Extracellular Matrix-Based Biomaterials and Their Influence Upon Cell Behavior

  • Madeline C. Cramer
  • Stephen F. BadylakEmail author
S.I. : Biomaterials - Engineering Cell Behavior


Biologic scaffold materials composed of allogeneic or xenogeneic extracellular matrix (ECM) are commonly used for the repair and remodeling of injured tissue. The clinical outcomes associated with implantation of ECM-based materials range from unacceptable to excellent. The variable clinical results are largely due to differences in the preparation of the material, including characteristics of the source tissue, the method and efficacy of decellularization, and post-decellularization processing steps. The mechanisms by which ECM scaffolds promote constructive tissue remodeling include mechanical support, degradation and release of bioactive molecules, recruitment and differentiation of endogenous stem/progenitor cells, and modulation of the immune response toward an anti-inflammatory phenotype. The methods of ECM preparation and the impact of these methods on the quality of the final product are described herein. Examples of favorable cellular responses of immune and stem cells associated with constructive tissue remodeling of ECM bioscaffolds are described.


Biologic scaffold Host response Constructive remodeling Decellularization 



Extracellular matrix


Small intestinal submucosa


Urinary bladder matrix




Sodium dodecyl sulfate


Sodium deoxycholate


Time of flight secondary ion mass spectroscopy


Hexamethylene diisocyanate


Matrix bound nanovesicles


United States Food and Drug Administration


International Organization for Standardization


Human cell and tissue product


Ethylene oxide


Tissue organization field theory


Damage associated molecular patterns


Perivascular stem cells


Conflict of interest

SF Badylak is the Chief Scientific Officer of ECM Therapeutics, Inc. MC Cramer has nothing to disclose.


MC Cramer was supported by the National Heart, Lung and Blood Institute of the National Institutes of Health (5T32HL076124-12).


  1. 1.
    Agmon, G., and K. L. Christman. Controlling stem cell behavior with decellularized extracellular matrix scaffolds. Curr. Opin. Solid State Mater. Sci. 20:193–201, 2016.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Agrawal, V., S. A. Johnson, J. Reing, L. Zhang, S. Tottey, G. Wang, K. K. Hirschi, S. Braunhut, L. J. Gudas, and S. F. Badylak. Epimorphic regeneration approach to tissue replacement in adult mammals. Proc. Natl. Acad. Sci. USA 107:3351–3355, 2010.PubMedGoogle Scholar
  3. 3.
    Agrawal, V., S. Tottey, S. A. Johnson, J. M. Freund, B. F. Siu, and S. F. Badylak. Recruitment of progenitor cells by an extracellular matrix cryptic peptide in a mouse model of digit amputation. Tissue Eng: Part A 17:2435–2443, 2011.Google Scholar
  4. 4.
    Aguiari, P., L. Iop, F. Favaretto, C. M. L. Fidalgo, F. Naso, G. Milan, V. Vindigni, M. Spina, F. Bassetto, A. Bagno, R. Vettor, and G. Gerosa. In vitro comparative assessment of decellularized bovine pericardial patches and commercial bioprosthetic heart valves. Biomed. Mater. 12:015021, 2017.PubMedGoogle Scholar
  5. 5.
    Allman, A. J., T. B. McPherson, S. F. Badylak, L. C. Merrill, B. Kallakury, C. Sheehan, R. H. Raeder, and D. W. Metzger. Xenogeneic extracellular matrix grafts elicit a Th2-restricted immune response. Transplantation 71:1631–1640, 2001.PubMedGoogle Scholar
  6. 6.
    Allman, A. J., T. B. McPherson, L. C. Merrill, S. F. Badylak, and D. W. Metzger. The Th2-restricted immune response to xenogeneic small intestinal submucosa does not influence systemic protective immunity to viral and bacterial pathogens. Tissue Eng. 8:53–62, 2002.PubMedGoogle Scholar
  7. 7.
    Armour, A. D., J. S. Fish, K. A. Woodhouse, and J. L. Semple. A comparison of human and porcine acellularized dermis: Interactions with human fibroblasts in vitro. Plast. Reconstr. Surg. 117:845–856, 2006.PubMedGoogle Scholar
  8. 8.
    Badylak, S. F. The extracellular matrix as a biologic scaffold material. Biomaterials 28:3587–3593, 2007.PubMedGoogle Scholar
  9. 9.
    Badylak, S. F., D. O. Freytes, and T. W. Gilbert. Extracellular matrix as a biological scaffold material: Structure and function. Acta Biomater. 5:1–13, 2009.PubMedGoogle Scholar
  10. 10.
    Badylak, S. F., and T. W. Gilbert. Immune response to biologic scaffold materials. Semin. Immunol. 20:109–116, 2008.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Badylak, S. F., T. Hoppo, A. Nieponice, T. W. Gilbert, J. M. Davison, and B. A. Jobe. Esophageal preservation in five male patients after endoscopic inner-layer circumferential resection in the setting of superficial cancer: A regenerative medicine approach with a biologic scaffold. Tissue Eng. Part A 17:1643–1650, 2011.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Badylak, S. F., P. V. Kochupura, I. S. Cohen, S. V. Doronin, A. E. Saltman, T. W. Gilbert, D. J. Kelly, R. A. Ignotz, and G. R. Gaudette. The use of extracellular matrix as an inductive scaffold for the partial replacement of functional myocardium. Cell Transplant. 15(Supp 1):S29–S40, 2006.PubMedGoogle Scholar
  13. 13.
    Badylak, S. F., B. Kropp, T. McPherson, H. Liang, and P. W. Snyder. Small intestional submucosa: A rapidly resorbed bioscaffold for augmentation cystoplasty in a dog model. Tissue Eng. 4:379–387, 1998.PubMedGoogle Scholar
  14. 14.
    Badylak, S. F., K. Park, N. Peppas, G. McCabe, and M. Yoder. Marrow-derived cells populate scaffolds composed of xenogeneic extracellular matrix. Exp. Hematol. 29:1310–1318, 2001.PubMedGoogle Scholar
  15. 15.
    Badylak, S. F., R. Tullius, K. Kokini, K. D. Shelbourne, T. Klootwyk, S. L. Voytik, M. R. Kraine, and C. Simmons. The use of xenogeneic small intestinal submucosa as a biomaterial for Achille’s tendon repair in a dog model. J. Biomed. Mater. Res. 29:977–985, 1995.PubMedGoogle Scholar
  16. 16.
    Badylak, S. F., J. E. Valentin, A. K. Ravindra, G. P. McCabe, and A. M. Stewart-Akers. Macrophage phenotype as a determinant of biologic scaffold remodeling. Tissue Eng. Part A 14:1835–1842, 2008.PubMedGoogle Scholar
  17. 17.
    Baiguera, S., C. Del Gaudio, E. Lucatelli, E. Kuevda, M. Boieri, B. Mazzanti, A. Bianco, and P. Macchiarini. Electrospun gelatin scaffolds incorporating rat decellularized brain extracellular matrix for neural tissue engineering. Biomaterials 35:1205–1214, 2014.PubMedGoogle Scholar
  18. 18.
    Bailey, A. J., and W. J. Tromans. Effects of ionizing radiation on the ultrastructure of collagen fibrils. Radiat. Res. 23:145–155, 1964.PubMedGoogle Scholar
  19. 19.
    Balestrini, J. L., A. Liu, A. L. Gard, J. Huie, K. M. S. Blatt, J. Schwan, L. Zhao, T. J. Broekelmann, R. P. Mecham, E. C. Wilcox, and L. E. Niklason. Sterilization of lung matrices by supercritical carbon dioxide. Tissue Eng. Part C Methods 22:260–269, 2016.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Bao, J., Q. Wu, Y. Wang, Y. Li, L. Li, F. Chen, X. Wu, M. Xie, and H. Bu. Enhanced hepatic differentiation of rat bone marrow-derived mesenchymal stem cells in spheroidal aggregate culture on a decellularized liver scaffold. Int. J. Mol. Med. 38:457–465, 2016.PubMedPubMedCentralGoogle Scholar
  21. 21.
    Barakat, O., S. Abbasi, G. Rodriguez, J. Rios, R. P. Wood, C. Ozaki, L. S. Holley, and P. K. Gauthier. Use of decellularized porcine liver for engineering humanized liver organ. J. Surg. Res. 173:e11–e25, 2012.PubMedGoogle Scholar
  22. 22.
    Beattie, A. J., T. W. Gilbert, J. P. Guyot, A. J. Yates, and S. F. Badylak. Chemoattraction of progenitor cells by remodeling extracellular matrix scaffolds. Tissue Eng. Part A 15:1119–1125, 2009.PubMedGoogle Scholar
  23. 23.
    Berger, A. Th1 and Th2 responses: What are they ? BMJ 321:424, 2000.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Bernhardt, A., M. Wehrl, B. Paul, T. Hochmuth, M. Schumacher, K. Schütz, and M. Gelinsky. Improved sterilization of sensitive biomaterials with supercritical carbon dioxide at low temperature. PLoS ONE 10:1–19, 2015.Google Scholar
  25. 25.
    Bhrany, A. D., C. J. Lien, B. L. Beckstead, N. D. Futran, N. H. Muni, C. M. Giachelli, and B. D. Ratner. Crosslinking of an oesophagus acellular matrix tissue scaffold. J. Tissue Eng. Regen. Med. 2:365–372, 2008.PubMedGoogle Scholar
  26. 26.
    Bissell, M. J., and T. G. Ram. Regulation of functional cytodifferentiation and histogenesis in mammary epithelial cells: Role of the extracellular matrix. Environ. Health Perspect. 80:61–70, 1989.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Bonandrini, B., M. Figliuzzi, E. Papadimou, M. Morigi, N. Perico, F. Casiraghi, C. Dipl, F. Sangalli, S. Conti, A. Benigni, A. Remuzzi, and G. Remuzzi. Recellularization of well-preserved acellular kidney scaffold using embryonic stem cells. Tissue Eng. Part A 20:1486–1498, 2014.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Boruch, A. V., A. Nieponice, I. R. Qureshi, T. W. Gilbert, and S. F. Badylak. Constructive remodeling of biologic scaffolds is dependent on early exposure to physiologic bladder filling in a canine partial cystectomy model. J. Surg. Res. 161:217–225, 2010.PubMedGoogle Scholar
  29. 29.
    Brennan, E. P., X. Tang, A. M. Stewart-Akers, L. J. Gudas, and S. F. Badylak. Chemoattractant activity of degradation products of fetal and adult skin extracellular matrix for keratinocyte progenitor cells. J. Tissue Eng. Regen. Med. 2:491–498, 2008.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Brightman, A. O., B. P. Rajwa, J. E. Sturgis, M. E. Mccallister, J. P. Robinson, and S. L. Voytik-Harbin. Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro. Biopolymers 54:222–234, 2000.PubMedGoogle Scholar
  31. 31.
    Browe, D. C., O. R. Mahon, P. J. Díaz-Payno, N. Cassidy, I. Dudurych, A. Dunne, C. T. Buckley, and D. J. Kelly. Glyoxal cross-linking of solubilised extracellular matrix to produce highly porous, elastic and chondro-permissive scaffolds for orthopaedic tissue engineering. J. Biomed. Mater. Res. Part A 2019. Scholar
  32. 32.
    Brown, B. N., C. A. Barnes, R. T. Kasick, R. Michel, T. W. Gilbert, D. Beer-Stolz, D. G. Castner, B. D. Ratner, and S. F. Badylak. Surface characterization of extracellular matrix scaffolds. Biomaterials 31:428–437, 2010.PubMedGoogle Scholar
  33. 33.
    Brown, B. N., J. M. Freund, L. Han, J. P. Rubin, J. E. Reing, E. M. Jeffries, M. T. Wolf, S. Tottey, C. A. Barnes, B. D. Ratner, and S. F. Badylak. Comparison of three methods for the derivation of a biologic scaffold composed of adipose tissue extracellular matrix. Tissue Eng. Part C Methods 17:411–421, 2010.Google Scholar
  34. 34.
    Brown, B. N., R. Londono, S. Tottey, L. Zhang, K. A. Kukla, M. T. Wolf, K. A. Daly, J. E. Reing, and S. F. Badylak. Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater. 8:978–987, 2012.PubMedGoogle Scholar
  35. 35.
    Brown, B. N., J. E. Valentin, A. M. Stewart-Akers, G. P. McCabe, and S. F. Badylak. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30:1482–1491, 2009.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Burgkart, R., A. Tron, P. Prodinger, M. Culmes, J. Tuebel, M. Van Griensven, B. Saldamli, and A. Schmitt. Decellularized kidney matrix for perfused bone engineering. Tissue Eng. Part C Methods 20:553–561, 2014.PubMedGoogle Scholar
  37. 37.
    Butler, C. E., N. K. Burns, K. T. Campbell, A. B. Mathur, M. V. Jaffari, and C. N. Rios. Comparison of cross-linked and non-cross-linked porcine acellular dermal matrices for ventral hernia repair. J. Am. Coll. Surg. 211:368–376, 2010.PubMedGoogle Scholar
  38. 38.
    Campbell, K. T., N. K. Burns, C. N. Rios, A. B. Mathur, and C. E. Butler. Human versus non-cross-linked porcine acellular dermal matrix used for ventral hernia repair: Comparison of in vivo fibrovascular remodeling and mechanical repair strength. Plast. Reconstr. Surg. 127:2321–2332, 2011.PubMedGoogle Scholar
  39. 39.
    Carver, D. A., A. W. Kirkpatrick, T. L. Eberle, and C. G. Ball. Performance of biological mesh materials in abdominal wall reconstruction: Study protocol for a randomised controlled trial. BMJ Open 9:e024091, 2019.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Casali, D. M., R. M. Handleton, T. Shazly, and M. A. Matthews. A novel supercritical CO2-based decellularization method for maintaining scaffold hydration and mechanical properties. J. Supercrit. Fluids 131:72–81, 2018.Google Scholar
  41. 41.
    Cavallo, J. A., S. C. Greco, J. Liu, M. M. Frisella, C. R. Deeken, and B. D. Matthews. Remodeling characteristics and biomechanical properties of a crosslinked versus a non-crosslinked porcine dermis scaffolds in a porcine model of ventral hernia repair. Hernia 19:207–218, 2015.PubMedGoogle Scholar
  42. 42.
    Cebotari, S., I. Tudorache, T. Jaekel, A. Hilfiker, S. Dorfman, W. Ternes, A. Haverich, and A. Lichtenberg. Detergent decellularization of heart valves for tissue engineering: Toxicological effects of residual detergents on human endothelial cells. Artif. Organs 34:206–210, 2010.PubMedGoogle Scholar
  43. 43.
    Chen, L., Z. He, B. Chen, M. Yang, Y. Zhao, W. Sun, Z. Xiao, J. Zhang, and J. Dai. Loading of VEGF to the heparin cross-linked demineralized bone matrix improves vascularization of the scaffold. J. Mater. Sci. Mater. Med. 21:309–317, 2010.PubMedGoogle Scholar
  44. 44.
    Cheng, A. M. Y. W., M. A. Abbas, and T. Tejirian. Outcome of abdominal wall hernia repair with biologic mesh: Permacol versus Strattice. Am. Surg. 80:999–1002, 2014.PubMedGoogle Scholar
  45. 45.
    Cheng, N. C., B. T. Estes, H. A. Awad, and F. Guilak. Chondrogenic differentiation of adipose-derived adult stem cells by a porous scaffold derived from native articular cartilage extracellular matrix. Tissue Eng. Part A 15:231–241, 2009.PubMedGoogle Scholar
  46. 46.
    Cheng, N.-C., B. T. Estes, T.-H. Young, and F. Guilak. Genipin-crosslinked cartilage-derived matrix as a scaffold for human adipose-derived stem cell chondrogenesis. Tissue Eng. Part A 19:484–496, 2012.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Choi, J. S., H. J. Yang, B. S. Kim, J. D. Kim, J. Y. Kim, B. Yoo, K. Park, H. Y. Lee, and Y. W. Cho. Human extracellular matrix (ECM) powders for injectable cell delivery and adipose tissue engineering. J. Control. Release 139:2–7, 2009.PubMedGoogle Scholar
  48. 48.
    Christo, S. N., K. R. Diener, A. Bachhuka, K. Vasilev, and J. D. Hayball. Innate Immunity and Biomaterials at the Nexus : Friends or Foes. Biomed Res. Int. 2015:342304, 2015.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Consigliere, P., I. Polyzois, T. Sarkhel, R. Gupta, O. Levy, and A. A. Narvani. Preliminary results of a consecutive series of large & massive rotator cuff tears treated with arthroscopic rotator cuff repairs augmented with extracellular matrix. Arch. Bone Jt. Surg. 5:14–21, 2017.PubMedPubMedCentralGoogle Scholar
  50. 50.
    Constantinou, C. D., and S. A. Jimenez. Structure of cDNAs encoding the triple-helical domain of murine alpha 2 (VI) collagen chain and comparison to human and chick homologues. Use of polymerase chain reaction and partially degenerate oligonucleotide for generation of novel cDNA clones. Matrix 11:1–9, 1991.PubMedGoogle Scholar
  51. 51.
    Cook, J. L., D. B. Fox, K. Kuroki, M. Jayo, and P. G. De Deyne. In vitro and in vivo comparison of five biomaterials used for orthopedic soft tissue augmentation. Am. J. Vet. Res. 69:148–156, 2008.PubMedGoogle Scholar
  52. 52.
    Cortiella, J., J. Niles, A. Cantu, A. Brettler, A. Pham, G. Vargas, S. Winston, J. Wang, S. Walls, and J. E. Nichols. Influence of acellular natural lung matrix on murine embryonic stem cell differentiation and tissue formation. Tissue Eng. Part A 16:2565–2580, 2010.PubMedGoogle Scholar
  53. 53.
    Costa, A., J. D. Naranjo, R. Londono, and S. F. Badylak. Biologic scaffolds. Cold Spring Harb. Perspect. Biol. 7:a025676, 2017.Google Scholar
  54. 54.
    Courtman, D. W., B. F. Errett, and G. J. Wilson. The role of crosslinking in modification of the immune response elicited against xenogenic vascular acellular matrices. J. Biomed. Mater. Res. 55:576–586, 2001.PubMedGoogle Scholar
  55. 55.
    Crapo, P. M., T. W. Gilbert, and D. V. M. Badylak. An overview of tissue and whole organ decellularization processes. Biomaterials 32:3233–3243, 2011.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Crapo, P. M., C. J. Medberry, J. E. Reing, S. Tottey, Y. van der Merwe, K. E. Jones, and S. F. Badylak. Biologic scaffolds composed of central nervous system extracellular matrix. Biomaterials 33:3539–3547, 2012.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Daly, A. B., J. M. Wallis, Z. D. Borg, R. W. Bonvillain, B. Deng, B. A. Ballif, D. M. Jaworski, G. B. Allen, and D. J. Weiss. Initial binding and recellularization of decellularized mouse lung scaffolds with bone marrow-derived mesenchymal stromal cells. Tissue Eng. Part A 18:1–16, 2012.PubMedGoogle Scholar
  58. 58.
    Davis, G. E., K. J. Bayless, M. J. Davis, and G. A. Meininger. Regulation of tissue injury responses by the exposure of matricryptic sites within extracellular matrix molecules. Am. J. Pathol. 156:1489–1498, 2000.PubMedPubMedCentralGoogle Scholar
  59. 59.
    De Waele, J., K. Reekmans, J. Daans, H. Goossens, Z. Berneman, and P. Ponsaerts. 3D culture of murine neural stem cells on decellularized mouse brain sections. Biomaterials 41:122–131, 2015.PubMedGoogle Scholar
  60. 60.
    Dearth, C. L., T. J. Keane, C. A. Carruthers, J. E. Reing, L. Huleihel, C. A. Ranallo, E. W. Kollar, and S. F. Badylak. The effect of terminal sterilization on the material properties and in vivo remodeling of a porcine dermal biologic scaffold. Acta Biomater. 33:78–87, 2016.PubMedGoogle Scholar
  61. 61.
    Deeken, C. R., L. Melman, E. D. Jenkins, S. C. Greco, M. M. Frisella, and B. D. Matthews. Histologic and biomechanical evaluation of crosslinked and non-crosslinked biologic meshes in a porcine model of ventral incisional hernia repair. J. Am. Coll. Surg. 212:880–888, 2011.PubMedPubMedCentralGoogle Scholar
  62. 62.
    Dejardin, L. M., S. P. Arnoczky, B. J. Ewers, R. C. Haut, and R. B. Clarke. Tissue-engineered rotator cuff tendon using porcine small intestine submucosa: Histologic and mechanical evaluation in dogs. Am. J. Sports Med. 29:175–184, 2001.PubMedGoogle Scholar
  63. 63.
    del Barrio, J. L. A., M. Chiesa, N. Garagorri, N. Garcia-Urquia, J. Fernandez-Delgado, L. Bataille, A. Rodriguez, F. Arnalich-Montiel, T. Zarnowski, J. P. Á. de Toledo, J. L. Alio, and M. P. De Miguel. Acellular human corneal matrix sheets seeded with human adipose-derived mesenchymal stem cells integrate functionally in an experimental animal model. Exp. Eye Res. 132:91–100, 2015.Google Scholar
  64. 64.
    Dellarco, V. L., W. M. Generoso, G. A. Sega, J. R. Fowle, D. Jacobson-Kram, and H. E. Brockman. Review of the mutagenicity of ethylene oxide. Environ. Mol. Mutagen. 16:85–103, 1990.PubMedGoogle Scholar
  65. 65.
    Dellavalle, A., G. Maroli, Azzoni E. CovarelloD, A. Innocenzi, L. Perani, S. Antonini, R. Sambasivan, S. Brunelli, S. Tajbakhsh, and G. Cossu. Pericytes resident in postnatal skeletal muscle differentiate into muscle fibres and generate satellite cells. Nat. Commun. 2:411–499, 2011.Google Scholar
  66. 66.
    Dequach, J. A., V. Mezzano, A. Miglani, S. Lange, G. M. Keller, and K. L. Christman. Simple and high yielding method for preparing tissue specific extracellular matrix coatings for cell culture. PLoS ONE 5:1–11, 2010.Google Scholar
  67. 67.
    Dequach, J. A., S. H. Yuan, L. S. B. Goldstein, and K. L. Christman. Decellularized porcine brain matrix for cell culture and tissue engineering scaffolds. Tissue Eng. Part A 17:2583–2592, 2011.PubMedPubMedCentralGoogle Scholar
  68. 68.
    Duan, Y., Z. Liu, J. O’Neill, L. Q. Wan, D. O. Freytes, and G. Vunjak-Novakovic. Hybrid gel composed of native heart matrix and collagen induces cardiac differentiation of human embryonic stem cells without supplemental growth factors. J. Cardiovasc. Transl. Res. 4:605–615, 2011.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Dziki, J., S. Badylak, M. Yabroudi, B. Sicari, F. Ambrosio, K. Stearns, N. Turner, A. Wyse, M. L. Boninger, E. H. P. Brown, and J. P. Rubin. An acellular biologic scaffold treatment for volumetric muscle loss: Results of a 13-patient cohort study. NPJ Regen. Med. 1:16008, 2016.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Dziki, J. L., L. Huleihel, M. E. Scarritt, and S. F. Badylak. Extracellular matrix bioscaffolds as immunomodulatory biomaterials. Tissue Eng. Part A 23:1152–1159, 2017.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Dziki, J. L., B. M. Sicari, M. T. Wolf, M. C. Cramer, and S. F. Badylak. Immunomodulation and mobilization of progenitor cells by extracellular matrix bioscaffolds for volumetric muscle loss treatment. Tissue Eng. Part A 22:1129–1139, 2016.PubMedGoogle Scholar
  72. 72.
    Dziki, J. L., D. S. Wang, C. Pineda, B. M. Sicari, T. Rausch, and S. F. Badylak. Solubilized extracellular matrix bioscaffolds derived from diverse source tissues differentially influence macrophage phenotype. J. Biomed. Mater. Res. Part A 105:138–147, 2017.Google Scholar
  73. 73.
    Efraim, Y., B. Schoen, S. Zahran, T. Davidov, G. Vasilyev, L. Baruch, E. Zussman, and M. Machluf. 3D structure and processing methods direct the biological attributes of ECM-based cardiac scaffolds. Sci. Rep. 9:1–13, 2019.Google Scholar
  74. 74.
    Exposito, J. Y., M. D’Alessio, M. Solursh, and F. Ramirez. Sea urchin collagen evolutionarily homologous to vertebrate pro-α2(I) collagen. J. Biol. Chem. 267:15559–15562, 1992.PubMedGoogle Scholar
  75. 75.
    Faulk, D. M., C. A. Carruthers, H. J. Warner, C. R. Kramer, J. E. Reing, L. Zhang, A. D’Amore, and S. F. Badylak. The effect of detergents on the basement membrane complex of a biologic scaffold material. Acta Biomater. 10:183–193, 2014.PubMedGoogle Scholar
  76. 76.
    Faulk, D. M., J. D. Wildemann, and S. F. Badylak. Decellularization and cell seeding of whole liver biologic scaffolds composed of extracellular matrix. J. Clin. Exp. Hepatol. 5:69–80, 2015.PubMedGoogle Scholar
  77. 77.
    Faust, A., A. Kandakatla, Y. Van Der Merwe, T. Ren, L. Huleihel, G. Hussey, J. D. Naranjo, S. Johnson, S. Badylak, and M. Steketee. Urinary bladder extracellular matrix hydrogels and matrix-bound vesicles differentially regulate central nervous system neuron viability and axon growth and branching. J. Biomater. Appl. 31:1277–1295, 2017.PubMedGoogle Scholar
  78. 78.
    Fishman, J. M., M. W. Lowdell, L. Urbani, T. Ansari, A. J. Burns, M. Turmaine, J. North, P. Sibbons, A. M. Seifalian, K. J. Wood, M. A. Birchall, and P. De Coppi. Immunomodulatory effect of a decellularized skeletal muscle scaffold in a discordant xenotransplantation model. Proc. Natl. Acad. Sci. USA 110:14360–14365, 2013.PubMedGoogle Scholar
  79. 79.
    Franz, S., S. Rammelt, D. Scharnweber, and J. C. Simon. Immune responses to implants—A review of the implications for the design of immunomodulatory biomaterials. Biomaterials 32:6692–6709, 2011.PubMedGoogle Scholar
  80. 80.
    French, K., A. Boopathy, J. DeQuach, L. Chingozha, H. Lu, K. L. Christman, and M. E. Davis. A naturally derived cardiac extracellular matrix enhances cardiac progenitor cell behavior in vitro. Acta Biomater. 8:4357–4364, 2012.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Freytes, D. O., S. F. Badylak, T. J. Webster, L. A. Geddes, and A. E. Rundell. Biaxial strength of multilaminated extracellular matrix scaffolds. Biomaterials 25:2353–2361, 2004.PubMedGoogle Scholar
  82. 82.
    Freytes, D. O., J. Martin, S. S. Velankar, A. S. Lee, and S. F. Badylak. Preparation and rheological characterization of a gel form of the porcine urinary bladder matrix. Biomaterials 29:1630–1637, 2008.PubMedGoogle Scholar
  83. 83.
    Freytes, D. O., J. D. O’Neill, Y. Duan-Arnold, E. Wrona, and G. Vunjak-Novakovic. Native cardiac extracellular matrix hydrogels for cultivation of human stem cell-derived cardiomyocytes. Methods Mol Biol 1181:69–81, 2014.PubMedPubMedCentralGoogle Scholar
  84. 84.
    Freytes, D. O., A. E. Rundell, J. Vande Geest, D. A. Vorp, T. J. Webster, and S. F. Badylak. Analytically derived material properties of multilaminated extracellular matrix devices using the ball-burst test. Biomaterials 26:5518–5531, 2005.PubMedGoogle Scholar
  85. 85.
    Freytes, D. O., R. M. Stoner, and S. F. Badylak. Uniaxial and biaxial properties of terminally sterilized porcine urinary bladder matrix scaffolds. J. Biomed. Mater. Res. B. Appl. Biomater. 84B:408–414, 2008.Google Scholar
  86. 86.
    Freytes, D. O., R. S. Tullius, J. E. Valentin, A. M. Stewart-Akers, and S. F. Badylak. Hydrated versus lyophilized forms of porcine extracellular matrix derived from the urinary bladder. J. Biomed. Mater. Res. A 87:862–872, 2008.PubMedGoogle Scholar
  87. 87.
    Gaetani, R., C. Yin, N. Srikumar, R. Braden, P. A. Doevendans, J. P. G. Sluijter, and K. L. Christman. Cardiac-derived extracellular matrix enhances cardiogenic properties of human cardiac progenitor cells. Cell Transplant. 25:1653–1663, 2016.PubMedGoogle Scholar
  88. 88.
    Geiger, S. E., O. A. Deigni, J. T. Watson, and B. A. Kraemer. Management of open distal lower extremity wounds with exposed tendons using porcine urinary bladder matrix. Wounds: A Compend. Clin. Res. Pract. 28:306–316, 2016.Google Scholar
  89. 89.
    Gilbert, T. W., J. Freund, and S. F. Badylak. Quantification of DNA in biologic scaffold materials. J. Surg. Res. 152:135–139, 2009.PubMedGoogle Scholar
  90. 90.
    Gilbert, T. W., A. Nieponice, A. R. Spievack, J. Holcomb, S. Gilbert, and S. F. Badylak. Repair of the thoracic wall with an extracellular matrix scaffold in a canine model. J. Surg. Res. 147:61–67, 2008.PubMedGoogle Scholar
  91. 91.
    Gilbert, T. W., A. M. Stewart-Akers, A. Simmons-Byrd, and S. F. Badylak. Degradation and remodeling of small intestinal submucosa in canine Achilles tendon repair. J. Bone Jt. Surg. Am. 89:621–630, 2007.Google Scholar
  92. 92.
    Gilbert, T. W., D. B. Stolz, F. Biancaniello, A. Simmons-Byrd, and S. F. Badylak. Production and characterization of ECM powder: Implications for tissue engineering applications. Biomaterials 26:1431–1435, 2005.PubMedGoogle Scholar
  93. 93.
    Gilot, G. J., A. M. Alvarez-Pinzon, L. Barcksdale, D. Westerdahl, M. Krill, and E. Peck. Outcome of large to massive rotator cuff tears repaired with and without extracellular matrix augmentation: A prospective comparative study. Arthrosc. J. Arthrosc. Relat. Surg. 31:1459–1465, 2015.Google Scholar
  94. 94.
    Gilpin, S. E., X. Ren, T. Okamoto, J. P. Guyette, H. Mou, J. Rajagopal, D. J. Mathisen, J. P. Vacanti, and H. C. Ott. Enhanced lung epithelial specification of human induced pluripotent stem cells on decellularized lung matrix. Ann. Thorac. Surg. 98:1721–1729, 2014.PubMedPubMedCentralGoogle Scholar
  95. 95.
    Gilpin, A., and Y. Yang. Decellularization strategies for regenerative medicine: From processing techniques to applications. Biomed Res. Int. 2017. Scholar
  96. 96.
    Glasberg, S. B., and D. Light. AlloDerm and Strattice in breast reconstruction: A comparison and techniques for optimizing outcomes. Plast. Reconstr. Surg. 129:1223–1233, 2012.PubMedGoogle Scholar
  97. 97.
    Godin, L. M., B. J. Sandri, D. E. Wagner, C. M. Meyer, A. P. Price, I. Akinnola, D. J. Weiss, and A. P. M. Panoskaltsis-Mortari. Decreased laminin expression by human lung epithelial cells and fibroblasts cultured in acellular lung scaffolds from aged mice. PLoS ONE 11:1–17, 2016.Google Scholar
  98. 98.
    Gordon, S., and P. R. Taylor. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:953–964, 2005.PubMedGoogle Scholar
  99. 99.
    Gouk, S.-S., T.-M. Lim, S.-H. Teoh, and W. Q. Sun. Alterations of human acellular tissue matrix by gamma irradiation: Histology, biomechanical property, stability, in vitro cell repopulation, and remodeling. J Biomed. Mater. Res. Part B Appl. Biomater. 84B:205–217, 2008.Google Scholar
  100. 100.
    Guler, S., B. Aslan, P. Hosseinian, and H. M. Aydin. Supercritical carbon dioxide-assisted decellularization of aorta and cornea. Tissue Eng. Part C Methods 23:540–547, 2017.PubMedGoogle Scholar
  101. 101.
    Harth, K. C., A. M. Broome, M. R. Jacobs, J. A. Blatnik, F. Zeinali, S. Bajaksouzian, and M. J. Rosen. Bacterial clearance of biologic grafts used in hernia repair: An experimental study. Surg. Endosc. 25:2224–2229, 2011.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Hashimoto, Y., S. Funamoto, T. Kimura, K. Nam, T. Fujisato, and A. Kishida. The effect of decellularized bone/bone marrow produced by high-hydrostatic pressurization on the osteogenic differentiation of mesenchymal stem cells. Biomaterials 32:7060–7067, 2011.PubMedGoogle Scholar
  103. 103.
    Haykal, S., Y. Zhou, P. Marcus, M. Salna, T. Machuca, S. O. P. Hofer, and T. K. Waddell. The effect of decellularization of tracheal allografts on leukocyte infiltration and of recellularization on regulatory T cell recruitment. Biomaterials 34:5821–5832, 2013.PubMedGoogle Scholar
  104. 104.
    Hennessy, R. S., S. Jana, B. J. Tefft, M. R. Helder, M. D. Young, R. R. Hennessy, N. J. Stoyles, and A. Lerman. Supercritical carbon dioxide–based sterilization of decellularized heart valves. JACC Basic Transl. Sci. 2:71–84, 2017.PubMedPubMedCentralGoogle Scholar
  105. 105.
    Hirsh, S. L., D. R. McKenzie, N. J. Nosworthy, J. A. Denman, O. U. Sezerman, and M. M. M. Bilek. The Vroman effect: Competitive protein exchange with dynamic multilayer protein aggregates. Coll. Surf. B Biointerfaces 103:395–404, 2013.Google Scholar
  106. 106.
    HO, K. L., V. M. N. Witte, and E. T. Bird. 8-ply small intestinal submucosa tension-free sling: Spectrum of postoperative inflammation. J. Urol. 171:268–271, 2004.PubMedGoogle Scholar
  107. 107.
    Hodde, J., A. Janis, D. Ernst, D. Zopf, D. Sherman, and C. Johnson. Effects of sterilization on an extracellular matrix scaffold: Part I. Composition and matrix architecture. J. Mater. Sci. Mater. Med. 18:537–543, 2007.PubMedGoogle Scholar
  108. 108.
    Hodde, J., A. Janis, and M. Hiles. Effects of sterilization on an extracellular matrix scaffold: Part II. Bioactivity and matrix interaction. J. Mater. Sci. Mater. Med. 18:545–550, 2007.PubMedGoogle Scholar
  109. 109.
    Hoganson, D. M., A. M. Meppelink, C. J. Hinkel, S. M. Goldman, X.-H. Liu, R. M. Nunley, J. P. Gaut, and J. P. Vacanti. Differentiation of human bone marrow mesenchymal stem cells on decellularized extracellular matrix materials. J. Biomed. Mater. Res. A 102:2875–2883, 2014.PubMedGoogle Scholar
  110. 110.
    Hong, X., Y. Yuan, X. Sun, M. Zhou, G. Guo, Q. Zhang, J. Hescheler, and J. Xi. Skeletal extracellular matrix supports cardiac differentiation of embryonic stem cells: A potential scaffold for engineered cardiac tissue. Cell. Physiol. Biochem. 45:319–331, 2018.PubMedGoogle Scholar
  111. 111.
    Hoppo, T., S. F. Badylak, and B. A. Jobe. A novel esophageal-preserving approach to treat high-grade dysplasia and superficial adenocarcinoma in the presence of chronic gastroesophageal reflux disease. World J. Surg. 36:2390–2393, 2012.PubMedGoogle Scholar
  112. 112.
    Huang, Y. H., F. W. Tseng, W. H. Chang, I. C. Peng, D. J. Hsieh, S. W. Wu, and M. L. Yeh. Preparation of acellular scaffold for corneal tissue engineering by supercritical carbon dioxide extraction technology. Acta Biomater. 58:238–243, 2017.PubMedGoogle Scholar
  113. 113.
    Huleihel, L., J. G. Bartolacci, J. L. Dziki, T. Vorobyov, B. Arnold, M. E. Scarritt, C. Pineda Molina, S. T. LoPresti, B. N. Brown, J. D. Naranjo, and S. F. Badylak. Matrix-bound nanovesicles recapitulate extracellular matrix effects on macrophage phenotype. Tissue Eng. Part A 23:1283–1294, 2017.PubMedPubMedCentralGoogle Scholar
  114. 114.
    Huleihel, L., J. L. Dziki, J. G. Bartolacci, T. Rausch, M. E. Scarritt, M. C. Cramer, T. Vorobyov, S. T. LoPresti, I. T. Swineheart, L. J. White, B. N. Brown, and S. F. Badylak. Macrophage phenotype in response to ECM bioscaffolds. Semin. Immunol. 29:2–13, 2017.PubMedPubMedCentralGoogle Scholar
  115. 115.
    Huleihel, L., G. S. Hussey, J. D. Naranjo, L. Zhang, J. L. Dziki, N. J. Turner, D. B. Stolz, and S. F. Badylak. Matrix-bound nanovesicles within ECM bioscaffolds. Sci. Adv. 2:e1600502, 2016.PubMedPubMedCentralGoogle Scholar
  116. 116.
    Hutter, H., B. E. Vogel, J. D. Plenefisch, C. R. Norris, R. B. Proenca, J. Spieth, C. Guo, S. Mastwal, X. Zhu, J. Scheel, and E. M. Hedgecock. Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science (80-) 287:989–1010, 2000.Google Scholar
  117. 117.
    Hynes, R. O. The evolution of metazoan extracellular matrix. J. Cell Biol. 196:671–679, 2012.PubMedPubMedCentralGoogle Scholar
  118. 118.
    Iozzo, R. V. Perlecan: A gem of a proteoglycan. Matrix Biol. 14:203–208, 1994.PubMedGoogle Scholar
  119. 119.
    ISO 13408-1. Aseptic processing of health care products — Part 1: General requirements., 2008.Google Scholar
  120. 120.
    ISO 22442-1. Medical devices utilizing animal tissues and their derivatives — Part 1: Application of risk management., 2015.Google Scholar
  121. 121.
    Jackson, D. W., E. S. Grood, P. Wilcox, D. L. Butler, T. M. Simon, and J. P. Holden. The effects of processing techniques on the mechanical properties of bone-anterior cruciate ligament-bone allografts. An experimental study in goats. Am. J. Sports Med. 16:101–105, 1988.PubMedGoogle Scholar
  122. 122.
    Jackson, D. W., G. E. Windler, and T. M. Simon. Intraarticular reaction associated with the use of freeze-dried, ethylene oxide-sterilized bone-patella tendon-bone allografts in the reconstruction of the anterior cruciate ligament. Am. J. Sports Med. 18:1–11, 1990.PubMedGoogle Scholar
  123. 123.
    Jang, J., T. G. Kim, B. S. Kim, S. W. Kim, S. M. Kwon, and D. W. Cho. Tailoring mechanical properties of decellularized extracellular matrix bioink by vitamin B2-induced photo-crosslinking. Acta Biomater. 33:88–95, 2016.PubMedGoogle Scholar
  124. 124.
    Ji, R., N. Zhang, N. You, Q. Li, W. Liu, N. Jiang, J. Liu, H. Zhang, D. Wang, K. Tao, and K. Dou. The differentiation of MSCs into functional hepatocyte-like cells in a liver biomatrix scaffold and their transplantation into liver-fibrotic mice. Biomaterials 33:8995–9008, 2012.PubMedGoogle Scholar
  125. 125.
    John, T. T., N. Aggarwal, A. K. Singla, and R. A. Santucci. Intense inflammatory reaction with porcine small intestine submucosa pubovaginal sling or tape for stress urinary incontinence. Urology 72:1036–1039, 2008.PubMedGoogle Scholar
  126. 126.
    Johnson, T. D., R. L. Braden, and K. L. Christman. Injectable ECM scaffolds for cardiac repair. Methods Mol. Biol. 1181:109–120, 2014.PubMedPubMedCentralGoogle Scholar
  127. 127.
    Johnson, T. D., J. A. Dequach, R. Gaetani, J. Ungerleider, D. Elhag, V. Nigam, A. Behfar, and K. L. Christman. Human versus porcine tissue sourcing for an injectable myocardial matrix hydrogel. Biomater. Sci. 29:13–17, 2014.Google Scholar
  128. 128.
    Johnson, T. D., S. Y. Lin, and K. L. Christman. Tailoring material properties of a nanofibrous extracellular matrix derived hydrogel. Nanotechnology 22:494015, 2011.PubMedPubMedCentralGoogle Scholar
  129. 129.
    Kaufmann, R., A. P. Jairam, I. M. Mulder, Z. Wu, J. Verhelst, S. Vennix, L. J. X. Giesen, M. C. Clahsen-van Groningen, and J. Jeekel. Lange JF (2019) Non-cross-linked collagen mesh performs best in a physiologic, noncontaminated rat model. Surg. Innov. 26:302–311, 2019.PubMedPubMedCentralGoogle Scholar
  130. 130.
    Kaufmann, R., A. P. Jairam, I. M. Mulder, Z. Wu, J. Verhelst, S. Vennix, L. J. X. Giesen, M. C. Clahsen-van Groningen, J. Jeekel, and J. F. Lange. Characteristics of different mesh types for abdominal wall repair in an experimental model of peritonitis. Br. J. Surg. 104:1884–1893, 2017.PubMedGoogle Scholar
  131. 131.
    Keane, T. J., and S. F. Badylak. The host response to allogeneic and xenogeneic biological scaffold materials. J. Tissue Eng. Regen. Med. 9:504–511, 2015.PubMedGoogle Scholar
  132. 132.
    Keane, T. J., A. DeWard, R. Londono, L. T. Saldin, A. A. Castleton, L. Carey, A. Nieponice, E. Lagasse, and S. F. Badylak. Tissue-specific effects of esophageal extracellular matrix. Tissue Eng. Part A 21:2293–2300, 2015.PubMedPubMedCentralGoogle Scholar
  133. 133.
    Keane, T. J., J. Dziki, E. Sobieski, A. Smoulder, A. Castleton, N. Turne, L. J. White, and S. F. Badylak. Restoring mucosal barrier function and modifying macrophage phenotype with an extracellular matrix hydrogel: Potential therapy for ulcerative colitis. J. Crohn’s Colitis 11:360–368, 2017.Google Scholar
  134. 134.
    Keane, T. J., R. Londono, N. J. Turner, and S. F. Badylak. Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33:1771–1781, 2012.PubMedGoogle Scholar
  135. 135.
    Keane, T. J., I. T. Swinehart, and S. F. Badylak. Methods of tissue decellularization used for preparation of biologic scaffolds and in vivo relevance. Methods 84:25–34, 2015.PubMedGoogle Scholar
  136. 136.
    Kelly, D. J., A. B. Rosen, A. J. T. Schuldt, P. V. Kochupura, S. V. Doronin, I. A. Potapova, E. U. Azeloglu, S. F. Badylak, P. R. Brink, I. S. Cohen, and G. R. Gaudette. Increased myocyte content and mechanical function within a tissue-engineered myocardial patch following implantation. Tissue Eng. Part A 15:2189–2201, 2009.PubMedPubMedCentralGoogle Scholar
  137. 137.
    Kimmel, H., M. Rahn, and T. W. Gilbert. The clinical effectiveness in wound healing with extracellular matrix derived from porcine urinary bladder matrix: A case series on severe chronic wounds. J. Am. Col. Certif. Wound Spec. 2:55–59, 2010.PubMedPubMedCentralGoogle Scholar
  138. 138.
    Knoll, L. D. Use of small intestinal submucosa graft for the surgical management of Peyronie’s disease. J. Urol. 178:2474–2478, 2007.PubMedGoogle Scholar
  139. 139.
    Kochupura, P. V., E. U. Azeloglu, D. J. Kelly, S. V. Doronin, S. F. Badylak, I. B. Krukenkamp, I. S. Cohen, and G. R. Gaudette. Tissue-engineered myocardial patch derived from extracellular matrix provides regional mechanical function. Circulation 112:144–149, 2005.Google Scholar
  140. 140.
    Koci, Z., K. Vyborny, J. Dubisova, I. Vackova, A. Jager, O. Lunov, K. Jirakova, and S. Kubinova. Extracellular matrix hydrogel derived from human umbilical cord as a scaffold for neural tissue repair and its comparison with extracellular matrix from porcine tissues. Tissue Eng. Part C Methods 23:333–345, 2017.PubMedGoogle Scholar
  141. 141.
    Kramer, J. Extracellular matrix. In: C. elegans II, edited by D. Riddle, T. Blumenthal, and B. Meyer. Boston: Springer, 1997.Google Scholar
  142. 142.
    Kropp, B. P., B. L. Eppley, C. D. Prevel, M. K. Rippy, R. C. Harruff, S. F. Badylak, M. C. Adams, R. C. Rink, and M. A. Keating. Experimental assessment of small intestinal submucosa as a bladder wall substitute. Urology 46:396–400, 1995.PubMedGoogle Scholar
  143. 143.
    Kulig, K. M., X. Luo, E. B. Finkelstein, X. H. Liu, S. M. Goldman, C. A. Sundback, J. P. Vacanti, and C. M. Neville. Biologic properties of surgical scaffold materials derived from dermal ECM. Biomaterials 34:5776–5784, 2013.PubMedGoogle Scholar
  144. 144.
    Lee, J. S., J. Shin, H. M. Park, Y. G. Kim, B. G. Kim, J. W. Oh, and S. W. Cho. Liver extracellular matrix providing dual functions of two-dimensional substrate coating and three-dimensional injectable hydrogel platform for liver tissue engineering. Biomacromolecules 15:206–218, 2014.PubMedGoogle Scholar
  145. 145.
    Liang, R., G. Yang, K. E. Kim, A. D’Amore, A. N. Pickering, C. Zhang, and S. L.-Y. Woo. Positive effects of an extracellular matrix hydrogel on rat anterior cruciate ligament fibroblast proliferation and collagen mRNA expression. J. Orthop. Transl. 3:114–122, 2015.Google Scholar
  146. 146.
    Liao, J., E. M. Joyce, and M. S. Sacks. Effects of decellularization on the mechanical and structural properties of the porcine aortic valve leaflet. Biomaterials 29:1065–1074, 2008.PubMedPubMedCentralGoogle Scholar
  147. 147.
    Liu, C. J., S. D. Dib-Hajj, and S. G. Waxman. Fibroblast growth factor homologous factor 1B binds to the C terminus of the tetrodotoxin-resistant sodium channel rNav1.9a (NaN). J. Biol. Chem. 276:18925–18933, 2001.Google Scholar
  148. 148.
    Liu, X., N. Li, D. Gong, C. Xia, and Z. Xu. Comparison of detergent-based decellularization protocols for the removal of antigenic cellular components in porcine aortic valve. Xenotransplantation 25:1–13, 2018.Google Scholar
  149. 149.
    Liu, Z., R. Tang, Z. Zhou, Z. Song, H. Wang, and Y. Gu. Comparison of two porcine-derived materials for repairing abdominal wall defects in rats. PLoS ONE 6:e20520, 2011.PubMedPubMedCentralGoogle Scholar
  150. 150.
    Londono, R., J. L. Dziki, E. Haljasmaa, N. J. Turner, C. A. Leifer, and S. F. Badylak. The effect of cell debris within biologic scaffolds upon the macrophage response. J. Biomed. Mater. Res. Part A 105:2109–2118, 2017.Google Scholar
  151. 151.
    Loneker, A. E., D. M. Faulk, G. S. Hussey, A. D’Amore, and S. F. Badylak. Solubilized liver extracellular matrix maintains primary rat hepatocyte phenotype in-vitro. J. Biomed. Mater. Res. A 104:957–965, 2016.PubMedGoogle Scholar
  152. 152.
    Longaker, M. T., E. S. Chu, N. S. Adzick, M. Stern, M. R. Harrison, and R. Stern. Studies in fetal wound healing. V. A prolonged presence of hyaluronic acid characterizes fetal wound fluid. Ann. Surg. 213:292–296, 1991.PubMedPubMedCentralGoogle Scholar
  153. 153.
    Longaker, M. T., D. J. Whitby, M. W. J. Ferguson, M. R. Harrison, T. M. Crombleholme, J. C. Langer, K. C. Cochrum, E. D. Verrier, and R. Stern. Studies in fetal wound healing: III. Early deposition of fibronectin distinguishes fetal from adult wound healing. J. Pediatr. Surg. 24:799–805, 1989.PubMedGoogle Scholar
  154. 154.
    LoPresti, S. T., and B. N. Brown. Effect of source animal age upon macrophage response to extracellular matrix biomaterials. J. Immunol. Regen. Med. 1:57–66, 2018.PubMedPubMedCentralGoogle Scholar
  155. 155.
    Lovvorn, III, H. N., D. T. Cheung, M. E. Nimni, N. Perelman, J. M. Estes, and N. S. Adzick. Relative distribution and crosslinking of collagen distinguish fetal from adult sheep wound repair. J. Pediatr. Surg. 34:218–223, 1999.PubMedGoogle Scholar
  156. 156.
    Lu, Q., M. Li, Y. Zou, and T. Cao. Delivery of basic fibroblast growth factors from heparinized decellularized adipose tissue stimulates potent de novo adipogenesis. J. Control. Release 174:43–50, 2014.PubMedGoogle Scholar
  157. 157.
    Lumpkins, S. B., N. Pierre, and P. S. McFetridge. A mechanical evaluation of three decellularization methods in the design of a xenogeneic scaffold for tissue engineering the temporomandibular joint disc. Acta Biomater. 4:808–816, 2008.PubMedGoogle Scholar
  158. 158.
    Ma, B., X. Wang, C. Wu, and J. Chang. Crosslinking strategies for preparation of extracellular matrix-derived cardiovascular scaffolds. Regen. Biomater. 1:81–89, 2014.PubMedPubMedCentralGoogle Scholar
  159. 159.
    Manji, R. A., L. F. Zhu, N. K. Nijjar, D. C. Rayner, G. S. Korbutt, T. A. Churchill, R. V. Rajotte, A. Koshal, and D. B. Ross. Glutaraldehyde-fixed bioprosthetic heart valve conduits calcify and fail from xenograft rejection. Circulation 114:318–327, 2006.PubMedGoogle Scholar
  160. 160.
    Mantovani, A., S. K. Biswas, M. R. Galdiero, A. Sica, and M. Locati. Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 229:176–185, 2013.PubMedGoogle Scholar
  161. 161.
    Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25:677–686, 2004.PubMedGoogle Scholar
  162. 162.
    Mase, V., J. Hsu, S. Wolf, J. Wenke, D. Baer, J. Owens, S. Badylak, and T. Walters. Clinical application of an acellular biologic scaffold for surgical repair of a large, traumatic quadriceps femoris muscle defect. Orthopedics 33:511, 2010.PubMedPubMedCentralGoogle Scholar
  163. 163.
    Matuska, A. M., and P. S. McFetridge. The effect of terminal sterilization on structural and biophysical properties of a decellularized collagen-based scaffold; Implications for stem cell adhesion. J. Biomed. Mater. Res. Part B Appl. Biomater. 103:397–406, 2015.PubMedGoogle Scholar
  164. 164.
    Medberry, C. J., P. M. Crapo, B. F. Siu, C. A. Carruthers, M. T. Wolf, S. P. Nagarkar, V. Agrawal, K. E. Jones, J. Kelly, S. A. Johnson, S. S. Velankar, S. C. Watkins, M. Modo, and S. F. Badylak. Hydrogels derived from central nervous system extracellular matrix. Biomaterials 34:1033–1040, 2013.PubMedGoogle Scholar
  165. 165.
    Melman, L., E. D. Jenkins, N. A. Hamilton, L. C. Bender, M. D. Brodt, C. R. Deeken, S. C. Greco, M. M. Frisella, and B. D. Matthews. Early biocompatibility of crosslinked and non-crosslinked biologic meshes in a porcine model of ventral hernia repair. Hernia 15:157–164, 2011.PubMedPubMedCentralGoogle Scholar
  166. 166.
    Meng, F. W., P. F. Slivka, C. L. Dearth, and S. F. Badylak. Solubilized extracellular matrix from brain and urinary bladder elicits distinct functional and phenotypic responses in macrophages. Biomaterials 46:131–140, 2015.PubMedGoogle Scholar
  167. 167.
    Mercuri, J. J., S. Patnaik, G. Dion, S. S. Gill, J. Liao, and D. T. Simionescu. Regenerative potential of decellularized porcine nucleus pulposus hydrogel scaffolds: Stem cell differentiation, matrix remodeling, and biocompatibility studies. Tissue Eng. Part A 19:952–966, 2013.PubMedGoogle Scholar
  168. 168.
    Merguerian, P. A., P. P. Reddy, D. J. Barrieras, G. J. Wilson, K. Woodhouse, D. J. Bagli, G. A. McLorie, and A. E. Khoury. Acellular bladder matrix allografts in the regeneration of functional bladders: Evaluation of large-segment (> 24 cm) substitution in a porcine model. BJU Int. 85:894–898, 2000.PubMedGoogle Scholar
  169. 169.
    Mestak, O., Z. Spurkova, K. Benkova, P. Vesely, V. Hromadkova, J. Miletin, R. Juzek, J. Mestak, M. Molitor, and A. Sukop. Comparison of cross-linked and non-cross-linked acellular porcine dermal scaffolds for long-term full-thickness hernia repair in a small animal model. Eplasty 14:172–183, 2014.Google Scholar
  170. 170.
    Meyer, S. R., B. Chiu, T. A. Churchill, L. Zhu, J. R. T. Lakey, and D. B. Ross. Comparison of aortic valve allograft decellularization techniques in the rat. J. Biomed. Mater. Res. 79A:254–262, 2006.Google Scholar
  171. 171.
    Mills, C. D., K. Kincaid, J. M. Alt, M. J. Heilman, and A. M. Hill. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164:6166–6173, 2000.Google Scholar
  172. 172.
    Miyazaki, K., and T. Maruyama. Partial regeneration and reconstruction of the rat uterus through recellularization of a decellularized uterine matrix. Biomaterials 35:8791–8800, 2014.PubMedGoogle Scholar
  173. 173.
    Mora-Solano, C., and J. H. Collier. Engaging adaptive immunity with biomaterials. J. Mater. Chem. B 2:2409–2421, 2014.PubMedGoogle Scholar
  174. 174.
    Moreau, M. F., Y. Gallois, M. F. Baslé, and D. Chappard. Gamma irradiation of human bone allografts alters medullary lipids and releases toxic compounds for osteoblast-like cells. Biomaterials 21:369–376, 2000.PubMedGoogle Scholar
  175. 175.
    Morris, A. H., J. Chang, and T. R. Kyriakides. Inadequate processing of decellularized dermal matrix reduces cell viability in vitro and increases apoptosis and acute inflammation in vivo. Biores. Open Access 5(1):177–187, 2016.PubMedPubMedCentralGoogle Scholar
  176. 176.
    Mosmann, T. R., and S. Sad. The expanding universe of T-cell subsets: Th1, Th2 and more. Immunol. Today 17:138–146, 1996.PubMedGoogle Scholar
  177. 177.
    Mulder, I. M., E. B. Deerenberg, W. A. Bemelman, J. Jeekel, and J. F. Lange. Infection susceptibility of crosslinked and non-crosslinked biological meshes in an experimental contaminated environment. Am. J. Surg. 210:159–166, 2015.PubMedGoogle Scholar
  178. 178.
    Nakatsu, H., T. Ueno, A. Oga, M. Nakao, T. Nishimura, S. Kobayashi, and M. Oka. Influence of mesenchymal stem cells on stomach tissue engineering using small intestinal submucosa. J. Tissue Eng. Regen. Med. 9:296–304, 2015.PubMedGoogle Scholar
  179. 179.
    Nakayama, K. H., C. C. I. Lee, C. A. Batchelder, and A. F. Tarantal. Tissue specificity of decellularized rhesus monkey kidney and lung scaffolds. PLoS ONE 8:e64134, 2013.PubMedPubMedCentralGoogle Scholar
  180. 180.
    Naso, F., A. Gandaglia, T. Bottio, V. Tarzia, M. B. Nottle, A. J. F. d’Apice, P. J. Cowan, E. Cozzi, C. Galli, I. Lagutina, G. Lazzari, L. Iop, M. Spina, and G. Gerosa. First quantification of alpha-Gal epitope in current glutaraldehyde-fixed heart valve bioprostheses. Xenotransplantation 20:252–261, 2013.PubMedGoogle Scholar
  181. 181.
    Navarro-Tableros, V., M. B. Herrera Sanchez, F. Figliolini, R. Romagnoli, C. Tetta, and G. Camussi. Recellularization of rat liver scaffolds by human liver stem cells. Tissue Eng. Part A 21:1929–1939, 2015.PubMedPubMedCentralGoogle Scholar
  182. 182.
    Ngo, M. D., H. M. Aberman, M. L. Hawes, B. Choi, and A. A. Gertzman. Evaluation of human acellular dermis versus porcine acellular dermis in an in vivo model for incisional hernia repair. Cell Tissue Bank. 12:135–145, 2011.PubMedPubMedCentralGoogle Scholar
  183. 183.
    Nieponice, A., F. F. Ciotola, F. Nachman, B. A. Jobe, T. Hoppo, R. Londono, S. Badylak, and A. E. Badaloni. Patch esophagoplasty: Esophageal reconstruction using biologic scaffolds. Ann. Thorac. Surg. 97:283–288, 2014.PubMedGoogle Scholar
  184. 184.
    Nieponice, A., K. McGrath, I. Qureshi, E. J. Beckman, J. D. Luketich, T. W. Gilbert, and S. F. Badylak. An extracellular matrix scaffold for esophageal stricture prevention after circumferential EMR. Gastrointest. Endosc. 69:289–296, 2009.PubMedGoogle Scholar
  185. 185.
    Novitsky, Y. W., S. B. Orenstein, and D. L. Kreutzer. Comparative analysis of histopathologic responses to implanted porcine biologic meshes. Hernia 18:713–721, 2014.PubMedGoogle Scholar
  186. 186.
    O’Neill, J. D., D. O. Freytes, A. Anandappa, J. A. Oliver, and G. Vunjak-Novakovic. The regulation of growth and metabolism of kidney stem cell with regional specificity using extracellular matrix derived from kidney. Biomaterials 34:1–7, 2013.Google Scholar
  187. 187.
    Okumura, M., R. J. Matthews, B. Robb, G. W. Litman, P. Bork, and M. L. Thomas. Comparison of CD45 extracellular domain sequences from divergent vertebrate species suggests the conservation of three fibronectin type III domains. J. Immunol. 157:1569–1575, 1996.PubMedGoogle Scholar
  188. 188.
    Omae, H., C. Zhao, L. S. Yu, K. N. An, and P. C. Amadio. Multilayer tendon slices seeded with bone marrow stromal cells: A novel composite for tendon engineering. J. Orthop. Res. 27:937–942, 2009.PubMedPubMedCentralGoogle Scholar
  189. 189.
    Oswal, D., S. Korossis, S. Mirsadraee, H. Wilcox, and K. Watterson. Biomechanical characterization of decellularized and cross-linked bovine pericardium. J. Heart Valve Dis. 16:165–174, 2007.PubMedGoogle Scholar
  190. 190.
    Pashos, N. C., M. E. Scarritt, Z. R. Eagle, J. M. Gimble, A. E. Chaffin, and B. A. Bunnell. Characterization of an acellular scaffold for a tissue engineering approach to the nipple-areolar complex reconstruction. Cells Tissues Organs 203:183–193, 2017.PubMedPubMedCentralGoogle Scholar
  191. 191.
    Pati, F., J. Jang, D.-H. Ha, S. Won Kim, J.-W. Rhie, J.-H. Shim, D.-H. Kim, and D.-W. Cho. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat. Commun. 5:3935, 2014.PubMedPubMedCentralGoogle Scholar
  192. 192.
    Patil, P. B., P. B. Chogue, V. K. Kumar, S. Almstrom, H. Backdahl, D. Banerjee, G. Hernlenius, M. Olausson, and S. Sumitran-Holgersson. Recellularization of acellular human small intestine using bone marrow stem cells. Stem Cells Transl. Med. 2:307–315, 2013.PubMedPubMedCentralGoogle Scholar
  193. 193.
    Perniconi, B., D. Coletti, P. Aulino, A. Costa, P. Aprile, L. Santacroce, E. Chiaravalloti, L. Coquelin, N. Chevallier, L. Teodori, S. Adamo, M. Marrelli, and M. Tatullo. Muscle acellular scaffold as a biomaterial: Effects on C2C12 cell differentiation and interaction with the murine host environment. Front. Physiol. 5:1–13, 2014.Google Scholar
  194. 194.
    Perniconi, B., A. Costa, P. Aulino, L. Teodori, S. Adamo, and D. Coletti. The pro-myogenic environment provided by whole organ scale acellular scaffolds from skeletal muscle. Biomaterials 32:7870–7882, 2011.PubMedGoogle Scholar
  195. 195.
    Price, A. P., K. A. England, A. M. Matson, B. R. Blazar, and A. Panoskaltsis-Mortari. Development of a decellularized lung bioreactor system for bioengineering the lung: The matrix reloaded. Tissue Eng. Part A 16:2581–2591, 2010.PubMedPubMedCentralGoogle Scholar
  196. 196.
    Quarti, A., S. Nardone, M. Colaneri, G. Santoro, and M. Pozzi. Preliminary experience in the use of an extracellular matrix to repair congenital heart diseases. Interact. Cardiovasc. Thorac. Surg. 13:569–572, 2011.PubMedGoogle Scholar
  197. 197.
    Rajabi-Zeleti, S., S. Jalili-Firoozinezhad, M. Azarnia, F. Khayyatan, S. Vahdat, S. Nikeghbalian, A. Khademhosseini, H. Baharvand, and N. Aghdami. The behavior of cardiac progenitor cells on macroporous pericardium-derived scaffolds. Biomaterials 35:970–982, 2014.PubMedGoogle Scholar
  198. 198.
    Reddy, P. P., D. J. Barrieras, G. Wilson, D. J. Bagli, G. A. McLorie, A. E. Khoury, and P. A. Merguerian. Regeneration of functional bladder substitutes using large segment acellular matrix allografts in a porcine model. J. Urol. 164:936–941, 2000.PubMedGoogle Scholar
  199. 199.
    Reing, J. E., B. N. Brown, K. A. Daly, J. M. Freund, T. W. Gilbert, S. X. Hsiong, A. Huber, K. E. Kullas, S. Tottey, M. T. Wolf, and S. F. Badylak. The effects of processing methods upon mechanical and biologic properties of porcine dermal extracellular matrix scaffolds. Biomaterials 31:8626–8633, 2010.PubMedPubMedCentralGoogle Scholar
  200. 200.
    Reing, J. E., L. Zhang, J. Myers-Irvin, K. E. Cordero, D. O. Freytes, E. Heber-Katz, K. Bedelbaeva, D. McIntosh, A. Dewilde, S. J. Braunhut, and S. F. Badylak. Degradation products of extracellular matrix affect cell migration and proliferation. Tissue Eng. Part A 15:605–614, 2009.PubMedGoogle Scholar
  201. 201.
    Rieder, E., M. T. Kasimir, G. Silberhumer, G. Seebacher, E. Wolner, P. Simon, and G. Weigel. Decellularization protocols of porcine heart valves differ importantly in efficiency of cell removal and susceptibility of the matrix to recellularization with human vascular cells. J. Thorac. Cardiovasc. Surg. 127:399–405, 2004.PubMedGoogle Scholar
  202. 202.
    Rommer, E. A., M. Peric, and A. Wong. Urinary bladder matrix for the treatment of recalcitrant nonhealing radiation wounds. Adv. Skin Wound Care 26:450–455, 2013.PubMedGoogle Scholar
  203. 203.
    Rosario, D. J., G. C. Reilly, E. A. Salah, M. Glover, A. J. Bullock, and S. MacNeil. Decellularization and sterilization of porcine urinary bladder matrix for tissue engineering in the lower urinary tract. Regen. Med. 3:145–156, 2008.PubMedGoogle Scholar
  204. 204.
    Ross, E. A., M. J. Williams, T. Hamazaki, N. Terada, W. L. Clapp, C. Adin, G. W. Ellison, M. Jorgensen, and C. D. Batich. Embryonic stem cells proliferate and differentiate when seeded into kidney scaffolds. J. Am. Soc. Nephrol. 20:2338–2347, 2009.PubMedPubMedCentralGoogle Scholar
  205. 205.
    Sadtler, K., B. W. Allen, K. Estrellas, F. Housseau, D. M. Pardoll, and J. H. Elisseeff. The scaffold immune microenvironment: Biomaterial-mediated immune polarization in traumatic and nontraumatic applications. Tissue Eng. Part A 23:1044–1053, 2017.PubMedPubMedCentralGoogle Scholar
  206. 206.
    Sadtler, K., K. Estrellas, B. W. Allen, M. T. Wolf, H. Fan, A. J. Tam, C. H. Patel, B. S. Luber, H. Wang, K. R. Wagner, J. D. Powell, F. Housseau, D. M. Pardoll, and J. H. Elisseeff. Developing a pro-regenerative biomaterial scaffold microenvironment requires T helper 2 cells. Science 352:366–370, 2016.PubMedPubMedCentralGoogle Scholar
  207. 207.
    Sadtler, K., M. T. Wolf, S. Ganguly, C. A. Moad, L. Chung, S. Majumdar, F. Housseau, D. M. Pardoll, and J. H. Elisseeff. Divergent immune responses to synthetic and biological scaffolds. Biomaterials 192:405–415, 2019.PubMedGoogle Scholar
  208. 208.
    Saldin, L. T., M. C. Cramer, S. S. Velankar, L. J. White, and S. F. Badylak. Extracellular matrix hydrogels from decellularized tissues: Structure and function. Acta Biomater. 49:1–15, 2017.PubMedGoogle Scholar
  209. 209.
    Sandor, M., H. Xu, J. Connor, J. Lombardi, J. R. Harper, R. P. Silverman, and D. J. McQuillan. Host response to implanted porcine-derived biologic materials in a primate model of abdominal wall repair. Tissue Eng. Part A 14:2021–2031, 2008.PubMedGoogle Scholar
  210. 210.
    Santoso, E. G., K. Yoshida, Y. Hirota, M. Aizawa, O. Yoshino, A. Kishida, Y. Osuga, S. Saito, T. Ushida, and K. S. Furukawa. Application of detergents or high hydrostatic pressure as decellularization processes in uterine tissues and their subsequent effects on in vivo uterine regeneration in murine models. PLoS ONE 9:e103201, 2014.PubMedPubMedCentralGoogle Scholar
  211. 211.
    Sarathchandra, P., R. T. Smolenski, A. H. Y. Yuen, A. H. Chester, S. Goldstein, A. E. Heacox, M. H. Yacoub, and P. M. Taylor. Impact of γ-irradiation on extracellular matrix of porcine pulmonary valves. J. Surg. Res. 176:376–385, 2012.PubMedGoogle Scholar
  212. 212.
    Sasikumar, S., S. Chameettachal, B. Cromer, F. Pati, and P. Kingshott. Decellularized extracellular matrix hydrogels– cell behavior as function of matrix stiffness. Curr. Opin. Biomed. Eng. 10:123–133, 2019.Google Scholar
  213. 213.
    Sawada, K., D. Terada, T. Yamaoka, S. Kitamura, and T. Fujisato. Cell removal with supercritical carbon dioxide for acellular artificial tissue. J. Chem. Technol. Biotechnol. 83:943–949, 2008.Google Scholar
  214. 214.
    Sawai, T., N. Usui, K. Sando, Y. Fukui, S. Kamata, A. Okada, N. Taniguchi, N. Itano, and K. Kimata. Hyaluronic acid of wound fluid in adult and fetal rabbits. J. Pediatr. Surg. 32:41–43, 1997.PubMedGoogle Scholar
  215. 215.
    Schoen, F. J., and R. J. Levy. Calcification of tissue heart valve substitutes: Progress toward understanding and prevention. Ann. Thorac. Surg. 79:1072–1080, 2005.PubMedGoogle Scholar
  216. 216.
    Scholl, F. G., M. M. Boucek, K.-C. Chan, L. Valdes-Cruz, and R. Perryman. Preliminary experience with cardiac reconstruction using decellularized porcine extracellular matrix scaffold: Human applications in congenital heart disease. World J. Pediatr. Congenit. Hear. Surg. 1:132–136, 2010.Google Scholar
  217. 217.
    Sclamberg, S. G., J. E. Tibone, J. M. Itamura, and S. Kasraeian. Six-month magnetic resonance imaging follow-up of large and massive rotator cuff repairs reinforced with porcine small intestinal submucosa. J. Shoulder Elb. Surg. 13:538–541, 2004.Google Scholar
  218. 218.
    Sellaro, T. L., A. K. Ravindra, D. B. Stolz, and S. F. Badylak. Maintenance of hepatic sinusoidal endothelial cell phenotype in vitro using organ-specific extracellular matrix scaffolds. Tissue Eng. 13:2301–2310, 2007.PubMedGoogle Scholar
  219. 219.
    Seo, Y., Y. Jung, and S. H. Kim. Decellularized heart ECM hydrogel using supercritical carbon dioxide for improved angiogenesis. Acta Biomater. 67:270–281, 2018.PubMedGoogle Scholar
  220. 220.
    Shah, M., P. Kc, K. M. Copeland, J. Liao, and G. Zhang. A thin layer of decellularized porcine myocardium for cell delivery. Sci. Rep. 8:1–11, 2018.Google Scholar
  221. 221.
    Shah, B. C., M. M. Tiwari, M. R. Goede, M. J. Eichler, R. R. Hollins, C. L. McBride, J. S. Thompson, and D. Oleynikov. Not all biologics are equal!. Hernia 15:165–171, 2011.PubMedGoogle Scholar
  222. 222.
    Shamis, Y., E. Hasson, A. Soroker, E. Bassat, Y. Shimoni, T. Ziv, R. V. Sionov, and E. Mitrani. Organ-specific scaffolds for in vitro expansion, differentiation, and organization of primary lung cells. Tissue Eng. Part C Methods 17:861–870, 2011.PubMedGoogle Scholar
  223. 223.
    Shin, K., K. H. Koo, J. Jeong, S. J. Park, D. J. Choi, Y.-G. Ko, and H. Kwon. Three-dimensional culture of salivary gland stem cell in orthotropic decellularized extracellular matrix hydrogels. Tissue Eng. Part A 2019. Scholar
  224. 224.
    Shojaie, S., L. Ermini, C. Ackerley, J. Wang, S. Chin, B. Yeganeh, M. Bilodeau, M. Sambi, I. Rogers, J. Rossant, C. E. Bear, and M. Post. Acellular lung scaffolds direct differentiation of endoderm to functional airway epithelial cells: Requirement of matrix-bound HS proteoglycans. Stem Cell Rep. 4:419–430, 2015.Google Scholar
  225. 225.
    Sicari, B. M., V. Agrawal, B. F. Siu, C. J. Medberry, C. L. Dearth, N. J. Turner, and S. F. Badylak. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng. Part A 18:1941–1948, 2012.PubMedPubMedCentralGoogle Scholar
  226. 226.
    Sicari, B. M., J. L. Dziki, B. F. Siu, C. J. Medberry, C. L. Dearth, and S. F. Badylak. The promotion of a constructive macrophage phenotype by solubilized extracellular matrix. Biomaterials 35:8605–8612, 2014.PubMedGoogle Scholar
  227. 227.
    Sicari, B. M., S. A. Johnson, B. F. Siu, P. M. Crapo, K. A. Daly, H. Jiang, C. J. Medberry, S. Tottey, N. J. Turner, and S. F. Badylak. The effect of source animal age upon the in vivo remodeling characteristics of an extracellular matrix scaffold. Biomaterials 33:5524–5533, 2012.PubMedPubMedCentralGoogle Scholar
  228. 228.
    Sicari, B. M., J. P. Rubin, C. L. Dearth, M. T. Wolf, F. Ambrosio, M. Boninger, N. J. Turner, D. J. Weber, T. W. Simpson, A. Wyse, E. H. P. Brown, J. L. Dziki, L. E. Fisher, S. Brown, and S. F. Badylak. An acellular biologic scaffold promotes skeletal muscle formation in mice and humans with volumetric muscle loss. Sci. Transl. Med. 6:234ra58, 2014.PubMedPubMedCentralGoogle Scholar
  229. 229.
    Sikin, A. M., and S. S. H. Rizvi. Recent patents on food, nutrition, and agriculture. Preface. Recent. Pat. Food Nutr. Agric 5:1, 2013.Google Scholar
  230. 230.
    Silva, A. C., S. C. Rodrigues, J. Caldeira, A. M. Nunes, V. Sampaio-Pinto, T. P. Resende, M. J. Oliveira, M. A. Barbosa, S. Thorsteinsdóttir, D. S. Nascimento, and P. Pinto-do-Ó. Three-dimensional scaffolds of fetal decellularized hearts exhibit enhanced potential to support cardiac cells in comparison to the adult. Biomaterials 104:52–64, 2016.PubMedGoogle Scholar
  231. 231.
    Simsa, R., A. M. Padma, P. Heher, M. Hellström, A. Teuschl, L. Jenndahl, N. Bergh, and P. Fogelstrand. Systematic in vitro comparison of decellularization protocols for blood vessels. PLoS ONE 13:1–19, 2018.Google Scholar
  232. 232.
    Singelyn, J. M., and J. A. DeQuach. Naturally derived myocardial matrix as an injectable scaffold for cardiac tissue engineering. Biomaterials 30:5409–5416, 2009.PubMedPubMedCentralGoogle Scholar
  233. 233.
    Sinha, P., D. Zurakowski, T. K. S. Kumar, D. He, C. Rossi, and R. A. Jonas. Effects of glutaraldehyde concentration, pretreatment time, and type of tissue (porcine versus bovine) on postimplantation calcification. J. Thorac. Cardiovasc. Surg. 143:224–227, 2012.PubMedGoogle Scholar
  234. 234.
    Slaughter, M. S., K. G. Soucy, R. G. Matheny, B. C. Lewis, M. F. Hennick, Y. Choi, G. Monreal, M. A. Sobieski, G. A. Giridharan, and S. C. Koenig. Development of an extracellular matrix delivery system for effective intramyocardial injection in ischemic tissue. ASAIO J. 60:730–736, 2014.PubMedGoogle Scholar
  235. 235.
    Soler, J. A., S. Gidwani, and M. J. Curtis. Early complications from the use of porcine dermal collagen implants (Permacol ™) as bridging constructs in the repair of massive rotator cuff tears: A report of 4 cases. Acta Orthop. Belg. 73:432–436, 2007.PubMedGoogle Scholar
  236. 236.
    Sonnenschein, C., and A. M. Soto. The society of cells—Cancer and control of cell proliferation. New York: Springer Verlag, pp. 99–133, 1999.Google Scholar
  237. 237.
    Soto, A. M., and C. Sonnenschein. The tissue organization field theory of cancer: A testable replacement for the somatic mutation theory. Bioessays 33:332–340, 2011.PubMedPubMedCentralGoogle Scholar
  238. 238.
    Soucy, K. G., E. F. Smith, G. Monreal, G. Rokosh, B. B. Keller, F. Yuan, R. G. Matheny, A. M. Fallon, B. C. Lewis, L. C. Sherwood, M. A. Sobieski, G. A. Giridharan, S. C. Koenig, and M. S. Slaughter. Feasibility study of particulate extracellular matrix (P-ECM) and left ventricular assist device (HVAD) therapy in chronic ischemic heart failure bovine model. ASAIO J. 61:161–169, 2015.PubMedGoogle Scholar
  239. 239.
    Spang, M. T., and K. L. Christman. Extracellular matrix hydrogel therapies: In vivo applications and development. Acta Biomater. 68:1–14, 2018.PubMedGoogle Scholar
  240. 240.
    Sun, Y., G. Chen, and Y. Lv. Effects of hypoxia on the biological behavior of MSCs seeded in demineralized bone scaffolds with different stiffness. Acta Mech. Sin. Xuebao 35:309–320, 2019.Google Scholar
  241. 241.
    Sun, W. Q., and P. Leung. Calorimetric study of extracellular tissue matrix degradation and instability after gamma irradiation. Acta Biomater. 4:817–826, 2008.PubMedGoogle Scholar
  242. 242.
    Sung, H. W., Y. Chang, C. T. Chiu, C. N. Chen, and H. C. Liang. Crosslinking characteristics and mechanical properties of a bovine pericardium fixed with a naturally occurring crosslinking agent. J. Biomed. Mater. Res. 47:116–126, 1999.PubMedGoogle Scholar
  243. 243.
    Sutherland, A. J., E. C. Beck, S. C. Dennis, G. L. Converse, R. A. Hopkins, C. J. Berkland, and M. S. Detamore. Decellularized cartilage may be a chondroinductive material for osteochondral tissue engineering. PLoS ONE 10:1–13, 2015.Google Scholar
  244. 244.
    Toole, B. P., T. N. Wight, and M. I. Tammi. Hyaluronan-cell interactions in cancer and vascular disease. J. Biol. Chem. 277:4593–4596, 2002.PubMedGoogle Scholar
  245. 245.
    Tottey, S., S. A. Johnson, P. M. Crapo, J. E. Reing, L. Zhang, H. Jiang, C. J. Medberry, B. Reines, and S. F. Badylak. The effect of source animal age upon extracellular matrix scaffold properties. Biomaterials 32:128–136, 2011.PubMedGoogle Scholar
  246. 246.
    Turner, N. J., J. S. Badylak, D. J. Weber, and S. F. Badylak. Biologic scaffold remodeling in a dog model of complex musculoskeletal injury. J. Surg. Res. 176:490–502, 2012.PubMedGoogle Scholar
  247. 247.
    Uriarte, J. J., P. N. Nonaka, N. Campillo, R. K. Palma, E. Melo, L. V. F. de Oliveira, D. Navajas, and R. Farré. Mechanical properties of acellular mouse lungs after sterilization by gamma irradiation. J. Mech. Behav. Biomed. Mater. 40:168–177, 2014.PubMedGoogle Scholar
  248. 248.
    Uriel, S., D. Ph, E. Labay, M. Francis-sedlak, M. L. Moya, R. R. Weichselbaum, N. Ervin, Z. Cankova, E. M. Brey, and D. Ph. Extraction and assembly of tissue-derived gels for cell culture and tissue engineering. Tissue Eng. Part C. Methods 15:309–321, 2009.PubMedGoogle Scholar
  249. 249.
    U.S. Food and Drug Administration. Guidance for industry: Current good tissue practice (CGTP) and additional requirements for manufacturers of human cells, tissues, and cellular and tissue-based products (HCT/Ps)., 2011.Google Scholar
  250. 250.
    U.S. Food and Drug Administration. Medical devices containing materials derived from animal sources (Except for in vitro diagnostic devices): Guidance for industry and Food and Drug Administration staff., 2019.Google Scholar
  251. 251.
    Utomo, L., M. Pleumeekers, L. Nimeskern, S. Nürnberger, K. S. Stok, F. Hildner, and G. J. V. M. Van Osch. Preparation and characterization of a decellularized cartilage scaffold for ear cartilage reconstruction. Biomed. Mater. 10:015010, 2015.PubMedGoogle Scholar
  252. 252.
    Valentin, J. E., J. S. Badylak, G. P. McCabe, and S. F. Badylak. Extracellular matrix bioscaffolds for orthopaedic applications: A comparative histologic study. J. Bone Jt. Surg. 88A:2673–2686, 2006.Google Scholar
  253. 253.
    Valentin, J. E., A. M. Stewart-Akers, T. W. Gilbert, and S. F. Badylak. Macrophage participation in the degradation and remodeling of extracellular matrix scaffolds. Tissue Eng. Part A 15:1687–1694, 2009.PubMedPubMedCentralGoogle Scholar
  254. 254.
    Valentin, J. E., N. J. Turner, T. W. Gilbert, and S. F. Badylak. Functional skeletal muscle formation with a biologic scaffold. Biomaterials 31:7475–7484, 2010.PubMedPubMedCentralGoogle Scholar
  255. 255.
    Van Der Merwe, Y., A. E. Faust, E. T. Sakalli, C. C. Westrick, G. Hussey, I. P. Con, V. L. N. Fu, S. F. Badylak, and M. B. Steketee. Matrix-bound nanovesicles prevent ischemia-induced retinal ganglion cell axon degeneration and death and preserve visual function. Sci. Rep. 9:3482, 2019.PubMedPubMedCentralGoogle Scholar
  256. 256.
    VeDepo, M. C., E. E. Buse, R. W. Quinn, T. D. Williams, M. S. Detamore, R. A. Hopkins, and G. L. Converse. Species-specific effects of aortic valve decellularization. Acta Biomater. 50:249–258, 2017.PubMedGoogle Scholar
  257. 257.
    Visser, J., P. A. Levett, N. C. R. Te Moller, J. Besems, K. W. M. Boere, M. H. P. Van Rijen, J. C. De Grauw, W. J. A. Dhert, P. R. Van Weeren, and J. Malda. Crosslinkable hydrogels derived from cartilage, meniscus, and tendon tissue. Tissue Eng. Part A 21:1195–1206, 2015.PubMedPubMedCentralGoogle Scholar
  258. 258.
    Voytik-Harbin, S. L., A. O. Brightman, B. Z. Waisner, J. P. Robinson, and C. H. Lamar. Small intestinal submucosa: A tissue-derived extracellular matrix that promotes tissue-specific growth and differentiation of cells in vitro. Tissue Eng. 4:157–174, 1998.Google Scholar
  259. 259.
    Walton, J. R., N. K. Bowman, Y. Khatib, J. Linklater, and G. A. C. Murrell. Restore orthobiologic implant: Not recommended for augmentation of rotator cuff repairs. J. Bone Jt. Surg. Ser. A 89:786–791, 2007.Google Scholar
  260. 260.
    Wang, Y., J. Bao, X. Wu, Q. Wu, Y. Li, Y. Zhou, L. Li, and H. Bu. Genipin crosslinking reduced the immunogenicity of xenogeneic decellularized porcine whole-liver matrices through regulation of immune cell proliferation and polarization. Sci. Rep. 6:1–16, 2016.Google Scholar
  261. 261.
    Wang, R. M., and K. L. Christman. Decellularized myocardial matrix hydrogels: In basic research and preclinical studies. Adv. Drug Deliv. Rev. 96:77–82, 2016.PubMedGoogle Scholar
  262. 262.
    Wang, L., J. A. Johnson, D. W. Chang, and Q. Zhang. Decellularized musculofascial extracellular matrix for tissue engineering. Biomaterials 34:2641–2654, 2013.PubMedPubMedCentralGoogle Scholar
  263. 263.
    Wang, R. M., T. D. Johnson, J. He, Z. Rong, M. Wong, V. Nigam, A. Behfar, Y. Xu, and K. L. Christman. Humanized mouse model for assessing the human immune response to xenogeneic and allogeneic decellularized biomaterials. Biomaterials 129:98–110, 2017.PubMedPubMedCentralGoogle Scholar
  264. 264.
    Wang, Z., D. W. Long, Y. Huang, W. C. W. Chen, K. Kim, and Y. Wang. Decellularized neonatal cardiac extracellular matrix prevents widespread ventricular remodeling in adult mammals after myocardial infarction. Acta Biomater. 87:140–151, 2019.PubMedGoogle Scholar
  265. 265.
    Wang, J. K., B. Luo, V. Guneta, L. Li, S. E. M. Foo, Y. Dai, T. T. Y. Tan, N. S. Tan, C. Choong, and M. T. C. Wong. Supercritical carbon dioxide extracted extracellular matrix material from adipose tissue. Mater. Sci. Eng. C 75:349–358, 2017.Google Scholar
  266. 266.
    Wang, Q., C. Zhang, L. Zhang, W. Guo, G. Feng, S. Zhou, Y. Zhang, T. Tian, Z. Li, and F. Huang. The preparation and comparison of decellularized nerve scaffold of tissue engineering. J. Biomed. Mater. Res. A 102:4301–4308, 2014.PubMedGoogle Scholar
  267. 267.
    Wassenaar, J. W., R. L. Braden, K. G. Osborn, and K. L. Christman. Modulating in vivo degradation rate of injectable extracellular matrix hydrogels. J. Mater. Chem. B 4:2794–2802, 2016.PubMedPubMedCentralGoogle Scholar
  268. 268.
    Wassenaar, J. W., R. Gaetani, J. J. Garcia, R. L. Braden, C. G. Luo, D. Huang, A. N. DeMaria, J. H. Omens, and K. L. Christman. Evidence for mechanisms underlying the functional benefits of a myocardial matrix hydrogel for post-MI treatment. J. Am. Coll. Cardiol. 67:1074–1086, 2016.PubMedPubMedCentralGoogle Scholar
  269. 269.
    Wei, H. J., H. C. Liang, M. H. Lee, Y. C. Huang, Y. Chang, and H. W. Sung. Construction of varying porous structures in acellular bovine pericardia as a tissue-engineering extracellular matrix. Biomaterials 26:1905–1913, 2005.PubMedGoogle Scholar
  270. 270.
    West, D. C., D. M. Shaw, P. Lorenz, N. S. Adzick, and M. T. Longaker. Fibrotic healing of adult and late gestation fetal wounds correlates with increased hyaluronidase activity and removal of hyaluronan. Int. J. Biochem. Cell Biol. 29:201–210, 1997.PubMedGoogle Scholar
  271. 271.
    Whitby, D. J., and M. W. J. Ferguson. The extracellular matrix of lip wounds in fetal, neonatal and adult mice. Development 112:651–668, 1991.PubMedGoogle Scholar
  272. 272.
    White, L. J., T. J. Keane, A. Smoulder, L. Zhang, A. A. Castleton, J. E. Reing, N. J. Turner, C. L. Dearth, and S. F. Badylak. The impact of sterilization upon extracellular matrix hydrogel structure and function. J. Immunol. Regen. Med. 2:11–20, 2018.Google Scholar
  273. 273.
    White, L. J., A. J. Taylor, D. M. Faulk, T. J. Keane, L. T. Saldin, J. E. Reing, I. T. Swinehart, N. J. Turner, B. D. Ratner, and S. F. Badylak. The impact of detergents on the tissue decellularization process: A ToF-SIMS study. Acta Biomater. 50:207–219, 2017.PubMedGoogle Scholar
  274. 274.
    Williams, C., K. P. Quinn, I. Georgakoudi, and L. D. Black. Young developmental age cardiac extracellular matrix promotes the expansion of neonatal cardiomyocytes in vitro. Acta Biomater. 10:194–204, 2014.PubMedGoogle Scholar
  275. 275.
    Wolf, M. T., K. A. Daly, E. P. Brennan-Pierce, S. A. Johnson, C. Carruthers, A. D. Amore, S. P. Nagarkar, S. S. Velankar, and S. F. Badylak. A hydrogel derived from decellularized dermal extracellular matrix. Biomaterials 33:7028–7038, 2012.PubMedPubMedCentralGoogle Scholar
  276. 276.
    Wolf, M. T., K. A. Daly, J. E. Reing, and S. F. Badylak. Biologic scaffold composed of skeletal muscle extracellular matrix. Biomaterials 33:2916–2925, 2012.PubMedPubMedCentralGoogle Scholar
  277. 277.
    Wolf, M. T., S. Ganguly, T. L. Wang, C. W. Anderson, K. Sadtler, R. Narain, C. Cherry, A. J. Parrillo, B. V. Park, G. Wang, F. Pan, S. Sukumar, D. M. Pardoll, and J. H. Elisseeff. A biologic scaffold–associated type 2 immune microenvironment inhibits tumor formation and synergizes with checkpoint immunotherapy. Sci. Transl. Med. 11:eaat7973, 2019.PubMedGoogle Scholar
  278. 278.
    Wolf, M. T., Y. Vodovotz, S. Tottey, B. N. Brown, and S. F. Badylak. Predicting in vivo responses to biomaterials via combined in vitro and in silico analysis. Tissue Eng. Part C Methods 21:148–159, 2015.PubMedGoogle Scholar
  279. 279.
    Wood, J. D., A. Simmons-Byrd, A. R. Spievack, and S. F. Badylak. Use of a particulate extracellular matrix bioscaffold for treatment of acquired urinary incontinence in dogs. J. Am. Vet. Med. Assoc. 226:1095–1097, 2005.PubMedGoogle Scholar
  280. 280.
    Yang, Q., J. Peng, Q. Guo, J. Huang, L. Zhang, J. Yao, F. Yang, S. Wang, W. Xu, A. Wang, and S. Lu. A cartilage ECM-derived 3-D porous acellular matrix scaffold for in vivo cartilage tissue engineering with PKH26-labeled chondrogenic bone marrow-derived mesenchymal stem cells. Biomaterials 29:2378–2387, 2008.PubMedGoogle Scholar
  281. 281.
    Yang, G., B. B. Rothrauff, H. Lin, R. Gottardi, P. G. Alexander, and R. S. Tuan. Enhancement of tenogenic differentiation of human adipose stem cells by tendon-derived extracellular matrix. Biomaterials 34:9295–9306, 2013.PubMedPubMedCentralGoogle Scholar
  282. 282.
    Yin, Z., X. Chen, T. Zhu, J. J. Hu, H. X. Song, W. L. Shen, L. Y. Jiang, B. C. Heng, J. F. Ji, and H. W. Ouyang. The effect of decellularized matrices on human tendon stem/progenitor cell differentiation and tendon repair. Acta Biomater. 9:9317–9329, 2013.PubMedGoogle Scholar
  283. 283.
    Young, D. A., V. Bajaj, and K. L. Christman. Decellularized adipose matrix hydrogels stimulate in vivo neovascularization and adipose formation. J. Biomed. Mater. Res. Part A 102:1641–1651, 2014.Google Scholar
  284. 284.
    Young, D. A., Y. S. Choi, A. J. Engler, and K. L. Christman. Stimulation of adipogenesis of adult adipose-derived stem cells using substrates that mimic the stiffness of adipose tissue. Biomaterials 34:8581–8588, 2013.PubMedPubMedCentralGoogle Scholar
  285. 285.
    Young, D. A., K. C. McGilvray, N. Ehrhart, and T. W. Gilbert. Comparison of in vivo remodeling of urinary bladder matrix and acellular dermal matrix in an ovine model. Regen. Med. 13:759–773, 2018.PubMedGoogle Scholar
  286. 286.
    Youngstrom, D. W., I. Rajpar, D. L. Kaplan, and J. G. Barrett. A bioreactor system for in vitro tendon differentiation and tendon tissue engineering. J. Orthop. Res. 33:911–918, 2015.PubMedPubMedCentralGoogle Scholar
  287. 287.
    Zambon, A., M. Vetralla, L. Urbani, M. F. Pantano, G. Ferrentino, M. Pozzobon, N. Pugno, P. De Coppi, N. Elvassore, and S. Spilimbergo. Dry acellular oesophageal matrix prepared by supercritical carbon dioxide. J. Supercrit. Fluids 115:33–41, 2016.Google Scholar
  288. 288.
    Zantop, T., T. W. Gilbert, M. Yoder, and S. F. Badylak. Extracellular matrix scaffolds are repopulated by bone marrow-derived cells in a mouse model of achilles tendon reconstruction. J. Orthop. Res. 24:1299–1309, 2006.PubMedGoogle Scholar
  289. 289.
    Zhang, X., and J. Dong. Direct comparison of different coating matrix on the hepatic differentiation from adipose-derived stem cells. Biochem. Biophys. Res. Commun. 456:938–944, 2015.PubMedGoogle Scholar
  290. 290.
    Zhang, J., B. Li, and J. H.-C. Wang. The role of engineered tendon matrix in the stemness of tendon stem cells in vitro and the promotion of tendon-like tissue formation in vivo. Biomaterials 32:6972–6981, 2011.PubMedPubMedCentralGoogle Scholar
  291. 291.
    Zhao, Z. Q., J. D. Puskas, D. Xu, N. P. Wang, M. Mosunjac, R. A. Guyton, J. Vinten-Johansen, and R. Matheny. Improvement in cardiac function with small intestine extracellular matrix is associated with recruitment of C-kit cells, myofibroblasts, and macrophages after myocardial infarction. J. Am. Coll. Cardiol. 55:1250–1261, 2010.PubMedGoogle Scholar
  292. 292.
    Zhou, Q., X. Ye, R. Sun, Y. Matsumoto, M. Moriyama, Y. Asano, Y. Ajioka, and Y. Sauo. Differentiation of mouse induced pluripotent stem cells into alveolar epithelial cells in vitro for use in vivo. Stem Cells Transl. Med. 3:675–685, 2014.PubMedPubMedCentralGoogle Scholar
  293. 293.
    Zhu, T., Q. Tang, Y. Shen, H. Tang, L. Chen, and J. Zhu. An acellular cerebellar biological scaffold: Preparation, characterization, biocompatibility and effects on neural stem cells. Brain Res. Bull. 113:48–57, 2015.PubMedGoogle Scholar
  294. 294.
    Zuo, H., D. Peng, B. Zheng, X. Liu, Y. Wang, L. Wang, X. Zhou, and J. Liu. Regeneration of mature dermis by transplanted particulate acellular dermal matrix in a rat model of skin defect wound. J. Mater. Sci. Mater. Med. 23:2933–2944, 2012.PubMedPubMedCentralGoogle Scholar

Copyright information

© Biomedical Engineering Society 2019

Authors and Affiliations

  1. 1.McGowan Institute for Regenerative MedicineUniversity of PittsburghPittsburghUSA
  2. 2.Department of BioengineeringUniversity of PittsburghPittsburghUSA
  3. 3.Department of SurgeryUniversity of PittsburghPittsburghUSA

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