Advertisement

Improved outcomes after mesenchymal stem cells injections for knee osteoarthritis: results at 12-months follow-up: a systematic review of the literature

  • Filippo MiglioriniEmail author
  • Björn Rath
  • Giorgia Colarossi
  • Arne Driessen
  • Markus Tingart
  • Marc Niewiera
  • Jörg Eschweiler
Orthopaedic Surgery

Abstract

Purpose

According to the World Health organization (WHO), more than 10% in people older than 60 years suffer from osteoarthritis (OA). Over the last years, there has been an increased interest around regenerative medicine, especially regarding stem cell treatments and related applications. We hypothesize that stem cell therapies can represent a feasible option for idiopathic knee OA, delaying or even avoiding the joint replacement. To emphasize the potential of percutaneous injections of mesenchymal stem cells for knee OA, a comprehensive systematic review of the literature was conducted.

Material and methods

Two independent authors (FM, GC) performed the literature search. This study was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines (PRISMA). The main databases were accessed: Pubmed, Embase, Google Scholar, Cochrane Systematic Reviews, Scopus, AMED. For this systematic review, all articles treating percutaneous injections of mesenchymal stem cells for knee OA were considered. Because of the rapid advancements promoted by the scientific progress on stem cell expansion and processing, only articles published within the last five years were included. Solely articles reporting the outcomes of interest across 6- and 12-month follow-up were recruited for eligibility. We included only studies reporting quantitative data under the outcomes of interest. We referred for the quality assessment to the Coleman Methodology Score (CMS). The statistical analysis was performed with Review Manager Software 5.3 (The Nordic Cochrane Centre, Copenhagen).

Results

A total of 18 studies were enrolled in the present study, comprising 1069 treated knees. The mean age of the samples was 57.39 ± 7.37 years. 72% of the included studies harvested the stem cells from the iliac crest (bone marrow-derived MSCs), the remaining 28% from the adipose tissue (adipose-derived MSCs). The mean visual analogic scale improved from 18.37 to 30.98 and 36.91 at 6- and 12-month follow-up, respectively. The mean WOMAC score improved from 25.66 to 25.23 and 15.60 at 6- and 12-month follow-up, respectively. The mean walking distance improved from 71.90 to 152.22 and 316.72 at 6- and 12-month follow-up, respectively. The mean Lequesne scale improved from 33.76 to 12.90 at 12-month follow-up. The KOOS score improved from 41.07 to 8.47% and 18.94 at 6- and 12-month follow-up. All the KOOS subscales improved significantly from the baseline. A total of 136 (12.7%) local complications were detected.

Conclusion

According to the current evidences and the main findings of this systematic review, we reported that MSC infiltrations for knee OA can represent a feasible option, leading to an overall remarkable improvement of all clinical and functional considered outcomes, regardless of the cell source. Patients treated at earlier-degeneration stages reported statistically significant greater outcomes. The pain and function scores were improved considerably, thus, leading to a significant improvement of patient participation in recreational activities and quality of life.

Keywords

Osteoarthritis Knee Mesenchymal stem cells Infiltrations 

Notes

Acknowledgements

We would like to thank Pia Offermanns B. A. (freelance editor, translator and proof-reader) for her professional editing of this study.

Funding

No external source of funding was used.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of study informed consent is not required.

References

  1. 1.
    Runhaar J, van Middelkoop M, Reijman M, Willemsen S, Oei EH, Vroegindeweij D, van Osch G, Koes B, Bierma-Zeinstra SM (2015) Prevention of knee osteoarthritis in overweight females: the first preventive randomized controlled trial in osteoarthritis. Am J Med 128(8):888–895.  https://doi.org/10.1016/j.amjmed.2015.03.006 CrossRefPubMedGoogle Scholar
  2. 2.
    Harirforoosh S, Asghar W, Jamali F (2013) Adverse effects of nonsteroidal antiinflammatory drugs: an update of gastrointestinal, cardiovascular and renal complications. J Pharm Pharm Sci 16(5):821–847CrossRefPubMedGoogle Scholar
  3. 3.
    Felson DT, Lawrence RC, Hochberg MC, McAlindon T, Dieppe PA, Minor MA, Blair SN, Berman BM, Fries JF, Weinberger M, Lorig KR, Jacobs JJ, Goldberg V (2000) Osteoarthritis: new insights Part 2: treatment approaches. Ann Intern Med 133(9):726–737CrossRefPubMedGoogle Scholar
  4. 4.
    Fibel KH, Hillstrom HJ, Halpern BC (2015) State-of-the-Art management of knee osteoarthritis. World J Clin Cases 3(2):89–101.  https://doi.org/10.12998/wjcc.v3.i2.89 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Pourcho AM, Smith J, Wisniewski SJ, Sellon JL (2014) Intraarticular platelet-rich plasma injection in the treatment of knee osteoarthritis: review and recommendations. Am J Phys Med Rehabil 93(11 Suppl 3):S108–121.  https://doi.org/10.1097/PHM.0000000000000115 CrossRefPubMedGoogle Scholar
  6. 6.
    Jevsevar D, Donnelly P, Brown GA, Cummins DS (2015) Viscosupplementation for osteoarthritis of the knee: a systematic review of the evidence. J Bone Joint Surg Am 97(24):2047–2060.  https://doi.org/10.2106/JBJS.N.00743 CrossRefPubMedGoogle Scholar
  7. 7.
    Peersman G, Jak W, Vandenlangenbergh T, Jans C, Cartier P, Fennema P (2014) Cost-effectiveness of unicondylar versus total knee arthroplasty: a Markov model analysis. Knee 21(Suppl 1):S37–42.  https://doi.org/10.1016/S0968-0160(14)50008-7 CrossRefPubMedGoogle Scholar
  8. 8.
    Song EK, Agrawal PR, Kim SK, Seo HY, Seon JK (2016) A randomized controlled clinical and radiological trial about outcomes of navigation-assisted TKA compared to conventional TKA: long-term follow-up. Knee Surg Sports Traumatol Arthrosc 24(11):3381–3386.  https://doi.org/10.1007/s00167-016-3996-2 CrossRefPubMedGoogle Scholar
  9. 9.
    Healy WL, Della Valle CJ, Iorio R, Berend KR, Cushner FD, Dalury DF, Lonner JH (2013) Complications of total knee arthroplasty: standardized list and definitions of the Knee Society. Clin Orthop Relat Res 471(1):215–220.  https://doi.org/10.1007/s11999-012-2489-y CrossRefPubMedGoogle Scholar
  10. 10.
    Aicher WK, Buhring HJ, Hart M, Rolauffs B, Badke A, Klein G (2011) Regeneration of cartilage and bone by defined subsets of mesenchymal stromal cells–potential and pitfalls. Adv Drug Deliv Rev 63(4–5):342–351.  https://doi.org/10.1016/j.addr.2010.12.004 CrossRefPubMedGoogle Scholar
  11. 11.
    Caplan AI, Dennis JE (2006) Mesenchymal stem cells as trophic mediators. J Cell Biochem 98(5):1076–1084.  https://doi.org/10.1002/jcb.20886 CrossRefPubMedGoogle Scholar
  12. 12.
    Akgun I, Unlu MC, Erdal OA, Ogut T, Erturk M, Ovali E, Kantarci F, Caliskan G, Akgun Y (2015) Matrix-induced autologous mesenchymal stem cell implantation versus matrix-induced autologous chondrocyte implantation in the treatment of chondral defects of the knee: a 2-year randomized study. Arch Orthop Trauma Surg 135(2):251–263.  https://doi.org/10.1007/s00402-014-2136-z CrossRefPubMedGoogle Scholar
  13. 13.
    Reichenbach S, Blank S, Rutjes AW, Shang A, King EA, Dieppe PA, Juni P, Trelle S (2007) Hylan versus hyaluronic acid for osteoarthritis of the knee: a systematic review and meta-analysis. Arthritis Rheum 57(8):1410–1418.  https://doi.org/10.1002/art.23103 CrossRefPubMedGoogle Scholar
  14. 14.
    Pecina M, Vukicevic S (2007) Biological aspects of bone, cartilage and tendon regeneration. Int Orthop 31(6):719–720.  https://doi.org/10.1007/s00264-007-0425-7 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Lind M, Bunger C (2005) Orthopaedic applications of gene therapy. Int Orthop 29(4):205–209.  https://doi.org/10.1007/s00264-005-0650-x CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535.  https://doi.org/10.1136/bmj.b2535 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Howick JCI, Glasziou P, Greenhalgh T, Heneghan C, Liberati A, Moschetti I, Phillips B, Thornton H, Goddard O, Hodgkinson M (2011) The 2011 Oxford Levels of Evidence. Oxford Centre for Evidence-Based Medicine Available at https://www.cebm.net/index.aspx?o=5653
  18. 18.
    Walker LC, Clement ND, Bardgett M, Weir D, Holland J, Gerrand C, Deehan DJ (2018) The WOMAC score can be reliably used to classify patient satisfaction after total knee arthroplasty. Knee Surg Sports Traumatol Arthrosc.  https://doi.org/10.1007/s00167-018-4879-5 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Roos EM, Lohmander LS (2003) The Knee injury and Osteoarthritis Outcome Score (KOOS): from joint injury to osteoarthritis. Health Qual Life Outcomes 1:64.  https://doi.org/10.1186/1477-7525-1-64 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Lecorney J, Verhoeven F, Chouk M, Guillot X, Prati C, Wendling D (2018) Correlation between catastrophizing and Lequesne index in case of osteoarthritis of the knee: a prospective study. Joint Bone Spine 85(5):605–607.  https://doi.org/10.1016/j.jbspin.2017.10.002 CrossRefPubMedGoogle Scholar
  21. 21.
    Al-Najar M, Khalil H, Al-Ajlouni J, Al-Antary E, Hamdan M, Rahmeh R, Alhattab D, Samara O, Yasin M, Abdullah AA, Al-Jabbari E, Hmaid D, Jafar H, Awidi A (2017) Intra-articular injection of expanded autologous bone marrow mesenchymal cells in moderate and severe knee osteoarthritis is safe: a phase I/II study. J Orthop Surg Res 12(1):190.  https://doi.org/10.1186/s13018-017-0689-6 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Bastos R, Mathias M, Andrade R, Bastos R, Balduino A, Schott V, Rodeo S, Espregueira-Mendes J (2018) Intra-articular injections of expanded mesenchymal stem cells with and without addition of platelet-rich plasma are safe and effective for knee osteoarthritis. Knee Surg Sports Traumatol Arthrosc.  https://doi.org/10.1007/s00167-018-4883-9 CrossRefPubMedGoogle Scholar
  23. 23.
    Centeno C, Pitts J, Al-Sayegh H, Freeman M (2014) Efficacy of autologous bone marrow concentrate for knee osteoarthritis with and without adipose graft. Biomed Res Int 2014:370621.  https://doi.org/10.1155/2014/370621 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Davatchi F, Abdollahi BS, Mohyeddin M, Nikbin B (2016) Mesenchymal stem cell therapy for knee osteoarthritis: 5 years follow-up of three patients. Int J Rheum Dis 19(3):219–225.  https://doi.org/10.1111/1756-185X.12670 CrossRefPubMedGoogle Scholar
  25. 25.
    Emadedin M, Aghdami N, Taghiyar L, Fazeli R, Moghadasali R, Jahangir S, Farjad R, Baghaban Eslaminejad M (2012) Intra-articular injection of autologous mesenchymal stem cells in six patients with knee osteoarthritis. Arch Iran Med 15(7):422–428. https://doi.org/012157/AIM.0010PubMedGoogle Scholar
  26. 26.
    Emadedin M, Ghorbani Liastani M, Fazeli R, Mohseni F, Moghadasali R, Mardpour S, Hosseini SE, Niknejadi M, Moeininia F, Aghahossein Fanni A, Baghban Eslaminejhad R, Vosough Dizaji A, Labibzadeh N, Mirazimi Bafghi A, Baharvand H, Aghdami N (2015) Long-term follow-up of intra-articular injection of autologous mesenchymal stem cells in patients with knee, ankle, or hip osteoarthritis. Arch Iran Med 18(6):336–344. https://doi.org/015186/AIM.003PubMedGoogle Scholar
  27. 27.
    Fodor PB, Paulseth SG (2016) Adipose derived stromal cell (ADSC) injections for pain management of osteoarthritis in the human knee joint. Aesthet Surg J 36(2):229–236.  https://doi.org/10.1093/asj/sjv135 CrossRefPubMedGoogle Scholar
  28. 28.
    Garay-Mendoza D, Villarreal-Martinez L, Garza-Bedolla A, Perez-Garza DM, Acosta-Olivo C, Vilchez-Cavazos F, Diaz-Hutchinson C, Gomez-Almaguer D, Jaime-Perez JC, Mancias-Guerra C (2018) The effect of intra-articular injection of autologous bone marrow stem cells on pain and knee function in patients with osteoarthritis. Int J Rheum Dis 21(1):140–147.  https://doi.org/10.1111/1756-185X.13139 CrossRefPubMedGoogle Scholar
  29. 29.
    Goncars V, Kalnberzs K, Jakobsons E, Engele I, Briede I, Blums K, Erglis K, Erglis M, Patetko L, Muiznieks I, Erglis A (2018) Treatment of knee osteoarthritis with bone marrow-derived mononuclear cell injection: 12-month follow-up. Cartilage:1947603517746721.  https://doi.org/10.1177/1947603517746721
  30. 30.
    Lamo-Espinosa JM, Mora G, Blanco JF, Granero-Molto F, Nunez-Cordoba JM, Sanchez-Echenique C, Bondia JM, Aquerreta JD, Andreu EJ, Ornilla E, Villaron EM, Valenti-Azcarate A, Sanchez-Guijo F, Del Canizo MC, Valenti-Nin JR, Prosper F (2016) Intra-articular injection of two different doses of autologous bone marrow mesenchymal stem cells versus hyaluronic acid in the treatment of knee osteoarthritis: multicenter randomized controlled clinical trial (phase I/II). J Transl Med 14(1):246.  https://doi.org/10.1186/s12967-016-0998-2 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Lamo-Espinosa JM, Mora G, Blanco JF, Granero-Molto F, Nunez-Cordoba JM, Lopez-Elio S, Andreu E, Sanchez-Guijo F, Aquerreta JD, Bondia JM, Valenti-Azcarate A, Del Consuelo Del Canizo M, Villaron EM, Valenti-Nin JR, Prosper F (2018) Intra-articular injection of two different doses of autologous bone marrow mesenchymal stem cells versus hyaluronic acid in the treatment of knee osteoarthritis: long-term follow up of a multicenter randomized controlled clinical trial (phase I/II). J Transl Med 16(1):213.  https://doi.org/10.1186/s12967-018-1591-7 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Orozco L, Munar A, Soler R, Alberca M, Soler F, Huguet M, Sentis J, Sanchez A, Garcia-Sancho J (2013) Treatment of knee osteoarthritis with autologous mesenchymal stem cells: a pilot study. Transplantation 95(12):1535–1541.  https://doi.org/10.1097/TP.0b013e318291a2da CrossRefPubMedGoogle Scholar
  33. 33.
    Pers YM, Rackwitz L, Ferreira R, Pullig O, Delfour C, Barry F, Sensebe L, Casteilla L, Fleury S, Bourin P, Noel D, Canovas F, Cyteval C, Lisignoli G, Schrauth J, Haddad D, Domergue S, Noeth U, Jorgensen C, Consortium A (2016) Adipose mesenchymal stromal cell-based therapy for severe osteoarthritis of the knee: a phase I dose-escalation trial. Stem Cells Transl Med 5(7):847–856.  https://doi.org/10.5966/sctm.2015-0245 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Pintat J, Silvestre A, Magalon G, Gadeau AP, Pesquer L, Perozziello A, Peuchant A, Mounayer C, Dallaudiere B (2017) Intra-articular injection of mesenchymal stem cells and platelet-rich plasma to treat patellofemoral osteoarthritis: preliminary results of a long-term pilot study. J Vasc Interv Radiol 28(12):1708–1713.  https://doi.org/10.1016/j.jvir.2017.08.004 CrossRefPubMedGoogle Scholar
  35. 35.
    Rajput B, Kulkarni R, Bopardikar A, Somalapur P, Kumar R (2018) Retrospective analysis of role of autologous bone marrow derived mononuclear stem cells in the management of degenerative arthritis of knee. J Stem Cell Res Ther 4(2):21–27Google Scholar
  36. 36.
    Soler R, Orozco L, Munar A, Huguet M, Lopez R, Vives J, Coll R, Codinach M, Garcia-Lopez J (2016) Final results of a phase I–II trial using ex vivo expanded autologous Mesenchymal Stromal Cells for the treatment of osteoarthritis of the knee confirming safety and suggesting cartilage regeneration. Knee 23(4):647–654.  https://doi.org/10.1016/j.knee.2015.08.013 CrossRefPubMedGoogle Scholar
  37. 37.
    Soler Rich R, Munar A, Soler Romagosa F, Peirau X, Huguet M, Alberca M, García SA, Sancho JLO (2015) Treatment of knee osteoarthritis with autologous expanded bone marrow mesenchymal stem cells: 50 cases clinical and mri results at one year follow-up. J Stem Cell Res Ther 5(6):1–7Google Scholar
  38. 38.
    Spasovski D, Spasovski V, Bascarevic Z, Stojiljkovic M, Vreca M, Andelkovic M, Pavlovic S (2018) Intra-articular injection of autologous adipose-derived mesenchymal stem cells in the treatment of knee osteoarthritis. J Gene Med.  https://doi.org/10.1002/jgm.3002 CrossRefPubMedGoogle Scholar
  39. 39.
    Vega A, Martin-Ferrero MA, Del Canto F, Alberca M, Garcia V, Munar A, Orozco L, Soler R, Fuertes JJ, Huguet M, Sanchez A, Garcia-Sancho J (2015) Treatment of knee osteoarthritis with allogeneic bone marrow mesenchymal stem cells: a randomized controlled trial. Transplantation 99(8):1681–1690.  https://doi.org/10.1097/TP.0000000000000678 CrossRefPubMedGoogle Scholar
  40. 40.
    Bellamy N, Campbell J, Robinson V, Gee T, Bourne R, Wells G (2006) Intraarticular corticosteroid for treatment of osteoarthritis of the knee. Cochrane Database Syst Rev.  https://doi.org/10.1002/14651858.CD005328.pub2 CrossRefPubMedGoogle Scholar
  41. 41.
    Caldwell JR (1996) Intra-articular corticosteroids. Guide to selection and indications for use. Drugs 52(4):507–514CrossRefPubMedGoogle Scholar
  42. 42.
    Wernecke C, Braun HJ, Dragoo JL (2015) The effect of intra-articular corticosteroids on articular cartilage: a systematic review. Orthop J Sports Med 3(5):2325967115581163.  https://doi.org/10.1177/2325967115581163 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Barker WD, Martinek J (1976) An ultrastructural evaluation of the effect of hydrocortisone on rabbit cartilage. Clin Orthop Relat Res 115:286–290Google Scholar
  44. 44.
    Dragoo JL, Danial CM, Braun HJ, Pouliot MA, Kim HJ (2012) The chondrotoxicity of single-dose corticosteroids. Knee Surg Sports Traumatol Arthrosc 20(9):1809–1814.  https://doi.org/10.1007/s00167-011-1820-6 CrossRefPubMedGoogle Scholar
  45. 45.
    Frisbie DD, Kawcak CE, Trotter GW, Powers BE, Walton RM, McIlwraith CW (1997) Effects of triamcinolone acetonide on an in vivo equine osteochondral fragment exercise model. Equine Vet J 29(5):349–359CrossRefPubMedGoogle Scholar
  46. 46.
    Yagi H, Soto-Gutierrez A, Parekkadan B, Kitagawa Y, Tompkins RG, Kobayashi N, Yarmush ML (2010) Mesenchymal stem cells: mechanisms of immunomodulation and homing. Cell Transpl 19(6):667–679.  https://doi.org/10.3727/096368910X508762 CrossRefGoogle Scholar
  47. 47.
    Aggarwal S, Pittenger MF (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105(4):1815–1822.  https://doi.org/10.1182/blood-2004-04-1559 CrossRefPubMedGoogle Scholar
  48. 48.
    Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, Cancedda R, Pennesi G (2005) Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 35(5):1482–1490.  https://doi.org/10.1002/eji.200425405 CrossRefPubMedGoogle Scholar
  49. 49.
    Plumas J, Chaperot L, Richard MJ, Molens JP, Bensa JC, Favrot MC (2005) Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia 19(9):1597–1604.  https://doi.org/10.1038/sj.leu.2403871 CrossRefPubMedGoogle Scholar
  50. 50.
    Wyles CC, Houdek MT, Wyles SP, Wagner ER, Behfar A, Sierra RJ (2015) Differential cytotoxicity of corticosteroids on human mesenchymal stem cells. Clin Orthop Relat Res 473(3):1155–1164.  https://doi.org/10.1007/s11999-014-3925-y CrossRefPubMedGoogle Scholar
  51. 51.
    Chen X, Gan Y, Li W, Su J, Zhang Y, Huang Y, Roberts AI, Han Y, Li J, Wang Y, Shi Y (2014) The interaction between mesenchymal stem cells and steroids during inflammation. Cell Death Dis 5:e1009.  https://doi.org/10.1038/cddis.2013.537 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Nuzzi R, Gunetti M, Rustichelli D, Roagna B, Fronticelli Bardelli F, Fagioli F, Ferrero I (2012) Effect of in vitro exposure of corticosteroid drugs, conventionally used in AMD treatment, on mesenchymal stem cells. Stem Cells Int 2012:946090.  https://doi.org/10.1155/2012/946090 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Feldman BJ (2009) Glucocorticoids influence on mesenchymal stem cells and implications for metabolic disease. Pediatr Res 65(2):249–251.  https://doi.org/10.1203/PDR.0b013e3181909c08 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Breu A, Eckl S, Zink W, Kujat R, Angele P (2013) Cytotoxicity of local anesthetics on human mesenchymal stem cells in vitro. Arthroscopy 29(10):1676–1684.  https://doi.org/10.1016/j.arthro.2013.06.018 CrossRefPubMedGoogle Scholar
  55. 55.
    Rahnama R, Wang M, Dang AC, Kim HT, Kuo AC (2013) Cytotoxicity of local anesthetics on human mesenchymal stem cells. J Bone Joint Surg Am 95(2):132–137.  https://doi.org/10.2106/JBJS.K.01291 CrossRefPubMedGoogle Scholar
  56. 56.
    Ahmad Z, Howard D, Brooks RA, Wardale J, Henson FM, Getgood A, Rushton N (2012) The role of platelet rich plasma in musculoskeletal science. JRSM Short Rep 3(6):40.  https://doi.org/10.1258/shorts.2011.011148 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Sheth U, Simunovic N, Klein G, Fu F, Einhorn TA, Schemitsch E, Ayeni OR, Bhandari M (2012) Efficacy of autologous platelet-rich plasma use for orthopaedic indications: a meta-analysis. J Bone Joint Surg Am 94(4):298–307.  https://doi.org/10.2106/JBJS.K.00154 CrossRefPubMedGoogle Scholar
  58. 58.
    Le ADK, Enweze L, DeBaun MR, Dragoo JL (2018) Current clinical recommendations for use of platelet-rich plasma. Curr Rev Musculoskelet Med 11(4):624–634.  https://doi.org/10.1007/s12178-018-9527-7 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Johal H, Khan M, Yung SP, Dhillon MS, Fu FH, Bedi A, Bhandari M (2019) Impact of platelet-rich plasma use on pain in orthopaedic surgery: a systematic review and meta-analysis. Sports Health 11(4):355–366.  https://doi.org/10.1177/1941738119834972 CrossRefPubMedGoogle Scholar
  60. 60.
    Franchini M, Cruciani M, Mengoli C, Marano G, Pupella S, Veropalumbo E, Masiello F, Pati I, Vaglio S, Liumbruno GM (2018) Efficacy of platelet-rich plasma as conservative treatment in orthopaedics: a systematic review and meta-analysis. Blood Transfus 16(6):502–513.  https://doi.org/10.2450/2018.0111-18 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Chen X, Jones IA, Park C, Vangsness CT Jr (2018) The efficacy of platelet-rich plasma on tendon and ligament healing: a systematic review and meta-analysis with bias assessment. Am J Sports Med 46(8):2020–2032.  https://doi.org/10.1177/0363546517743746 CrossRefPubMedGoogle Scholar
  62. 62.
    Fitzpatrick J, Bulsara M, Zheng MH (2017) The effectiveness of platelet-rich plasma in the treatment of tendinopathy: a meta-analysis of randomized controlled clinical trials. Am J Sports Med 45(1):226–233.  https://doi.org/10.1177/0363546516643716 CrossRefPubMedGoogle Scholar
  63. 63.
    Martin DR, Cox NR, Hathcock TL, Niemeyer GP, Baker HJ (2002) Isolation and characterization of multipotential mesenchymal stem cells from feline bone marrow. Exp Hematol 30(8):879–886CrossRefPubMedGoogle Scholar
  64. 64.
    Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143–147.  https://doi.org/10.1126/science.284.5411.143 CrossRefGoogle Scholar
  65. 65.
    Baker N, Boyette LB, Tuan RS (2015) Characterization of bone marrow-derived mesenchymal stem cells in aging. Bone 70:37–47.  https://doi.org/10.1016/j.bone.2014.10.014 CrossRefGoogle Scholar
  66. 66.
    Caplan AI, Correa D (2011) The MSC: an injury drugstore. Cell Stem Cell 9(1):11–15.  https://doi.org/10.1016/j.stem.2011.06.008 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Murray IR, Corselli M, Petrigliano FA, Soo C, Peault B (2014) Recent insights into the identity of mesenchymal stem cells: Implications for orthopaedic applications. Bone Joint J 96B(3):291–298.  https://doi.org/10.1302/0301-620X.96B3.32789 CrossRefGoogle Scholar
  68. 68.
    Petersson IF, Boegard T, Saxne T, Silman AJ, Svensson B (1997) Radiographic osteoarthritis of the knee classified by the Ahlback and Kellgren & Lawrence systems for the tibiofemoral joint in people aged 35–54 years with chronic knee pain. Ann Rheum Dis 56(8):493–496CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Harichandan A, Buhring HJ (2011) Prospective isolation of human MSC. Best Pract Res Clin Haematol 24(1):25–36.  https://doi.org/10.1016/j.beha.2011.01.001 CrossRefPubMedGoogle Scholar
  70. 70.
    Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, Moseley A, Hoffman R (2002) Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 30(1):42–48CrossRefPubMedGoogle Scholar
  71. 71.
    Desando G, Cavallo C, Sartoni F, Martini L, Parrilli A, Veronesi F, Fini M, Giardino R, Facchini A, Grigolo B (2013) Intra-articular delivery of adipose derived stromal cells attenuates osteoarthritis progression in an experimental rabbit model. Arthritis Res Ther 15(1):R22.  https://doi.org/10.1186/ar4156 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Guercio A, Di Marco P, Casella S, Cannella V, Russotto L, Purpari G, Di Bella S, Piccione G (2012) Production of canine mesenchymal stem cells from adipose tissue and their application in dogs with chronic osteoarthritis of the humeroradial joints. Cell Biol Int 36(2):189–194.  https://doi.org/10.1042/CBI20110304 CrossRefPubMedGoogle Scholar
  73. 73.
    Jurgens WJ, Kroeze RJ, Zandieh-Doulabi B, van Dijk A, Renders GA, Smit TH, van Milligen FJ, Ritt MJ, Helder MN (2013) One-step surgical procedure for the treatment of osteochondral defects with adipose-derived stem cells in a caprine knee defect: a pilot study. Biores Open Access 2(4):315–325.  https://doi.org/10.1089/biores.2013.0024 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Jung M, Kaszap B, Redohl A, Steck E, Breusch S, Richter W, Gotterbarm T (2009) Enhanced early tissue regeneration after matrix-assisted autologous mesenchymal stem cell transplantation in full thickness chondral defects in a minipig model. Cell Transpl 18(8):923–932.  https://doi.org/10.3727/096368909X471297 CrossRefGoogle Scholar
  75. 75.
    Di Ianni M, Del Papa B, De Ioanni M, Moretti L, Bonifacio E, Cecchini D, Sportoletti P, Falzetti F, Tabilio A (2008) Mesenchymal cells recruit and regulate T regulatory cells. Exp Hematol 36(3):309–318.  https://doi.org/10.1016/j.exphem.2007.11.007 CrossRefPubMedGoogle Scholar
  76. 76.
    Benvenuto F, Ferrari S, Gerdoni E, Gualandi F, Frassoni F, Pistoia V, Mancardi G, Uccelli A (2007) Human mesenchymal stem cells promote survival of T cells in a quiescent state. Stem Cells 25(7):1753–1760.  https://doi.org/10.1634/stemcells.2007-0068 CrossRefPubMedGoogle Scholar
  77. 77.
    Zhang W, Ge W, Li C, You S, Liao L, Han Q, Deng W, Zhao RC (2004) Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev 13(3):263–271.  https://doi.org/10.1089/154732804323099190 CrossRefPubMedGoogle Scholar
  78. 78.
    Kafienah W, Al-Fayez F, Hollander AP, Barker MD (2003) Inhibition of cartilage degradation: a combined tissue engineering and gene therapy approach. Arthritis Rheum 48(3):709–718.  https://doi.org/10.1002/art.10842 CrossRefPubMedGoogle Scholar
  79. 79.
    Bondeson J, Lauder S, Wainwright S, Amos N, Evans A, Hughes C, Feldmann M, Caterson B (2007) Adenoviral gene transfer of the endogenous inhibitor IkappaBalpha into human osteoarthritis synovial fibroblasts demonstrates that several matrix metalloproteinases and aggrecanases are nuclear factor-kappaB-dependent. J Rheumatol 34(3):523–533PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of OrthopaedicUniversity Clinic Aachen, RWTH Aachen University ClinicAachenGermany
  2. 2.Department of Thoracic SurgeryUniversity Clinic Aachen, RWTH Aachen University ClinicAachenGermany
  3. 3.Department of General SurgerySimmerathGermany

Personalised recommendations