Differentiation Ability of Tendon-Derived Stem Cells and Histological Characteristics of Rotator Cuff Remnant on the Greater Tuberosity Degenerated With Age and Chronicity

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Differentiation Ability of Tendon-Derived Stem Cells and Histological Characteristics of Rotator Cuff Remnant on the Greater Tuberosity Degenerated With Age and Chronicity
Song Zhao
Correspondence
Address correspondence to Jinzhong Zhao, M.D; and Song Zhao, M.D., Department of Sports Medicine, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, 600 Yishan Road, Shanghai, China.
Jinzhong Zhao
Correspondence
Address correspondence to Jinzhong Zhao, M.D; and Song Zhao, M.D., Department of Sports Medicine, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, 600 Yishan Road, Shanghai, China.
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Published:September 30, 2021DOI: https://doi.org/10.1016/j.arthro.2021.09.027
Next ArticleEditorial Commentary: Tendon-Derived Stem Cells Are in the Rotator Cuff Remnant and Decline With Age and Tear Chronicity—But the Clinical Relevance Is Not Known
Purpose
To explore and measure the presence and activity of tendon-derived stem cells (TDSCs), as well as histological changes of rotator cuff remnant by age and chronicity of the rotator cuff tear (RCT).
Methods
154 patients with a full-thickness tear of supraspinatus and/or infraspinatus tendon were included. 52 qualified remnants of the greater tuberosity were captured through arthroscopy. TDSCs in the remnants were isolated for proliferation ability, basal gene expression, and trilineage differentiation detection. Histological characteristics were evaluated by observation of staining under a light microscope and transmission electron microscopy (TEM). To observe the effect of age, samples were divided into two groups: young (＜60 years old) and old (≥60 years old). For chronicity comparison, samples were divided into three groups: acute group (＜3 months), intermediate group (3-12 months), and chronic group (≥12 months).
Results
Between age groups, the remnants in older patients were found to have lower TDSC proliferation ability (cell counting kit-8 results, old: .5325 ± .050, young: .6623 ± .196; P = .008) and basal expression of aggrecan (.630 ± .239; P = .002) and TGF-β1 (transforming growth factor-β1, .589 ± .326, P = .008), weaker ability of chondrogenic differentiation. Furthermore, the remnant tendons in chronic group was found to have weaker adipogenic and chondrogenic differentiation ability of TDSCs, lower tendon degenerative score (acute: 3.57 ± 1.902, intermediate: 5.94 ± 2.313, chronic: 6.86 ± 2.193; P = .023), increased type III collagen region ratio in insertion area (acute: 86.10% ± 8.29%, intermediate: 94.06% ± 5.36%, chronic: 98.90% ± .49%; P = .023), and larger fibril diameters.
Conclusion
Differentiation ability of TDSCs derived from the rotator cuff remnant was reduced with age and chronicity. Histological degeneration of remnant tendon deteriorated with chronicity. Remnant in the greater tuberosity was still alive, but those in young or acute injury patients were more active after full-thickness RCT.
Clinical Relevance
TDSCs exist in rotator cuff remnant on the greater tuberosity and have multilineage differentiation ability. But the remnant degenerated with age and chronicity.
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Seo J.
Chun Y.
Arthroscopic repair of massive contracted rotator cuff tears: Aggressive release with anterior and posterior interval slides do not improve cuff healing and integrity.
J Bone Joint Surg Am. 2013; 95: 1482-1488
The outcome and repair integrity of completely arthroscopically repaired large and massive rotator cuff tears.
J Bone Joint Surg Am. 2004; 86: 219-224
Lunsjö K.
Frobell R.
Early repair of trauma-related full-thickness rotator cuff tears does not eliminate the problem of healing failure.
Bone Joint J. 2019; : 603-609
Risk factors affecting rotator cuff retear after arthroscopic repair: A meta-analysis and systematic review.
J Shoulder Elbow Surg. 2021; S1058-2746: 00477-00478
Kawaguchi Y.
Kitamura N.
Effects of remnant tissue preservation on clinical and arthroscopic results after anatomic double-bundle anterior cruciate ligament reconstruction.
Am J Sports Med. 2015; 43: 1882-1892
Sonographic differences in the appearance of acute and chronic full-thickness rotator cuff tears.
J Ultrasound Med. 2000; 19 (quiz 383): 377-378
Ohtani S.
Murakami G.
Fibrous connection to bone after immediate repair of the canine infraspinatus: The most effective bony surface for tendon attachment.
J Shoulder Elbow Surg. 2001; 10: 123-128
Remnant tendon preservation enhances rotator cuff healing: Remnant preserving versus removal in a rabbit model.
Arthroscopy. 2020; 36: 1834-1842
Native enthesis preservation versus removal in rotator cuff repair in a rabbit model.
Arthroscopy. 2018; 34: 2054-2062
Migration of mesenchymal stem cells of bursal tissue after rotator cuff repair in rats.
Joints. 2018; 6: 4-9
Baldino J.
et al.
Comparison of preparation techniques for isolating subacromial bursa-derived cells as a potential augment for rotator cuff repair.
Arthroscopy. 2020; 36: 80-85
Yoon T.
Chun Y.
Bone marrow stimulation in arthroscopic repair for large to massive rotator cuff tears with incomplete footprint coverage.
Am J Sports Med. 2020; 48: 3322-3327
Mifune Y.
et al.
Characterization of progenitor cells derived from torn human rotator cuff tendons by gene expression patterns of chondrogenesis, osteogenesis, and adipogenesis.
J Orthop Surg Res. 2016; 11: 40
Moridera K.
Nakamura T.
Isolation and characterization of human mesenchymal stem cells derived from shoulder tissues involved in rotator cuff tears.
Am J Sports Med. 2013; 41: 657-668
Histopathology of residual tendon in high-grade articular-sided partial-thickness rotator cuff tears (PASTA lesions).
Arthroscopy. 2012; 28: 474-480
Qiao Y.
et al.
A long preoperative duration of symptoms is associated with worse functional outcomes after 1-stage arthroscopic treatment of rotator cuff tears with shoulder stiffness.
Am J Sports Med. 2017; 45: 2336-2344
Piccoli M.
et al.
Isolation and characterization of 2 new human rotator cuff and long head of biceps tendon cells possessing stem cell-like self-renewal and multipotential differentiation capacity.
Am J Sports Med. 2013; 41: 1653-1664
Isolation and characterization of multipotent rat tendon-derived stem cells.
Tissue Eng Part A. 2010; 16: 1549-1558
New insights into the cellular makeup and progenitor potential of palatal connective tissues.
Microsc Res Tech. 2017; 80: 1270-1282
Characterization of differential properties of rabbit tendon stem cells and tenocytes.
BMC Musculoskelet Disord. 2010; 11: 10
Chronic Achilles tendinopathy. A survey of surgical and histopathologic findings.
Clin Orthop Relat Res. 1995; 316: 151-164
Tendon pathology in long-standing achillodynia. Biopsy findings in 40 patients.
Acta Orthop Scand. 1997; 68: 170
Histological and ultrastructural changes in the undersurface of the acromion with subacromial impingement.
Acta Orthop. 2005; 76: 386-391
Hallström E.
et al.
More histologic and ultrastructural degenerative signs in the subscapularis tendon and the joint capsule in male patients with shoulder impingement.
Knee Surg Sports Traumatol Arthrosc. 2018; 26: 79-87
The skeletal attachment of tendons—Tendon 'entheses'.
Comp Biochem Physiol A Mol Integr Physiol. 2002; 133: 931-945
Jeon Y.
Kim R.
Preservation of bursal-sided tendon in partial-thickness articular-sided rotator cuff tears: A novel arthroscopic transtendon anatomic repair technique.
Arch Orthop Trauma Surg. 2016; 136: 1701-1708
Native enthesis preservation versus removal in rotator cuff repair in a rabbit model.
Arthroscopy. 2018; (S0749806318302238)
Age-related differences in anterior cruciate ligament remnant vascular-derived cells.
Am J Sports Med. 2014; 42: 1478-1486
Nag T.
Sharma S.
Quantitative correlation of mechanoreceptors in tibial remnant of ruptured human anterior cruciate ligament with duration of injury and its significance: an immunohistochemistry-based observational study.
J Orthop Traumatol. 2018; 19: 5
Yokota M.
et al.
The effect of intraoperative graft coverage with preserved remnant tissue on the results of the pivot-shift test after anatomic double-bundle anterior cruciate ligament reconstruction: Quantitative evaluations with an electromagnetic sensor system.
Am J Sports Med. 2017; 45: 2217-2225
Remnant-preserving and re-tensioning technique to cover the graft in anterior cruciate ligament reconstruction.
Knee Surg Sports Traumatol Arthrosc. 2017; 25: 1205-1210
Clinical outcome of remnant-preserving and I.D.E.A.L. femoral tunnel technique for anterior cruciate ligament reconstruction.
Orthop Surg. 2020; 12: 1693-1702
Pauline Po
et al.
Comparison of potentials of stem cells isolated from tendon and bone marrow for musculoskeletal tissue engineering.
Tissue Eng Part A. 2012; 18: 840-851
Loss of tenomodulin results in reduced self-renewal and augmented senescence of tendon stem/progenitor cells.
Stem Cells Dev. 2015; 24: 597-609
Klotz B.
et al.
Uncovering the cellular and molecular changes in tendon stem/progenitor cells attributed to tendon aging and degeneration.
Aging Cell. 2013; 12: 988-999
Characteristics of the rat supraspinatus tendon during tendon-to-bone healing after acute injury.
J Orthop Res. 2010; 24: 541-550
Kirchhoff C.
Milz S.
Attachment sites of the coracoclavicular ligaments are characterized by fibrocartilage differentiation: a study on human cadaveric tissue.
Scand J Med Sci Sports. 2012; 22: 12-17
The effect of mesenchymal stromal cell sheets on the inflammatory stage of flexor tendon healing.
Stem Cell Res Ther. 2016; 7: 144
Time-dependent alterations of MMPs, TIMPs and tendon structure in human Achilles tendons after acute rupture.
Int J Mol Sci. 2017; 18: 2199
Age-dependent healing potential of anterior cruciate ligament remnant-derived cells.
Am J Sports Med. 2015; 43: 700-708
Anterior cruciate ligament remnant tissue harvested within 3-months after injury predicts higher healing potential.
BMC Musculoskelet Disord. 2015; 16: 390
Yamato M.
et al.
Characterization of layered chondrocyte sheets created in a co-culture system with synoviocytes in a hypoxic environment.
J Tissue Eng Regen Med. 2017; 11: 2885-2894
Oh K.
Chung S.
Fatty acid-binding protein 4 regulates fatty infiltration after rotator cuff tear by hypoxia-inducible factor 1 in mice.
J Cachexia Sarcopenia Muscle. 2017; 8: 839-850
Light microscopic histology of quadriceps tendon ruptures.
Int Orthop. 2012; 36: 2367-2371
The enthesis: A review of the tendon-to-bone insertion.
Muscles Ligaments Tendons J. 2014; 4: 333-342
Entheses—The bony attachments of tendons and ligaments.
Ital J Anat Embryol. 2001; 106: 151