is well established and often used, with reproducible results when different types of tissue are examined [11 17]. Overall, we found no statistical evidence that longterm precrimping leads to higher rate of calcification compared with noncrimping or the control group. However, histologic and electron microscopic examinations showed major changes in the structural morphology of collagen fibers. No significant changes in the structure were detected when precrimping was performed for less than 1 day. There was, however, a higher rate of phagocytosis and cell destruction when the precrimp duration extended beyond 1 day. Fig 7. Samples of 1-month crimped pericardium Sapien leaflets. Intense fragmentations of the collagen and elastic fibers (arrows) are seen (picrosirius red stain). (No electron microscopy.) In conclusion, precrimping of the Sapien valve seems to have no influence on the grade of calcification; however, it significantly influences the ultrastructure of the pericardial tissue. To what extent these changes correlate with medium-term and long-term durability is unknown so far; however, we deduce from the results of this study that extensive precrimping should be avoided. For the future, it will be interesting to examine the potential effect of even tighter crimping on durability. This will be of special clinical importance because smaller devices are being developed. References 1. Carabello BA. Clinical practice aortic stenosis. N Engl J Med 2002;346: Bonow RO, Carabello BA, Chatterjee K. ACC/AHA 2006 guidelines for the management of patients with valvular heart disease: executive summary. Circulation 2006;114: Grocott-Mason RM, Lund O, Elwidaa H, et al. Long-term results after aortic valve replacement in patients with congestive heart failure. Homografts vs prosthetic valves. Eur Heart J 2000;21: Borger MA, Ivanov J, Armstrong S, et al. Twenty-year results of the Hancock II bioprosthesis. J Heart Valve Dis 2006;15: Walther T, Falk V, Borger MA, et al. Minimally invasive transapical beating heart aortic valve implantation-proof of concept. Eur J Cardiothorac Surg 2007;31: Cribier A, Eltchaninoff H, Bash A, et al. Percutaneous transcatheter implantation of an aortic valve prosthesis for calcific aortic stenosis: first human case description. Circulation 2002;106: Walther T, Kempfert J, Borger MA, et al. Human minimally invasive off-pump valve-in-a-valve implantation. Ann Thorac Surg 2008;85: Kempfert J, Van Linden A, Linke A, et al. Transapical off-pump valve-on-valve implantation in patients with degenerated aortic xenografts. Ann Thorac Surg 2010;89: Walther T, Dewey T, Borger MA, et al. Transapical aortic valve implantation: step by step. Ann Thorac Surg 2009; 87: Walther T, Chu MWA, Mohr FW. Transcatheter aortic valve implantation: time to expand? Curr Opin Cardiol 2008;23: Schoen FJ, Tsao JW, Levy RJ. Calcification of bovine pericardium used in cardiac valve bioprostheses. Am J Pathol 1986;123: Owen J, Lantz GC, Hiles MC, VanVleet J, Martin BR, Geddes LA. Calcification potential of small intestinal submucosa in a rat subcutaneous model. J Surg Res 1997;71: Milano A, Bortolotti U, Talenti E, Valfre C, Arbustini E, Valante M. Calcific degeneration as the main cause of porcine bioprosthetic valve failure. Am J Cardiol 1984;53:
6 ADULT CARDIAC 160 KIEFER ET AL Ann Thorac Surg CRIMPING AFFECTS TRANSCATHETER VALVES 2011;92: Schoen FJ, Levy RJ. Bioprosthetic heart valve failure: pathology and pathogenesis. Cardiol Clin 1984;2: Mako WJ, Shah A, Vesely I. Mineralization of glutaraldehyde-fixed porcine aortic valve cusps in the subcutaneous rat model: analysis of variations in implant site and cuspal quadrants. J Biomed Mater Res 1999;45: Levy RJ, Schoen FJ, Golomb G. Bioprosthetic heart valve calcification: Clinical features, pathobiology, and prospects for prevention. CRC Crit Rev Biocompat 1986;2: Walther T, Falk V, Autschbach R, et al. Comparison of different anticalcification treatments for stentless bioprostheses. Ann Thorac Surg. 1998;66: Walther T, Falk V, Diegeler A, et al. Effectiveness of different anticalcification treatments for stentless aortic bioprostheses. Thorac Cardiovasc Surg 1999;47: Brockbank KGM, Song YC. Mechanisms of bioprosthetic heart valve calcification. Transplantation 2003;75: The Society of Thoracic Surgeons: Forty-Eighth Annual Meeting Mark your calendars for the Forty-Eighth Annual Meeting of The Society of Thoracic Surgeons (STS) to be held at the Greater Fort Lauderdale/Broward County Convention Center, Fort Lauderdale, Florida, from January 30 February 1, Come to Fort Lauderdale to learn from the experts, network with colleagues from around the world, and prepare for whatever the future may hold. This pre-eminent educational event in cardiothoracic surgery is open to all physicians, residents, fellows, engineers, perfusionists, physician assistants, nurses, or other interested individuals who work with cardiothoracic surgeons. Meeting attendees will be provided with the latest scientific information for practicing cardiothoracic surgeons. Attendees will benefit from traditional Abstract Presentations, as well as Surgical Forums, Breakfast Sessions, Surgical Motion Pictures, and Procedural Hands-On Courses. Parallel sessions on Monday and Tuesday will focus on specific subspecialty interests. An advance program with a registration form, hotel reservation information, and details regarding spouse/ guest activities will be mailed to STS members this fall. Nonmembers may contact the Society s secretary, David A. Fullerton, MD, to receive a copy of the advanced program; however, detailed meeting information will be available on the STS website at David A. Fullerton, MD Secretary The Society of Thoracic Surgeons 633 N Saint Clair St, Suite 2320 Chicago, IL Telephone: (312) Fax: (312) sts@sts.org website: by The Society of Thoracic Surgeons Ann Thorac Surg 2011;92: /$36.00 Published by Elsevier Inc
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