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PHYS THER
Vol. 89, No. 4, April 2009, pp. 333-341
DOI: 10.2522/ptj.20080248

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Research Reports

Lengthening of the Pectoralis Minor Muscle During Passive Shoulder Motions and Stretching Techniques: A Cadaveric Biomechanical Study

Takayuki Muraki, Mitsuhiro Aoki, Tomoki Izumi, Misaki Fujii, Egi Hidaka and Shigenori Miyamoto

T Muraki, PT, PhD, is Doctoral Student, Doctoral Course of Physical Therapy, Graduate School of Health Sciences, Sapporo Medical University, South 1, West 17, Chuo-ku, Sapporo 060-8556, Japan.
M Aoki, MD, PhD, is Associate Professor, Department of Physical Therapy, School of Health Sciences, Sapporo Medical University.
T Izumi, PT, MS, is Doctoral Student, Doctoral Course of Physical Therapy, Graduate School of Health Sciences, Sapporo Medical University.
M Fujii, PT, MS, is Doctoral Student, Doctoral Course of Physical Therapy, Graduate School of Health Sciences, Sapporo Medical University.
E Hidaka, PT, MS, is Doctoral Student, Doctoral Course of Physical Therapy, Graduate School of Health Sciences, Sapporo Medical University.
S Miyamoto, PT, PhD, is Professor, Department of Physical Therapy, Hokkaido Bunkyo University, Sapporo, Japan.

Address all correspondence to Dr Muraki at: takayukimurakipt{at}yahoo.co.jp

Submitted August 13, 2008; Accepted January 9, 2009

 
Background and Purpose: Lengthening of the pectoralis minor muscle (PMi) during passive shoulder motions and the effect of stretching techniques for this muscle are unclear. The purposes of this study were: (1) to investigate the amount and pattern of the lengthening between passive shoulder motions and (2) to determine which stretching technique effected the greatest change in PMi length.

Methods: Nine fresh cadaveric transthoracic specimens were used. Lengthening in the lateral and medial fiber group of the PMi was directly measured during 3 passive shoulder motions (flexion, scaption, and external rotation at 90° of abduction) and 3 stretching techniques (scapular retraction at 0° and 30° of flexion and horizontal abduction) for this muscle. The measurement was conducted by using a precise displacement sensor.

Results: Although the length of the PMi linearly increased during all shoulder motions, lengthening during flexion and scaption was steeper and significantly larger than that during external rotation at 90 degrees of abduction. For the stretching techniques, scapular retraction at 30 degrees of flexion and horizontal abduction stretched the PMi more than scapular retraction at 0 degrees of flexion. In comparison with lengthening at 150 degrees of flexion, scapular retraction at 30 degrees of flexion significantly stretched the medial fiber group of the muscle.

Discussion and Conclusion: The extensive lengthening of the PMi is necessary during shoulder motions, especially flexion and scaption. Scapular retraction at 30 degrees of flexion makes the greatest change in PMi length. This study suggests the importance of the PMi in shoulder motion and provides anatomical and biomechanical evidence that might guide appropriate selection of stretching techniques.

Top Abstract Introduction Method Results Discussion Conclusion References

 
The potential relationship of scapular position and motion to shoulder disorders has made them of great interest to many clinicians and researchers.^1–6 Studies using 3-dimensional motion analysis clarified the details of the scapular motion during shoulder motion.^7–10 Upward and external rotation and posterior tilting of the scapula were seen during shoulder elevation, regardless of elevation plane.^8,10 Similar scapular motions also were confirmed near the end range of external rotation at 90 degrees of abduction.⁸

The differences in scapular motion between people who are healthy and patients with shoulder disorders have been investigated. Previous studies demonstrated decreases in scapular posterior tilting, upward rotation, and external rotation during shoulder elevation in patients with subacromial impingement compared with participants who were healthy.^11–13 In patients with shoulder instability, a decrease of scapular motion was observed from 0 to 90 degrees of shoulder elevation.^2,14 These losses in scapular motion led to narrowing of the subacromial space^1,15 and altered glenohumeral motions,⁸ contributing to injuries of the labrum, joint cartilage, and cuff tendons of the shoulder joint.

The pectoralis minor muscle (PMi) is the sole muscle connecting the scapula and anterior side of the thoracic region and functions to depress the scapula. Therefore, shortening of this muscle is expected to restrain scapular motion in the superior and posterior direction. A previous study¹⁶ indicated that the resting length of the PMi during standing with the arm at the side affected the scapular kinematics. Based on these findings, techniques to stretch the PMi are performed in clinical practice to lengthen the muscle.^17–21 In order to increase the distance between the insertion and origin of the PMi, the scapula is manipulated directly or indirectly without glenohumeral motion in these stretching techniques. However, to our knowledge, no study has investigated the amount of PMi lengthening associated with shoulder motions and how far the specific techniques stretch the muscle.

In order to measure lengthening of the PMi directly, we developed a transthoracic cadaveric model capable of simulating passive shoulder motion, including glenohumeral and scapulothoracic joint motion.²² The purposes of this study were: (1) to investigate the amount and pattern of PMi lengthening during passive shoulder motions and (2) to examine PMi stretching techniques to obtain greatest change in length. Information provided by this study is useful to understand how lengthening of the PMi is related to shoulder motions we studied and how various stretches affect the muscle. It also is useful to direct patient care related to stretching the PMi when tightness is determined.

Top Abstract Introduction Method Results Discussion Conclusion References

 
Preparation of the Specimen

Nine transthoracic specimens were harvested from fresh cadavers obtained after acquisition of informed consent prior to death. The mean age was 84 years (range=67–96). The transthoracic specimen included the thoracic cage and the C4 through T12 vertebral bodies. Specimens with evidence of rotator cuff tear, osteoarthritis, or contracture were excluded. Specimens were kept in a freezer at –20°C after disarticulation, and then thawed at room temperature 24 hours prior to the experiment. Thawing was confirmed through 10 repetitions of preconditioned shoulder movement in each of 6 directions: flexion, abduction, internal and external rotation, and horizontal adduction and abduction. At this point, the study specimens were selected according to the following criteria for shoulder range of motion: (1) more than 150 degrees of flexion and (2) 90 degrees of external rotation at 90 degrees of abduction. In order to measure the PMi directly, the skin, subcutaneous tissue, and pectoralis major muscle were removed, as needed, before the measurement. The specimen was secured in the upright position on a wooden pole by inserting Kirschner wire at the thoracic spine and sternum (Fig. 1). This setup allowed the shoulder to move freely as previously reported in the literature.²² The experiment was performed at room temperature (22°C), and the specimens were kept moist by spraying with saline solution every 5 to 10 minutes.

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Figure 1. Illustration of the experimental setting. Two pulse coder sensors were attached on the lateral and medial fiber groups of the pectoralis minor muscle. Another illustration in the upper right box is an enlargement of the pulse coder.

Measurement of PMi Lengthening

The PMi originates from the third, fourth, and fifth ribs; runs superolaterally, converging, and inserting at the coracoid process; and forms a shape similar to a triangle. Lengthening of muscle fibers on the lateral side (fibers originating from the fifth rib) and medial side (fibers originating from the third rib) could differ because of the differing angles relative to the line of force. Thus, the lengthening on both the lateral and medial fiber groups of the PMi was measured in this study (Fig. 2).

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Figure 2. Anterolateral view of the pectoralis minor muscle on the left side during shoulder elevation in the scapular plane. This picture shows 3 origins of the pectoralis minor muscle. Arrows indicate the lateral and medial fibers of the muscle.

Two precise displacement sensors (Pulse coder^*), each consisting of a coil sensor and a brass pipe, were used to determine the change in length. Displacement was measured by detecting the position of the brass pipe relative to a coil sensor that generated the magnetic field. Analog data of the displacement were represented and recorded on a digital scaling meter (HV35) that converted the data to a digital format. The device had a range of measurement of 40 mm, and its accuracy was 0.1 mm root mean square. These sensors were mounted on the center of the muscle belly of the medial and lateral fibers, parallel to the muscle fiber, in order to accurately reflect the shortening and lengthening behavior of the muscle. A preliminary study confirmed that the center part of the muscle was lengthened most during shoulder motions. The center of the muscle belly was determined by measuring its length and width with a digital caliper. Fishhook-like barbed points attached to each coil sensor and brass pipe prevented the sensor from slipping out of the muscle.

Passive Shoulder Motions and Stretching Techniques

For passive shoulder motion, muscle lengthening was measured during flexion, elevation in the scapular plane (scaption), and external rotation at 90 degrees of abduction (ER90), which were expected to lengthen the PMi based on anatomical knowledge and scapular motions measured by a previous study.⁸ The measurement was performed in a range of 0 to 150 degrees, in 30-degree increments, for flexion and scaption, whereas measurement from 0 to 90 degrees in 15-degree increments was used for ER90. Neutral position was defined as 0 degrees of elevation with neutral rotation in the shoulder joint. Furthermore, in the neutral position, the scapula was settled so that the medial border was perpendicular to the ground and the scapular spine was angled 30 degrees anterior relative to the coronal plane.²³

Three standard stretching techniques were selected for this study. Figure 3 shows each technique performed on the cadaveric specimen in this study. The first technique was scapular retraction at 0 degrees of flexion (retraction-0). With this technique, the examiner manually applied a posterior force on the coracoid process^17,18 (Fig. 3A). The second technique was scapular retraction at 30 degrees of flexion (retraction-30). The examiner flexed the shoulder joint and applied a posterosuperior force to the elbow along the longitudinal axis of the humerus (Fig. 3B). The third technique was horizontal abduction at 90 degrees of external rotation (horizontal abduction).^19–21,24 The examiner abducted the shoulder joint with 90 degrees of external rotation and then horizontally abducted it by applying posterior force to the proximal humerus (Fig. 3C). All techniques were performed to the position of end-feel by one examiner (TI). Each position was maintained for more than 10 seconds, until no increase or decrease in lengthening values was observed. The measurement was repeated 3 times for each shoulder motion and stretching technique. The measurement order was randomized in order to eliminate the stretching effect.

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Figure 3. Stretching techniques simulated in this study: (A) scapular retraction at 0 degrees of flexion, (B) scapular retraction at 30 degrees of flexion, and (C) horizontal abduction at 90 degrees of external rotation. Arrows show the direction in which stretching force is applied.

Data Analysis

For the normalization of the data, the lengthening ratio of the PMi during all shoulder motions and stretching techniques was calculated by the following formula:

where L and L are the displacement of the PMi and the distance of the sensor at the neutral position, respectively.

A 2-way repeated-measures analysis of variance (ANOVA) was used to test the differences of lengthening ratio regarding end position of shoulder motion and muscle fiber group factors and stretching technique and muscle fiber group factors. Bonferroni multiple comparisons were used as a post hoc test for the factors of end position of shoulder motion and stretching technique in each fiber group.

After finding stretching techniques that showed a greater lengthening ratio, a 2-way repeated-measures ANOVA and a Dunnett multiple comparison test were used to compare the lengthening ratios in the stretching techniques with 150 degrees of flexion, while determining muscle fiber group factor. Statistical analysis was performed with a statistical software package (StatView for Windows version 5.0.1). The alpha level was set to .05.

Top Abstract Introduction Method Results Discussion Conclusion References

 
Lengthening During Passive Shoulder Motions

The lengthening ratio in the lateral and medial fiber groups of the PMi during each passive shoulder motion is shown in Figure 4. In flexion and scaption, a similar pattern of the increase in lengthening ratio for both fiber groups was observed regardless of the different elevation plane. This curve pattern was characterized by small increases (0.8%–1.8%) up to 30 degrees and large increases (4.0%–25.5%) after that (Fig. 4A and 4B). A video of the lengthening of the pectoralis minor muscle during passive elevation in the scapular plane is available. At 150 degrees of both flexion and scaption, the lengthening ratio achieved in the lateral and medial fiber groups was 50% and 40%, respectively. In ER90, the PMi was less-steeply lengthened compared with flexion and scaption (Fig. 4C).

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Figure 4. Relationship between the lengthening of the lateral and medial fibers versus angle in each shoulder motion: (A) flexion, (B) scaption, and (C) external rotation at 90 degrees of abduction. The marker and bar in the relationship curves represent the mean lengthening and standard deviation, respectively.

A 2-way repeated-measures ANOVA showed significant differences in the maximum lengthening ratio among the 3 motions (F_2,32=14.52, P<.001). However, there was no significant difference between the 2 muscle fiber groups (F_1,16=1.43, P=.249). No significant interaction between passive shoulder motion and muscle fiber group was shown (F_2,32=0.07, P=.937). Post hoc tests showed that the lengthening ratios at 150 degrees of flexion and scaption were significantly greater than at 90 degrees of ER90 for both muscle fiber groups, although the difference between flexion and scaption was not significant (Tab. 1).

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Table 1. Lengthening Ratio (%) of the Lateral and Medial Muscle Fibers at the End Range of Each Shoulder Motiona

Lengthening Ratio During Stretching Techniques

There were significant differences in the lengthening ratio among the 3 stretching techniques (F_2,32=51.26, P<.001), whereas no significant difference between the 2 muscle fiber groups was shown (F_1,16=.19, P=.673). There was no interaction between stretching technique and muscle fiber group (F_2,32=2.45, P=.102). Of the 3 stretching techniques, the lengthening ratios during retraction-30 and horizontal abduction were significantly greater than that during retraction-0 for both muscle fiber groups (Tab. 2). The mean lengthening ratio during retraction-30 was largest, but this was not significantly different from horizontal abduction.

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Table 2. Lengthening Ratio (%) of the Lateral and Medial Muscle Fibers During Each Stretching Techniquea

Comparison of Lengthening Ratio Between Stretching Techniques and Shoulder Flexion

Of the 3 stretching techniques, retraction-30 and horizontal abduction, which showed greater lengthening ratios than retraction-0, were compared with 150 degrees of flexion. A significant difference in lengthening ratio among retraction-30, horizontal abduction, and 150 degrees of shoulder flexion was shown (F_2,32=9.08, P<.001). There was no significant interaction between these shoulder positions and muscle fiber group (F_2,32=0.10, P<.901). For retraction-30, although the post hoc test showed no significant difference compared with the lengthening ratio at 150 degrees of flexion in the lateral muscle fiber group, the lengthening ratio was significantly greater in the medial muscle fiber group (P<.05). For the horizontal abduction, the lengthening ratio was smaller than 150 degrees of shoulder flexion for both muscle fiber groups, but not significant.

Top Abstract Introduction Method Results Discussion Conclusion References

 
The PMi has been considered to be lengthened with scapular upward and external rotation and posterior tilting, which occur during shoulder elevation and external rotation at 90 degrees of abduction.⁸ These scapular motions are expected to move the coracoid process, which is the insertion of the PMi, superiorly and posteriorly, thereby increasing the distance between the origin and insertion of the muscle. Thus, the lengthening of the PMi might be estimated from the amount of the scapular motion or distance between its origin and insertion. However, anatomically, the PMi originates from different 3 ribs and converges into 1 muscle. Accurate measurement of the length of each of these muscles is difficult in vivo. Therefore, in order to determine the exact lengthening of this muscle, direct measurement is necessary. The measurement technique used in this study enabled us to measure the lengthening of the PMi directly.

This study demonstrated that 150 degrees of flexion and 150 degrees of scaption significantly lengthened the PMi compared with 90 degrees of ER90. In addition, the slope of the curve of the PMi length increased greatly with angle during flexion and scaption, whereas ER90 was lengthened gradually. These findings can be explained in terms of the scapular motions during flexion, scaption, and ER90. McClure et al⁸ observed larger scapular posterior tilting, upward rotation, and external rotation in flexion and scaption than in ER90.

The lengthening ratios in flexion and scaption were almost 50% for the lateral muscle fiber group and 40% for the medial muscle fiber group relative to the lengths in the neutral position. Muraki and colleagues^25,26 previously observed the lengthening of the rotator cuff muscles relative to the length in the same position as in this study. Of the rotator cuff muscles, the lower fibers of the subscapularis muscle were lengthened the most: 26.6% during external rotation at horizontal abduction. This difference in muscle lengthening patterns is interesting and is considered to come from anatomical features of these muscles. The PMi is located on the anterior part of the scapulothoracic joint and lengthened with scapular motion, whereas the subscapularis muscle originates from the subscapular fossa, inserting at the lesser tuberosity and being lengthened with humeral motion. Because the lengthening ratio of the PMi during scaption and flexion was greater than that of rotator cuff muscles, shortening of this muscle by contracture could restrict the scapular motion.

The 3 stretching techniques used were modified for this study. Evjenth and Hamberg²⁷ introduced scapular retraction with flexion as a selective stretching technique for the PMi in their textbook. However, they did not clearly describe the exact angle of shoulder flexion. The flexion angle was set to 30 degrees for 2 reasons. First, it is reasonable to stretch the muscle along muscle fiber direction, which is close to 30 degrees relative to the coronal plane, as this has been shown to lengthen fibers the most. Second, approximately 90 degrees of flexion causes pain in a patient with subacromial impingement. Therefore, 30 degrees of flexion is considered to be more comfortable than a higher angle of flexion, as well as the angle closest to the line of force.

As we expected, retraction-30 greatly lengthened the PMi compared to retraction-0. In comparison with the lengthening ratio at 150 degrees of flexion, this technique significantly lengthened the medial and lateral muscle fiber groups. These findings indicate that retraction-30 is useful for maintaining or obtaining the PMi length necessary to reach 150 degrees of flexion.

Horizontal abduction also significantly lengthened the PMi. In a previous study,²⁴ self-stretching by horizontal abduction was reported to stretch the PMi more than scapular retraction with the arm at the side (0° of flexion) or 90 degrees of external rotation at 90 degrees of abduction. This stretching technique often is included in rehabilitation programs for patients with subacromial impingement.^19–21 However, in terms of the comparison of the lengthening at 150 degrees of flexion, this technique did not stretch the PMi as much as retraction-30. In addition, the average lengthening during this technique was somewhat less than lengthening obtained at 150 degrees of flexion. Therefore, the effect of the horizontal abduction on the PMi might be less than retraction-30.

Our findings demonstrated that retraction-0 lengthened the PMi approximately half as much as other techniques. Scapular retraction in the supine position with the arm at the side has classically been used to test the length of the PMi.¹⁸ Such a result seems reasonable because this retraction shifts the coracoid process, the insertion of the PMi, posteriorly relative to the thorax. However, posterior shift of the coracoid process alone might be insufficient to stretch the PMi.

The PMi showed little change in length at lower shoulder flexion angles because the coracoid process did not move superiorly. Particularly until 30 degrees of shoulder flexion was reached, previous studies^8,28 showed little scapular and clavicular motions. The PMi actually started lengthening from 30 degrees of flexion. Furthermore, horizontal abduction lengthened the muscle similarly to retraction-30. This finding may suggest the importance of moving the coracoid process posteriorly as well as superiorly. Thus, we believe that applying passive force to the scapula in both superior and posterior directions, as with retraction-30, is the most effective maneuver to stretch the PMi because it appeared to be consistent with the traditional concept of increase in the distance between the origin and insertion of the muscle.

Limitations

The limitations of this study should be considered. First, shoulder joint motion in this experiment may differ from in vivo motion, as a cadaveric shoulder was used. According to previous data,^29,30 the scapular motion was small up to 30 degrees, but greatly increased after that during scaption, similar to our lengthening data. This study might be able to simulate the in vivo motion properly.

Second, this study did not determine tensile properties on the PMi. Therefore, altered viscoelastic and other material behaviors of cadaver muscle, which are reported to be quite different from those of muscles in vivo, were not accounted for. Gottsauner-Wolf et al³¹ and Leitschuh et al³² compared the tensile properties of muscle immediately after death and in frozen and thawed specimens. Breaking strength and stiffness of frozen and thawed specimens were 50% to 60%, respectively, of those in specimens taken immediately after death. Furthermore, Van Ee et al³³ compared the tensile properties of muscles before and after postmortem rigor. There were no differences in breaking strength or stiffness; however, toe regions of postmortem muscles were elongated compared with muscles before rigor mortis. In this study, we kept specimens at room temperature after thawing for longer than 6 hours, and they were preconditioned with 10 repetitions of joint stretching in each direction before the experiment.

Third, the pectoralis major muscle and clavi-pectoral fascia were removed in order to expose the PMi. It is possible that the tension of the pectoralis major muscle restricts scapular motions, while the clavi-pectoral fascia is thought to have a role in holding the PMi; therefore, removal of these tissues might affect the behavior of the muscle.

Finally, there was little spinal motion during shoulder motion because the specimen was secured at the thoracic spine. The motion of the thoracic spine, which is the base of the PMi, could affect lengthening. However, the spinal motion during flexion and scaption from 0 degrees to 150 degrees is small.³⁴ The influence of the spinal motion also was considered to be small.

Top Abstract Introduction Method Results Discussion Conclusion References

 
This study utilizing fresh transthoracic specimens suggests that significant lengthening of the PMi is observed during shoulder motions, especially flexion and scaption. Based on our findings, scapular retraction at 30 degrees of flexion is the stretching technique that causes the greatest change in the length of the PMi. Clinically, this study suggests the importance of the PMi in shoulder motion and provides the anatomical and biomechanical background for choosing the appropriate stretching techniques. Although the amount of the passive lengthening in the PMi in vitro was estimated by this experiment, the effectiveness of these techniques on muscle in vivo was not studied. This issue should be investigated in further studies.

 
Dr Muraki and Dr Aoki provided concept/idea/research design. Dr Muraki provided writing and data analysis. Dr Muraki, Mr Izumi, Ms Fujii, and Ms Hidaka provided data collection. Dr Aoki provided project management. Dr Miyamoto provided facilities/equipment and consultation (including review of manuscript before submission). The authors thank Dr Haruyuki Tatsumi, Dr Gen Murakami, Dr Eiichi Uchiyama, and Dr Daisuke Suzuki for their assistance in the collection of specimens. They also thank Hiroshi Takasaki, Sadanori Ohshiro, and Hitoshi Miyamoto for their assistance during the experiment.

This study was performed in the Department of Physical Therapy and the Department of Anatomy, Sapporo Medical University, as a thesis of the Graduate School of Health Sciences.

An oral presentation of this research was given at the International Congress of the World Confederation for Physical Therapy; June 2–6, 2007; Vancouver, British Columbia, Canada.

^* LEVEX, Fujikogyo Bldg 2f 102, Minamimachi, Shichijogoshonouchi, Shimogyo-Ku, Kyoto, Japan.

Allied Control Co Ltd, 3-5-5, Sotokanda, Chiyoda-Ku, Tokyo 101-0021 Japan.

SAS Institute Inc, PO Box 8000, Cary, NC 60606.

Top Abstract Introduction Method Results Discussion Conclusion References

 

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				T. S. Ellenbecker and A. Cools Rehabilitation of shoulder impingement syndrome and rotator cuff injuries: an evidence-based review Br. J. Sports Med., April 1, 2010; 44(5): 319 - 327. [Abstract] [Full Text] [PDF]

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