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Intra-Articular Implantation of Collagen Scaffold Carriers Is Safe in Both Native and Arthrofibrotic Rabbit Knee Joints

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Intra-Articular Implantation of Collagen Scaffold Carriers Is Safe in Both Native and Arthrofibrotic Rabbit Knee Joints 62.BJRBJR0010.1302/2046-3758.62.BJR-2016-0193 research-article2017 Freely available online OPEN ACCESS BJR RESEARCH Intra-articular implantation of collagen scaffold carriers is safe in both native and arthrofibrotic rabbit knee joints J. A. Walker, Objectives T. J. Ewald, Sustained intra-articular delivery of pharmacological agents is an attractive modality but requires E. Lewallen, use of a safe carrier that would not induce cartilage damage or fibrosis. Collagen scaffolds are A. Van Wijnen, widely available and could be used intra-articularly, but no investigation has looked at the safety A. D. Hanssen, of collagen scaffolds within synovial joints. The aim of this study was to determine the safety of B. F. Morrey, collagen scaffold implantation in a validated in vivo animal model of knee arthrofibrosis. M. E. Morrey, Materials and Methods M. P. Abdel, A total of 96 rabbits were randomly and equally assigned to four different groups: arthrot- J. Sanchez-Sotelo omy alone; arthrotomy and collagen scaffold placement; contracture surgery; and contrac- ture surgery and collagen scaffold placement. Animals were killed in equal numbers at 72 Mayo Clinic, hours, two weeks, eight weeks, and 24 weeks. Joint contracture was measured, and cartilage Rochester, Minnesota, and synovial samples underwent histological analysis. United States Results Animals that underwent arthrotomy had equivalent joint contractures regardless of scaffold implantation (-13.9° versus -10.9°, equivalence limit 15°). Animals that underwent surgery to J. A. Walker, MD, Consultant, induce contracture did not demonstrate equivalent joint contractures with (41.8°) or without Department of Orthopaedic Surgery, (53.9°) collagen scaffold implantation. Chondral damage occurred in similar rates with (11 of 48) T. J. Ewald, MD, Consultant, and without (nine of 48) scaffold implantation. No significant difference in synovitis was noted Department of Orthopaedic between groups. Absorption of the collagen scaffold occurred within eight weeks in all animals Surgery, E. Lewallen, PhD, Research Conclusion Associate, Orthopedic Surgery, A. Van Wijnen, PhD, Professor, Our data suggest that intra-articular implantation of a collagen sponge does not induce Orthopedic Surgery, synovitis or cartilage damage. Implantation in a native joint does not seem to induce con- A. D. Hanssen, MD, Professor, tracture. Implantation of the collagen sponge in a rabbit knee model of contracture may Department of Orthopedic Surgery, decrease the severity of the contracture. B. F. Morrey, MD, Professor, Department of Orthopedic Cite this article: Bone Joint Res 2016;6:162–171 Surgery, M. E. Morrey, MD, Associate Keywords: Collagen scaffold, Arthrofibrosis, Knee joint, Biocompatibility, Biodegradation Professor, Department of Orthopedic Surgery, cartilage damage or fibrosis with contrac- M. P. Abdel, MD, Associate Article focus Professor, Department of A total of 96 rabbits were randomly allo- ture in the rabbit joint. Orthopedic Surgery, cated to four experimental groups: All collagen sponges were resorbed in J. Sanchez-Sotelo, MD, Associate Professor, Department of arthrotomy alone; arthrotomy and colla- this model by eight weeks. Orthopedic Surgery, Mayo Clinic, gen scaffold placement; contracture sur- Collagen sponges may be considered a 200 First Street SW, Rochester, MN gery; and contracture surgery and safe carrier for intra-articular administra- 55905, USA. collagen scaffold placement. tion of pharmacological agents. Correspondence should be sent to Animals were killed at 72 hours and two, J. Sanchez-Sotelo; Strength and limitations e-mail: sanchezsotelo.joaquin@ eight and 24 weeks. Strengths: large sample size, four study mayo.edu Joint contracture, chondral damage and groups, multiple time points, validated doi: 10.1302/2046-3758.63.BJR- synovitis were assessed. 2016-0193 scales for grading. Key messages Limitations: assessment of chondral dam- Bone Joint Res 2017;6:162–171. Received: 27 July 2016; Intra-articular implantation of a collagen age was difficult due to artefacts at the Accepted: 20 October 2016 sponge does not induce synovitis, time of sectioning. VOL. 6, NO. 3, MARCH 2017 162 163 Intra-artICULAR IMPLANTATION OF COLLAGEN SCAFFOLD CARRIERS IS SAFE IN BOTH NATIVE AND ARTHROFIBROTIC RABBIT KNEE JOINTS Introduction We hypothesised that a collagen scaffold could be Arthrofibrosis, or fibrosis of the tissues around synovial placed in an intra-articular location in the rabbit knee, joints, remains a difficult clinical problem in orthopae- without causing alteration of joint range of movement dics, despite numerous treatment modalities.1,2,3 In order (ROM), significant cartilage damage, or synovial inflam- to study the pathophysiology behind arthrofibrosis, ani- matory reaction, as assessed by mechanical and histolog- mal models have been developed using the New Zealand ical analysis. Secondly, we hypothesised that intra-articular White rabbit knee.4,5 These models involve an intracapsu- placement of a collagen scaffold in a rabbit model of lar knee injury followed by Kirschner-wire (K-wire) immo- arthrofibrosis would not alter the expected joint contrac- bilisation for eight weeks, and result in substantial ture, nor cause damage to the articular cartilage, nor cre- contracture that resembles the human biomechanical, ate a synovial inflammatory reaction, as assessed by cellular, and molecular response to injury, with increased mechanical and histological analysis. Thirdly, we hypoth- myofibroblasts and transforming growth factor beta esised that collagen scaffold absorption would occur (TGF-β) activity.6-12 within eight weeks. Previous studies have demonstrated significant upregulation of myofibroblasts early in the process of Materials and Methods joint contracture (within two weeks of injury),12 as well After obtaining approval from our departmental Review as notable changes in messenger ribonucleic acid Board and Institutional Animal Care and Use Committee, (mRNA) expression within the first 72 hours of injury. 102 skeletally mature female New Zealand White rabbits Furthermore, microarray analysis of mRNA has demon- (using the same gender rabbits increased likelihood of strated that the most notable changes in mRNA expres- homogeneity), were randomly and equally divided into sion in capsular tissues occurred within the first 24 to four study groups: sham arthrotomy (SA); collagen scaf- 72 hours after injury.13,14 Other studies have suggested fold arthrotomy (CSA); sham Mayo contracture model the possible influence of mast cells on the development (MCM); and collagen scaffold Mayo contracture model of arthrofibrosis in the four weeks after injury.11 The (CMCM), with six animals assigned as non-operative his- early onset of changes, both on the cellular and molec- tological controls (Fig. 1). National Institutes of Health ular level, seems to indicate the need for early interven- guidelines for the care and use of laboratory animals tion to prevent or abort the development of were observed at all times. Rabbits in the arthrotomy arthrofibrosis. Using these animal models, attempts to groups underwent an arthrotomy, as described below. find an effective anti-fibrosis medication are underway. Rabbits assigned to the arthrofibrosis model underwent Ketotifen, a mast cell stabiliser, has already shown some the same initial procedure to develop a contracture as promise in reducing contracture severity in a rabbit described in previous studies and briefly outlined model.15 Decorin, while demonstrating change in the below.5,12-14,33 Collagen scaffolds used in this study were local mRNA expression, did not affect the overall degree commercially available collagen sponges, derived from of contracture.13 purified bovine tendon, currently used in dental applica- If administration of a pharmacological agent is proven tions. These scaffolds are pre-sterilised, eliminating the to be effective in the prevention or treatment of joint con- need for sterilisation. The sterile scaffolds were fashioned tracture, the route of administration becomes critical. into 1 cm × 1 cm implants prior to implantation. Systemic administration may lead to unpredictable phar- Initial procedure – arthrotomy (groups SA and CSA). Under macological levels at the joint, and could be associated appropriate inhalational anaesthesia, a lateral parapatel- with side effects. Local intra-articular administration is lar arthrotomy was completed on the right knee. Of the very appealing, but would require the use of a carrier for 48 rabbits assigned to the arthrotomy cohort, 24 under- sustained administration and release. However, intra- went placement of a 1 cm × 1 cm collagen scaffold (CSA), articular implantation of a carrier could potentially have whereas 24 underwent arthrotomy alone (SA). The scaf- adverse effects, such as cartilage damage, an inflamma- fold was placed in the medial recess of the suprapatel- tory synovial response, or fibrosis. lar pouch, taking care not to trap the sponge within the Collagen, a naturally occurring polymer, presents an patellofemoral articulation. The arthrotomy and wound attractive option for intra-articular drug delivery. were then closed with absorbable sutures. All animals Currently, collagen scaffolds are clinically employed for in the arthrotomy cohort were allowed free cage activity (or under investigation for use in) ophthalmologic appli- (0.19 m3) following the operation. cations,16 local antibiotic delivery,17-24 local wound Initial procedure – arthrofibrosis (groups MCM
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