Healing of full-thickness tears of avian supracoracoid tendons: in situ hybridization of alpha1(I) and alpha1(III) procollagen mRNA.

Although clinically significant, much remains unknown about the healing of the torn rotator cuff tendon, because of unavailability of appropriate animal model. The human supraspinatus tendon faces the subacromial bursa superiorly, and the joint capsule inferiorly, while the digital flexor tendon is surrounded by the synovium. We hypothesized that the supraspinatus tendon heals by the process which is different from that observed with digital flexor tendons, in which epitenon cells migrate into the torn portion circumferentially. The avian supracoracoid tendon was adopted for this experiment because of its similarity to the human supraspinatus tendon. We developed a full-thickness tendon laceration followed by primary suture. The objective of this study was to detect localization of the responsible cells for repair of the tendon. We examined the process using histology and in situ hybridization. Starting at week 1 the peritendon cells of the bursal side proliferated and migrated into the laceration site. At week 6, the tendon stumps were continuous with new connective tissue. High-level expression of procollagen mRNA in the proliferating peritendon cells on the bursal side demonstrates to contribute to the reparative process, which progressed to the joint side. This mode of repair is different from that of the digital flexor tendon.     

Pathological study of the supraspinatus tendon

To clarify the aging process and pathogenesis of rotator cuff tears, left supraspinatus tendons from 268 cadaveric specimens (171 men and 97 women, ages 0 to 87 years) were studied. The incidence of complete thickness tear was 6.7%, and that of incomplete thickness tear was 13.8% (bursal side tears: 2.6%, intratendinous tears: 7.5% and joint side tears: 3.7%). Microscopic examinations were conducted topographically in five sites near the supraspinatus insertion. In the articular side of the tendon, there were fewer tenocytes, fewer arterioles and more chondrocyte like cells than in any other portions. The incidence of hyperplasia of intima was higher in the specimens of aged persons in all portions. At the insertion in the aged specimens the arrangement of four transitional zones became much more irregular and the numbers of tidemark was occasionally increased with granulomatous tissue. The pathogenesis of the rotator cuff tear can be ascribed to the combination of aging, enthesopathy, inherent property of the supraspinatus tendon, injury and subacromial impingement.     

Expression and enzymatic activity of MMP-2 during healing process of the acute supraspinatus tendon tear in rabbits.

We investigated the spontaneous healing process of a surgically created supraspinatus tendon tear in rabbits with specific reference to the expression of matrix metalloproteinase-2 (MMP-2) and its time-course change in enzymatic activity along with the expression of tissue inhibitors of metalloproteinases (TIMPs). A transverse, full thickness tear of the supraspinatus tendon was created and examined. Immunohistochemical analysis revealed that MMP-2 positive cells were mainly localized at both cutting ends of the tendon, and reparative tissue encroached into the gap from the bursal side. The expression of TIMP-1 was induced in the cells at not only the tendon edges but also the reparative tissue during the healing process. TIMP-2 was constitutively expressed in both the tendon and the reparative tissue. Gelatin zymography using tissue culture media demonstrated latent and active forms of MMP-2 and characteristic time-linked changes of the enzymatic activity. Western blotting confirmed the bands as the latent form of MMP-2. These results suggest that MMP-2 is expressed and activated during the healing process of acute supraspinatus tendon tear and can play an important role in the remodeling process.     

肩袖损伤后修复的实验研究

目的观察肩峰下撞击征所致肩袖损伤后的修复反应及碱性成纤维细胞生长因子(basicfibroblastgrowthfactor,bFGF)的表达。方法雄性SD大鼠50只,剪取同侧肩胛冈骨块移位于肩峰底面,建立肩峰下撞击模型,对侧行假手术作为对照。分别于术后第3、7、14、28、56d处死动物,切取整个肩关节,观察冈下肌肌腱的修复反应及bFGF的表达,并使用计算机图像分析系统检测bFGF的表达变化,图像分析结果中光密度值(OD)和阳性面积值分别表示bFGF的表达强度和阳性细胞数。结果所有动物实验侧的冈下肌肌腱均出现滑囊面撕裂,肌腱断端细胞增生,来自肩峰下滑囊的结缔组织覆盖其表面。对照侧冈下肌肌腱完好,仅有少量的腱细胞和滑囊细胞表达bFGF;而实验侧沿腱外膜排列的腱细胞、从肩峰下滑囊迁移的炎细胞和成纤维细胞表达信号增强。结论肌腱损伤后bFGF的表达增强;肩峰下滑囊是肩袖修复的基础和bFGF分泌的主要来源,修补肩袖时应尽量给予保留。     

Histologic evidence of degeneration at the insertion of 3 rotator cuff tendons: a comparative study with human cadaveric shoulders

We determined on histologic examination the degree of degeneration at the insertion of 3 rotator cuff tendons in 76 cadaveric shoulders, 17 of which had a partial tear of the supraspinatus. Fiber thinning, the presence of granulation tissue, and incomplete tearing of fibers, all evidence of degeneration, were quantified separately for each tendon. Among the shoulders that were intact on macroscopy, no significant difference in degeneration score could be found. In all 3 tendons degeneration was more prominent on the articular sides compared with the bursal sides (P < .0001). The degeneration score of partially torn supraspinatus was significantly higher than that of the intact tendons (P < .0001). The extent of granulation tissue, 1 criterion of degeneration, seemed to contribute mostly to this difference. Intrinsic degeneration occurred foremost in the articular side of the rotator cuff and might constitute the primary cause of rotator cuff tearing.     

Inhomogeneous mechanical behavior of the human supraspinatus tendon under uniaxial loading.

Disorders of the rotator cuff, particularly tears of the rotator cuff tendons, cause significant shoulder disability. Among numerous factors thought to be responsible for the initiation and progression of supraspinatus tears are those related to the tendon's biomechanical properties. We hypothesized that in supraspinatus tendons subjected to tensile loading a strain gradient (difference) exists between the articular and bursal tendon surfaces, that regional strain differences exist on each of these two tendon surfaces, and that tendon surface strains vary with glenohumeral abduction. To test these hypotheses, the intrinsic inhomogeneous deformational characteristics of the articular and bursal surfaces of eight intact human cadaveric supraspinatus tendons were studied at three glenohumeral abduction angles using a novel multiple strain measuring system which simultaneously recorded surface marker displacements on two opposing soft tissue surfaces. Under applied tensile loads, the articular surface exhibited greater strain at 22 degrees (7.4+/-2.6% vs. 1.3+/-0.7%, p=0.0002) and 63 degrees (6.4+/-1.6% vs. 2.7+/-1.2%, p=0.0001) whereas the bursal surface exhibited greater strain at 90 degrees (7.6+/-2.8% vs. 4.9+/-0.4%, p=0.013). At all abduction angles, insertion strains were higher than those of the mid-tendon and tendon-muscle junction regions. The existence of inhomogeneous surface strains in the intact supraspinatus tendon demonstrates that intratendinous shear occurs within the tendon. The higher strain on the articular side of the tendon, especially at the insertion region, suggests a propensity for tears to initiate in the articular tendinous zone.     

Mechanical properties of the long‐head of the biceps tendon are altered in the presence of rotator cuff tears in a rat model

Rotator cuff tears are disabling conditions that result in changes in joint loading and functional deficiencies. Clinically, damage to the long‐head of the biceps tendon has been found in conjunction with rotator cuff tears, and this damage is thought to increase with increasing tear size. Despite its importance, controversy exists regarding the optimal treatment for the biceps. An animal model of this condition would allow for controlled studies to investigate the etiology of this problem and potential treatment strategies. We created rotator cuff tears in the rat model by detaching single (supraspinatus) and multiple (supraspinatus + infraspinatus or supraspinatus + subscapularis) rotator cuff tendons and measured the mechanical properties along the length of the long‐head of the biceps tendon 4 and 8 weeks following injury. Cross‐sectional area of the biceps was increased in the presence of a single rotator cuff tendon tear (by ～150%), with a greater increase in the presence of a multiple rotator cuff tendon tear (by up to 220%). Modulus values decreased as much as 43 and 56% with one and two tendon tears, respectively. Also, multiple tendon tear conditions involving the infraspinatus in addition to the supraspinatus affected the biceps tendon more than those involving the subscapularis and supraspinatus. Finally, biceps tendon mechanical properties worsened over time in multiple rotator cuff tendon tears. Therefore, the rat model correlates well with clinical findings of biceps tendon pathology in the presence of rotator cuff tears, and can be used to evaluate etiology and treatment modalities. © 2008 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 27:416–420, 2009     

Stress distribution in the supraspinatus tendon with partial-thickness tears: an analysis using two-dimensional finite element model

The purpose of this study was to clarify the stress distribution in the rotator cuff tendon with 3 types of partial-thickness tears by use of 2-dimensional finite element analysis. In the finite element model of the normal human shoulder, a tendon defect was created on the articular surface, on the bursal surface, or in the midsubstance close to the insertion. A tensile force was applied to the proximal end of the tendon, and the stress distribution was calculated. In all 3 types of tears, a high stress concentration appeared around the articular surface at the insertion and at the site of the tear, which extended proximally. The maximum value of the von Mises stress increased with the presence of a partial-thickness tear. With the arm in abduction, a high stress concentration was also observed around the site of the tear. These biomechanical conditions of the supraspinatus tendon may eventually lead to a full-thickness tear at the critical zone.     

Suprascapular nerve neuropathy leads to supraspinatus tendon degeneration

BackgroundNowadays most of attention regarding rotator cuff is payed to how to reduce the failure after rotator cuff surgical repair rather than how to prevent the rotator cuff tear before surgery. The etiologies of rotator cuff tear are still unclear. As we all know, the nerve system include brain, spinal cord, sensory organs and all the neurons allover our body coordinates the homoeostasis of our body. We hypothesis that the nerve injury proximal to suprascapular nerve can leads to rotator cuff degeneration even tear.MethodsThirty-six SD rats were used. A defect on the suprascapular nerve was made on the right side and a sham surgery on the nerve (expose nerve only) at the left side. The insertion of supraspinatus tendon and supraspinatus muscle were harvested for testing. Twelve rats were sacrificed for biomechanical (six rats) and histological (six rats) properties were evaluated at 3, 6, and 9 weeks after surgery, respectively.ResultsSignificant inferior biomechanical properties of rotator cuff were found in nerve injured side compared to the nerve intact side at 6–9 weeks. Significant muscle atrophy was found at nerve injured side from 3 to 9 weeks. The enthesis of nerve injured side showed significant excessive cell maturity, reduced cellularity, smaller metachromasia area and more type-III collagen especially at 9 weeks after surgery.ConclusionsThe neuropathy proximal to suprascapular nerve can leads to rotator cuff degeneration even tear. The nerve dysfunction maybe an important etiology for rotator cuff tear.     

The microvascular pattern of the supraspinatus tendon

The vascular pattern of the supraspinatus tendon was studied in 18 human anatomic specimens. The ages of the specimens ranged from 26 to 84 years. Selective vascular injection with a silicon-rubber compound allowed visualization of the vascular bed of the rotator cuff and humeral head. The presence of a hypovascular or critical zone close to the insertion of the supraspinatus tendon into the humeral head was confirmed. However, only a uniformly sparse vascular distribution was found at the articular side, as opposed to the well-vascularized bursal side. This was also confirmed with histologic sections of the tendon. The poor vascularity of the tendon in this area could be a significant factor in the pathogenesis of degenerative rotator cuff tears.     

Mechanical environment of the supraspinatus tendon: three-dimensional finite element model analysis

BACKGROUND: We analyzed the mechanical environment of the supraspinatus tendon using a three-dimensional finite element model with the software programs MENTAT and MARC. METHODS: The supraspinatus tendon that attaches to the superior facet was extracted and modeled. The geometric shape of the humeral head was determined from computed tomography images, and the shape of the supraspinatus tendon was determined from magnetic resonance images of the shoulder at 0 degrees of abduction in a healthy 27-year-old man. The distal portion of the humeral head was fixed, and 10 N of tensile force was applied to the proximal end of the tendon. The tensile stress was calculated. RESULTS: The tensile stress was 1.8 MPa for the bursal side and 15.0 MPa for the articular side of the anterior portion of the supraspinatus tendon. The intensity was 0 MPa for the bursal side and 4.5 MPa for the articular side of the middle portion of the tendon. The intensity was 0.1 MPa for the bursal side and 5.2 MPa for the posterior edge of the tendon. CONCLUSIONS: Based on the three-dimensional finite element method, the maximal tensile stress was observed on the articular side of the anterior edge of the supraspinatus tendon. Our result may explain the frequent occurrence of rotator cuff tears at this site.     

The supraspinatus footprint: an anatomic study of the supraspinatus insertion

PurposeManagement of articular sided partial-thickness rotator cuff tears is controversial. Most management decisions rest on determining the thickness of tendon loss and location of tendon involvement, without any clear guidelines offered on how to make this determination. This study attempts to confirm the normal cuff thickness at its humeral head attachment and correlate the amount of exposed bone at the “footprint” attachment of the supraspinatus as an accurate measurement of the amount of tendon loss.Type of studyAnatomic study.MethodsForty-eight cadaver shoulders with an average age of 71.5 years were examined. Specimens with full- or partial-thickness rotator cuff tears were not measured, leaving 17 specimens with an average age of 70 for analysis. The anterior to posterior width of the supraspinatus was measured with a caliper, as well as the medial to lateral width at the rotator interval, at midtendon, and at the posterior limit determined by the spine of the scapula raphe. The distance from the articular cartilage margin to the supraspinatus tendon insertion was also measured.ResultsThe mean anteroposterior dimension of the supraspinatus insertion was 25 mm. The mean superior to inferior tendon thickness at the rotator interval was 11.6 mm, 12.1 mm at midtendon, and 12 mm at the posterior edge. The distance from the articular cartilage margin to the bony tendon insertion was 1.5 to 1.9 mm, with a mean of 1.7 mm.ConclusionsArticular partial-thickness tears with > 7 mm of exposed bone lateral to the articular margin should be considered significant tears approximating 50% of the tendon substance. Arthroscopic measurement of the exposed bone between the articular margin and the supraspinatus tendon insertion (footprint) is an accurate way to estimate tear depth and provide a rational, reproducible guideline for treatment.     

Modified arthroscopic double row repair of partial thickness tear of the rotator Cuff involving articular and bursal side

Partial thickness of rotator cuff tears is considered as a common cause of shoulder disability. Various techniques for arthroscopic repair of partial thickness tear of rotator cuff have been reported in the literature. These techniques have addressed the articular side partial thickness cuff tear. We present an arthroscopic repair of partial thickness tear of rotator cuff involving both articular and bursal surfaces without converting into a full thickness tear. Each side of the tear was repaired with suture anchors separately.     

The bubble sign: An arthroscopic indicator of an intratendinous rotator cuff tear

Intratendinous tears of the rotator cuff are, by definition, difficult to diagnose due to the absence of overt tendon disruption on both the bursal and articular surface of the rotator cuff. The authors describe the bubble sign, a bulging expansion of the rotator cuff tendon following injection of saline into the suspected lesion, as a useful indicator of an intratendinous tear of the rotator cuff.     

Apoptosis in rotator cuff tendonopathy.

The aim of this study was to investigate the involvement of apoptosis (programmed cell death) in the pathogenesis of rotator cuff disorders. The edges of torn supraspinatus rotator cuff tendons were collected from patients with rotator cuff tear (n = 25). Samples of the intra-articular portion of subscapularis tendons were collected from patients without rotator cuff tear as control (n = 6). To minimize individual variance, we also collected six pairs of supraspinatus tendon and subscapularis tendon from six patients with rotator cuff tears. Apoptosis was detected by in situ DNA end labelling assay and DNA laddering assay. Immunohistochemical staining was performed to identify cells undergoing apoptosis. Control subscapularis tendon had normal morphology. Tendon from torn supraspinatus rotator cuff showed significant mucoid degeneration. Within the areas of degeneration, there were large numbers of apoptotic cells. The percentage of apoptotic cells in the degenerative rotator cuff (34%) was significantly higher than that in controls (13%) (p < 0.001). The excessive apoptosis detected in degenerative rotator cuff tissue was confirmed by DNA laddering assays. This is the first report of excessive apoptosis in degenerating rotator cuff tendon. Cells undergoing apoptosis in rotator cuff were mainly fibroblast-like cells. These finding indicate that apoptosis may play an important role in the pathogenesis of rotator cuff degeneration.     

Cell‐based tissue engineering augments tendon‐to‐bone healing in a rat supraspinatus model

Rotator cuff pathology causes substantial pain/disability and health care costs. Cell‐based tissue engineering offers promise for improved outcomes in tendon to bone healing. Cells from the tendon‐bone interface were used here to amplify surgical defect healing in a rat model. Cells from tendon‐to‐bone interface of the rotator cuff were seeded in sponges and implanted into critical rotator cuff defects: Group I, control; II, surgical defect only; III, suture‐repaired defect; IV, surgical defect, repair with sponge only; V, surgical defect, repair with sponge with cells. Three, 6‐, and 12‐week results were assessed for histologic features. At 3 weeks, histologic indices in Group V were significantly increased versus other treatment groups. Group V (12 weeks) showed significantly improved collagen organization versus other treatment groups; there was no difference in collagen organization in Group I versus V. In summary, increased cellularity, inflammation, vascularity, and collagen organization were present at 3 weeks; increased collagen organization at 12 weeks in Group V provides evidence for improved healing with cells. Data further support the utility of tendon‐bone interface cells in rotator cuff healing. © 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 31: 407–412, 2013     

Acromial spur: relationship to aging and morphologic changes in the rotator cuff

This study's objective is to elucidate the relationship between acromial spur formation and rotator cuff pathology or aging. The subjects comprised 1029 shoulders in control, cadaveric, and operative groups. A radiograph in the supraspinatus outlet view was taken in all subjects. The lengths of the incident spurs were measured and classified into 3 sizes (small, <5 mm; medium, <10 mm; and large, > or =10 mm). The rotator cuff was macroscopically classified as normal or as having bursal-side fraying, joint-side tear, intratendinous tear, bursal-side tear, complete tear limited to the supraspinatus tendon, or massive tear. In the control group, the overall incidence of spurs and spur size increased with advancing age (P < .001), but the majority of spurs were small (<5 mm). In the cadaveric group, the overall incidence did not correlate with advancing age (P > .05). However, spur size increased with age in subjects aged 50 years or older (P < .001). The incidence of spurs in rotator cuffs with bursal-side tears was highest and was significantly higher than that in normal cuffs and cuffs with bursal-side fraying and intratendinous tears. We observed 40% of medium spurs and 69% of large spurs in cases with bursal-side tears, complete tears limited to the supraspinatus tendon, and massive tears. In the operative group, the overall incidence correlated to advancing age (P < .001), reaching 80% or more in subjects aged 30 years or older. In addition, the size of spurs was larger than that in the other 2 groups in all age groups with few exceptions (P < .05). Small spurs were associated with advancing age. Morphologic change to the bursal side of the rotator cuff may enhance spur growth. The presence of a small spur has no diagnostic value for rotator cuff tears. Spurs measuring 5 mm or more, however, are of diagnostic value because of their high rate of association with bursal-side tear, complete tears limited to the supraspinatus tendon, or massive tears.     

肩峰下激素局部注射治疗大鼠肩袖损伤

目的 通过测定Ⅲ型胶原的动态变化观察肩峰下激素局部注射对大鼠肩袖损伤修复的影响.方法 将36只SD大鼠随机分成4组:正常肩袖组6例(A组);肩袖损伤组6例(B组);正常肩袖+皮质激素治疗组12例(C组);肩袖损伤+皮质激素治疗组12例(D组).B、D组使用大鼠双侧冈下肌腱滑膜面建模,切开冈下肌腱全厚层的50%,宽约5 mm.C,D组肩峰下滑囊注射0.05 ml皮质激素(得保松).分别于3、6周取冈下肌腱标本进行苏木素-伊红(HE)染色、Masson染色检查以及免疫组织化学染色测定Ⅲ型胶原的表达.结果 组织形态学:激素治疗肩袖损伤后3周可见胶原纤维排列紊乱,胶原索断裂和坏死;6周后略好转.Ⅲ型胶原:(1)肩袖损伤后Ⅲ型胶原表达升高(P＜0.05);(2)激素在治疗肩袖损伤后3周Ⅲ型胶原明显较正常组和肩袖损伤组高(P＜0.01);(3)激素治疗肩袖损伤后6周,Ⅲ型胶原表达仍高;(4)正常肩袖激素治疗后3周Ⅲ型胶原表达明显增高,但在6周后恢复到正常水平(P＞0.05).结论 激素在治疗肩袖损伤时能通过刺激Ⅲ型胶原的表达促进肩袖修复,但肌腱的组织学结构和强度发生显著变化.即使正常的肩袖组织,在激素局部注射后也会产生暂时性的肩袖损伤修复反应.     

Arthroscopic debridement and acromioplasty versus mini-open repair in the treatment of significant partial-thickness rotator cuff tears.

Partial tears of the rotator cuff, especially of the articular side, have received attention only with the recent ability of magnetic resonance imaging (MRI) and arthroscopy to diagnose these lesions. Several early reports showed nearly 100% success in managing these lesions with arthroscopic debridement with or without acromioplasty. This series compares 32 patients with significant partial-thickness rotator cuff tears treated with debridement and acromioplasty versus 33 patients with mini-open repair. Follow-up was from 2 to 7 years. Preoperative MRI was not useful; when positive, preoperative arthrography was useful for articular side tears. Of the tears, 12% were bursal side tears and the remainder were articular side tears; all were at least 50% or more of the thickness of the tendon. A significant number of the arthroscopic group had fair results by UCLA score criteria. Three patients reruptured the remaining cuff later despite adequate acromioplasty. Healing of the partial tear was never observed at second-look arthroscopy. Although postoperative pain was significantly greater and recovery slower with open repair, no patient was reoperated on and rerupture of the repair did not occur. The outstanding results of prior studies of cuff debridement were not duplicated in this series of cuff debridements with long-term follow-up. Adequate acromioplasty alone does not prophylactically prevent rotator cuff tear progression. Recognition and repair of these significant partial tears may be advisable for the long-term function of the shoulder despite short-term improvement in morbidity with arthroscopic treatment.     

Estimation of Total Collagen and Types I and III Collagen in Canine Rotator Cuff Tendons

The collagen composition of the supraspinatus, infraspinatus, and subscapularis tendons, which form part of the rotator cuff of the shoulder, was determined. Tendons were obtained from adult, male beagle dogs and total collagen was estimated by measurement of hydroxyproline. There was little variation in collagen content among the three major cuff tendons and the quantity approximated that cited in the literature for other tendons. However, the collagen content in the insertion zone of the supraspinatus tendon was significantly higher than in the tendon proper. NaCl fractionation of supraspinatus collagen indicated that type I was the predominant collagen but significant amounts of type III and possibly some type II and type V were also present. Interestingly, there appeared to be more type III collagen in the insertion zone than in the tendon proper, cyanogen bromide digestion and peptide mapping confirmed this finding. The differential collagen composition of the supraspinatus tendon may contribute to the high incidence of tear that is associated with this rotator cuff tendon. Received: 10 May 1996 / Accepted: 23 April 1997