Abstract
Background: The development of atrioventricular bioprosthesis has witnessed an increasing drive toward clinical translation over the last few decades. A significant challenge in the clinical translation of an atrioventricular bioprosthesis from bench to bedside is the appropriate choice of a large animal model to test the safety and effectiveness of the device.
Methods: We conducted a systematic review of pre-clinical in vivo studies that would enable us to synthesize a recommended framework. PRISMA (Preferred Reporting Items for Systematic Reviews and MetaAnalyses) guidelines were followed to identify and extract relevant articles.
Results: Sheep was the most common choice of animal, with nine out of the 12 included studies being conducted on sheep. There were acute and chronic studies based on our search criteria. An average of ~20 and 5 animals were used for chronic and acute studies. One out of three acute studies and eight out of nine chronic studies were on stented heart valve bioprosthesis. All analyses were conducted on the implantation of atrioventricular valves with trileaflet, except for one chronic study on unileaflet valves and one chronic and acute study on bileaflet valves.
Conclusion: Understanding the variance in past pre-clinical study designs may increase the appropriate utilization of large animal models. This synthesized evidence provides a pre-clinical in vivo studies framework for future research on an atrioventricular bioprosthesis.
Keywords: Bioprosthesis, atrioventricular valve, mitral bioprosthesis, tricuspid, hydrodynamic, large animal, in vivo, pre-clinical.
Graphical Abstract
[1]
Zhang BL, Bianco RW, Schoen FJ. Preclinical assessment of cardiac valve substitutes: Current status and considerations for engineered tissue heart valves. Front Cardiovasc Med 2019; 6: 72.
[http://dx.doi.org/10.3389/fcvm.2019.00072] [PMID: 31231661]
[http://dx.doi.org/10.3389/fcvm.2019.00072] [PMID: 31231661]
[2]
Tsang HG, Rashdan NA, Whitelaw CBA, Corcoran BM, Summers KM, MacRae VE. Large animal models of cardiovascular disease. Cell Biochem Funct 2016; 34(3): 113-32.
[http://dx.doi.org/10.1002/cbf.3173] [PMID: 26914991]
[http://dx.doi.org/10.1002/cbf.3173] [PMID: 26914991]
[3]
Keene BW, Atkins CE, Bonagura JD, et al. ACVIM consensus guidelines for the diagnosis and treatment of myxomatous mitral valve disease in dogs. J Vet Intern Med 2019; 33(3): 1127-40.
[http://dx.doi.org/10.1111/jvim.15488] [PMID: 30974015]
[http://dx.doi.org/10.1111/jvim.15488] [PMID: 30974015]
[4]
Faustich JTS, Carney JP, Lahti MT, Zhang BL, Bianco RW. Establishing background pathologic changes of valve replacement surgery in sheep. Cardiovasc Eng Technol 2022; 13(1): 181-90.
[http://dx.doi.org/10.1007/s13239-021-00563-6] [PMID: 34263418]
[http://dx.doi.org/10.1007/s13239-021-00563-6] [PMID: 34263418]
[5]
Kheradvar A, Zareian R, Kawauchi S, Goodwin RL, Rugonyi S. Animal models for heart valve research and development. Drug Discov Today Dis Models 2017; 24: 55-62.
[http://dx.doi.org/10.1016/j.ddmod.2018.04.001] [PMID: 30631375]
[http://dx.doi.org/10.1016/j.ddmod.2018.04.001] [PMID: 30631375]
[6]
Alaa M, Tsopanomichalou Gklotsou M, Vu TD, Ti LK, Lee CN, Kofidis T. Comprehensive and integrative experimentation setup for large animal hybrid valvular heart surgery. J Surg Res 2019; 234: 249-61.
[http://dx.doi.org/10.1016/j.jss.2018.09.019] [PMID: 30527481]
[http://dx.doi.org/10.1016/j.jss.2018.09.019] [PMID: 30527481]
[7]
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Ann Intern Med 2009; 151(4): 264-9.
[8]
Collatusso C, Roderjan JG, de Noronha L, et al. Decellularization as a method to reduce calcification in bovine pericardium bioprosthetic valves. Interact Cardiovasc Thorac Surg 2019; 29(2): 302-11.
[http://dx.doi.org/10.1093/icvts/ivz041] [PMID: 30848795]
[http://dx.doi.org/10.1093/icvts/ivz041] [PMID: 30848795]
[9]
Daebritz S, Fausten B, Hermanns B, et al. Introduction of a flexible polymeric heart valve prosthesis with special design for aortic position1. Eur J Cardiothorac Surg 2004; 25(6): 946-52.
[http://dx.doi.org/10.1016/j.ejcts.2004.02.040] [PMID: 15144993]
[http://dx.doi.org/10.1016/j.ejcts.2004.02.040] [PMID: 15144993]
[10]
Flameng W, Hermans H, Verbeken E, Meuris B. A randomized assessment of an advanced tissue preservation technology in the juvenile sheep model. J Thorac Cardiovasc Surg 2015; 149(1): 340-5.
[http://dx.doi.org/10.1016/j.jtcvs.2014.09.062] [PMID: 25439467]
[http://dx.doi.org/10.1016/j.jtcvs.2014.09.062] [PMID: 25439467]
[11]
Fukamachi K, Ootaki Y, Ootaki C, et al. Innovative, replaceable heart valve: Concept, in vitro study, and acute in vivo study. Artif Organs 2008; 32(3): 226-9.
[http://dx.doi.org/10.1111/j.1525-1594.2007.00527.x] [PMID: 18201287]
[http://dx.doi.org/10.1111/j.1525-1594.2007.00527.x] [PMID: 18201287]
[12]
Hassoulas J, Ayzenberg O. Experimental evaluation of the mitroflow pericardial heart valve prosthesis. Part I. in vivo hemodynamic evaluation. Angiology 1988; 39(8): 725-32.
[http://dx.doi.org/10.1177/000331978803900804] [PMID: 3421506]
[http://dx.doi.org/10.1177/000331978803900804] [PMID: 3421506]
[13]
Hassoulas J, Rose AG. Experimental evaluation of the mitroflow pericardial heart valve prosthesis. Part II. pathologic examination. Angiology 1988; 39(8): 733-41.
[http://dx.doi.org/10.1177/000331978803900805] [PMID: 3421507]
[http://dx.doi.org/10.1177/000331978803900805] [PMID: 3421507]
[14]
Keeling WB, Maxey TS, Sayad D, Martini N, Blazick E, Sommers KE. A novel stentless mitral valve. Surg Innov 2007; 14(1): 9-11.
[http://dx.doi.org/10.1177/1553350606298719] [PMID: 17442873]
[http://dx.doi.org/10.1177/1553350606298719] [PMID: 17442873]
[15]
Navia JL, Doi K, Atik FA, et al. Acute in vivo evaluation of a new stentless mitral valve. J Thorac Cardiovasc Surg 2007; 133(4): 986-994.e2.
[http://dx.doi.org/10.1016/j.jtcvs.2006.11.044] [PMID: 17382639]
[http://dx.doi.org/10.1016/j.jtcvs.2006.11.044] [PMID: 17382639]
[16]
Parravicini R, Cocconcelli F, Verona A, Parravicini V, Giuliani E, Barbieri A. Tuna cornea as biomaterial for cardiac applications. Tex Heart Inst J 2012; 39(2): 179-83.
[PMID: 22740728]
[PMID: 22740728]
[17]
Shemin RJ, Schoen FJ, Hein R, Austin J, Cohn LH. Hemodynamic and pathologic evaluation of a unileaflet pericardial bioprosthetic valve. J Thorac Cardiovasc Surg 1988; 95(5): 912-9.
[http://dx.doi.org/10.1016/S0022-5223(19)35706-X] [PMID: 3361939]
[http://dx.doi.org/10.1016/S0022-5223(19)35706-X] [PMID: 3361939]
[18]
Spyt TJ, Fisher J, Reid J, Anderson JD, Wheatley DJ. Animal evaluation of a new pericardial bioprosthetic heart valve. Artif Organs 1988; 12(4): 328-36.
[http://dx.doi.org/10.1111/j.1525-1594.1988.tb02782.x] [PMID: 3178521]
[http://dx.doi.org/10.1111/j.1525-1594.1988.tb02782.x] [PMID: 3178521]
[19]
Thiene G, Laborde F, Valente M, et al. Morphological survey of a new pericardial valve prosthesis (Pericarbon): Long-term animal experimental model. Eur J Cardiothorac Surg 1989; 3(1): 65-74.
[http://dx.doi.org/10.1016/1010-7940(89)90014-6] [PMID: 2534050]
[http://dx.doi.org/10.1016/1010-7940(89)90014-6] [PMID: 2534050]
[20]
Wheatley D, Raco L, Bernacca GM, Sim I, Belcher PR, Boyd JS. Polyurethane: Material for the next generation of heart valve prostheses? Eur J Cardiothorac Surg 2000; 17(4): 440-8.
[http://dx.doi.org/10.1016/S1010-7940(00)00381-X] [PMID: 10773568]
[http://dx.doi.org/10.1016/S1010-7940(00)00381-X] [PMID: 10773568]
[21]
Cochrane Handbook for Systematic Reviews of Interventions version 6.0. 2019. Available from: https://training.cochrane.org/handbook/current/chapter-14 (Accessed May 31, 2022).
[22]
Harding J, Roberts RM, Mirochnitchenko O. Large animal models for stem cell therapy. Stem Cell Res Ther 2013; 4(2): 23.
[http://dx.doi.org/10.1186/scrt171] [PMID: 23672797]
[http://dx.doi.org/10.1186/scrt171] [PMID: 23672797]
[23]
Chong JJH, Murry CE. Cardiac regeneration using pluripotent stem cells—Progression to large animal models. Stem Cell Res 2014; 13(3) (3 Pt B): 654-65.
[http://dx.doi.org/10.1016/j.scr.2014.06.005] [PMID: 25087896]
[http://dx.doi.org/10.1016/j.scr.2014.06.005] [PMID: 25087896]
[24]
US FDA guidance document (FDA-2015-D-3419) on general considerations for animal studies for medical devices. Available from: https://www.fda.gov/regulatory-information/search-fda-guidance-documents/general-considerations-animal-studies-medical-devices (Accessed May 31, 2022).
[25]
Recchia FA, Lionetti V. Animal models of dilated cardiomyopathy for translational research. Vet Res Commun 2007; 31(S1) (Suppl. 1): 35-41.
[http://dx.doi.org/10.1007/s11259-007-0005-8] [PMID: 17682844]
[http://dx.doi.org/10.1007/s11259-007-0005-8] [PMID: 17682844]
[26]
Milani-Nejad N, Janssen PML. Small and large animal models in cardiac contraction research: Advantages and disadvantages. Pharmacol Ther 2014; 141(3): 235-49.
[http://dx.doi.org/10.1016/j.pharmthera.2013.10.007] [PMID: 24140081]
[http://dx.doi.org/10.1016/j.pharmthera.2013.10.007] [PMID: 24140081]
[27]
Al Abri R, Kolethekkat AA, Kelleher M, Myles LM, Glasby MA. Effect of locally administered ciliary neurotrophic factor on the survival of transected and repaired adult sheep facial nerve. Oman Med J 2014; 29(3): 208-13.
[http://dx.doi.org/10.5001/omj.2014.51] [PMID: 24936272]
[http://dx.doi.org/10.5001/omj.2014.51] [PMID: 24936272]
[28]
Diogo CC, Camassa JA, Pereira JE, et al. The use of sheep as a model for studying peripheral nerve regeneration following nerve injury: Review of the literature. Neurol Res 2017; 39(10): 926-39.
[http://dx.doi.org/10.1080/01616412.2017.1331873] [PMID: 28604272]
[http://dx.doi.org/10.1080/01616412.2017.1331873] [PMID: 28604272]
[29]
Rogers CS. Genetically engineered livestock for biomedical models. Transgenic Res 2016; 25(3): 345-59.
[http://dx.doi.org/10.1007/s11248-016-9928-6] [PMID: 26820410]
[http://dx.doi.org/10.1007/s11248-016-9928-6] [PMID: 26820410]
[30]
Rabbani S, Soleimani M, Sahebjam M, et al. Effects of endothelial and mesenchymal stem cells on improving myocardial function in a sheep animal model. J Tehran Heart Cent 2017; 12(2): 65-71.
[PMID: 28828021]
[PMID: 28828021]
[31]
Kluin J, Talacua H, Smits AIPM, et al. In situ heart valve tissue engineering using a bioresorbable elastomeric implant – From material design to 12 months follow-up in sheep. Biomaterials 2017; 125: 101-17.
[http://dx.doi.org/10.1016/j.biomaterials.2017.02.007] [PMID: 28253994]
[http://dx.doi.org/10.1016/j.biomaterials.2017.02.007] [PMID: 28253994]
[32]
Polejaeva IA, Rutigliano HM, Wells KD. Livestock in biomedical research: History, current status and future prospective. Reprod Fertil Dev 2016; 28(2): 112-24.
[http://dx.doi.org/10.1071/RD15343] [PMID: 27062879]
[http://dx.doi.org/10.1071/RD15343] [PMID: 27062879]
[33]
Mariscal A, Caldarone L, Tikkanen J, et al. Pig lung transplant survival model. Nat Protoc 2018; 13(8): 1814-28.
[http://dx.doi.org/10.1038/s41596-018-0019-4] [PMID: 30072720]
[http://dx.doi.org/10.1038/s41596-018-0019-4] [PMID: 30072720]
[34]
Denner J. Can antiretroviral drugs be used to treat Porcine Endogenous Retrovirus (PERV) infection after xenotransplantation? Viruses 2017; 9(8): 213.
[http://dx.doi.org/10.3390/v9080213] [PMID: 28786944]
[http://dx.doi.org/10.3390/v9080213] [PMID: 28786944]
[35]
Jackson SJ, Andrews N, Ball D, et al. Does age matter? The impact of rodent age on study outcomes. Lab Anim 2017; 51(2): 160-9.
[http://dx.doi.org/10.1177/0023677216653984] [PMID: 27307423]
[http://dx.doi.org/10.1177/0023677216653984] [PMID: 27307423]
[36]
Mienaltowski MJ, Dunkman AA, Buckley MR, et al. Injury response of geriatric mouse patellar tendons. J Orthop Res 2016; 34(7): 1256-63.
[http://dx.doi.org/10.1002/jor.23144] [PMID: 26704368]
[http://dx.doi.org/10.1002/jor.23144] [PMID: 26704368]
[37]
van Weeren PR, Back W. Musculoskeletal disease in aged horses and its management. Vet Clin North Am Equine Pract 2016; 32(2): 229-47.
[http://dx.doi.org/10.1016/j.cveq.2016.04.003] [PMID: 27449390]
[http://dx.doi.org/10.1016/j.cveq.2016.04.003] [PMID: 27449390]
Article Metrics
5