- Email: [email protected]
Comparison of three stretches for the pectoralis minor muscle
Comparison of three stretches for the pectoralis minor muscle John D. Borstad, PhD, PT,a and Paula M. Ludewig, PhD, PT,b Columbus, OH, and Minneapolis, MN
Pectoralis minor adaptive shortening in healthy individuals is associated with altered scapular kinematics similar to the alterations demonstrated in individuals with subacromial impingement. This associative relationship suggests that stretching of the pectoralis minor may improve scapular kinematics and assist in the management of shoulder impingement. Several stretches for the pectoralis minor are used clinically, although it is not known which stretch optimally lengthens the muscle. The purpose of this analysis was to compare the mean length change for 3 pectoralis minor stretches. Fifty subjects without shoulder pathology were examined for the change in length of the pectoralis minor during 3 separate stretches by use of an electromagnetic motion-capture system. The stretches analyzed were a unilateral self-stretch, a supine manual stretch, and a sitting manual stretch. Each stretch was significantly different from the other two (df, 2/98; F ratio, 39.09; P ⬍ .00001), with the unilateral self-stretch demonstrating the greatest length change (2.24 cm), followed by the supine manual stretch (1.69 cm) and the sitting manual stretch (0.77 cm). Knowledge of the most effective method of elongating the pectoralis minor muscle may improve clinical decision making when targeting this anterior scapulothoracic muscle as part of intervention for or prevention of shoulder impingement. (J Shoulder Elbow Surg 2006;15: 324-330.)
M any authors have described skeletal muscle adap-
tations such as muscle length changes and strength imbalances.11,20,23 Postural faults,11,20,22 chronic use of a muscle at a specific length or joint angle,9 and higher activation of muscles on one side of a joint From the aPhysical Therapy Division, School of Allied Medical Professions, The Ohio State University, Columbus, and bProgram in Physical Therapy, Department of Physical Medicine and Rehabilitation, University of Minnesota, Minneapolis. Reprint requests: John D. Borstad, PhD, PT, Division of Physical Therapy, The Ohio State University, 1583 Perry St, Columbus, OH 43210-1234 (E-mail: [email protected]). Copyright © 2006 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2006/$32.00 doi:10.1016/j.jse.2005.08.011
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compared with the antagonist muscles23 are all proposed mechanisms of skeletal muscle adaptation. At the shoulder complex, prolonged exposure to postures of increased scapular protraction and anterior tipping is proposed to result in a shortening or tightness of the pectoralis minor muscle.11,20 Repetitive use of the upper extremities in positions that protract and downwardly rotate the scapulae may also result in pectoralis minor adaptive shortening.14,15 Manual stretching of the pectoralis minor is, therefore, often performed as an intervention when posture deviates from neutral or for shoulder impingement.11,20 Home exercise programs have also included a self-stretch for the pectoralis minor.13,17,22 The pectoralis minor attaches at the coracoid process of the scapula and at the third, fourth, and fifth ribs near their sternocostal junctions. This muscle elongates during arm elevation, allowing the scapula to upwardly rotate, externally rotate, and tip posteriorly18 (Figure 1). A relatively short pectoralis minor muscle, as a result of adaptation, would demonstrate less total excursion than a relatively longer muscle,24,25 limiting full scapular motion. Limitation of scapular motion during arm elevation is believed to decrease the available subacromial space and contribute to shoulder pathology.8,14,15,18,19,22 A decrease in the subacromial space combined with exposure to overhead use has demonstrated rotator cuff changes similar to those seen in individuals with impingement.21 Individuals with symptoms of shoulder impingement, including workers exposed to overhead work, have exhibited these scapular motion limitations in several controlled studies.8,14,15 It is possible that one important mechanistic connection between limitations in scapular motion, particularly tipping, and shoulder symptoms is a decreased resting length of the pectoralis minor. A decreased resting length of the pectoralis minor could be either a causative factor for scapular kinematic alterations or a result of altered scapular position or motion. The end result of either of these possibilities is the need to stretch the muscle in an attempt to increase its excursion and help restore normal scapular kinematics during arm elevation. The purpose of this study was to compare 3 stretches to determine the most effective method for stretching the pectoralis minor muscle. This information will be valuable to clinicians wishing to include a
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Figure 1 Three-dimensional scapular rotations. Upward rotation and downward rotation occur about an axis perpendicular to the plane of the scapula. Anterior tipping and posterior tipping occur about a medial-lateral axis. Internal rotation and external rotation occur about a vertical axis.
pectoralis minor stretch for their patients. We hypothesized that manual stretches would be more effective than would a self-stretch because more precise separation of the muscle’s origin and insertion could be obtained through direct contact by a therapist on the coracoid process and through improved stabilization of the thorax, as compared with the more general anterior shoulder stretch performed by the patient. MATERIALS AND METHODS Subjects Fifty healthy individuals without current shoulder pain or a history of shoulder trauma were recruited for this analysis. Subjects were required to be aged between 20 and 40 years (mean, 27.5 years) to ensure full skeletal growth while avoiding the developing joint degenerative changes that are common in individuals aged over 60 years.5 An attempt to avoid including subjects with joint degenerative changes was made to minimize the potential effect of this variable on normal joint motion. Volunteers were recruited by personal contact, advertising on campus (University of Minnesota, Minneapolis, MN), and addressing graduate classes in physical therapy and kinesiology. All subjects were required to sign both a University of Minnesota– approved informed consent form and a Health Insurance Portability and Accountability Act form before entering the study. A clinical examination was performed on each subject to ensure that no underlying pathology was present in the tested shoulder. The examination included range of motion; the impingement tests of Hawkins, Neer, and Jobe; the apprehension test for determining anterior instability; and the sulcus sign to test laxity.16
Instrumentation The Flock-of-Birds electromagnetic motion-capture system (Ascension Technology Corp, Burlington, VT) was used for measuring pectoralis minor length and analyzing stretches in this study. To determine pectoralis minor
length and length change, 3 mini-bird sensors were used for each subject. A scapular sensor was fixed to the subject’s skin over the broad, flat area of the acromion, and a sternal sensor was fixed to the skin just distal to the sternal notch with double-sided adhesive tape. A third sensor was attached to a thermoplastic cuff and secured over the subject’s distal humerus with Velcro straps. The source transmitter of the system was located at acromion height behind the subject. A digitization sequence established local anatomically based axis systems for each segment (Figure 2). In addition, the coracoid process and the fourth rib/sternum junction were digitized to represent the length of the pectoralis minor. This length measurement was validated in vitro with an Intraclass Correlation Coefficient (ICC) of 0.96 comparing the surface palpation and digitization of the previously mentioned landmarks with digitization of the same landmarks after dissection to visualize the actual origin and insertion of the muscle.7 Reliability and validity of electromagnetic tracking systems in capturing 3-dimensional movements have been demonstrated.1,4,10 Data were collected at 100 Hz per sensor, and all post-processing was performed by use of MotionMonitor software (Innovative Sports Training, Chicago, IL) integrated with the Flock-ofBirds system. To determine the length of the pectoralis minor, the digitized point representing the muscles’ origin and insertion was mathematically converted to be in the reference frame of one of the local sensors. The coracoid process point was calculated to be in the reference frame of the scapular sensor, and the fourth rib point was calculated in the reference frame of the trunk sensor. The 3-dimensional vector from each pectoralis minor landmark to its respective sensor was then calculated. Given the assumption that the scapula and trunk are rigid bodies, these landmark-to-sensor vectors remain constant. The position and orientation of both sensors are also calculated relative to the transmitter reference frame. Finally, with these variables known, the 3-dimensional
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Figure 2 Local orthogonal axis systems for scapula, humerus, and trunk. Dotted lines on the humeral figure represent the thermoplastic cuff used for sensor placement and digitization. Origins are the acromioclavicular joint for the scapula, medial epicondyle for the humerus, and sternal notch for the trunk.
Figure 3 Unilateral corner stretch. The subject’s forearm is stabilized by a vertical plane before the trunk is rotated in the opposite direction.
Figure 4 Sitting manual stretch. The investigator’s hypothenar eminence is used to apply force to the scapula through the coracoid process.
vector lengths between the 2 digitized points were calculated in the varying stretch positions.7
on a flat planar surface. The subject then rotated the trunk away from the elevated arm, increasing the horizontal abduction at the shoulder and maximizing the stretch across the chest (Figure 3). The subject held this position for 3 seconds. The second and third stretches were both performed after lowering the transmitter to keep the sensors within the magnetic field. The second stretch was performed manually by the examiner with the subject sitting in a plastic chair without resting against the back of the chair and the arm in the dependent position. The subject was instructed to inhale deeply and hold his or her breath while the muscle was fully elongated by the examiner. To stretch the muscle, the examiner applied a posterior force to the coracoid process with one hand while stabilizing the inferior angle of the scapula with the other hand (Figure 4).
Procedures To determine the pectoralis minor resting length reference value for each subject, data were collected for 1 second in the normal, relaxed standing position. The pectoralis minor resting length was defined as the mean vector length calculated over this 1-second file. The stretched pectoralis minor vector length was subsequently determined by data collected during each of the 3 stretches. The first stretch was a self-stretch done in the standing position and required the subject to abduct the humerus to 90° with the elbow flexed to 90° and place the palm
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Table I Mean length change for pectoralis minor by stretch type Stretch type
Mean (SE) (cm)
Corner Sitting manual Supine manual
2.24 (0.10) 0.77 (0.11) 1.70 (0.19)
minor landmarks after skin motion would have occurred as a result of the combined effect of arm elevation and the stretch position.
RESULTS
Figure 5 Supine manual stretch. The investigator holds the ipsilateral shoulder in 90° abduction and elbow in 90° flexion before applying force to the scapula through the coracoid process with the hypothenar eminence. The subject is lying with a towel roll between the thoracic spine and the treatment table.
After positioning the muscle in the stretch position, the subject was instructed to exhale.12 The examiner held this stretch position for 3 seconds. The third stretch was performed manually by the examiner with the subject lying in a supine position on a treatment plinth with a towel roll running the length of the thoracic spine. The examiner positioned the subject’s shoulder at 90° of abduction and external rotation and the elbow at 90° flexion while applying a posterior force to the coracoid process, again holding the stretch position for 3 seconds (Figure 5). The resting length value for each subject was subtracted from each stretch length value to arrive at a length change for each stretch position. This resulted in change values for each stretch relative to an individual subject’s pectoralis minor resting length. A 1-way repeated-measures analysis of variance with stretch type as the repeated factor was used to examine potential differences between stretches. The dependent variable was the length change score for each stretch type. Statistically significant main effects of stretch type were further explored with a post hoc Tukey-Kramer multiple comparisons test. A limitation of the Flock-of-Birds system is that the accuracy and validity of the values may be compromised by motion between the skin-mounted sensor and the underlying bone with positioning into extreme ranges of motion.10 This is more likely to be a problem with the arm at 90° because larger errors are created as arm elevation progresses to angles above 120° humeral elevation.10 This potential effect was examined by digitizing 1 subject according to the protocol, recording a corner self-stretch, and then digitizing this same subject a second time as he held the corner stretch position. The pectoralis minor origin and insertion landmarks were also directly palpated and re-digitized after the subject was in the stretch position. This second digitization calculated the distance between the pectoralis
A summary of the amount of change from resting length for each stretch type is presented in Table I. There was a statistically significant main effect of stretch type (df, 2/98; F ratio, 39.09; P ⬍ .00001) (Table II). The Tukey-Kramer multiple comparisons test indicated that each stretch type was significantly different from each of the other two stretch types (Table III). The corner stretch demonstrated the greatest change (2.24 cm), followed by the supine manual stretch (1.69 cm) and the sitting manual stretch (0.77 cm) (Figure 6). For the single-subject skin-slip assessment, the value for the pectoralis minor length was 17.35 cm during the original condition and 17.50 cm in the re-digitized validation condition, an offset of 0.15 cm. This offset value is similar to the SEM for the change in pectoralis minor length during all stretches (Table I). In addition, the pectoralis minor was estimated to be longer in the re-digitized condition, an indication that the length used for the stretch comparisons was likely to be underestimated. The amount of offset is also not enough to influence the betweenstretch differences, which were all considerably larger than 0.15 cm. DISCUSSION Stretching of the pectoralis minor is often included in the rehabilitation of individuals with shoulder symptoms.3,13,17,22 Manual stretches may be performed in a clinical setting, and home stretches are also typically prescribed to patients. The frequency and duration guidelines for an effective stretch are not firmly established,2 so it is important to maximize the muscle length with the optimal stretch. The results of this analysis indicate that a unilateral self-stretch most effectively lengthens the pectoralis minor muscle relative to its resting length. The second most effective stretch was demonstrated to be a unilateral manual supine stretch, whereas a sitting manual stretch was the least effective at maximizing the pectoralis minor length. The 3 stretches were determined to be statistically different from one another (Table II).
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Table II One-way repeated-measures analysis of variance for stretch type Factor
df
Sum of squares
Mean square
F ratio
Probability level
Subject Stretch type Subject ⫻ stretch type Total
49 2 98 149
76.37 54.60 68.44 199.41
1.56 27.30 0.70
39.09
⬍.00001*
*Statistically significant at P ⬍ .05
Table III Tukey-Kramer multiple comparisons results for stretch type (n ⫽ 50)
Stretch type Corner Sitting manual Supine manual
Significantly different from type
Mean difference (cm)
Sitting manual Supine manual Corner Supine manual Corner Sitting manual
1.47 0.54 –1.47 –0.93 –0.54 0.93
A positive mean difference indicates a greater length change relative to the comparison stretch type.
Both the self-stretch and the supine manual stretch position the humerus at approximately 90° of both abduction and external rotation, whereas the sitting stretch positions the arm at the side in neutral rotation. Because the sitting stretch was shown to be least effective, it may indicate that humeral elevation and external rotation to 90° are important components of pectoralis minor stretching. This humeral position likely tensions soft tissues such as the anterior capsule, pulling the scapula into posterior tipping and external rotation, thus increasing the distance between the coracoid process and the fourth rib landmarks. It was hypothesized that manual pressure to the coracoid process would create increased stretching of the muscle by more precise separation of the muscle’s origin and insertion. This hypothesis was not supported, as the self-stretch was found to be most effective and was the only stretch that did not require manual assistance. The subjects may have felt that they had increased control over how aggressively and how far they stretched during the self-stretch. Similarly, subjects may have had discomfort from the pressure on the coracoid process provided by the examiner, leading to more guarding and a less effective stretch. Perhaps with several repetitions of a manual stretch over several treatment sessions, patient comfort would allow for a more effective manual stretch. The self-stretch also may have created more scapular external rotation in addition to scapular posterior tipping than the manual stretches were able to create. The combined effect of external rotation
and posterior tipping may, therefore, be more effective than a stretch emphasizing either posterior tipping or external rotation of the scapula in isolation. The supine stretch was performed unilaterally with the subject lying prone on a towel roll placed beneath the thoracic spine. This stretch can also be performed bilaterally, which may be more effective. The bilateral stretch will stabilize the client and prevent trunk rotation toward the side of the stretch, possibly maximizing stretch effectiveness. Another concern with this particular stretch is scapular contact with the plinth. It is possible that there were subjects who may not have reached the fullest pectoralis minor length possible because of this mechanical block. This stretch exhibited the largest SE, which perhaps reflects these sources of variability. Even with the limitations of this particular stretch, it was still determined to be more effective in changing muscle length than the sitting manual stretch. The potential influence of pectoralis minor adaptation on scapular kinematics was recently analyzed in 2 asymptomatic groups separated by the normalized resting length of the pectoralis minor.6 Healthy subjects rather than subjects with impingement were used because of the potential for pain to alter scapular motion and confound the motion effects of pectoralis minor length variability. The relatively short pectoralis minor group demonstrated significantly limited scapular posterior tipping at higher arm elevation angles and increased scapular internal rotation compared with the relatively long pectoralis minor group.6 This associative relationship between pectoralis minor length and scapular biomechanics is evidence supporting the assessment of pectoralis minor length in individuals with impingement symptoms and stretching the muscle if indicated. Several studies have included pectoralis minor stretching as part of an intervention intended to alter scapular kinematics or to reduce shoulder impingement symptoms.3,13,17,22 Wang et al22 examined the effects of shoulder posture and exercises on 3dimensional scapular kinematics. Twenty asymptomatic subjects with forward shoulder posture were analyzed with regard to scapular kinematics at rest (arm at side), at elevation in the scapular plane to horizontal, and at maximum elevation in the scapular plane. Subjects were instructed on a 6-week home exercise program designed to mimic a clinical regimen. The
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Figure 6 Comparison of pectoralis minor stretch positions. The amount of change represents the mean difference between maximum length during stretch and resting length in 50 subjects. The asterisk indicates statistically significant differences between all 3 stretch types. Error bars represent SEM.
program included resisted strengthening exercises by use of a Thera-band (Hygenic Corporation, Akron, OH), as well as a corner stretch for the pectoralis muscles, 3 times per week for 6 weeks. Significant changes discovered included a decrease in scapular upward rotation, an increase in scapular internal rotation, and a decrease in scapular superior translation at horizontal, with a decrease in upper thoracic inclination at all 3 positions. No kinematic changes that could be attributed to increases in pectoralis minor length or extensibility (eg, scapular posterior tipping) were demonstrated. McClure et al17 examined the effects of a similar exercise program performed at home for 6 weeks by 39 subjects with impingement symptoms. Strengthening and flexibility exercises were prescribed for all subjects after the initial testing. All subjects were assessed by 3-dimensional kinematic analysis, by analysis of range of motion and posture, and by 2 outcome scales before and after the intervention. The pectoralis minor stretch was performed by grasping a doorway at shoulder height and rotating away from the arm. Subjects demonstrated improvement in some range-of-motion and strength variables and reported subjective im-
provement in pain and functional scores but did not demonstrate kinematic alterations. Bang and Deyle3 compared the effects of a supervised exercise program with the same program plus manual therapy for patients with shoulder impingement. Exercises included 2 stretching exercises including 1 for the pectorals, as well as 6 strengthening exercises. The manual therapy group also received manual therapy aimed at treating movement restrictions, such as techniques to increase glenohumeral caudal glide range of motion and thoracic or cervical mobility and to improve soft-tissue restrictions in the pectoralis minor or other soft tissues. Both groups showed improvement, but the manual therapy group showed significantly greater improvement. Ludewig and Borstad13 examined the effects of a home exercise program on shoulder pain and function in construction workers. The exercise intervention consisted of 2 stretching exercises including a bilateral pectoralis minor stretch, 2 strengthening exercises, and 1 relaxation exercise. Subjects receiving the intervention demonstrated statistically significant improvement in pain and satisfaction with their shoulder and improvements in work-related pain and disability scores.
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A limitation for these intervention studies is the inability to partition out the effects of each specific exercise as it relates to improvement in symptoms and function. It is difficult to know whether the pectoralis minor stretch was specifically beneficial in these analyses. With the determination in our study of the effectiveness of several pectoralis minor stretches, interventions can be more specific to this muscle when it is determined to be adaptively short. A potential limitation of our analysis is an order effect of the stretches. The stretches were performed in the same sequence for each subject—self-stretch, sitting manual stretch, and supine manual stretch. It does not appear that there was an order effect of preconditioning the muscle to make it more extensible, as the first stretch was determined to be the most effective, rather than the last stretch. Similarly, an order effect of inhibiting extensibility is not supported, because the last stretch was determined to be more effective than the second stretch. Even though the results do not indicate an order effect, randomizing the stretch types would have strengthened the study. Randomization was not done in an effort to minimize subject movement from position to position and to minimize the time required to complete data collection. As mentioned in the “Materials and Methods” section, the possibility of skin slip is also a limitation of our study. Skin-mounted sensors have been demonstrated to be valid with the humerus below 120° elevation,10 which was the case for all 3 stretches. In conclusion, this study demonstrated that, of the stretches investigated, a unilateral self-stretch best accomplishes elongation of the pectoralis minor muscle, followed by a unilateral supine manual stretch and, finally, a unilateral sitting manual stretch. Monitoring the subject’s ability to relax during a manual stretch, adding humeral abduction and external rotation, and positioning the scapula in external rotation in addition to posterior tipping are factors to consider when attempting to maximize the length of the pectoralis minor. Interventions or intervention studies targeting shoulder impingement that include a pectoralis minor stretch can now select a stretch based on experimental evidence. REFERENCES
1. An K-N, Browne AO, Korinek S, Tanaka S, Morrey BF. Threedimensional kinematics of glenohumeral elevation. J Orthop Res 1991;9:143-9. 2. Bandy WD, Irion JM. The effect of time on static stretch on the flexibility of the hamstring muscles. Phys Ther 1994;74:845-52. 3. Bang MD, Deyle GD. Comparison of supervised exercise with and without manual physical therapy for patients with shoulder impingement syndrome. J Orthop Sports Phys Ther 2000;30: 126-37. 4. Barnett ND, Duncan RDD, Johnson GR. The measurement of three dimensional scapulohumeral kinematics—a study of reliability. Clin Biomech 1999;14:287-90. 5. Boissonnault WG, Goodman CC. Introduction to pathology of the musculoskeletal system. In: Goodman CC, Boissonnault WG,
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6. 7.
8. 9.
10. 11. 12. 13. 14. 15.
16. 17.
18.
19. 20. 21.
22. 23. 24. 25.
Fuller KS, editors. Pathology: implications for the physical therapist. Philadelphia: Saunders; 2003 821-8. Borstad JD, Ludewig PM. The effect of long versus short pectoralis minor resting length on scapular kinematics in healthy individuals. J Orthop Sports Phys Ther 2005;35:227-38. Borstad JD. The effect of pectoralis minor resting length variability on scapular kinematics [doctoral dissertation]. UMI Dissertation Services, Ann Arbor, MI. 2004. Available from: URL: www.il. proquest.com/umi/dissertations/. p. 83-147. Accessed November 12, 2004. Hebert LJ, Moffet H, McFadyen BJ, Dionne CE. Scapular behavior in shoulder impingement syndrome. Arch Phys Med Rehabil 2002;83:60-9. Herzog W, Guimaraes AC, Anton MC, Carter-Erdman KA. Moment-length relations of rectus femoris muscles of speed skaters/cyclists and runners. Med Sci Sports Exerc 1991;23:128996. 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. Kendall FP, McCreary EK, Provance PG. Muscles: testing and function. 4th ed. Baltimore: Lippincott Williams & Wilkins; 1993. p. 19-106. Kisner C, Colby LA. The shoulder and shoulder girdle. In: Kisner C, Colby LA, editors. Therapeutic exercise: foundations and techniques. 4th ed. Philadelphia: F. A. Davis; 2002 368-9. Ludewig PM, Borstad JD. Effects of a home exercise program on shoulder pain and functional status in construction workers. Occup Environ Med 2003;60:841-9. 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. Lukasiewicz AC, McClure P, Michener L, Pratt N, Sennett B. Comparison of 3-dimensional scapular position and orientation between subjects with and without shoulder impingement. J Orthop Sports Phys Ther 1999;298:574-86. Magee DJ. Orthopedic physical assessment. 4th ed. Philadelphia: Saunders; 2002. p. 243-89. McClure PW, Bialker J, Neff N, Williams G, Karduna A. Shoulder function and 3-dimensional kinematics in people with shoulder impingement syndrome before and after a 6-week exercise program. Phys Ther 2004;84:832-48. 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;10:26977. Michener LA, McClure PW, Karduna AR. Anatomical and biomechanical mechanisms of subacromial impingement syndrome. Clin Biomech 2003;18:369-79. Sahrmann SA. Movement impairment syndromes of the shoulder girdle. In: Diagnosis and treatment of movement impairment syndromes. St Louis: Mosby; 2002. p. 193-261. Soslowsky LJ, Thomopoulos S, Esmail A, Flanagan CL, Iannotti JP, Williamson JD III, et al. Development and use of an animal model for investigation on rotator cuff disease. J Shoulder Elbow Surg 1996;5:383-92. Wang C-H, McClure P, Pratt NE, Nobilini R. Stretching and strengthening exercises: their effect on three-dimensional scapular kinematics. Arch Phys Med Rehabil 1999;80:923-9. Wang SS, Whitney SL, Burdett RG, Janosky JE. Lower extremity muscular flexibility in long distance runners. J Orthop Sports Phys Ther 1993;17:102-7. Williams PE, Goldspink G. The effect of immobilization on the longitudinal growth of striated muscle fibres. J Anat 1973;116: 45-55. Williams PE, Goldspink G. Changes in sarcomere length and physiological properties in immobilized muscle. J Anat 1978;3:459-68.
Pectoralis minor adaptive shortening in healthy individuals is associated with altered scapular kinematics similar to the alterations demonstrated in individuals with subacromial impingement. This associative relationship suggests that stretching of the pectoralis minor may improve scapular kinematics and assist in the management of shoulder impingement. Several stretches for the pectoralis minor are used clinically, although it is not known which stretch optimally lengthens the muscle. The purpose of this analysis was to compare the mean length change for 3 pectoralis minor stretches. Fifty subjects without shoulder pathology were examined for the change in length of the pectoralis minor during 3 separate stretches by use of an electromagnetic motion-capture system. The stretches analyzed were a unilateral self-stretch, a supine manual stretch, and a sitting manual stretch. Each stretch was significantly different from the other two (df, 2/98; F ratio, 39.09; P ⬍ .00001), with the unilateral self-stretch demonstrating the greatest length change (2.24 cm), followed by the supine manual stretch (1.69 cm) and the sitting manual stretch (0.77 cm). Knowledge of the most effective method of elongating the pectoralis minor muscle may improve clinical decision making when targeting this anterior scapulothoracic muscle as part of intervention for or prevention of shoulder impingement. (J Shoulder Elbow Surg 2006;15: 324-330.)
M any authors have described skeletal muscle adap-
tations such as muscle length changes and strength imbalances.11,20,23 Postural faults,11,20,22 chronic use of a muscle at a specific length or joint angle,9 and higher activation of muscles on one side of a joint From the aPhysical Therapy Division, School of Allied Medical Professions, The Ohio State University, Columbus, and bProgram in Physical Therapy, Department of Physical Medicine and Rehabilitation, University of Minnesota, Minneapolis. Reprint requests: John D. Borstad, PhD, PT, Division of Physical Therapy, The Ohio State University, 1583 Perry St, Columbus, OH 43210-1234 (E-mail: [email protected]). Copyright © 2006 by Journal of Shoulder and Elbow Surgery Board of Trustees. 1058-2746/2006/$32.00 doi:10.1016/j.jse.2005.08.011
324
compared with the antagonist muscles23 are all proposed mechanisms of skeletal muscle adaptation. At the shoulder complex, prolonged exposure to postures of increased scapular protraction and anterior tipping is proposed to result in a shortening or tightness of the pectoralis minor muscle.11,20 Repetitive use of the upper extremities in positions that protract and downwardly rotate the scapulae may also result in pectoralis minor adaptive shortening.14,15 Manual stretching of the pectoralis minor is, therefore, often performed as an intervention when posture deviates from neutral or for shoulder impingement.11,20 Home exercise programs have also included a self-stretch for the pectoralis minor.13,17,22 The pectoralis minor attaches at the coracoid process of the scapula and at the third, fourth, and fifth ribs near their sternocostal junctions. This muscle elongates during arm elevation, allowing the scapula to upwardly rotate, externally rotate, and tip posteriorly18 (Figure 1). A relatively short pectoralis minor muscle, as a result of adaptation, would demonstrate less total excursion than a relatively longer muscle,24,25 limiting full scapular motion. Limitation of scapular motion during arm elevation is believed to decrease the available subacromial space and contribute to shoulder pathology.8,14,15,18,19,22 A decrease in the subacromial space combined with exposure to overhead use has demonstrated rotator cuff changes similar to those seen in individuals with impingement.21 Individuals with symptoms of shoulder impingement, including workers exposed to overhead work, have exhibited these scapular motion limitations in several controlled studies.8,14,15 It is possible that one important mechanistic connection between limitations in scapular motion, particularly tipping, and shoulder symptoms is a decreased resting length of the pectoralis minor. A decreased resting length of the pectoralis minor could be either a causative factor for scapular kinematic alterations or a result of altered scapular position or motion. The end result of either of these possibilities is the need to stretch the muscle in an attempt to increase its excursion and help restore normal scapular kinematics during arm elevation. The purpose of this study was to compare 3 stretches to determine the most effective method for stretching the pectoralis minor muscle. This information will be valuable to clinicians wishing to include a
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Figure 1 Three-dimensional scapular rotations. Upward rotation and downward rotation occur about an axis perpendicular to the plane of the scapula. Anterior tipping and posterior tipping occur about a medial-lateral axis. Internal rotation and external rotation occur about a vertical axis.
pectoralis minor stretch for their patients. We hypothesized that manual stretches would be more effective than would a self-stretch because more precise separation of the muscle’s origin and insertion could be obtained through direct contact by a therapist on the coracoid process and through improved stabilization of the thorax, as compared with the more general anterior shoulder stretch performed by the patient. MATERIALS AND METHODS Subjects Fifty healthy individuals without current shoulder pain or a history of shoulder trauma were recruited for this analysis. Subjects were required to be aged between 20 and 40 years (mean, 27.5 years) to ensure full skeletal growth while avoiding the developing joint degenerative changes that are common in individuals aged over 60 years.5 An attempt to avoid including subjects with joint degenerative changes was made to minimize the potential effect of this variable on normal joint motion. Volunteers were recruited by personal contact, advertising on campus (University of Minnesota, Minneapolis, MN), and addressing graduate classes in physical therapy and kinesiology. All subjects were required to sign both a University of Minnesota– approved informed consent form and a Health Insurance Portability and Accountability Act form before entering the study. A clinical examination was performed on each subject to ensure that no underlying pathology was present in the tested shoulder. The examination included range of motion; the impingement tests of Hawkins, Neer, and Jobe; the apprehension test for determining anterior instability; and the sulcus sign to test laxity.16
Instrumentation The Flock-of-Birds electromagnetic motion-capture system (Ascension Technology Corp, Burlington, VT) was used for measuring pectoralis minor length and analyzing stretches in this study. To determine pectoralis minor
length and length change, 3 mini-bird sensors were used for each subject. A scapular sensor was fixed to the subject’s skin over the broad, flat area of the acromion, and a sternal sensor was fixed to the skin just distal to the sternal notch with double-sided adhesive tape. A third sensor was attached to a thermoplastic cuff and secured over the subject’s distal humerus with Velcro straps. The source transmitter of the system was located at acromion height behind the subject. A digitization sequence established local anatomically based axis systems for each segment (Figure 2). In addition, the coracoid process and the fourth rib/sternum junction were digitized to represent the length of the pectoralis minor. This length measurement was validated in vitro with an Intraclass Correlation Coefficient (ICC) of 0.96 comparing the surface palpation and digitization of the previously mentioned landmarks with digitization of the same landmarks after dissection to visualize the actual origin and insertion of the muscle.7 Reliability and validity of electromagnetic tracking systems in capturing 3-dimensional movements have been demonstrated.1,4,10 Data were collected at 100 Hz per sensor, and all post-processing was performed by use of MotionMonitor software (Innovative Sports Training, Chicago, IL) integrated with the Flock-ofBirds system. To determine the length of the pectoralis minor, the digitized point representing the muscles’ origin and insertion was mathematically converted to be in the reference frame of one of the local sensors. The coracoid process point was calculated to be in the reference frame of the scapular sensor, and the fourth rib point was calculated in the reference frame of the trunk sensor. The 3-dimensional vector from each pectoralis minor landmark to its respective sensor was then calculated. Given the assumption that the scapula and trunk are rigid bodies, these landmark-to-sensor vectors remain constant. The position and orientation of both sensors are also calculated relative to the transmitter reference frame. Finally, with these variables known, the 3-dimensional
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Figure 2 Local orthogonal axis systems for scapula, humerus, and trunk. Dotted lines on the humeral figure represent the thermoplastic cuff used for sensor placement and digitization. Origins are the acromioclavicular joint for the scapula, medial epicondyle for the humerus, and sternal notch for the trunk.
Figure 3 Unilateral corner stretch. The subject’s forearm is stabilized by a vertical plane before the trunk is rotated in the opposite direction.
Figure 4 Sitting manual stretch. The investigator’s hypothenar eminence is used to apply force to the scapula through the coracoid process.
vector lengths between the 2 digitized points were calculated in the varying stretch positions.7
on a flat planar surface. The subject then rotated the trunk away from the elevated arm, increasing the horizontal abduction at the shoulder and maximizing the stretch across the chest (Figure 3). The subject held this position for 3 seconds. The second and third stretches were both performed after lowering the transmitter to keep the sensors within the magnetic field. The second stretch was performed manually by the examiner with the subject sitting in a plastic chair without resting against the back of the chair and the arm in the dependent position. The subject was instructed to inhale deeply and hold his or her breath while the muscle was fully elongated by the examiner. To stretch the muscle, the examiner applied a posterior force to the coracoid process with one hand while stabilizing the inferior angle of the scapula with the other hand (Figure 4).
Procedures To determine the pectoralis minor resting length reference value for each subject, data were collected for 1 second in the normal, relaxed standing position. The pectoralis minor resting length was defined as the mean vector length calculated over this 1-second file. The stretched pectoralis minor vector length was subsequently determined by data collected during each of the 3 stretches. The first stretch was a self-stretch done in the standing position and required the subject to abduct the humerus to 90° with the elbow flexed to 90° and place the palm
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Table I Mean length change for pectoralis minor by stretch type Stretch type
Mean (SE) (cm)
Corner Sitting manual Supine manual
2.24 (0.10) 0.77 (0.11) 1.70 (0.19)
minor landmarks after skin motion would have occurred as a result of the combined effect of arm elevation and the stretch position.
RESULTS
Figure 5 Supine manual stretch. The investigator holds the ipsilateral shoulder in 90° abduction and elbow in 90° flexion before applying force to the scapula through the coracoid process with the hypothenar eminence. The subject is lying with a towel roll between the thoracic spine and the treatment table.
After positioning the muscle in the stretch position, the subject was instructed to exhale.12 The examiner held this stretch position for 3 seconds. The third stretch was performed manually by the examiner with the subject lying in a supine position on a treatment plinth with a towel roll running the length of the thoracic spine. The examiner positioned the subject’s shoulder at 90° of abduction and external rotation and the elbow at 90° flexion while applying a posterior force to the coracoid process, again holding the stretch position for 3 seconds (Figure 5). The resting length value for each subject was subtracted from each stretch length value to arrive at a length change for each stretch position. This resulted in change values for each stretch relative to an individual subject’s pectoralis minor resting length. A 1-way repeated-measures analysis of variance with stretch type as the repeated factor was used to examine potential differences between stretches. The dependent variable was the length change score for each stretch type. Statistically significant main effects of stretch type were further explored with a post hoc Tukey-Kramer multiple comparisons test. A limitation of the Flock-of-Birds system is that the accuracy and validity of the values may be compromised by motion between the skin-mounted sensor and the underlying bone with positioning into extreme ranges of motion.10 This is more likely to be a problem with the arm at 90° because larger errors are created as arm elevation progresses to angles above 120° humeral elevation.10 This potential effect was examined by digitizing 1 subject according to the protocol, recording a corner self-stretch, and then digitizing this same subject a second time as he held the corner stretch position. The pectoralis minor origin and insertion landmarks were also directly palpated and re-digitized after the subject was in the stretch position. This second digitization calculated the distance between the pectoralis
A summary of the amount of change from resting length for each stretch type is presented in Table I. There was a statistically significant main effect of stretch type (df, 2/98; F ratio, 39.09; P ⬍ .00001) (Table II). The Tukey-Kramer multiple comparisons test indicated that each stretch type was significantly different from each of the other two stretch types (Table III). The corner stretch demonstrated the greatest change (2.24 cm), followed by the supine manual stretch (1.69 cm) and the sitting manual stretch (0.77 cm) (Figure 6). For the single-subject skin-slip assessment, the value for the pectoralis minor length was 17.35 cm during the original condition and 17.50 cm in the re-digitized validation condition, an offset of 0.15 cm. This offset value is similar to the SEM for the change in pectoralis minor length during all stretches (Table I). In addition, the pectoralis minor was estimated to be longer in the re-digitized condition, an indication that the length used for the stretch comparisons was likely to be underestimated. The amount of offset is also not enough to influence the betweenstretch differences, which were all considerably larger than 0.15 cm. DISCUSSION Stretching of the pectoralis minor is often included in the rehabilitation of individuals with shoulder symptoms.3,13,17,22 Manual stretches may be performed in a clinical setting, and home stretches are also typically prescribed to patients. The frequency and duration guidelines for an effective stretch are not firmly established,2 so it is important to maximize the muscle length with the optimal stretch. The results of this analysis indicate that a unilateral self-stretch most effectively lengthens the pectoralis minor muscle relative to its resting length. The second most effective stretch was demonstrated to be a unilateral manual supine stretch, whereas a sitting manual stretch was the least effective at maximizing the pectoralis minor length. The 3 stretches were determined to be statistically different from one another (Table II).
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Table II One-way repeated-measures analysis of variance for stretch type Factor
df
Sum of squares
Mean square
F ratio
Probability level
Subject Stretch type Subject ⫻ stretch type Total
49 2 98 149
76.37 54.60 68.44 199.41
1.56 27.30 0.70
39.09
⬍.00001*
*Statistically significant at P ⬍ .05
Table III Tukey-Kramer multiple comparisons results for stretch type (n ⫽ 50)
Stretch type Corner Sitting manual Supine manual
Significantly different from type
Mean difference (cm)
Sitting manual Supine manual Corner Supine manual Corner Sitting manual
1.47 0.54 –1.47 –0.93 –0.54 0.93
A positive mean difference indicates a greater length change relative to the comparison stretch type.
Both the self-stretch and the supine manual stretch position the humerus at approximately 90° of both abduction and external rotation, whereas the sitting stretch positions the arm at the side in neutral rotation. Because the sitting stretch was shown to be least effective, it may indicate that humeral elevation and external rotation to 90° are important components of pectoralis minor stretching. This humeral position likely tensions soft tissues such as the anterior capsule, pulling the scapula into posterior tipping and external rotation, thus increasing the distance between the coracoid process and the fourth rib landmarks. It was hypothesized that manual pressure to the coracoid process would create increased stretching of the muscle by more precise separation of the muscle’s origin and insertion. This hypothesis was not supported, as the self-stretch was found to be most effective and was the only stretch that did not require manual assistance. The subjects may have felt that they had increased control over how aggressively and how far they stretched during the self-stretch. Similarly, subjects may have had discomfort from the pressure on the coracoid process provided by the examiner, leading to more guarding and a less effective stretch. Perhaps with several repetitions of a manual stretch over several treatment sessions, patient comfort would allow for a more effective manual stretch. The self-stretch also may have created more scapular external rotation in addition to scapular posterior tipping than the manual stretches were able to create. The combined effect of external rotation
and posterior tipping may, therefore, be more effective than a stretch emphasizing either posterior tipping or external rotation of the scapula in isolation. The supine stretch was performed unilaterally with the subject lying prone on a towel roll placed beneath the thoracic spine. This stretch can also be performed bilaterally, which may be more effective. The bilateral stretch will stabilize the client and prevent trunk rotation toward the side of the stretch, possibly maximizing stretch effectiveness. Another concern with this particular stretch is scapular contact with the plinth. It is possible that there were subjects who may not have reached the fullest pectoralis minor length possible because of this mechanical block. This stretch exhibited the largest SE, which perhaps reflects these sources of variability. Even with the limitations of this particular stretch, it was still determined to be more effective in changing muscle length than the sitting manual stretch. The potential influence of pectoralis minor adaptation on scapular kinematics was recently analyzed in 2 asymptomatic groups separated by the normalized resting length of the pectoralis minor.6 Healthy subjects rather than subjects with impingement were used because of the potential for pain to alter scapular motion and confound the motion effects of pectoralis minor length variability. The relatively short pectoralis minor group demonstrated significantly limited scapular posterior tipping at higher arm elevation angles and increased scapular internal rotation compared with the relatively long pectoralis minor group.6 This associative relationship between pectoralis minor length and scapular biomechanics is evidence supporting the assessment of pectoralis minor length in individuals with impingement symptoms and stretching the muscle if indicated. Several studies have included pectoralis minor stretching as part of an intervention intended to alter scapular kinematics or to reduce shoulder impingement symptoms.3,13,17,22 Wang et al22 examined the effects of shoulder posture and exercises on 3dimensional scapular kinematics. Twenty asymptomatic subjects with forward shoulder posture were analyzed with regard to scapular kinematics at rest (arm at side), at elevation in the scapular plane to horizontal, and at maximum elevation in the scapular plane. Subjects were instructed on a 6-week home exercise program designed to mimic a clinical regimen. The
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Figure 6 Comparison of pectoralis minor stretch positions. The amount of change represents the mean difference between maximum length during stretch and resting length in 50 subjects. The asterisk indicates statistically significant differences between all 3 stretch types. Error bars represent SEM.
program included resisted strengthening exercises by use of a Thera-band (Hygenic Corporation, Akron, OH), as well as a corner stretch for the pectoralis muscles, 3 times per week for 6 weeks. Significant changes discovered included a decrease in scapular upward rotation, an increase in scapular internal rotation, and a decrease in scapular superior translation at horizontal, with a decrease in upper thoracic inclination at all 3 positions. No kinematic changes that could be attributed to increases in pectoralis minor length or extensibility (eg, scapular posterior tipping) were demonstrated. McClure et al17 examined the effects of a similar exercise program performed at home for 6 weeks by 39 subjects with impingement symptoms. Strengthening and flexibility exercises were prescribed for all subjects after the initial testing. All subjects were assessed by 3-dimensional kinematic analysis, by analysis of range of motion and posture, and by 2 outcome scales before and after the intervention. The pectoralis minor stretch was performed by grasping a doorway at shoulder height and rotating away from the arm. Subjects demonstrated improvement in some range-of-motion and strength variables and reported subjective im-
provement in pain and functional scores but did not demonstrate kinematic alterations. Bang and Deyle3 compared the effects of a supervised exercise program with the same program plus manual therapy for patients with shoulder impingement. Exercises included 2 stretching exercises including 1 for the pectorals, as well as 6 strengthening exercises. The manual therapy group also received manual therapy aimed at treating movement restrictions, such as techniques to increase glenohumeral caudal glide range of motion and thoracic or cervical mobility and to improve soft-tissue restrictions in the pectoralis minor or other soft tissues. Both groups showed improvement, but the manual therapy group showed significantly greater improvement. Ludewig and Borstad13 examined the effects of a home exercise program on shoulder pain and function in construction workers. The exercise intervention consisted of 2 stretching exercises including a bilateral pectoralis minor stretch, 2 strengthening exercises, and 1 relaxation exercise. Subjects receiving the intervention demonstrated statistically significant improvement in pain and satisfaction with their shoulder and improvements in work-related pain and disability scores.
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A limitation for these intervention studies is the inability to partition out the effects of each specific exercise as it relates to improvement in symptoms and function. It is difficult to know whether the pectoralis minor stretch was specifically beneficial in these analyses. With the determination in our study of the effectiveness of several pectoralis minor stretches, interventions can be more specific to this muscle when it is determined to be adaptively short. A potential limitation of our analysis is an order effect of the stretches. The stretches were performed in the same sequence for each subject—self-stretch, sitting manual stretch, and supine manual stretch. It does not appear that there was an order effect of preconditioning the muscle to make it more extensible, as the first stretch was determined to be the most effective, rather than the last stretch. Similarly, an order effect of inhibiting extensibility is not supported, because the last stretch was determined to be more effective than the second stretch. Even though the results do not indicate an order effect, randomizing the stretch types would have strengthened the study. Randomization was not done in an effort to minimize subject movement from position to position and to minimize the time required to complete data collection. As mentioned in the “Materials and Methods” section, the possibility of skin slip is also a limitation of our study. Skin-mounted sensors have been demonstrated to be valid with the humerus below 120° elevation,10 which was the case for all 3 stretches. In conclusion, this study demonstrated that, of the stretches investigated, a unilateral self-stretch best accomplishes elongation of the pectoralis minor muscle, followed by a unilateral supine manual stretch and, finally, a unilateral sitting manual stretch. Monitoring the subject’s ability to relax during a manual stretch, adding humeral abduction and external rotation, and positioning the scapula in external rotation in addition to posterior tipping are factors to consider when attempting to maximize the length of the pectoralis minor. Interventions or intervention studies targeting shoulder impingement that include a pectoralis minor stretch can now select a stretch based on experimental evidence. REFERENCES
1. An K-N, Browne AO, Korinek S, Tanaka S, Morrey BF. Threedimensional kinematics of glenohumeral elevation. J Orthop Res 1991;9:143-9. 2. Bandy WD, Irion JM. The effect of time on static stretch on the flexibility of the hamstring muscles. Phys Ther 1994;74:845-52. 3. Bang MD, Deyle GD. Comparison of supervised exercise with and without manual physical therapy for patients with shoulder impingement syndrome. J Orthop Sports Phys Ther 2000;30: 126-37. 4. Barnett ND, Duncan RDD, Johnson GR. The measurement of three dimensional scapulohumeral kinematics—a study of reliability. Clin Biomech 1999;14:287-90. 5. Boissonnault WG, Goodman CC. Introduction to pathology of the musculoskeletal system. In: Goodman CC, Boissonnault WG,
J Shoulder Elbow Surg May/June 2006
6. 7.
8. 9.
10. 11. 12. 13. 14. 15.
16. 17.
18.
19. 20. 21.
22. 23. 24. 25.
Fuller KS, editors. Pathology: implications for the physical therapist. Philadelphia: Saunders; 2003 821-8. Borstad JD, Ludewig PM. The effect of long versus short pectoralis minor resting length on scapular kinematics in healthy individuals. J Orthop Sports Phys Ther 2005;35:227-38. Borstad JD. The effect of pectoralis minor resting length variability on scapular kinematics [doctoral dissertation]. UMI Dissertation Services, Ann Arbor, MI. 2004. Available from: URL: www.il. proquest.com/umi/dissertations/. p. 83-147. Accessed November 12, 2004. Hebert LJ, Moffet H, McFadyen BJ, Dionne CE. Scapular behavior in shoulder impingement syndrome. Arch Phys Med Rehabil 2002;83:60-9. Herzog W, Guimaraes AC, Anton MC, Carter-Erdman KA. Moment-length relations of rectus femoris muscles of speed skaters/cyclists and runners. Med Sci Sports Exerc 1991;23:128996. 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. Kendall FP, McCreary EK, Provance PG. Muscles: testing and function. 4th ed. Baltimore: Lippincott Williams & Wilkins; 1993. p. 19-106. Kisner C, Colby LA. The shoulder and shoulder girdle. In: Kisner C, Colby LA, editors. Therapeutic exercise: foundations and techniques. 4th ed. Philadelphia: F. A. Davis; 2002 368-9. Ludewig PM, Borstad JD. Effects of a home exercise program on shoulder pain and functional status in construction workers. Occup Environ Med 2003;60:841-9. 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. Lukasiewicz AC, McClure P, Michener L, Pratt N, Sennett B. Comparison of 3-dimensional scapular position and orientation between subjects with and without shoulder impingement. J Orthop Sports Phys Ther 1999;298:574-86. Magee DJ. Orthopedic physical assessment. 4th ed. Philadelphia: Saunders; 2002. p. 243-89. McClure PW, Bialker J, Neff N, Williams G, Karduna A. Shoulder function and 3-dimensional kinematics in people with shoulder impingement syndrome before and after a 6-week exercise program. Phys Ther 2004;84:832-48. 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;10:26977. Michener LA, McClure PW, Karduna AR. Anatomical and biomechanical mechanisms of subacromial impingement syndrome. Clin Biomech 2003;18:369-79. Sahrmann SA. Movement impairment syndromes of the shoulder girdle. In: Diagnosis and treatment of movement impairment syndromes. St Louis: Mosby; 2002. p. 193-261. Soslowsky LJ, Thomopoulos S, Esmail A, Flanagan CL, Iannotti JP, Williamson JD III, et al. Development and use of an animal model for investigation on rotator cuff disease. J Shoulder Elbow Surg 1996;5:383-92. Wang C-H, McClure P, Pratt NE, Nobilini R. Stretching and strengthening exercises: their effect on three-dimensional scapular kinematics. Arch Phys Med Rehabil 1999;80:923-9. Wang SS, Whitney SL, Burdett RG, Janosky JE. Lower extremity muscular flexibility in long distance runners. J Orthop Sports Phys Ther 1993;17:102-7. Williams PE, Goldspink G. The effect of immobilization on the longitudinal growth of striated muscle fibres. J Anat 1973;116: 45-55. Williams PE, Goldspink G. Changes in sarcomere length and physiological properties in immobilized muscle. J Anat 1978;3:459-68.