A Comparative Study on the Biomechanical and Histological Properties of Bone-to-Bone,Bone-to-Tendon,and Tendon-to-Tendon Healing

Abstract

Background:

Surgical repair around the bone-tendon insertion (BTI) may involve bone-to-bone (BB), bone-to-tendon (BT), or tendon-to-tendon (TT) reattachment with varying healing outcome.

Hypothesis:

The repair of Achilles tendon–calcaneus (ATC) by reattachment of homogeneous tissue (BB or TT) would heal faster, with respect to tensile properties at the healing complex, than those of reattachment of heterogeneous tissues (BT) over time.

Study Design:

Controlled laboratory study.

Methods:

Forty-seven adolescent male Chinese goats were divided into BB, BT, and TT groups. Osteotomy of the calcaneus, reattachment of Achilles tendon to the calcaneus after removal of the insertion, and tenotomy of the Achilles tendon were performed to simulate BB, BT, and TT repair, respectively. The ATC healing complexes were harvested at 6, 12, or 24 weeks postoperatively. Mechanical and morphological properties of the healing ATC complexes were assessed by tensile testing and qualitative histology, respectively. The contralateral intact ATC complex was used as the control.

Results:

Failure load of BT was 33.4% lower than that of TT (P = .0243) at week 12. Ultimate strength of BT was 50.2% and 45.3% lower than that of TT at weeks 12 (P = .0002) and 24 (P = .0001), respectively. Tissue morphological characteristics of the BB and TT groups showed faster remodeling. The BT group showed limited regeneration of fibrocartilage zone and excessive formation of fibrous tissue at the healing interface.

Conclusion:

BTI repair between homogeneous tissues (BB and TT healing) showed better healing quality with respect to mechanical and histological assessments than did healing between heterogeneous tissues (BT healing).

Clinical Relevance:

Anatomic reconstruction of ATC complex injury may be a primary concern when selecting the proper surgical approach. However, it is recommended to select fracture fixation (BB) or tendon repair (TT) instead of bone-tendon reattachment (BT) if possible to ensure better outcome at the healing interface.

Keywords

bone tendon insertion healing Achilles tendon–calcaneus complex goat model mechanical test histological morphology

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References

Archer

Buxton

Hall

Francis-West

. Mechanical regulation of secondary chondrogenesis. Biorheology. 2006;43(3-4):355-370.

Auer

Goodship

Arnoczky

. Refining animal models in fracture research: seeking consensus in optimising both animal welfare and scientific validity for appropriate biomedical use. BMC Musculoskelet Disord. 2007;8:72.

Benjamin

Toumi

Ralphs

Bydder

Best

Milz

. Where tendons and ligaments meet bone: attachment sites (“entheses”) in relation to exercise and/or mechanical load. J Anat. 2006;208(4):471-490.

Biewener

. Musculoskeletal design in relation to body size. J Biomech. 1991;24(suppl 1):19-29.

Carter

Beaupre

Giori

Helms

. Mechanobiology of skeletal regeneration. Clin Orthop Relat Res. 1998;355:S41-S55.

Cheung

Silverio

Sperling

. Strategies in biologic augmentation of rotator cuff repair: a review. Clin Orthop Relat Res. 2010;468(6):1476-1484.

Chim

Miller

Gliniak

Alsberg

. Stromal-cell-derived factor (SDF) 1-alpha in combination with BMP-2 and TGF-β1 induces site-directed cell homing and osteogenic and chondrogenic differentiation for tissue engineering without the requirement for cell seeding. Cell Tissue Res. 2012;350(1):89-94

Chow

Suen

Huang

. Extracorporeal shockwave enhanced regeneration of fibrocartilage in a delayed tendon-bone insertion repair model. J Orthop Res. 2014;32(4):507-514.

Chow

DHK

Suen

. Extracorporeal shockwave therapy for treatment of delayed tendon-bone insertion healing in a rabbit model: a dose-response study. Am J Sports Med. 2012;40(12):2862-2871.

10.

Eliasson

Andersson

Aspenberg

. Rat Achilles tendon healing: mechanical loading and gene expression. J Appl Physiol (1985). 2009;107(2):399-407.

11.

Eliasson

Fahlgren

Aspenberg

. Mechanical load and BMP signaling during tendon repair: a role for follistatin? Clin Orthop Relat Res. 2008;466(7):1592-1597.

12.

Farnebo

Woon

Kim

Pham

Chang

. Reconstruction of the tendon-bone insertion with decellularized tendon-bone composite grafts: comparison with conventional repair. J Hand Surg Am. 2014;39(1):65-74.

13.

S-C

Cheng

W-H

Cheuk

Y-C

. Development of vitamin C irrigation saline to promote graft healing in anterior cruciate ligament reconstruction. J Orthop Transl. 2013;1(1):67-77.

14.

Hettrich

Rodeo

Hannafin

Ehteshami

Shubin Stein

. The effect of muscle paralysis using Botox on the healing of tendon to bone in a rat model. J Shoulder Elbow Surg. 2011;20(5):688-697.

15.

Hibino

Hamada

Sairyo

Yukata

Sano

Yasui

. Callus formation during healing of the repaired tendon-bone junction: a rat experimental model. J Bone Joint Surg Br. 2007;89(11):1539-1544.

16.

Huang

Hagar

Frost

Sun

Cheung

. Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells. 2004;22(3):313-323.

17.

Leung

Qin

Cheung

. A Practical Manual for Musculoskeletal Research. Singapore: World Scientific; 2008.

18.

Leung

K-S

Qin

Chan

. A comparative study of bone to bone repair and bone to tendon healing in patella-patellar tendon complex in rabbits. Clin Biomech (Bristol, Avon). 2002;17(8):594-602.

19.

Liu

Wan

Tan

Wang

Yang

. Preclinical investigation of an innovative magnesium-based bone graft substitute for potential orthopaedic applications. J Orthop Transl. 2014;2(3):139-148.

20.

Qin

Chan

. Area, length and mineralization content of new bone at bone-tendon junction predict its repair quality. J Orthop Res. 2011;29(5):672-677.

21.

Thomopoulos

. Functional attachment of soft tissues to bone: development, healing, and tissue engineering. Annu Rev Biomed Eng. 2013;15:201-226.

22.

Lui

Zhang

Chan

Qin

. Biology and augmentation of tendon-bone insertion repair. J Orthop Surg Res. 2010;5:59.

23.

McCoy

Haddad

. The strength of achilles tendon repair: a comparison of three suture techniques in human cadaver tendons. Foot Ankle Int. 2010;31(8):701-705.

24.

McGuigan

Yoo

Lee

Biewener

. Dynamics of goat distal hind limb muscle-tendon function in response to locomotor grade. J Exp Biol. 2009;212(pt 13):2092-2104.

25.

Meretoja

Dahlin

Kasper

Mikos

. Enhanced chondrogenesis in co-cultures with articular chondrocytes and mesenchymal stem cells. Biomaterials. 2012;33(27):6362-6369.

26.

Lui

PPY

Rui

. Tendon-derived stem cells (TDSCs) promote tendon repair in a rat patellar tendon window defect model. J Orthop Res. 2012;30(4):613-619.

27.

Nunley

. The Achilles Tendon: Treatment and Rehabilitation. New York, NY: Springer; 2009.

28.

O’Conor

Case

Guilak

. Mechanical regulation of chondrogenesis. Stem Cell Res Ther. 2013;4(4):61.

29.

Plate

Brown

Walters

. Advanced age diminishes tendon-to-bone healing in a rat model of rotator cuff repair. Am J Sports Med. 2014;42(4):859-868.

30.

Qin

Leung

Chan

Rosier

. Enlargement of remaining patella after partial patellectomy in rabbits. Med Sci Sports Exerc. 1999;31(4):502-506.

31.

Qin

Wang

Wong

MWN

. Osteogenesis induced by extracorporeal shockwave in treatment of delayed osteotendinous junction healing. J Orthop Res. 2010;28(1):70-76.

32.

Rodeo

Arnoczky

Torzilli

Hidaka

Warren

. Tendon-healing in a bone tunnel: a biomechanical and histological study in the dog. J Bone Joint Surg Am. 1993;75(12):1795-1803.

33.

Rui

Lui

Chan

Lee

Chan

. Mechanical loading increased BMP-2 expression which promoted osteogenic differentiation of tendon-derived stem cells. J Orthop Res. 2011;29(3):390-396.

34.

Sah

Ratcliffe

. Translational models for musculoskeletal tissue engineering and regenerative medicine. Tissue Eng Part B Rev. 2010;16(1):1-3.

35.

Schneider

. Zur Struktur der Sehnenansatzzonen. Z Anat Entwickl Gesch. 1956;119(5):431-456.

36.

Schneider

Buhrmann

Mobasheri

Matis

Shakibaei

. Three-dimensional high-density co-culture with primary tenocytes induces tenogenic differentiation in mesenchymal stem cells. J Orthop Res. 2011;29(9):1351-1360.

37.

Schwartz

Lipner

Pasteris

Genin

Thomopoulos

. Muscle loading is necessary for the formation of a functional tendon enthesis. Bone. 2013;55(1):44-51.

38.

Sharma

Snedeker

. Biochemical and biomechanical gradients for directed bone marrow stromal cell differentiation toward tendon and bone. Biomaterials. 2010;31(30):7695-7704.

39.

Sharma

Snedeker

. Paracrine interactions between mesenchymal stem cells affect substrate driven differentiation toward tendon and bone phenotypes. PLoS One. 2012;7(2):e31504.

40.

Shi

Cheung

Qin

Leung

. Low-magnitude high-frequency vibration treatment augments fracture healing in ovariectomy-induced osteoporotic bone. Bone. 2010;46(5):1299-1305.

41.

Thomopoulos

Hattersley

Rosen

. The localized expression of extracellular matrix components in healing tendon insertion sites: an in situ hybridization study. J Orthop Res. 2002;20(3):454-463.

42.

Thomopoulos

Marquez

Weinberger

Birman

Genin

. Collagen fiber orientation at the tendon to bone insertion and its influence on stress concentrations. J Biomech. 2006;39(10):1842-1851.

43.

Walsh

. Repair and Regeneration of Ligaments, Tendons, and Joint Capsule. Totowa, NJ: Humana Press; 2006.

44.

Wang

I-NE

Mitroo

Chen

Doty

. Age-dependent changes in matrix composition and organization at the ligament-to-bone insertion. J Orthop Res. 2006;24(8):1745-1755.

45.

Wang

Chen

Yang

Chan

Qin

. Postoperative programmed muscle tension augmented osteotendinous junction repair. Int J Sports Med. 2007;28(8):691-696.

46.

Wong

Qin

Lee

. Healing of bone-tendon junction in a bone trough: a goat partial patellectomy model. Clin Orthop Relat Res. 2003;413:291-302.

47.

Wong

MWN

Qin

Lee

Leung

K-S

. Articular cartilage increases transition zone regeneration in bone-tendon junction healing. Clin Orthop Relat Res. 2009;467(4):1092-1100.

48.

Woo

Gomez

Seguchi

Endo

Akeson

. Measurement of mechanical properties of ligament substance from a bone-ligament-bone preparation. J Orthop Res. 1983;1(1):22-29.

49.

Wren

Yerby

Beaupre

Carter

. Influence of bone mineral density, age, and strain rate on the failure mode of human Achilles tendons. Clin Biomech (Bristol, Avon). 2001;16(6):529-534.

50.

. Circulating mesenchymal stem cells and their clinical implications. J Orthop Transl. 2014;2(1):1-7.

51.

Zhang

Pan

Wang

JHC

. Cryotherapy suppresses tendon inflammation in an animal model. J Orthop Transl. 2014;2(2):75-81.

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