Effect of autologous osteochondral tissue and periosteum transplantation on tendon-bone healing of rotator cuff in rabbits_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

FANG Sen ¹ , ZHANG Mingtao ¹ , YANG Xudong ¹ , DAOJI Cairang ¹ , LI Mingchun ¹ , NIAN Zhixuan ¹ , LIANG Junwen ¹ ,  YUN Xiangdong ^1,2

1. Department of Orthopedics, the Second Hospital of Lanzhou University, Gansu Lanzhou, 730000, P. R. China;
2. Key Laboratory of Bone and Joint Disease of Gansu Province, Gansu Lanzhou, 730000, P. R. China;

Corresponding?author：

YUN Xiangdong, Email: xiangdongyun@126.com

Keywords：

Rotator cuff injury; tendon-bone healing; osteochondral tissue; periosteum; autogenous transplantation; rabbit

DOI：

10.7507/1002-1892.202409094

Video：

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Objective To investigate the effect of autologous osteochondral tissue and periosteum transplantation on tendon-bone healing of rotator cuff in rabbits. Methods Twenty-four male New Zealand white rabbits were randomly divided into autologous osteochondral tissue and periosteum transplantation group (experimental group, n=12) and simple suture group (control group, n=12). Both groups were subjected to acute supraspinatus tendon injury and repaired with corresponding techniques. At 4, 8, and 12 weeks after operation, 4 specimens from each group were taken from the right shoulder joint for histological examination (HE staining, Masson staining, and Safranin O-fast green staining), and the left shoulder was subjected to biomechanical tests (maximum tensile load and stiffness). Results Both groups of animals survived until the completion of the experiment after operation. At 4 weeks after operation, both groups showed less collagen fibers and disorder at the tendon-bone junction. At 8 weeks, both groups showed reduced inflammation at the tendon-bone junction, with more organized and denser collagen fibers and chondrocytes. The experimental group showed better results than the control group. At 12 weeks, the experimental group showed typical tendon-bone transition structure, with increased generation of collagen fibers and chondrocytes, and the larger cartilage staining area. Both groups showed an increase in maximum tensile load and stiffness over time (P<0.05). The stiffness at 4 weeks and the maximum tensile load at 4, 8, and 12 weeks in the experimental group were superior to control group, and the differences were significant (P<0.05). There was no significant difference in stiffness at 8, 12 weeks between the two groups (P>0.05). Conclusion Autologous osteochondral tissue and periosteum transplantation can effectively promote the fiber and cartilage regeneration at the tendon-bone junction of rotator cuff and improve the biomechanical effect of shoulder joint in rabbits.

Citation： FANG Sen, ZHANG Mingtao, YANG Xudong, DAOJI Cairang, LI Mingchun, NIAN Zhixuan, LIANG Junwen, YUN Xiangdong. Effect of autologous osteochondral tissue and periosteum transplantation on tendon-bone healing of rotator cuff in rabbits. Chinese Journal of Reparative and Reconstructive Surgery, 2025, 39(2): 187-192. doi: 10.7507/1002-1892.202409094 Copy

1.	Hurley ET, Twomey-Kozack J, Doyle TR, et al. Bioinductive collagen implant has potential to improve rotator cuff healing: a systematic review. Arthroscopy, 2024. doi: 10.1016/j.arthro.2024.09.028.
2.	Beraldo RA, Assun??o JH, Helito PV, et al. Predictive factors for the healing of rotator cuff repairs. Cureus, 2024, 16(8): e67608. doi: 10.7759/cureus.67608.
3.	Prabhath A, Vernekar VN, Sanchez E, et al. Growth factor delivery strategies for rotator cuff repair and regeneration. Int J Pharm, 2018, 544(2): 358-371.
4.	何樹坤, 秦廷武. 肩袖損傷修復的界面組織工程研究進展. 中國修復重建外科雜志, 2021, 35(10): 1341-1351.
5.	Guevara JA, Entezari V, Ho JC, et al. An update on surgical management of the repairable large-to-massive rotator cuff tear. J Bone Joint Surg (Am), 2020, 102(19): 1742-1754.
6.	Mahardawi B, Tompkins KA, Mattheos N, et al. Periosteum-derived micrografts for bone regeneration. Connect Tissue Res, 2023, 64(4): 400-412.
7.	Chang CH, Chen CH, Su CY, et al. Rotator cuff repair with periosteum for enhancing tendon-bone healing: a biomechanical and histological study in rabbits. Knee Surg Sports Traumatol Arthrosc, 2009, 17(12): 1447-1453.
8.	崔小明, 吳佳奇, 熊小天, 等. 兔關節軟骨塊和骨髓間充質干細胞共培養. 中國矯形外科雜志, 2020, 28(04): 349-355.
9.	李奉龍, 姜春巖, 魯誼, 等. 兔肩袖損傷模型的建立及初步組織學研究. 中國組織工程研究, 2012, 16(20): 3685-3689.
10.	Youn I, Jones DG, Andrews PJ, et al. Periosteal augmentation of a tendon graft improves tendon healing in the bone tunnel. Clin Orthop Relat Res, 2004, (419): 223-231.
11.	趙楊, 戴海峰, 劉莎莎, 等. 自體骨膜促進兔肩袖腱-骨愈合的療效. 中國比較醫學雜志, 2018, 28(02): 74-79.
12.	Chen CH, Chang CH, Su CI, et al. Arthroscopic single-bundle anterior cruciate ligament reconstruction with periosteum-enveloping hamstring tendon graft: clinical outcome at 2 to 7 years. Arthroscopy, 2010, 26(7): 907-917.
13.	Rutgers C, Verweij LPE, Priester-Vink S, et al. Recurrence in traumatic anterior shoulder dislocations increases the prevalence of Hill-Sachs and bankart lesions: a systematic review and meta-analysis. Knee Surg Sports Traumatol Arthrosc, 2022, 30(6): 2130-2140.
14.	Ahmed AF, Polisetty TS, Wang C, et al. Higher return to sport and lower revision rates when performing arthroscopic Bankart repair with remplissage for anterior shoulder instability with a Hill-Sachs lesion: a meta-analysis. J Shoulder Elbow Surg, 2024, 33(8): 1836-1846.
15.	張明濤, 劉嘉鑫, 楊智濤, 等. 關節鏡自體骨軟骨移植治療復發性肩關節前脫位早期療效. 中國骨傷, 2022, 35(3): 233-237.
16.	Shin MJ, Shim IK, Kim DM, et al. Engineered cell sheets for the effective delivery of adipose-derived stem cells for tendon-to-bone healing. Am J Sports Med, 2020, 48(13): 3347-3358.
17.	陳剛, 鄭乾, 劉蒙飛, 等. Kartogenin聯合脂肪干細胞對前交叉韌帶重建術后腱骨愈合的影響. 中國修復重建外科雜志, 2023, 37(8): 1002-1010.
18.	Cheng B, Ge H, Zhou J, et al. TSG-6 mediates the effect of tendon derived stem cells for rotator cuff healing. Eur Rev Med Pharmacol Sci, 2014, 18(2): 247-2451.
19.	Xu Y, Zhang WX, Wang LN, et al. Stem cell therapies in tendon-bone healing. World J Stem Cells, 2021, 13(7): 753-775.
20.	張峻瑋, 陸海濤, 袁峰, 等. 兔骨膜細胞分離培養的方法改進. 中國組織工程研究, 2016, 20(24): 3523-3528.
21.	He L, He T, Xing J, et al. Bone marrow mesenchymal stem cell-derived exosomes protect cartilage damage and relieve knee osteoarthritis pain in a rat model of osteoarthritis. Stem Cell Res Ther, 2020, 11(1): 276. doi: 10.1186/s13287-020-01781-w.
22.	Wang J, Xu J, Wang X, et al. Magnesium-pretreated periosteum for promoting bone-tendon healing after anterior cruciate ligament reconstruction. Biomaterials, 2021, 268: 120576. doi: 10.1016/j.biomaterials.2020.120576.

1. Hurley ET, Twomey-Kozack J, Doyle TR, et al. Bioinductive collagen implant has potential to improve rotator cuff healing: a systematic review. Arthroscopy, 2024. doi: 10.1016/j.arthro.2024.09.028.
2. Beraldo RA, Assun??o JH, Helito PV, et al. Predictive factors for the healing of rotator cuff repairs. Cureus, 2024, 16(8): e67608. doi: 10.7759/cureus.67608.
3. Prabhath A, Vernekar VN, Sanchez E, et al. Growth factor delivery strategies for rotator cuff repair and regeneration. Int J Pharm, 2018, 544(2): 358-371.
4. 何樹坤, 秦廷武. 肩袖損傷修復的界面組織工程研究進展. 中國修復重建外科雜志, 2021, 35(10): 1341-1351.
5. Guevara JA, Entezari V, Ho JC, et al. An update on surgical management of the repairable large-to-massive rotator cuff tear. J Bone Joint Surg (Am), 2020, 102(19): 1742-1754.
6. Mahardawi B, Tompkins KA, Mattheos N, et al. Periosteum-derived micrografts for bone regeneration. Connect Tissue Res, 2023, 64(4): 400-412.
7. Chang CH, Chen CH, Su CY, et al. Rotator cuff repair with periosteum for enhancing tendon-bone healing: a biomechanical and histological study in rabbits. Knee Surg Sports Traumatol Arthrosc, 2009, 17(12): 1447-1453.
8. 崔小明, 吳佳奇, 熊小天, 等. 兔關節軟骨塊和骨髓間充質干細胞共培養. 中國矯形外科雜志, 2020, 28(04): 349-355.
9. 李奉龍, 姜春巖, 魯誼, 等. 兔肩袖損傷模型的建立及初步組織學研究. 中國組織工程研究, 2012, 16(20): 3685-3689.
10. Youn I, Jones DG, Andrews PJ, et al. Periosteal augmentation of a tendon graft improves tendon healing in the bone tunnel. Clin Orthop Relat Res, 2004, (419): 223-231.
11. 趙楊, 戴海峰, 劉莎莎, 等. 自體骨膜促進兔肩袖腱-骨愈合的療效. 中國比較醫學雜志, 2018, 28(02): 74-79.
12. Chen CH, Chang CH, Su CI, et al. Arthroscopic single-bundle anterior cruciate ligament reconstruction with periosteum-enveloping hamstring tendon graft: clinical outcome at 2 to 7 years. Arthroscopy, 2010, 26(7): 907-917.
13. Rutgers C, Verweij LPE, Priester-Vink S, et al. Recurrence in traumatic anterior shoulder dislocations increases the prevalence of Hill-Sachs and bankart lesions: a systematic review and meta-analysis. Knee Surg Sports Traumatol Arthrosc, 2022, 30(6): 2130-2140.
14. Ahmed AF, Polisetty TS, Wang C, et al. Higher return to sport and lower revision rates when performing arthroscopic Bankart repair with remplissage for anterior shoulder instability with a Hill-Sachs lesion: a meta-analysis. J Shoulder Elbow Surg, 2024, 33(8): 1836-1846.
15. 張明濤, 劉嘉鑫, 楊智濤, 等. 關節鏡自體骨軟骨移植治療復發性肩關節前脫位早期療效. 中國骨傷, 2022, 35(3): 233-237.
16. Shin MJ, Shim IK, Kim DM, et al. Engineered cell sheets for the effective delivery of adipose-derived stem cells for tendon-to-bone healing. Am J Sports Med, 2020, 48(13): 3347-3358.
17. 陳剛, 鄭乾, 劉蒙飛, 等. Kartogenin聯合脂肪干細胞對前交叉韌帶重建術后腱骨愈合的影響. 中國修復重建外科雜志, 2023, 37(8): 1002-1010.
18. Cheng B, Ge H, Zhou J, et al. TSG-6 mediates the effect of tendon derived stem cells for rotator cuff healing. Eur Rev Med Pharmacol Sci, 2014, 18(2): 247-2451.
19. Xu Y, Zhang WX, Wang LN, et al. Stem cell therapies in tendon-bone healing. World J Stem Cells, 2021, 13(7): 753-775.
20. 張峻瑋, 陸海濤, 袁峰, 等. 兔骨膜細胞分離培養的方法改進. 中國組織工程研究, 2016, 20(24): 3523-3528.
21. He L, He T, Xing J, et al. Bone marrow mesenchymal stem cell-derived exosomes protect cartilage damage and relieve knee osteoarthritis pain in a rat model of osteoarthritis. Stem Cell Res Ther, 2020, 11(1): 276. doi: 10.1186/s13287-020-01781-w.
22. Wang J, Xu J, Wang X, et al. Magnesium-pretreated periosteum for promoting bone-tendon healing after anterior cruciate ligament reconstruction. Biomaterials, 2021, 268: 120576. doi: 10.1016/j.biomaterials.2020.120576.

Chinese Journal of Reparative and Reconstructive Surgery

Effect of autologous osteochondral tissue and periosteum transplantation on tendon-bone healing of rotator cuff in rabbits

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