Biomechanical comparison of singlerow ... - Wiley Online Library

Biomechanical Comparison of Single-Row, Double-Row, and Transosseous-Equivalent Repair Techniques after Healing in an Animal Rotator Cuff Tear Model Ryan J. Quigley,1 Akash Gupta,1 Joo-Han Oh,1,2 Kyung-Chil Chung,1 Michelle H. McGarry,1 Ranjan Gupta,1 James E. Tibone,1,3 Thay Q. Lee1 1 Orthopaedic Biomechanics Laboratory, Long Beach VA Healthcare System and University of California, Irvine, California, 2Department of Orthopedic Surgery, Seoul National University College of Medicine, Seoul National University Bundang Hospital, Korea, 3Department of Orthopedic Surgery, University of Southern California, Los Angeles, California

Received 28 November 2012; accepted 11 March 2013 Published online 9 April 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.22363

ABSTRACT: The transosseous-equivalent (TOE) rotator cuff repair technique increases failure loads and contact pressure and area between tendon and bone compared to single-row (SR) and double-row (DR) repairs, but no study has investigated if this translates into improved healing in vivo. We hypothesized that a TOE repair in a rabbit chronic rotator cuff tear model would demonstrate a better biomechanical profile than SR and DR repairs after 12 weeks of healing. A two-stage surgical procedure was performed on 21 New Zealand White Rabbits. The right subscapularis tendon was transected and allowed to retract for 6 weeks to simulate a chronic tear. Repair was done with the SR, DR, or TOE technique and allowed to heal for 12 weeks. Cyclic loading and load to failure biomechanical testing was then performed. The TOE repair showed greater biomechanical characteristics than DR, which in turn were greater than SR. These included yield load (p < 0.05), energy absorbed to yield (p < 0.05), and ultimate load (p < 0.05). For repair of a chronic, retracted rotator cuff tear, the TOE technique was the strongest biomechanical construct after healing followed by DR with SR being the weakest. ß 2013 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 31:1254–1260, 2013. Keywords: transosseous-equivalent; rotator cuff tear; rotator cuff repair; animal model; biomechanics

Despite numerous advances in techniques and materials, failure rates after rotator cuff repairs remain high with re-tear rates ranging from 20% to 70%.1–11 This suggests that with current techniques, healing of the tendon to bone interface occurs incompletely or inadequately.12 A study by Park et al. introduced the transosseous-equivalent (TOE) suture bridge technique that utilizes anchor points both medially and laterally to provide greater fixation and compression of the tendon to its native footprint compared to singlerow (SR) and double-row (DR) repairs.13 It provides superior biomechanical properties, specifically higher ultimate failure loads compared to DR.14 Subsequent studies showed that modified single and double-row repairs that incorporate additional sutures can provide equivalent or superior biomechanical properties to the TOE.15–18 Clinical outcomes of the TOE repair showed mixed results; some studies showed improved outcomes compared to SR and DR techniques,19,20 while others reported equivalent results.21–25 In spite of these mixed biomechanical and clinical results, the TOE provides improved tendon to bone pressurized contact area over the footprint as shown in cadaveric studies,26–28 which theoretically could improve healing. However, limited evidence exists that this translates into better healing and biomechanical properties in vivo. Conversely, increased compression Grant sponsor: Veterans Affairs Rehabilitation Research and Development and Merit Review; Grant sponsor: John C. Griswold Foundation; Grant sponsor: California Orthopaedic Research Institute. Correspondence to: Thay Q Lee (T: 562-826-5344; F: 562-8265675; E-mail: [email protected] [email protected]; http://www.ucirvineorthopaedicsurgery.com/faculty/lee.html) # 2013 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.

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across the repair offered by the TOE could be excessive and lead to hypovascularity of the tendon, thereby hindering tendon healing and increasing failure rates. Thus, rotator cuff repair constructs must be investigated using in vivo healing models. Most studies that evaluate healing after rotator cuff repair have relied on clinical results or imaging in humans, making biomechanical analysis impossible. One study, however, by Ozbaydar et al., did look at time-dependent differences between SR and DR repair techniques in biomechanical and histological properties in a rabbit model. They showed that at 4 and 8 weeks postoperatively the increased number of anchors in the DR repair led to a higher failure load due to a larger surface area of healed tendon to bone.29 This result suggests that healing potential is related to the amount of tendon to bone contact area created by the repair. However, to our knowledge, no study has compared the TOE repair, with its improved contact area and pressure, with SR and DR repairs in terms of their biomechanical properties after a period of tendon healing in vivo. Rats have been a commonly used animal model for rotator cuff tears, but they have certain limitations. The rat glenohumeral joint is restricted by its small size thereby making it challenging to perform repairs and to perform biomechanical testing. Anatomically, the rat supraspinatus passes under a bony acromial arch30 similar to humans; however, the rat supraspinatus is muscular at this point while in humans it is tendinous.31,32 Furthermore, controversy exists over the presence of fatty infiltration of torn rotator cuff muscles in rats,33–35 which is an important factor in the poor outcomes of surgical repair in humans.36 To address these concerns, a model was developed using

IN VIVO ROTATOR CUFF REPAIRS

the subscapularis of rabbits as a model for human supraspinatus tears.37 This model provides a sufficiently sized glenohumeral joint for reproducible biomechanical testing, and also has soft-tissue and bony similarities to the human rotator cuff. The subscapularis travels within a bony tunnel during normal forward locomotion and is tendinous at this point. Additional biomechanical and histological studies demonstrated that the rabbit subscapularis undergoes fatty degeneration at 6 weeks after a subscapularis tear, with an increase of up to 11% in fat content and a 19% decrease in muscle fiber cross sectional area of the subscapularis muscle belly,38 similar to that in the human condition. Using this model, we compared the biomechanical results of the SR, DR, and TOE repair techniques. We hypothesized that the increased strength and contact characteristics of the TOE repair lead to a better biomechanical profile after healing compared to DR and SR repairs in a chronic rotator cuff tear.

MATERIALS AND METHODS Twenty-one New Zealand White Rabbits weighing 3–4 kg were used. Rabbits were assigned to three groups: SR, DR, and TOE (n ¼ 7/group). The study was divided into a twostage surgical procedure followed by biomechanical testing. For all stages, the left shoulder served as a sham control, while the right shoulder was used for the experimental groups. The protocol was approved by IACUC at the VA Long Beach Healthcare System which is an AAALAC approved facility. Tear Creation Rabbits were anesthetized using ketamine and xylazine and given penicillin prior to surgical incision. Both shoulders were shaved, prepped, and draped in the normal sterile fashion. A transverse incision was made over the ventral shoulder followed by dissection down to the subscapularis insertion onto the lesser tubercle. The tendon of the left shoulder was used as a sham control by exposing it and observing it to be free of any tendon pathology. The subscapularis tendon of the right shoulder was then resected at its insertion on the lesser tubercle, followed by wrapping of the resected end in sterile penrose drain to prevent spontaneous reattachment. The wound was then closed in layers using suture material. Post-operatively, rabbits were given buprenorphine for pain control, and wounds were inspected for infection for 7 days after which sutures were removed. Rabbits were allowed ad-lib activity immediately after surgery and were monitored for 6 weeks following resection to allow for adequate tendon atrophy and fatty infiltration. Tear Repair Six weeks after tendon resection, rabbits underwent surgical repair of the tear. Both shoulders were shaved, prepped, and draped in sterile fashion and ketamine and xylazine were used for anesthesia with penicillin given prior to incision. The left subscapularius tendon was again exposed and noted to be free of any pathology to serve as a sham control. The right tendon was carefully dissected free from any scarring to surrounding tissues, and the penrose drain was removed from the tendon end. The tendon was mobilized as much as

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possible to allow maximum excursion back to the footprint, followed by repair using the assigned method. For single-row repair (Fig. 1A) two holes were punched and tapped in the middle of the footprint, one dorsally and the other ventrally. Two 1.3 mm Micro Quickanchor suture anchors (Depuy Mitek, Raynham, MA), which were single loaded with #3/0 Orthocord braided composite sutures, were sunk into the holes orthogonally to the footprint surface. A simple suture configuration was then used to tie and fix the tendon down. For double-row repair (Fig. 1B) four of the same anchors used in the SR repair were used. The first row of anchors was placed at the medial part of the footprint, one dorsally and one ventrally, orthogonally to the footprint surface. A horizontal mattress suture configuration was used to tie these sutures down. The second row was placed at the lateral part of the footprint to allow for maximal tendon contact area over the footprint. These sutures were then tied down using a simple suture configuration. For transosseous-equivalent repair (Fig. 1C) the medial row of sutures was placed in the exact same manner as with the DR repair, except that after tying the horizontal mattress sutures the limbs were not cut. Two lateral suture anchors were then placed 5 mm to 1 cm distal to the lateral edge of the footprint in line with the anchors from the medial row. One suture limb from each of the medial row anchors was then tied to a suture limb from the lateral row, thus creating a crossing pattern that compressed the end of the tendon down to the footprint. In a true TOE a knotless suture anchor would be used for lateral fixation; however, no knotless anchors are available that are sufficiently small for the rabbit humerus. Rabbits were rested for 12 weeks to allow for tendon to bone healing and to simulate post-operative rehabilitation and range of motion. Pain medication and wound checks were performed in the same manner as after the tear creation, and rabbits were allowed activity ad-lib. Following the resting period, rabbits were anesthetized using ketamine and xylazine and euthanized by delivering a lethal dose of sodium pentobarbital. Immediately after euthanization, both shoulders were dissected out leaving only the subscapularis muscle attached to the humerus (Fig. 2). At euthanasia the tendons for all three repairs were covered with a large amount of fibrotic scar tissue compared to the control shoulder. In all cases, we were unable to visualize any suture material from the underlying repair. All surrounding tissue and loosely adhered scar tissue was removed from the lesser tuberosity and specimens were then stored at 20˚C until testing.

Figure 1. Schematic of the (A) single-row repair, (B) doublerow repair, and (C) transosseous-equivalent repair. JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2013

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Figure 2. Isolated humerus and subscapuarlis muscle.

Biomechanical Testing Both the repaired and intact tendon were tested with an Instron materials testing machine (Instron, Canton, MA) and a video digitizing system (VDS) (Fig. 3). The specimens were thawed, and the proximal humerus was then potted with plaster of Paris in an aluminum box. The box was mounted onto the machine, and the tendon secured to a custom cryoclamp 5 mm from the medial footprint in such a fashion

Figure 4. Linear stiffness for single-row, double-row, and transosseous-equivalent, shown as a ratio of the repaired value to its control.

that the pull would be directly in line with the pull of the muscle fibers. Care was taken to ensure symmetric tension across the tendon before clamping. After the specimen was mounted, one marker was placed on the bone, one was placed on the clamp, and two were placed on the dorsal and ventral aspects of the tendon at a fixed distance from the medial footprint to allow for VDS analysis. Using the Instron, the tendon was first loaded with a 5 N preload for 10 s, followed by cyclic loading from 5 to 50 N for 10 cycles at 1 mm/s to measure hysteresis and to precondition the construct for load to failure testing. Pilot specimens showed that 50 N was well below the yield load, thus making it safe to cyclically load without causing non-elastic deformation, and 10 cycles was sufficient to remove the majority of the hysteresis. The loading rate was selected to assure accurate data collection, though loading rates do not affect biomechanical tests in skeletally mature tissues.39 The tendon was then loaded to failure at 1 mm/s. Data Analysis From the cyclic loading, the parameters determined at the 1st and the 10th cycles were: Hysteresis, initial stiffness, and linear stiffness. Initial stiffness was defined as the slope of the first 20% of the load–displacement curve, and linear stiffness was defined as the slope of the last 20% of the curve. For load to failure, the parameters were: Initial stiffness, linear stiffness, yield load, ultimate load, and energy

Figure 3. Biomechanical testing setup. JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2013

Figure 5. Yield and ultimate loads for single-row, double-row, and transosseous-equivalent, shown as a ratio of the repaired value to its control.


absorbed to yield and ultimate loads. All parameters were normalized by calculating the ratio of the repaired side to the control side to serve as an internal control and account for any variation in the animals among repair groups. Using the VDS, strain was determined in the dorsal and ventral portions of the tendon. The strain was calculated by measuring the change in distance between the bone marker and the markers on the dorsal and ventral aspects of the tendon and dividing by their respective lengths following preload. The strain was calculated at the 1st and 10th cycles and at both yield and ultimate loads. Non-paired t-tests were used to compare the normalized values between groups with a Bonferroni correction to account for multiple comparisons. Significance was set at p < 0.05.

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Figure 7. Dorsal strain at the 1st cycle, 10th cycle, yield load, and ultimate load for single-row, double-row, and transosseousequivalent repairs shown as a ratio of the repaired value to its control.

RESULTS Two rabbits from the SR group, one from the DR group and two from the TOE group were excluded as the tendon was irreparable due to excessive retraction. For VDS testing, one additional rabbit was excluded from the SR group and the DR group due to the inability to accurately track markers. Cyclic Loading No significant differences were found across the three repairs for normalized values of hysteresis, initial stiffness, and linear stiffness at the 1st or 10th cycles (Fig. 4).

compared to SR. No significant differences were found between the repair groups for initial stiffness, linear stiffness, and energy absorbed at ultimate load. Strains No significant differences in dorsal or ventral tendon strain were found during cyclic loading (Figs. 7, 8). During load to failure, the TOE group demonstrated higher ventral strain at ultimate load compared to the SR group (Fig. 8). No significant differences were found between the DR group and either of the other two repair groups (Figs. 7, 8).

Load to Failure The TOE group demonstrated a significantly higher yield load (77% of control) than both the DR (39% of control) and SR repairs (11% of control) (Fig. 5). The DR also had a significantly higher yield load compared to SR. The TOE had a significantly higher ultimate load (83% of control) than both DR (44% of control) and SR (22% of control). The DR also had a significantly higher ultimate load compared to SR. The TOE had a significantly higher energy absorbed at yield load (103% of control) compared to both DR (40% of control) and SR (3% of control) (Fig. 6). The DR also had significantly higher energy absorbed at yield load

With the rate of persistent cuff tears remaining high, focus has been placed on developing repair techniques that optimize the tendon to bone healing environment. Numerous factors contribute to re-tear after repair including suture strength,40 contact area and pressure at the tendon–bone interface,41 fatty degeneration and atrophy of the torn muscle and tendon, and bone quality. One study demonstrated through 3D analysis that the larger the interface at the rotator cuff insertion site, as with a TOE repair, the better the potential for tendon to bone healing.42 However, the

Figure 6. Energy absorbed at yield and ultimate loads for single-row, double-row, and transosseous-equivalent, shown as a ratio of the repaired value to its control.

Figure 8. Ventral strain at the 1st cycle, 10th cycle, yield load, and ultimate load for single-row, double-row, and transosseousequivalent repairs shown as a ratio of the repaired value to its control.

DISCUSSION


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clinical results of the TOE repair have been mixed,19–25 and subsequent biomechanical studies showed promise for modified single- and double-row repairs incorporating additional sutures.15–18 Despite this, studies demonstrated that the TOE repair provides increased pressurized contact area at the footprint compared with the SR and DR repair.26–28 We hypothesized that this increased area created by the TOE would lead to improve healing in vivo compared to SR and DR. Our results showed that the TOE group provides better biomechanical strength after 12 weeks of healing compared with the DR and SR groups. After 12 weeks, the TOE repaired tendon yield load was returned to 77% of its original intact state. The DR and SR repairs only returned the yield load to 39% and 11% of intact, respectively. In the only other study that compared biomechanical parameters of repair techniques after healing in a rabbit supraspinatus model, Ozbaydar et al. found that the DR technique showed a significant increase in ultimate failure load over the SR repair of 43%, 27%, and 26% immediately post-operative, and at the 4th and 8th week postoperatively, respectively.29 These results are similar to ours that showed a 100% increase in ultimate load at 12 weeks post-operatively of the DR repair compared to the SR repair. In addition, we showed that the TOE improved ultimate failure load by 277% and 89% over SR and DR techniques, respectively. The previous study had key differences though, as repairs in that study were performed immediately after tendon resection, not allowing for tendon retraction, and was performed on the rabbit supraspinatus tendon. A previous cadaveric study showed the TOE technique had a 48% higher ultimate load compared to the double row-repair at time zero.14 Previous studies in our laboratory using a rabbit subscapularius model showed at time zero the TOE had a 38.5% increase in ultimate load compared to the DR group.43 In our present study, the TOE repair group had an ultimate load that was 89% higher than the DR group. This higher in vivo value at a later time point compared with time zero suggests that the TOE group was not just stronger because of the repair construct used, but also that an additive effect existed, that is, the stronger construct led to an improved healing environment. These results suggest that the improved contact area and mean pressure of the tendon to footprint of the TOE technique did in fact lead to better healing. Our results also showed that at yield and ultimate loads, the strain in the tendon was greater for the TOE than the SR, indicating that under higher loads a greater distribution of stress occurred between the repair construct and the intact tendon for the TOE. While clinically most patients cannot achieve maximal contraction of their repaired rotator cuff muscle due to fatty infiltration and atrophy,44 the increased yield loads 12-weeks postoperatively indicates that the TOE technique might allow for more aggressive rehabilitation after surgery compared to the other techniques. JOURNAL OF ORTHOPAEDIC RESEARCH AUGUST 2013

These results are important in that they alleviate the ever-present concern that pressurized repairs could in fact lead to strangulation and hypovascularity of the healing tendon. The additional strength gained after healing of the repair site is indicative that the tendon can in fact heal better and is not being strangled to the point that the only gain in strength is provided by the repair construct alone. However, we did not control the amount of tension applied to the crossing sutures in the TOE technique, so further in vivo studies are necessary to determine the required tension to optimize the healing environment. There are several limitations to this study. While the repairs were performed in a model that we believe is analogous to the human rotator cuff, they were performed in rabbits, a quadruped species that utilizes the shoulder as a weight-bearing joint. This is exacerbated by the fact that post-operatively, rabbits were free to move ad lib while in humans, rotator cuff repairs are usually followed by a period of immobilization. Whether the weight-bearing nature of the rabbit aids recovery or damages the repair is unknown. Secondly, we can speculate that healing in rabbits is similar to humans, but the nature of vascularity, healing, and growth factors, and speed of healing are sure to differ from humans in unpredictable ways. We do not believe these limitations discredit the general pattern of findings as the rabbit subscapularis behaves in many similar ways to the human supraspinatus, and thus healing likely follows similarly, albeit in a different time course. The study was also limited by the fact that it only provides a snap-shot in time. While more time points should be investigated, we believe that the differences seen in healing at 12 weeks will only be further amplified as recovery continues. However, at later time points the differences between the repairs could become smaller. Thirdly, as is the case with in vivo studies, a considerable amount of inter-specimen variability occurred, as evidenced by the fact that several rabbits had irreparably retracted tendons; however, this fits in the spectrum of human rotator cuff tears, some of which cannot be repaired. Our study demonstrates that the TOE repair, which is known to demonstrate better biomechanical characteristics in cadavers, does in fact lead to a stronger healed tendon to bone construct in vivo. We believe this is due to the repair having better pressurized contact area and mean pressure between the tendon and footprint, leading to better and faster healing. We suggest, therefore, that when possible, surgeons should use a TOE repair for supraspinatus tears over DR or SR configurations.

ACKNOWLEDGMENTS Anchors were donated by DePuy Mitek, Raynham, MA. The funding sources did not play a role in the investigation. One or more authors have potential conflicts of interest: consultancy, Conmed Linvatec; speakers bureau/paid presentations for a company or supplier, Arthrex, Inc.; research support


from a company or supplier as a PI, Arthrex, Inc., Smith & Nephew, Synthes; royalties, financial or material support from publishers, McGraw; medical/orthopaedic publications editorial/governing board, Journal of Orthopedic Research and reviews, Journal of Shoulder and Elbow Surgery; board member/committee appointments for a society, AAOS, American Society for Surgery of the Hand, Orthopaedic Research Society, American Shoulder and Elbow Surgeons; royalties from a company or supplier, Arthrex, Inc.; grants received from Veterans Affairs Rehabilitation Research and Development and Merit Review; paid expert testimony for law firms.

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