Clin Orthop Surg.  2018 Mar;10(1):99-110. 10.4055/cios.2018.10.1.99.

Enhanced Tendon-to-Bone Healing of Chronic Rotator Cuff Tears by Bone Marrow Aspirate Concentrate in a Rabbit Model

• Liu XN
• Yang CJ
• Kim JE
• Du ZW
• Ren M
• Zhang W
• Zhao HY
• Kim KO
• Noh KC

• KMID: 2405489
• DOI: http://doi.org/10.4055/cios.2018.10.1.99

Abstract

BACKGROUND
To evaluate the influence of bone marrow aspirate concentrate (BMAC) on tendon-to-bone healing in a rabbit rotator cuff model and to characterize the composition of growth factors in BMAC.
METHODS
In this in vivo study, 40 rabbits were allocated into five groups: control (C), repair + saline (RS), repair + platelet-rich plasma (PRP; RP), repair + BMAC (RB) and repair + PRP + BMAC (RPB). A tear model was created by supraspinatus tendon transection at the footprint. Six weeks after transection, the torn tendon was repaired along with BMAC or PRP administration. Six weeks after repair, shoulder samples were harvested for biomechanical and histological testing. Ten rabbits were used for processing PRP and BMAC, followed by analysis of blood cell composition and the levels of growth factors in vitro.
RESULTS
The ultimate load-to-failure was significantly higher in RPB group compared to RS group (p = 0.025). BMAC-treated groups showed higher values of biomechanical properties than RS group. The histology of BMAC-treated samples showed better collagen fiber continuity and orientation than RS group. BMAC contained significantly higher levels of the several growth factors than PRP.
CONCLUSIONS
Locally administered BMAC enhanced tendon-to-bone healing and has potential for clinical applications.

Keyword

Bone marrow; Platelet-rich plasma; Rotator cuff

MeSH Terms

Blood Cells
Bone Marrow*
Collagen
In Vitro Techniques
Intercellular Signaling Peptides and Proteins
Platelet-Rich Plasma
Rabbits
Rotator Cuff*
Shoulder
Tears*
Tendons
Collagen
Intercellular Signaling Peptides and Proteins

Figure

• 

  Fig. 1 Flowchart of the in vivo study. PRP: platelet-rich plasma, BMAC: bone marrow aspirate concentrate.

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  Fig. 2 Creation of a chronic rotator cuff tear model. The supraspinatus tendon is completely detached at the insertion site and wrapped with a Penrose drain to inhibit adhesion to the surrounding tissue. The black arrow indicates the greater tuberosity and the white arrow indicates the supraspinatus tendon.

• 

  Fig. 3 (A) Repair of the torn supraspinatus tendon to the greater tuberosity in an open transosseous manner. The black arrow indicates the greater tuberosity. (B) Each suture end is then tied over the lateral humeral cortex, reattaching the supraspinatus tendon to the footprint. The white arrow indicates the repaired supraspinatus tendon.

• 

  Fig. 4 (A) AGS-X materials testing machine (Shimadzu, Japan). (B) Fixture clamping system. (C) Tensile testing of the repaired supraspinatus tendon.

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  Fig. 5 Biomechanical tests among the groups. (A) The ultimate load-to-failure is significantly higher in the repair + PRP + BMAC (RPB) group than the repair + saline (RS) group. (B) Stiffness is significantly higher in the repair + BMAC (RB) group than both the RS and repair + PRP (RP) groups. (C) The Young's modulus is significantly lower in all experimental groups than the control group. (D) Yield strength of the RB and RPB groups showed no statistical differences from the control group. Asterisks and error bars show the statistical difference between the two groups (*p < 0.05). C: control, PRP: platelet-rich plasma, BMAC: bone marrow aspirate concentrate.

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  Fig. 6 Tendon-to-bone interface H&E staining shows increased cellular and vascular fibrous tissues in the four groups: (A) repair + saline (RS) group, (B) repair + platelet-rich plasma (RP) group, (C) repair + bone marrow aspirate concentrate (RB) group, and (D) repair + platelet-rich plasma + bone marrow aspirate concentrate (RPB) group.

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  Fig. 7 Masson-trichrome staining demonstrates better collagen fiber continuity and arrangement at tendon-to-bone attachment sites in the bone marrow aspirate concentrate (BMAC)-treated groups: (A) repair + saline (RS) group, (B) repair + platelet-rich plasma (RP) group, (C) repair + BMAC (RB) group, and (D) repair + platelet-rich plasma + BMAC (RPB) group. The arrows indicate the improved collagen fiber continuity and arrangement of the RB and RPB groups compared to the control and RS groups. Collagen fibers run parallel along the tendon-to-bone attachment sites (in this figure, they run diagonally). However, there are few collagen fibers in the control and RS groups.

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  Fig. 8 The platelet counts (A) and WBC counts (B) of BMA and peripheral blood series. Asterisks and error bars show the statistical difference between the two groups (*p < 0.05, **p < 0.01). WB: whole blood, PRP: platelet-rich plasma, BMA: bone marrow aspirate, BMAC: bone marrow aspirate concentrate, WBC: white blood cell.

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  Fig. 9 Growth factor levels in BMA and peripheral blood. (A) Platelet-derived growth factor-AB level. (B) Insulin-like growth factor 1 level. (C) Transforming growth factor beta 1 level. (D) Vascular endothelial growth factor level. Asterisks and error bars show the statistical difference between the two groups (*p < 0.05, **p < 0.01). WB: whole blood, PRP: platelet-rich plasma, BMA: bone marrow aspirate, BMAC: bone marrow aspirate concentrate.

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