Effect of lyophilized amniotic membrane, hyaluronic acid, and their combination in preventing adhesion after tendon repair in New Zealand white rabbits

  • Syaiful A. Hadi Department of Orthopaedic & Traumatology, Faculty of Medicine, Universitas Indonesia, Jakarta
  • Jefri Sukmawan Department of Orthopaedic & Traumatology, Faculty of Medicine, Universitas Indonesia, Jakarta
Keywords: hyaluronic acid, lyophilized amniotic membrane, peritendinous adhesion, repaired tendon
Abstract viewed: 1561 times
PDF downloaded: 660 times


Background: Several promising methods to reduce the peritendinous adhesion after repair include amniotic membrane and hyaluronic acid application on the repaired tendon site. This study aimed to compare the effect of lyophilized amniotic membrane, application of hyaluronic acid, and their combination in preventing peritendinous adhesion after tendon repair in New Zealand white rabbits.

Methods: 64 flexor digitorum fibularis tendon from 16 rabbits were cut and then repaired by modified Kessler technique. Samples were allocated into four test groups; group I as control had simple tendon repair, group II had amniotic membrane wrapping at repair site, group III had hyaluronic acid application at repair site, and group IV had combination of amniotic membrane wrapping and hyaluronic acid application. On 6th week, 8 tendon from each group underwent macroscopic and histologic evaluation of peritendon adhesion by Tang scoring system. The rest of samples were evaluated for tendon gliding at tenth week by measuring active and passive range of motion of metatarsophalangeal joint.

Results: At 6th week, macroscopic and histologic evaluation showed that groups II, III, and IV had significantly lower peritendinous adhesion compared to control group (p < 0.05). However, there was no significant difference found among groups II, III, and IV (p > 0.05). Similar results were found in tendon gliding evaluation, groups II, III, and IV had significantly better range of motion compared to control group (p < 0.05), but there was no significant difference found between these groups (p > 0.05).

Conclusion: The application of lyophilized amniotic membrane, hyaluronic acid, or their combination significantly reduce the formation of peritendinous adhesion in repaired flexor digitorum fibularis tendon in rabbit model.


Download data is not yet available.

Author Biography

Syaiful A. Hadi, Department of Orthopaedic & Traumatology, Faculty of Medicine, Universitas Indonesia, Jakarta

Senior Lecturer, Hand Surgery Consultant,

Departement of Orthopaedic and Traumatology RSCM / FMUI


  1. Ozgenel GY. The effects of a combination of hyaluronic and amniotic membrane on the formation of peritendineous adhesions after flexor tendon surgery in chickens. J Bone Joint Surg Br. 2004;86(2):301-7. http://dx.doi.org/10.1302/0301-620X.86B2.14435

  2. Peterson WW, Manske PR, Dunlap J, Horwitz DS, Kahn B. Effect of various methods of restoring flexor sheath integrity on the formation of adhesions after tendon injury. J Hand Surg Am. 1990;15(1):48-56. http://dx.doi.org/10.1016/S0363-5023(09)91105-4

  3. Beredjiklian PK. Biologic aspects of flexor tendon laceration and repair. J Bone Joint Surg Am. 2003;85-A(3):539-50.

  4. Sharma P, Maffulli N. Biology of tendon injury: healing, modeling, remodeling. J Musculoskelet Neuronal Interact. 2006;6(2):181-90.

  5. Szabo RM, Younger E. Effects of indomethacin on adhesion formation after repair of zone II tendon laceratios in the rabbit. J Hand Surg Am. 1990;15(3):480-3. http://dx.doi.org/10.1016/0363-5023(90)90066-Z

  6. Speer DP, Feldman S, Chvrapil M. The control of peritendinous adhesions using topical beta-aminopropionitrile base. J Surg Res. 1985;38(3):252-7. http://dx.doi.org/10.1016/0022-4804(85)90034-4

  7. Moran SL, Ryan CK, Orlando GS, Pratt CE, Michalko KB. Effect of 5-fluorouracil on flexor tendon repair. J Hand Surg Am. 2000;25(2):242-51. http://dx.doi.org/10.1053/jhsu.2000.jhsu25a0242

  8. Komurcu M, Akkus O, Basbozkurt M, Gur E, Akkas N. Reduction of restrictive adhesions by local aprotinin application and primary sheath repair in surgically traumatized flexor tendons of the rabbit. J Hand Surg Am. 1997;22(5):826-32. http://dx.doi.org/10.1016/S0363-5023(97)80076-7

  9. Hagberg L, Gerdin B. Sodium hyaluronate as an adjunct in adhesion prevention after flexor tendon surgery in rabbits. J Hand Surg Am. 1992;17(5):935-41. http://dx.doi.org/10.1016/0363-5023(92)90474-4

  10. Tuncay I, Ozbek H, Atik B, Ozen S, Akpinar F. Effects of hyaluronic acid on postoperative adhesion of tendocalcaneous surgery: an experimental study in rats. J Foot Ankle Surg. 2002;41(2):104-8. http://dx.doi.org/10.1016/S1067-2516(02)80033-3

  11. Strauch B, de Moura W, Ferder M, Hall C, Sagi A, Greenstein B. The fate of tendon healing after restoration of the integrity of the tendon sheath with autogenous vein grafts. J Hand Surg Am. 1985;10:790-5. http://dx.doi.org/10.1016/S0363-5023(85)80153-2

  12. Hanff G, Hagberg L. Prevention of restrictive adhesions with expanded polytetrafluoroethylene diffusable membrane following flexor tendon repair: an experimental study in rabbits. J Hand Surg Am. 1998;23(4):658-64. http://dx.doi.org/10.1016/S0363-5023(98)80052-X

  13. Stark HH, Boyes JH, Johnson L, Asworth CR. The use of paratenon, polyethylene film, or silastic sheeting to prevent restricting adhesions to tendons in the hand. J Bone Joint Surg Am. 1977;59(7):908-13.

  14. Tang JB, Shi D, Zhag QG. Biomechanical and histologic evaluation of tendon sheath management. J Hand Surg Am. 1996;21(5):900-8. http://dx.doi.org/10.1016/S0363-5023(96)80212-7

  15. Colocho G, Graham WP III, Greene AE, Matheson DW, Lynch D. Human amniotic membrane as physiologic wound dressing. Arch Surg. 1974;109(3):370-3. http://dx.doi.org/10.1001/archsurg.1974.01360030022006

  16. Talmi YP, Finkelstein Y, Zohar Y. Use of human amniotic membrane as a biologic dressing. Eur J Plast Surg. 1990;13(4):160-2. http://dx.doi.org/10.1007/BF00236370

  17. Azuara-Blanco A, Pillai CT, Dua HS. Amniotic membrane transplantation for ocular surface reconstruction. Br J Ophthalmol. 1999;83(4):399-402. http://dx.doi.org/10.1136/bjo.83.4.399

  18. Tancer ML, Katz M, Veridiano NP. Vaginal epithelialization with human amnion. Obstet Gynecol. 1979;54(3):345-9.

  19. Zohar Y, Talmi YP, Finkelstein Y, Shvili Y, Sadov R, Laurian N. Use of human amniotic membrane in otolaryngologic practice. Laryngoscope. 1987;97:978-80. http://dx.doi.org/10.1288/00005537-198708000-00018

  20. Badawy SZ, Baggish MS, ElBakry MM, Baltoyannis P. Evaluation of tissue healing and adhesion formation after an intraabdominal amniotic membrane graft in the rat. J Reprod Med. 1989;34(3):198-202.

  21. Young RL, Cota J, Zund G, Mason BA, Wheeler JM. The use of an amniotic membrane graft to prevent postoperative adhesions. Fertil Steril. 1991;55(3):624-8.

  22. Bennett NT, Schultz GS. Growth factors and wound healing: biochemical properties of growth factors and their receptors. Am J Surg. 1993;165(6):728-37. http://dx.doi.org/10.1016/S0002-9610(05)80797-4

  23. Chang J, Thunder R, Most D, Longaker MT, Lineaweaver WC. Studies in flexor tendon wound healing: neutralizing antibody to TGF-[beta]1 increases postoperative range of motion. Plast Reconstr Surg. 2000;105(1):148-55. http://dx.doi.org/10.1097/00006534-200001000-00025

  24. Amiel D, Ishizue K, Billings EJr, Wiig M, Vande Berg J, Akeson WH, et al. Hyaluronan in flexor tendon repair. J Hand Surg Am. 1989;14(5):837-43. http://dx.doi.org/10.1016/S0363-5023(89)80085-1

  25. Potenza AD. Critical evaluation of flexor-tendon healing and adhesion formation within artificial digital sheaths. J Bone Joint Surg Am. 1963;45(6):1217-33.

  26. Akle CA, Adinolfi M, Welsh KI, Leibowitz S, McColl I. Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet. 1981;2(8254):1003-5. http://dx.doi.org/10.1016/S0140-6736(81)91212-5

  27. Ozgenel GY, Samli B, Ozcan M. Effects of human amniotic fluid on peritendinous adhesion formation and tendon healing after flexor tendon surgery in rabbits. J Hand Surg Am. 2001;26(2):332-9. http://dx.doi.org/10.1053/jhsu.2001.22524

  28. Rahmadian R, Ismono D, Chaidir MR, Hidajat NN, Yusuf M. Pengaruh penggunaan membran amnion liofilisasi terhadap pencegahan pembentukan adhesi peritendon pada penyembuhan ruptur tendon achilles kelinci [thesis]. Mount Pleasant (MI): Departement Orthopaedi dan Traumatologi FKUP/RSHS; 2006. Indonesian.

  29. Hagberg L, Tengbald A, Gerdin B. Hyaluronic acid in flexor tendon sheath fluid after sheath reconstruction in rabbits. A comparison between tendon sheath transplantation and conventional two stage procedures. Scand J Plast Reconstr Hand Surg. 1991;25(2):103-7. http://dx.doi.org/10.3109/02844319109111269

  30. Yoneda M, Yamagata M, Suzuki S, Kimata K. Hyaluronic acid modulates proliferation of mouse dermal fibroblasts in culture. J Cell Sci. 1988;90:265-73.

  31. Rydell N. Decreased granulation tissue reaction after installment of hyaluronic acid. Acta Orthop Scan. 1970;41(3):307-11. http://dx.doi.org/10.3109/17453677008991516

  32. Dahlgren C, Bjorksten B. Effect of hyaluronic acid on polymorphonuclear leucocyte cell surface properties. Scand J Haematol. 1982;28(5):376-80. http://dx.doi.org/10.1111/j.1600-0609.1982.tb00542.x

  33. Hagberg L, Tengblad A, Gerdin B. Elimination of exogenously injected sodium-hyaluronate from rabbit flexor tendon sheaths. J Orthop Res. 1991;9(6):792-7. http://dx.doi.org/10.1002/jor.1100090604

  34. Meyers SA, Seaber AV, Glisson RR, Nunley JA. Effect of hyaluronic acid/chondroitin sulfate on healing of full-thickness tendon lacerations in rabbits. J Orthop Res. 1989;7(5):683-9. http://dx.doi.org/10.1002/jor.1100070508

  35. Comper WD, Laurent TC. Physiological function of connective tissue polysaccharides. Physiol Rev. 1978;58(1):255-315.

  36. Hagberg L. Exogenous hyaluronate as an adjunct in the prevention of adhesions after flexor tendon surgery: a controlled clinical trial. J Hand Surg. 1992;17(1):132-6. http://dx.doi.org/10.1016/0363-5023(92)90128-C

  37. Hellström S, Laurent C. Hyaluronan and healing of tympanic membrane perforations. An experimental study. Acta Otolaryngol Suppl. 1987;442:54-61. http://dx.doi.org/10.3109/00016488709102840

  38. Bentley JP. Rate of chondroitin sulfate formation in wound healing. Ann Surg. 1967;165(2):186-91. http://dx.doi.org/10.1097/00000658-196702000-00004

  39. Higa K, Shimmura S, Shimazaki J, Tsubota K. Hyaluronic acid-CD44 interaction mediates the adhesion of lymphocytes by amniotic membrane stroma. Cornea. 2005;24(2):206-12. http://dx.doi.org/10.1097/01.ico.0000133999.45262.83

How to Cite
Hadi SA, Sukmawan J. Effect of lyophilized amniotic membrane, hyaluronic acid, and their combination in preventing adhesion after tendon repair in New Zealand white rabbits. Med J Indones [Internet]. 2014Jul.2 [cited 2024Jul.15];23(2):65-3. Available from: http://mji.ui.ac.id/journal/index.php/mji/article/view/932
Basic Medical Research