Skip to main content
Top
Published in: Knee Surgery, Sports Traumatology, Arthroscopy 6/2004

01-11-2004 | Experimental Study

Sodium hyaluronate regulating angiogenesis during Achilles tendon healing

Authors: Mehmet Halici, Sinan Karaoglu, Ozlem Canoz, Sevki Kabak, Ali Baktir

Published in: Knee Surgery, Sports Traumatology, Arthroscopy | Issue 6/2004

Login to get access

Abstract

The aim of this study was to evaluate the effect of SH (sodium hyaluronate—NaHA) on vascular endothelial growth factor (VEGF) and type IV collagen expression during the Achilles-tendon healing process. Adult New Zealand white rabbits (n=32) aged 4 months and weighing 2.7–3.9 kg were used. The rabbits were randomly divided into two groups, and each group was divided into two subgroups and monitored for 6 and 12 weeks. Tendo calcanei were incised transversely and repaired. An injection of 0.5 ml NaHA (15 mg/ml) was administered between the tendon and paratenon of the right leg and repeated twice at one-week intervals. Equal numbers of animals were sacrificed at the 6th and 12th weeks, and the repaired tissue was examined macroscopically and histologically for the presence of VEGF and type IV collagen expression every week. The decrease in the amount of adhesion tissue and the acceleration of tendon healing in the NaHA group were significantly high when compared with control groups at 6 and 12 weeks (p<0.001, p<0.05). In the NaHA group, due to vascular proliferation VEGF immunostaining was strongly positive in the 6th week (p<0.05), and remained positive in the 12th week (p<0.05). Similar immunostaining findings were detected for type IV collagen in the 6th week. However, there was a significant decline in immunostaining rate in the 12th week (p<0.05). The increases in VEGF and type IV collagen expression following SH administration might be an indication that SH may partly be involved in regulation of angiogenesis.
Literature
1.
go back to reference Alfredson H, Ohberg L, Forsgren S (2003) In vasculo-neural ingrowth the cause of pain in chronic Achill tendinosis? An investigation using ultrasonography and color Doppler, immunohistochemistry, and diagnostic injections. Knee Surg Sports Traumatol Arthrosc 11:334–338CrossRefPubMed Alfredson H, Ohberg L, Forsgren S (2003) In vasculo-neural ingrowth the cause of pain in chronic Achill tendinosis? An investigation using ultrasonography and color Doppler, immunohistochemistry, and diagnostic injections. Knee Surg Sports Traumatol Arthrosc 11:334–338CrossRefPubMed
2.
go back to reference Aspenberg P, Forslund C (1999) Enhanced tendon healing with GDF 5 and 6. Acta Orthop Scand 70:551–554 Aspenberg P, Forslund C (1999) Enhanced tendon healing with GDF 5 and 6. Acta Orthop Scand 70:551–554
3.
go back to reference Ferrara N (1999) Molecular and biological properties of vascular endothelial growth factor. J Mol Med 77:527–543CrossRefPubMed Ferrara N (1999) Molecular and biological properties of vascular endothelial growth factor. J Mol Med 77:527–543CrossRefPubMed
4.
go back to reference Folkman J (1995) Clinical application of research on angiogenesis. N Eng J Med 333:1757–1763CrossRef Folkman J (1995) Clinical application of research on angiogenesis. N Eng J Med 333:1757–1763CrossRef
5.
go back to reference Forslund C, Aspenberg P (2003) Improved healing of transected rabbit Achilles tendon after injection of cartilage derived morphogenic protein-2. Am J Sports Med 31:555–559PubMed Forslund C, Aspenberg P (2003) Improved healing of transected rabbit Achilles tendon after injection of cartilage derived morphogenic protein-2. Am J Sports Med 31:555–559PubMed
6.
go back to reference Frase JR, Laurent TC, Laurent UBG (1997) Hayluronan: its nature, distribution, functions, and turnover. J Intern Med 242:27–33CrossRefPubMed Frase JR, Laurent TC, Laurent UBG (1997) Hayluronan: its nature, distribution, functions, and turnover. J Intern Med 242:27–33CrossRefPubMed
7.
go back to reference Frykman E, Jacobson S, Widenfalk B (1993) Fibrin sealant in prevention of flexor tendon adhesions: an experimental study in the rabbit. J Hand Surg [Am] 18:68–75 Frykman E, Jacobson S, Widenfalk B (1993) Fibrin sealant in prevention of flexor tendon adhesions: an experimental study in the rabbit. J Hand Surg [Am] 18:68–75
8.
go back to reference Gaughan EM, Nixon AJ, Krook LP, Yeager AE, Mann KA, Mohammed H, Bartel DL (1991) Effects of sodium hyaluronate on tendon healing and adhesion formation in horses. Am J Vet Res 52:764–773PubMed Gaughan EM, Nixon AJ, Krook LP, Yeager AE, Mann KA, Mohammed H, Bartel DL (1991) Effects of sodium hyaluronate on tendon healing and adhesion formation in horses. Am J Vet Res 52:764–773PubMed
9.
go back to reference Hagberg L, Gerdin B (1992) Sodium hyaluronate as an adjunct in adhesion prevention after flexor tendon surgery in rabbits. J Hand Surg [Am] 17:935–941 Hagberg L, Gerdin B (1992) Sodium hyaluronate as an adjunct in adhesion prevention after flexor tendon surgery in rabbits. J Hand Surg [Am] 17:935–941
10.
go back to reference Inoue M, Katakami C (1993) The effect of hyaluronic acid on corneal epithelial cell proliferation. Invest Opthalmol Visual Sci 34:2313–2315 Inoue M, Katakami C (1993) The effect of hyaluronic acid on corneal epithelial cell proliferation. Invest Opthalmol Visual Sci 34:2313–2315
11.
go back to reference Isık S, Ozturk S, Gurses S, Yetmez M, Guler M, Selmanpakoglu N, Gunhan O (1999) Prevention of restrictive adhesion in primary tendon repair by HA-membrane: experimental research in chickens. Br J Plast Surg 52:373–379CrossRefPubMed Isık S, Ozturk S, Gurses S, Yetmez M, Guler M, Selmanpakoglu N, Gunhan O (1999) Prevention of restrictive adhesion in primary tendon repair by HA-membrane: experimental research in chickens. Br J Plast Surg 52:373–379CrossRefPubMed
12.
go back to reference Kawasaki K, Ochi M, Uchio Y, Adachi N, Matsusaki M (1999) Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels. J Cell Physiol 179:142–148CrossRefPubMed Kawasaki K, Ochi M, Uchio Y, Adachi N, Matsusaki M (1999) Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels. J Cell Physiol 179:142–148CrossRefPubMed
13.
go back to reference Kleinert HE, Kutz JE, Atasoy EL, Stormo A (1973) Primary repair of flexor tendons. Orthop Clin North Am 4:865–876PubMed Kleinert HE, Kutz JE, Atasoy EL, Stormo A (1973) Primary repair of flexor tendons. Orthop Clin North Am 4:865–876PubMed
14.
go back to reference Lees VC, Fan TP, West DC (1995) Angiogenesis in a delayed revascularization model is accelerated by angiogenic oligosaccharides of hyaluronan. Lab Invest 73:259–266PubMed Lees VC, Fan TP, West DC (1995) Angiogenesis in a delayed revascularization model is accelerated by angiogenic oligosaccharides of hyaluronan. Lab Invest 73:259–266PubMed
15.
go back to reference Lisignoli G, Grassi F, Zini N, Toneguzzi S, Piacentini A, Guidolin D, Bevilacqua C, Facchini A (2001) Anti-Fas-induced apoptosis in chondrocytes reduced by hyaluronan. Evidence for CD 44 and CD 54 (intracellular adhesion molecule 1) involvement. Arthritis Rheum 44:1800–1807CrossRefPubMed Lisignoli G, Grassi F, Zini N, Toneguzzi S, Piacentini A, Guidolin D, Bevilacqua C, Facchini A (2001) Anti-Fas-induced apoptosis in chondrocytes reduced by hyaluronan. Evidence for CD 44 and CD 54 (intracellular adhesion molecule 1) involvement. Arthritis Rheum 44:1800–1807CrossRefPubMed
16.
go back to reference Miller JA, Ferguson RL, Powers DL, Burns JW, Shalaby SW (1997) Efficacy of hyaluronic acid/nonsteroidal anti-inflamatory drug system in preventing postsurgical tendon adhesion. J Biomed Mat Res 38:25–33CrossRef Miller JA, Ferguson RL, Powers DL, Burns JW, Shalaby SW (1997) Efficacy of hyaluronic acid/nonsteroidal anti-inflamatory drug system in preventing postsurgical tendon adhesion. J Biomed Mat Res 38:25–33CrossRef
17.
go back to reference Moses MA, Klagsbrun M, Shing Y (1995) The role of growth factors in vascular cell development and differentiation. Int Rev Cytol 161:1–48PubMed Moses MA, Klagsbrun M, Shing Y (1995) The role of growth factors in vascular cell development and differentiation. Int Rev Cytol 161:1–48PubMed
18.
go back to reference Nicosia RF, Madri JA (1987) The microvascular extracellular matrix. Developmental changes during angiogenesis in the aortic ring-plasma clot model. Am J Pathol 128:78–90PubMed Nicosia RF, Madri JA (1987) The microvascular extracellular matrix. Developmental changes during angiogenesis in the aortic ring-plasma clot model. Am J Pathol 128:78–90PubMed
19.
go back to reference Ohberg L, Lorentzon R, Alfredson H (2000) Neovascularisation in Achilles tendons with painful tendinosis not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc 9:233–238 Ohberg L, Lorentzon R, Alfredson H (2000) Neovascularisation in Achilles tendons with painful tendinosis not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc 9:233–238
20.
go back to reference Peterson WW, Manske PR, Dunlap J, Horwitz DS, Kahn B (1990) Effect of various methods of restoring flexor sheath integrity on the formation of adhesion after tendon injury. J Hand Surg [Am]15:48–56 Peterson WW, Manske PR, Dunlap J, Horwitz DS, Kahn B (1990) Effect of various methods of restoring flexor sheath integrity on the formation of adhesion after tendon injury. J Hand Surg [Am]15:48–56
21.
go back to reference Sheehan KM, DeLott LB, Day SM, DeHeer DH (2003) Hyalgan has a dose-dependent differential effect on macrophage proliferation and cell death. J Orthop Res 21:744–775CrossRefPubMed Sheehan KM, DeLott LB, Day SM, DeHeer DH (2003) Hyalgan has a dose-dependent differential effect on macrophage proliferation and cell death. J Orthop Res 21:744–775CrossRefPubMed
22.
go back to reference Szabo RM, Younger E (1990) Effects of indomethacin on adhesion formation after repair zone II tendon lacerations in the rabbit. J Hand Surg [Am] 15:480–483 Szabo RM, Younger E (1990) Effects of indomethacin on adhesion formation after repair zone II tendon lacerations in the rabbit. J Hand Surg [Am] 15:480–483
23.
go back to reference Tang JB, Shi D, Zhang QG (1996) Biomechanical and histologic evaluation of tendon sheath management. J Hand Surg [Am] 21:900–908 Tang JB, Shi D, Zhang QG (1996) Biomechanical and histologic evaluation of tendon sheath management. J Hand Surg [Am] 21:900–908
24.
go back to reference Tuncay I, Ozbek H, Atik B, Ozen S, Akpinar F (2002) Effects of hyaluronic acid on postoperative adhesion of tendo calcaneus surgery: an experimental study in rats. J Foot Ankle Surg 41:104–108PubMed Tuncay I, Ozbek H, Atik B, Ozen S, Akpinar F (2002) Effects of hyaluronic acid on postoperative adhesion of tendo calcaneus surgery: an experimental study in rats. J Foot Ankle Surg 41:104–108PubMed
25.
go back to reference Wiig M, Abrahamson SO (2000) Hyaluronic acid modulates unequally intrasynovial and extrasynovial rabbit tendons in vitro. J Hand Surg [Br] 25:183–187CrossRef Wiig M, Abrahamson SO (2000) Hyaluronic acid modulates unequally intrasynovial and extrasynovial rabbit tendons in vitro. J Hand Surg [Br] 25:183–187CrossRef
26.
go back to reference Wiig MA, Abrahamsson SO, Lundborg G (1997) Tendon repair. Cellular activities in rabbit deep flexor tendons and surrounding synovial sheats and the effects of hyaluronan: an experimental study in vivo and in vitro. J Hand Surg [Am] 22:818–825 Wiig MA, Abrahamsson SO, Lundborg G (1997) Tendon repair. Cellular activities in rabbit deep flexor tendons and surrounding synovial sheats and the effects of hyaluronan: an experimental study in vivo and in vitro. J Hand Surg [Am] 22:818–825
27.
go back to reference Woo SLY, Hildebrand K, Watanabe N, Fenwick CA, Papageorgiou C, Wang JHC (1999) Tissue engineering of ligament and tendon healing. Clin Orthop 367(Suppl):312–323CrossRef Woo SLY, Hildebrand K, Watanabe N, Fenwick CA, Papageorgiou C, Wang JHC (1999) Tissue engineering of ligament and tendon healing. Clin Orthop 367(Suppl):312–323CrossRef
28.
go back to reference Wrenn RN, Goldner JL, Markee JL (1954) An experimental study of the effect of cortisone on the healing process and tensile strength of tendons. J Bone Joint Surg Am 36:588–601 Wrenn RN, Goldner JL, Markee JL (1954) An experimental study of the effect of cortisone on the healing process and tensile strength of tendons. J Bone Joint Surg Am 36:588–601
Metadata
Title
Sodium hyaluronate regulating angiogenesis during Achilles tendon healing
Authors
Mehmet Halici
Sinan Karaoglu
Ozlem Canoz
Sevki Kabak
Ali Baktir
Publication date
01-11-2004
Publisher
Springer-Verlag
Published in
Knee Surgery, Sports Traumatology, Arthroscopy / Issue 6/2004
Print ISSN: 0942-2056
Electronic ISSN: 1433-7347
DOI
https://doi.org/10.1007/s00167-004-0536-2

Other articles of this Issue 6/2004

Knee Surgery, Sports Traumatology, Arthroscopy 6/2004 Go to the issue