DOI QR코드

DOI QR Code

Effect of co-administration of atelocollagen and hyaluronic acid on rotator cuff healing

  • Jeong, Jeung Yeol (Department of Orthopedic Surgery, Hallym University Dongtan Sacred Heart Hospital, Medical College of Hallym University) ;
  • Khil, Eun Kyung (Department of Radiology, Hallym University Dongtan Sacred Heart Hospital, Medical College of Hallym University) ;
  • Kim, Tae Soung (Department of Orthopedic Surgery, Hallym University Dongtan Sacred Heart Hospital, Medical College of Hallym University) ;
  • Kim, Young Woo (Department of Orthopedic Surgery, Hallym University Dongtan Sacred Heart Hospital, Medical College of Hallym University)
  • Received : 2021.04.08
  • Accepted : 2021.05.23
  • Published : 2021.09.01

Abstract

Background: This study aimed to evaluate the co-administration effect of atelocollagen combined with hyaluronic acid (HA) injections for treatment of full-thickness rotator cuff tear (RCT). Methods: Eighty patients who underwent arthroscopic rotator cuff repair for full-thickness RCT from March 2018 to November 2019 were enrolled. The patients were randomly allocated to the following groups: combined atelocollagen and HA injection (group I, n=28), only HA injection (group II, n=26), and no injection (group III, n=26). Clinical outcomes were assessed at 3, 6, and 12 months after surgery using the American Shoulder and Elbow Surgeons score, visual analog scale pain score, functional scores (pain visual analog scale, function visual analog score), and range of motion. Magnetic resonance imaging was performed 12 months after surgery to evaluate rotator cuff integrity. Results: Preoperative demographic data and postoperative clinical outcomes did not differ significantly among the three groups (p>0.05). However, in group I, the number of steroid injections after surgery was significantly lower than that in the other groups (p=0.011). The retear rate on follow-up magnetic resonance imaging was significantly higher in group II (9.5%, n=2) and group III (13.6%, n=3) than in group I (0%) (p=0.021). Conclusions: Co-administration of atelocollagen and HA improves healing of the rotator cuff and increases the integrity of the rotator cuff repair site. This study provides encouraging evidence for use of combined atelocollagen-HA injections to treat patients with full-thickness RCT.

Keywords

References

  1. Li H, Chen Y, Chen S. Enhancement of rotator cuff tendon-bone healing using bone marrow-stimulating technique along with hyaluronic acid. J Orthop Translat 2019;17:96-102. https://doi.org/10.1016/j.jot.2019.01.001
  2. Minagawa H, Yamamoto N, Abe H, et al. Prevalence of symptomatic and asymptomatic rotator cuff tears in the general population: from mass-screening in one village. J Orthop 2013;10:8-12. https://doi.org/10.1016/j.jor.2013.01.008
  3. Cho NS, Moon SC, Jeon JW, Rhee YG. The influence of diabetes mellitus on clinical and structural outcomes after arthroscopic rotator cuff repair. Am J Sports Med 2015;43:991-7. https://doi.org/10.1177/0363546514565097
  4. Park JS, Park HJ, Kim SH, Oh JH. Prognostic factors affecting rotator cuff healing after arthroscopic repair in small to medium-sized tears. Am J Sports Med 2015;43:2386-92. https://doi.org/10.1177/0363546515594449
  5. Sugaya H, Maeda K, Matsuki K, Moriishi J. Repair integrity and functional outcome after arthroscopic double-row rotator cuff repair: a prospective outcome study. J Bone Joint Surg Am 2007;89:953-60. https://doi.org/10.2106/JBJS.F.00512
  6. Im GI, Ahn JH, Kim SY, Choi BS, Lee SW. A hyaluronate-atelocollagen/beta-tricalcium phosphate-hydroxyapatite biphasic scaffold for the repair of osteochondral defects: a porcine study. Tissue Eng Part A 2010;16:1189-200. https://doi.org/10.1089/ten.tea.2009.0540
  7. Suh DS, Lee JK, Yoo JC, et al. Atelocollagen enhances the healing of rotator cuff tendon in rabbit model. Am J Sports Med 2017;45:2019-27. https://doi.org/10.1177/0363546517703336
  8. Honda H, Gotoh M, Kanazawa T, et al. Hyaluronic acid accelerates tendon-to-bone healing after rotator cuff repair. Am J Sports Med 2017;45:3322-30. https://doi.org/10.1177/0363546517720199
  9. Mazzocca AD, McCarthy MB, Chowaniec DM, et al. The positive effects of different platelet-rich plasma methods on human muscle, bone, and tendon cells. Am J Sports Med 2012;40:1742-9. https://doi.org/10.1177/0363546512452713
  10. Prockop DJ, Kivirikko KI. Collagens: molecular biology, diseases, and potentials for therapy. Annu Rev Biochem 1995;64:403-34. https://doi.org/10.1146/annurev.bi.64.070195.002155
  11. Pins GD, Christiansen DL, Patel R, Silver FH. Self-assembly of collagen fibers: influence of fibrillar alignment and decorin on mechanical properties. Biophys J 1997;73:2164-72. https://doi.org/10.1016/S0006-3495(97)78247-X
  12. Lynn AK, Yannas IV, Bonfield W. Antigenicity and immunogenicity of collagen. J Biomed Mater Res B Appl Biomater 2004;71:343-54.
  13. Kim JH, Kim DJ, Lee HJ, Kim BK, Kim YS. Atelocollagen injection improves tendon integrity in partial-thickness rotator cuff tears: a prospective comparative study. Orthop J Sports Med 2020;8:2325967120904012.
  14. Mitsui Y, Gotoh M, Nakama K, Yamada T, Higuchi F, Nagata K. Hyaluronic acid inhibits mRNA expression of proinflammatory cytokines and cyclooxygenase-2/prostaglandin E(2) production via CD44 in interleukin-1-stimulated subacromial synovial fibroblasts from patients with rotator cuff disease. J Orthop Res 2008;26:1032-7. https://doi.org/10.1002/jor.20558
  15. Hays PL, Kawamura S, Deng XH, et al. The role of macrophages in early healing of a tendon graft in a bone tunnel. J Bone Joint Surg Am 2008;90:565-79. https://doi.org/10.2106/JBJS.F.00531
  16. Manferdini C, Guarino V, Zini N, et al. Mineralization behavior with mesenchymal stromal cells in a biomimetic hyaluronic acid-based scaffold. Biomaterials 2010;31:3986-96. https://doi.org/10.1016/j.biomaterials.2010.01.148
  17. Osti L, Berardocco M, di Giacomo V, Di Bernardo G, Oliva F, Berardi AC. Hyaluronic acid increases tendon derived cell viability and collagen type I expression in vitro: comparative study of four different Hyaluronic acid preparations by molecular weight. BMC Musculoskelet Disord 2015;16:284. https://doi.org/10.1186/s12891-015-0735-7
  18. Chou WY, Ko JY, Wang FS, et al. Effect of sodium hyaluronate treatment on rotator cuff lesions without complete tears: a randomized, double-blind, placebo-controlled study. J Shoulder Elbow Surg 2010;19:557-63. https://doi.org/10.1016/j.jse.2009.08.006
  19. Zhao J, Huang H, Liang G, Zeng LF, Yang W, Liu J. Effects and safety of the combination of platelet-rich plasma (PRP) and hyaluronic acid (HA) in the treatment of knee osteoarthritis: a systematic review and meta-analysis. BMC Musculoskelet Disord 2020;21:224. https://doi.org/10.1186/s12891-020-03262-w
  20. Cunningham G, Ladermann A, Denard PJ, Kherad O, Burkhart SS. Correlation between American shoulder and elbow surgeons and single assessment numerical evaluation score after rotator cuff or SLAP repair. Arthroscopy 2015;31:1688-92. https://doi.org/10.1016/j.arthro.2015.03.010
  21. Yoo JC, Ahn JH, Yang JH, Koh KH, Choi SH, Yoon YC. Correlation of arthroscopic repairability of large to massive rotator cuff tears with preoperative magnetic resonance imaging scans. Arthroscopy 2009;25:573-82. https://doi.org/10.1016/j.arthro.2008.12.015
  22. Kim KC, Shin HD, Lee WY. Repair integrity and functional outcomes after arthroscopic suture-bridge rotator cuff repair. J Bone Joint Surg Am 2012;94:e48. https://doi.org/10.2106/JBJS.K.00158
  23. Oh JH, Oh CH, Choi JA, Kim SH, Kim JH, Yoon JP. Comparison of glenohumeral and subacromial steroid injection in primary frozen shoulder: a prospective, randomized short-term comparison study. J Shoulder Elbow Surg 2011;20:1034-40. https://doi.org/10.1016/j.jse.2011.04.029
  24. Sugaya H, Maeda K, Matsuki K, Moriishi J. Functional and structural outcome after arthroscopic full-thickness rotator cuff repair: single-row versus dual-row fixation. Arthroscopy 2005;21:1307-16. https://doi.org/10.1016/j.arthro.2005.08.011
  25. Park MC, Tibone JE, ElAttrache NS, Ahmad CS, Jun BJ, Lee TQ. Part II: biomechanical assessment for a footprint-restoring transosseous-equivalent rotator cuff repair technique compared with a double-row repair technique. J Shoulder Elbow Surg 2007;16:469-76. https://doi.org/10.1016/j.jse.2006.09.011
  26. Kaizawa Y, Leyden J, Behn AW, et al. Human tendon-derived collagen hydrogel significantly improves biomechanical properties of the tendon-bone interface in a chronic rotator cuff injury model. J Hand Surg Am 2019;44:899.e1-11. https://doi.org/10.1016/j.jhsa.2018.11.021
  27. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull 1979;86:420-8. https://doi.org/10.1037/0033-2909.86.2.420
  28. Walsh MR, Nelson BJ, Braman JP, et al. Platelet-rich plasma in fibrin matrix to augment rotator cuff repair: a prospective, single-blinded, randomized study with 2-year follow-up. J Shoulder Elbow Surg 2018;27:1553-63. https://doi.org/10.1016/j.jse.2018.05.003
  29. Atesok K, Fu FH, Wolf MR, et al. Augmentation of tendon-to-bone healing. J Bone Joint Surg Am 2014;96:513-21. https://doi.org/10.2106/JBJS.M.00009
  30. Thon SG, O'Malley L 2nd, O'Brien MJ, Savoie FH 3rd. Evaluation of healing rates and safety with a bioinductive collagen patch for large and massive rotator cuff tears: 2-year safety and clinical outcomes. Am J Sports Med 2019;47:1901-8. https://doi.org/10.1177/0363546519850795
  31. 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.
  32. Kawamura S, Ying L, Kim HJ, Dynybil C, Rodeo SA. Macrophages accumulate in the early phase of tendon-bone healing. J Orthop Res 2005;23:1425-32. https://doi.org/10.1016/j.orthres.2005.01.014
  33. Weeks KD 3rd, Dines JS, Rodeo SA, Bedi A. The basic science behind biologic augmentation of tendon-bone healing: a scientific review. Instr Course Lect 2014;63:443-50.
  34. Schlegel TF, Abrams JS, Bushnell BD, Brock JL, Ho CP. Radiologic and clinical evaluation of a bioabsorbable collagen implant to treat partial-thickness tears: a prospective multicenter study. J Shoulder Elbow Surg 2018;27:242-51. https://doi.org/10.1016/j.jse.2017.08.023
  35. Kovacevic D, Rodeo SA. Biological augmentation of rotator cuff tendon repair. Clin Orthop Relat Res 2008;466:622-33. https://doi.org/10.1007/s11999-007-0112-4
  36. Li H, Ge Y, Zhang P, Wu L, Chen S. The effect of layer-by-layer chitosan-hyaluronic acid coating on graft-to-bone healing of a poly(ethylene terephthalate) artificial ligament. J Biomater Sci Polym Ed 2012;23:425-38. https://doi.org/10.1163/092050610X551989
  37. Nakamura H, Gotoh M, Kanazawa T, et al. Effects of corticosteroids and hyaluronic acid on torn rotator cuff tendons in vitro and in rats. J Orthop Res 2015;33:1523-30. https://doi.org/10.1002/jor.22921
  38. Lee MI, Kim JH, Kwak HH, et al. A placebo-controlled study comparing the efficacy of intra-articular injections of hyaluronic acid and a novel hyaluronic acid-platelet-rich plasma conjugate in a canine model of osteoarthritis. J Orthop Surg Res 2019;14:314. https://doi.org/10.1186/s13018-019-1352-1
  39. Kanazawa T, Gotoh M, Ohta K, et al. Histomorphometric and ultrastructural analysis of the tendon-bone interface after rotator cuff repair in a rat model. Sci Rep 2016;6:33800. https://doi.org/10.1038/srep33800