Augmentation of tendon healing with butyric acid-impregnated sutures: Biomechanical evaluation in a rabbit model

American Journal of Sports Medicine

Volumn 40, Issue 8, 2012, Pages 1762-1771

  Leek, Bryan T ^a   Tasto, James P ^a   Tibor, Lisa M ^a   Healey, Robert M ^b   Freemont, Anthony ^c   Linn, Michael S ^b   Chase, Derek E ^b   Amiel, David ^a,b  

^a San Diego Sports Medicine and Orthopaedic Center   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

angiogenesis; butyric acid; suture material; tendon repair

Indexed keywords

BIOMATERIAL; BUTYRIC ACID;

ACHILLES TENDON; ANGIOGENESIS; ANIMAL; ANIMAL MODEL; ARTICLE; BIOMECHANICS; DRUG EFFECT; PHYSIOLOGY; RABBIT; SUTURE; WOUND HEALING;

ACHILLES TENDON; ANIMALS; BIOMECHANICS; BUTYRIC ACID; COATED MATERIALS, BIOCOMPATIBLE; MODELS, ANIMAL; NEOVASCULARIZATION, PHYSIOLOGIC; RABBITS; SUTURES; WOUND HEALING;

EID: 84864692213     PISSN: 03635465     EISSN: 15523365     Source Type: Journal    
DOI: 10.1177/0363546512450691     Document Type: Article

References (57)

1. Acton D, Perry AR, Stephens P, et al. Meniscal healing using a suture soaked with butyric acid/polyhydroxybutyrate (PHB). J Bone Joint Surg Br. 2004 ; 86: 122
2. Amiel D, Woo SL, Harwood FL, Akeson WH. The effect of immobilization on collagen turnover in connective tissue: a biochemical-biomechanical correlation. Acta Orthop Scand. 1982 ; 53 (3). 325-332
3. Andersson T, Eliasson P, Aspenberg P. Tissue memory in healing tendons: short loading episodes stimulate healing. J Appl Physiol. 2009 ; 107 (2). 417-421
4. Aspenberg P. Stimulation of tendon repair: mechanical loading, GDFs and platelets. A mini-review. Int Orthop. 2007 ; 31 (6). 783-789
5. Aspenberg P, Forslund C. Enhanced tendon healing with GDF 5 and 6. Acta Orthop Scand. 1999 ; 70 (1). 51-54
6. Boyer MI, Watson JT, Lou J, Manske PR, Gelberman RH, Cai SR. Quantitative variation in vascular endothelial growth factor mRNA expression during early flexor tendon healing: an investigation in a canine model. J Orthop Res. 2001 ; 19 (5). 869-872
7. Brodie M, Vollenweider L, Murphy JL, et al. Biomechanical properties of Achilles tendon repair augmented with a bioadhesive-coated scaffold. Biomed Mater. 2011 ; 6 (1). 015014
8. Cheung EV, Silverio L, Sperling JW. Strategies in biologic augmentation of rotator cuff repair: a review. Clin Orthop Relat Res. 2010 ; 468 (6). 1476-1484
9. Christiansen DL, Huang EK, Silver FH. Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol. 2000 ; 19 (5). 409-420
10. Dahlgren LA, Mohammed HO, Nixon AJ. Expression of insulin-like growth factor binding proteins in healing tendon lesions. J Orthop Res. 2006 ; 24 (2). 183-192
11. Desmoulière A, Chaponnier C, Gabbiani G. Tissue repair, contraction, and the myofibroblast. Wound Repair Regen. 2005 ; 13 (1). 7-12
12. Díaz-Flores L, Gutiérrez R, Varela H. Angiogenesis: an update. Histol Histopathol. 1994 ; 9 (4). 807-843
13. Dines JS, Grande DA, Dines DM. Tissue engineering and rotator cuff tendon healing. J Shoulder Elbow Surg. 2007 ; 16 (5 Suppl). S204 - S207
14. Dobson DE, Kambe A, Block E, et al. 1-Butyryl-glycerol: a novel angiogenesis factor secreted by differentiating adipocytes. Cell. 1990 ; 61 (2). 223-230
15. Freemont AJ, Hoyland J, Fielding P, Hodson N, Jayson MI. Studies of the microvascular endothelium in uninvolved skin of patients with systemic sclerosis: direct evidence for a generalized microangiopathy. Br J Dermatol. 1992 ; 126 (6). 561-568
16. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol. 2003 ; 200 (4). 500-503
17. 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 (7). 975-982
18. Gelberman RH, Manske PR, Akeson WH, Woo SL, Lundborg G, Amiel D. Flexor tendon repair. J Orthop Res. 1986 ; 4 (1). 119-128
19. Gururaj AE, Belakavadi M, Salimath BP. Anti-angiogenic effects of butyric acid involve inhibition of VEGF/KDR gene expression and endothelial cell proliferation. Mol Cell Biochem. 2003 ; 243 (1-2). 107-112
20. Halvorsen YC, Bursell S, Wilkison WO, et al. Vasodilation of rat retinal microvessels induced by monobutyrin dysregulation in diabetes. J Clin Invest. 1993 ; 92 (6). 2872-2876
21. Hou Y, Mao Z, Wei X, et al. Effects of transforming growth factor-beta1 and vascular endothelial growth factor 165 gene transfer on Achilles tendon healing. Matrix Biol. 2009 ; 28 (6). 324-335
22. Isaac C, Gharaibeh B, Witt M, Wright VJ, Huard J. Biologic approaches to enhance rotator cuff healing after injury. J Shoulder Elbow Surg. 2012 ; 21 (2). 181-190
23. Jialili A, Jielile J, Abudoureyimu S, et al. Differentially expressed proteins on postoperative 3 days healing in rabbit Achilles tendon rupture model after early kinesitherapy. Chin J Traumatol. 2011 ; 14 (2). 84-91
24. Kearney RS, McGuinness KR, Achten J, Costa ML. A systematic review of early rehabilitation methods following a rupture of the Achilles tendon. Physiotherapy. 2012 ; 98 (1). 24-32
25. Kim HM, Galatz LM, Das R, Havlioglu N, Rothermich SY, Thomopoulos S. The role of transforming growth factor beta isoforms in tendon-to-bone healing. Connect Tissue Res. 2011 ; 52 (2). 87-98
26. Kim HM, Nelson G, Thomopoulos S, Silva MJ, Das R, Gelberman RH. Technical and biological modifications for enhanced flexor tendon repair. J Hand Surg Am. 2010 ; 35 (6). 1031-1038
27. Kovacevic D, Rodeo SA. Biological augmentation of rotator cuff tendon repair. Clin Orthop Relat Res. 2008 ; 466 (3). 622-633
28. Larsen A, Kristensen G, Thorlacius-Ussing O, Oxlund H. The influence of ultrasound on the mechanical properties of healing tendons in rabbits. Acta Orthop. 2005 ; 76 (2). 225-230
29. Lin JL, Carreira D, Ponnappan R, Volz B, Cole BJ. Use of bipolar radiofrequency energy in delayed repair of acute supraspinatus tears in rats. J Shoulder Elbow Surg. 2007 ; 16 (5). 640-648
30. Molloy T, Wang Y, Murrell G. The roles of growth factors in tendon and ligament healing. Sports Med. 2003 ; 33 (5). 381-394
31. Nakamura K, Kitaoka K, Tomita K. Effect of eccentric exercise on the healing process of injured patellar tendon in rats. J Orthop Sci. 2008 ; 13 (4). 371-378
32. Ng GY, Oakes BW, Deacon OW, McLean ID, Eyre DR. Long-term study of the biochemistry and biomechanics of anterior cruciate ligament-patellar tendon autografts in goats. J Orthop Res. 1996 ; 14 (6). 851-856
33. Prasanna Kumar S, Thippeswamy G, Sheela ML, Prabhakar BT, Salimath BP. Butyrate-induced phosphatase regulates VEGF and angiogenesis via Sp1. Arch Biochem Biophys. 2008 ; 478 (1). 85-95
34. Pufe T, Petersen WJ, Mentlein R, Tillmann BN. The role of vasculature and angiogenesis for the pathogenesis of degenerative tendon disease. Scand J Med Sci Sports. 2005 ; 15 (4). 211-222
35. Qin L, Wang L, Wong MW, et al. Osteogenesis induced by extracorporeal shockwave in treatment of delayed osteotendinous junction healing. J Orthop Res. 2010 ; 28 (1). 70-76
36. Raines EW, Ross R Clinical Applications of Cytokines: Role in Pathogenesis, Diagnosis, and Therapy. Oppenheim JJ Rossio JL Gearing AJH, ed. New York: Oxford University Press ; 1993
37. 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 (11). 2485-2497
38. Sah RL, Yang AS, Chen AC, et al. Physical properties of rabbit articular cartilage after transection of the anterior cruciate ligament. J Orthop Res. 1997 ; 15 (2). 197-203
39. Salehpour A, Butler DL, Proch FS, et al. Dose-dependent response of gamma irradiation on mechanical properties and related biochemical composition of goat bone-patellar tendon-bone allografts. J Orthop Res. 1995 ; 13: 898-906
40. Savitskaya YA, Izaguirre A, Sierra L, et al. Effect of angiogenesis-related cytokines on rotator cuff disease: the search for sensitive biomarkers of early tendon degeneration. Clin Med Insights Arthritis Musculoskelet Disord. 2011 ; 4: 43-53
41. Schepull T, Kvist J, Aspenberg P. Early E-modulus of healing Achilles tendons correlates with late function: similar results with or without surgery. Scand J Med Sci Sports. 2012 ; 22: 18-23
42. Scott A, Lian Ø, Bahr R, Hart D, Duronio V. VEGF expression in patellar tendinopathy: a preliminary study. Clin Orthop. 2008 ; 466 (7). 1598-1604
43. Seiler JG, Chu CR, Amie lD, Woo SL, Gelberman RH. The Marshall R. Urist Young Investigator Award. Autogenous flexor tendon grafts: biologic mechanisms for incorporation. Clin Orthop Relat Res. 1997 ; 345: 239-247
44. Sharma P, Maffulli N. Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg Am. 2005 ; 87: 187-202
45. Stevenson DP, Milligan SR, Collins WP. Effects of platelet-derived endothelial cell growth factor/thymidine phosphorylase, substrate, and products in a three-dimensional model of angiogenesis. Am J Pathol. 1998 ; 152 (6). 1641-1646
46. Taylor DW, Petrera M, Hendry M, Theodoropoulos JS. A systematic review of the use of platelet-rich plasma in sports medicine as a new treatment for tendon and ligament injuries. Clin J Sport Med. 2011 ; 21 (4). 344-352
47. Thomopoulos S, Das R, Silva MJ, et al. Enhanced flexor tendon healing through controlled delivery of PDGF-BB. J Orthop Res. 2009 ; 27 (9). 1209-1215
48. Thomopoulos S, Harwood FL, Silva MJ, Amiel D, Gelberman RH. Effect of several growth factors on canine flexor tendon fibroblast proliferation and collagen synthesis in vitro. J Hand Surg Am. 2005 ; 30: 441-447
49. Tracy SC, Tasto JP, Oshima Y, Murata R, Garcia J, Amiel D. The effect of butyric acid on normal tendons: a potential stimulus of extracellular matrix compression. Am J Orthop. 2011 ; 40 (3). 142-147
50. Wei X, Mao Z, Hou Y, et al. Local administration of TGFβ-1/VEGF165 gene-transduced bone mesenchymal stem cells for Achilles allograft replacement of the anterior cruciate ligament in rabbits. Biochem Biophys Res Commun. 2011 ; 406 (2). 204-210
51. Wilkison WO, Choy L, Spiegelman BM. Biosynthetic regulation of monobutyrin, an adipocyte-secreted lipid with angiogenic activity. J Biol Chem. 1991 ; 266 (25). 16886-16891
52. Wilkison WO, Spiegelman BM. Biosynthesis of the vasoactive lipid monobutyrin: central role of diacylglycerol. J Biol Chem. 1993 ; 268 (4). 2844-2849
53. Williams EA, Coxhead JM, Mathers JC. Anti-cancer effects of butyrate: use of micro-array technology to investigate mechanisms. Proc Nutr Soc. 2003 ; 62 (1). 107-115
54. Willits K, Amendola A, Bryant D, et al. Operative versus nonoperative treatment of acute Achilles tendon ruptures: a multicenter randomized trial using accelerated functional rehabilitation. J Bone Joint Surg Am. 2010 ; 92 (17). 2767-2775
55. Woo SL, Ritter MA, Amiel D, et al. The biomechanical and biochemical properties of swine tendons: long term effects of exercise on the digital extensors. Connect Tissue Res. 1980 ; 7 (3). 177-183
56. Wright E, Walsh WR, Stephens P, et al. Meniscal healing using butyric acid impregnated sutures. Trans Orthop Res Soc.. 2004
57. Zhao C, Sun YL, Amadio PC, Tanaka T, Ettema AM, An KN. Surface treatment of flexor tendon autografts with carbodiimide-derivatized hyaluronic acid: an in vivo canine model. J Bone Joint Surg Am. 2006 ; 88: 2181-2191