Iranian Journal of Veterinary Surgery

Iranian Journal of Veterinary Surgery

Radiographic and Histopathologic Evidences of Movement versus Immobilization Effects on Enthesis Formation in Rabbits

Document Type : Original Article

Authors
Neda Erfani 1
Siamak Kazemi-Darabadi 1
Seyed Mohammad Hashemi-Asl 2
Amir Ali Shahbazfar 3
1 Department of Clinical Sciences, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.
2 Department of Surgery and Diagnostic Imaging, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.
3 Department of Pathobiology, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, Iran.
10.30500/ivsa.2021.289128.1264
Abstract
Enthesis joins tendon, ligament, or joint capsule to the bone, which are two very different tissues. As a result, it is more prone to stress and increased risk of rupture. The purposes of this study were to evaluate the role of limb movement or immobilization in enthesis healing after surgical repair and found out if radiography could be a reliable method for determining its prognosis. Fourteen New Zealand white rabbits were randomly divided into two groups. After detaching the Achilles tendon from the bone surface, the tendon was re-attached to the bone with a modified Kessler suture pattern. The limb of group 1 rabbits was externally fixed with the fiberglass cast. In group 2, however, no cast was used. Radiographs were taken after surgery and in weeks 2, 4, 6, and 8 post-operation. Samples were taken from the area after 8 weeks and stained by the hematoxylin-eosin method. The results were reported descriptively. Bone growth, increased chondrocytes in the cartilaginous region, and increased fibroblasts and fibrocytes were seen in group 1. While erosion, collagen fibers regularity, and tissue maturity were more predominant in group 2. Although early limb movement during the enthesis healing period helps to increase the regularity of collagen fibers in the tendinous zone of the enthesis, it does not increase the amount of callus in the bone and increases the risk of bone erosions and even fractures. While stabilizing the limb in the first two months of enthesis healing protects the bone against the forces and helps bone formation, which has a positive role in healing the enthesis.
Keywords
Tendon-to-bone junction
Enthesis
Movement
Rabbit
Radiography

Subjects

  1. Benjamin M, McGonagle D. Entheses: tendon and ligament attachment sites. Scandinavian Journal of Medicine and Science in Sports. 2009; 19(4): 520-527.
  2. Shaw HM, Benjamin M. Structure–function relationships of entheses in relation to mechanical load and exercise. Scandinavian Journal of Medicine and Science in Sports. 2007; 17(4): 303-315.
  3. Thomopoulos S, Genin GM, Galatz LM. The development and morphogenesis of the tendon-to-bone insertion. What development can teach us about healing? Journal of Musculoskeletal and Neuronal Interactions. 2020; 10(1): 35.
  4. Bunker DLJ, Ilie V, Ilie V, Nicklin S. Tendon to bone healing and its implications for surgery. Muscles, Ligaments and Tendons Journal. 2014; 4(3): 343.
  5. Noyes FR, DeLucas JL, Torvik PJ. Biomechanics of anterior cruciate ligament failure: an analysis of strain-rate sensitivity and mechanisms of failure in primates. Journal of Bone and Joint Surgery. 1974; 56: 236-253.
  6. Saadat F, Deymier AC, Birman V, Thomopoulos S, Genin GM. The concentration of stress at the rotator cuff tendon-to-bone attachment site is conserved across species. Journal of the Mechanical Behavior of Biomedical Materials. 2016; 62: 24-32.
  7. Kyung, HS, Kim SY, Oh CW, Kim SJ. Tendon-to-bone tunnel healing in a rabbit model: the effect of periosteum augmentation at the tendon-to-bone interface. Knee Surgery, Sports Traumatology, Arthroscopy. 2003; 11(1): 9-15.
  8. Martinek V, Latterman C, Usas A, Abramowitch S, Woo SL, Fu FH, Huard J. Enhancement of tendon-bone integration of anterior cruciate ligament grafts with bone morphogenetic protein-2 gene transfer: a histological and biomechanical study. Journal of Bone and Joint Surgery. 2002; 84(7): 1123-1131.
  9. Lim JK, Hui J, Li L, Thambyah A, Goh J, Lee EH. Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction. Arthroscopy: Journal of Arthroscopic and Related Surgery. 2004; 20(9): 899-910.
  10. Mihelic R, Pecina M, Jelic M, Zoricic S, Kusec V, Simic P, Bobinac D, Lah B, Legovic D, Vukicevic S. Bone morphogenetic protein–7 (osteogenic protein–1) promotes tendon graft integration in anterior cruciate ligament reconstruction in sheep. American Journal of Sports Medicine. 2004; 32(7): 1619-1625.
  11. Yamazaki S, Yasuda K, Tomita F, Tohyama H, Minami A. The effect of transforming growth factor-β1 on intraosseous healing of flexor tendon autograft replacement of anterior cruciate ligament in dogs. Arthroscopy: The Journal of Arthroscopic & Related Surgery. 2005; 21(9): 1034-1041.
  12. Lu HH, Thomopoulos S. Functional attachment of soft tissues to bone: development, healing, and tissue engineering. Annual Review of Biomedical Engineering. 2013; 15: 201-226.
  13. Eliasson P, Andersson T, Aspenberg P. Achilles tendon healing in rats is improved by intermittent mechanical loading during the inflammatory phase. Journal of Orthopaedic Research. 2012; 30(2): 274-279.
  14. Yershov AL, Jordan BS, Fudge JM, Dubick MA. Influence of the mode of ventilation on ketamine/xylazine requirements in rabbits. Veterinary Anaesthesia and Analgesia. 2007; 34(3): 157-163.
  15. Tan H, Wang D, Lebaschi AH, Hutchinson ID, Ying L, Deng XH, Rodeo SA, Warren RF. Comparison of bone tunnel and cortical surface tendon-to-bone healing in a rabbit model of biceps tenodesis. The Journal of Bone and Joint Surgery. 2018; 100(6): 479-486.
  16. Fujioka H, Thakur R, Wang GJ, Mizuno K, Balian G, Hurwitz SR. Comparison of surgically attached and non-attached repair of the rat Achilles tendon-bone interface. Cellular organization and type X collagen expression. Connective Tissue Research. 1998; 37(3-4): 205-218.
  17. Zhou J, Koike Y, Uhthoff HK, Trudel G. Quantitative histology and ultrastructure fail to explain weakness of immobilized rabbit Achilles’ tendons. Archives of Physical Medicine and Rehabilitation. 2007; 88(9): 1177-1184.
  18. Sharma P, Maffulli N. Tendon injury and tendinopathy: Healing and Repair. Journal of Bone and Joint Surgery. 2005; 87(1): 187-202.
  19. Benjamin M, Toumi H, Ralphs JR, Bydder G, Best TM, Milz S. Where tendons and ligaments meet bone: attachment sites (‘entheses’) in relation to exercise and/or mechanical load. Journal of Anatomy. 2006; 208(4): 471-490.
  20. Dovan TT, Ritty T, Ditsios K, Silva MJ, Kusano N, Gelberman RH. Flexor digitorum profundus tendon to bone tunnel repair: a vascularization and histologic study in canines. Journal of Hand Surgery. 2005; 30(2): 246-257.
  21. Uhthoff HK, Seki M, Backman DS, Trudel G, Himori K, Sano H. Tensile strength of the supraspinatus after reimplantation into a bony trough: an experimental study in rabbits. Journal of Shoulder and Elbow Surgery. 2002; 11(5): 504-509.
  22. Wong MW, Qin L, Lee KM, Tai KO, Chong WS, Leung KS, Chan KM. Healing of bone-tendon junction in a bone trough: a goat partial patellectomy model. Clinical Orthopaedics and Related Research. 2003; 413: 291-302.
  23. Thomopoulos S, Williams GR, Gimbel JA, Favata M, Soslowsky LJ. Variation of biomechanical, structural, and compositional properties along the tendon to bone insertion site. Journal of Orthopaedic Research. 2003; 21(3): 413-419.
  24. Silva MJ, Boyer MI, Ditsios K, Burns ME, Harwood FL, Amiel D, Gelberman RH. The insertion site of the canine flexor digitorum profundus tendon heals slowly following injury and suture repair. Journal of Orthopaedic Research. 2002; 20(3): 447-453.
  25. Walsh WR, Harrison JA, Van Sickle D, Alvis M, Gillies RM. Patellar tendon-to-bone healing using high-density collagen bone anchor at 4 years in a sheep model. American Journal of Sports Medicine. 2004; 32(1): 91-95.
  26. Soda Y, Sumen Y, Murakami Y, Ikuta Y, Ochi M. Attachment of autogenous tendon graft to cortical bone is better than to cancellous bone: a mechanical and histological study of MCL reconstruction in rabbits. Acta Orthopaedica Scandinavica. 2003; 74(3): 322-326.
  27. St Pierre P, Olson EJ, Elliott JJ, O'Hair KC, McKinney LA, Ryan J. Tendon-healing to cortical bone compared with healing to a cancellous trough. A biomechanical and histological evaluation in goats. Journal of Bone and Joint Surgery. 1995; 77(12): 1858-1866.
  28. Aoki M, Oguma H, Fukushima S, Ishii S, Ohtani S, Murakami G. Fibrous connection to bone after immediate repair of the canine infraspinatus: the most effective bony surface for tendon attachment. Journal of Shoulder and Elbow Surgery. 2001; 10(2): 123-128.
  29. Kachlik D, Baca V, Cepelik M, Hajek P, Mandys V, Musil V. Clinical anatomy of the calcaneal tuberosity. Annals of Anatomy-Anatomischer Anzeiger. 2008; 190(3): 284-291.
  30. Sano H, Kumagai J, Sawai T. Experimental fascial autografting for the supraspinatus tendon defect: remodeling process of the grafted fascia and the insertion into bone. Journal of Shoulder and Elbow Surgery. 2002; 11(2): 166-173.
  31. Leung KS, Qin L, Fu LK, Chan CW. A comparative study of bone to bone repair and bone to tendon healing in patella–patellar tendon complex in rabbits. Clinical Biomechanics. 2002; 17(8): 594-602.
  32. Hibino N, Hamada Y, Sairyo K, Yukata K, Sano T, Yasui N. Callus formation during healing of the repaired tendon-bone junction: a rat experimental model. Journal of Bone and Joint Surgery. 2007; 89(11): 1539-1544.
  33. Newsham‐West R, Nicholson H, Walton M, Milburn P. Long‐term morphology of a healing bone–tendon interface: a histological observation in the sheep model. Journal of Anatomy. 2007; 210(3): 318-327.
  34. Benjamin M, Toumi H, Suzuki D, Redman S, Emery P, McGonagle D. Microdamage and altered vascularity at the enthesis–bone interface provides an anatomic explanation for bone involvement in the HLA–B27–associated spondylarthritides and allied disorders. Arthritis & Rheumatism. 2007; 56(1): 224-233.
  35. Gimbel JA, Van Kleunen JP, Williams GR, Thomopoulos S, Soslowsky LJ. Long durations of immobilization in the rat result in enhanced mechanical properties of the healing supraspinatus tendon insertion site. Journal of Biomechanical Engineering. 2007; 129: 400-404.
  36. Thomopoulos S, Williams GR, Soslowsky LJ. Tendon to bone healing: differences in biomechanical, structural, and compositional properties due to a range of activity levels. Journal of Biomechanical Engineering. 2003; 125(1): 106-113.
  37. Kamps BS, Linder LH, DeCamp CE, Haut RC. The influence of immobilization versus exercise on scar formation in the rabbit patellar tendon after excision of the central third. American Journal of Sports Medicine. 1994; 22(6): 803-811.
  38. Hettrich CM, Gasinu S, Beamer BS, Stasiak M, Fox A, Birmingham P, Ying O, Deng XH, Rodeo SA. The effect of mechanical load on tendon-to-bone healing in a rat model. American Journal of Sports Medicine. 2014; 42(5): 1233-1241.
  39. Frank C, MacFarlane B, Edwards P, Rangayyan R, Liu ZQ, Walsh S, Bray R. A quantitative analysis of matrix alignment in ligament scars: a comparison of movement versus immobilization in an immature rabbit model. Journal of Orthopaedic Research. 1991; 9(2): 219-227.
  40. Gelberman RH, Manske PR, Akeson WH, Woo SL, Lundborg G, Amiel D. Flexor tendon repair. Journal of Orthopaedic Research. 1986; 4(1): 119-128.
  41. Peltz CD, Sarver JJ, Dourte LM, Würgler‐Hauri CC, Williams GR, Soslowsky LJ. Exercise following a short immobilization period is detrimental to tendon properties and joint mechanics in a rat rotator cuff injury model. Journal of Orthopaedic Research. 2010; 28(7): 841-845.
  42. Schwartz AG, Lipner JH, Pasteris JD, Genin GM, Thomopoulos S. Muscle loading is necessary for the formation of a functional tendon enthesis. Bone. 2013; 55(1): 44-51.
  43. Atesok K, Fu FH, Wolf MR, Ochi M, Jazrawi LM, Doral MN, Lubowitz JH, Rodeo SA. Augmentation of tendon-to-bone healing. Journal of Bone and Joint Surgery. 2014; 96(6): 513-521.

  • Receive Date 03 June 2021
  • Revise Date 22 July 2021
  • Accept Date 28 August 2021
  • First Publish Date 28 August 2021