Report on a large animal study with Göttingen Minipigs where regenerates and controls for articular cartilage were created in a large number. Focus on the conditions of the operated stifle joints and suggestions for standardized procedures
Autoři:
Markus L. Schwarz aff001; Gregor Reisig aff001; Andy Schütte aff001; Kristianna Becker aff002; Susanne Serba aff002; Elmar Forsch aff003; Steffen Thier aff001; Stefan Fickert aff001; Tamara Lenz aff006; Christel Weiß aff007; Svetlana Hetjens aff007; Frederic Bludau aff001; Friederike Bothe aff008; Wiltrud Richter aff008; Barbara Schneider-Wald aff001
Působiště autorů:
Section for experimental Orthopaedics and Trauma Surgery, Orthopaedic and Trauma Surgery Centre (OUZ), Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
aff001; Interfaculty Biomedical Facility, Heidelberg University, Heidelberg, Germany
aff002; Department of Experimental Pain Research, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
aff003; Sportchirurgie Heidelberg, Klonz—Thier–Stock, ATOS Klinik Heidelberg, Heidelberg, Germany
aff004; Sporthopaedicum Regensburg/Straubing, Straubing, Germany
aff005; Statistical Consulting, Mannheim, Germany
aff006; Department of Medical Statistics, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
aff007; Research Centre for Experimental Orthopaedics, Heidelberg University Hospital, Heidelberg, Germany
aff008
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224996
Souhrn
The characterization of regenerated articular cartilage (AC) can be based on various methods, as there is an unambiguous accepted criterion neither for the natural cartilage tissue nor for regenerates. Biomechanical aspects should be considered as well, leading to the need for more equivalent samples. The aim of the study was to describe a large animal model where 8 specimens of regenerated AC can be created in one animal plus the impact of two surgeries on the welfare of the animals. The usefulness of the inclusion of a group of untreated animals (NAT) was to analyzed. Based on the histological results the conditions of the regenerates were to be described and the impact on knee joints were to be explored in terms of degenerative changes of the cartilage. The usefulness of the statistical term “effect size” (ES) will be explained with histological results. We analyzed an animal model where 8 AC regenerates were obtained from one Göttingen Minipig, on both sides of the trochleae. 60 animals were divided into 6 groups of 10 each, where the partial thickness defects in the trochlea were filled with matrices made of Collagen I with or without autologous chondrocytes or left empty over the healing periods of 24 and 48 weeks. One additional control group consisting of 10 untreated animals was used to provide untouched “external” cartilage. We harvested 560 samples of regenerated tissue and “external” controls, besides that, twice the number of further samples from other parts of the joints referred to as “internal” controls were also harvested. The animals recovered faster after the 1st operation when the defects were set compared to the 2nd operation when the defects were treated. 9% of all animals were lost. Other complications were for example superficial infections, seroma, diarrhea, febrile state and an injury of a claw. The histological results of the treatments proved the robustness of the study design where we included an “external” control group (NAT) in which the animals were not operated. Comparable significant differences between treated groups and the NAT group were detected both after ½ year and after 1 year. Spontaneous regenerated AC as control revealed differences after an observation time of nearly 1 year. The impact of the treatment on cartilage adjacent to the defect as well as the remaining knee joint was low. The ES was helpful for planning the study as it is shown that the power of a statistical comparison seems to be more influenced by the ES than by the sample size. The ranking of the ES was done exemplarily, listing the results according to their magnitude, thus making the results comparable. We were able to follow the 3 R requirements also in terms of a numerical reduction of animals due to the introduction of a group of untreated animals. This makes the model cost effective. The presented study may contribute as an improvement of the standardization of large animal models for research and regulatory requirements for regenerative therapies of AC.
Klíčová slova:
Surgical and invasive medical procedures – Skeletal joints – Cartilage – Knee joints – Histology – Swine – Chondrocytes – Articular cartilage
Zdroje
1. Niemeyer P, Albrecht D, Andereya S, Angele P, Ateschrang A, Aurich M, et al. Autologous chondrocyte implantation (ACI) for cartilage defects of the knee: A guideline by the working group "Clinical Tissue Regeneration" of the German Society of Orthopaedics and Trauma (DGOU). The Knee. 2016;23(3):426–35. doi: 10.1016/j.knee.2016.02.001 26947215.
2. Rodriguez-Merchan EC. Regeneration of articular cartilage of the knee. Rheumatology international. 2013;33(4):837–45. doi: 10.1007/s00296-012-2601-3 23263546.
3. Roessler PP, Pfister B, Gesslein M, Figiel J, Heyse TJ, Colcuc C, et al. Short-term follow up after implantation of a cell-free collagen type I matrix for the treatment of large cartilage defects of the knee. International orthopaedics. 2015;39(12):2473–9. doi: 10.1007/s00264-015-2695-9 25676840.
4. Williams RJ, Gamradt SC. Articular cartilage repair using a resorbable matrix scaffold. Instructional course lectures. 2008;57:563–71. 18399610.
5. Anz AW, Bapat A, Murrell WD. Concepts in regenerative medicine: Past, present, and future in articular cartilage treatment. Journal of clinical orthopaedics and trauma. 2016;7(3):137–44. doi: 10.1016/j.jcot.2016.05.006 27489407; PubMed Central PMCID: PMC4949414.
6. Boushell MK, Hung CT, Hunziker EB, Strauss EJ, Lu HH. Current strategies for integrative cartilage repair. Connective tissue research. 2017;58(5):393–406. doi: 10.1080/03008207.2016.1231180 27599801.
7. Correa D, Lietman SA. Articular cartilage repair: Current needs, methods and research directions. Seminars in cell & developmental biology. 2016;62:67–77. doi: 10.1016/j.semcdb.2016.07.013 27422331.
8. LaPrade RF, Dragoo JL, Koh JL, Murray IR, Geeslin AG, Chu CR. AAOS Research Symposium Updates and Consensus: Biologic Treatment of Orthopaedic Injuries. The Journal of the American Academy of Orthopaedic Surgeons. 2016;24(7):e62–78. doi: 10.5435/JAAOS-D-16-00086 27227987.
9. Schneider-Wald B, von Thaden AK, Schwarz ML. [Defect models for the regeneration of articular cartilage in large animals]. Der Orthopade. 2013;42(4):242–53. doi: 10.1007/s00132-012-2044-2 23575559.
10. Swindle MM, Smith AC. Best practices for performing experimental surgery in swine. Journal of investigative surgery: the official journal of the Academy of Surgical Research. 2013;26(2):63–71. doi: 10.3109/08941939.2012.693149 23281597.
11. Hurschler C, Abedian R. [Possibilities for the biomechanical characterization of cartilage: a brief update]. Der Orthopade. 2013;42(4):232–41. doi: 10.1007/s00132-013-2074-4 23575558.
12. Griffin DJ BE, Lachowsky DJ, Hart JC, Sparks HD, Moran N, Matthews G, Nixon AJ, Cohen I, Bonassar LJ. Mechanical characterization of matrix-induced autologous chondrocyte implantation (MACI®) grafts in an equine model at 53 weeks. Journal of biomechanics. 2015;48(10):6. doi: 10.1016/j.jbiomech.2015.04.010 25920896
13. Kim IL, Pfeifer CG, Fisher MB, Saxena V, Meloni GR, Kwon MY, et al. Fibrous Scaffolds with Varied Fiber Chemistry and Growth Factor Delivery Promote Repair in a Porcine Cartilage Defect Model. Tissue engineering Part A. 2015;21(21–22):2680–90. doi: 10.1089/ten.tea.2015.0150 26401910; PubMed Central PMCID: PMC4652183.
14. Gotterbarm T, Breusch SJ, Schneider U, Jung M. The minipig model for experimental chondral and osteochondral defect repair in tissue engineering: retrospective analysis of 180 defects. Laboratory animals. 2008;42(1):71–82. doi: 10.1258/la.2007.06029e 18348768.
15. Blanke M, Carl HD, Klinger P, Swoboda B, Hennig F, Gelse K. Transplanted chondrocytes inhibit endochondral ossification within cartilage repair tissue. Calcified tissue international. 2009;85(5):421–33. doi: 10.1007/s00223-009-9288-9 19763370.
16. Mainil-Varlet P, Rieser F, Grogan S, Mueller W, Saager C, Jakob RP. Articular cartilage repair using a tissue-engineered cartilage-like implant: an animal study. Osteoarthritis and cartilage. 2001;9 Suppl A:S6–15. doi: 10.1053/joca.2001.0438 11680690.
17. Schwarz ML, Schneider-Wald B, Brade J, Schleich D, Schutte A, Reisig G. Instruments for reproducible setting of defects in cartilage and harvesting of osteochondral plugs for standardisation of preclinical tests for articular cartilage regeneration. Journal of orthopaedic surgery and research. 2015;10:117. doi: 10.1186/s13018-015-0257-x 26215154; PubMed Central PMCID: PMC4517650.
18. Schinhan M, Gruber M, Vavken P, Dorotka R, Samouh L, Chiari C, et al. Critical-size defect induces unicompartmental osteoarthritis in a stable ovine knee. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 2012;30(2):214–20. Epub 2011/08/06. doi: 10.1002/jor.21521 21818770.
19. Strauss EJ, Goodrich LR, Chen CT, Hidaka C, Nixon AJ. Biochemical and biomechanical properties of lesion and adjacent articular cartilage after chondral defect repair in an equine model. The American journal of sports medicine. 2005;33(11):1647–53. doi: 10.1177/0363546505275487 16093540.
20. Heard BJ, Achari Y, Chung M, Shrive NG, Frank CB. Early joint tissue changes are highly correlated with a set of inflammatory and degradative synovial biomarkers after ACL autograft and its sham surgery in an ovine model. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 2011;29(8):1185–92. doi: 10.1002/jor.21404 21387397.
21. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. Osteoarthritis and cartilage. 2012;20(4):256–60. doi: 10.1016/j.joca.2012.02.010 22424462.
22. National_Research_Council. Guide for the care and use of laboratory animals (8th edition). Washington, DC: 2011.
23. Russell WMS, Burch RL. The Principles of Humane Experimental Technique (Special Edition; Reprint from 1959). Wheathampstead, Hertfordshire, UK: Universities Federation for Animal Welfare; 1992.
24. Tannenbaum J, Bennett BT. Russell and Burch's 3Rs then and now: the need for clarity in definition and purpose. Journal of the American Association for Laboratory Animal Science: JAALAS. 2015;54(2):120–32. 25836957; PubMed Central PMCID: PMC4382615.
25. Cohen J. Statistical power analysis for the behavioral sciences (2nd edition). Hillsdale NJ: Lawrence Erlbaum associates; 1988.
26. Cohen J. A power primer. Psychological bulletin. 1992;112(1):155–9. doi: 10.1037//0033-2909.112.1.155 19565683.
27. Christensen BB. Autologous tissue transplantations for osteochondral repair. Danish medical journal. 2016;63(4). Epub 2016/04/02. 27034191.
28. Allen MJ, Houlton JE, Adams SB, Rushton N. The surgical anatomy of the stifle joint in sheep. Veterinary surgery: VS. 1998;27(6):596–605. doi: 10.1111/j.1532-950x.1998.tb00536.x 9845224.
29. Parvizi J, Shohat N, Gehrke T. Prevention of periprosthetic joint infection: new guidelines. Bone Joint J. 2017;99-B(4 Supple B):3–10. doi: 10.1302/0301-620X.99B4.BJJ-2016-1212.R1 28363888.
30. Caminal M, Fonseca C, Peris D, Moll X, Rabanal RM, Barrachina J, et al. Use of a chronic model of articular cartilage and meniscal injury for the assessment of long-term effects after autologous mesenchymal stromal cell treatment in sheep. New biotechnology. 2014;31(5):492–8. doi: 10.1016/j.nbt.2014.07.004 25063342.
31. Sharma A, Swan KG. Franz Weitlaner: the great spreader of surgery. The Journal of trauma. 2009;67(6):1431–4. doi: 10.1097/TA.0b013e3181b2fe3e 20009698.
32. Redman SN, Oldfield SF, Archer CW. Current strategies for articular cartilage repair. European cells & materials. 2005;9:23–32; discussion 23–32. doi: 10.22203/ecm.v009a04 15830323.
33. Schneider U, Schmidt-Rohlfing B, Gavenis K, Maus U, Mueller-Rath R, Andereya S. A comparative study of 3 different cartilage repair techniques. Knee surgery, sports traumatology, arthroscopy: official journal of the ESSKA. 2011;19(12):2145–52. doi: 10.1007/s00167-011-1460-x 21409471.
34. O'Driscoll SW, Keeley FW, Salter RB. The chondrogenic potential of free autogenous periosteal grafts for biological resurfacing of major full-thickness defects in joint surfaces under the influence of continuous passive motion. An experimental investigation in the rabbit. The Journal of bone and joint surgery American volume. 1986;68(7):1017–35. 3745239.
35. Little CB, Smith MM, Cake MA, Read RA, Murphy MJ, Barry FP. The OARSI histopathology initiative—recommendations for histological assessments of osteoarthritis in sheep and goats. Osteoarthritis and cartilage. 2010;18 Suppl 3:S80–92. doi: 10.1016/j.joca.2010.04.016 20864026.
36. Häuselmann HJ, Masuda K, Hunziker EB, Neidhart M, Mok SS, Michel BA, et al. Adult human chondrocytes cultured in alginate form a matrix similar to native human articular cartilage. The American journal of physiology. 1996;271(3 Pt 1):C742–52. doi: 10.1152/ajpcell.1996.271.3.C742 8843703.
37. Kellgren JH, Lawrence JS. Radiological assessment of osteo-arthrosis. Annals of the rheumatic diseases. 1957;16(4):494–502. doi: 10.1136/ard.16.4.494 13498604; PubMed Central PMCID: PMC1006995.
38. Cook JL, Kuroki K, Visco D, Pelletier JP, Schulz L, Lafeber FP. The OARSI histopathology initiative—recommendations for histological assessments of osteoarthritis in the dog. Osteoarthritis and cartilage. 2010;18 Suppl 3:S66–79. doi: 10.1016/j.joca.2010.04.017 20864024.
39. O'Driscoll SW KF, Salter RB. Durability of regenerated articular cartilage produced by free autogenous periosteal grafts in major full-thickness defects in joint surfaces under the influence of continuous passive motion. A follow-up report at one year. The Journal of bone and joint surgery American volume. 1988;70(4):12.
40. Mangram AJ, Horan TC, Pearson ML, Silver LC, Jarvis WR. Guideline for Prevention of Surgical Site Infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. American journal of infection control. 1999;27(2):97–132; quiz 3–4; discussion 96. 10196487.
41. Sosio C, Di Giancamillo A, Deponti D, Gervaso F, Scalera F, Melato M, et al. Osteochondral repair by a novel interconnecting collagen-hydroxyapatite substitute: a large-animal study. Tissue engineering Part A. 2015;21(3–4):704–15. doi: 10.1089/ten.TEA.2014.0129 25316498.
42. Jung M, Breusch S, Daecke W, Gotterbarm T. The effect of defect localization on spontaneous repair of osteochondral defects in a Gottingen minipig model: a retrospective analysis of the medial patellar groove versus the medial femoral condyle. Laboratory animals. 2009;43(2):191–7. doi: 10.1258/la.2008.007149 19116289.
43. Wang CJ, Chen CY, Tsung SM, Chen WJ, Huang HY. Cartilage repair by free periosteal grafts in the knees of pigs: a histologic study. Journal of the Formosan Medical Association = Taiwan yi zhi. 2000;99(4):324–9. 10870317.
44. Kääb MJ, Gwynn IA, Notzli HP. Collagen fibre arrangement in the tibial plateau articular cartilage of man and other mammalian species. Journal of anatomy. 1998;193 (Pt 1):23–34. doi: 10.1046/j.1469-7580.1998.19310023.x 9758134; PubMed Central PMCID: PMC1467820.
45. Xerogeanes JW, Fox RJ, Takeda Y, Kim HS, Ishibashi Y, Carlin GJ, et al. A functional comparison of animal anterior cruciate ligament models to the human anterior cruciate ligament. Annals of biomedical engineering. 1998;26(3):345–52. doi: 10.1114/1.91 9570217.
46. Taylor WR, Ehrig RM, Heller MO, Schell H, Seebeck P, Duda GN. Tibio-femoral joint contact forces in sheep. Journal of biomechanics. 2006;39(5):791–8. doi: 10.1016/j.jbiomech.2005.02.006 16488218.
47. Sumner DR, Turner TM, Urban RM, Turek T, Seeherman H, Wozney JM. Locally delivered rhBMP-2 enhances bone ingrowth and gap healing in a canine model. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 2004;22(1):58–65. doi: 10.1016/S0736-0266(03)00127-X 14656660.
48. Fisher MB, Belkin NS, Milby AH, Henning EA, Bostrom M, Kim M, et al. Cartilage repair and subchondral bone remodeling in response to focal lesions in a mini-pig model: implications for tissue engineering. Tissue engineering Part A. 2015;21(3–4):850–60. doi: 10.1089/ten.TEA.2014.0384 25318414; PubMed Central PMCID: PMC4333259.
49. Schwarz ML, Schneider-Wald B, Krase A, Richter W, Reisig G, Kreinest M, et al. [Tribological assessment of articular cartilage. A system for the analysis of the friction coefficient of cartilage, regenerates and tissue engineering constructs; initial results]. Der Orthopade. 2012;41(10):827–36. doi: 10.1007/s00132-012-1951-6 23052849.
50. Stoffel M, Yi JH, Weichert D, Zhou B, Nebelung S, Muller-Rath R, et al. Bioreactor cultivation and remodelling simulation for cartilage replacement material. Medical engineering & physics. 2012;34(1):56–63. doi: 10.1016/j.medengphy.2011.06.018 21784691.
51. Hunziker EB, Rosenberg LC. Repair of partial-thickness defects in articular cartilage: cell recruitment from the synovial membrane. The Journal of bone and joint surgery American volume. 1996;78(5):721–33. doi: 10.2106/00004623-199605000-00012 8642029.
52. Hembry RM, Dyce J, Driesang I, Hunziker EB, Fosang AJ, Tyler JA, et al. Immunolocalization of matrix metalloproteinases in partial-thickness defects in pig articular cartilage. A preliminary report. The Journal of bone and joint surgery American volume. 2001;83-A(6):826–38. doi: 10.2106/00004623-200106000-00003 11407790.
53. Buschmann MD, Soulhat J, Shirazi-Adl A, Jurvelin JS, Hunziker EB. Confined compression of articular cartilage: linearity in ramp and sinusoidal tests and the importance of interdigitation and incomplete confinement. Journal of biomechanics. 1998;31(2):171–8. doi: 10.1016/s0021-9290(97)00124-3 9593212.
54. Jurvelin JS, Buschmann MD, Hunziker EB. Optical and mechanical determination of Poisson's ratio of adult bovine humeral articular cartilage. Journal of biomechanics. 1997;30(3):235–41. doi: 10.1016/s0021-9290(96)00133-9 9119822.
55. Dell'Accio F, Vanlauwe J, Bellemans J, Neys J, De Bari C, Luyten FP. Expanded phenotypically stable chondrocytes persist in the repair tissue and contribute to cartilage matrix formation and structural integration in a goat model of autologous chondrocyte implantation. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 2003;21(1):123–31. doi: 10.1016/S0736-0266(02)00090-6 12507589.
56. Lind M, Larsen A, Clausen C, Osther K, Everland H. Cartilage repair with chondrocytes in fibrin hydrogel and MPEG polylactide scaffold: an in vivo study in goats. Knee surgery, sports traumatology, arthroscopy: official journal of the ESSKA. 2008;16(7):690–8. doi: 10.1007/s00167-008-0522-1 18418579.
57. Jones CW, Willers C, Keogh A, Smolinski D, Fick D, Yates PJ, et al. Matrix-induced autologous chondrocyte implantation in sheep: objective assessments including confocal arthroscopy. Journal of orthopaedic research: official publication of the Orthopaedic Research Society. 2008;26(3):292–303. doi: 10.1002/jor.20502 17902176.
58. Murray MM, Fleming BC. Use of a bioactive scaffold to stimulate anterior cruciate ligament healing also minimizes posttraumatic osteoarthritis after surgery. The American journal of sports medicine. 2013;41(8):1762–70. doi: 10.1177/0363546513483446 23857883; PubMed Central PMCID: PMC3735821.
59. Birck MM, Vegge A, Stockel M, Gogenur I, Thymann T, Hammelev KP, et al. Laparoscopic Roux-en-Y gastric bypass in super obese Gottingen minipigs. American journal of translational research. 2013;5(6):643–53. 24093061; PubMed Central PMCID: PMC3786271.
60. Ellegaard L, Cunningham A, Edwards S, Grand N, Nevalainen T, Prescott M, et al. Welfare of the minipig with special reference to use in regulatory toxicology studies. Journal of pharmacological and toxicological methods. 2010;62(3):167–83. doi: 10.1016/j.vascn.2010.05.006 20621655.
61. Simianer H, Köhn F. Genetic management of the Gottingen Minipig population. Journal of pharmacological and toxicological methods. 2010;62(3):221–6. doi: 10.1016/j.vascn.2010.05.004 20570747.
62. Adkisson HDt, Martin JA, Amendola RL, Milliman C, Mauch KA, Katwal AB, et al. The potential of human allogeneic juvenile chondrocytes for restoration of articular cartilage. The American journal of sports medicine. 2010;38(7):1324–33. doi: 10.1177/0363546510361950 20423988; PubMed Central PMCID: PMC3774103.
63. Bonasia DE, Martin JA, Marmotti A, Amendola RL, Buckwalter JA, Rossi R, et al. Cocultures of adult and juvenile chondrocytes compared with adult and juvenile chondral fragments: in vitro matrix production. The American journal of sports medicine. 2011;39(11):2355–61. doi: 10.1177/0363546511417172 21828366; PubMed Central PMCID: PMC3708454.
64. Liu H, Zhao Z, Clarke RB, Gao J, Garrett IR, Margerrison EE. Enhanced tissue regeneration potential of juvenile articular cartilage. The American journal of sports medicine. 2013;41(11):2658–67. doi: 10.1177/0363546513502945 24043472.
65. Namba RS, Meuli M, Sullivan KM, Le AX, Adzick NS. Spontaneous repair of superficial defects in articular cartilage in a fetal lamb model. The Journal of bone and joint surgery American volume. 1998;80(1):4–10. doi: 10.2106/00004623-199801000-00003 9469302.
66. Reisig G, Kreinest M, Richter W, Wagner-Ecker M, Dinter D, Attenberger U, et al. Osteoarthritis in the Knee Joints of Gottingen Minipigs after Resection of the Anterior Cruciate Ligament? Missing Correlation of MRI, Gene and Protein Expression with Histological Scoring. PloS one. 2016;11(11). doi: 10.1371/journal.pone.0165897 27820852; PubMed Central PMCID: PMC5098790.
67. Chaganti RK, Lane NE. Risk factors for incident osteoarthritis of the hip and knee. Current reviews in musculoskeletal medicine. 2011;4(3):99–104. doi: 10.1007/s12178-011-9088-5 21808997; PubMed Central PMCID: PMC3261259.
68. Prieto-Alhambra D, Judge A, Javaid MK, Cooper C, Diez-Perez A, Arden NK. Incidence and risk factors for clinically diagnosed knee, hip and hand osteoarthritis: influences of age, gender and osteoarthritis affecting other joints. Annals of the rheumatic diseases. 2014;73(9):1659–64. doi: 10.1136/annrheumdis-2013-203355 23744977; PubMed Central PMCID: PMC3875433.
69. Appleyard RC, Burkhardt D, Ghosh P, Read R, Cake M, Swain MV, et al. Topographical analysis of the structural, biochemical and dynamic biomechanical properties of cartilage in an ovine model of osteoarthritis. Osteoarthritis and cartilage. 2003;11(1):65–77. doi: 10.1053/joca.2002.0867 12505489.
70. Young AA, Appleyard RC, Smith MM, Melrose J, Little CB. Dynamic biomechanics correlate with histopathology in human tibial cartilage: a preliminary study. Clinical orthopaedics and related research. 2007;462:212–20. doi: 10.1097/BLO.0b013e318076b431 17496559.
71. Erben RG, Silva-Lima B, Reischl I, Steinhoff G, Tiedemann G, Dalemans W, et al. White paper on how to go forward with cell-based advanced therapies in Europe. Tissue engineering Part A. 2014;20(19–20):2549–54. doi: 10.1089/ten.TEA.2013.0589 24749762; PubMed Central PMCID: PMC4195483.
72. (EMEA) EMA. GUIDELINE ON SAFETY AND EFFICACY FOLLOW-UP—RISK MANAGEMENT OF ADVANCED THERAPY MEDICINAL PRODUCTS London: European Medicines Agency, 2008 Contract No.: Doc. Ref. EMEA/149995/2008.
73. Zscharnack M, Krause C, Aust G, Thummler C, Peinemann F, Keller T, et al. Preclinical good laboratory practice-compliant safety study to evaluate biodistribution and tumorigenicity of a cartilage advanced therapy medicinal product (ATMP). Journal of translational medicine. 2015;13:160. doi: 10.1186/s12967-015-0517-x 25990108; PubMed Central PMCID: PMC4445304.
74. Murray MM, Magarian EM, Harrison SL, Mastrangelo AN, Zurakowski D, Fleming BC. The effect of skeletal maturity on functional healing of the anterior cruciate ligament. The Journal of bone and joint surgery American volume. 2010;92(11):2039–49. doi: 10.2106/JBJS.I.01368 20810854; PubMed Central PMCID: PMC2924734.
75. Gotterbarm T, Reitzel T, Schneider U, Voss HJ, Stofft E, Breusch SJ. [Integration of periosteum covered autogenous bone grafts with and without autologous chondrocytes. An animal experiment using the Gottinger minipig]. Der Orthopade. 2003;32(1):65–73. doi: 10.1007/s00132-002-0396-8 12557088.
76. Kreinest M, Reisig G, Strobel P, Dinter D, Attenberger U, Lipp P, et al. A Porcine Animal Model for Early Meniscal Degeneration—Analysis of Histology, Gene Expression and Magnetic Resonance Imaging Six Months after Resection of the Anterior Cruciate Ligament. PloS one. 2016;11(7). doi: 10.1371/journal.pone.0159331 27434644; PubMed Central PMCID: PMC4951152.
77. Schwarz ML, Kowarsch M, Rose S, Becker K, Lenz T, Jani L. Effect of surface roughness, porosity, and a resorbable calcium phosphate coating on osseointegration of titanium in a minipig model. Journal of biomedical materials research Part A. 2009;89(3):667–78. doi: 10.1002/jbm.a.32000 18442101.
78. Harris JD, Siston RA, Brophy RH, Lattermann C, Carey JL, Flanigan DC. Failures, re-operations, and complications after autologous chondrocyte implantation—a systematic review. Osteoarthritis and cartilage. 2011;19(7):779–91. doi: 10.1016/j.joca.2011.02.010 21333744.
79. Pietschmann MF, Niethammer TR, Horng A, Gulecyuz MF, Feist-Pagenstert I, Jansson V, et al. The incidence and clinical relevance of graft hypertrophy after matrix-based autologous chondrocyte implantation. The American journal of sports medicine. 2012;40(1):68–74. doi: 10.1177/0363546511424396 22031857.
80. Henderson I, Gui J, Lavigne P. Autologous chondrocyte implantation: natural history of postimplantation periosteal hypertrophy and effects of repair-site debridement on outcome. Arthroscopy: the journal of arthroscopic & related surgery: official publication of the Arthroscopy Association of North America and the International Arthroscopy Association. 2006;22(12):1318–24. doi: 10.1016/j.arthro.2006.07.057 17157731.
81. Maher JM, Markey JC, Ebert-May D. The other half of the story: effect size analysis in quantitative research. CBE life sciences education. 2013;12(3):345–51. doi: 10.1187/cbe.13-04-0082 24006382; PubMed Central PMCID: PMC3763001.
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Úspěšná resuscitativní thorakotomie v přednemocniční neodkladné péči
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts