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Mesenchymal Stem Cells: Potential Role in the Treatment of Osteochondral Lesions of the Ankle

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Mesenchymal Stem Cells: Potential Role in the Treatment of Osteochondral Lesions of the Ankle REVIEW Cartilage Tissue Engineering www.biotechnology-journal.com Mesenchymal Stem Cells: Potential Role in the Treatment of Osteochondral Lesions of the Ankle Howard C. Tribe, Josephine McEwan, Heath Taylor, Richard O. C. Oreffo, and Rahul S. Tare* 1. Introduction Given articular cartilage has a limited repair potential, untreated osteochon- Hyaline articular cartilage (AC) covers the dral lesions of the ankle can lead to debilitating symptoms and joint ends of articulating bones and its unique deterioration necessitating joint replacement. While a wide range of repara- biomechanical characteristics reduce fric- tive and restorative surgical techniques have been developed to treat tion during bone movement by facilitating osteochondral lesions of the ankle, there is no consensus in the literature adsorption of mechanical load. This com- regarding which is the ideal treatment. Tissue engineering strategies, plex tissue is avascular, aneural, alym- encompassing stem cells, somatic cells, biomaterials, and stimulatory signals phatic, and is sparsely populated with chondrocytes that procure nutrients from (biological and mechanical), have a potentially valuable role in the treatment the synovial fluid solely via diffusion. These of osteochondral lesions. Mesenchymal stem cells (MSCs) are an attractive biological characteristics severely limit the resource for regenerative medicine approaches, given their ability to self- ability of AC to self-repair. Due to the renew and differentiate into multiple stromal cell types, including chondro- limited potential for self-repair, defects in cytes. Although MSCs have demonstrated significant promise in in vitro and AC caused by acute trauma or as a consequence of more chronic pathologies, in vivo preclinical studies, their success in treating osteochondral lesions of such as osteoarthritis (OA), osteonecrosis, the ankle is inconsistent, necessitating further clinical trials to validate their and osteochondritis dissecans, may lead to application. This review highlights the role of MSCs in cartilage regeneration gradual cartilage deterioration and loss. and how the application of biomaterials and stimulatory signals can enhance The deterioration of AC has been [1] chondrogenesis. The current treatments for osteochondral lesions of the recognized since the time of Hippocrates ankle using regenerative medicine strategies are reviewed to provide a clinical and the clinical symptoms of pain, swell- ing, and loss of function are well docu- context. The challenges for cartilage regeneration, along with potential mented.[2] With an increasing aging solutions and safety concerns are also discussed. population, there is a high incidence of AC disorders, and the physical, psycholog- ical, and socio-economic burden to patients [3] H. C. Tribe, J. McEwan, Prof. R. O. C. Oreffo, Dr. R. S. Tare, Bone and and society is considerable. Over the years, a number of Joint Research Group different surgical as well as non-surgical strategies have been Centre for Human Development developed to treat the symptoms of articular joint deterioration, Stem Cells and Regeneration but, to date, none have been able to show the long-term Faculty of Medicine University of Southampton restoration of innate joint function that patients require. The Southampton SO16 6YD, UK inadequacy of current treatments has encouraged the prolifera- E-mail: [email protected] tion of technologies that aim to regenerate the native cartilage H. C. Tribe, H. Taylor tissue. Foot and Ankle Orthopaedic Department The discipline of regenerative medicine is defined as a Royal Bournemouth Hospital scientific field that replaces or regenerates human cells, tissue, Bournemouth BH7 7DW, UK or organs to restore or establish normal function.[4] Regenera- Dr. R. S. Tare tion of articular cartilage refers to the restoration of the articular Bioengineering Science, Mechanical Engineering Department, Faculty of Engineering and the Environment surface and mechanical integrity in order to improve function, University of Southampton reduce pain, and prevent end-stage joint degeneration. Since Southampton SO17 1BJ, UK their inception, cartilage regenerative strategies have focused © 2017 The Authors. Biotechnology Journal Published by Wiley- primarily on the knee joint, but the ankle is also a suitable VCHVerlag GmbH & Co. KGaA. This is an open access article under the target. The incidence of ankle injuries has been recorded at 107 terms of the Creative Commons Attribution License, which permits use, fractures per 105 person-years[5] and up to 61% of fractures distribution and reproduction in any medium, provided the original damage the articular surface of the ankle.[6] Damage to the work is properly cited. articular cartilage surface results in a chondral lesion that, if left DOI: 10.1002/biot.201700070 untreated, can progress deeper and affect the underlying bone, Biotechnol. J. 2017, 12, 1700070 1700070 (1 of 10) © 2017 The Authors. Biotechnology Journal Published by Wiley-VCHVerlag GmbH & Co. KGaA www.advancedsciencenews.com www.biotechnology-journal.com contributing to the development of an osteochondral lesion. The technical challenges of treating articular cartilage lesions in Howard Tribe is currently a PhD the ankle joints compared to articular cartilage lesions in the student investigating cartilage knee joints include the difficulty in accessing all areas of the regeneration. His focus is on a ankle joint, smaller size, and the lack of non-weight bearing specific population of skeletal stem cartilage that can be utilized for regeneration strategies. cells and comparing their Chondrocytes have been used to treat AC lesions for the last chondrogenic ability with human few decades using the technique of autologous chondrocyte articular chondrocytes. Before he implantation (ACI).[7] The third generation of the technique started his PhD, he was training as an involves taking a cartilage biopsy, culture-expanding the orthopaedic surgeon within the south chondrocytes, seeding the chondrocytes onto a collagen type- of the U.K. His specialist interest is I/III scaffold, and subsequently implanting the cellularized foot and ankle pathology. He completed his medical scaffold into the cartilage lesion (Figure 1). The technique has training at Imperial College London, U.K., where he also been shown to have favorable long-term results when treating completed a Bachelor’s degree in Pharmacology and cartilage lesions in the ankle[8] but a meta-analysis in 2012 found Toxicology. Since graduation, he has completed a Master insufficient evidence to support ACI over the simple and of Education degree in Surgical Education from Imperial inexpensive technique of bone marrow stimulation.[9] Further- College London, U.K. more, the two-step procedure of ACI doubles the surgical risk to Richard Oreffo holds the chair of Musculoskeletal Science and is co- founder and Director of the Centre for Human Development, Stem Cells and Regeneration. He leads the Bone and Joint Research Group, a large multidisciplinary research group focused on developing strategies to repair bone & cartilage and understanding bone development; including the role of epigenetics in musculoskeletal diseases with translation a key personal driver. To achieve these goals, he has brought together and developed teams of clinicians and life scientists over the last twenty years. He has published over 250 peer-reviewed papers, including breakthrough publications on skeletal stem cells and nanotopography, bone regeneration as well as epigenetics in Osteoarthritis, in Nature Materials, ACS Nano, Stem Cells, Arthritis and Rheumatism. In 2017, he founded and is CSO of Renovos Biologics Limited, a spin- out from the University of Southampton. Rahul Tare is a Lecturer in Musculoskeletal Science and Bioengineering in the University of Southampton. He leads an interdisciplinary research group in the Centre for Human Development, Stem Cells and Regeneration that harnesses innovative approaches encompassing human stem cells, tissue engineering and acoustofluidics to generate 3-D cartilage grafts for the regeneration of articular cartilage Figure 1. An illustration of third-generation autologous chondrocyte defects, and seeks to gain insight into the development of implantation for the repair of a chondral lesion in the ankle. 1) During the first operation, a cartilage biopsy is taken from areas of damaged cartilage skeletal diseases such as osteoporosis and osteoarthritis within the ankle or from the ipsilateral knee. 2) Chondrocytes are isolated through improved appreciation of the molecular regulation of from the biopsied cartilage via enzymatic digestion and cultured in 2-D skeletal development. Rahul has published 40 peer-reviewed monolayer cultures. 3) Monolayer culture-expanded chondrocytes are papers and contributed to 5 book chapters, to date, on stem seeded on to a collagen types I–III membrane. 4) In the second operation, cells, skeletal tissue engineering and bone development. the cartilage lesion is prepared and the collagen membrane is then cut to size, placed in the lesion, and secured with fibrin glue. Biotechnol. J. 2017, 12, 1700070 1700070 (2 of 10) © 2017 The Authors. Biotechnology Journal Published by Wiley-VCHVerlag GmbH & Co. KGaA www.advancedsciencenews.com www.biotechnology-journal.com the patient, thus, chondrocytes may have to be harvested from however, ethical concerns related to the harvesting of human the uninjured ipsilateral knee and the problems of culture- ESCs and the risk of teratoma
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