Advertisement

International Orthopaedics

, Volume 42, Issue 7, pp 1755–1767 | Cite as

Effects of press-fit biphasic (collagen and HA/βTCP) scaffold with cell-based therapy on cartilage and subchondral bone repair knee defect in rabbits

  • Jacques HernigouEmail author
  • Pascale Vertongen
  • Esfandiar Chahidi
  • Theofylaktos Kyriakidis
  • Jean-Paul Dehoux
  • Magalie Crutzen
  • Sébastien Boutry
  • Lionel Larbanoix
  • Sarah Houben
  • Nathalie Gaspard
  • Dimitrios Koulalis
  • Joanne Rasschaert
Original Paper

Abstract

Introduction

Human spontaneous osteonecrosis of the knee (SPONK) is still challenging as the current treatments do not allow the production of hyaline cartilage tissue. The aim of the present study was to explore the therapeutic potential of cartilage regeneration using a new biphasic scaffold (type I collagen/hydroxyapatite) previously loaded or not with concentrated bone marrow cells.

Material and methods

Female rabbits were operated of one knee to create articular lesions of the trochlea (three holes of 4 × 4mm). The holes were left empty in the control group or were filled with the scaffold alone or the scaffold previously loaded with concentrated bone marrow cells. After two months, rabbits were sacrificed and the structure of the newly formed tissues were evaluated by macroscopic, MRI, and immunohistochemistry analyses.

Results

Macroscopic and MRI evaluation of the knees did not show differences between the three groups (p > 0.05). However, histological analysis demonstrated that a higher O’Driscoll score was obtained in the two groups treated with the scaffold, as compared to the control group (p < 0.05). The number of cells in treated area was higher in scaffold groups compared to the control group (p < 0.05). There was no difference for intensity of collagen type II between the groups (p > 0.05) but subchondral bone repair was significantly thicker in scaffold-treated groups than in the control group (1 mm for the control group vs 2.1 and 2.6 mm for scaffold groups). Furthermore, we observed that scaffolds previously loaded with concentrated bone marrow were more reabsorbed (p < 0.05).

Conclusion

The use of a biphasic scaffold previously loaded with concentrated bone marrow significantly improves cartilage lesion healing.

Keywords

Spontaneous osteonecrosis of the knee Cartilage repair Bone marrow cells Biphasic scaffold 

Notes

Funding

This work was supported by a research subvention of Novagenit Srl and a research grant of the “Société Royale Belge de Chirurgie Orthopédique et de Traumatologie” (SORBCOT).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed in the study were in accordance with the ethical standards of the institution.

Ethics approval was granted by Université libre de Bruxelles (ULB) Animal Ethics Committee (618N June 2016) and Université catholique de Louvain (UCL) Animal Ethics Committee (2016/UCL/MD/014 August 2016).

References

  1. 1.
    Karim AR, Cherian JJ, Jauregui JJ et al (2015) Osteonecrosis of the knee: review. Ann Transl Med 3:6.  https://doi.org/10.3978/j.issn.2305-5839.2014.11.13 PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Erggelet C, Endres M, Neumann K et al (2009) Formation of cartilage repair tissue in articular cartilage defects pretreated with microfracture and covered with cell-free polymer-based implants. J Orthop Res 27:1353–1360.  https://doi.org/10.1002/jor.20879 CrossRefPubMedGoogle Scholar
  3. 3.
    de Mulder ELW, Hannink G, van Kuppevelt TH et al (2014) Similar hyaline-like cartilage repair of osteochondral defects in rabbits using isotropic and anisotropic collagen scaffolds. Tissue Eng Part A 20:635–645.  https://doi.org/10.1089/ten.TEA.2013.0083 PubMedCrossRefGoogle Scholar
  4. 4.
    Buma P, Pieper JS, van Tienen T et al (2003) Cross-linked type I and type II collagenous matrices for the repair of full-thickness articular cartilage defects—a study in rabbits. Biomaterials 24:3255–3263CrossRefPubMedGoogle Scholar
  5. 5.
    Hoemann CD, Chen G, Marchand C et al (2010) Scaffold-guided subchondral bone repair: implication of neutrophils and alternatively activated arginase-1+ macrophages. Am J Sports Med 38:1845–1856.  https://doi.org/10.1177/0363546510369547 CrossRefPubMedGoogle Scholar
  6. 6.
    van der Linden MH, Saris DBF, Bulstra SK, Buma P (2013) Treatment of cartilaginous defects in the knee: recommendations from the Dutch Orthopaedic Association. Ned Tijdschr Geneeskd 157:A5719PubMedGoogle Scholar
  7. 7.
    Orth P, Rey-Rico A, Venkatesan JK et al (2014) Current perspectives in stem cell research for knee cartilage repair. Stem Cells Cloning 7:1–17.  https://doi.org/10.2147/SCCAA.S42880 PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Dai L, He Z, Zhang X et al (2014) One-step repair for cartilage defects in a rabbit model: a technique combining the perforated decalcified cortical-cancellous bone matrix scaffold with microfracture. Am J Sports Med 42:583–591.  https://doi.org/10.1177/0363546513518415 CrossRefPubMedGoogle Scholar
  9. 9.
    Pot MW, Gonzales VK, Buma P et al (2016) Improved cartilage regeneration by implantation of acellular biomaterials after bone marrow stimulation: a systematic review and meta-analysis of animal studies. PeerJ 4:e2243.  https://doi.org/10.7717/peerj.2243 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Tampieri A, Sandri M, Landi E et al (2008) Design of graded biomimetic osteochondral composite scaffolds. Biomaterials 29:3539–3546.  https://doi.org/10.1016/j.biomaterials.2008.05.008 CrossRefPubMedGoogle Scholar
  11. 11.
    Pittenger MF, Mackay AM, Beck SC et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147CrossRefPubMedGoogle Scholar
  12. 12.
    Mithoefer K, Saris DBF, Farr J et al (2011) Guidelines for the design and conduct of clinical studies in knee articular cartilage repair: International Cartilage Repair Society recommendations based on current scientific evidence and standards of clinical care. Cartilage 2:100–121.  https://doi.org/10.1177/1947603510392913 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Domayer SE, Welsch GH, Dorotka R et al (2008) MRI monitoring of cartilage repair in the knee: a review. Semin Musculoskelet Radiol 12:302–317.  https://doi.org/10.1055/s-0028-1100638 CrossRefPubMedGoogle Scholar
  14. 14.
    Bondulich MK, Guo T, Meehan C et al (2016) Tauopathy induced by low level expression of a human brain-derived tau fragment in mice is rescued by phenylbutyrate. Brain J Neurol 139:2290–2306.  https://doi.org/10.1093/brain/aww137 CrossRefGoogle Scholar
  15. 15.
    Schmitz N, Laverty S, Kraus VB, Aigner T (2010) Basic methods in histopathology of joint tissues. Osteoarthr Cartil 18(Suppl 3):S113–S116.  https://doi.org/10.1016/j.joca.2010.05.026 CrossRefPubMedGoogle Scholar
  16. 16.
    Qi Y, Zhao T, Xu K et al (2012) The restoration of full-thickness cartilage defects with mesenchymal stem cells (MSCs) loaded and cross-linked bilayer collagen scaffolds on rabbit model. Mol Biol Rep 39:1231–1237.  https://doi.org/10.1007/s11033-011-0853-8 CrossRefPubMedGoogle Scholar
  17. 17.
    O’Driscoll SW, Keeley FW, Salter RB (1986) 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. Stem Cells Cloning 68:1017–1035Google Scholar
  18. 18.
    Estes BT, Diekman BO, Gimble JM, Guilak F (2010) Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc 5:1294–1311.  https://doi.org/10.1038/nprot.2010.81 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Chevalier X (1998) Physiopathology of arthrosis. The normal cartilage. Presse Med 27:75–80PubMedGoogle Scholar
  20. 20.
    Buckwalter JA, Brown TD (2004) Joint injury, repair, and remodeling: roles in post-traumatic osteoarthritis. Clin Orthop Relat Res 423:7–16CrossRefGoogle Scholar
  21. 21.
    Lee JK, Responte DJ, Cissell DD et al (2014) Clinical translation of stem cells: insight for cartilage therapies. Crit Rev Biotechnol 34:89–100.  https://doi.org/10.3109/07388551.2013.823596 CrossRefPubMedGoogle Scholar
  22. 22.
    Beghé F, Menicagli C, Neggiani P et al (1992) Lyophilized non-denatured type-I collagen (Condress) extracted from bovine Achilles’ tendon and suitable for clinical use. Int J Tissue React 14(Suppl):11–19PubMedGoogle Scholar
  23. 23.
    Hunziker EB, Rosenberg LC (1996) Repair of partial-thickness defects in articular cartilage: cell recruitment from the synovial membrane. J Bone Joint Surg Am 78:721–733CrossRefPubMedGoogle Scholar
  24. 24.
    Clavé A, Potel J-F, Servien E et al (2016) Third-generation autologous chondrocyte implantation versus mosaicplasty for knee cartilage injury: 2-year randomized trial. J Orthop Res 34:658–665.  https://doi.org/10.1002/jor.23152 CrossRefPubMedGoogle Scholar
  25. 25.
    Aglietti P, Insall JN, Buzzi R, Deschamps G (1983) Idiopathic osteonecrosis of the knee. Aetiology, prognosis and treatment. J Bone Joint Surg Br 65:588–597CrossRefPubMedGoogle Scholar
  26. 26.
    Wei X, Messner K (1999) Maturation-dependent durability of spontaneous cartilage repair in rabbit knee joint. J Biomed Mater Res 46:539–548CrossRefPubMedGoogle Scholar
  27. 27.
    Shapiro F, Koide S, Glimcher MJ (1993) Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am 75:532–553CrossRefPubMedGoogle Scholar
  28. 28.
    Kamisan N, Naveen SV, Ahmad RE et al (2013) Chondrocyte density, proteoglycan content and gene expressions from native cartilage are species specific and not dependent on cartilage thickness: a comparative analysis between rat, rabbit and goat. BMC Vet Res 9:62.  https://doi.org/10.1186/1746-6148-9-62 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© SICOT aisbl 2018

Authors and Affiliations

  • Jacques Hernigou
    • 1
    • 2
    Email author
  • Pascale Vertongen
    • 2
  • Esfandiar Chahidi
    • 1
  • Theofylaktos Kyriakidis
    • 3
  • Jean-Paul Dehoux
    • 4
  • Magalie Crutzen
    • 4
  • Sébastien Boutry
    • 5
  • Lionel Larbanoix
    • 5
  • Sarah Houben
    • 6
  • Nathalie Gaspard
    • 2
  • Dimitrios Koulalis
    • 3
  • Joanne Rasschaert
    • 2
  1. 1.Department of Orthopaedic and Traumatology SurgeryEpiCURA HospitalHornuBelgium
  2. 2.Laboratory of Bone and Metabolic Biochemistry, Faculty of MedicineUniversité libre de BruxellesBrusselsBelgium
  3. 3.Department of Orthopaedic and Traumatology Surgery – Erasme HospitalUniversité libre de BruxellesBrusselsBelgium
  4. 4.Institute of Experimental and Clinical Research (IREC), Laboratory of Experimental Surgery and Transplantation (CHEX)Université catholique de LouvainBrusselsBelgium
  5. 5.Center for Microscopy and Molecular Imaging (CMMI)Université de Mons (UMONS)CharleroiBelgium
  6. 6.Laboratory of Histology, Neuroanatomy and Neuropathology, Faculty of MedicineUniversité libre de BruxellesBrusselsBelgium

Personalised recommendations