Abstract
Despite the wide choice of commercial heart valve prostheses, cryopreserved semilunar allograft heart valves (C-AHV) are required, and successfully transplanted in selected groups of patients. The expiration limit (EL) criteria have not been defined yet. Most Tissue Establishments (TE) use the EL of 5 years. From physiological, functional, and surgical point of view, the morphology and mechanical properties of aortic and pulmonary roots represent basic features limiting the EL of C-AHV. The aim of this work was to review methods of AHV tissue structural analysis and mechanical testing from the perspective of suitability for EL validation studies. Microscopic structure analysis of great arterial wall and semilunar leaflets tissue should clearly demonstrate cells as well as the extracellular matrix components by highly reproducible and specific histological staining procedures. Quantitative morphometry using stereological grids has proved to be effective, as the exact statistics was feasible. From mechanical testing methods, tensile test was the most suitable. Young’s moduli of elasticity, ultimate stress and strain were shown to represent most important AHV tissue mechanical characteristics, suitable for exact statistical analysis. C-AHV are prepared by many different protocols, so as each TE has to work out own EL for C-AHV.
Similar content being viewed by others
References
Adham M, Gournier JP, Favre JP et al (1996) Mechanical characteristics of fresh and frozen human descending thoracic aorta. J Surg Res 64:32–34. https://doi.org/10.1006/jsre.1996.0302
Avanzini A, Battini D (2016) Integrated experimental and numerical comparison of different approaches for planar biaxial testing of a hyperelastic material. Adv Mater Sci Eng 2016:1–12. https://doi.org/10.1155/2016/6014129
Azadani AN, Chitsaz S, Matthews PB et al (2012) Comparison of mechanical properties of human ascending aorta and aortic sinuses. Ann Thorac Surg 93:87–94. https://doi.org/10.1016/j.athoracsur.2011.08.002
Bäck M, Gasser TC, Michel JB, Caligiuri G (2013) Biomechanical factors in the biology of aortic wall and aortic valve diseases. Cardiovasc Res 99:232–241. https://doi.org/10.1093/cvr/cvt040
Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. Churchill Livingstone, Edinburgh
Barratt-Boyes BG (1964) Homograft aortic valve replacement in aortic incompetence and stenosis. Thorax 19:131–150. https://doi.org/10.1136/thx.19.2.131
Barrett TJ (2020) Macrophages in atherosclerosis regression. ATVB 40:20–33. https://doi.org/10.1161/ATVBAHA.119.312802
Berillis P (2013) The role of collagen in the aorta’s structure. Open Circ Vasc J 6:1–8. https://doi.org/10.2174/1877382601306010001
Billiar KL, Sacks MS (2000) Biaxial mechanical properties of the native and glutaraldehyde-treated aortic valve cusp: Part II—A structural constitutive model. J Biomech Eng 122:327–335. https://doi.org/10.1115/1.1287158
Blassova T, Tonar Z, Tomasek P et al (2019) Inflammatory cell infiltrates, hypoxia, vascularization, pentraxin 3 and osteoprotegerin in abdominal aortic aneurysms—A quantitative histological study. PLoS ONE 14:e0224818. https://doi.org/10.1371/journal.pone.0224818
Boethig D, Goerler H, Westhoff-Bleck M et al (2007) Evaluation of 188 consecutive homografts implanted in pulmonary position after 20 years. Eur J Cardio-thoracic Surg 32:133–142. https://doi.org/10.1016/j.ejcts.2007.02.025
Boethig D, Horke A, Hazekamp M et al (2019) An European study on decellularized homografts for pulmonary valve replacement: initial results from the prospective ESPOIR Trial and ESPOIR Registry data. Eur J Cardiothorac Surg 56:503–509. https://doi.org/10.1093/ejcts/ezz054
Borghi A, New SEP, Chester AH et al (2013) Time-dependent mechanical properties of aortic valve cusps: effect of glycosaminoglycan depletion. Acta Biomater 9:4645–4652. https://doi.org/10.1016/j.actbio.2012.09.001
Brazile B, Wang B, Wang G et al (2015) On the bending properties of porcine mitral, tricuspid, aortic, and pulmonary valve leaflets. J Long Term Eff Med Implants 25:41–53. https://doi.org/10.1615/JLongTermEffMedImplants.2015011741
Brewer RJ, Deck JD, Capati B, Nolan SP (1976) The dynamic aortic root. Its role in aortic valve function. J Thorac Cardiovasc Surg 72:413–417. https://doi.org/10.1016/S0022-5223(19)40069-X
Brockbank KG, Schenke-Layland K, Greene ED et al (2012) Ice-free cryopreservation of heart valve allografts: better extracellular matrix preservation in vivo and preclinical results. Cell Tissue Bank 13(4):663–671. https://doi.org/10.1007/s10561-011-9288-7
Brockbank KG, Wright GJ, Yao H et al (2011) Allogeneic heart valve storage above the glass transition at -80°C. Ann Thorac Surg 91(6):1829–1835. https://doi.org/10.1016/j.athoracsur.2011.02.043
Carr-White G, Afoke A, Birks E et al (2000) Aortic root characteristics of human pulmonary autografts. Circulation 102:III-15–III-21. https://doi.org/10.1161/01.CIR.102.suppl
Cavalcante JL, Lima JAC, Redheuil A, Al-Mallah MH (2011) Aortic stiffness: current understanding and future directions. J Am Coll Cardiol 57:1511–1522. https://doi.org/10.1016/j.jacc.2010.12.017
Cavinato C, Helfenstein-Didier C, Olivier T et al (2017) Biaxial loading of arterial tissues with 3D in situ observations of adventitia fibrous microstructure: A method coupling multi-photon confocal microscopy and bulge inflation test. J Mech Behav Biomed Mater 74:488–498. https://doi.org/10.1016/j.jmbbm.2017.07.022
Cebotari S, Lichtenberg A, Tudorache I et al (2006) Clinical application of tissue engineered human heart valves using autologous progenitor cells. Circulation 114:132–137. https://doi.org/10.1161/CIRCULATIONAHA.105.001065
Chandran KB, Udaykumar HS, Reinhardt JM (2011) Image-based computational modeling of the human circulatory and pulmonary systems: methods and applications. Springer, Switzerland
Chiang H-Y, Korshunov VA, Serour A et al (2009) Fibronectin is an important regulator of flow-induced vascular remodeling. ATVB 29:1074–1079. https://doi.org/10.1161/ATVBAHA.108.181081
Chow MJ, Zhang Y (2011) Changes in the mechanical and biochemical properties of aortic tissue due to cold storage. J Surg Res 171:434–442. https://doi.org/10.1016/j.jss.2010.04.007
Christie G, Barratt-Boyes B (1995) Mechanical properties of porcine pulmonary valve leaflets: How do they differ from aortic leaflets? Ann Thorac Surg 60:S195–S199. https://doi.org/10.1016/0003-4975(95)00279-T
Cocciolone AJ, Hawes JZ, Staiculescu MC et al (2018) Elastin, arterial mechanics, and cardiovascular disease. Am J Physiol Hear Circ Physiol 315:H189–H205. https://doi.org/10.1152/ajpheart.00087.2018
Conza N (2005) Part 3: Tissue preconditioning. Exp Tech 29:43–46. https://doi.org/10.1111/j.1747-1567.2005.tb00213.x
Cox R (1981) Basis for the altered arterial wall mechanics in the spontaneously hypertensive rat. Hypertension 3:485–495. https://doi.org/10.1161/01.HYP.3.4.485
Davies H, Lessof MH, Roberts CI et al (1965) Homograft replacement of the aortic valve: follow-up studies in twelve patients. Lancet 1:926–929. https://doi.org/10.1016/S0140-6736(65)91252-3
de By TMMH, Parker R, Delmo Walter EM, Hetzer R (2012) Cardiovascular tissue banking in Europe. HSR Proc Intensive Care Cardiovasc Anesth 4:251–260
de By TMMH, McDonald C, Susner S et al (2017) Validation of microbiological testing incardiovascular tissue banks: results of a quality round trial. Eur J Cardiothorac Surg 52:895–900. https://doi.org/10.1093/ejcts/ezx178
de By TMMH (2020) International benchmarking in cardio-thoracic surgery. Dissertation, Erasmus University, Rotterdam, Netherlands
Deboer O, Becker A, Vanderwal A (2003) T lymphocytes in atherogenesis—functional aspects and antigenic repertoire. Cardiovasc Res 60:78–86. https://doi.org/10.1016/S0008-6363(03)00341-9
Dekker S, van Geemen D, van den Bogaerdt AJ et al (2018) Sheep-specific immunohistochemical panel for the evaluation of regenerative and inflammatory processes in tissue-engineered heart valves. Front Cardiovasc Med 15(5):105. https://doi.org/10.3389/fcvm.2018.00105
Dekens E, van Damme E, Jashari R et al (2019) Durability of pulmonary homografts for reconstruction of the right ventricular outflow tract: How relevant are donor-related factors? Interact Cardiovasc Thorac Surg 28(4):503–509. https://doi.org/10.1093/icvts/ivy316
Delgadillo JOV, Delorme S, El-Ayoubi R et al (2010) Effect of freezing on the passive mechanical properties of arterial samples. J Biomed Sci Eng 03:645–652. https://doi.org/10.4236/jbise.2010.37088
Drangova M, Holdsworth DW, Boyd CJ et al (1993) Elasticity and geometry measurements of vascular specimens using a high-resolution laboratory CT scanner. Physiol Meas 14:277–290
Duran CG, Gunning AJ (1962) A method for placing a total homologous aortic valve in the subcoronary position. Lancet 2:488–489. https://doi.org/10.1016/S0140-6736(62)90346-X
Eckert CE, Fan R, Mikulis B et al (2013) On the biomechanical role of glycosaminoglycans in the aortic heart valve leaflet. Acta Biomater 9:4653–4660. https://doi.org/10.1016/j.actbio.2012.09.031
Ferguson JJ, Julius S, Randall OS (1984) Stroke volume - Pulse pressure relationships in borderline hypertension: A possible indicator a decreased arterial compliance. J Hypertens 2:S397–S399
Fiala R, Kochová P, Kubíková T et al (2019) Mechanical and structural properties of human aortic and pulmonary allografts do not deteriorate in the first 10 years of cryopreservation and storage in nitrogen. Cell Tissue Bank 20:221–241. https://doi.org/10.1007/s10561-019-09762-x
Fridez P, Makino A, Miyazaki H et al (2001) Short-term biomechanical adaptation of the rat carotid to acute hypertension: contribution of smooth muscle. Ann Biomed Eng 29:26–34. https://doi.org/10.1114/1.1342054
Fridez P, Zulliger M, Bobard F et al (2003) Geometrical, functional, and histomorphometric adaptation of rat carotid artery in induced hypertension. J Biomech 36:671–680. https://doi.org/10.1016/S0021-9290(02)00445-1
Germain M, Strong DM, Dowling G et al (2016) Disinfection of human cardiac valve allografts in tissue banking: systematic review report. Cell Tissue Bank 17(4):593–601. https://doi.org/10.1007/s10561-016-9570-9
Gilpin CM (2005) Cyclic loading of porcine coronary arteries. Disertation, Georgia Institute of Technology
Goffin YAH, de Gouveia RH, Szombathelyi T et al (1997) Morphologis study of homograft valves before and after cryopreservation and after short-term implantation in patients. Cardiovasc Pathol 6:35–42. https://doi.org/10.1016/S1054-8807(96)00072-5
Grashow JS, Sacks MS, Liao J, Yoganathan AP (2006) Planar biaxial creep and stress relaxation of the mitral valve anterior leaflet. Ann Biomed Eng 34:1509–1518. https://doi.org/10.1007/s10439-006-9183-8
Greenwald SE (2007) Ageing of the conduit arteries. J Pathol 211:157–172. https://doi.org/10.1002/path.2101
Halushka MK, Angelini A, Bartoloni G et al (2016) Consensus statement on surgical pathology of the aorta from the Society for Cardiovascular Pathology and the Association For European Cardiovascular Pathology: II. Noninflammatory degenerative diseases — nomenclature and diagnostic criteria. Cardiovasc Pathol 25:247–257. https://doi.org/10.1016/j.carpath.2016.03.002
Hamdan A, Guetta V, Konen E et al (2012) Deformation dynamics and mechanical properties of the aortic annulus by 4-dimensional computed tomography: insights into the functional anatomy of the aortic valve complex and implications for transcatheter aortic valve therapy. J Am Coll Cardiol 59:119–127. https://doi.org/10.1016/j.jacc.2011.09.045
Hasan A, Ragaert K, Swieszkowski W et al (2014) Biomechanical properties of native and tissue engineered heart valve constructs. J Biomech 47:1949–1963. https://doi.org/10.1016/j.jbiomech.2013.09.023
He R, Guo D-C, Sun W et al (2008) Characterization of the inflammatory cells in ascending thoracic aortic aneurysms in patients with Marfan syndrome, familial thoracic aortic aneurysms, and sporadic aneurysms. J Thorac Cardiovasc Surg 136(922–929):929.e1. https://doi.org/10.1016/j.jtcvs.2007.12.063
Heimbecker RO, Baird RJ, Lajos TZ et al (1962) Homograft replacement of the human mitral valve. A preliminary report. Can Med Assoc J 86:805–809
Hepfer RG, Brockbank KG, Chen Z et al (2016) Comparison and evaluation of biomechanical, electrical, and biological methods for assessment of damage to tissue collagen. Cell Tissue Bank 17(3):531–539. https://doi.org/10.1007/s10561-016-9560-y
Hlubocký J, Mokráček A, Nováček V et al (2011) Mechanical properties of mitral allografts are not reasonably influenced by cryopreservation in sheep model. Physiol Res 60:475–482. https://doi.org/10.33549/physiolres.932074
Holzapfel GA, Ogden RW (eds) (2003) Biomechanics of soft tissue in cardiovascular systems. Springer, Udine
Huang HY, Balhouse BN, Huang S (2012) Application of simple biomechanical and biochemical tests to heart valve leaflets: Implications for heart valve characterization and tissue engineering. Proc Inst Mech Eng Part H J Eng Med 226:868–876. https://doi.org/10.1177/0954411912455004
Huber AJ, Aberle T, Schleicher M et al (2013) Characterization of a simplified ice-free cryopreservation method for heart valves. Cell Tissue Bank 14(2):195–203. https://doi.org/10.1007/s10561-012-9319-z
Imura T, Yamamoto K, Satoh T et al (1990) In vivo viscoelastic behavior in the human aorta. Circ Res 66:1413–1419. https://doi.org/10.1161/01.RES.66.5.1413
Iop L, Paolin A, Aguiari P et al (2017) Decellularized cryopreserved allografts as off-the-shelf allogeneic alternative for heart valve replacement: In vitro assessment before clinical translation. J Cardiovasc Transl Res 10(2):93–103. https://doi.org/10.1007/s12265-017-9738-0
Jett S, Laurence D, Kunkel R et al (2018a) An investigation of the anisotropic mechanical properties and anatomical structure of porcine atrioventricular heart valves. J Mech Behav Biomed Mater 87:155–171. https://doi.org/10.1016/j.jmbbm.2018.07.024
Jett S, Laurence D, Kunkel R et al (2018b) Biaxial mechanical data of porcine atrioventricular valve leaflets. Data Br 21:358–363. https://doi.org/10.1016/j.dib.2018.09.073
Kassab GS (2006) Biomechanics of the cardiovascular system: the aorta as an illustratory example. J R Soc Interface 3:719–740. https://doi.org/10.1098/rsif.2006.0138
Kaushik SD, Vinchurkar M, Patwardhan AM et al (1995) MTT assay as a viability test of homograft valves. Indian J Thorac Cardiovasc Sur 11:38–41
Khan S, Fakhouri F, Majeed W, Kolipaka A (2018) Cardiovascular magnetic resonance elastography: a review. NMR Biomed 31:e3853. https://doi.org/10.1002/nbm.3853
Kochová P, Kuncová J, Švíglerová J et al (2012) The contribution of vascular smooth muscle, elastin and collagen on the passive mechanics of porcine carotid arteries. Physiol Meas 33:1335–1351. https://doi.org/10.1088/0967-3334/33/8/1335
Kocová J (1970) Overall staining of connective tissue and the muscular layer of vessels. Folia Morphol (Praha) 18:293–295
Korossis S (2018) Structure-function relationship of heart valves in health and disease. In: Kirali K (ed) Structural insufficiency anomalies in cardiac valves. IntechOpen, Rijeka, pp 1–37
Kortsmit J, Driessen NJB, Rutten MCM, Baaijens FPT (2009) Non-destructive and non-invasive assessment of mechanical properties in heart valve tissue engineering. Tissue Eng - Part A 15:797–806. https://doi.org/10.1089/ten.tea.2008.0197
Krishnamurthy G, Ennis DB, Itoh A et al (2008) Material properties of the ovine mitral valve anterior leaflet in vivo from inverse finite element analysis. Am J Physiol Hear Circ Physiol 295:1141–1149. https://doi.org/10.1152/ajpheart.00284.2008
Kubíková T, Kochová P, Brázdil J et al (2017) The composition and biomechanical properties of human cryopreserved aortas, pulmonary trunks, and aortic and pulmonary cusps. Ann Anat 212:17–26. https://doi.org/10.1016/j.aanat.2017.03.004
Kular JK, Basu S, Sharma RI (2014) The extracellular matrix: Structure, composition, age-related differences, tools for analysis and applications for tissue engineering. J Tissue Eng 5:204173141455711. https://doi.org/10.1177/2041731414557112
Lacolley P, Regnault V, Avolio AP (2018) Smooth muscle cell and arterial aging: basic and clinical aspects. Cardiovasc Res 114:513–528. https://doi.org/10.1093/cvr/cvy009
Lally C, Reid AJ, Prendergast PJ (2004) Elastic behavior of porcine coronary artery tissue under uniaxial and equibiaxial tension. Ann Biomed Eng 32:1355–1364. https://doi.org/10.1114/B:ABME.0000042224.23927.ce
Länne T, Sonesson B, Bergqvist D et al (1992) Diameter and compliance in the male human abdominal aorta: influence of age and aortic aneurysm. Eur J Vasc Surg 6:178–184. https://doi.org/10.1016/s0950-821x(05)80237-3
Laurence D, Ross C, Jett S et al (2019) An investigation of regional variations in the biaxial mechanical properties and stress relaxation behaviors of porcine atrioventricular heart valve leaflets. J Biomech 83:16–27. https://doi.org/10.1016/j.jbiomech.2018.11.015
Li ZY, U-King-Im J, Tang TY et al (2008) Impact of calcification and intraluminal thrombus on the computed wall stresses of abdominal aortic aneurysm. J Vasc Surg 47:928–935. https://doi.org/10.1016/j.jvs.2008.01.006
Logrippo GA, Overhulse PR, Szilagyi DE et al (1955) Procedure for sterilization of arterial homografts with beta-propiolactone. Lab Invest 4:217–231
Longmore DB, Lockey E, Ross DN, Pickering BN (1966) The preparation of aortic valve homografts. Lancet 288:463–464. https://doi.org/10.1016/S0140-6736(66)92770-X
Macrae RA, Miller K, Doyle BJ (2016) Methods in mechanical testing of arterial tissue: a review. Strain 52:380–399. https://doi.org/10.1111/str.12183
Marra SP, Daghlian CP, Fillinger MF, Kennedy FE (2006a) Elemental composition, morphology and mechanical properties of calcified deposits obtained from abdominal aortic aneurysms. Acta Biomater 2:515–520. https://doi.org/10.1016/j.actbio.2006.05.003
Marra SP, Kennedy FE, Kinkaid JN, Fillinger MF (2006b) Elastic and rupture properties of porcine aortic tissue measured using inflation testing. Cardiovasc Eng 6:123–131. https://doi.org/10.1007/s10558-006-9021-5
Martin C, Sun W (2012) Biomechanical characterization of aortic valve tissue in humans and common animal models. J Biomed Mater Res A 100:1591–1599. https://doi.org/10.1002/jbm.a.34099
Mayne AS, Christie GW, Smaill BH et al (1989) An assessment of the mechanical properties of leaflets from four second-generation porcine bioprostheses with biaxial testing techniques. J Thorac Cardiovasc Surg 98:170–180
McNally RT, Brockbank KGM (1992) Issues surrounding the preservation of viable allograft heart valves. J Med Eng Technol 16:34–38. https://doi.org/10.3109/03091909209021955
Meershoek A, van Dijk RA, Verhage S et al (2016) Histological evaluation disqualifies IMT and calcification scores as surrogates for grading coronary and aortic atherosclerosis. Int J Cardiol 224:328–334. https://doi.org/10.1016/j.ijcard.2016.09.043
Mendelson K, Schoen FJ (2006) Heart valve tissue engineering: Concepts, approaches, progress, and challenges. Ann Biomed Eng 34:1799–1819. https://doi.org/10.1007/s10439-006-9163-z
Meng L-B, Yu Z-M, Guo P et al (2018) Neutrophils and neutrophil-lymphocyte ratio: Inflammatory markers associated with intimal-media thickness of atherosclerosis. Thromb Res 170:45–52. https://doi.org/10.1016/j.thromres.2018.08.002
Merryman WD, Engelmayr GC, Liao J, Sacks MS (2006) Defining biomechanical endpoints for tissue engineered heart valve leaflets from native leaflet properties. Prog Pediatr Cardiol 21:153–160. https://doi.org/10.1016/j.ppedcard.2005.11.001
Meyers MA, Chen P-Y, Lin AY-M, Seki Y (2008) Biological materials: Structure and mechanical properties. Prog Mater Sci 53:1–206. https://doi.org/10.1016/j.pmatsci.2007.05.002
Meyns B, Jashari R, Gewillig M et al (2005) Factors influencing the survival of cryopreserved homografts. The second homograft performs as well as the first. Eur J Cardiothorac Surg 28:211–216. https://doi.org/10.1016/j.ejcts.2005.03.041
Mirabet V, Carda C, Solves P et al (2008) Long-term storage in liquid nitrogen does not affect cell viability in cardiac valve allografts. Cryobiology 57(2):113–121. https://doi.org/10.1016/j.cryobiol.2008.07.008
Mohammad SN (1994) Effect of storage on tensile properties of natural heart valve tissue. University of Surrey, Disertation
Mohan D, Melvin J (1982) Failure properties of passive human aortic tissue. I—uniaxial tension tests. J Biomech 15:887–902. https://doi.org/10.1016/0021-9290(82)90055-0
Mohan D, Melvin JW (1983) Failure properties of passive human aortic tissue. II-Biaxial tension tests J Biomech 16:31–44. https://doi.org/10.1016/0021-9290(83)90044-1
Mori S, Spicer DE, Anderson RH (2018) Living anatomy of the aortic root. In: Vojáček J, Žáček P, Dominik J (eds) Aortic regurgitation. Springer, New York, pp 23–31
Mulligan-Kehoe MJ, Simons M (2014) Vasa vasorum in normal and diseased arteries. Circulation 129:2557–2566. https://doi.org/10.1161/CIRCULATIONAHA.113.007189
Muresian H (2018) Clinical and surgical anatomy of the aortic root. In: Vojáček J, Žáček P, Dominik J (eds) Aortic Regurgitation. Springer, New York, pp 7–21
Nava A, Mazza E, Haefner O, Bajka M (2004) Experimental observation and modelling of preconditioning in soft biological tissues. Lect Notes Comput Sci (including Subser Lect Notes Artif Intell Lect Notes Bioinform) 3078:1–8. https://doi.org/10.1007/978-3-540-25968-8_1
Nicosia MA (2007) A theoretical framework to analyze bend testing of soft tissue. J Biomech Eng 129:117–120. https://doi.org/10.1115/1.2401191
Novotný R, Slížová D, Hlubocký J et al (2018) Structural changes arising from different thawing protocols on cryopreserved human allograft's aortic valve leaflets. Adv Clin Exp Med 27(8):1133–1036. https://doi.org/10.17219/acem/73713
O'Brien MF, Stafford EG, Gardner MA et al (1987) A comparison of aortic valve replacement with viable cryopreserved and fresh allograft valves, with a note on chromosomal studies. J Thorac Cardiovasc Surg 94:812–823
Oveissi F, Naficy S, Lee A et al (2020) Materials and manufacturing perspectives in engineering heart valves: A review. Mater Today Bio 5:100038. https://doi.org/10.1016/j.mtbio.2019.100038
Papazafiropoulou A, Tentolouris N (2009) Matrix metalloproteinases and cardiovascular diseases. Hippokratia 13:76–82. https://doi.org/10.1016/s0828-282x(06)70983-7
Parker R (1997) An international survey of allograft banks. In: Yankah AC, Yacoub MH, Hetzer R (eds) Cardiac valve allografts. Springer, New York, New York, pp 5–9
Parker R, Hunt C (2000) European Association of Tissue Banks standards for cryopreserved cardiovascular tissue banking. Cell Tissue Banking 1:241–245. https://doi.org/10.1023/A:1026557718029
Pejcic S, Ali Hassan SM, Rival DE, Bisleri G (2019) Characterizing the mechanical properties of the aortic wall. Vessel Plus 2019:1–12. https://doi.org/10.20517/2574-1209.2019.18
Pham T, Sulejmani F, Shin E et al (2017) Quantification and comparison of the mechanical properties of four human cardiac valves. Acta Biomater 54:345–355. https://doi.org/10.1016/j.actbio.2017.03.026
Puntmann VO, Nagel E, Hughes AD et al (2012) Gender-specific differences in myocardial deformation and aortic stiffness at rest and dobutamine stress. Hypertension 59:712–718. https://doi.org/10.1161/HYPERTENSIONAHA.111.183335
Rauch U, Saxena A, Lorkowski S et al (2011) Laminin isoforms in atherosclerotic arteries from mice and man. Histol Histopathol 26:711–724. https://doi.org/10.14670/HH-26.711
Rego BV, Khalighi AH, Drach A et al (2018) A noninvasive method for the determination of in vivo mitral valve leaflet strains. Int J Numer Method Biomed Eng 34:e3142. https://doi.org/10.1002/cnm.3142
Rendal Vázquez ME, Díaz Román TM, Rodríguez Cabarcos M et al (2008) Apoptosis in fresh and cryopreserved cardiac valves of pig samples. Cell Tissue Bank 9(2):101–107. https://doi.org/10.1007/s10561-008-9063-6
Rich L, Whittaker P (2005) Collagen and Picrosirius Red staining: a polarized light assessment of fibrillar hue and spatial distribution. Braz J Morphol Sci 2005:97–104
Ross DN (1962) Homograft replacement of the aortic valve. Lancet 2:487. https://doi.org/10.1016/s0140-6736(62)90345-8
Ross DN (1967) Replacement of aortic and mitral valves with a pulmonary autograft. Lancet 2:956–958. https://doi.org/10.1016/s0140-6736(67)90794-5
Ross DN, Yacoub MH (1969) Homografts replacement of the aortic valve: a critical review. Prog Cardiovasc Dis 11(4):275–293. https://doi.org/10.1016/0033-0620(69)90054-1
Ross D, Martelli V, Wain WH (1979) Allograft and autograft valves used for aortic valve replacement. In: Ionescu MI (ed) Tissue heart valves. Springer, London, pp 127–172
Sacks MS (2000) Biaxial mechanical evaluation of planar biological materials. J Elast. https://doi.org/10.1023/A:1010917028671
Samila ZJ, Carter SA (1981) The effect of age on the unfolding of elastin lamellae and collagen fibers with stretch in human carotid arteries. Can J Physiol Pharmacol 59:1050–1057. https://doi.org/10.1139/y81-160
Sands MP, Nelson RJ, Mohri H et al (1967) The procurement and preparation of aortic valve homografts. Surgery 62:839–842
Sanz-Garcia A, Oliver-de-la-Cruz J, Mirabet V et al (2015) Heart valve tissue engineering: how far is the bedside from the bench? Expert Rev Mol Med 17:e16. https://doi.org/10.1017/erm.2015.15
Sarikouch S, et al (2019a) Pediatric aortic valve replacement using decellularized allografts, Congenital, Original Article (EJCTS-2019-801834R1), in press
Sarikouch S, et al (2019b) Early results from a prospective, single-arm European trial on decellularized allografts for aortic valve replacement: the ARISE Study and ARISE registry data, Valves, Original Article (EJCTS-2019-801837R1), in press
Sauren AAHJ, van Hout MC, van Steenhoven AA et al (1983) The mechanical properties of porcine aortic valve tissues. J Biomech 16:327–337. https://doi.org/10.1016/0021-9290(83)90016-7
Schulze-Bauer CA, Regitnig P, Holzapfel GA (2002) Mechanics of the human femoral adventitia including the high-pressure response. Am J Physiol Heart Circ Physiol 282:H2427–H2440. https://doi.org/10.1152/ajpheart.00397.2001
Seebacher G, Grasl C, Stoiber M et al (2008) Biomechanical properties of decellularized porcine pulmonary valve conduits. Artif Organs 32:28–35. https://doi.org/10.1111/j.1525-1594.2007.00452.x
Seibert H, Scheffer T, Diebels S (2014) Biaxial testing of elastomers - Experimental setup, measurement and experimental optimisation of specimen’s shape. Tech Mech 34:72–89
Sherratt MJ (2009) Tissue elasticity and the ageing elastic fibre. Age (Dordr) 31:305–325. https://doi.org/10.1007/s11357-009-9103-6
Shinoka T, Breuer CK, Tanel RE et al (1995) Tissue engineering heart valves: valve leaflet replacement study in a lamb model. Ann Thorac Surg 60:513–516. https://doi.org/10.1016/0003-4975(95)00733-4
Silver FH, Snowhill PB, Foran DJ (2003) Mechanical behavior of vessel wall: a comparative study of aorta, vena cava, and carotid artery. Ann Biomed Eng 31:793–803. https://doi.org/10.1114/1.1581287
Slørdahl SA, Piene H, Linker DT, Vik A (1991) Segmental aortic wall stiffness from intravascular ultrasound at normal and subnormal aortic pressure in pigs. Acta Physiol Scand 143:227–232. https://doi.org/10.1111/j.1748-1716.1991.tb09226.x
Sokolis DP, Savva GD, Papadodima SA, Kourkoulis SK (2017) Regional distribution of circumferential residual strains in the human aorta according to age and gender. J Mech Behav Biomed Mater 67:87–100. https://doi.org/10.1016/j.jmbbm.2016.12.003
Špatenka J, Burkert J (2018) Allograft heart valve in aortic valve surgery. In: Vojáček J, Záček P, Dominik J (eds) Aortic regurgitation. Springer, Cham, pp 155–168
Stefanadis C, Stratos C, Vlachopoulos C et al (1995) Pressure-diameter relation of the human aorta. A new method of determination by the application of a special ultrasonic dimension catheter. Circulation 92:2210–2219. https://doi.org/10.1161/01.CIR.92.8.2210
Stella JA, Liao J, Sacks MS (2007) Time-dependent biaxial mechanical behavior of the aortic heart valve leaflet. J Biomech 40:3169–3177. https://doi.org/10.1016/j.jbiomech.2007.04.001
Stemper BD, Yoganandan N, Pintar FA (2007) Mechanics of arterial subfailure with increasing loading rate. J Biomech 40:1806–1812. https://doi.org/10.1016/j.jbiomech.2006.07.005
Stone JR, Bruneval P, Angelini A et al (2015) Consensus statement on surgical pathology of the aorta from the Society for cardiovascular pathology and the association for European cardiovascular pathology: I. Inflammatory Diseases Cardiovasc Pathol 24(5):267–278. https://doi.org/10.1016/j.carpath.2015.05.001
Stradins P, Lacis R, Ozolanta I et al (2004) Comparison of biomechanical and structural properties between human aortic and pulmonary valve. Eur J Cardiothorac Surg 26:634–639. https://doi.org/10.1016/j.ejcts.2004.05.043
Theocharis AD, Tsolakis I, Tzanakakis GN, Karamanos NK (2006) Chondroitin sulfate as a key molecule in the development of atherosclerosis and cancer progression. Adv Pharmacol 53:281–295. https://doi.org/10.1016/S1054-3589(05)53013-8
Theodoridis K, Tudorache I, Calistru A et al (2015) Successful matrix guided tissue regeneration of decellularized pulmonary heart valve allografts in elderly sheep. Biomaterials 52:221–228. https://doi.org/10.1016/j.biomaterials.2015.02.023
Tian L, Chesler NC (2012) In vivo and in vitro measurements of pulmonary arterial stiffness: A brief review. Pulm Circ 2:505–517. https://doi.org/10.4103/2045-8932.105040
Tonar Z (2018) Smooth muscle phenotype in aortic diseases: Are there other histopathological markers besides contractile myofibrils? Anatol J Cardiol 19(1):17–18. https://doi.org/10.14744/AnatolJCardiol.2017.25927
Tremblay D, Cartier R, Mongrain R, Leask RL (2010) Regional dependency of the vascular smooth muscle cell contribution to the mechanical properties of the pig ascending aortic tissue. J Biomech 43:2448–2451. https://doi.org/10.1016/j.jbiomech.2010.04.018
Tsamis A, Krawiec JT, Vorp DA (2013) Elastin and collagen fibre microstructure of the human aorta in ageing and disease: A review. J R Soc Interface 10:20121004. https://doi.org/10.1098/rsif.2012.1004
Vafaee T, Thomas D, Desai A et al (2018) Decellularization of human donor aortic and pulmonary valved conduits using low concentration sodium dodecyl sulfate. J Tissue Eng Regen Med 12(2):e841–e853. https://doi.org/10.1002/term.2391
van Geemen D, Soares ALF, Oomen PJA et al (2016) Age-dependent changes in geometry, tissue composition and mechanical properties of fetal to adult cryopreserved human heart valves. PLoS ONE 11:e0149020. https://doi.org/10.1371/journal.pone.0149020
Vesely I (1998) The role of elastin in aortic valve mechanics. J Biomech 31:115–123. https://doi.org/10.1016/S0021-9290(97)00122-X
Vesely I, Boughner D (1989) Analysis of the bending behaviour of porcine xenograft leaflets and of natural aortic valve material: Bending stiffness, neutral axis and shear measurements. J Biomech 22:655–671. https://doi.org/10.1016/0021-9290(89)90016-X
Vesely I, Gonzalez-Lavin D, Graf D, Boughner DR (1990) Mechanical testing of cryopreserved aortic allografts: comparison with xenografts and fresh tissue. J Thorac Cardiovasc Surg 99:119–123
Viidik A (1979) Biomechanical behavior of soft connective tissues. In: Akkas N (ed) Progress in Biomechanics. Sijthoff & Nordhoff, Alphen aan den Rijn, pp 75–113
Vincent JFV (1982) Structural Biomaterials, 3rd edn. Macmillan Education UK, Princeton
Vorp DA, Schiro BJ, Ehrlich MP et al (2003) Effect of aneurysm on the tensile strength and biomechanical behavior of the ascending thoracic aorta. Ann Thorac Surg 75:1210–1214. https://doi.org/10.1016/S0003-4975(02)04711-2
Waite L (2005) Biofluid mechanics in cardiovascular systems, 1st edn. McGraw-Hill Professional, New York
Waldman SD, Lee MJ (2002) Boundary conditions during biaxial testing of planar connective tissues. Part 1: Dynamic behavior. J Mater Sci Mater Med 13:933–938. https://doi.org/10.1023/A:1019896210320
Waldman SD, Lee JM (2005) Effect of sample geometry on the apparent biaxial mechanical behaviour of planar connective tissues. Biomaterials 26:7504–7513. https://doi.org/10.1016/j.biomaterials.2005.05.056
Welch W (1969) A comparative study of different methods of processing aortic homografts. Thorax 24:746–749. https://doi.org/10.1136/thx.24.6.746
Woloszyn D, Johnson D, Yacoub MH (1997) Homograft viability, assessment and significance. In: Yankah AC, Yacoub MH, Hetzer R (eds) Cardiac valve allografts. Springer, New York, pp 11–21
Xu J, Shi G-P (2014) Vascular wall extracellular matrix proteins and vascular diseases. Biochim Biophys Acta Mol Basis Dis 1842:2106–2119. https://doi.org/10.1016/j.bbadis.2014.07.008
Zahra S, Galea G, Jashari R et al (2019a) Significant variation in heart valve banking practice. Eur J Clin Microbiol Infect Dis 38(8):1491–1498. https://doi.org/10.1007/s10096-019-03577-0
Zahra S, Galea G, Jashari R et al (2019b) Validation of microbiological testing in cardiovascular tissue establishments: results of a second international quality-round trial. Eur J Clin Microbiol Infect Dis 38:1481–1490. https://doi.org/10.1007/s10096-019-03576-1
Zieman SJ, Melenovsky V, Kass DA (2005) Mechanisms, pathophysiology, and therapy of arterial stiffness. Arterioscler Thromb Vasc Biol 25:932–943. https://doi.org/10.1161/01.ATV.0000160548.78317.29
Funding
This study was funded by the Project LO1506 of the Czech Ministry of Education, Youth and Sports under the program NPU I, from European Regional Development Fund-Project “Application of Modern Technologies in Medicine and Industry” (No. CZ.02.1.01/0.0/0.0/17_048/0007280), by the National Sustainability Program I (NPU I) Nr. LO1503, and by the Charles University Research Fund—Progres Q39.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Burkert, J., Kochová, P., Tonar, Z. et al. The time has come to extend the expiration limit of cryopreserved allograft heart valves. Cell Tissue Bank 22, 161–184 (2021). https://doi.org/10.1007/s10561-020-09843-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10561-020-09843-2