Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Rotator cuff repair with periosteum for enhancing tendon–bone healing: a biomechanical and histological study in rabbits

Abstract

During rotator cuff repair surgery, fixation and incorporation of ruptured rotator cuff tendon into the bone is a major concern. The repair usually fails at the tendon–bone interface, especially in cases where the tear is massive. The periosteum contains multipotent stem cells that have the potential to differentiate into osteogenic and chondrogenic tissues, which may restore the original structure at the tendon–bone interface, fibrocartilage. In this study, we investigated the effect of periosteum on the healing of the infraspinatus tendon and bone using a clinically relevant rabbit model of rotator cuff tear. We used 36 skeletally mature New Zealand white rabbits in the study. The infraspinatus tendon at right limb was detached from greater tuberosity, and a periosteal flap taken from the proximal tibia was sutured onto the torn end of tendon. The contralateral limb, which was used as a control, received the same treatment without a periosteum. The rabbits were sacrificed at 4, 8, and 12 weeks, and the tendon–bone interface was put to histological exam and the biomechanical testing to assess strength of tendon–bone interface. Histological analysis of the tendon–bone interface revealed that the periosteum formed a fibrous layer over the interface between tendon and bone. At 4 weeks, fibrotic tissue showed progressive integration over the interface between cuff tendon and bone. At 8 weeks, progressive formation of fibrovascular tissue and fibrocartilage was observed between tendon and bone. At 12 weeks, extensive formation of fibrocartilage and bone was noted in the interface. The significant increase of failure load with time indicated a progressive increase in the tendon–bone incorporation strength. At 4 weeks after operation, the attachment strength of the limbs with the periosteum treated was higher than that of the control limbs; however, this difference was not statistically significant. At 8 and 12 weeks, a statistically significant increase was noted in the attachment strength of the limb treated with the periosteum. Most specimens failed at the tendon–bone interface (18/20). In the treatment of a torn rotator cuff in rabbit model, improved healing process with greater attachment strength could be achieved by suturing the periosteum between the end of tendon and the bone trough. Histological examination revealed that the cambium layer of the periosteum could serve as a potent interface layer and become progressively mature and organized during the healing process, resulting in fibrocartilage formation and the subsequent integration of the disrupted tendon into the bone. Biomechanical testing revealed a progressive increase in the attachment strength with time indicating the progressive tendon–bone incorporation. When performing rotator cuff repair in a large or massive tear, a periosteal flap can be sutured onto the torn end of tendon to enhance tendon–bone healing.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. 1.

    Augustin G, Antabak A, Davila S (2007) The periosteum. Part 1: Anatomy, histology and molecular biology. Injury 38:1115–1130

  2. 2.

    Baysal D, Balyk R, Otto D, Luciak-Corea C, Beaupre L (2005) Functional outcome and health-related quality of life after surgical repair of full-thickness rotator cuff tear using a mini-open technique. Am J Sports Med 33:1346–1355

  3. 3.

    Burkhart SS, Diaz Pagan JL, Wirth MA, Athanasiou KA (1997) Cyclic loading of anchor-based rotator cuff repairs: confirmation of the tension overload phenomenon and comparison of suture anchor fixation with transosseous fixation. Arthroscopy 13:720–724

  4. 4.

    Burman MS, Umansky M (1930) An experimental study of free periosteal transplants wrapped around tendon. With a review of the literature. J Bone Joint Surg Am 12:579–594

  5. 5.

    Chen CH, Chen WJ, Shih CH, Chou SW (2004) Arthroscopic anterior cruciate ligament reconstruction with periosteum-enveloping hamstring tendon graft. Knee Surg Sports Traumatol Arthrosc 12:398–405

  6. 6.

    Chen CH, Chen WJ, Shih CH, Yang CY, Liu SJ, Lin PY (2003) Enveloping the tendon graft with periosteum to enhance tendon–bone healing in a bone tunnel: a biomechanical and histologic study in rabbits. Arthroscopy 19:290–296

  7. 7.

    Gazielly DF, Gleyze P, Montagnon C (1994) Functional and anatomical results after rotator cuff repair. Clin Orthop Relat Res 304:43–53

  8. 8.

    Gerber C, Fuchs B, Hodler J (2000) The results of repair of massive tears of the rotator cuff. J Bone Joint Surg Am 82:505–515

  9. 9.

    Goradia VK, Mullen DJ, Boucher HR, Parks BG, O’Donnell JB (2001) Cyclic loading of rotator cuff repairs: a comparison of bioabsorbable tacks with metal suture anchors and transosseous sutures. Arthroscopy 17:360–364

  10. 10.

    Goutallier D, Postel JM, Gleyze P, Leguilloux P, Van Driessche S (2003) Influence of cuff muscle fatty degeneration on anatomic and functional outcomes after simple suture of full-thickness tears. J Shoulder Elbow Surg 12:550–554

  11. 11.

    Harris MT, Butler DL, Boivin GP, Florer JB, Schantz EJ, Wenstrup RJ (2004) Mesenchymal stem cells used for rabbit tendon repair can form ectopic bone and express alkaline phosphatase activity in constructs. J Orthop Res 22:998–1003

  12. 12.

    Harryman DT 2nd, Mack LA, Wang KY, Jackins SE, Richardson ML, Matsen FA 3rd (1991) Repairs of the rotator cuff. Correlation of functional results with integrity of the cuff. J Bone Joint Surg Am 73:982–989

  13. 13.

    Hopper RA, Zhang JR, Fourasier VL, Morova-Protzner I, Protzner KF, Pang CY, Forrest CR (2001) Effect of isolation of periosteum and dura on the healing of rabbit calvarial inlay bone grafts. Plast Reconstr Surg 107:454–462

  14. 14.

    Jost B, Pfirrmann CW, Gerber C, Switzerland Z (2000) Clinical outcome after structural failure of rotator cuff repairs. J Bone Joint Surg Am 82:304–314

  15. 15.

    Kessler KJ, Bullens-Borrow AE, Zisholtz J (2002) LactoSorb plates for rotator cuff repair. Arthroscopy 18:279–283

  16. 16.

    Klepps S, Bishop J, Lin J, Cahlon O, Strauss A, Hayes P, Flatow EL (2004) Prospective evaluation of the effect of rotator cuff integrity on the outcome of open rotator cuff repairs. Am J Sports Med 32:1716–1722

  17. 17.

    Koh JL, Szomor Z, Murrell GA, Warren RF (2002) Supplementation of rotator cuff repair with a bioresorbable scaffold. Am J Sports Med 30:410–413

  18. 18.

    L’Insalata JC, Klatt B, Fu FH, Harner CD (1997) Tunnel expansion following anterior cruciate ligament reconstruction: a comparison of hamstring and patellar tendon autografts. Knee Surg Sports Traumatol Arthrosc 5:234–238

  19. 19.

    Malcarney HL, Bonar F, Murrell GA (2005) Early inflammatory reaction after rotator cuff repair with a porcine small intestine submucosal implant: a report of four cases. Am J Sports Med 33:907–911

  20. 20.

    Mansat P, Cofield RH, Kersten TE, Rowland CM (1997) Complications of rotator cuff repair. Orthop Clin North Am 28:205–213

  21. 21.

    McLaughlin HL (1963) Repair of major cuff ruptures. Surg Clin North Am 43:1535–1540

  22. 22.

    Oguma H, Murakami G, Takahashi-Iwanaga H, Aoki M, Ishii S (2001) Early anchoring collagen fibers at the bone-tendon interface are conducted by woven bone formation: light microscope and scanning electron microscope observation using a canine model. J Orthop Res 19:873–880

  23. 23.

    Ritsila VA, Santavirta S, Alhopuro S, Poussa M, Jaroma H, Rubak JM, Eskola A, Hoikka V, Snellman O, Osterman K (1994) Periosteal and perichondral grafting in reconstructive surgery. Clin Orthop Relat Res 302:259–265

  24. 24.

    Ritsila V, Alhopuro S, Rintala A (1972) Bone formation with free periosteum. An experimental study. Scand J Plast Reconstr Surg 6:51–56

  25. 25.

    Rodeo SA, Arnoczky SP, Torzilli PA, Hidaka C, Warren RF (1993) Tendon-healing in a bone tunnel. A biomechanical and histological study in the dog. J Bone Joint Surg Am 75:1795–1803

  26. 26.

    Rodeo SA, Suzuki K, Deng XH, Wozney J, Warren RF (1999) Use of recombinant human bone morphogenetic protein-2 to enhance tendon healing in a bone tunnel. Am J Sports Med 27:476–488

  27. 27.

    Rubak JM (1983) Osteochondrogenesis of free periosteal grafts in the rabbit iliac crest. Acta Orthop Scand 54:826–831

  28. 28.

    Scheibel M, Brown A, Woertler K, Imhoff AB (2007) Preliminary results after rotator cuff reconstruction augmented with an autologous periosteal flap. Knee Surg Sports Traumatol Arthrosc 15:305–314

  29. 29.

    Sclamberg SG, Tibone JE, Itamura JM, Kasraeian S (2004) Six-month magnetic resonance imaging follow-up of large and massive rotator cuff repairs reinforced with porcine small intestinal submucosa. J Shoulder Elbow Surg 13:538–541

  30. 30.

    Uddstromer L, Ritsila V (1978) Osteogenic capacity of periosteal grafts. A qualitative and quantitative study of membranous and tubular bone periosteum in young rabbits. Scand J Plast Reconstr Surg 12:207–214

  31. 31.

    Youn I, Jones DG, Andrews PJ, Cook MP, Suh JK (2004) Periosteal augmentation of a tendon graft improves tendon healing in the bone tunnel. Clin Orthop Relat Res 419:223–231

Download references

Author information

Correspondence to Chih-Hwa Chen.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Chang, C., Chen, C., Su, C. et al. Rotator cuff repair with periosteum for enhancing tendon–bone healing: a biomechanical and histological study in rabbits. Knee Surg Sports Traumatol Arthrosc 17, 1447–1453 (2009). https://doi.org/10.1007/s00167-009-0809-x

Download citation

Keywords

  • Periosteum
  • Rotator cuff
  • Tendon–bone healing