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The function of the clavicle on scapular motion: a cadaveric study
J Shoulder Elbow Surg (2013) 22, 333-339
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The function of the clavicle on scapular motion: a cadaveric study Noboru Matsumura, MD, PhDa,*, Noriaki Nakamichi, MDa, Hiroyasu Ikegami, MD, PhDa, Takeo Nagura, MD, PhDa, Nobuaki Imanishi, MD, PhDb, Sadakazu Aiso, MD, PhDb, Yoshiaki Toyama, MD, PhDa a b
Department of Orthopedic Surgery, School of Medicine, Keio University, Tokyo, Japan Department of Anatomy, School of Medicine, Keio University, Tokyo, Japan Hypothesis: The clavicle serves as a strut between the thorax and scapula, and lack of this function could affect shoulder mobility. We hypothesized that clavicular discontinuity changes shoulder kinematics, particularly affecting scapular motion. Materials and methods: The study used 14 cadaveric shoulders. Cadavers were stabilized in the sitting position. Manual elevation in the sagittal, scapular, and coronal planes was performed in the intact and clavicular discontinuity models. The thorax-scapula distance and 3-dimensional scapular motion during shoulder elevation were recorded using an electromagnetic tracking device. The differences between the 2 experimental models at each position were analyzed. Results: Clavicular discontinuity resulted in a decreased thorax-scapula distance and in reduced external rotation, upward rotation, and posterior tilting of the scapula. The kinematic changes were observed during elevations in all 3 planes but were greatest in the sagittal plane compared with the scapular and coronal planes. Conclusions: The findings of this study revealed that discontinuity of the clavicle affects shoulder kinematics. Because of its anatomic shape and position, the clavicle stabilizes the external, upward, and posterior rotation of the scapula during arm movement. This function of the clavicle may assist glenohumeral joint motion and help prevent subacromial impingement. Level of evidence: Basic Science Study, Biomechanics, Cadaver Model. Ó 2013 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Clavicular nonunion; clavicular function; clavicle fracture; shoulder kinematics; scapular kinematics; shoulder motion; scapular motion; electromagnetic tracking device
Although most conservatively treated midshaft clavicular fractures were traditionally thought to unite,6,14,18 recent clinical evidence suggests that nonunion after No Investigational Review Board approval was required for this in vitro cadaveric study. *Reprint requests: Noboru Matsumura, MD, PhD, Department of Orthopedic Surgery, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. E-mail address: [email protected] (N. Matsumura).
fractures is rather common.5,16,17,23 Unfortunately, nonunion often causes pain and impaired function of the shoulder girdle.7 In addition to stabilizing shoulder motion, the main role of the clavicle is to act as a strut that connects the thorax and scapula.21 Accordingly, disruption of this connection could affect the mobility of the upper extremity. To the best of our knowledge, no prior study has documented the kinematic changes of clavicular discontinuity.
1058-2746/$ - see front matter Ó 2013 Journal of Shoulder and Elbow Surgery Board of Trustees. doi:10.1016/j.jse.2012.02.006
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A number of recent kinematic studies have clarified the 3-dimensional motion of the shoulder girdle, a structure formed by the union of the thorax, clavicle, scapula, and humerus.4,11,12 Scapular motion has been shown to change with various pathologies arising in this girdle.9,10,19 The purpose of this study was to examine scapular kinematics in clavicular discontinuity models using cadaveric shoulders and to clarify the function of the clavicle on scapular motion.
Materials and methods Subjects Experiments were performed on 14 shoulders from 5 male and 2 female whole cadavers (mean age, 86.1 5.5 years; range, 75-91 years) within 3 days of the respective deaths of the individuals. The cadavers were stabilized in the sitting position on a wooden stool with a pair of columns to which three polyester straps were tied at the level of the second cervical and first and fifth lumbar vertebra. Care was taken not to interrupt the motion of the clavicle, scapula, and humerus. The study excluded cadavers with obvious spinal deformity, complete rotator cuff tears, or severe arthritic changes that were confirmed by direct inspection and radiographs after the experiments.
Experimental protocol The 3-dimensional position and orientation of the thorax, scapula, and humerus were tracked using an electromagnetic tracking device (3Space Fastrak, Polhemus, Colchester, VT, USA). This system, which has been widely used in kinematic studies of the shoulder girdle,3,10,12,19 comprises a transmitter and positiondetecting sensors. The tracking device has a root mean square accuracy for position and orientation of 0.08 cm and 0.15 , respectively. The thorax sensor was sewn tightly to the skin at the level of the first thoracic vertebra using nylon strings. The scapula and humerus sensors were directly fixed using plastic screws inserted through small skin incisions to the scapular spine and lateral cortex of the humeral shaft just anterior to the deltoid tuberosity. The transmitter was mounted and fixed on a plastic base, and the sensors were kept within 75 cm of the transmitter during the experiments. The kinematic data from sensors located on the thorax, scapula, and humerus were synchronously recorded at a sampling rate of 120 Hz using MotionMonitor software (Innovate Sports Training, Chicago, IL, USA). Three consecutive elevations were manually performed in each of the sagittal, scapular, and coronal planes, at 90 , 30 , and 0 anterior to the coronal plane of the thorax local coordinate system, respectively. Each plane of elevation was assessed through direct visual feedback using the software. In case the deviation from the plane exceeded our acceptable range of error (15 ), the trial was repeated. During each trial, the forearm was gripped by the extended elbow, with the thumb pointing upwards. Each elevation from the resting position to the end point, where the capsules or ligaments could not be stretched any further, lasted for 5 seconds.
Figure 1 Scapular angular positions with the arm positioned at the side of the body in the intact and clavicular discontinuity groups.
After assessments of the intact state (intact group), a 4-cm section of the clavicular midshaft was removed through a 6-cm skin incision to simulate clavicular discontinuity. All assessments described were repeated under the condition of clavicular discontinuity (discontinuity group). In each experiment, the right shoulder of the specimen was examined first. For the examination of the left shoulder, the original length of the right clavicle was recovered through the use of an external fixator (Orthofix M-100, EBI, Parsippany, NJ, USA). During the restoration of the clavicle with the fixator, 2 pins were inserted into the proximal and distal fragments of the clavicle as marked before the resection. After fixation, we confirmed that the thorax-scapula distance has been recovered to its intact state. The motion of the scapula and humerus tracked by their respective sensors was transformed to the local coordinate system of the thorax. Specifically, we calculated scapulothoracic motion (scapular rotation with respect to the thorax) against humerothoracic motion (humeral rotation with respect to the thorax). The local coordinate systems of the individual segments were constructed after palpating and digitizing anatomic landmarks. Subsequently, the rotations of the distal with respect to the proximal coordinate system were described using the Cardan and Euler angles. The specific bony landmarks, local coordinate systems, and rotation sequences used in this study were derived from the International Society of Biomechanics (ISB) standardization proposal.24
Data analysis The thorax-scapula distance and scapular rotations were assessed at each position. The thorax-scapula distance was defined as the length between the sternal notch and the posterior lateral acromion, the recommended origin of the thorax and the scapula coordinate system, respectively.24 Scapular rotation was defined as 3-dimensional scapulothoracic joint motion at each position and described by scapular external/internal rotation, upward/ downward rotation, and posterior/anterior tilting. The thorax-scapula distance and scapular angular position were first evaluated in the resting position with the arm at the side. Subsequently, the thorax-scapula distance and scapular rotations were computed at each data point during humerothoracic
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Figure 2 Thorax-scapula distance and scapular rotations during sagittal plane humerothoracic elevation. The clavicular discontinuity group is compared with the intact group at each elevated position from 30 to 130 . (A) Thorax-scapula distance. (B) Scapular external rotation. (C) Scapular upward rotation. (D) Scapular posterior tilting. The dashed line represents the intact group, the solid line represents the discontinuity group, and the error bar shows the standard deviation. )P < .05. ))P < .01. )))P < .001.
elevation using specialized software. We interpolated the data into 10 increments of humerothoracic elevation from 30 to 130 , a range achieved by all specimens in all planes of elevation under the intact and discontinuous models. The interpolated values for each shoulder were averaged across the 3 trials at each position and plane of elevation. The average thorax-scapula distance and scapular rotations were also calculated at the peak of maximum humerothoracic elevation angle, regardless of the elevation angle. Statistical analysis was performed using PASW 17.0 software (SPSS Inc, Chicago, IL, USA). Intraclass correlation coefficients (type 1.1) were used to calculate the measurement reliability of the thorax-scapula distance and scapular rotations in the 3 trials of arm elevation. Wilcoxon signed rank tests were used to assess differences between the intact and discontinuity group in the thorax-scapula distance and scapular rotations at the resting position and at all humerothoracic elevated positions between 30 to 130 in all 3 planes. The maximum humerothoracic elevation angles of the 2 groups in 3 planes were also assessed using Wilcoxon signed rank tests. To assess the influence of elevation planes and elevation angles, we calculated the differences of the thorax-scapula distance and scapular rotations at each position between the discontinuity and the intact group. These differences were analyzed with 2-factor repeated-measure
analysis of variance, followed by Tukey post hoc tests, as appropriate. The significance level for all analyses was set at P ¼ .05.
Results The thorax-scapula distance at the resting position was significantly higher in the intact than in the discontinuity group (23.8 1.6 vs 23.2 1.6 cm; P ¼ .013). The scapular angular position at the resting position also changed with clavicular discontinuity (Fig. 1). Specifically, the discontinuity group showed decreased external rotation (3.7 , P ¼ .005), upward rotation (3.9 , P < .001), and posterior tilting (2.0 , P ¼ .019) of the scapula compared with the intact group, showing that the scapula inclined internally, downwardly, and anteriorly with clavicular discontinuity. In the intact group, the average intraclass correlation coefficients for trial-to-trial reliability in the thorax-scapula distance and in the scapular rotations were 0.976 (range, 0.972-0.979) and 0.994 (range, 0.989-0.997), respectively.
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Figure 3 Thorax-scapula distance and scapular rotations during scapular plane humerothoracic elevation. (A) Thorax-scapula distance. (B) Scapular external rotation. (C) Scapular upward rotation. (D) Scapular posterior tilting. The dashed line represents the intact group, the solid line represents the discontinuity group, and the error bar shows the standard deviation. )P < .05. ))P < .01. )))P < .001.
The corresponding values in the discontinuity group were 0.958 (range, 0.941-0.969) and 0.969 (range, 0.906-0.988), respectively. The discontinuity group showed significantly decreased thorax-scapula distance relative to the intact group throughout sagittal plane elevation (P < .001; Fig. 2, A) and at some positions during scapular plane elevation (P < .05; Fig. 3, A), but at no points during coronal plane elevation (Fig. 4, A). The distance difference between the 2 groups was significantly greater in the sagittal vs the scapular and coronal planes (P < .001 for both), whereas no difference was found between the scapular and coronal plane. The thorax-scapula distance in all planes did not differ according to elevation angle. Rotation patterns of the scapula during arm elevation were similar in the 2 experimental groups (Fig. 2-4, B-D). However, scapular external rotation changed its pattern with the plane of elevation. Specifically, compared with the intact group, the discontinuity group showed significantly decreased external rotation throughout arm elevation with same rotation patterns at all positions in the sagittal plane (P < .004; Fig. 2, B), at positions of 70 in the scapular plane (P < .05; Fig. 3, B), and at the positions of 70 and
90 in the coronal plane (P ¼ .041 for both; Fig. 4, B). The scapula consistently rotated upwardly and posteriorly irrespective of the elevation planes in both experimental groups. In the discontinuity group, scapular upward rotation significantly decreased at a humerothoracic elevation of 110 in the sagittal plane (P < .02; Fig. 2, C) and 80 in the scapular plane (P < .05; Fig. 3, C), respectively, but recovered to the level of the intact group in the late phase. This rotation ultimately showed larger values at the highly elevated positions and gave rise to the significantly larger maximum humerothoracic elevation angle in the discontinuity group than in the intact group (4.3 , P ¼ .022 in the sagittal plane; 6.6 , P ¼ .003 in the scapular plane; 8.4 , P ¼ .004 in the coronal plane). Scapular posterior tilting was also decreased at most of positions in the sagittal plane (P < .02; Fig. 2, D) and in some positions in the scapular plane (P < .05; Fig. 3, D) but in no positions in the coronal plane (Fig. 4, D). The differences between the groups in all 3 scapular rotations were significantly greater in the sagittal plane compared with those in the scapular and coronal planes (P < .001 for both), but not significantly different between the scapular and coronal plane in all rotations. Although the differences
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Figure 4 Thorax-scapula distance and scapular rotations during coronal plane humerothoracic elevation. (A) Thorax-scapula distance. (B) Scapular external rotation. (C) Scapular upward rotation. (D) Scapular posterior tilting. The dashed line represents the intact group, the solid line represents the discontinuity group, and the error bar shows the standard deviation. )P < .05. ))P < .01. )))P < .001.
in scapular external rotation and posterior tilting were not influenced by elevation angles, the differences between the groups in scapular upward rotation were significantly smaller at humerothoracic elevations of 120 and 130 compared with those <80 (P < .03).
Discussion The many roles of the clavicle include acting as a strut to hold the scapula away from the body, serving as a bony anchor for the origin and insertion of muscles, providing protection for large underlying blood vessels and nerves, and transmitting the supporting force to the scapula.1 In this study, we highlighted the strut function of the clavicle in maintaining the thorax-scapula distance in the resting position and during arm movement. Our findings also demonstrated that the clavicle assists with the external, upward, and posterior rotation of the scapula. The role of scapular rotation remains unclear but is speculated to lessen the requirement for glenohumeral elevation and external rotation12 and to elevate the lateral
and anterior acromion.10 Upward scapular rotation elevates the lateral acromion, whereas its posterior tilting elevates the anterior acromion; thus, by influencing scapular motion, the clavicle may assist the motion of the glenohumeral joint and decrease subacromial pressure. The clavicle connects to the sternum at its proximal end through the sternoclavicular joint. Leading externally, upwardly, and posteriorly, the clavicle connects to the acromion at its distal end through the acromioclavicular joint. Accordingly, the acromion will be guided externally, upwardly, and posteriorly. In return, these acromion movements could assist in the external, upward, and posterior rotation of the scapula. Shoulder dyskinesis appears to affect the surrounding muscles and the entire kinematic chain from the trunk to the upper extremity.2,9 This study revealed that clavicular discontinuity changes the shoulder girdle kinematics, resulting in decreased external rotation, upward rotation, and posterior tilting of the scapula. Decreased scapular rotation could increase the motion demand on the glenohumeral joint and augment subacromial pressure, possibly leading to secondary impingement. In contrast to the
338 scapular and coronal planes, differences of the thoraxscapula distance and scapular rotations between the two conditions became significant during elevation in the sagittal plane. Because the humerus rotates externally during arm elevation in the scapular and coronal planes, the resulting distractive force could stabilize shoulder girdle motion and minimize clavicular discontinuity through the glenohumeral joint capsule. In cases of discontinuity between the thorax and scapula, movement in the sagittal plane might be affected more profoundly than movement in the scapular and coronal planes. Using the same cadaveric shoulders with direct attachment of the scapular and humeral sensors, our study eliminated individual variability in shoulder kinematics and also reduced skin motion artifacts.8 Furthermore, because pain of motion20 or joint contracture19 are estimated to affect the shoulder kinematics, this cadaveric study also reduced the error inherent to in vivo studies. Conversely, this study had several limitations, including the completely passive motion of our cadaveric models. However, several studies have reported that scapular kinematics during active and passive motion is rather similar,3,15,22 and the scapular rotation in our intact group showed a similar rotation pattern to those reported in prior in vivo studies.11-13 Nevertheless, because the clavicle acts as a bony anchor of some muscles, the activities of the shoulder girdle muscles might affect the results. The second limitation of this study concerns the plane of elevation. Because complete elimination of error in elevation on a uniform plane is impossible, we controlled movement in each plane to within 15 . The trial-to-trial reliability of the thorax-scapula distance and scapular rotations was excellent throughout elevation, and our elevation trials appeared to be reproducible. However, this error may have caused overlap between the scapular and coronal planes. Another potential limitation of this study was the removal of a 4-cm section of the clavicle to simulate clavicular discontinuity. A preliminary study showed a small excision resulted in very limited movement at the point of clavicular osteotomy, possibly due to the contact between the proximal and distal fragments during elevation. The thorax-scapula distance decreased to 3.5 cm in specimens under the discontinuity condition. Thus, we removed a 4-cm section of the clavicle to simulate discontinuity because this amount appeared to be sufficient. Obviously, the clavicle would not lose such a large piece in a clinical fracture, and fibrous union could be expected regardless of clavicular bony nonunion. Thus, our discontinuity model might not accurately simulate physiologic clavicular nonunion. We could not find a stable bony fixation for the sensor on the thorax. Although we directly tracked the scapular and humeral motion, the thorax sensor was sewn to the skin, which might have resulted in a small skin motion artifact. Finally, it remains unclear whether the statistical
N. Matsumura et al. significance in this cadaveric study can be translated to clinically significant symptoms.
Conclusion The present study is the first to describe the kinematic changes associated with clavicular discontinuity in the shoulder girdle. The findings of this study indicate that clavicular discontinuity causes shoulder dyskinesis, which could lead to clinical symptoms. We conclude that the clavicle functions to assist with the external, upward, and posterior rotation of the scapula during arm movement.
Disclaimer The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
References 1. Abbott LC, Lucas DB. The function of the clavicle; its surgical significance. Ann Surg 1954;140:583-99. 2. Burkhart SS, Morgan CD, Kibler WB. The disabled throwing shoulder: spectrum of pathology part III: The SICK scapula, scapular dyskinesis, the kinetic chain, and rehabilitation. Arthroscopy 2003;19: 641-61. doi:10.1016/S0749-8063(03)00389-X 3. Ebaugh DD, McClure PW, Karduna AR. Three-dimensional scapulothoracic motion during active and passive arm elevation. Clin Biomech (Bristol, Avon) 2005;20:700-9. doi:10.1016/j.clinbiomech. 2005.03.008 4. Fung M, Kato S, Barrance PJ, Elias JJ, McFarland EG, Nobuhara K, et al. Scapular and clavicular kinematics during humeral elevation: a study with cadavers. J Shoulder Elbow Surg 2001;10:278-85. 5. Hill JM, McGuire MH, Crosby LA. Closed treatment of displaced middle-third fractures of the clavicle gives poor results. J Bone Joint Surg Br 1997;79:537-9. 6. Johnson EW Jr, Collins HR. Nonunion of the Clavicle. Arch Surg 1963;87:963-6. 7. Jupiter JB, Leffert RD. Non-union of the clavicle. Associated complications and surgical management. J Bone Joint Surg Am 1987; 69:753-60. 8. Karduna AR, McClure PW, Michener LA, Sennett B. Dynamic measurements of three-dimensional scapular kinematics: a validation study. J Biomech Eng 2001;123:184-90. 9. Kibler WB, McMullen J. Scapular dyskinesis and its relation to shoulder pain. J Am Acad Orthop Surg 2003;11:142-51. 10. Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther 2000;80:276-91. 11. Ludewig PM, Phadke V, Braman JP, Hassett DR, Cieminski CJ, LaPrade RF. Motion of the shoulder complex during multiplanar humeral elevation. J Bone Joint Surg Am 2009;91:378-89. doi:10. 2106/JBJS.G.01483
Clavicular function on scapular motion 12. McClure PW, Michener LA, Sennett BJ, Karduna AR. Direct 3-dimensional measurement of scapular kinematics during dynamic movements in vivo. J Shoulder Elbow Surg 2001;10: 269-77. 13. Meskers CG, Vermeulen HM, de Groot JH, van Der Helm FC, Rozing PM. 3D shoulder position measurements using a six-degreeof-freedom electromagnetic tracking device. Clin Biomech (Bristol, Avon) 1998;13:280-92. 14. Neer CS 2nd. Nonunion of the clavicle. JAMA 1960;172:1006-11. 15. Price CI, Franklin P, Rodgers H, Curless RH, Johnson GR. Active and passive scapulohumeral movement in healthy persons: a comparison. Arch Phys Med Rehabil 2000;81:28-31. 16. Robinson CM. Fractures of the clavicle in the adult. Epidemiology and classification. J Bone Joint Surg Br 1998;80:476-84. 17. Robinson CM, Court-Brown CM, McQueen MM, Wakefield AE. Estimating the risk of nonunion following nonoperative treatment of a clavicular fracture. J Bone Joint Surg Am 2004;86:1359-65. 18. Rowe CR. An atlas of anatomy and treatment of midclavicular fractures. Clin Orthop Relat Res 1968;58:29-42. 19. Rundquist PJ, Anderson DD, Guanche CA, Ludewig PM. Shoulder kinematics in subjects with frozen shoulder. Arch
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Phys Med Rehabil 2003;84:1473-9. doi:10.1053/S0003-9993(03) 00359-9 Scibek JS, Mell AG, Downie BK, Carpenter JE, Hughes RE. Shoulder kinematics in patients with full-thickness rotator cuff tears after a subacromial injection. J Shoulder Elbow Surg 2008;17:172-81. doi: 10.1016/j.jse.2007.05.010 Simpson NS, Jupiter JB. Clavicular nonunion and malunion: evaluation and surgical management. J Am Acad Orthop Surg 1996;4:1-8. Teece RM, Lunden JB, Lloyd AS, Kaiser AP, Cieminski CJ, Ludewig PM. Three-dimensional acromioclavicular joint motions during elevation of the arm. J Orthop Sports Phys Ther 2008;38:181-90. doi:10.2519/jospt.2008.2386 The Canadian Orthopaedic Trauma Society. Nonoperative treatment compared with plate fixation of displaced midshaft clavicular fractures. A multicenter, randomized clinical trial. J Bone Joint Surg Am 2007;89:1-10. doi:10.2106/JBJS.F.00020 Wu G, van der Helm FC, Veeger HEJ, Makhsous M, Van Roy P, Anglin C, et al. ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motion–Part II: shoulder, elbow, wrist and hand. J Biomech 2005;38:981-92. doi: 10.1016/j.jbiomech.2004.05.042
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The function of the clavicle on scapular motion: a cadaveric study Noboru Matsumura, MD, PhDa,*, Noriaki Nakamichi, MDa, Hiroyasu Ikegami, MD, PhDa, Takeo Nagura, MD, PhDa, Nobuaki Imanishi, MD, PhDb, Sadakazu Aiso, MD, PhDb, Yoshiaki Toyama, MD, PhDa a b
Department of Orthopedic Surgery, School of Medicine, Keio University, Tokyo, Japan Department of Anatomy, School of Medicine, Keio University, Tokyo, Japan Hypothesis: The clavicle serves as a strut between the thorax and scapula, and lack of this function could affect shoulder mobility. We hypothesized that clavicular discontinuity changes shoulder kinematics, particularly affecting scapular motion. Materials and methods: The study used 14 cadaveric shoulders. Cadavers were stabilized in the sitting position. Manual elevation in the sagittal, scapular, and coronal planes was performed in the intact and clavicular discontinuity models. The thorax-scapula distance and 3-dimensional scapular motion during shoulder elevation were recorded using an electromagnetic tracking device. The differences between the 2 experimental models at each position were analyzed. Results: Clavicular discontinuity resulted in a decreased thorax-scapula distance and in reduced external rotation, upward rotation, and posterior tilting of the scapula. The kinematic changes were observed during elevations in all 3 planes but were greatest in the sagittal plane compared with the scapular and coronal planes. Conclusions: The findings of this study revealed that discontinuity of the clavicle affects shoulder kinematics. Because of its anatomic shape and position, the clavicle stabilizes the external, upward, and posterior rotation of the scapula during arm movement. This function of the clavicle may assist glenohumeral joint motion and help prevent subacromial impingement. Level of evidence: Basic Science Study, Biomechanics, Cadaver Model. Ó 2013 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Clavicular nonunion; clavicular function; clavicle fracture; shoulder kinematics; scapular kinematics; shoulder motion; scapular motion; electromagnetic tracking device
Although most conservatively treated midshaft clavicular fractures were traditionally thought to unite,6,14,18 recent clinical evidence suggests that nonunion after No Investigational Review Board approval was required for this in vitro cadaveric study. *Reprint requests: Noboru Matsumura, MD, PhD, Department of Orthopedic Surgery, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan. E-mail address: [email protected] (N. Matsumura).
fractures is rather common.5,16,17,23 Unfortunately, nonunion often causes pain and impaired function of the shoulder girdle.7 In addition to stabilizing shoulder motion, the main role of the clavicle is to act as a strut that connects the thorax and scapula.21 Accordingly, disruption of this connection could affect the mobility of the upper extremity. To the best of our knowledge, no prior study has documented the kinematic changes of clavicular discontinuity.
1058-2746/$ - see front matter Ó 2013 Journal of Shoulder and Elbow Surgery Board of Trustees. doi:10.1016/j.jse.2012.02.006
334
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A number of recent kinematic studies have clarified the 3-dimensional motion of the shoulder girdle, a structure formed by the union of the thorax, clavicle, scapula, and humerus.4,11,12 Scapular motion has been shown to change with various pathologies arising in this girdle.9,10,19 The purpose of this study was to examine scapular kinematics in clavicular discontinuity models using cadaveric shoulders and to clarify the function of the clavicle on scapular motion.
Materials and methods Subjects Experiments were performed on 14 shoulders from 5 male and 2 female whole cadavers (mean age, 86.1 5.5 years; range, 75-91 years) within 3 days of the respective deaths of the individuals. The cadavers were stabilized in the sitting position on a wooden stool with a pair of columns to which three polyester straps were tied at the level of the second cervical and first and fifth lumbar vertebra. Care was taken not to interrupt the motion of the clavicle, scapula, and humerus. The study excluded cadavers with obvious spinal deformity, complete rotator cuff tears, or severe arthritic changes that were confirmed by direct inspection and radiographs after the experiments.
Experimental protocol The 3-dimensional position and orientation of the thorax, scapula, and humerus were tracked using an electromagnetic tracking device (3Space Fastrak, Polhemus, Colchester, VT, USA). This system, which has been widely used in kinematic studies of the shoulder girdle,3,10,12,19 comprises a transmitter and positiondetecting sensors. The tracking device has a root mean square accuracy for position and orientation of 0.08 cm and 0.15 , respectively. The thorax sensor was sewn tightly to the skin at the level of the first thoracic vertebra using nylon strings. The scapula and humerus sensors were directly fixed using plastic screws inserted through small skin incisions to the scapular spine and lateral cortex of the humeral shaft just anterior to the deltoid tuberosity. The transmitter was mounted and fixed on a plastic base, and the sensors were kept within 75 cm of the transmitter during the experiments. The kinematic data from sensors located on the thorax, scapula, and humerus were synchronously recorded at a sampling rate of 120 Hz using MotionMonitor software (Innovate Sports Training, Chicago, IL, USA). Three consecutive elevations were manually performed in each of the sagittal, scapular, and coronal planes, at 90 , 30 , and 0 anterior to the coronal plane of the thorax local coordinate system, respectively. Each plane of elevation was assessed through direct visual feedback using the software. In case the deviation from the plane exceeded our acceptable range of error (15 ), the trial was repeated. During each trial, the forearm was gripped by the extended elbow, with the thumb pointing upwards. Each elevation from the resting position to the end point, where the capsules or ligaments could not be stretched any further, lasted for 5 seconds.
Figure 1 Scapular angular positions with the arm positioned at the side of the body in the intact and clavicular discontinuity groups.
After assessments of the intact state (intact group), a 4-cm section of the clavicular midshaft was removed through a 6-cm skin incision to simulate clavicular discontinuity. All assessments described were repeated under the condition of clavicular discontinuity (discontinuity group). In each experiment, the right shoulder of the specimen was examined first. For the examination of the left shoulder, the original length of the right clavicle was recovered through the use of an external fixator (Orthofix M-100, EBI, Parsippany, NJ, USA). During the restoration of the clavicle with the fixator, 2 pins were inserted into the proximal and distal fragments of the clavicle as marked before the resection. After fixation, we confirmed that the thorax-scapula distance has been recovered to its intact state. The motion of the scapula and humerus tracked by their respective sensors was transformed to the local coordinate system of the thorax. Specifically, we calculated scapulothoracic motion (scapular rotation with respect to the thorax) against humerothoracic motion (humeral rotation with respect to the thorax). The local coordinate systems of the individual segments were constructed after palpating and digitizing anatomic landmarks. Subsequently, the rotations of the distal with respect to the proximal coordinate system were described using the Cardan and Euler angles. The specific bony landmarks, local coordinate systems, and rotation sequences used in this study were derived from the International Society of Biomechanics (ISB) standardization proposal.24
Data analysis The thorax-scapula distance and scapular rotations were assessed at each position. The thorax-scapula distance was defined as the length between the sternal notch and the posterior lateral acromion, the recommended origin of the thorax and the scapula coordinate system, respectively.24 Scapular rotation was defined as 3-dimensional scapulothoracic joint motion at each position and described by scapular external/internal rotation, upward/ downward rotation, and posterior/anterior tilting. The thorax-scapula distance and scapular angular position were first evaluated in the resting position with the arm at the side. Subsequently, the thorax-scapula distance and scapular rotations were computed at each data point during humerothoracic
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Figure 2 Thorax-scapula distance and scapular rotations during sagittal plane humerothoracic elevation. The clavicular discontinuity group is compared with the intact group at each elevated position from 30 to 130 . (A) Thorax-scapula distance. (B) Scapular external rotation. (C) Scapular upward rotation. (D) Scapular posterior tilting. The dashed line represents the intact group, the solid line represents the discontinuity group, and the error bar shows the standard deviation. )P < .05. ))P < .01. )))P < .001.
elevation using specialized software. We interpolated the data into 10 increments of humerothoracic elevation from 30 to 130 , a range achieved by all specimens in all planes of elevation under the intact and discontinuous models. The interpolated values for each shoulder were averaged across the 3 trials at each position and plane of elevation. The average thorax-scapula distance and scapular rotations were also calculated at the peak of maximum humerothoracic elevation angle, regardless of the elevation angle. Statistical analysis was performed using PASW 17.0 software (SPSS Inc, Chicago, IL, USA). Intraclass correlation coefficients (type 1.1) were used to calculate the measurement reliability of the thorax-scapula distance and scapular rotations in the 3 trials of arm elevation. Wilcoxon signed rank tests were used to assess differences between the intact and discontinuity group in the thorax-scapula distance and scapular rotations at the resting position and at all humerothoracic elevated positions between 30 to 130 in all 3 planes. The maximum humerothoracic elevation angles of the 2 groups in 3 planes were also assessed using Wilcoxon signed rank tests. To assess the influence of elevation planes and elevation angles, we calculated the differences of the thorax-scapula distance and scapular rotations at each position between the discontinuity and the intact group. These differences were analyzed with 2-factor repeated-measure
analysis of variance, followed by Tukey post hoc tests, as appropriate. The significance level for all analyses was set at P ¼ .05.
Results The thorax-scapula distance at the resting position was significantly higher in the intact than in the discontinuity group (23.8 1.6 vs 23.2 1.6 cm; P ¼ .013). The scapular angular position at the resting position also changed with clavicular discontinuity (Fig. 1). Specifically, the discontinuity group showed decreased external rotation (3.7 , P ¼ .005), upward rotation (3.9 , P < .001), and posterior tilting (2.0 , P ¼ .019) of the scapula compared with the intact group, showing that the scapula inclined internally, downwardly, and anteriorly with clavicular discontinuity. In the intact group, the average intraclass correlation coefficients for trial-to-trial reliability in the thorax-scapula distance and in the scapular rotations were 0.976 (range, 0.972-0.979) and 0.994 (range, 0.989-0.997), respectively.
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Figure 3 Thorax-scapula distance and scapular rotations during scapular plane humerothoracic elevation. (A) Thorax-scapula distance. (B) Scapular external rotation. (C) Scapular upward rotation. (D) Scapular posterior tilting. The dashed line represents the intact group, the solid line represents the discontinuity group, and the error bar shows the standard deviation. )P < .05. ))P < .01. )))P < .001.
The corresponding values in the discontinuity group were 0.958 (range, 0.941-0.969) and 0.969 (range, 0.906-0.988), respectively. The discontinuity group showed significantly decreased thorax-scapula distance relative to the intact group throughout sagittal plane elevation (P < .001; Fig. 2, A) and at some positions during scapular plane elevation (P < .05; Fig. 3, A), but at no points during coronal plane elevation (Fig. 4, A). The distance difference between the 2 groups was significantly greater in the sagittal vs the scapular and coronal planes (P < .001 for both), whereas no difference was found between the scapular and coronal plane. The thorax-scapula distance in all planes did not differ according to elevation angle. Rotation patterns of the scapula during arm elevation were similar in the 2 experimental groups (Fig. 2-4, B-D). However, scapular external rotation changed its pattern with the plane of elevation. Specifically, compared with the intact group, the discontinuity group showed significantly decreased external rotation throughout arm elevation with same rotation patterns at all positions in the sagittal plane (P < .004; Fig. 2, B), at positions of 70 in the scapular plane (P < .05; Fig. 3, B), and at the positions of 70 and
90 in the coronal plane (P ¼ .041 for both; Fig. 4, B). The scapula consistently rotated upwardly and posteriorly irrespective of the elevation planes in both experimental groups. In the discontinuity group, scapular upward rotation significantly decreased at a humerothoracic elevation of 110 in the sagittal plane (P < .02; Fig. 2, C) and 80 in the scapular plane (P < .05; Fig. 3, C), respectively, but recovered to the level of the intact group in the late phase. This rotation ultimately showed larger values at the highly elevated positions and gave rise to the significantly larger maximum humerothoracic elevation angle in the discontinuity group than in the intact group (4.3 , P ¼ .022 in the sagittal plane; 6.6 , P ¼ .003 in the scapular plane; 8.4 , P ¼ .004 in the coronal plane). Scapular posterior tilting was also decreased at most of positions in the sagittal plane (P < .02; Fig. 2, D) and in some positions in the scapular plane (P < .05; Fig. 3, D) but in no positions in the coronal plane (Fig. 4, D). The differences between the groups in all 3 scapular rotations were significantly greater in the sagittal plane compared with those in the scapular and coronal planes (P < .001 for both), but not significantly different between the scapular and coronal plane in all rotations. Although the differences
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Figure 4 Thorax-scapula distance and scapular rotations during coronal plane humerothoracic elevation. (A) Thorax-scapula distance. (B) Scapular external rotation. (C) Scapular upward rotation. (D) Scapular posterior tilting. The dashed line represents the intact group, the solid line represents the discontinuity group, and the error bar shows the standard deviation. )P < .05. ))P < .01. )))P < .001.
in scapular external rotation and posterior tilting were not influenced by elevation angles, the differences between the groups in scapular upward rotation were significantly smaller at humerothoracic elevations of 120 and 130 compared with those <80 (P < .03).
Discussion The many roles of the clavicle include acting as a strut to hold the scapula away from the body, serving as a bony anchor for the origin and insertion of muscles, providing protection for large underlying blood vessels and nerves, and transmitting the supporting force to the scapula.1 In this study, we highlighted the strut function of the clavicle in maintaining the thorax-scapula distance in the resting position and during arm movement. Our findings also demonstrated that the clavicle assists with the external, upward, and posterior rotation of the scapula. The role of scapular rotation remains unclear but is speculated to lessen the requirement for glenohumeral elevation and external rotation12 and to elevate the lateral
and anterior acromion.10 Upward scapular rotation elevates the lateral acromion, whereas its posterior tilting elevates the anterior acromion; thus, by influencing scapular motion, the clavicle may assist the motion of the glenohumeral joint and decrease subacromial pressure. The clavicle connects to the sternum at its proximal end through the sternoclavicular joint. Leading externally, upwardly, and posteriorly, the clavicle connects to the acromion at its distal end through the acromioclavicular joint. Accordingly, the acromion will be guided externally, upwardly, and posteriorly. In return, these acromion movements could assist in the external, upward, and posterior rotation of the scapula. Shoulder dyskinesis appears to affect the surrounding muscles and the entire kinematic chain from the trunk to the upper extremity.2,9 This study revealed that clavicular discontinuity changes the shoulder girdle kinematics, resulting in decreased external rotation, upward rotation, and posterior tilting of the scapula. Decreased scapular rotation could increase the motion demand on the glenohumeral joint and augment subacromial pressure, possibly leading to secondary impingement. In contrast to the
338 scapular and coronal planes, differences of the thoraxscapula distance and scapular rotations between the two conditions became significant during elevation in the sagittal plane. Because the humerus rotates externally during arm elevation in the scapular and coronal planes, the resulting distractive force could stabilize shoulder girdle motion and minimize clavicular discontinuity through the glenohumeral joint capsule. In cases of discontinuity between the thorax and scapula, movement in the sagittal plane might be affected more profoundly than movement in the scapular and coronal planes. Using the same cadaveric shoulders with direct attachment of the scapular and humeral sensors, our study eliminated individual variability in shoulder kinematics and also reduced skin motion artifacts.8 Furthermore, because pain of motion20 or joint contracture19 are estimated to affect the shoulder kinematics, this cadaveric study also reduced the error inherent to in vivo studies. Conversely, this study had several limitations, including the completely passive motion of our cadaveric models. However, several studies have reported that scapular kinematics during active and passive motion is rather similar,3,15,22 and the scapular rotation in our intact group showed a similar rotation pattern to those reported in prior in vivo studies.11-13 Nevertheless, because the clavicle acts as a bony anchor of some muscles, the activities of the shoulder girdle muscles might affect the results. The second limitation of this study concerns the plane of elevation. Because complete elimination of error in elevation on a uniform plane is impossible, we controlled movement in each plane to within 15 . The trial-to-trial reliability of the thorax-scapula distance and scapular rotations was excellent throughout elevation, and our elevation trials appeared to be reproducible. However, this error may have caused overlap between the scapular and coronal planes. Another potential limitation of this study was the removal of a 4-cm section of the clavicle to simulate clavicular discontinuity. A preliminary study showed a small excision resulted in very limited movement at the point of clavicular osteotomy, possibly due to the contact between the proximal and distal fragments during elevation. The thorax-scapula distance decreased to 3.5 cm in specimens under the discontinuity condition. Thus, we removed a 4-cm section of the clavicle to simulate discontinuity because this amount appeared to be sufficient. Obviously, the clavicle would not lose such a large piece in a clinical fracture, and fibrous union could be expected regardless of clavicular bony nonunion. Thus, our discontinuity model might not accurately simulate physiologic clavicular nonunion. We could not find a stable bony fixation for the sensor on the thorax. Although we directly tracked the scapular and humeral motion, the thorax sensor was sewn to the skin, which might have resulted in a small skin motion artifact. Finally, it remains unclear whether the statistical
N. Matsumura et al. significance in this cadaveric study can be translated to clinically significant symptoms.
Conclusion The present study is the first to describe the kinematic changes associated with clavicular discontinuity in the shoulder girdle. The findings of this study indicate that clavicular discontinuity causes shoulder dyskinesis, which could lead to clinical symptoms. We conclude that the clavicle functions to assist with the external, upward, and posterior rotation of the scapula during arm movement.
Disclaimer The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.
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