One-stage cartilage repair using the autologous matrix-induced chondrogenesis combined with simultaneous use of autologous adipose tissue graft and adipose tissue mesenchymal cells technique: clinical results and magnetic resonance imaging evaluation at five-year follow-up.
Adipose tissue graft
Adipose tissue stem cells
Cartilage defects
Cartilage repair
LIPO-AMIC
Matrix-induced chondrogenesis
Journal
International orthopaedics
ISSN: 1432-5195
Titre abrégé: Int Orthop
Pays: Germany
ID NLM: 7705431
Informations de publication
Date de publication:
01 Sep 2023
01 Sep 2023
Historique:
received:
13
04
2023
accepted:
30
07
2023
medline:
1
9
2023
pubmed:
1
9
2023
entrez:
1
9
2023
Statut:
aheadofprint
Résumé
To evaluate medium-term outcomes of knee cartilage defects repair by autologous matrix-induced chondrogenesis combined with simultaneous use of autologous adipose tissue graft and adipose tissue mesenchymal cells, defined as LIPO-AMIC technique. The LIPO-AMIC technique has been used in ICRS degree III-IV knee defects. Eighteen patients have been prospectively evaluated during two and five years both clinically and by MRI. Patients showed progressive significant improvement of all scores starting early at six months, and further increased values were noted till the last follow-up at 60 months. Mean subjective pre-operative IKDC score of 36.1 significantly increased to 86.4 at 24 months and to 87.2 at 60 months. Mean pre-operative Lysholm score of 44.4 reached 93.5 at two years and 93.5 at five years. MRI examination showed early subchondral lamina regrowth and progressive maturation of repair tissue and filling of defects. The mean total MOCART score showed that a significative improvement from two year follow-up (69.1 points) to last follow-up was 81.9 points (range, 30-100 points, SD 24). Complete filling of the defect at the level of the surrounding cartilage was found in 77.8%. Adipose tissue can represent ideal source of MSCs since easiness of withdrawal and definite chondrogenic capacity. This study clearly demonstrated the LIPO-AMIC technique to be feasible for treatment of knee cartilage defects and to result in statistically significant progressive clinical, functional and pain improvement in all treated patients better than what reported for the AMIC standard technique, starting very early from the 6-month follow-up and maintaining the good clinical results more durably with stable results at mid-term follow-up.
Identifiants
pubmed: 37656198
doi: 10.1007/s00264-023-05921-8
pii: 10.1007/s00264-023-05921-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s).
Références
Widuchowski W, Widuchowski J, Trzaska T (2007) Articular cartilage defects: study of 25,124 knee arthroscopies. Knee 14:177–182
doi: 10.1016/j.knee.2007.02.001
pubmed: 17428666
Curl WW, Krome J, Gordon ES, Rushing J, Smith BP, Poehling GG (1997) Cartilage injuries: a review of 31,516 knee arthroscopies. Arthroscopy 13:456–460
doi: 10.1016/S0749-8063(97)90124-9
pubmed: 9276052
Benthien JP, Behrens P (2010) Autologous matrix-induced chondrogenesis (AMIC): combining microfracturing and a collagen I/III matrix for articular cartilage resurfacing. Cartilage (1):65–68. https://doi.org/10.1177/1947603509360044
Gille J, Behrens P, Volpi P, de Girolamo L, Reiss E, Zoch W, Anders S (2013) Outcome of autologous matrix induced chondrogenesis (AMIC) in cartilage knee surgery: data of the AMIC Registry. Arch Orthop Trauma Surg 133:87–93
doi: 10.1007/s00402-012-1621-5
pubmed: 23070222
Steinwachs MR, Gille J, Volz M, Anders S, Jakob R, De Girolamo L, Volpi P, Schiavone-Panni A, Scheffler S, Reiss E, Wittmann U (2021) Systematic review and meta-analysis of the clinical evidence on the use of autologous matrix-induced chondrogenesis in the knee. Cartilage 13(1 suppl):42S–56S. https://doi.org/10.1177/1947603519870846
doi: 10.1177/1947603519870846
pubmed: 31508990
Gobbi A, Karnatzikos G, Scotti C, Mahajan V, Mazzucco L, Grigolo B (2011) One-step cartilage repair with bone marrow aspirate concentrated cells and collagen matrix in full-thickness knee cartilage lesions: results at 2-year follow-up. Cartilage 2(3):286–299. https://doi.org/10.1177/1947603510392023
doi: 10.1177/1947603510392023
pubmed: 26069587
pmcid: 4300809
Sciarretta FV, Ascani C, Fossati C, Campisi S (2017) LIPO-AMIC: technical description and eighteen pilot patients report on AMIC® technique modified by adipose tissue mesenchymal cells augentation. Giornale Italiano di Ortopedia (GIOT) 43:156–162
Marlovits S, Singer P, Zeller P, Mandl I, Haller J, Trattnig S (2006) Magnetic resonance observation of cartilage repair tissue (MOCART) for the evaluation of autologous chondrocyte transplantation: determination of interobserver variability and correlation to clinical outcome after 2 years. Eur J Radiol 57(1):16–23
doi: 10.1016/j.ejrad.2005.08.007
pubmed: 16203119
Kaiser N, Jacob RP, Pagenstert G, Tannast M, Petek D (2021) Stable clinical long-term results after AMIC in the aligned knee. Arch Orthop Trauma Surg 141:1845–1854
doi: 10.1007/s00402-020-03564-7
pubmed: 32794150
Gille J, Reiss E, Freitag M et al (2021) Autologous matrix-induced chondrogenesis for treatment of focal cartilage defects in the knee: a follow-up study. Orthopaedic. J Sports Med 9(2). https://doi.org/10.1177/2325967120981872
Pareek A, Reardon PJ, Maak TG, Levy BA, Stuart MJ, Krych AJ (2016) Long-term outcomes after osteochondral autograft transfer: a systematic review at mean follow-up of 10.2 years. Arthroscopy Jun 32(6):1174–1184. https://doi.org/10.1016/j.arthro.2015.11.037
doi: 10.1016/j.arthro.2015.11.037
Kramer J, Böhrnsen F, Lindner U, Behrens P, Schlenke P, Rohwedel J (2006) In vivo matrix-guided human mesenchymal stem cells. Cell Mol Life Sci 63(5):616–626. https://doi.org/10.1007/s00018-005-5527-z
doi: 10.1007/s00018-005-5527-z
pubmed: 16482398
Dickhut A, Gottwald E, Steck E et al (2008) Chondrogenesis of mesenchymal stem cells in gel-like biomaterials in vitro and in vivo. Front Biosci 13(12):4517–4528
doi: 10.2741/3020
pubmed: 18508526
Gille J, Kunow J, Boisch L, Behrens P, Bos I, Hoffmann C, Köller W, Russlies M, Kurz B (2010) Cell-laden and cell-free matrix-induced chondrogenesis versus microfracture for the treatment of articular cartilage defects: a histological and biomechanical study in sheep. Cartilage. https://doi.org/10.1177/1947603509358721
Zuk PA, Zhu M, Mizuno H et al (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7(2):211–228
doi: 10.1089/107632701300062859
pubmed: 11304456
Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H et al (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295
doi: 10.1091/mbc.e02-02-0105
pubmed: 12475952
pmcid: 138633
Gimble J, Guilak F (2003) Adipose-derived adult stem cells: isolation, characterization, and differentiation potential. Cytotherapy 5(5):362–369. https://doi.org/10.1080/14653240310003026
doi: 10.1080/14653240310003026
pubmed: 14578098
Gimble JM, Katz AJ, Bunnell BA (2007) Adipose-derived stem cells for regenerative medicine. Cr Res 100:1249–1260
doi: 10.1161/01.RES.0000265074.83288.09
Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F (2002) Chondrogenic potential f adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 290:763–769
doi: 10.1006/bbrc.2001.6270
pubmed: 11785965
Gronthos S, Franklin DM, Leddy HA, Robey PG, Storms RW, Gimble JM (2001) Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 189:5463
doi: 10.1002/jcp.1138
Winter A, Breit S, Parsch D, Benz K, Steck E, Hauner H, Weber RM, Ewerbeck V, Richter W (2003) Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells. Arthritis Rheum 48:418–449
doi: 10.1002/art.10767
pubmed: 12571852
McIntosh K, Zvonic S, Garrett S, Mitchell JB, Floyd ZE, Hammill L, Kloster A, Di Halvorsen Y, Ting JP, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM (2006) The immunogenicity of human adipose-derived cells: temporal changes in vitro. Stem Cells 24(5):1246–1253. https://doi.org/10.1634/stemells.2005-0235
doi: 10.1634/stemells.2005-0235
pubmed: 16410391
Jo CH, Lee YG, Shin WH (2014) Intra-articular injection of mesenchymal stem cells for the treatment of osteoarthritis of the knee: a proof-of-concept clinical trial. Stem Cells 32:1254–1266
doi: 10.1002/stem.1634
pubmed: 24449146
Freitag J, Bates D, Boyd R et al (2016) Mesenchymal stem cell therapy in the treatment of osteoarthritis: reparative pathways, safety and efficacy—a review. BMC Musculoskelet Disord 17:230
doi: 10.1186/s12891-016-1085-9
pubmed: 27229856
pmcid: 4880954
Hong Z, Chen J, Zhang S, Zhao C, Bi M, Chen X, Bi Q (2019) Intra-articular injection of autologous adipose-derived stromal vascular fractions for knee osteoarthritis: a double-blind randomized self-controlled trial. Int Orthop 43:1123–1134. https://doi.org/10.1007/s00264-018-4099-0
doi: 10.1007/s00264-018-4099-0
pubmed: 30109404
Lee WS, Kim HJ, Kim KI, Kim GB, Jin W (2019) Intra-articular injection of autologous adipose tissue-derived mesenchymal stem cells for the treatment of knee osteoarthritis: a phase IIb, randomized, placebo-controlled clinical trial. Stem Cells Transl Med 8:504–511
doi: 10.1002/sctm.18-0122
pubmed: 30835956
pmcid: 6525553
Koh Y-G et al (2014) Comparative outcomes of open-wedge high tibial osteotomy with platelet-rich plasma alone or in combination with mesenchymal stem cell treatment: a prospective study. Arthroscoy 30(11):1453–1460
doi: 10.1016/j.arthro.2014.05.036
Bunnell BA, Flaat M, Gagliardi C, Patel B, Ripoll C (2008) Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45(2):115–120. https://doi.org/10.1016/j.ymeth.2008.03.006
doi: 10.1016/j.ymeth.2008.03.006
pubmed: 18593609
pmcid: 3668445
Baptista LS, do Amaral RJ, Carias RB, Aniceto M, Claudio-da-Silva C, Borojevic R (2009) An alternative method for the isolation of mesenchymal stromal cells derived from lipoaspirate samples. Cytotherapy 11(6):76–15. https://doi.org/10.3109/14653240902981144
doi: 10.3109/14653240902981144
Ishige I, Nagamura-Inoue T, Honda MJ, Harnprasopwat R, Kido M, Sugimoto M, Nakauchi H, Tojo A (2009) Comparison of mesenchymal stem cells derived from arterial, venous, and Wharton’s jelly explants of human umbilical cord. Int J Hematol 90(2):261–269. https://doi.org/10.1007/s12185-009-0377-3
doi: 10.1007/s12185-009-0377-3
pubmed: 19657615
Markarian CF, Frey GZ, Silveira MD, Chem EM, Milani AR, Ely PB et al (2014) Isolation of adipose-derived stem cells: a comparison among different methods. Biotechnol Lett 364:693–702. https://doi.org/10.1007/s10529-01-1425-x
doi: 10.1007/s10529-01-1425-x
Paspaliaris B, Thornton JF (2012) Methods and apparatuses for isolating and preparing stem cells. US. Patent Application 13/66,834, filed April 26, 2012
Aronowitz JA, Ellenhorn JD (2013) Adipose stromal vascular fraction isolation: a head-to-head comparison of four commercial cell separation systems. Plast Reconstr Surg 132(6):932e–939e. https://doi.org/10.1097/PRS.0b013e3182a80652
doi: 10.1097/PRS.0b013e3182a80652
pubmed: 24281640
Stubbers R, Coleman ME (2015) Apparatus and methods for cell isolation. US Patent Application 2015006691A
Zhu M, Cohen SR, Hicok KC, Shanahan RK, Strem BM, Yu JC et al (2013) Comparison of three different fat graft preparation methods: gravity separation, centrifugation, and simultaneous washing with filtration in a closed system. Plast Reconstr Surg 131(4):838. https://doi.org/10.1097/PRS.0b013e31828276e9
doi: 10.1097/PRS.0b013e31828276e9
Chu DT et al (2019) Adipose tissue stem cells for therapy: an update on the progress of isolation, culture, storage and clinical application. J Clin Med 8(7):917
doi: 10.3390/jcm8070917
pubmed: 31247996
pmcid: 6678927
Lam ATL, Reuveny S, Oh SK (2020) Human mesenchymal stem cell therapy for cartilage repair: review on isolation, expansion, and constructs. Stem Cell Res 44:101738. https://doi.org/10.1016/j.scr.2020.1738
doi: 10.1016/j.scr.2020.1738
pubmed: 32109723
Patrikoski M, Mannerström B, Miettinen S (2019) Perspectives for clinical translation of adipose stromal/stem cells. Stem Cells Int 2019:5858247. https://doi.org/10.1155/2019/5858247
doi: 10.1155/2019/5858247
pubmed: 31191677
pmcid: 6525805
Tremolada C et al (2016) Adipose tissue and mesenchymal stem cells: state of the art and Lipogems(R) technology development. Curr Stem Cell Rep 2:304–312
doi: 10.1007/s40778-016-0053-5
pubmed: 27547712
pmcid: 4972861
Tremolada C, Ricordi C, Caplan AI, Ventura C (2016) Mesenchymal stem cells in Lipogems, reverse story: from clinical practice to basic science. Methods Mol Biol 1416:109–122
doi: 10.1007/978-1-4939-3584-0_6
pubmed: 27236668
Bianchi F, Maioli M, Leonardi E, Olivi E, Pasquinelli G, Valente S et al (2013) A new nonenzymatic method and device to obtain a fat tissue derivative highly enriched in pericyte-like elements by mild mechanical forces from human lipoaspirates. Cell Transplant 22(11):2063–2077. https://doi.org/10.3727/096368912X657855
doi: 10.3727/096368912X657855
pubmed: 23051701
Carelli S, Messaggio F, Canazza A, Hebda DM, Caremoli F, Latorre E, Grimoldi MG, Colli M, Bulfamante G, Tremolada C, Di Giulio AM, Gorio A (2015) Characteristics and properties o mesenchymal stem cells derived from microfragmented adipose tissue. Cell Transplant 24(7):1233–1252. https://doi.org/10.3727/096368914X681603
doi: 10.3727/096368914X681603
pubmed: 24806078
Garcia-Contreras M, Messaggio F, Mendez AJ, Ricordi C (2018) Metabolomic changes in human adipose tissue derived products following non-enzymatic microfacturing. Eur Rev Med Pharmacol Sci 22:3249–3260
pubmed: 29863273
Vezzani B, Shaw I, Lesme H, Yong L, Khan N, Tremolada C, Péault B (2018) Higher pericyte content and secretory activity of microfragmented human adipose tissue compared to enzymatically derived stromal vascular fraction. Stem Cells Transl Med 7(12):876–886. https://doi.org/10.1002/sctm.18-0051
doi: 10.1002/sctm.18-0051
pubmed: 30255987
pmcid: 6265639
Bosetti M, Borrone A, Follenzi A, Messaggio F, Tremolada C, Cannas M (2016) Human lipoaspirate as autologous injectable active scaffold for one-step repair of cartilage defects. Cell Transplant 25:1043–1056
doi: 10.3727/096368915X689514
pubmed: 26395761
García-Contreras M, Messaggio F, Jimenez O, Mendez A (2015) Differences in exosome content of human adipose tissue processed by non-enzymatic and enzymatic methods. CellR4 3(1):e123
Kaewsuwan S, Song SY, Kim JH, Sung JH (2012) Mimicking the functional niche of adipose-derived stem cells for regenerative medicine. Expert Opin Biol Ther 12(12):1575–1588
doi: 10.1517/14712598.2012.721763
pubmed: 22953993
Xu T, Yu X, Liu X, Fang J, Dai X (2019) Autologous micro-fragmented adipose tissue as a stem-base natural scaffold for cartilage direct repair. Cell Transplant 28(12):1709–1720
doi: 10.1177/0963689719880527
pubmed: 31565996
pmcid: 6923561
Matsiko A, Gleeson JP, O’Brien FJ (2015) Scaffold mean pore size influences mesenchymal stem cell chondrogenic differentiation and matrix deposition. Tissue Eng Part A 21:486–497
doi: 10.1089/ten.tea.2013.0545
pubmed: 25203687
Nöth U, Rackwitz L, Heymer A, Weber M, Baumann B, Steinert A et al (2007) Chondrogenic differentiation of human mesenchymal stem cells in collagen type I hydrogels. J Biomed Mater Res A 83:626–663
doi: 10.1002/jbm.a.31254
pubmed: 17503531
Ashworth JC, Mehr M, Buxton PG, Best SM, Cameron RE (2018) Optimising collagen scaffold architecture for enhanced periodontal ligament fibroblast migration. J Mater Sci Mater Med 29:166. https://doi.org/10.1007/s10856-018-6175-9
doi: 10.1007/s10856-018-6175-9
pubmed: 30392028
pmcid: 6223802
Landers R, Pfister A, Hübner U, John H, Schmelzeisen R, Mülhaupt R (2002) Fabrication of soft tissue engineering scaffolds by means of rapid prototyping techniques. J Mater Sci 37:3107–3116. https://doi.org/10.1023/A:1016189724389
doi: 10.1023/A:1016189724389
Davidenko N, Campbell JJ, Thian ES, Watson CJ, Cameron RE (2010) Collagen-hyaluronic acid scaffolds for adipose tissue engineering. Acta Biomater 6(10):3957–3968
doi: 10.1016/j.actbio.2010.05.005
pubmed: 20466086
Zhang Y-S, Gao J-H, Lu F, Zhu M, Liao Y-J (2007) Cellular compatibility of type collagen I scaffold and human adipose-derived stem cells. Nan Fang Yi Ke Da Xue Xue Bao 27(2):223–225
pubmed: 17355943
Lu Z, Doulabi BZ, Huang C, Bank RA, Helder MN (2010) Collagen type II enhances chondrogenesis in adipose tissue-derived stem cells by affecting cell shape. Tissue Eng Part A 16:81–90
doi: 10.1089/ten.tea.2009.0222
pubmed: 19624244
Kim SA, Sur YJ, Cho ML et al (2020) Atelocollagen promotes chondrogenic differentiation of human adipose-derived mesenchymal stem cells. Sci Rep 10:10678. https://doi.org/10.1038/s41598-020-67836-3
doi: 10.1038/s41598-020-67836-3
pubmed: 32606308
pmcid: 7327030