Louis J. Soslowsky

Development and use of an animal model for investigations on rotator cuff disease

Although both intrinsic and extrinsic factors have been implicated in the cause of rotator cuff disease, previous studies have not been designed to test hypotheses of this disease, partly because of the lack of an appropriate animal model. Thirty-three animals were evaluated according to a 34 item checklist of criteria to determine their appropriateness as an animal model for investigations on the rotator cuff. Only the rat shoulder satisfactorily fulfilled all criteria, with a prominent supraspinatus tendon passing under an enclosed arch. Once the rat was identified, 36 rats were randomized to three experimental groups. One group (n = 12) was treated with an intratendinous injection of bacterial collagenase simulating an acute intrinsic injury, another group (n = 12) was treated with an acromial alteration to reduce the subacromial space simulating an external compression, and the third group (n = 12) was treated with a combination of both modifications. Significant increases in cellularity, number of fibroblasts, and collagen disorganization were seen in all experimental tendons compared with a contralateral control group. Semiquantitative grading of histologic sections revealed marked changes in all groups at 4 and 8 weeks. Injuries appeared to be healing at 12 weeks except in the combination group, which seemed to demonstrate persistent alterations. This study supports the rat as an appropriate model for investigating rotator cuff disease. In addition, this study demonstrates that both intrinsic and extrinsic alterations can induce changes in the supraspinatus tendon, which may have similarities to human tendon disease.

Excursion of the Rotator Cuff Under the Acromion Patterns of Subacromial Contact

Nine fresh-frozen, human cadaveric shoulders were el evated in the scapular plane in two different humeral rotations by applying forces along action lines of rotator cuff and deltoid muscles. Stereophotogrammetry deter mined possible regions of subacromial contact using a proximity criterion; radiographs measured acromio humeral interval and position of greater tuberosity. Con tact starts at the anterolateral edge of the acromion at 0° of elevation; it shifts medially with arm elevation. On the humeral surface, contact shifts from proximal to dis tal on the supraspinatus tendon with arm elevation. When external rotation is decreased, distal and poste rior shift in contact is noted. Acromial undersurface and rotator cuff tendons are in closest proximity between 60° and 120° of elevation; contact was consistently more pronounced for Type III acromions. Mean acro miohumeral interval was 11.1 mm at 0° of elevation and decreased to 5.7 mm at 90°, when greater tuberosity was closest to the acromion. Radiographs show bone- to-bone relationship; stereophotogrammetry assesses contact on soft tissues of the subacromial space. Con tact centers on the supraspinatus insertion, suggesting altered excursion of the greater tuberosity may initially damage this rotator cuff region. Conditions limiting ex ternal rotation or elevation may also increase rotator cuff compression. Marked increase in contact with Type III acromions supports the role of anterior acromioplasty when clinically indicated, usually in older patients with primary impingement.

Quantitation of articular surface topography and cartilage thickness in knee joints using stereophotogrammetry

An analytical stereophotogrammetry (SPG) technique has been developed based upon some of the pioneering work of Selvik [Ph.D. thesis, University of Lund, Sweden (1974)] and Huiskes and coworkers [J. Biomechanics 18, 559-570 (1985)], and represents a fundamental step in the construction of biomechanical models of diarthrodial joints. Using this technique, the precise three-dimensional topography of the cartilage surfaces of various diarthrodial joints has been obtained. The system presented in this paper delivers an accuracy of 90 microns in the least favorable conditions with 95% coverage using the same calibration method as Huiskes et al. (1985). In addition, a method has been developed, using SPG, to quantitatively map the cartilage thickness over the entire articular surface of a joint with a precision of 134 microns (95% coverage). In the present study, our SPG system has been used to quantify the topography, including surface area, of the articular surfaces of the patella, distal femur, tibial plateau, and menisci of the human knee. Furthermore, examples of cartilage thickness maps and corresponding thickness data including coefficient of variation, minimum, maximum, and mean cartilage thickness are also provided for the cartilage surfaces of the knee. These maps illustrate significant variations over the joint surfaces which are important in the determination of the stresses and strains within the cartilage during diarthrodial joint function. In addition, these cartilage surface topographies and thickness data are essential for the development of anatomically accurate finite element models of diarthrodial joints.(ABSTRACT TRUNCATED AT 250 WORDS)

Rotator cuff defect healing: A biomechanical and histologic analysis in an animal model

Rotator cuff tears are one of the most common causes of pain and disability in the upper extremity. With the use of an animal model, we studied the healing response of a controlled defect in the normal supraspinatus tendon and in a tendon with a reduced intrinsic healing capacity. In 36 Sprague-Dawley rats, defects (2 mm x 2 mm) were created in the supraspinatus tendons bilaterally. To model a tendon with an intrinsically reduced capacity to heal, the tissue adjacent to the defect area in the left shoulder was treated with in situ freezing. The contralateral tendon was not frozen. After 3 (n = 12), 6 (n = 12), and 12 (n = 12) weeks, animals were killed and underwent histologic (n = 4 from each group) and biomechanical (n = 8 from each group) evaluation. An additional group of untreated animals served as a normal control group. On histologic evaluation 78% of tendons had persistent defects (defined as incomplete closure of the defect site). Over time, the tissue from both groups demonstrated an improved histologic grade but did not reach normal levels, even at 12 weeks. No histologic differences were found between defect healing in normal tendons and in those treated with in situ freezing. On biomechanical evaluation there were also no significant differences between treatment groups. Over time, an improvement occurred in tissue properties, indicating that some healing of the defects had occurred. However, these tissue properties remained an order of magnitude lower than those of normal control tendons. These findings indicate that there is an active but inadequate repair response to the defect in the rat supraspinatus tendon, which is not significantly worsened by in situ freezing of the tissue around the defect. This model has applications toward the study of techniques to improve or accelerate cuff defect healing.

Inferior glenohumeral ligament: Geometric and strain-rate dependent properties

The inferior glenohumeral ligament (IGHL) is an important structure for maintaining shoulder stability. This study was aimed at determining the geometric and anatomic characteristics of the IGHL and its tensile properties at a higher strain rate than previously tested. Eight fresh-frozen human cadaver shoulders (average age 69 years, age range 62 to 73 years) from four female and four male cadavers were used to harvest bone-ligament-bone specimens from the three regions of the IGHL (superior band, anterior axillary pouch, and posterior axillary pouch). Uniaxial tensile tests were performed at the moderately high strain rate of approximately 10% per second with a servo-hydraulic testing machine. This represented a strain rate that was approximately 100 to 1000 times faster than that previously reported. During tensile testing, bone-ligament-bone strains were calculated from grip-to-grip motion on the testing machine, and mid-substance strains were determined by a video dimensional analyzer. Although all regions of the IGHL had similar lengths (averaging 43.4 mm), their thickness varied by region and by proximal-to-distal location. The superior band was the thickest (2.23 +/- 0.38 mm) of the three regions. Of the remaining two regions the anterior axillary pouch (1.94 +/- 0.38 mm) was thicker than the posterior axillary pouch (1.59 +/- 0.64 mm). By proximal-to-distal location the IGHL was thicker for all three regions near the glenoid (2.30 +/- 0.57 mm) than near the humerus (1.61 +/- 0.52 mm). The superior band had a greater stiffness (62.63 +/- 9.78 MPa) than either the anterior axillary pouch (47.75 +/- 17.89 MPa) or the posterior axillary pouch (39.97 +/- 13.29 MPa). Tensile stress at failure was greater in the superior band (8.4 +/- 2.2 MPa) and the anterior axillary pouch (7.8 +/- 3.1 MPa) than the posterior axillary pouch (5.9 +/- 1.7 MPa). The anterior axillary pouch demonstrated greater bone-to-bone and mid-substance strains (30.4% +/- 4.3% and 10.8% +/- 2.4%, respectively) before failure than the other two regions (superior band: 20.8% +/- 3.8% and 9.1% +/- 2.8%, respectively; posterior axillary pouch: 25.2% +/- 5.8% and 7.8% +/- 2.6%, respectively). Bone-to-bone strain was always greater than mid-substance strain, indicating that when the IGHL is stretched, the tissue near the insertion sites will experience much greater strain than the tissue in the mid-substance. insertion failures were more likely at slower strain rates, and ligamentous failures were predominant at the fast strain rate. When compared with other tensile studies of the IGHL at slower strain rates (0.01% per second and 0.1% per second), the superior band and the anterior axillary pouch demonstrated the viscoelastic effects of increased stiffness and failure stress. This superior band and anterior axillary pouch pouch viscoelastic stiffening effect suggests that these two regions may function to restrain the humeral head from rapid abnormal anterior displacement in the clinically vulnerable position of abduction and external rotation.

A stereophotogrammetric method for determining in situ contact areas in diarthrodial joints, and a comparison with other methods.

Determination of contact areas in diarthrodial joints is necessary for understanding the state of stress within the articular cartilage layers and the supporting bony structures. The present study describes the use of a stereophotogrammetry (SPG) system [Huiskes et al., J. Biomechanics 18, 559-570 (1985) and Ateshian et al., J. Biomechanics 24, 761-776 (1991)] for determining contact areas in diarthrodial joints, using a surface proximity concept similar to the one used by Scherrer et al. [ASME J. biomech. Engng 101, 271-278 (1979)]. This method consists of evaluating the proximity of the articular surfaces to determine joint contact areas using precise geometric models of the joint surfaces obtained from the SPG system, and precise kinematic data, also obtained from SPG. In this study, the SPG method for determining contact areas is compared to other commonly used methods such as dye staining, silicone rubber casting and Fuji film contact measurement techniques which have been often used and reported by other investigators. The bovine glenohumeral joint and the bovine lateral tibiofemoral articulation (without the meniscus) were used to represent congruent and incongruent joints, respectively. While all the methods yielded consistent contact patterns for the incongruent tibiofemoral articulations, the results for the congruent bovine glenohumeral joints showed that the SPG and Fuji film methods were in better agreement than those obtained from the dye staining and silicone rubber casting methods. The advantages of the new SPG method are that it can be used for intact joints, and used repeatedly and quickly thus making contact-area movement analyses possible [Soslowsky et al., J. orthop. Res. 10, 524-534 (1992)]. The results of this comparison study show that the SPG technique is a reliable and versatile method for determining contact areas in diarthrodial joints.

The Effects of Overuse Combined With Intrinsic or Extrinsic Alterations in an Animal Model of Rotator Cuff Tendinosis

An in vivo animal model was used to evaluate overuse and overuse plus intrinsic tendon injury or extrinsic tendon compression in the development of rotator cuff injury. Forty-four male Sprague-Dawley rats were divided into groups of 22. Each left shoulder received an intrinsic or extrinsic injury plus overuse (treadmill running), and each right shoulder received only overuse. Eleven rats from each group were sacrificed at 4 and 8 weeks. Supraspinatus tendons were evaluated histologically or geometrically and biomechanically. Ten rats constituted a cage-activity control group. Both supraspinatus tendons of the experimental groups had increases in cellularity and collagen disorganization and changes in cell shape compared with control tendons. Tendons with injury plus overuse exhibited a worse histologic grade than those with overuse alone. The cross-sectional area of both supraspinatus tendons of the experimental rats was significantly more than in control tendons. The area of the injury plus overuse tendons was increased on average compared with overuse-alone tendons. Biomechanically, the tissue moduli of overuse/intrinsic injury tendons at 4 weeks and those of the overuse/extrinsic injury tendons at 8 weeks were significantly lower than in control tendons. Tissue moduli of the overuse/injury tendons were significantly lower than in the overuse-alone tendons at 8 weeks. This study demonstrated that damage to the supraspinatus tendon can be caused by overuse and intrinsic injury, overuse and extrinsic compression, and overuse alone.

BIOMECHANICS OF THE ROTATOR CUFF

Thorough understanding of rotator cuff mechanics is important for effective treatment and/or prevention of cuff injuries. This understanding is achieved through knowledge of normal cuff structure and mechanics. Only then, can the effects of injuries and pathologic processes on normal cuff function be carefuly assessed. Rotator cuff structures are viewed and analyzed on a number of different levels. This article presents current knowledge of rotator cuff mechanics through review of cuff structure and anatomy, corocoacromial arch structure and biomechanics, and biomechanical models.

Geometric and mechanical properties of the coracoacromial ligament and their relationship to rotator cuff disease

One of the most common causes of pain and disability in the upper limb is inflammation of the rotator cuff tendons. When no significant bony abnormality exists in the surrounding structures, the coracoacromial ligament has been implicated as a possible cause of impingement on the cuff tendons. Geometric and mechanical properties of 20 coracoacromial ligaments, 10 from shoulders with rotator cuff tears and 10 from normal shoulders, were accurately determined. In comparing rotator cuff tear and normal specimens, statistically significant changes in geometric properties were measured in the lateral band, but not in the medial band, of the ligament. The lateral band, which is the region most likely to impinge on the rotator cuff, was shorter and had a larger cross-sectional area in specimens with rotator cuff tears. Although there were no statistical differences in structural properties of the ligament between normal and rotator cuff tear groups, significant changes were evident in material properties. Previously reported histologic differences in the ligament in shoulders with rotator cuff tears are supported by the decreased material properties measured in the current study. Whether the differences in the coracoacromial ligament cause impingement or are due to impingement is still unknown at this time.

Proteoglycans and glycosaminoglycan fine structure in the mouse tail tendon fascicle

The isolated mouse tail tendon fascicle, a functional and homogenous volume of tendon extracellular matrix, was utilized as an experimental system to examine the structure–function relationships in tendon. Our previous work using this model system demonstrated relationships between mean collagen fibril diameter and fascicle mechanical properties in isolated tail tendon fascicles from three different groups of mice (3‐week and 8‐week control and 8‐week Mov13 transgenic) K.A. Derwin, L.J. Soslowsky, J. Biomech. Eng. 121 (1999) 598–604. These groups of mice were chosen to obtain tendon tissues with varying collagen fibril structure and/or biochemistry, such that relationships with material properties could be investigated. To further investigate the molecular details of matrix composition and organization underlying tendon function, we report now on the preparation, characterization, and quantitation of fascicle PGs (proteoglycans) from these three groups. The chondroitin sulfate/dermatan sulfate (CS/DS)‐substituted PGs, biglycan and decorin, which are the abundant proteoglycans of whole tendons, were also shown to be the predominant PGs in isolated fascicles. Furthermore, similar to the postnatal maturation changes in matrix composition previously reported for whole tendons, isolated fascicles from 8‐week mice had lower CS/DS PG contents (both decorin and biglycan) and a higher collagen content than 3‐week mice. In addition, CS/DS chains substituted on PGs from 8‐week fascicles were shorter (based on a number average) and richer in disulfated disaccharide residues than chains from 3‐week mice. Fascicles from 8‐week Mov13 transgenic mice were found to contain similar amounts of total collagen and total CS/DS PG as age‐matched controls, and CS/DS chain lengths and sulfation also appeared normal. However, both decorin and biglycan in Mov13 tissue migrated slightly faster on sodium dodecyl sulfate polyacrylamide gel electorphoresis (SDS‐PAGE) than the corresponding species from 8‐week control, and biglycan from the 8‐week Mov13 fascicles appeared to migrate as a more polydisperse band, suggesting the presence of a unique PG population in the transgenic tissue. These observations, together with our biomechanical data [Derwin and Soslowsky, 1999] suggest that compensatory pathways of extracellular matrix assembly and maturation may exist, and that tissue mechanical properties may not be simply determined by the contents of individual matrix components or collagen fibril size.