The fixation of a collagen type I/III membrane in the distal radioulnar joint of a human cadaver model

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1 WRIST AND HAND The fixation of a collagen type I/III membrane in the distal radioulnar joint of a human cadaver model E. A. van Amerongen, L. B. Creemers, N. Kaoui, J. E. J. Bekkers, M. Kon, A. H. Schuurman From University Medical Center Utrecht, Department of Plastic, Reconstructive and Hand Surgery, Utrecht, The Netherlands Damage to the cartilage of the distal radioulnar joint frequently leads to pain and limitation of movement, therefore repair of this joint cartilage would be highly desirable. The purpose of this study was to investigate the fixation of scaffold in cartilage defects of this joint as part of matrix-assisted regenerative autologous cartilage techniques. Two techniques of fixation of collagen scaffolds, one involving fibrin glue alone and one with fibrin glue and sutures, were compared in artificially created cartilage defects of the distal radioulnar joint in a human cadaver. After being subjected to continuous passive rotation, the methods of fixation were evaluated for cover of the defect and pull out force. No statistically significant differences were found between the two techniques for either cover of the defect or integrity of the scaffold. However, a significantly increased mean pull out force was found for the combined procedure, N (0.150 to 1.160) versus N (0.060 to 0.730) for glue fixation (p = 0.001). This suggests that although successful fixation of a collagen type I/III scaffold in a distal radioulnar joint cartilage defect is feasible with both forms of fixation, fixation with glue and sutures is preferable. Cite this article: Bone Joint J 2014;96-B: E. A. van Amerongen, MD, Resident plastic surgery Utrecht, Department of Plastic, Reconstructive and Hand surgery, P. O. Box 85500, 3508 GA, The Netherlands. L. B. Creemers, PhD, Associate Professor J. E. J. Bekkers, MD, PhD, Resident Orthopaedic Surgery Utrecht, Department of Orthopaedic surgery, P. O. Box 85500, 3508 GA, The Netherlands. N. Kaoui, MD, Resident M. Kon, MD, PhD, Professor Plastic surgery, Head of the Department of Plastic Surgery A. H. Schuurman, MD, PhD, Plastic Surgeon, Chair of the Department of Plastic Surgery Utrecht, Department of Plastic, Reconstructive and Hand Surgery, P. O. Box 85500, 3508 GA, The Netherlands. Correspondence should be sent to Ms E. A. van Amerongen; The British Editorial Society of Bone & Joint Surgery doi: / x.96b $2.00 Bone Joint J 2014;96B: Received 12 August 2013; Accepted after revision 21 January 2014 The distal radioulnar joint (DRUJ) is an important structure in the combined function of the forearm, wrist and hand through rotational and translational movement. 1,2 Damage to the articular surfaces of the joint frequently leads to pain and a reduced range of movement. Persistent symptoms after failed conservative treatment can result in the need for joint replacement or arthrodesis of the wrist. 3,4 Avoidance of these radical procedures by restoration of the cartilage of the DRUJ would be highly desirable, especially for young and active patients and athletes. 5 The treatment of articular cartilage damage in the knee was successfully achieved in 1994 by autologous chondrocyte implantation (ACI) 6 and good results have subsequently been described for matrix-assisted autologous chondrocyte implantation (MACI) MACI requires the harvesting and digesting of fullthickness cartilage to obtain chondrocytes. After expansion and seeding the chondrocytes onto a three-dimensional biodegradable scaffold, it is implanted into the defect. 12 We studied the feasibility of using a MACI scaffold in the DRUJ. The success of this form of treatment depends upon obtaining adequate fixation of the scaffold. Two studies have dealt with fixation of the scaffold in the knee joint 13,14 and one in bovine patellae. 15 Various methods of fixation are currently available including sutures and fibrin glue, and more recently biodegradable pins and transosseous fixation, or a combination of these techniques The choice of technique depends on the nature of the scaffold and the type of joint. Fibrin glue is typically used for MACI scaffold fixation. 9,19,20 Due to the convex-shaped articulating surface of the ulnar head 1 and the combination of rotational and translational forces on the DRUJ joint, we speculated that the addition of glue to two cartilage sutures on both sides of the scaffold would strengthen its fixation and protect it from shear forces. The purpose of this study was to determine the feasibility of fixation of a scaffold into a cartilage defect of the DRUJ by comparing fibrin glue and fibrin glue combined with sutures in the upper limbs of human cadavers. Patients and Methods A total of 20 human fresh-frozen cadaver arms were obtained from the Department of Anatomy according to local ethical and practical guidelines. Only cadaver arms were included that were clinically stable at the DRUJ, free of visible scarring over the joint and could be rotated at least 508 THE BONE & JOINT JOURNAL

2 THE FIXATION OF A COLLAGEN TYPE I/III MEMBRANE IN THE DISTAL RADIOULNAR JOINT OF A HUMAN CADAVER MODEL 509 Fig. 1a Fig. 1b Fig. 1c Fig. 1d Fig. 1e Fig. 1f Clinical photographs showing a) a longitudinal midline incision on dorsal side of the wrist, b) opening of the fifth extension compartment and retraction of the extensor digiti quinti tendon, c) opening of the dorsal joint capsule through an ulnar-based flap, d) creation of a standardised circumferential cartilage defect, e) fixation of the membrane with fibrin glue and f) fixation of the membrane with fibrin glue and sutures (sutures are marked with arrows). to 45 pronation and 45 supination from an anatomically neutral position. The arms had been sectioned at the midhumerus and all cadavers were thawed to room temperature. A longitudinal incision was made across the dorsum of the wrist and the fifth extensor compartment was opened and the tendon of the extensor digiti quinti muscle was retracted to the ulnar side. The dorsal DRUJ capsule was opened through an ulnar-based flap as described by Garcia- Elias and Hagert 21 in such a way that closure of the capsule remained possible. The complete surface of the ulnar head could be seen following rotation of the forearm. A standardised cartilage defect (width 2.5 mm; depth 1 mm; length 14 mm) was made circumferentially on the ulnar head using a surgical knife and a custom-made rotary burr, mimicking a clinically relevant traumatic groove. A collagen type I/III ACI-Maix collagen membrane (Matricel VOL. 96-B, No. 4, APRIL 2014

3 510 E. A. VAN AMERONGEN, L. B. CREEMERS, N. KAOUI, J. E. J. BEKKERS, M. KON, A. H. SCHUURMAN Fig. 2 Clinical photograph showing the custom-made continuous passive movement (CPM) device for rotation of the forearm. Fig. 3a GmbH, Herzogenrath, Germany) without seeded chondrocytes was cut to the exact size of the defect in the cartilage. The wrists were randomly assigned to the two fixation techniques. For ten, fibrin glue (Tissucol duo 500, Baxter AG, Vienna, Austria) alone was used and for ten it was combined with two atraumatic Vicryl 6.0 sutures (Ethicon, Johnson and Johnson, New Brunswick, New Jersey), which were placed on each side of the defect with the knot placed on the membrane (Fig. 1). A thin layer of fibrin glue was then applied under the membrane. The process of polymerisation and the application of the glue was similar for all 20 wrists. The fibrin glue was warmed in water (37 C) prior to application. It was applied after heating the joint with a continuous warm air flow using a drying engine for five minutes to simulate body temperature. Subsequently the glue achieved sufficient polymerisation in warm air for ten minutes, simulating body temperature. During the whole procedure, dehydration of the operating field was prevented by continuous local moisturisation using saline. The capsule and skin were then closed. After fixation of the scaffold, the arms were secured onto a custom-made continuous passive movement (CPM) device, which had been designed to rotate the forearm (Fig. 2). The upper arm was fixed to the rotating panel in an upright position, with the elbow flexed to 90 and the wrist in the neutral position. One rotational movement cycle of the forearm and hand began in the neutral position, went to 45 supination and 45 pronation and returned to neutral. Each cycle lasted three seconds. The wrists were opened after ten cycles and the cover of the defect was photographed and evaluated. The capsule and skin were closed again and re-opened after a further 100 cycles. Again, the fixation was photographed and evaluated. Completion of the motion protocol implied a total of 110 cycles for each arm. The fixation was scored on the cover of the defect by the scaffold at the time of ten and then a further 100 cycles. The area of cover was visually evaluated by two independent observers (EAvA, NK) with the consensus recorded. The area was expressed as the percentage of the defect that was Fig. 3b Fig. 3c Clinical photographs showing a) 100% cover, b) 75% cover and c) 25% cover. covered on a scale of 0% to 100% and outlined per 5% (Fig. 3). Cover of < 50% was considered a failure. The integrity of the scaffold was inspected for fissures and tears. The force required to pull the scaffold out was then measured in Newtons (N), by gradually pulling it out using increasing weights in steps of 0.01 N. A non-absorbable suture was attached to the scaffold. This suture was led over a pulley block and weights were attached until the scaffold became detached. Any damage to the cartilage, sutures and scaffold was recorded. THE BONE & JOINT JOURNAL

4 THE FIXATION OF A COLLAGEN TYPE I/III MEMBRANE IN THE DISTAL RADIOULNAR JOINT OF A HUMAN CADAVER MODEL 511 Statistical analysis. Baseline data were equally distributed between groups. The data for the area that was covered and the endpoint fixation data were presented in mean values with range. As there is no previous data available, a power study was not performed. Fisher s exact test was used for categorical data and Student s t-test for normally distributed quantitative data. The non-parametric Mann Whitney U test was used for skewed data. Statistical analyses were carried out with SPSS version (SPSS Inc., Chicago, Illinois). All comparisons were two-sided at an alpha level of < Results The mean age of the donors was 76.9 years (59 to 93) for the DRUJs, in which only fibrin glue was used and 71.5 years (53 to 85) for those with combined fibrin glue and sutures. The male to female ratio was 7:3 for glue fixation and 6:4 for the combination. The depth and width of the defect was 1.0 mm and 2.5 mm, respectively. The mean length of the defect was similar in the two groups, being 14.6 mm (14 to 16) for glue fixation alone and 14.3 mm (12 to 16) for glue and sutures fixation, which were not significant (p = 0.540; Student s t-test). As only the effect of glue and/or sutures was tested, it was not expected that the suture pull-out resistance would be affected by the age of the cadavers. After ten cycles, the mean area that was covered was 93% (75% to 100%) for glue alone and 95% (80% to 100%) for the combined fixation. After the additional 100 cycles, the mean area that was covered was 88% (25% to 100%) and 95% (80% to 100%), respectively. These differences were not significant (both, p = 0.631; Mann Whitney U test). In one defect within which the scaffold was attached with glue only, the area was 25% after the 110 cycles. None of the fixation procedures led to a full detachment of the scaffolds and no scaffold was damaged upon completion of the CPM protocol, at which point the mean pull-out force of the scaffold was significantly lower in those fixed with glue alone (0.242 N [0.060 to 0.730] vs N [0.150 to 1.160] (p = 0.001; Student s t-test) (Fig. 3). Discussion Successful fixation of a collagen type I/III membrane, as used for MACI, was found to be feasible in cartilage defects of the DRUJ. Although the area of the defect that was covered was slightly larger when fixation was performed with glue combined with sutures than with glue alone, the difference was not significant (p = 0.631). An additional 100 cycles of testing did not further affect the area that was covered. However, fixation measured by pull-out force was significantly better when glue and sutures were combined. Increasing the number of cadavers and hence data would possibly have led to a statistically significant difference between these groups. However, commonly cadaver studies are based on similar numbers 13,14 due to their limited availability. Several different scaffolds are currently available for MACI of natural or synthetic origin 14,22 and there is an extensive choice of shape, form and biomechanical properties. Being a distinctly different joint from the knee, specific features of the DRUJ are likely to affect the choice of scaffold and type of fixation. From a surgical point of view, it requires specific characteristics for implantation into the small convex ulnar head. It should be pliable and withstand shear forces with a minimal amount of axial loading. Self-adhesive gel-like matrix materials may be less resistant to shear forces exerted by rotation and translation during DRUJ movement and therefore these materials may be less suitable for a convex-shaped defect. 15 In contrast, a thin collagen type I/III membrane is pliable 23 and can be easily shaped during surgery, particularly fitting for the convex-shaped thin articulating surface of the ulnar head. 1 These favourable features, as well as extensive clinical experience with the type I/III collagen scaffolds, 12 make it suitable to work with the specific anatomy and biomechanics of the DRUJ. Previous studies on fixation of the scaffold have focused on both the human cadaveric knee joint 13,14 and bovine patellae. 15 The fixation (maximal tensile load) of the collagen membranes in bovine patellae was significantly stronger with sutures than with fibrin glue. A study on human cadaveric knee joints evaluating four types of fixation with a copolymer printed scaffold 13 also showed that sutures provided better attachment than glue. Central point fixation using a biodegradable pin and transosseous fixation provided even stronger fixation than suturing. However, fixation by sutures, pin or using a transosseous technique caused more damage to the edges of the scaffold than glue. In another study on human cadaveric knee joints, the fixation of a collagen fleece using four different techniques including self-adhesion, fibrin glue, bone transosseous sutures and periosteal cover (transchondral) sutures, 14 were tested. Similar to the previously mentioned study, 13 stronger fixation was effected by bone sutures and periosteal cover sutures over glue. The sutures were even stronger but caused more deformities of the scaffold. None of these studies tried to combine different methods of fixation. In this study we attempted to overcome these drawbacks by combining techniques of fixation. As transosseous fixation or transchondral sutures were shown to cause more damage to the scaffolds during joint movement, 13 central point fixation by transosseous sutures or pin fixation in our model was technically not feasible, due to the small size of the defect. Transchondral suturing can be easily performed for the DRUJ. In our model, applying glue was straightforward and it is generally used for MACI, yet a common assumption is that it provides weaker fixation of the scaffold. By combining sutures with glue, we have attempted to combine the advantages of both methods of fixation. Although previous studies yielded similar results with respect to the choice of method of fixation on the pull-out force, a direct comparison cannot be made due to the difference in scaffolds, the type of joint and the size and shape of the defect. In addition, it should be noted that although the test system which was used represents a common VOL. 96-B, No. 4, APRIL 2014

5 512 E. A. VAN AMERONGEN, L. B. CREEMERS, N. KAOUI, J. E. J. BEKKERS, M. KON, A. H. SCHUURMAN technique of measuring pull-out force, it applies only perpendicular forces to detach the scaffold, disregarding the rotational and translational forces that would act on the scaffold during rotation of the forearm. Due to the intrinsic stiffness of the cadaver models, only 45 of pronation and 45 of supination was possible. However, pronation and supination were executed from the neutral position and this range is clinically the most important. This arc of movement will provide the most contact between the joint surfaces of the radius and ulna. Moreover, this range most likely represents the post-operative situation. When used clinically, the scaffold would probably be protected by a forearm cast post-operatively. The cast restricts the range of movement, so that the scaffold may grow into the defect with minimal local friction. In conclusion, this study demonstrated a straightforward and feasible surgical approach for cartilage repair in the DRUJ and that a combination of fibrin glue and sutures could be used for the fixation of a collagen type I/III membrane in this joint. We would like to thank Prof. Dr. R. L. A. W. Bleys and W. van Wolferen from the Department of Functional Anatomy for providing materials and assisting in the experiments. No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. This article was primary edited by J. Scott and first proof edited by D. Rowley. References 1. Ekenstam F. Osseous anatomy and articular relationships about the distal ulna. Hand Clin 1998;14: Hagert CG. The distal radioulnar joint. Hand Clin 1987;3: Buck-Gramcko D. On the priorities of publication of some operative procedures on the distal end of the ulna. J Hand Surg Br 1990;15: Herzberg G. 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