RESEARCH PROGRESS OF STRATEGIES TO AUGMENT TENDON-TO-BONE HEALING_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHANGChenghao , LIQi , TANGXin ,  LIJian

Department of Orthopedics, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P. R. China;

Corresponding author：

LIJian, Email: 18980601388@163.com

Keywords：

Tendon-to-bone healing; Periosteum; Biomaterial; Growth factor; Platelet-rich plasma

DOI：

10.7507/1002-1892.20150195

Video：

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Objective To summarize the application status and progress of the strategies to augment tendon-to-bone healing. Methods The present researches focused on augmentation of tendon-to-bone healing were extensively reviewed. Results The present strategies to augment healing of tendon-to-bone by enhancing the location environment, and increasing the cell numbers and relative growth factor. The mainly strategies include using calcium phosphate materials, biocompatible scaffolds and glue, growth factors, cell matrix, platelet-rich plasma, and periosteum. Although periosteum have been used in clinical and got some possitive effects, the others still not be used in clinical and needs further studies. Conclusion There are many strategies to enhance the ability of tendon-to-bone healing, which got some positive results, but results of studies were varied. Thus, further fundamental research and clinical studies are required to achieve the best effects.

Citation： ZHANGChenghao, LIQi, TANGXin, LIJian. RESEARCH PROGRESS OF STRATEGIES TO AUGMENT TENDON-TO-BONE HEALING. Chinese Journal of Reparative and Reconstructive Surgery, 2015, 29(7): 912-916. doi: 10.7507/1002-1892.20150195 Copy

1.	Hamner DL,Brown CH Jr,Steiner ME,et al.Hamstring tendon grafts for reconstruction of the anterior cruciate ligament:biomechanical evaluation of the use of multiple strands and tensioning techniques.J Bone Joint Surg (Am),1999,81(4):549-557.
2.	Cooper DE,Deng XH,Burstein AL,et al.The strength of the central third patellar tendon graft.A biomechanical study.Am J Sports Med,1993,21(6):818-824.
3.	Apostolakos J,Durant TJ,Dwyer CR,et al.The enthesis:a review of the tendon-to-bone insertion.Muscles Ligaments Tendons J,2014,4(3):333-342.
4.	Rothrauff BB,Tuan RS.Cellular therapy in bone-tendon interface regeneration.Organogenesis,2014,10(1):13-28.
5.	Shen H,Qiao G,Cao H,et al.An histological study of the influence of osteoinductive calcium phosphate ceramics on tendon healing pattern in a bone tunnel with suspensory fixation.Int Orthop,2010,34(6):917-924.
6.	Weiler A,Hoffmann RF,Bail HJ,et al.Tendon healing in a bone tunnel.Part Ⅱ:Histologic analysis after biodegradable interference fit fixation in a model of anterior cruciate ligament reconstruction in sheep.Arthroscopy,2002,18(2):124-135.
7.	Tabuchi K,Soejima T,Kanazawa T,et al.Chronological changes in the collagen-type composition at tendon-bone interface in rabbits.Bone Joint Res, 2012,1(9):218-224.
8.	蒋青,林共周,曲绵域,等.前十字韧带重建后止点转归的研究.中华骨科杂志,2001,21(3):176-178.
9.	Muller B,Bowman KF Jr,Bedi A.ACL graft healing and biologics.Clin Sports Med,2013,32(1):93-109.
10.	Zhang X,Bogdanowicz D,Erisken C,et al.Biomimetic scaffold design for functional and integrative tendon repair.J Shoulder Elbow Surg,2012,21(2):266-277.
11.	Smith L,Xia Y,Galatz LM,et al.Tissue-engineering strategies for the tendon/ligament-to-bone insertion.Connect Tissue Res,2012,53(2):95-105.
12.	陈百成,栾广,张展翅,等.自体骨膜包裹肌腱对腱骨愈合的影响.中华骨科杂志,2006,26(2):118-122.
13.	王智慧,陈百成,张晓阳,等.自体骨膜包裹同种异体肌腱重建前交叉韧带的前瞻性研究.中国修复重建外科杂志,2011,25(10):1256-1260.
14.	Karaoglu S,Celik C,Korkusuz P.The effects of bone marrow or periosteum on tendon-to-bone tunnel healing in a rabbit model.Knee Surg Sports Traumatol Arthrosc,2009,17(2):170-178.
15.	Chen CH,Chen WJ,Shih CH,et al.Enveloping the tendon graft with periosteum to enhance tendon-bone healing in a bone tunnel:A biomechanical and histologic study in rabbits.Arthroscopy,2003,19(3):290-296.
16.	Chen CH,Chen WJ,Shih CH.Enveloping of periosteum on the hamstring tendon graft in anterior cruciate ligament reconstruction.Arthroscopy,2002,18(5):27E.
17.	Chen CH,Chen WJ,Shih CH,et al.Arthroscopic anterior cruciate ligament reconstruction with periosteum-enveloping hamstring tendon graft.Knee Surg Sports Traumatol Arthrosc,2004,12(5):398-405.
18.	Horiuchi K,Amizuka N,Takeshita S,et al.Identification and characterization of a novel protein,periostin,with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta.J Bone Miner Res,1999,14(7):1239-1249.
19.	Fu WL,Ao YF,Ke XY,et al.Repair of large full-thickness cartilage defect by activating endogenous peripheral blood stem cells and autologous periosteum flap transplantation combined with patellofemoral realignment.Knee,2014,21(2):609-612.
20.	Shibata S,Sakamoto Y,Yokohama-Tamaki T,et al.Distribution of matrix proteins in perichondrium and periosteum during the incorporation of Meckel's cartilage into ossifying mandible in midterm human fetuses:an immunohistochemical study.Anat Rec (Hoboken),2014,297(7):1208-1217.
21.	Kuang GM,Yau WP,Lu WW,et al.Local application of strontium in a calcium phosphate cement system accelerates healing of soft tissue tendon grafts in anterior cruciate ligament reconstruction:experiment using a rabbit model.Am J Sports Med,2014,42(12):2996-3002.
22.	Zhao S,Peng L,Xie G,et al. Effect of the interposition of calcium phosphate materials on tendon-bone healing during repair of chronic rotator cuff tear.Am J Sports Med,2014,42(8):1920-1929.
23.	Weimin P,Dan L,Yiyong W,et al.Tendon-to-bone healing using an injectable calcium phosphate cement combined with bone xenograft/BMP composite.Biomaterials,2013,34(38):9926-9936.
24.	Thomopoulos S,Zampiakis E,Das R,et al.Use of a magnesium-based bone adhesive for flexor tendon-to-bone healing.J Hand Surg (Am),2009,34(6):1066-1073.
25.	Wu X,Ren J,Li J.Fibrin glue as the cell-delivery vehicle for mesenchymal stromal cells in regenerative medicine.Cytotherapy,2012,14(5):555-562.
26.	Yokoya S,Mochizuki Y,Nagata Y,et al.Tendon-bone insertion repair and regeneration using polyglycolic acid sheet in the rabbit rotator cuff injury model.Am J Sports Med,2008,36(7):1298-1309.
27.	Lovric V,Chen D,Yu Y,et al. Effects of demineralized bone matrix on tendon-bone healing in an intra-articular rodent model.Am J Sports Med,2012,40(10):2365-2374.
28.	Kadonishi Y,Deie M,Takata T,et al.Acceleration of tendon-bone healing in anterior cruciate ligament reconstruction using an enamel matrix derivative in a rat model.J Bone Joint Surg (Br),2012,94(2):205-209.
29.	Würgler-Hauri CC,Dourte LM,Baradet TC,et al.Temporal expression of 8 growth factors in tendon-to-bone healing in a rat supraspinatus model.J Shoulder Elbow Surg,2007,16(5 Suppl):S198-203.
30.	Lyras DN,Kazakos K,Agrogiannis G,et al.Experimental study of tendon healing early phase:is IGF-1 expression influenced by platelet rich plasma gel? Orthop Traumatol Surg Res,2010,96(4):381-387.
31.	Buchmann S,Sandmann GH,Walz L,et al.Refixation of the supraspinatus tendon in a rat model-influence of continuousgrowth factor application on tendon structure.J Orthop Res,2013,31(2):300-305.
32.	Holladay C,Abbah SA,O'Dowd C,et al.Preferential tendon stem cell response to growth factor supplementation.J Tissue Eng Regen Med,2014.[Epub ahead of print].
33.	Kim JG,Kim HJ,Kim SE,et al.Enhancement of tendon-bone healing with the use of bone morphogenetic protein-2 inserted into the suture anchor hole in a rabbit patellar tendon model.Cytotherapy,2014,16(6):857-867.
34.	Kovacevic D,Fox AJ,Bedi A,et al.Calcium-phosphate matrix with or without TGF-β₃ improves tendon-bone healing after rotator cuff repair.Am J Sports Med,2011,39(4):811-819.
35.	Hsu SL,Wang CJ.The use of demineralized bone matrix for anterior cruciate ligament reconstruction:a radiographic,histologic,and immunohistochemical study in rabbits.J Surg Res,2014,187(1):219-224.
36.	Engebretsen L,Steffen K,Alsousou J,et al.IOC consensus paper on the use of platelet-rich plasma in sports medicine.Br J Sports Med,2010,44(15):1072-1081.
37.	Nurden AT.Platelets,inflammation and tissue regeneration.Thromb Haemost,2011,105 Suppl 1:S13-33.
38.	Halpern BC,Chaudhury S,Rodeo SA.The role of platelet-rich plasma in inducing musculoskeletal tissue healing.HSS J,2012,8(2):137-145.
39.	Andia I,Abate M.Platelet-rich plasma:underlying biology and clinical correlates.Regen Med,2013,8(5):645-658.
40.	Lyras DN,Kazakos K,Verettas D,et al.The effect of platelet-rich plasma gel in the early phase of patellar tendon healing.Arch Orthop Trauma Surg,2009,129(11):1577-1582.
41.	Xie X,Zhao S,Wu H,et al.Platelet-rich plasma enhances autograft revascularization and reinnervation in a dog model of anterior cruciate ligament reconstruction.J Surg Res,2013,183(1):214-222.
42.	Zhao JG,Zhao L,Jiang YX,et al.Platelet-rich plasma in arthroscopic rotator cuff repair:a meta-analysis of randomized controlled trials.Arthroscopy,2015,31(1):125-135.
43.	Malavolta EA,Gracitelli ME,Ferreira Neto AA,et al.Platelet-rich plasma in rotator cuff repair:a prospective randomized study.Am J Sports Med,2014,42(10):2446-2454.
44.	Seijas R,Ares O,Catala J,et al.Magnetic resonance imaging evaluation of patellar tendon graft remodelling after anterior cruciate ligament reconstruction with or without platelet-rich plasma.J Orthop Surg (Hong Kong), 2013,21(1):10-14.
45.	Rha DW,Park GY,Kim YK,et al.Comparison of the therapeutic effects of ultrasound-guided platelet-rich plasma injection and dry needling in rotator cuff disease:a randomized controlled trial.Clin Rehabil,2013,27(2):113-122.
46.	Dallaudière B,Pesquer L,Meyer P,et al.Intratendinous injection of platelet-rich plasma under US guidance to treat tendinopathy:a long-term pilot study.J Vasc Interv Radiol,2014,25(5):717-723.

1. Hamner DL,Brown CH Jr,Steiner ME,et al.Hamstring tendon grafts for reconstruction of the anterior cruciate ligament:biomechanical evaluation of the use of multiple strands and tensioning techniques.J Bone Joint Surg (Am),1999,81(4):549-557.
2. Cooper DE,Deng XH,Burstein AL,et al.The strength of the central third patellar tendon graft.A biomechanical study.Am J Sports Med,1993,21(6):818-824.
3. Apostolakos J,Durant TJ,Dwyer CR,et al.The enthesis:a review of the tendon-to-bone insertion.Muscles Ligaments Tendons J,2014,4(3):333-342.
4. Rothrauff BB,Tuan RS.Cellular therapy in bone-tendon interface regeneration.Organogenesis,2014,10(1):13-28.
5. Shen H,Qiao G,Cao H,et al.An histological study of the influence of osteoinductive calcium phosphate ceramics on tendon healing pattern in a bone tunnel with suspensory fixation.Int Orthop,2010,34(6):917-924.
6. Weiler A,Hoffmann RF,Bail HJ,et al.Tendon healing in a bone tunnel.Part Ⅱ:Histologic analysis after biodegradable interference fit fixation in a model of anterior cruciate ligament reconstruction in sheep.Arthroscopy,2002,18(2):124-135.
7. Tabuchi K,Soejima T,Kanazawa T,et al.Chronological changes in the collagen-type composition at tendon-bone interface in rabbits.Bone Joint Res, 2012,1(9):218-224.
8. 蒋青,林共周,曲绵域,等.前十字韧带重建后止点转归的研究.中华骨科杂志,2001,21(3):176-178.
9. Muller B,Bowman KF Jr,Bedi A.ACL graft healing and biologics.Clin Sports Med,2013,32(1):93-109.
10. Zhang X,Bogdanowicz D,Erisken C,et al.Biomimetic scaffold design for functional and integrative tendon repair.J Shoulder Elbow Surg,2012,21(2):266-277.
11. Smith L,Xia Y,Galatz LM,et al.Tissue-engineering strategies for the tendon/ligament-to-bone insertion.Connect Tissue Res,2012,53(2):95-105.
12. 陈百成,栾广,张展翅,等.自体骨膜包裹肌腱对腱骨愈合的影响.中华骨科杂志,2006,26(2):118-122.
13. 王智慧,陈百成,张晓阳,等.自体骨膜包裹同种异体肌腱重建前交叉韧带的前瞻性研究.中国修复重建外科杂志,2011,25(10):1256-1260.
14. Karaoglu S,Celik C,Korkusuz P.The effects of bone marrow or periosteum on tendon-to-bone tunnel healing in a rabbit model.Knee Surg Sports Traumatol Arthrosc,2009,17(2):170-178.
15. Chen CH,Chen WJ,Shih CH,et al.Enveloping the tendon graft with periosteum to enhance tendon-bone healing in a bone tunnel:A biomechanical and histologic study in rabbits.Arthroscopy,2003,19(3):290-296.
16. Chen CH,Chen WJ,Shih CH.Enveloping of periosteum on the hamstring tendon graft in anterior cruciate ligament reconstruction.Arthroscopy,2002,18(5):27E.
17. Chen CH,Chen WJ,Shih CH,et al.Arthroscopic anterior cruciate ligament reconstruction with periosteum-enveloping hamstring tendon graft.Knee Surg Sports Traumatol Arthrosc,2004,12(5):398-405.
18. Horiuchi K,Amizuka N,Takeshita S,et al.Identification and characterization of a novel protein,periostin,with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta.J Bone Miner Res,1999,14(7):1239-1249.
19. Fu WL,Ao YF,Ke XY,et al.Repair of large full-thickness cartilage defect by activating endogenous peripheral blood stem cells and autologous periosteum flap transplantation combined with patellofemoral realignment.Knee,2014,21(2):609-612.
20. Shibata S,Sakamoto Y,Yokohama-Tamaki T,et al.Distribution of matrix proteins in perichondrium and periosteum during the incorporation of Meckel's cartilage into ossifying mandible in midterm human fetuses:an immunohistochemical study.Anat Rec (Hoboken),2014,297(7):1208-1217.
21. Kuang GM,Yau WP,Lu WW,et al.Local application of strontium in a calcium phosphate cement system accelerates healing of soft tissue tendon grafts in anterior cruciate ligament reconstruction:experiment using a rabbit model.Am J Sports Med,2014,42(12):2996-3002.
22. Zhao S,Peng L,Xie G,et al. Effect of the interposition of calcium phosphate materials on tendon-bone healing during repair of chronic rotator cuff tear.Am J Sports Med,2014,42(8):1920-1929.
23. Weimin P,Dan L,Yiyong W,et al.Tendon-to-bone healing using an injectable calcium phosphate cement combined with bone xenograft/BMP composite.Biomaterials,2013,34(38):9926-9936.
24. Thomopoulos S,Zampiakis E,Das R,et al.Use of a magnesium-based bone adhesive for flexor tendon-to-bone healing.J Hand Surg (Am),2009,34(6):1066-1073.
25. Wu X,Ren J,Li J.Fibrin glue as the cell-delivery vehicle for mesenchymal stromal cells in regenerative medicine.Cytotherapy,2012,14(5):555-562.
26. Yokoya S,Mochizuki Y,Nagata Y,et al.Tendon-bone insertion repair and regeneration using polyglycolic acid sheet in the rabbit rotator cuff injury model.Am J Sports Med,2008,36(7):1298-1309.
27. Lovric V,Chen D,Yu Y,et al. Effects of demineralized bone matrix on tendon-bone healing in an intra-articular rodent model.Am J Sports Med,2012,40(10):2365-2374.
28. Kadonishi Y,Deie M,Takata T,et al.Acceleration of tendon-bone healing in anterior cruciate ligament reconstruction using an enamel matrix derivative in a rat model.J Bone Joint Surg (Br),2012,94(2):205-209.
29. Würgler-Hauri CC,Dourte LM,Baradet TC,et al.Temporal expression of 8 growth factors in tendon-to-bone healing in a rat supraspinatus model.J Shoulder Elbow Surg,2007,16(5 Suppl):S198-203.
30. Lyras DN,Kazakos K,Agrogiannis G,et al.Experimental study of tendon healing early phase:is IGF-1 expression influenced by platelet rich plasma gel? Orthop Traumatol Surg Res,2010,96(4):381-387.
31. Buchmann S,Sandmann GH,Walz L,et al.Refixation of the supraspinatus tendon in a rat model-influence of continuousgrowth factor application on tendon structure.J Orthop Res,2013,31(2):300-305.
32. Holladay C,Abbah SA,O'Dowd C,et al.Preferential tendon stem cell response to growth factor supplementation.J Tissue Eng Regen Med,2014.[Epub ahead of print].
33. Kim JG,Kim HJ,Kim SE,et al.Enhancement of tendon-bone healing with the use of bone morphogenetic protein-2 inserted into the suture anchor hole in a rabbit patellar tendon model.Cytotherapy,2014,16(6):857-867.
34. Kovacevic D,Fox AJ,Bedi A,et al.Calcium-phosphate matrix with or without TGF-β₃ improves tendon-bone healing after rotator cuff repair.Am J Sports Med,2011,39(4):811-819.
35. Hsu SL,Wang CJ.The use of demineralized bone matrix for anterior cruciate ligament reconstruction:a radiographic,histologic,and immunohistochemical study in rabbits.J Surg Res,2014,187(1):219-224.
36. Engebretsen L,Steffen K,Alsousou J,et al.IOC consensus paper on the use of platelet-rich plasma in sports medicine.Br J Sports Med,2010,44(15):1072-1081.
37. Nurden AT.Platelets,inflammation and tissue regeneration.Thromb Haemost,2011,105 Suppl 1:S13-33.
38. Halpern BC,Chaudhury S,Rodeo SA.The role of platelet-rich plasma in inducing musculoskeletal tissue healing.HSS J,2012,8(2):137-145.
39. Andia I,Abate M.Platelet-rich plasma:underlying biology and clinical correlates.Regen Med,2013,8(5):645-658.
40. Lyras DN,Kazakos K,Verettas D,et al.The effect of platelet-rich plasma gel in the early phase of patellar tendon healing.Arch Orthop Trauma Surg,2009,129(11):1577-1582.
41. Xie X,Zhao S,Wu H,et al.Platelet-rich plasma enhances autograft revascularization and reinnervation in a dog model of anterior cruciate ligament reconstruction.J Surg Res,2013,183(1):214-222.
42. Zhao JG,Zhao L,Jiang YX,et al.Platelet-rich plasma in arthroscopic rotator cuff repair:a meta-analysis of randomized controlled trials.Arthroscopy,2015,31(1):125-135.
43. Malavolta EA,Gracitelli ME,Ferreira Neto AA,et al.Platelet-rich plasma in rotator cuff repair:a prospective randomized study.Am J Sports Med,2014,42(10):2446-2454.
44. Seijas R,Ares O,Catala J,et al.Magnetic resonance imaging evaluation of patellar tendon graft remodelling after anterior cruciate ligament reconstruction with or without platelet-rich plasma.J Orthop Surg (Hong Kong), 2013,21(1):10-14.
45. Rha DW,Park GY,Kim YK,et al.Comparison of the therapeutic effects of ultrasound-guided platelet-rich plasma injection and dry needling in rotator cuff disease:a randomized controlled trial.Clin Rehabil,2013,27(2):113-122.
46. Dallaudière B,Pesquer L,Meyer P,et al.Intratendinous injection of platelet-rich plasma under US guidance to treat tendinopathy:a long-term pilot study.J Vasc Interv Radiol,2014,25(5):717-723.

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Chinese Journal of Reparative and Reconstructive Surgery

RESEARCH PROGRESS OF STRATEGIES TO AUGMENT TENDON-TO-BONE HEALING

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