Stress Distribution in Superior Labral Complex and Rotator Cuff During In Vivo Shoulder Motion: A Finite Element Analysis Seong W. Jang, M.S., Yon-Sik Yoo, M.D., Hwang-Young Lee, M.D., Yoon S. Kim, Ph.D., Pranay K. Srivastava, M.S., and Ayyappan Vijayachandran Nair, M.D.
Purpose: To quantitatively and qualitatively evaluate the impingement behavior between structures within the glenohumeral joint under simulated abductioneexternal rotation (ABER) motion using finite element analysis. Methods: Computed tomography (CT) scanning of 1 shoulder in a volunteer was performed at 0 and 120 of shoulder abduction with external rotation (ABER position), followed by magnetic resonance imaging at 0 of abduction. The CT and magnetic resonance images were then imported into a customized software program to undergo 3-dimensional reconstruction followed by finite element modeling of the bone and soft tissue including the upper part of the rotator cuff and glenohumeral labral complex. Glenohumeral motion from 0 to the ABER position was simulated by CT images in 2 different humeral positions. On the basis of simulated humeral motion with respect to the scapula, we measured the stress value on the biceps-labral complex and upper part of the rotator cuff as a consequence of their structural deformation. In addition, we intended to design 2 types of labrada normal stable labrum and an unstable posterosuperior labrumdto evaluate the geometric alteration and resulting stress change on the posterosuperior labrum against a compressive force from the humeral head and rotator cuff. Results: In the ABER position, the posterosuperior labrum was deformed by the humeral head and interposed posterior part of the rotator cuff. When viewed from the rotator cuff, the posterior part of the rotator cuff came into contact with the posterosuperior labrum as external rotation increased. The measured peak contact stress values were 19.7 MPa and 23.5 MPa for the posterosuperior labrum and the upper rotator cuff, respectively. The stress values for both structures decreased to 5.8 MPa and 18.1 MPa, respectively, in the simulated SLAP model. The root of the long head of the biceps became compressed halfway through the range of motion by the humeral head, especially from the part involving horizontal extension and external rotation, resulting in a high stress of 22.4 MPa. Conclusions: In this simulated SLAP model, the posterosuperior labrum was medially displaced by the humeral head and upper rotator cuff in the ABER position, causing a functional loss of the spacer effect. Clinical Relevance: In SLAP lesions, the posterosuperior labrum loses its ability to function as a spacer in certain positions (especially ABER) and may decrease the important spacer effect between the humerus and the rotator cuff; this may lead to posterosuperior subluxation of the humeral head or rotator cuff abnormalities and tears during repetitive ABER tasks.
From the School of Computer Science and Engineering, Korea University of Technology and Education (S.W.J., Y.S.K.), Cheonan; and Department of Orthopaedic Surgery, Hallym University (Y-S.Y., H-Y.L., P.K.S., A.V.N.), Dongtan, Republic of Korea. The authors report the following potential conflict of interest or source of funding: Funded by the National Research Foundation of Korea, Ministry of Education (grant 2013R1A1A2011589 to Y-S.Y.). Received January 13, 2014; accepted April 10, 2015. Address correspondence to Yon-Sik Yoo, M.D., Department of Orthopaedic Surgery, Hallym University Hospital, Dongtan, 40 Sukwoo-Dong, Hwasung, Gyung-gi, 445-170 Republic of Korea. E-mail: [email protected] Ó 2015 by the Arthroscopy Association of North America 0749-8063/1430/$36.00 http://dx.doi.org/10.1016/j.arthro.2015.04.082
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nternal impingement of the shoulder has been shown to be one of the important factors that cause significant disability in the throwing athlete.1-9 Although this phenomenon is known to occur mainly in throwing athletes, it is also present in the general population, especially persons with altered scapulothoracic positions and rhythm.10 In fact, a magnetic resonance imaging (MRI) study performed by Halbrecht et al.11 showed contact between the undersurface of the rotator cuff and the posterosuperior labrum in the abducted externally rotated position in both throwing and non-throwing shoulders. A similar phenomenon can be seen in the computer worker, the
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Fig 1. (A) Coordinate system associated with humeral motion with respect to scapula. The x-axis is parallel to the glenoid plane and is directed superior-inferiorly. The y-axis is the longitudinal axis of the supraspinatus muscle and is directed medial-laterally. The z-axis is the cross product of the x- and y-axes. (B) Scapular-plane abduction (ABD) using spatial coordinate set on center of humeral head. (C) Horizontal extension (HE) and external rotation (ER) using spatial linkage between heads. The gray bar indicates the screw axis.
recreational athlete, and the elderly patient, who commonly have a protracted scapula.12-17 Altered glenoid version as a result of scapular protraction induces posterosuperior internal impingement even while one is performing simple abduction tasks.17 This implies that posterosuperior internal impingement due to scapular protraction might be one of the initiating factors of SLAP lesions and rotator cuff tears in non-throwing shoulders, when contact is magnified both in intensity and in frequency. However, the exact kinematics of the surrounding structures and its pathogenesis during contact are yet to be understood. Likewise, modeling of the throwing shoulder and simulation of abnormal kinematics of the scapula in the laboratory are more technically demanding. Therefore we intended to construct an in vivo 3-dimensional (3D) glenohumeral motion model and simulate the phenomenon of internal impingement of the shoulder using the abductioneexternal rotation (ABER) position. Glenohumeral motion was simulated based on computed tomography (CT) images in 2 different humeral positions. On the basis of simulated humeral motion with respect to the scapula, we measured the stress value on the glenoid labrum and upper part of the rotator cuff as a consequence of their structural changes. In addition, we designed the SLAP model by changing the contact condition between the posterosuperior quadrant of the labrum and corresponding glenoid margin to observe the geometrical changes in the labrum under repetitive motion simulation. The objective of this study was to quantitatively and qualitatively evaluate the impingement behavior between structures within the glenohumeral joint under simulated ABER motion using finite element analysis. We hypothesized that the structural contact in the ABER position mainly would occur at the posterosuperior portion of the glenoid as a consequence of
impingement between the rotator cuff and posterosuperior labrum. Furthermore, we hypothesized that the simulated SLAP model would lead to a decrease in contact stress between structures due to medial displacement of the posterosuperior labrum against a compressive force from the humeral head and upper rotator cuff during ABER movement.
Methods 3D Bone Modeling and Motion Simulation Procedure The right shoulder of a 29-year-old volunteer was scanned with a high-resolution CT scanner (Somatom Sensation; Siemens, Erlangen, Germany) with 1-mm slices taken at 2 different shoulder angles in the prone position: 0 (neutral rotation) and the ABER position. The prone position was selected because it was believed to allow appropriate scapular motion while positioning the shoulder at different abduction angles in limited space. The study was approved by our institutional review board (2014-12), and informed consent was obtained from the volunteer. The ABER position was achieved by placing the hand behind the occiput at 120 of abduction. The 120 angle was determined by measuring the humeral position relative to the trunk. The DICOM (Digital Imaging and Communications in Medicine) files obtained were imported into visualization software (Amira R 4.0; Mercury Computer Systems, Chelmsford, MA) to construct virtual 3D bone models. Humeral motion from 0 to the ABER position with respect to the fixed scapula proceeded in 3 steps: (1) We superimposed the scapula at 120 onto the scapula at 0 of shoulder abduction using positional information of the coordinates. (2) We accurately determined the position and orientation of the humerus in space at 0 and the
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Fig 2. Overall computer 3dimensional (3D) modeling and simulation process. (ABER, abductioneexternal rotation; CT, computed tomography; DICOM, Digital Imaging and Communications in Medicine; MRI, magnetic resonance imaging.)
ABER position with respect to the scapula. (3) By use of spatial coordinates with the humerus set at 0 and the spatial linkage between the humeral heads, an arc of humeral motion from 0 to the ABER position was simulated. The total arc of humeral motion was designed to focus on the realistic arm path to the latecocked position, which has been considered initial scapular-plane abduction followed by horizontal extension combined with external rotation of the humerus. The origin of the local coordinate system in space was set at the center of the humeral head. A Euler angle system was used to describe the motion of the humerus with respect to the scapula. The x-axis was parallel to the glenoid plane and was directed superior-inferiorly. The y-axis followed the longitudinal axis of the supraspinatus muscle and was directed medial-laterally. The z-axis was directed externally and obtained by the cross product of the x- and y-axes (Fig 1A). The first motion
was scapular-plane abduction ranging from 0 to 68 with the rotation center set within the humeral head at 0 of abduction based on the z-axis of the scapula. We set 68 as the maximal abduction angle just before the impingement between the humeral head and corresponding labrum. In this circumstance, the glenohumeral joint was considered a ball-and-socket joint and the rotation center was determined by fitting a sphere to the articulating surface of the humeral head, although the humeral head was not a real sphere. For the remaining motion, we intended to adopt an instantaneous center of rotation to accomplish the best fit during scapular-plane abduction to the ABER position because there was no constant rotation center between the 2 humeral heads. The spatial linkage (also known as the “screw axis”) was used to simulate motion for horizontal extension combined with external rotation of the humerus. The screw axis motion, which is the movement using the
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Table 1. Constitutive Laws Used in Model Element Bone Biceps tendon Labrum Rotator cuff
Type of Law Linear elasticity Linear elasticity Linear elasticity Hyperelasticity
Mechanical Properties E0 ¼ 15,000 MPa E0 ¼ 629 MPa E0 ¼ 33 MPa W ¼ a exp[b(I1 3)] ¼ ab/2(I2 2), a ¼ 0.12 MPa, b ¼ 1.0
Poisson Ratio 0.3 0.478 0.478 0.478
NOTE. I1 and I2 are the first and second invariants, respectively, of the Cauchy-Green tensor. E0, elastic modulus.
instantaneous center of rotation, is the most appropriate method of simulation, which represents the shortest path from position to position containing rotation and translation components.18,19 Each motion was designed to avoid excessive twisting and bending of the intra-articular portion of the biceps tendon, which are major causes of analysis failure (Fig 1B). 3D Modeling of Rotator Cuff and Biceps-Labral Complex Next, we performed MRI with the upper limb in neutral rotation. MRI was performed in the supine position to minimize any motion artifacts related to the uncomfortable prone position, which is a more challenging position because of the long imaging time. The
5-inch general purpose surface coil was centered on the rotator interval. The following main parameters were used: slice thickness, 3 mm; distance between slices, 1 mm; and spin echo T2-weighted sequence (echo time, 20 milliseconds; repetition time, 2,000 milliseconds). To obtain a 3D image of the biceps-labral complex and upper part of the rotator cuff, all coronal, axial, and sagittal views were used. Multiple primitive 3D images of the biceps-labral complex and rotator cuff obtained separately from these 3 different views were combined and optimized through a reverse engineering process. Structural Assembly for Glenohumeral Joint Model The 3D images that were created using both CT and MRI were imported into a validated customized software program (Rapidform 2006; Rapidform, Seoul,
Fig 3. Contact condition of biceps-labral complex on glenoid. (A) Full contact between glenoid edge and corresponding labral complex, indicating stable biceps-labral complex. (B) Unstable biceps-labral complex on posterosuperior quadrant, simulating SLAP lesion. Dotted line illustrates the detached portion of the glenoid labrum out of the posterosuperior glenoid.
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Fig 4. Impingement pattern in abductioneexternal rotation position. (A) Posterior part of rotator cuff interposing between humeral head and glenoid. (B) Stress value for rotator cuff. (C) Stress value for posterosuperior labrum.
Republic of Korea) to analyze spatial relations between anatomic structures. The size and shape of the scapula at 0 from the CT and MRI scans were almost identical because both scapular images were obtained from the same subject. Both scapular datasets had the same orientation, and at least 3 pairs of anatomic landmark points were determined to be detected in both datasets. Those landmark points were used as registration points to register both image datasets on top of each other. With this methodology, the MRIbased scapula combined with biceps-labral complex and rotator cuff was superimposed onto the CT-based scapula with high measurement accuracy of 0.01 mm and 0.5 . After superimposition of the two scapulae into one, the bony images from MRI were eliminated. The assembled 3D glenohumeral joint model including the rotator cuff and biceps-labral complex was then exported to the special-purpose finite element preprocessor Hyperworks (Altair Engineering, Troy, MI), in Table 2. Maximal Value of von Mises Stress in Stable Labrum Versus Unstable Posterosuperior Labrum in AbductioneExternal Rotation Position von Mises Stress, MPa Normal labrum model SLAP model
Labrum 19.7 5.8
Rotator Cuff 23.5 18.1
which the final computational model was constructed for virtual analysis. Finite element analysis from 0 to the ABER position of the glenohumeral model was performed with Abaqus/Explicit code (Simulia, Providence, Rhode Island), in which the scapula and humerus were modeled as rigid bodies because the stiffness of bony structures is much higher than that of soft tissues. The overall computerized 3D modeling process is depicted in Figure 2. Geometrical Data and Boundary Conditions The glenoid and humeral head were assumed to be rigid. The constructed biceps-labral complex was considered elastic material with its own elastic modulus, which is the mathematical description of an object’s or substance’s tendency to be deformed elastically (i.e., non-permanently) when a force is applied. The rotator cuff was composed of exponential hyperelastic incompressible rubber-like material with the expectation of excessive torsion of the nodes in the process of reaching the ABER position.20 The elastic moduli for the labrum and biceps tendon were assumed to be 33 MPa and 629 MPa, respectively,19-23 as shown in Table 1. Each soft-tissue structure was bonded to its own attachment site using mesh tie kinematic constraints.24 The glenoid labrum and long head of the biceps (LHB) were fixed to the corresponding glenoid margin. In
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Fig 5. Structural changes in designed SLAP model. (A) Posterosuperior labrum with abduction and horizontal extension of humeral head. (B) Medial displacement of posterosuperior labrum with additional external rotation.
particular, the LHB was designed to attach separately to the supraglenoid tubercle and to have the least number of kinematic ties to the adjacent superior labrum. This boundary condition was inevitably set because the posterosuperior labrum should not be affected by a change in tension of the biceps tendon during the simulation process. We constructed 2 types of labral attachment models, an entirely tied glenoid labrum on the glenoid margin and a partially untied labrum on the glenoid margin, through choosing suitable attachment as depicted in Figure 3. The bursal side of the rotator cuff tissue over the medial insertion line of the footprint was intentionally eliminated because of expected excessive twisting of the nodes, resulting in analysis failure. As a result, the rotator cuff insertion was prescribed as the only linearshaped attachment along the articular border. The elements around the bicipital groove and LHB tendon were defined as contact bodies. The friction coefficient was determined as 0 in this study. During the humeral motion between 0 and the ABER position, 2 constant force springs, pre-tensioned to 10 N each, were applied to sustain the geometry of the rotator cuff and LHB. These pre-tensioned muscle forces were essential not only to avoid spatial changes of the rotator cuff and LHB but also to ensure that the rotator cuff and LHB were well positioned within the supraspinatus fossa and bicipital groove, respectively, during the positional change of the humerus with
respect to the scapula. The magnitude of pre-tension force was determined as the minimum force that might not affect the outcome and should be extrapolated by pure contact force. Finally, the kinematics for shoulder abduction and shoulder rotation was prescribed as input to the finite element simulations, and the resulting stress values on the rotator cuff and labrum were predicted.
Results In the ABER position, the posterosuperior labrum was deformed by the humeral head and interposed posterior part of the rotator cuff. When viewed from the rotator cuff, the posterior part of the rotator cuff came into contact with the posterosuperior labrum as external rotation increased, as depicted in Figure 4. In the designed SLAP model, the posterosuperior labrum moved medially rather than undergoing structural deformation during ABER movement. The peak contact stress values at the ABER position were 19.7 MPa and 23.5 MPa for the posterosuperior labrum and the upper rotator cuff, respectively (Fig 4, Table 2). The peak contact stress values for both structures decreased to 5.8 MPa and 18.1 MPa, respectively, in the designed SLAP model. The root of the LHB became compressed halfway through the range of motion by the humeral head, especially from the beginning of horizontal extension and external rotation, resulting in a high stress of 22.4 MPa (Fig 5).
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Discussion The principal findings of this study determined that the posterior part of the upper rotator cuff, LHB, and posterosuperior labrum were the structures at risk with the ABER position. These findings suggest that those structures might be damaged by repetitive impingement when the arm is in an abducted and maximally externally rotated position.14,15,25 High stresses especially on the undersurface of the posterior rotator cuff and posterosuperior labrum were caused by mutual compression between the humeral head and corresponding posterosuperior glenoid rim. This finding partly supports studies from Jobe,2,3 who described the junction of the posterior supraspinatus and anterior infraspinatus as a highly vulnerable area. In vivo simulation of the shoulder during motion has, in fact, been challenging. Likewise, modeling a certain range of glenohumeral motion considering scapulothoracic motion in the laboratory is technically difficult. For this reason, the main theories regarding the pathogenesis in internal impingement seemed to be extrapolated from surgical and radiologic findings observed in overhead athletes who had shoulder pain.11,14,15,26 These theoretical backgrounds of internal impingement led us to design an in vivo glenohumeral model moving from 0 of abduction to the ABER position with finite elementemodeled soft-tissue structures. To enhance the accurate motion of the glenohumeral joint in this study, we used a voxel-based registration technique followed by fine manual transformation of the local coordinate system with reverse engineering software.27,28 These techniques were developed to transform the coordinates of a point from one coordinate system to another coordinate system. By use of these techniques, a segmented scapula at 0 of abduction was accurately superimposed on a scapula in the ABER position, resulting in 2 different humeral positions on one scapula. On the basis of the spatial coordinates with the humerus set at 0 and the spatial linkage between the humeral heads, an optimal arc of humeral motion from 0 to the ABER position was simulated. As mentioned in the “Methods” section, we designed humeral motion from 0 of abduction to the ABER position with 2 phases. Phase 1 was scapular-plane abduction ranging from 0 to 68 with the rotation center set within the humeral head at 0 of abduction based on the z-axis of the scapula. The 68 angle of scapular-plane abduction was the maximal angle just before impingement of the great tubercle occurred against the lateral acromion. Phase 2 was horizontal extension combined with external rotation from the position at the end of phase 1. Phase 2 motion was controlled by the screw axis passing through 2 humeral heads in abduction and the ABER position. Each phase of motion was designed to avoid excessive twisting and
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bending of the soft-tissue element models, which are major causes of analytical failure. Although this stepwise humeral motion could not exactly replicate real glenohumeral motion, it might be rather similar to the optimal arm path to the late-cocked position. Another important process was to reconstruct the soft-tissue structures from the magnetic resonance images. This was accomplished by merging each incomplete 3D image from multiple planes on MRI. A merged image consisted of 3 aligned images. That is, we aligned the data for 3 MRI soft-tissue views (with sagittal, axial, and coronal views as the main axis, which was considered the axis that had the best resolution or slicing direction) to provide 1 MRI merged image, which presented high resolution in all views. These merged images from MRI were remodeled with a reverse engineering process by trimming, filling, and smoothing the merging surface. In the final process to reconstruct the complete 3D glenohumeral joint, merged images were correctly attached to 3D bony structures obtained on CT images by a superimposing process, as depicted in Figure 1. These combined 3D images from both CT and MRI provided important insight into the role of the biceps-labral complex between 0 and the ABER position by identifying the contact area and magnitude of contact stress. As a consequence, our findings suggest that the posterosuperior labrum plays a dynamic role along with the LHB in stabilizing the humeral head by positioning together between the inner rotator cuff tendon and posterosuperior margin of the glenoid, which helps to prevent abnormal translation of the humeral head at the ABER position. This speculation was also supported by data from the simulated SLAP model. There was a decrease in stress due to the medial displacement of the posterosuperior labrum instead of its structural deformation against force from the humeral head. However, these findings generated from the SLAP model could be contradictory to the real situation because of the possibility of posterosuperior subluxation of the humeral head in the ABER position. Consequently, the loss of the biceps-labral complex might lead to gradual damage to the rotator cuff while performing tasks such as throwing a ball in overhead athletes or tasks involving simple abduction in the elderly population with protracted scapulae. Thus a SLAP lesion, which possibly deletes the positional effect of the LHB in the overhead position, may act as a precursor for a rotator cuff tear. Our results support the findings of an MRI study performed by Chhadia et al.,29 who reported that the humeral head was slightly subluxated posterosuperiorly in the ABER position in patients with type II SLAP lesions. This finding indicates that the posterosuperior labral complex is a key structure that inhibits
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the upward displacement of the humeral head during shoulder abduction. In addition, this study supports the theory of Burkhart et al.30,31 that tears in the posterosuperior labrum occur with external rotation of the arm combined with shear. On the basis of their arthroscopic findings, they stated that glenohumeral internal rotation deficit, exceeding external rotation gain, might contribute to pathologic shoulder internal impingement and the peel-back phenomenon of the superior labrum. Our study also provides information regarding structural and tension changes in the bicepsesuperior labral complex. On the basis of this information, we assume that the main dynamic roles of the LHB tendon and superior labrum are to diminish the stress that would be loaded on the undersurface of the rotator cuff in internal impingement and to contribute to posterosuperior glenohumeral stability in an excessively abducted and externally rotated position by its structural and positional changes under tension. Limitations This study has some limitations. First, we assumed that both the labrum and rotator cuff were incompressible hyperelastic materials, although actual in vivo soft tissues are compressible. For this reason, we compared only the patterns of stress distribution on the labrum and upper part of the rotator cuff and did not seek to determine the absolute values of equivalent stresses. Second, the stress patterns were considered only at 2 discrete abduction angles, rather than as a continuum. In fact, we could not determine the constant rotation center during motion from 0 to the ABER position of the humerus. For this reason, we intended to add an instantaneous center to continue humeral motion simulation. Although we successfully simulated humeral motion between 0 and 120 with precise methods, this motion track would not be the same as real glenohumeral motion. Therefore data obtained during the whole simulation arc, except the final ABER position, were not used in this study. Third, we admit that the position in which either the labrum or rotator cuff was attached would not be completely accurate compared with cadaveric models. Therefore, to decrease error, we constructed the labrum and rotator cuff multiple times to minimize manufacturer error and attached them to the natural footprint as precisely as possible based on outlines of each footprint by reproducing marginal ridges, which were considered to be the borderlines of the footprints. Finally, this study evaluated only theoretical application of shear to the labrum through the humeral head and did not investigate pure tensile failure mechanics to the posterosuperior labrum through the eccentric load on the biceps. Nevertheless, by performing only compressive failure mechanics, we did reproduce the
peel-back phenomenon, which is frequently observed in SLAP lesions.32 Therefore we assume that the results of our study might well explain the pathomechanisms of SLAP lesions and rotator cuff tears from a biomechanical point of view.
Conclusions In this simulated SLAP model, the posterosuperior labrum was medially displaced by the humeral head and upper rotator cuff in the ABER position, causing a functional loss of the spacer effect.
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double-bundle anterior cruciate ligament reconstruction at different knee flexion angles: A study using a 3-dimensional finite element model. Arthroscopy 2011;27: 1400-1408. Yeh ML, Lintner D, Luo ZP. Stress distribution in the superior labrum during throwing motion. Am J Sports Med 2005;33:395-401. Kaplan LD, McMahon PJ, Towers J, Irrgang JJ, Rodosky MW. Internal impingement: Findings on magnetic resonance imaging and arthroscopic evaluation. Arthroscopy 2004;20:701-704. Hill DL, Batchelor PG, Holden M, Hawkes DJ. Medical image registration. Phys Med Biol 2001;46:R1-R45. Sahara W, Sugamoto K, Murai M, Tanaka H, Yoshikawa H. The three-dimensional motions of glenohumeral joint under semi-loaded condition during arm abduction using vertically open MRI. Clin Biomech 2007;22:304-312. Chhadia AM, Goldberg BA, Hutchinson MR. Abnormal translation in SLAP lesions on magnetic resonance imaging abducted externally rotated view. Arthroscopy 2010;26:19-25. Mihata T, Jun BJ, Bui CN, et al. Effect of scapular orientation on shoulder internal impingement in a cadaveric model of the cocking phase of throwing. J Bone Joint Surg Am 2012;94:1576-1583. Burkhart SS, Morgan CD, Ben Kibler W. The disabled throwing shoulder: Spectrum of pathology Part III: The SICK scapula, scapular dyskinesis, the kinetic chain, and rehabilitation. Arthroscopy 2003;19:641-661. Burkhart SS, Morgan CD, Kibler WB. The disabled throwing shoulder: Spectrum of pathology Part I: pathoanatomy and biomechanics. Arthroscopy 2003;19: 404-420.
Purpose: To quantitatively and qualitatively evaluate the impingement behavior between structures within the glenohumeral joint under simulated abductioneexternal rotation (ABER) motion using finite element analysis. Methods: Computed tomography (CT) scanning of 1 shoulder in a volunteer was performed at 0 and 120 of shoulder abduction with external rotation (ABER position), followed by magnetic resonance imaging at 0 of abduction. The CT and magnetic resonance images were then imported into a customized software program to undergo 3-dimensional reconstruction followed by finite element modeling of the bone and soft tissue including the upper part of the rotator cuff and glenohumeral labral complex. Glenohumeral motion from 0 to the ABER position was simulated by CT images in 2 different humeral positions. On the basis of simulated humeral motion with respect to the scapula, we measured the stress value on the biceps-labral complex and upper part of the rotator cuff as a consequence of their structural deformation. In addition, we intended to design 2 types of labrada normal stable labrum and an unstable posterosuperior labrumdto evaluate the geometric alteration and resulting stress change on the posterosuperior labrum against a compressive force from the humeral head and rotator cuff. Results: In the ABER position, the posterosuperior labrum was deformed by the humeral head and interposed posterior part of the rotator cuff. When viewed from the rotator cuff, the posterior part of the rotator cuff came into contact with the posterosuperior labrum as external rotation increased. The measured peak contact stress values were 19.7 MPa and 23.5 MPa for the posterosuperior labrum and the upper rotator cuff, respectively. The stress values for both structures decreased to 5.8 MPa and 18.1 MPa, respectively, in the simulated SLAP model. The root of the long head of the biceps became compressed halfway through the range of motion by the humeral head, especially from the part involving horizontal extension and external rotation, resulting in a high stress of 22.4 MPa. Conclusions: In this simulated SLAP model, the posterosuperior labrum was medially displaced by the humeral head and upper rotator cuff in the ABER position, causing a functional loss of the spacer effect. Clinical Relevance: In SLAP lesions, the posterosuperior labrum loses its ability to function as a spacer in certain positions (especially ABER) and may decrease the important spacer effect between the humerus and the rotator cuff; this may lead to posterosuperior subluxation of the humeral head or rotator cuff abnormalities and tears during repetitive ABER tasks.
From the School of Computer Science and Engineering, Korea University of Technology and Education (S.W.J., Y.S.K.), Cheonan; and Department of Orthopaedic Surgery, Hallym University (Y-S.Y., H-Y.L., P.K.S., A.V.N.), Dongtan, Republic of Korea. The authors report the following potential conflict of interest or source of funding: Funded by the National Research Foundation of Korea, Ministry of Education (grant 2013R1A1A2011589 to Y-S.Y.). Received January 13, 2014; accepted April 10, 2015. Address correspondence to Yon-Sik Yoo, M.D., Department of Orthopaedic Surgery, Hallym University Hospital, Dongtan, 40 Sukwoo-Dong, Hwasung, Gyung-gi, 445-170 Republic of Korea. E-mail: [email protected] Ó 2015 by the Arthroscopy Association of North America 0749-8063/1430/$36.00 http://dx.doi.org/10.1016/j.arthro.2015.04.082
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nternal impingement of the shoulder has been shown to be one of the important factors that cause significant disability in the throwing athlete.1-9 Although this phenomenon is known to occur mainly in throwing athletes, it is also present in the general population, especially persons with altered scapulothoracic positions and rhythm.10 In fact, a magnetic resonance imaging (MRI) study performed by Halbrecht et al.11 showed contact between the undersurface of the rotator cuff and the posterosuperior labrum in the abducted externally rotated position in both throwing and non-throwing shoulders. A similar phenomenon can be seen in the computer worker, the
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Fig 1. (A) Coordinate system associated with humeral motion with respect to scapula. The x-axis is parallel to the glenoid plane and is directed superior-inferiorly. The y-axis is the longitudinal axis of the supraspinatus muscle and is directed medial-laterally. The z-axis is the cross product of the x- and y-axes. (B) Scapular-plane abduction (ABD) using spatial coordinate set on center of humeral head. (C) Horizontal extension (HE) and external rotation (ER) using spatial linkage between heads. The gray bar indicates the screw axis.
recreational athlete, and the elderly patient, who commonly have a protracted scapula.12-17 Altered glenoid version as a result of scapular protraction induces posterosuperior internal impingement even while one is performing simple abduction tasks.17 This implies that posterosuperior internal impingement due to scapular protraction might be one of the initiating factors of SLAP lesions and rotator cuff tears in non-throwing shoulders, when contact is magnified both in intensity and in frequency. However, the exact kinematics of the surrounding structures and its pathogenesis during contact are yet to be understood. Likewise, modeling of the throwing shoulder and simulation of abnormal kinematics of the scapula in the laboratory are more technically demanding. Therefore we intended to construct an in vivo 3-dimensional (3D) glenohumeral motion model and simulate the phenomenon of internal impingement of the shoulder using the abductioneexternal rotation (ABER) position. Glenohumeral motion was simulated based on computed tomography (CT) images in 2 different humeral positions. On the basis of simulated humeral motion with respect to the scapula, we measured the stress value on the glenoid labrum and upper part of the rotator cuff as a consequence of their structural changes. In addition, we designed the SLAP model by changing the contact condition between the posterosuperior quadrant of the labrum and corresponding glenoid margin to observe the geometrical changes in the labrum under repetitive motion simulation. The objective of this study was to quantitatively and qualitatively evaluate the impingement behavior between structures within the glenohumeral joint under simulated ABER motion using finite element analysis. We hypothesized that the structural contact in the ABER position mainly would occur at the posterosuperior portion of the glenoid as a consequence of
impingement between the rotator cuff and posterosuperior labrum. Furthermore, we hypothesized that the simulated SLAP model would lead to a decrease in contact stress between structures due to medial displacement of the posterosuperior labrum against a compressive force from the humeral head and upper rotator cuff during ABER movement.
Methods 3D Bone Modeling and Motion Simulation Procedure The right shoulder of a 29-year-old volunteer was scanned with a high-resolution CT scanner (Somatom Sensation; Siemens, Erlangen, Germany) with 1-mm slices taken at 2 different shoulder angles in the prone position: 0 (neutral rotation) and the ABER position. The prone position was selected because it was believed to allow appropriate scapular motion while positioning the shoulder at different abduction angles in limited space. The study was approved by our institutional review board (2014-12), and informed consent was obtained from the volunteer. The ABER position was achieved by placing the hand behind the occiput at 120 of abduction. The 120 angle was determined by measuring the humeral position relative to the trunk. The DICOM (Digital Imaging and Communications in Medicine) files obtained were imported into visualization software (Amira R 4.0; Mercury Computer Systems, Chelmsford, MA) to construct virtual 3D bone models. Humeral motion from 0 to the ABER position with respect to the fixed scapula proceeded in 3 steps: (1) We superimposed the scapula at 120 onto the scapula at 0 of shoulder abduction using positional information of the coordinates. (2) We accurately determined the position and orientation of the humerus in space at 0 and the
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Fig 2. Overall computer 3dimensional (3D) modeling and simulation process. (ABER, abductioneexternal rotation; CT, computed tomography; DICOM, Digital Imaging and Communications in Medicine; MRI, magnetic resonance imaging.)
ABER position with respect to the scapula. (3) By use of spatial coordinates with the humerus set at 0 and the spatial linkage between the humeral heads, an arc of humeral motion from 0 to the ABER position was simulated. The total arc of humeral motion was designed to focus on the realistic arm path to the latecocked position, which has been considered initial scapular-plane abduction followed by horizontal extension combined with external rotation of the humerus. The origin of the local coordinate system in space was set at the center of the humeral head. A Euler angle system was used to describe the motion of the humerus with respect to the scapula. The x-axis was parallel to the glenoid plane and was directed superior-inferiorly. The y-axis followed the longitudinal axis of the supraspinatus muscle and was directed medial-laterally. The z-axis was directed externally and obtained by the cross product of the x- and y-axes (Fig 1A). The first motion
was scapular-plane abduction ranging from 0 to 68 with the rotation center set within the humeral head at 0 of abduction based on the z-axis of the scapula. We set 68 as the maximal abduction angle just before the impingement between the humeral head and corresponding labrum. In this circumstance, the glenohumeral joint was considered a ball-and-socket joint and the rotation center was determined by fitting a sphere to the articulating surface of the humeral head, although the humeral head was not a real sphere. For the remaining motion, we intended to adopt an instantaneous center of rotation to accomplish the best fit during scapular-plane abduction to the ABER position because there was no constant rotation center between the 2 humeral heads. The spatial linkage (also known as the “screw axis”) was used to simulate motion for horizontal extension combined with external rotation of the humerus. The screw axis motion, which is the movement using the
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Table 1. Constitutive Laws Used in Model Element Bone Biceps tendon Labrum Rotator cuff
Type of Law Linear elasticity Linear elasticity Linear elasticity Hyperelasticity
Mechanical Properties E0 ¼ 15,000 MPa E0 ¼ 629 MPa E0 ¼ 33 MPa W ¼ a exp[b(I1 3)] ¼ ab/2(I2 2), a ¼ 0.12 MPa, b ¼ 1.0
Poisson Ratio 0.3 0.478 0.478 0.478
NOTE. I1 and I2 are the first and second invariants, respectively, of the Cauchy-Green tensor. E0, elastic modulus.
instantaneous center of rotation, is the most appropriate method of simulation, which represents the shortest path from position to position containing rotation and translation components.18,19 Each motion was designed to avoid excessive twisting and bending of the intra-articular portion of the biceps tendon, which are major causes of analysis failure (Fig 1B). 3D Modeling of Rotator Cuff and Biceps-Labral Complex Next, we performed MRI with the upper limb in neutral rotation. MRI was performed in the supine position to minimize any motion artifacts related to the uncomfortable prone position, which is a more challenging position because of the long imaging time. The
5-inch general purpose surface coil was centered on the rotator interval. The following main parameters were used: slice thickness, 3 mm; distance between slices, 1 mm; and spin echo T2-weighted sequence (echo time, 20 milliseconds; repetition time, 2,000 milliseconds). To obtain a 3D image of the biceps-labral complex and upper part of the rotator cuff, all coronal, axial, and sagittal views were used. Multiple primitive 3D images of the biceps-labral complex and rotator cuff obtained separately from these 3 different views were combined and optimized through a reverse engineering process. Structural Assembly for Glenohumeral Joint Model The 3D images that were created using both CT and MRI were imported into a validated customized software program (Rapidform 2006; Rapidform, Seoul,
Fig 3. Contact condition of biceps-labral complex on glenoid. (A) Full contact between glenoid edge and corresponding labral complex, indicating stable biceps-labral complex. (B) Unstable biceps-labral complex on posterosuperior quadrant, simulating SLAP lesion. Dotted line illustrates the detached portion of the glenoid labrum out of the posterosuperior glenoid.
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Fig 4. Impingement pattern in abductioneexternal rotation position. (A) Posterior part of rotator cuff interposing between humeral head and glenoid. (B) Stress value for rotator cuff. (C) Stress value for posterosuperior labrum.
Republic of Korea) to analyze spatial relations between anatomic structures. The size and shape of the scapula at 0 from the CT and MRI scans were almost identical because both scapular images were obtained from the same subject. Both scapular datasets had the same orientation, and at least 3 pairs of anatomic landmark points were determined to be detected in both datasets. Those landmark points were used as registration points to register both image datasets on top of each other. With this methodology, the MRIbased scapula combined with biceps-labral complex and rotator cuff was superimposed onto the CT-based scapula with high measurement accuracy of 0.01 mm and 0.5 . After superimposition of the two scapulae into one, the bony images from MRI were eliminated. The assembled 3D glenohumeral joint model including the rotator cuff and biceps-labral complex was then exported to the special-purpose finite element preprocessor Hyperworks (Altair Engineering, Troy, MI), in Table 2. Maximal Value of von Mises Stress in Stable Labrum Versus Unstable Posterosuperior Labrum in AbductioneExternal Rotation Position von Mises Stress, MPa Normal labrum model SLAP model
Labrum 19.7 5.8
Rotator Cuff 23.5 18.1
which the final computational model was constructed for virtual analysis. Finite element analysis from 0 to the ABER position of the glenohumeral model was performed with Abaqus/Explicit code (Simulia, Providence, Rhode Island), in which the scapula and humerus were modeled as rigid bodies because the stiffness of bony structures is much higher than that of soft tissues. The overall computerized 3D modeling process is depicted in Figure 2. Geometrical Data and Boundary Conditions The glenoid and humeral head were assumed to be rigid. The constructed biceps-labral complex was considered elastic material with its own elastic modulus, which is the mathematical description of an object’s or substance’s tendency to be deformed elastically (i.e., non-permanently) when a force is applied. The rotator cuff was composed of exponential hyperelastic incompressible rubber-like material with the expectation of excessive torsion of the nodes in the process of reaching the ABER position.20 The elastic moduli for the labrum and biceps tendon were assumed to be 33 MPa and 629 MPa, respectively,19-23 as shown in Table 1. Each soft-tissue structure was bonded to its own attachment site using mesh tie kinematic constraints.24 The glenoid labrum and long head of the biceps (LHB) were fixed to the corresponding glenoid margin. In
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Fig 5. Structural changes in designed SLAP model. (A) Posterosuperior labrum with abduction and horizontal extension of humeral head. (B) Medial displacement of posterosuperior labrum with additional external rotation.
particular, the LHB was designed to attach separately to the supraglenoid tubercle and to have the least number of kinematic ties to the adjacent superior labrum. This boundary condition was inevitably set because the posterosuperior labrum should not be affected by a change in tension of the biceps tendon during the simulation process. We constructed 2 types of labral attachment models, an entirely tied glenoid labrum on the glenoid margin and a partially untied labrum on the glenoid margin, through choosing suitable attachment as depicted in Figure 3. The bursal side of the rotator cuff tissue over the medial insertion line of the footprint was intentionally eliminated because of expected excessive twisting of the nodes, resulting in analysis failure. As a result, the rotator cuff insertion was prescribed as the only linearshaped attachment along the articular border. The elements around the bicipital groove and LHB tendon were defined as contact bodies. The friction coefficient was determined as 0 in this study. During the humeral motion between 0 and the ABER position, 2 constant force springs, pre-tensioned to 10 N each, were applied to sustain the geometry of the rotator cuff and LHB. These pre-tensioned muscle forces were essential not only to avoid spatial changes of the rotator cuff and LHB but also to ensure that the rotator cuff and LHB were well positioned within the supraspinatus fossa and bicipital groove, respectively, during the positional change of the humerus with
respect to the scapula. The magnitude of pre-tension force was determined as the minimum force that might not affect the outcome and should be extrapolated by pure contact force. Finally, the kinematics for shoulder abduction and shoulder rotation was prescribed as input to the finite element simulations, and the resulting stress values on the rotator cuff and labrum were predicted.
Results In the ABER position, the posterosuperior labrum was deformed by the humeral head and interposed posterior part of the rotator cuff. When viewed from the rotator cuff, the posterior part of the rotator cuff came into contact with the posterosuperior labrum as external rotation increased, as depicted in Figure 4. In the designed SLAP model, the posterosuperior labrum moved medially rather than undergoing structural deformation during ABER movement. The peak contact stress values at the ABER position were 19.7 MPa and 23.5 MPa for the posterosuperior labrum and the upper rotator cuff, respectively (Fig 4, Table 2). The peak contact stress values for both structures decreased to 5.8 MPa and 18.1 MPa, respectively, in the designed SLAP model. The root of the LHB became compressed halfway through the range of motion by the humeral head, especially from the beginning of horizontal extension and external rotation, resulting in a high stress of 22.4 MPa (Fig 5).
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Discussion The principal findings of this study determined that the posterior part of the upper rotator cuff, LHB, and posterosuperior labrum were the structures at risk with the ABER position. These findings suggest that those structures might be damaged by repetitive impingement when the arm is in an abducted and maximally externally rotated position.14,15,25 High stresses especially on the undersurface of the posterior rotator cuff and posterosuperior labrum were caused by mutual compression between the humeral head and corresponding posterosuperior glenoid rim. This finding partly supports studies from Jobe,2,3 who described the junction of the posterior supraspinatus and anterior infraspinatus as a highly vulnerable area. In vivo simulation of the shoulder during motion has, in fact, been challenging. Likewise, modeling a certain range of glenohumeral motion considering scapulothoracic motion in the laboratory is technically difficult. For this reason, the main theories regarding the pathogenesis in internal impingement seemed to be extrapolated from surgical and radiologic findings observed in overhead athletes who had shoulder pain.11,14,15,26 These theoretical backgrounds of internal impingement led us to design an in vivo glenohumeral model moving from 0 of abduction to the ABER position with finite elementemodeled soft-tissue structures. To enhance the accurate motion of the glenohumeral joint in this study, we used a voxel-based registration technique followed by fine manual transformation of the local coordinate system with reverse engineering software.27,28 These techniques were developed to transform the coordinates of a point from one coordinate system to another coordinate system. By use of these techniques, a segmented scapula at 0 of abduction was accurately superimposed on a scapula in the ABER position, resulting in 2 different humeral positions on one scapula. On the basis of the spatial coordinates with the humerus set at 0 and the spatial linkage between the humeral heads, an optimal arc of humeral motion from 0 to the ABER position was simulated. As mentioned in the “Methods” section, we designed humeral motion from 0 of abduction to the ABER position with 2 phases. Phase 1 was scapular-plane abduction ranging from 0 to 68 with the rotation center set within the humeral head at 0 of abduction based on the z-axis of the scapula. The 68 angle of scapular-plane abduction was the maximal angle just before impingement of the great tubercle occurred against the lateral acromion. Phase 2 was horizontal extension combined with external rotation from the position at the end of phase 1. Phase 2 motion was controlled by the screw axis passing through 2 humeral heads in abduction and the ABER position. Each phase of motion was designed to avoid excessive twisting and
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bending of the soft-tissue element models, which are major causes of analytical failure. Although this stepwise humeral motion could not exactly replicate real glenohumeral motion, it might be rather similar to the optimal arm path to the late-cocked position. Another important process was to reconstruct the soft-tissue structures from the magnetic resonance images. This was accomplished by merging each incomplete 3D image from multiple planes on MRI. A merged image consisted of 3 aligned images. That is, we aligned the data for 3 MRI soft-tissue views (with sagittal, axial, and coronal views as the main axis, which was considered the axis that had the best resolution or slicing direction) to provide 1 MRI merged image, which presented high resolution in all views. These merged images from MRI were remodeled with a reverse engineering process by trimming, filling, and smoothing the merging surface. In the final process to reconstruct the complete 3D glenohumeral joint, merged images were correctly attached to 3D bony structures obtained on CT images by a superimposing process, as depicted in Figure 1. These combined 3D images from both CT and MRI provided important insight into the role of the biceps-labral complex between 0 and the ABER position by identifying the contact area and magnitude of contact stress. As a consequence, our findings suggest that the posterosuperior labrum plays a dynamic role along with the LHB in stabilizing the humeral head by positioning together between the inner rotator cuff tendon and posterosuperior margin of the glenoid, which helps to prevent abnormal translation of the humeral head at the ABER position. This speculation was also supported by data from the simulated SLAP model. There was a decrease in stress due to the medial displacement of the posterosuperior labrum instead of its structural deformation against force from the humeral head. However, these findings generated from the SLAP model could be contradictory to the real situation because of the possibility of posterosuperior subluxation of the humeral head in the ABER position. Consequently, the loss of the biceps-labral complex might lead to gradual damage to the rotator cuff while performing tasks such as throwing a ball in overhead athletes or tasks involving simple abduction in the elderly population with protracted scapulae. Thus a SLAP lesion, which possibly deletes the positional effect of the LHB in the overhead position, may act as a precursor for a rotator cuff tear. Our results support the findings of an MRI study performed by Chhadia et al.,29 who reported that the humeral head was slightly subluxated posterosuperiorly in the ABER position in patients with type II SLAP lesions. This finding indicates that the posterosuperior labral complex is a key structure that inhibits
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the upward displacement of the humeral head during shoulder abduction. In addition, this study supports the theory of Burkhart et al.30,31 that tears in the posterosuperior labrum occur with external rotation of the arm combined with shear. On the basis of their arthroscopic findings, they stated that glenohumeral internal rotation deficit, exceeding external rotation gain, might contribute to pathologic shoulder internal impingement and the peel-back phenomenon of the superior labrum. Our study also provides information regarding structural and tension changes in the bicepsesuperior labral complex. On the basis of this information, we assume that the main dynamic roles of the LHB tendon and superior labrum are to diminish the stress that would be loaded on the undersurface of the rotator cuff in internal impingement and to contribute to posterosuperior glenohumeral stability in an excessively abducted and externally rotated position by its structural and positional changes under tension. Limitations This study has some limitations. First, we assumed that both the labrum and rotator cuff were incompressible hyperelastic materials, although actual in vivo soft tissues are compressible. For this reason, we compared only the patterns of stress distribution on the labrum and upper part of the rotator cuff and did not seek to determine the absolute values of equivalent stresses. Second, the stress patterns were considered only at 2 discrete abduction angles, rather than as a continuum. In fact, we could not determine the constant rotation center during motion from 0 to the ABER position of the humerus. For this reason, we intended to add an instantaneous center to continue humeral motion simulation. Although we successfully simulated humeral motion between 0 and 120 with precise methods, this motion track would not be the same as real glenohumeral motion. Therefore data obtained during the whole simulation arc, except the final ABER position, were not used in this study. Third, we admit that the position in which either the labrum or rotator cuff was attached would not be completely accurate compared with cadaveric models. Therefore, to decrease error, we constructed the labrum and rotator cuff multiple times to minimize manufacturer error and attached them to the natural footprint as precisely as possible based on outlines of each footprint by reproducing marginal ridges, which were considered to be the borderlines of the footprints. Finally, this study evaluated only theoretical application of shear to the labrum through the humeral head and did not investigate pure tensile failure mechanics to the posterosuperior labrum through the eccentric load on the biceps. Nevertheless, by performing only compressive failure mechanics, we did reproduce the
peel-back phenomenon, which is frequently observed in SLAP lesions.32 Therefore we assume that the results of our study might well explain the pathomechanisms of SLAP lesions and rotator cuff tears from a biomechanical point of view.
Conclusions In this simulated SLAP model, the posterosuperior labrum was medially displaced by the humeral head and upper rotator cuff in the ABER position, causing a functional loss of the spacer effect.
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double-bundle anterior cruciate ligament reconstruction at different knee flexion angles: A study using a 3-dimensional finite element model. Arthroscopy 2011;27: 1400-1408. Yeh ML, Lintner D, Luo ZP. Stress distribution in the superior labrum during throwing motion. Am J Sports Med 2005;33:395-401. Kaplan LD, McMahon PJ, Towers J, Irrgang JJ, Rodosky MW. Internal impingement: Findings on magnetic resonance imaging and arthroscopic evaluation. Arthroscopy 2004;20:701-704. Hill DL, Batchelor PG, Holden M, Hawkes DJ. Medical image registration. Phys Med Biol 2001;46:R1-R45. Sahara W, Sugamoto K, Murai M, Tanaka H, Yoshikawa H. The three-dimensional motions of glenohumeral joint under semi-loaded condition during arm abduction using vertically open MRI. Clin Biomech 2007;22:304-312. Chhadia AM, Goldberg BA, Hutchinson MR. Abnormal translation in SLAP lesions on magnetic resonance imaging abducted externally rotated view. Arthroscopy 2010;26:19-25. Mihata T, Jun BJ, Bui CN, et al. Effect of scapular orientation on shoulder internal impingement in a cadaveric model of the cocking phase of throwing. J Bone Joint Surg Am 2012;94:1576-1583. Burkhart SS, Morgan CD, Ben Kibler W. The disabled throwing shoulder: Spectrum of pathology Part III: The SICK scapula, scapular dyskinesis, the kinetic chain, and rehabilitation. Arthroscopy 2003;19:641-661. Burkhart SS, Morgan CD, Kibler WB. The disabled throwing shoulder: Spectrum of pathology Part I: pathoanatomy and biomechanics. Arthroscopy 2003;19: 404-420.
