All of the dogs were walking by one to three days postoperatively, and no adverse events were noted throughout the twelve-week healing period.
All of the repairs at twelve weeks were considered to show tendon retraction to some extent (Table II). Tendon retraction was significantly greater in unaugmented control repairs than in augmented repairs (p = 0.008). Five of eight unaugmented repairs retracted by ≥2 cm, whereas five of eight augmented repairs retracted ≤1 cm and none of the augmented repairs retracted >2 cm.
After twelve weeks of healing, the cross-sectional area of the augmented repairs averaged 70 ± 30 mm2 (137% ± 95%) more than that of the paired, unaugmented control repairs (p < 0.001) (Fig. 4).
Biomechanical failure started at the soft-tissue freezing front (i.e., “grip artifact”) for two samples in the augmented group and one sample in the unaugmented group at twelve weeks; hence, the ultimate loads for these samples were excluded from the analysis.
After twelve weeks of healing, the stiffness of the augmented repairs averaged 44 ± 26 N/mm (26% ± 21%) more than paired, unaugmented repairs (p = 0.002) (Fig. 3-A). Further, at twelve weeks, the ultimate load of augmented repairs averaged 246 ± 143 N (35% ± 29%) more than the six paired, unaugmented repairs (p = 0.009) (Fig. 3-B). The failure mode of all twelve-week samples in both groups started in soft tissue, either by failure of the repair or failure of the intact portion of the tendon (Table I). Because soft tissues covered the device and/or tendon in all twelve-week samples, it was not possible to determine more precisely the location where failure started. In no instance was osseous avulsion observed nor did the X-Repair device fail during mechanical testing.
A significant ordered difference was found between tendon retraction distance and both stiffness (p = 0.004) (Fig. 5-A) and ultimate load (p = 0.006) (Fig. 5-B). Stiffness was not found to be significantly correlated to the sample cross-sectional area (comparison not shown). Ultimate load was moderately correlated to sample cross-sectional area (r = 0.59, p = 0.034) (Fig. 6).
Histologic analysis revealed only the expected host cell response to a biocompatible biomaterial such as poly-L-lactide. Specifically, macrophages and giant cells were identified in sporadic regions along the surface of the X-Repair device, but no neutrophils or lymphocytes were observed (Fig. 7-A). Regions of fibrous tissue ingrowth were observed as well as occasional areas that appeared fibrocartilage-like (Fig. 7-B).
The cross-sectional area of both the unaugmented and augmented repairs at twelve weeks was two to fourfold greater than that of the normal controls (p < 0.001; Table III).
The stiffness of unaugmented repairs did not increase significantly between time zero and twelve weeks of healing (p = 0.944; Table III) and remained significantly less (an average of 39%) compared with that of normal controls at twelve weeks (p < 0.001; Table III). The ultimate load of unaugmented repairs was not significantly increased between time zero and twelve weeks of healing (p = 0.097, post hoc power = 0.585; Table III), and remained significantly less (an average of 62%) compared with that of normal controls at twelve weeks (p = 0.002; Table III).
The stiffness of augmented repairs was not significantly increased between time zero and twelve weeks of healing (p = 0.709; Table III), and it remained significantly less (an average of 47%) than that of normal controls at twelve weeks (p < 0.001; Table III). In contrast to the results in unaugmented repairs, the ultimate load of augmented repairs at twelve weeks was significantly increased compared with time zero (p = 0.016; Table III), yet it remained significantly less (an average of 77%) than that of normal controls (p = 0.034; Table III).
We evaluated the extent to which augmentation of acute rotator cuff tendon repairs with a newly designed poly-L-lactide repair device would affect stiffness, ultimate load, and failure mode of the repair in a canine model. The device has high suture retention (approximately 400 N), and its stiffness (approximately 200 N/mm) and ultimate load (approximately 800 N) are similar to those of human rotator cuff tendon strips of similar width57-59.
At time zero, device augmentation did not significantly increase the stiffness of the repair construct in this animal model compared with repairs without augmentation, despite the use of a device with mechanical properties similar to the tendon and deliberately pretensioning the device so as to off-load the repair. (The lack of difference should not be interpreted as meaning the groups were equivalent, as this study was underpowered to detect differences of <40 N/mm.) The potential for device augmentation to increase construct stiffness may have been abrogated by the prefailure loading cycles. The cyclic protocol (100 loading cycles from 5 to 100 N) was intended to represent a realistic early loading paradigm; hence, it should be appreciated that the potential clinical benefit of device augmentation (even with pretensioning) may be mitigated by so-called suture setting in the device and tendon fibers during the early loading period. However, the parallel organization of the canine infraspinatus tendon likely makes it more sensitive to suture setting and/or slippage than the more interwoven organization of the human rotator cuff. The 23% increased ultimate load achieved with device augmentation at time zero may simply be the result of having five points of tendon fixation (two sutures between tendon and bone as well as three sutures between device and tendon) rather than three points. Note that the ultimate load with device augmentation sometimes occurred at a point after the tendon had completely separated from the bone. In these cases, the device would act as a bridge between the bone and tendon beyond what would have been the failure point for an unaugmented repair.
At twelve weeks after surgery, all of the repairs were considered to show evidence of tendon retraction, revealing that the loads and/or displacements experienced by all repair constructs were in excess of those required to pull sutures through tendon to some extent. So-called gap formation (or tendon retraction) following rotator cuff tendon repair has been reported previously in animal models23,33, and is a common mode of failure in patients following rotator cuff repair24,25. Augmented repairs demonstrated significantly lessretraction than repairs that had not been augmented, preventing massive (>2 cm) tendon retraction and maintaining a connected tendon-bone bridge. The relevance of this outcome is made manifest by the significant relationship found between tendon retraction distance and both stiffness and ultimate load—that is, the repairs that retracted less had higher stiffness and higher ultimate load. A similar, inverse correlation between retraction distance and repair strength and stiffness has been shown in healing flexor tendon repair60,61. Together, these data emphasize that achieving less retraction by way of device augmentation translates into a stiffer and stronger tendon repair.
At twelve weeks, augmented repairs demonstrated significantly greater stiffness (an average increase of 26%) than did repairs that had not been augmented. Our data showed that increased stiffness is not explained by increased cross-sectional area of the repair. It is possible that repair stiffness actually first decreases from time zero during the early weeks following repair as the suture attachments that primarily govern stiffness at time zero soften62,63. By twelve weeks, the stiffness of the repairs may be increasing by way of device integration to host tissues, tendon healing, and/or new tissue deposition. At twelve weeks, we would expect minimal degradation of the poly-L-lactide device; therefore, if the device has become integrated to some degree with the host tissue, it could contribute to the functional properties of the repair.
Similarly, at twelve weeks, augmented repairs demonstrated significantly greater ultimate load (an average increase of 35%) than did repairs that had not been augmented. Ultimate load was moderately correlated with cross-sectional area, so the increased tissue mass associated with augmented repairs may explain at least in part the increase in ultimate load. As with stiffness, device integration with host tissues and/or new tissue deposition may also play a role. The ultimate load of augmented repairs at twelve weeks was significantly increased compared with time-zero controls and was 77% of normal. One caveat must be raised in interpreting this result: the failure mode of normal tendon was exclusively osseous avulsion of the humeral head, indicating that normal control tendon strength is even greater than the ultimate loads measured. Notwithstanding this consideration, the results suggest that the ultimate load of augmented repairs is improving toward a normal functional outcome in this animal model.
The ability of scaffold devices to provide rotator cuff repair augmentation and support tendon regeneration has been investigated in animal models. Studies in which devices were investigated for repair augmentation (i.e., the device was applied over the primary tendon-bone repair)28,33,64 are more appropriate for comparison with our work than are studies in which devices were investigated as interpositional scaffolds to replace a resected tendon26,29-31,34,36,37. Schlegel et al. performed full-width infraspinatus injury and repair in sheep33. They placed a 10 × 20-mm patch of small intestine submucosa over the superficial aspect of the repaired tendon. The control was tendon repair without a graft. They reported that “both constructs showed evidence of gap formation as the tendon healed medial to the original repair site,” suggesting that graft augmentation was insufficient to prevent tendon retear in this animal model. At twelve weeks, repairs augmented with small intestine submucosa were significantly stiffer (39%) than unaugmented repairs, and stiffness was 40% of normal. The ultimate load of augmented repairs averaged 27% more than that of unaugmented repairs; however, this result was not significant. Nicholson et al. performed a partial-width infraspinatus injury and repair in sheep, investigating the effect of repair augmentation with small intestine submucosa or cross-linked porcine dermis grafts64. They reported little or no difference in ultimate load between graft-augmented and unaugmented repairs at nine or twenty-four weeks of healing. MacGillivray et al. performed the only study with use of a woven poly-L-lactide scaffold for rotator cuff repair augmentation28. Using the goat model, they created a full-width infraspinatus tendon injury with a 6 × 6-mm tendon defect prior to repair with or without augmentation. The poly-L-lactide device was fixed to the superficial aspect of the repaired tissue in a manner that may have offered some resistance to suture pull-through27. Ultimate loads of augmented repairs were not significantly different from unaugmented controls at twelve weeks.
As we continue to assess device augmentation strategies in animal models, it is clear that our interpretation and comparison of various approaches would be greatly aided by the adoption of some commonalities in experimental design with respect to species, surgical injury, study design, surgical technique, outcome measures, and spectrum of controls. In this study, we reasoned that a partial-width-injury model might moderate the rate of repair failures and mimic the mechanical environment of many single tendon tears in the human injury condition. However, we observed a 100% rate of retear with the partial-width model, which, in hindsight, we postulate to be a consequence of the parallel aligned fascicles in the canine tendon that are able to retract independently when the muscle contracts.
Our study was not without limitations. First, the twelve-week time point, while commonly used33, does not allow us to investigate the long-term effects of device augmentation. Second, while all repairs had four holes (two transosseous tunnels) drilled in the bone, repairs with the device had a fifth hole in the bone. This fifth hole was subsequently filled with the cortical screw; however, it is possible that the extra bone hole may have slightly biased healing in the augmented group. Third, we performed histologic analysis after mechanical testing and only on the augmented repair samples to assess biocompatibility of the X-Repair device. This study did not seek to evaluate differences in histologic outcomes between the unaugmented and augmented groups. Finally, the study was powered primarily to evaluate the clinically important differences of 40 N/mm in stiffness and 200 N in ultimate load between paired unaugmented and augmented samples at time zero and at twelve weeks. To detect the same-sized differences between unpaired groups, the study was underpowered. To more rigorously address comparisons among time zero, twelve weeks, and normal control groups, a greater sample size would be required in order to accommodate the increased between-dog variance that is introduced by the unpaired analysis.
In conclusion, rotator cuff repair augmentation with a poly-L-lactide device reduces tendon retraction distance and improves the stiffness and ultimate load of the repair at twelve weeks in the canine model. The mechanically robust poly-L-lactide scaffold was biocompatible and would be expected to be resorbed by the host over a period of months or years. While limiting but not eliminating tendon repair retraction, the augmentation device provided a tendon-bone bridge for host tissue deposition and ingrowth, resulting in improved biomechanical function of the repair at twelve weeks. Such a device, applied in a similar manner, might offer a functional benefit to human patients undergoing rotator cuff repair. However, if the fourfold increase in cross-sectional area associated with device augmentation in this animal model were to occur in human repairs, impingement against the acromial arch could occur.
Investigation performed at the Departments of Orthopaedic Surgery and Biomedical Engineering, Cleveland Clinic, Cleveland, Ohio
1. American Academy of Orthopaedic Surgeons. Number of patients, number of procedures, average patient age, average length of stay—National Hospital Discharge Survey 1998-2005. http://http://www.aaos.org
2. Accousti KJ, Flatow EL. Technical pearls on how to maximize healing of the rotator cuff. Instr Course Lect. 2007;56:3-12.
3. Bishop J, Klepps S, Lo IK, Bird J, Gladstone JN, Flatow EL. Cuff integrity after arthroscopic versus open rotator cuff repair: a prospective study. J Shoulder Elbow Surg. 2006;15:290-9.
4. Boileau P, Brassart N, Watkinson DJ, Carles M, Hatzidakis AM, Krishnan SG. Arthroscopic repair of full-thickness tears of the supraspinatus: does the tendon really heal? J Bone Joint Surg Am. 2005;87:1229-40.
5. Galatz LM, Ball CM, Teefey SA, Middleton WD, Yamaguchi K. The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears. J Bone Joint Surg Am. 2004;86:219-24.
6. Gazielly DF, Gleyze P, Montagnon C. Functional and anatomical results after rotator cuff repair. Clin Orthop Relat Res. 1994;304:43-53.
7. Gerber C, Fuchs B, Hodler J. The results of repair of massive tears of the rotator cuff. J Bone Joint Surg Am. 2000;82:505-15.
8. Harryman DT 2nd, Mack LA, Wang KY, Jackins SE, Richardson ML, Matsen FA 3rd. Repairs of the rotator cuff. Correlation of functional results with integrity of the cuff. J Bone Joint Surg Am. 1991;73:982-9.
9. Romeo AA, Hang DW, Bach BR Jr, Shott S. Repair of full thickness rotator cuff tears. Gender, age, and other factors affecting outcome. Clin Orthop Relat Res. 1999;367:243-55.
10. Cofield RH, Parvizi J, Hoffmeyer PJ, Lanzer WL, Ilstrup DM, Rowland CM. Surgical repair of chronic rotator cuff tears. A prospective long-term study. J Bone Joint Surg Am. 2001;83:71-7.
11. Bartolozzi A, Andreychik D, Ahmad S. Determinants of outcome in the treatment of rotator cuff disease. Clin Orthop Relat Res. 1994;308:90-7.
12. Riley GP, Harrall RL, Constant CR, Chard MD, Cawston TE, Hazleman BL. Tendon degeneration and chronic shoulder pain: changes in the collagen composition of the human rotator cuff tendons in rotator cuff tendinitis. Ann Rheum Dis. 1994;53:359-66.
13. Goutallier D, Postel JM, Gleyze P, Leguilloux P, Van Driessche S. Influence of cuff muscle fatty degeneration on anatomic and functional outcomes after simple suture of full-thickness tears. J Shoulder Elbow Surg. 2003;12:550-4.
14. Hamada K, Tomonaga A, Gotoh M, Yamakawa H, Fukuda H. Intrinsic healing capacity and tearing process of torn supraspinatus tendons: in situ hybridization study of alpha 1 (I) procollagen mRNA. J Orthop Res. 1997;15:24-32.
15. Thomopoulos S, Soslowsky LJ, Flanagan CL, Tun S, Keefer CC, Mastaw J, Carpenter JE. The effect of fibrin clot on healing rat supraspinatus tendon defects. J Shoulder Elbow Surg. 2002;11:239-47.
16. Iannotti JP. Full-thickness rotator cuff tears: factors affecting surgical outcome. J Am Acad Orthop Surg. 1994;2:87-95.
17. Uhthoff HK, Trudel G, Himori K. Relevance of pathology and basic research to the surgeon treating rotator cuff disease. J Orthop Sci. 2003;8:449-56.
18. Melillo AS, Savoie FH 3rd, Field LD. Massive rotator cuff tears: debridement versus repair. Orthop Clin North Am. 1997;28:117-24.
19. Rockwood CA Jr, Williams GR Jr, Burkhead WZ Jr. Débridement of degenerative, irreparable lesions of the rotator cuff. J Bone Joint Surg Am. 1995;77:857-66.
20. Hawkins RH, Dunlop R. Nonoperative treatment of rotator cuff tears. Clin Orthop Relat Res. 1995;321:178-88.
21. Burkhart SS. Partial repair of massive rotator cuff tears: the evolution of a concept. Orthop Clin North Am. 1997;28:125-32.
22. Dines DM, Moynihan DP, Dines JS, McCann P. Irreparable rotator cuff tears: what to do and when to do it; the surgeon's dilemma. Instr Course Lect. 2007;56:13-22.
23. Rodeo SA, Potter HG, Kawamura S, Turner AS, Kim HJ, Atkinson BL. Biologic augmentation of rotator cuff tendon-healing with use of a mixture of osteoinductive growth factors. J Bone Joint Surg Am. 2007;89:2485-97.
24. Burkhart SS, Diaz Pagàn JL, Wirth MA, Athanasiou KA. Cyclic loading of anchor-based rotator cuff repairs: confirmation of the tension overload phenomenon and comparison of suture anchor fixation with transosseous fixation. Arthroscopy. 1997;13:720-4.
25. Cummins CA, Murrell GA. Mode of failure for rotator cuff repair with suture anchors identified at revision surgery. J Shoulder Elbow Surg. 2003;12:128-33.
26. Aoki M, Miyamoto S, Okamura K, Yamashita T, Ikada Y, Matsuda S. Tensile properties and biological response of poly(L-lactic acid) felt graft: an experimental trial for rotator-cuff reconstruction. J Biomed Mater Res B Appl Biomater. 2004;71:252-9.
27. Koh JL, Szomor Z, Murrell GA, Warren RF. Supplementation of rotator cuff repair with a bioresorbable scaffold. Am J Sports Med. 2002;30:410-3.
28. MacGillivray JD, Fealy S, Terry MA, Koh JL, Nixon AJ, Warren RF. Biomechanical evaluation of a rotator cuff defect model augmented with a bioresorbable scaffold in goats. J Shoulder Elbow Surg. 2006;15:639-44.
29. Kimura A, Aoki M, Fukushima S, Ishii S, Yamakoshi K. Reconstruction of a defect of the rotator cuff with polytetrafluoroethylene felt graft. Recovery of tensile strength and histocompatibility in an animal model. J Bone Joint Surg Br. 2003;85:282-7.
30. Adams JE, Zobitz ME, Reach JS Jr, An KN, Steinmann SP. Rotator cuff repair using an acellular dermal matrix graft: an in vivo study in a canine model. Arthroscopy. 2006;22:700-9.
31. Dejardin LM, Arnoczky SP, Ewers BJ, Haut RC, Clarke RB. Tissue-engineered rotator cuff tendon using porcine small intestine submucosa. Histologic and mechanical evaluation in dogs. Am J Sports Med. 2001;29:175-84.
32. Sano H, Kumagai J, Sawai T. Experimental fascial autografting for the supraspinatus tendon defect: remodeling process of the grafted fascia and the insertion into bone. J Shoulder Elbow Surg. 2002;11:166-73.
33. Schlegel TF, Hawkins RJ, Lewis CW, Motta T, Turner AS. The effects of augmentation with Swine small intestine submucosa on tendon healing under tension: histologic and mechanical evaluations in sheep. Am J Sports Med. 2006;34:275-80.
34. Zalavras CG, Gardocki R, Huang E, Stevanovic M, Hedman T, Tibone J. Reconstruction of large rotator cuff tendon defects with porcine small intestinal submucosa in an animal model. J Shoulder Elbow Surg. 2006;15:224-31.
35. Zheng MH, Chen J, Kirilak Y, Willers C, Xu J, Wood D. Porcine small intestine submucosa (SIS) is not an acellular collagenous matrix and contains porcine DNA: possible implications in human implantation. J Biomed Mater Res B Appl Biomater. 2005;73:61-7.
36. Funakoshi T, Majima T, Suenaga N, Iwasaki N, Yamane S, Minami A. Rotator cuff regeneration using chitin fabric as an acellular matrix. J Shoulder Elbow Surg. 2006;15:112-8.
37. Funakoshi T, Majima T, Iwasaki N, Suenaga N, Sawaguchi N, Shimode K, Minami A, Harada K, Nishimura S. Application of tissue engineering techniques for rotator cuff regeneration using a chitosan-based hyaluronan hybrid fiber scaffold. Am J Sports Med. 2005;33:1193-201.
38. Aurora A, McCarron J, Iannotti JP, Derwin K. Commercially available extracellular matrix materials for rotator cuff repairs: state of the art and future trends. J Shoulder Elbow Surg. 2007;16(5 Suppl):S171-8.
39. Derwin KA, Baker AR, Spragg RK, Leigh DR, Iannotti JP. Commercial extracellular matrix scaffolds for rotator cuff tendon repair. Biomechanical, biochemical, and cellular properties. J Bone Joint Surg Am. 2006;88:2665-72.
40. Barber FA, Herbert MA, Coons DA. Tendon augmentation grafts: biomechanical failure loads and failure patterns. Arthroscopy. 2006;22:534-8.
41. Metcalf MH, Savoie FH 3rd, Kellum B. Surgical technique for xenograft (SIS) augmentation of rotator-cuff repairs. Oper Tech Orthop. 2002;12:204-8.
42. Iannotti JP, Codsi MJ, Kwon YW, Derwin K, Ciccone J, Brems JJ. Porcine small intestine submucosa augmentation of surgical repair of chronic two-tendon rotator cuff tears. A randomized, controlled trial. J Bone Joint Surg Am. 2006;88:1238-44.
43. Malcarney HL, Bonar F, Murrell GA. Early inflammatory reaction after rotator cuff repair with a porcine small intestine submucosal implant: a report of 4 cases. Am J Sports Med. 2005;33:907-11.
44. Sclamberg SG, Tibone JE, Itamura JM, Kasraeian S. Six-month magnetic resonance imaging follow-up of large and massive rotator cuff repairs reinforced with porcine small intestinal submucosa. J Shoulder Elbow Surg. 2004;13:538-41.
45. Walton JR, Bowman NK, Khatib Y, Linklater J, Murrell GA. Restore orthobiologic implant: not recommended for augmentation of rotator cuff repairs. J Bone Joint Surg Am. 2007;89:786-91.
46. Burkhead WZ Jr, Schiffern SC, Krishnan SG. Use of Graft Jacket as an augmentation for massive rotator cuff tears. Semin Arthrop. 2007;18:11-8.
47. Dopirak R, Bond JL, Snyder SJ. Arthroscopic total rotator cuff replacement with an acellular human dermal allograft matrix. Intl J Shoulder Surg. 2007;1:7-15.
48. Badhe SP, Lawrence TM, Smith FD, Lunn PG. An assessment of porcine dermal xenograft as an augmentation graft in the treatment of extensive rotator cuff tears. J Shoulder Elbow Surg. 2008;17(1 Suppl):35S-9S.
49. Soler JA, Gidwani S, Curtis MJ. Early complications from the use of porcine dermal collagen implants (Permacol) as bridging constructs in the repair of massive rotator cuff tears. A report of 4 cases. Acta Orthop Belg. 2007;73:432-6.
50. Lee S, Mahar A, Bynum K, Pedowitz R. Biomechanical comparison of bioabsorbable sutureless screw anchor versus suture anchor fixation for rotator cuff repair. Arthroscopy. 2005;21:43-7.
51. Tominaga K, Habu M, Khanal A, Mimori Y, Yoshioka I, Fukuda J. Biomechanical evaluation of different types of rigid internal fixation techniques for subcondylar fractures. J Oral Maxillofac Surg. 2006;64:1510-6.
52. Barber FA, Boothby MH. Bilok interference screws for anterior cruciate ligament reconstruction: clinical and radiographic outcomes. Arthroscopy. 2007;23:476-81.
53. Derwin KA, Baker AR, Codsi MJ, Iannotti JP. Assessment of the canine model of rotator cuff injury and repair. J Shoulder Elbow Surg. 2007;16(5 Suppl):S140-8.
54. Ma CB, Comerford L, Wilson J, Puttlitz CM. Biomechanical evaluation of arthroscopic rotator cuff repairs: double-row compared with single-row fixation. J Bone Joint Surg Am. 2006;88:403-10.
55. Baker AR, Abreu EL, Mascha E, Derwin KA. Homotypic variation of canine flexor tendons: implications for the design of experimental studies in animal models. J Biomech. 2004;37:959-68. Erratum in: J Biomech. 2004;37:1955.
56. Bey MJ, Song HK, Wehrli FW, Soslowsky LJ. A noncontact, nondestructive method for quantifying intratissue deformations and strains. J Biomech Eng. 2002;124:253-8.
57. Itoi E, Berglund LJ, Grabowski JJ, Schultz FM, Growney ES, Morrey BF, An KN. Tensile properties of the supraspinatus tendon. J Orthop Res. 1995;13:578-84.
58. Halder A, Zobitz ME, Schultz E, An KN. Structural properties of the subscapularis tendon. J Orthop Res. 2000;18:829-34.
59. Halder A, Zobitz ME, Schultz F, An KN. Mechanical properties of the posterior rotator cuff. Clin Biomech (Bristol, Avon). 2000;15:456-62.
60. Gelberman RH, Boyer MI, Brodt MD, Winters SC, Silva MJ. The effect of gap formation at the repair site on the strength and excursion of intrasynovial flexor tendons. An experimental study on the early stages of tendon-healing in dogs. J Bone Joint Surg Am. 1999;81:975-82.
61. Thomopoulos S, Zampiakis E, Das R, Silva MJ, Gelberman RH. The effect of muscle loading on flexor tendon-to-bone healing in a canine model. J Orthop Res. 2008;26:1611-7.
62. Yildirim Y, Kara H, Cabukoglu C, Esemenli T. Suture holding capacity of the Achilles tendon during the healing period: an in vivo experimental study in rabbits. Foot Ankle Int. 2006;27:121-4.
63. McDowell CL, Marqueen TJ, Yager D, Owen J, Wayne JS. Characterization of the tensile properties and histologic/biochemical changes in normal chicken tendon at the site of suture insertion. J Hand Surg [Am]. 2002;27:605-14.
64. Nicholson GP, Breur GJ, Van Sickle D, Yao JQ, Kim J, Blanchard CR. Evaluation of a cross-linked acellular porcine dermal patch for rotator cuff repair augmentation in an ovine model. J Shoulder Elbow Surg. 2007;16(5 Suppl):S184-90.