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Role of Matrix-Associated Autologous Chondrocyte Implantation with Spheroids in the Treatment of Large Chondral Defects in the Knee: a Systematic Review

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Role of Matrix-Associated Autologous Chondrocyte Implantation with Spheroids in the Treatment of Large Chondral Defects in the Knee: a Systematic Review International Journal of Molecular Sciences Review Role of Matrix-Associated Autologous Chondrocyte Implantation with Spheroids in the Treatment of Large Chondral Defects in the Knee: A Systematic Review Lucienne Angela Vonk 1,2 , Giulietta Roël 1, Jacques Hernigou 3,4, Christian Kaps 1 and Philippe Hernigou 5,* 1 CO.DON AG, 14513 Teltow, Germany; [email protected] (L.A.V.); [email protected] (G.R.); [email protected] (C.K.) 2 Department of Orthopaedics, University Medical Center Utrecht, Utrecht University, 3584 CX Utrecht, The Netherlands 3 Department of Orthopedic Surgery, EpiCURA Hospital, 7331 Baudour, Belgium; [email protected] 4 Laboratory of Bone and Metabolic Biochemistry, Faculty of Medecine, Université Libre de Bruxelles, 1070 Brussels, Belgium 5 Department of Orthopaedic Surgery, Faculty of Medicine, UPEC (University Paris-Est, Créteil), 94000 Créteil, France * Correspondence: [email protected] Abstract: Autologous chondrocyte implantation (ACI) is a cell therapy for the treatment of focal carti- lage defects. The ACI product that is currently approved for use in the European Union (EU) consists of spheroids of autologous matrix-associated chondrocytes. These spheroids are spherical aggregates of ex vivo expanded human autologous chondrocytes and their self-synthesized extracellular matrix. Citation: Vonk, L.A.; Roël, G.; The aim is to provide an overview of the preclinical and nonclinical studies that have been performed Hernigou, J.; Kaps, C.; Hernigou, P. to ensure reproducible quality, safety, and efficacy of the cell therapy, and to evaluate the clinical data Role of Matrix-Associated on ACI with spheroids. A systematic review was performed to include all English publications on Autologous Chondrocyte self-aggregated spheroids of chondrocytes cultured in autologous serum without other supplements. Implantation with Spheroids in the A total of 20 publications were included, 7 pre- and nonclinical and 13 clinical research publications. Treatment of Large Chondral Defects in the Knee: A Systematic Review. Int. The pre- and nonclinical research publications describe the development from concept to in vivo effi- J. Mol. Sci. 2021, 22, 7149. https:// cacy and quality- and safety-related aspects such as biodistribution, tumorigenicity, genetic stability, doi.org/10.3390/ijms22137149 and potency. The evaluation of clinical research shows short- to mid-term safety and efficacy for the ACI with spheroid-based treatment of cartilage defects in both randomized clinical trials with Academic Editor: Marcus Jäger selected patients, as well as in routine treatment providing real-world data in more complex patients. Received: 8 June 2021 Keywords: autologous chondrocyte implantation; spheroids; Spherox; cartilage defects; advanced Accepted: 29 June 2021 therapy medicinal product; preclinical research Published: 1 July 2021 Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- Articular cartilage is the cartilage that covers the end of bones in synovial joints. iations. It provides a smooth surface for the movement of articulating bones, and it allows to withstand compressive and shear forces. This cartilage is hyaline cartilage that contains only a small number of cells, chondrocytes (<10%), and the extracellular matrix is composed of collagens, mainly type II collagen, and glycosaminoglycan containing proteoglycans. It Copyright: © 2021 by the authors. has no blood supply and is not innervated by nerves or lymphatic vessels [1]. Licensee MDPI, Basel, Switzerland. Focal cartilage defects can cause symptoms such as pain, swelling, stiffness, giving This article is an open access article way, or locking of the knee affecting quality of life. As cartilage has a very limited ability distributed under the terms and to repair itself, these defects require surgical treatment. Moreover, if cartilage defects conditions of the Creative Commons Attribution (CC BY) license (https:// are left untreated, the damage progresses leading to osteoarthritis [2]. Osteoarthritis is creativecommons.org/licenses/by/ a whole-joint disease characterized by progressive cartilage and meniscus degradation, 4.0/). synovitis, the formation of osteophytes, and thickening of the subchondral bone [3,4]. Int. J. Mol. Sci. 2021, 22, 7149. https://doi.org/10.3390/ijms22137149 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 17 whole-joint disease characterized by progressive cartilage and meniscus degradation, synovitis, the formation of osteophytes, and thickening of the subchondral bone [3,4]. Autologous chondrocyte implantation (ACI) is a cell therapy that is used for the treat- ment of medium to larger sized (>2 cm2) focal cartilage defects. ACI has been used for over Int. J. Mol. Sci. 2021, 22, 7149 30 years and it provides good to satisfactory results and it is a well proven treatment2 of 17 with level 1 evidence [5,6]. ACI is a two-step procedure. In a first surgery, a biopsy of healthy cartilage from a non-weight bearing site of the cartilage is taken. Subsequently, chondro- cytes are isolated from the biopsy and culture expanded. In a second surgery, the culture- Autologous chondrocyte implantation (ACI) is a cell therapy that is used for the expanded autologous chondrocytes are implanted in the cartilage defect. By implanting treatment of medium to larger sized (>2 cm2) focal cartilage defects. ACI has been used for over 30chondrocytes years and it directly provides into good the to defect, satisfactory the defect results will and be itfilled is a wellwith proven new hyaline treatment cartilage with leveltissue. 1 evidence [5,6]. ACI is a two-step procedure. In a first surgery, a biopsy of healthy cartilageRegulatory from wise, a non-weight ACI is an bearingadvanced site therapy of the cartilagemedicinal is product taken. Subsequently,(ATMP). Thus, ex- chondrocytestensive preclinical, are isolated nonclinical, from the biopsyand clinical and studies culture need expanded. to be performed In a second to ensure surgery, repro- the culture-expandedducible quality, safety autologous, and efficacy chondrocytes of the cell are therapy. implanted Currently, in the cartilage Spherox defect. (CO.DON By AG, implantingTeltow, chondrocytes Germany) is directly approved into for the the defect, repair the of defectsymptomatic will be filledarticular with cartilage new hyaline defects of cartilagethe tissue.femoral condyle and the patella of the knee (International Cartilage Repair Society Regulatory(ICRS) grade wise, III or ACI IV) with is an defect advanced sizes up therapy to 10 cm medicinal2 in adults product in the EU. (ATMP). Spherox Thus, has been extensiveused preclinical,under the name nonclinical, chondrosphere and clinical since studies2004 in Germany need to be and performed changed to to Spherox ensure after reproducibleobtaining quality, the EU safety,-wide andmarketing efficacy authorization. of the cell therapy. Chondrosphere Currently, Spheroxis currently (CO.DON still used in AG, Teltow,Germany Germany) for joints is other approved than forthe the knee. repair Spherox of symptomatic contains spheroids articular of cartilage autologous defects matrix- of theassociated femoral condyle chondrocytes. and the The patella spheroids of the kneeare spherical (International aggregates Cartilage of ex Repair vivo expanded Society hu- (ICRS)man grade autologous III or IV) chondrocytes with defect sizes and up their to 10self cm-synthesized2 in adults inextracellular the EU. Spherox matrix. has The been novelty used underof this theACI name with chondrospherespheroids is that since both 2004 the cell in Germany culture and and the changed implantation to Spherox of the after ACI are obtainingfully theautologous EU-wide (Figure marketing 1). The authorization. cell cultures Chondrosphere are performed with is currently autologous still usedserum in with- Germanyout other for joints supplements other than such the knee.as growth Spherox factors, contains cytokines spheroids, and/ ofor autologousantibiotics. matrix-In addition, associatedthe spheroids chondrocytes. are self The-adhesive spheroids to the are subchondral spherical aggregates bone and therefore, of ex vivo the expanded implantation humandoes autologous not require chondrocytes any sutures, andmembranes, their self-synthesized covers, or glue extracellular[7]. matrix. The novelty ofThe this purpose ACI with of spheroidsthis review is is that to bothsystematically the cell culture evaluate and the the available implantation literature of on the ACIfully are autologous fully autologous ACI with (Figure spheroids.1). The cellAs such, cultures an areoverview performed of the with available autologous preclinical serumand without nonclinical other data supplements is provided, such covering as growth required factors, quality cytokines, aspect and/ors related antibiotics. to the manu- In addition,facturing the process. spheroids Furthermore, are self-adhesive the clinical to the data subchondral on the use of bone ACI and with therefore, spheroids the for the implantationtreatment does of cartilage not require defects any sutures,in the knee membranes, are documented covers, and or glue analyzed. [7]. Figure 1. For the manufacturing of ACI with spheroids, autologous chondrocytes are culture ex- panded and subsequently cultured as spheroids using culture medium supplemented with only autologous serum and without other supplements such as growth factors, cytokines, and or antibi-
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