Cartilage repair and subchondral bone remodeling in response to focal lesions in a mini-pig model: Implications for tissue engineering

Tissue Engineering - Part A

Volumn 21, Issue 3-4, 2015, Pages 850-860

  Fisher, Matthew B ^a,b   Belkin, Nicole S ^a,b   Milby, Andrew H ^a,b   Henning, Elizabeth A ^a,b   Bostrom, Marc ^a,b   Kim, Minwook ^a,b   Pfeifer, Christian ^a,b   Meloni, Gregory ^a,b   Dodge, George R ^a,b   Burdick, Jason A ^b,c   Schaer, Thomas P ^d   Steinberg, David R ^a,b   Mauck, Robert L ^a,b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARTILAGE; COLLAGEN; COMPUTERIZED TOMOGRAPHY; DEFECTS; HYALURONIC ACID; MAMMALS; SURGERY; TISSUE; TISSUE ENGINEERING;

BIOLOGICAL PHENOMENA; HISTOLOGICAL SCORING SYSTEMS; HYALURONIC ACID HYDROGELS; IMMUNOHISTOCHEMISTRY; LOAD TRANSMISSION; MECHANICAL LOADING; MICROCOMPUTED TOMOGRAPHY; YUCATAN MINI-PIGS;

REPAIR;

COLLAGEN TYPE 2; PROTEOGLYCAN;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DEFECT; BONE REMODELING; BONE STRENGTH; CARTILAGE INJURY; CARTILAGE TRANSPLANTATION; CELL COMPOSITION; CELL ELONGATION; CELL SHAPE; CELL STRUCTURE; CELL SURFACE; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOARCHITECTURE; FINITE ELEMENT ANALYSIS; FULL THICKNESS DEFECT; IN VIVO STUDY; MALE; MICRO-COMPUTED TOMOGRAPHY; MICROFRACTURE; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; PARTIAL THICKNESS DEFECT; POSTOPERATIVE COMPLICATION; POSTOPERATIVE HEMORRHAGE; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; SCORING SYSTEM; SURFACE PROPERTY; THICKNESS; TISSUE ENGINEERING; YUCATAN MICROPIG; ANIMAL; CARTILAGE; FRACTURE HEALING; FRACTURES, CARTILAGE; MINIPIG; PHYSIOLOGY; PIG; PROCEDURES; RADIOGRAPHY; TISSUE SCAFFOLD; TRANSPLANTATION; TREATMENT OUTCOME;

ANIMALIA; SUIDAE;

ANIMALS; BONE REMODELING; CARTILAGE; FRACTURE HEALING; FRACTURES, CARTILAGE; SWINE; SWINE, MINIATURE; TISSUE ENGINEERING; TISSUE SCAFFOLDS; TREATMENT OUTCOME;

EID: 84923280301     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2014.0384     Document Type: Article

References (54)

1. Widuchowski, W., Widuchowski, J., and Trzaska, T. Articular cartilage defects: Study of 25, 124 knee arthroscopies. Knee 14, 177, 2007.
2. Curl, W.W., Krome, J., Gordon, E.S., Rushing, J., Smith, B.P., and Poehling, G.G. Cartilage injuries: a review of 31, 516 knee arthroscopies. Arthroscopy 13, 456, 1997.
3. Heir, S., Nerhus, T.K., Rotterud, J.H., Loken, S., Ekeland, A., Engebretsen, L., and Aroen, A. Focal cartilage defects in the knee impair quality of life as much as severe osteoarthritis: a comparison of knee injury and osteoarthritis outcome score in 4 patient categories scheduled for knee surgery. Am J Sports Med 38, 231, 2010.
4. Guettler, J.H., Demetropoulos, C.K., Yang, K.H., and Jurist, K.A. Osteochondral defects in the human knee: influ-ence of defect size on cartilage rim stress and load redistribution to surrounding cartilage. Am J Sports Med 32, 1451, 2004.
5. Wang, Y., Ding, C., Wluka, A.E., Davis, S., Ebeling, P.R., Jones, G., and Cicuttini, F.M. Factors affecting progression of knee cartilage defects in normal subjects over 2 years. Rheumatology (Oxford) 45, 79, 2006.
6. Brittberg, M. Cell carriers as the next generation of cell therapy for cartilage repair: a review of the matrix-induced autologous chondrocyte implantation procedure. Am J Sports Med 38, 1259, 2010.
7. Alford, J.W., and Cole, B.J. Cartilage restoration, part 1: basic science, historical perspective, patient evaluation, and treatment options. Am J Sports Med 33, 295, 2005.
8. Steadman, J.R., Rodkey, W.G., and Briggs, K.K. Microfracture to treat full-Thickness chondral defects: surgical technique, rehabilitation, and outcomes. J Knee Surg 15, 170, 2002.
9. Steadman, J.R., Rodkey, W.G., and Rodrigo, J.J. Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin Orthop Relat Res (391 Suppl), S362, 2001.
10. Hangody, L., Kish, G., Karpati, Z., Szerb, I., and Udvarhelyi, I. Arthroscopic autogenous osteochondral mosaicplasty for the treatment of femoral condylar articular defects. A preliminary report. Knee Surg Sports Traumatol Arthrosc 5, 262, 1997.
11. Baumbach, K., Petersen, J.P., Ueblacker, P., Schroder, J., Gopfert, C., Stork, A., Rueger, J.M., Amling, M., and Meenen, N.M. The fate of osteochondral grafts after autologous osteochondral transplantation: a one-year followup study in a minipig model. Arch Orthop Trauma Surg 128, 1255, 2008.
12. Bartlett, W., Skinner, J.A., Gooding, C.R., Carrington, R.W., Flanagan, A.M., Briggs, T.W., and Bentley, G. Autologous chondrocyte implantation versus matrix-induced autologous chondrocyte implantation for osteochondral defects of the knee: a prospective, randomised study. J Bone Joint Surg Br 87, 640, 2005.
13. Obradovic, B., Martin, I., Padera, R.F., Treppo, S., Freed, L.E., and Vunjak-Novakovic, G. Integration of engineered cartilage. J Orthop Res 19, 1089, 2001.
14. Erickson, I.E., Kestle, S.R., Zellars, K.H., Farrell, M.J., Kim, M., Burdick, J.A., and Mauck, R.L. High mesenchymal stem cell seeding densities in hyaluronic acid hydrogels produce engineered cartilage with native tissue properties. Acta Biomater 8, 3027, 2012.
15. Ng, K.W., O'Conor, C.J., Kugler, L.E., Cook, J.L., Ateshian, G.A., and Hung, C.T. Transient supplementation of anabolic growth factors rapidly stimulates matrix synthesis in engineered cartilage. Ann Biomed Eng 39, 2491, 2011.
16. Cheng, N.C., Estes, B.T., Awad, H.A., and Guilak, F. 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, 2009.
17. Vinardell, T., Sheehy, E.J., Buckley, C.T., and Kelly, D.J. A comparison of the functionality and in vivo phenotypic stability of cartilaginous tissues engineered from different stem cell sources. Tissue Eng Part A 18, 1161, 2012.
18. Lima, E.G., Bian, L., Ng, K.W., Mauck, R.L., Byers, B.A., Tuan, R.S., Ateshian, G.A., and Hung, C.T. The beneficial effect of delayed compressive loading on tissue-engineered cartilage constructs cultured with tgf-beta3. Osteoarthritis Cartilage 15, 1025, 2007.
19. Erickson, I.E., Kestle, S.R., Zellars, K.H., Dodge, G.R., Burdick, J.A., and Mauck, R.L. Improved cartilage repair via in vitro pre-maturation of msc-seeded hyaluronic acid hydrogels. Biomed Mater 7, 024110, 2012.
20. Burdick, J.A., Chung, C., Jia, X.Q., Randolph, M.A., and Langer, R. Controlled degradation and mechanical behavior of photopolymerized hyaluronic acid networks. Biomacromolecules 6, 386, 2005.
21. Fisher, M.B., Henning, E.A., Soegaard, N.B., Dodge, G.R., Steinberg, D.R., and Mauck, R.L. Maximizing cartilage formation and integration via a trajectory-based tissue engineering approach. Biomaterials 35, 2140, 2014.
22. Erickson, I.E., Huang, A.H., Chung, C., Li, R.T., Burdick, J.A., and Mauck, R.L. Differential maturation and structurefunction relationships in mesenchymal stem cell- And chondrocyte-seeded hydrogels. Tissue Eng Part A 15, 1041, 2009.
23. Chu, C.R., Szczodry, M. and Bruno, S. Animal models for cartilage regeneration and repair. Tissue Eng Part B Rev 16, 105, 2010.
24. Ahern, B.J., Parvizi, J., Boston, R., and Schaer, T.P. Preclinical animal models in single site cartilage defect testing: a systematic review. Osteoarthritis Cartilage 17, 705, 2009.
25. Chawla, K., Klein, T.J., Schumacher, B.L., Jadin, K.D., Shah, B.H., Nakagawa, K., Wong, V.W., Chen, A.C., Masuda, K., and Sah, R.L. Short-Term retention of labeled chondrocyte subpopulations in stratified tissue-engineered cartilaginous constructs implanted in vivo in mini-pigs. Tissue Eng 13, 1525, 2007.
26. Gotterbarm, T., Breusch, S.J., Schneider, U., and Jung, M. The minipig model for experimental chondral and osteochondral defect repair in tissue engineering: retrospective analysis of 180 defects. Lab Anim 42, 71, 2008.
27. Dorotka, R., Windberger, U., Macfelda, K., Bindreiter, U., Toma, C., and Nehrer, S. Repair of articular cartilage defects treated by microfracture and a three-dimensional collagen matrix. Biomaterials 26, 3617, 2005.
28. Frisbie, D.D., Oxford, J.T., Southwood, L., Trotter, G.W., Rodkey, W.G., Steadman, J.R., Goodnight, J.L., and McIlwraith, C.W. Early events in cartilage repair after subchondral bone microfracture. Clin Orthop Relat Res 215, 2003.
29. Lane, J.G., Healey, R.M., Chen, A.C., Sah, R.L., and Amiel, D. Can osteochondral grafting be augmented with microfracture in an extended-size lesion of articular cartilage?. Am J Sports Med 38, 1316, 2010.
30. Vasara, A.I., Hyttinen, M.M., Pulliainen, O., Lammi, M.J., Jurvelin, J.S., Peterson, L., Lindahl, A., Helminen, H.J., and Kiviranta, I. Immature porcine knee cartilage lesions show good healing with or without autologous chondrocyte transplantation. Osteoarthritis Cartilage 14, 1066, 2006.
31. Li, W.J., Chiang, H., Kuo, T.F., Lee, H.S., Jiang, C.C., and Tuan, R.S. Evaluation of articular cartilage repair using biodegradable nanofibrous scaffolds in a swine model: a pilot study. J Tissue Eng Regen Med 3, 1, 2009.
32. Liu, Y., Chen, F., Liu, W., Cui, L., Shang, Q., Xia, W., Wang, J., Cui, Y., Yang, G., Liu, D., Wu, J., Xu, R., Buonocore, S.D., and Cao, Y. Repairing large porcine fullthickness defects of articular cartilage using autologous chondrocyte-engineered cartilage. Tissue Eng 8, 709, 2002.
33. Vasara, A.I., Hyttinen, M.M., Lammi, M.J., Lammi, P.E., Langsjo, T.K., Lindahl, A., Peterson, L., Kellomaki, M., Konttinen, Y.T., Helminen, H.J., and Kiviranta, I. Subchondral bone reaction associated with chondral defect and attempted cartilage repair in goats. Calcif Tissue Int 74, 107, 2004.
34. Orth, P., Goebel, L., Wolfram, U., Ong, M.F., Graber, S., Kohn, D., Cucchiarini, M., Ignatius, A., Pape, D., and Madry, H. Effect of subchondral drilling on the microarchitecture of subchondral bone: analysis in a large animal model at 6 months. Am J Sports Med 40, 828, 2012.
35. Goulet, R.W., Goldstein, S.A., Ciarelli, M.J., Kuhn, J.L., Brown, M.B., and Feldkamp, L.A. The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech 27, 375, 1994.
36. Xie, L., Lin, A.S., Levenston, M.E., and Guldberg, R.E. Quantitative assessment of articular cartilage morphology via epic-microct. Osteoarthritis Cartilage 17, 313, 2009.
37. Mainil-Varlet, P., Van Damme, B., Nesic, D., Knutsen, G., Kandel, R., and Roberts, S. A new histology scoring system for the assessment of the quality of human cartilage repair: ICRS II. Am J Sports Med 38, 880, 2010.
38. Maas, S.A., Ellis, B.J., Ateshian, G.A., and Weiss, J.A. Febio: finite elements for biomechanics. J Biomech Eng 134, 011005, 2012.
39. Ateshian, G.A., Rajan, V., Chahine, N.O., Canal, C.E., and Hung, C.T. Modeling the matrix of articular cartilage using a continuous fiber angular distribution predicts many observed phenomena. J Biomech Eng 131, 061003, 2009.
40. Huang, C.Y., Soltz, M.A., Kopacz, M., Mow, V.C., and Ateshian, G.A. Experimental verification of the roles of intrinsic matrix viscoelasticity and tension-compression nonlinearity in the biphasic response of cartilage. J Biomech Eng 125, 84, 2003.
41. Erickson, I.E., Huang, A.H., Sengupta, S., Kestle, S., Burdick, J.A., and Mauck, R.L. Macromer density influences mesenchymal stem cell chondrogenesis and maturation in photocrosslinked hyaluronic acid hydrogels. Osteoarthritis Cartilage 17, 1639, 2009.
42. Pei, M., He, F., Li, J., Tidwell, J.E., Jones, A.C., and McDonough, E.B. Repair of large animal partial-Thickness cartilage defects through intraarticular injection of matrixrejuvenated synovium-derived stem cells. Tissue Eng Part A 19, 1144, 2013.
43. Mainil-Varlet, P., Rieser, F., Grogan, S., Mueller, W., Saager, C., and Jakob, R.P. Articular cartilage repair using a tissue-engineered cartilage-like implant: an animal study. Osteoarthritis Cartilage 9 Suppl A, S6, 2001.
44. Orth, P., Cucchiarini, M., Kohn, D., and Madry, H. Alterations of the subchondral bone in osteochondral repair- Translational data and clinical evidence. Eur Cell Mater 25, 299; discussion 314, 2013.
45. Chiang, H., Kuo, T.F., Tsai, C.C., Lin, M.C., She, B.R., Huang, Y.Y., Lee, H.S., Shieh, C.S., Chen, M.H., Ramshaw, J.A., Werkmeister, J.A., Tuan, R.S., and Jiang, C.C. Repair of porcine articular cartilage defect with autologous chondrocyte transplantation. J Orthop Res 23, 584, 2005.
46. Pallante, A.L., Chen, A.C., Ball, S.T., Amiel, D., Masuda, K., Sah, R.L., and Bugbee, W.D. The in vivo performance of osteochondral allografts in the goat is diminished with extended storage and decreased cartilage cellularity. Am J Sports Med 40, 1814, 2012.
47. Horas, U., Pelinkovic, D., Herr, G., Aigner, T., and Schnettler, R. Autologous chondrocyte implantation and osteochondral cylinder transplantation in cartilage repair of the knee joint. A prospective, comparative trial. J Bone Joint Surg Am 85-A, 185, 2003.
48. Lane, J.G., Massie, J.B., Ball, S.T., Amiel, M.E., Chen, A.C., Bae, W.C., Sah, R.L., and Amiel, D. Follow-up of osteochondral plug transfers in a goat model: a 6-month study. Am J Sports Med 32, 1440, 2004.
49. Mankin, H.J. The response of articular cartilage to mechanical injury. J Bone Joint Surg Am. 64, 460, 1982.
50. Insall, J. The pridie debridement operation for osteoarthritis of the knee. Clin Orthop Relat Res 61, 1974.
51. Pallante-Kichura, A.L., Cory, E., Bugbee, W.D., and Sah, R.L. Bone cysts after osteochondral allograft repair of cartilage defects in goats suggest abnormal interaction between subchondral bone and overlying synovial joint tissues. Bone 57, 259, 2013.
52. Hoemann, C.D., Hurtig, M., Rossomacha, E., Sun, J., Chevrier, A., Shive, M.S., and Buschmann, M.D. Chitosanglycerol phosphate/blood implants improve hyaline cartilage repair in ovine microfracture defects. J Bone Joint Surg Am 87, 2671, 2005.
53. Sharma, B., Fermanian, S., Gibson, M., Unterman, S., Herzka, D. A., Cascio, B., Coburn, J., Hui, A.Y., Marcus, N., Gold, G.E., and Elisseeff, J.H. Human cartilage repair with a photoreactive adhesive-hydrogel composite. Sci Transl Med 5, 167ra166, 2013.
54. Bian, L., Zhai, D.Y., Tous, E., Rai, R., Mauck, R.L., and Burdick, J.A. Enhanced msc chondrogenesis following delivery of tgf-beta3 from alginate microspheres within hyaluronic acid hydrogels in vitro and in vivo. Biomaterials 32, 6425, 2011.