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Effects of a stretching protocol for the pectoralis minor on muscle length, function, and scapular kinematics in individuals with and without shoulder pain
Journal of Hand Therapy xxx (2016) 1e9
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Scientific/Clinical Article
Effects of a stretching protocol for the pectoralis minor on muscle length, function, and scapular kinematics in individuals with and without shoulder pain Dayana P. Rosa PT, MS a, John D. Borstad PT, PhD b, Lívia S. Pogetti PT, MS c, Paula R. Camargo PT, PhD c, * a
Physical Therapist, Master of Physical Therapy Program, Methodist University of Piracicaba, Piracicaba, SP, Brazil Associate Professor, Physical Therapy Division, The Ohio State University, Columbus, OH, USA c Physical Therapist, Adjunct Professor, Physical Therapy Department, Federal University of São Carlos, São Carlos, SP, Brazil b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 April 2015 Received in revised form 9 May 2016 Accepted 17 June 2016 Available online xxx
Study Design: Parallel-group intervention with repeated measures. Introduction: Shortening of the pectoralis minor (PM) may contribute to alterations in scapular kinematics. Purpose of the Study: To evaluate the effects of a stretching protocol on function, muscle length, and scapular kinematics in subjects with and without shoulder pain. Methods: A sample of 25 patients with shoulder pain and 25 healthy subjects with PM tightness performed a daily stretching protocol for 6 weeks. Outcome measures included Disabilities of the Arm, Shoulder, and Hand questionnaire, PM length, and scapular kinematics. Results: Disabilities of the Arm, Shoulder, and Hand scores decreased (P < .05) in the patient group at post-intervention. No differences (P > .05) were found for PM length in both groups. Scapular anterior tilt increased (P < .05) at 90 of flexion in the healthy group. Discussion: This study demonstrated that a daily home stretching protocol significantly decreases pain and improves function in subjects with shoulder pain. The mechanism responsible for these improvements does not appear directly related to PM muscle length or scapula kinematics, suggesting that other neuromuscular mechanisms are involved. Conclusion: The PM stretching protocol did not change the PM length or scapular kinematics in subjects with or without shoulder pain. However, pain and function of the upper limbs improved in patients with shoulder pain. Level of Evidence: 2b. Ó 2016 Hanley & Belfus, an imprint of Elsevier Inc. All rights reserved.
Keywords: Physical therapy Scapula Shortening Shoulder impingement syndrome
Introduction Shoulder impingement syndrome (SIS) represents 44%-65% of all cases of shoulder pain1,2 and may be related to abnormal shoulder kinematics.3-10 In individuals with SIS, alterations in scapular kinematics have been described as a possible consequence Funding: This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (2012/20305-8 and 2013/50363-2). Conflict of interest: All named authors affirm that they have no financial affiliation or involvement with any commercial organization that has a direct financial interest in any matter included in this article, except as disclosed in an attachment and cited in the article. Any other conflict of interest (ie, personal associations or involvement as a director, officer, or expert witness) is also disclosed in the attachment. This study was registered at ClinicalTrials.gov: identifier NCT01956240. * Corresponding author. Universidade Federal de São Carlos, Departamento de Fisioterapia, Rodovia Washington Luís, Km 235, 13565-905 São Carlos, SP, Brazil. Tel.: þ55 16 3306 6696; fax: þ55 16 3361 2081. E-mail address: [email protected] (P.R. Camargo).
of pectoralis minor (PM) tightness,5,11 posterior capsule tightness,7,12 changes in activity of the scapular and rotator cuff muscles,5,13 and/or repetitive overhead activity.6,14 The PM is the only scapulothoracic muscle with both origin and insertion anterior to the scapula.11,15 The fiber orientation of the PM muscle favors scapular internal rotation (IR), downward rotation, and anterior tilt (AT), and for this reason, it is considered an antagonist to the necessary scapular motions during arm elevation.3,5,11,13 Relative to subjects with greater PM length, healthy subjects with a short PM had increased scapular IR and decreased scapular posterior tilt (PT) during arm elevation,11 similar to the alterations described in subjects with SIS.4,5,16,17 These scapular kinematic alterations support a potential relationship between PM shortening and SIS. Muscle length will decrease through loss of sarcomeres in series when immobilized at a shorter length.18-21 A shortened muscle will also demonstrate increased passive tension as it elongates,22,23 limiting full joint motion.11,22 There is also a
0894-1130/$ e see front matter Ó 2016 Hanley & Belfus, an imprint of Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jht.2016.06.006
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greater percentage of connective tissue in immobilized muscle that further increases passive tension.23 Changes in posture that approximate the origin and insertion of muscle may also result in decreased length,22,24,25 although empirical evidence for this phenomenon is lacking. Based on these muscle adaptations, it is hypothesized that the forward shoulder posture commonly observed in the clinical setting may lead to decreased PM length.26-28 With increased passive tension in the PM secondary to decreased resting length, the normal scapular motions of upward rotation (UR), external rotation (ER), and PT that occur during arm elevation may be restricted and contribute to shoulder dysfunction.11,28 As such, people with shoulder pain and PM tightness may benefit from interventions to improve PM muscle flexibility. PM stretching is often included in comprehensive rehabilitation strategies for individuals with SIS.29-32 However, because PM stretching is typically one of many techniques applied, it is difficult to determine the direct beneficial effect it has on movement, function, and symptoms in subjects with SIS. Therefore, the purpose of this study was to evaluate the effects of a standard PM stretching protocol on muscle length, pain, function, and scapular kinematics in subjects with PM tightness with or without shoulder pain. We hypothesized that PM stretching would increase PM resting length and scapular UR, ER, and PT during arm elevation in all subjects. We also hypothesized that PM stretching would decrease pain and improve function in subjects with shoulder pain.
Methods A total of 100 subjects with or without shoulder pain were initially recruited and evaluated for eligibility, and 78 subjects with PM tightness were included in the study. Fifty subjects (25 patients with shoulder pain and 25 healthy subjects) completed the study (Fig. 1). The participation of all subjects was voluntary, and no incentives were given to encourage enrollment. Each group was considered separately using a within-group repeatedmeasures design. To detect clinically meaningful angular change of 5 in scapular kinematics and achieve a statistical significance level of .05 with a power of 0.80, 25 subjects per group were required.11,33 The clinically meaningful angular change of 5 was selected to be larger than the standard measurement error for scapular kinematics from a recent study in our laboratory, with between-day error ranging from 2.7 to 4.9 in asymptomatic subjects and from 3.1 to 3.8 in subjects with SIS.34 Fliers posted in the local university setting and surrounding community were used to recruit individuals with shoulder pain. Healthy individuals were recruited through personal contacts of the investigators. A healthy group was included to determine the effect of stretching on PM length and scapular kinematics without the additional influence of pain. Individuals with shoulder pain were required to present with at least 1 week of symptoms consistent with SIS using a combination of criteria shown to maximize diagnostic accuracy.35 Subjects were also required to have active arm elevation close to 150 as
Fig. 1. Flow diagram representing enrollment, allocation, procedures, and analysis for both groups.
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determined by digital inclinometer to ensure that scapular kinematic data were captured over the painful arc for impingement.34,36,37 The diagnosis for SIS was made based on a clinical examination and self-reported history.29,34,35,37 SIS was considered to be present when at least 3 of the following signs or symptoms were noted29,32,34,37-39: positive Neer test,40 positive Hawkins test,30 positive Jobe test,41 pain with passive or isometric resisted shoulder ER,31,42,43 pain with active shoulder elevation,44 and pain in the anterolateral shoulder region.5,8,29,45,46 Healthy subjects were excluded if they had any of the positive signs and symptoms for SIS noted previously. Individuals from either group were excluded if they were pregnant; demonstrated glenohumeral joint ligamentous laxity based on a positive sulcus,47,48 an apprehension,49 or an anterior drawer test8; reported a history of traumatic shoulder pathology, fracture, or shoulder surgery; had a history of adhesive capsulitis, scoliosis, or systemic illnesses; had a body mass index of greater than 28 kg/m2 because higher indexes may increase error through skin motion artifact during kinematics data collection; were allergic to transpore tape; or had received physical therapy treatment in the last 6 months, to have no influence from recent interventions.32 Individuals from both groups also had to present with shortened PM muscle length as determined with the pectoralis minor index (PMI) and the methods described by Borstad and Ludewig.11 Pilot data from 12 healthy subjects (6 women and 6 men; 26.58 4.5 years; 66.58 11.86 kg; 1.69 0.08 m) were used to determine the PMI for the present study using an established formula ([(muscle length [cm]/height [cm]) 100]).11 PM length was measured with a tape measure and considered relatively short when the PMI was less than 1 standard deviation below the mean PMI (10.54 cm) calculated using pilot data.11,28,50,51 Thus, in the present study, individuals were classified with shortened PM if their PMI was below 9.93. The study was approved by the Ethics Committee of the University (protocol number 100/12) and registered at ClinicalTrials.gov (registration number, NCT01956240). The data collection was performed in the Laboratory of Analysis and Intervention of the Shoulder Complex at Federal University of São Carlos. All subjects gave their written and informed consent to participate in this study, which was conducted according to the Helsinki statement. Only the symptomatic shoulder was evaluated in the shoulder pain group. For healthy participants with bilateral shortening, the side evaluated was randomly determined using a computergenerated randomization list.
PM length assessment PM length was measured in both the resting and shoulder retraction positions using a tape measure with 0.10-cm resolution. All measurements were taken by the primary investigator who was
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blinded to the result by covering the side of the tape measure facing them with adhesive tape. A second examiner then read the result and recorded the measurement values. The caudal edge of the fourth rib at the sternum and the inferomedial aspect of the coracoid process were palpated, marked with a pencil, and used to represent PM length, as suggested by Borstad and Ludewig.11 The distance between these landmarks was measured twice with 2 minutes between trials. During the resting position measurements (Fig. 2A), participants were asked to remain in a relaxed posture with the arms at the side in a neutral position, avoid postural correction, and exhale just before the measurement. The pencil marks were removed after each measurement. The intrarater reliability (intraclass correlation coefficient [ICC] ¼ 0.950.97; standard error of measurement [SEM] ¼ 0.31-0.42 cm), interrater reliability (ICC ¼ 0.86-0.87; SEM ¼ 0.70-0.84 cm), and between-days reliability (ICC ¼ 0.95; SEM ¼ 0.40-0.41 cm) of this measurement was established in a previous study for subjects with and without shoulder pain.32 To evaluate the PM length in the retraction position, individuals performed scapular retraction and held this position as the primary investigator measured the muscle length (Fig. 2B). The measurement in this position was also taken twice, and the second examiner recorded the values.
Disabilities of the Arm, Shoulder, and Hand questionnaire The Brazilian version of the Disabilities of the Arm, Shoulder, and Hand (DASH) questionnaire was used to evaluate upper limb physical function and symptoms.52 The DASH self-assessment questionnaire contains 30 questions, and a maximum score of 100 indicates the worst possible condition.53 This questionnaire is reliable, valid, and responsive52,54 and has been widely used in individuals with SIS.34,38,55
Three-dimensional scapular kinematics For 3-dimensional scapular kinematics, Flock of Birds (miniBird) hardware (Ascension Technology Corporation, Burlington, VT) integrated with MotionMonitor software (Innovative Sports Training, Inc, Chicago, IL) was used for data capture and analysis.11,34,37,56 The tridimensional position and orientation of 3 sensors were tracked simultaneously at a sampling rate of 100 Hz. Sensors were secured to subjects’ skin with double-sided adhesive tape and transpore tape to the sternum, the acromion of the scapula, and a thermoplastic cuff secured to the distal humerus. The subject stood with the arms relaxed at the side in a neutral position with the transmitter directly behind the shoulder tested, whereas bony landmarks on the thorax, scapula, and humerus were palpated and
Fig. 2. Measurement of pectoralis minor length: distance between coracoid process (white arrow) and fourth rib (black arrow) taken with a tape measure on (A) resting and (B) retraction positions.
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digitized to allow transformation of the sensor data to local anatomically based coordinate systems. Local coordinate systems were established for the trunk, scapula, and humerus as recommended by the International Society of Biomechanics.57 For all local coordinate systems, the z-axis pointed laterally, x-axis anteriorly, and y-axis superiorly. The YX0 Z00 Euler sequence57 was used to describe scapular motions relative to the trunk in the sequence of IR/ER, UR/downward rotation, and AT/PT. Humeral orientation with reference to the trunk was determined using the YX0 Y00 Euler sequence, which defines the plane of elevation, elevation, and IR/ER.
Procedure Kinematic data were collected with the subjects in a relaxed standing position. Subjects elevated their arm from a dependent position through their full range of motion at a speed such that it took around 3 seconds to elevate their arm and 3 seconds to lower it. Subjects maintained light fingertip contact with a flat planar surface, and their thumb pointed superiorly during these motions to maintain a consistent positioning of the arm in the sagittal plane. Data were collected during 3 consecutive repetitions. This procedure has been shown to be reliable in healthy subjects and subjects with shoulder impingement symptoms.34 All measurements were taken by the primary investigator.
Intervention Both groups performed a daily PM stretching protocol for 6 weeks.58,59 The protocol consisted of 4 repetitions of 1-minute stretches with a 30-second interval between repetitions.58,59 A minimum of 4 minutes of stretching to decrease muscle passive resistance is recommended.59 The subjects were instructed by a physical therapist to perform a unilateral corner stretch using a wall (Fig. 3). The starting position for this stretch is with the individual in the standing position, 90 of arm abduction, 90 of elbow flexion, and the palmar surface of the hand on the wall. The contralateral leg to the shoulder being stretched was positioned forward of the other leg. To apply the stretch, the trunk is shifted forward and rotated opposite to the side being stretched.50 This stretch position resulted in the largest separation between the fourth rib and coracoid process landmarks when compared with sitting and supine manual PM stretches.50 The stretching protocol was performed at home. The physical therapist was available to answer questions or clarify procedures during the intervention period and contacted the individuals weekly to remind them to do the protocol. A daily exercise log to record compliance and a picture of the stretch were given to participants. At the end of the 6 weeks, all participants returned the log to the investigators. Individuals were included in the data analysis if they performed at least 4 weeks of stretching as this time is described as the minimal period to achieve a decrease in muscle passive resistance.59 Two baseline evaluations were performed 1 week apart before the intervention. The follow-up evaluation was performed immediately after completion of the 6-week stretch protocol (evaluation 3). The double baseline design was used to assure stability of the dependent variables before the intervention. DASH, PM muscle length, and scapular kinematics were assessed at each evaluation. The DASH was also evaluated in the healthy group to evaluate whether PM stretching, as would be done preventively, could provoke shoulder region irritation.
Fig. 3. Unilateral corner stretch.
Statistical analysis Adherence was quantified as the number of days in which a participant performed the stretching protocol, and descriptive data were calculated. The data were analyzed using the SPSS statistical package (17.0 version; SPSS, Chicago, IL). Normality was evaluated by Kolmogorov-Smirnov test, and it was violated for DASH questionnaire (P < .05). Thus, the Friedman test with Wilcoxon post hoc tests was used to verify differences between evaluations within each group for the questionnaire. If significant differences were revealed, a Bonferroni adjustment to the a level was calculated. As 3 comparisons were performed, a P value of less than .016 (0.05/3) was adopted to be more conservative in identifying differences between evaluations for the questionnaire score. For PM length in both the resting and retraction positions, a 2way repeated-measures analysis of variance was used to test interactions of group (healthy and shoulder pain) evaluation (1, 2, and 3) and for main effects of group or evaluation. Scapular kinematic data at rest and at humerothoracic elevation angles of 30 ,
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60 , 90 , and 120 were selected for analysis. For scapular IR, UR, and PT, separate 2-way repeated-measures analyses of variance with Bonferroni post hoc tests were used to test for interactions of angle (rest, 30 , 60 , 90 , and 120 ) evaluation (1, 2, and 3), and for main effects of evaluation. For scapula kinematics, the groups were analyzed separately. A P value of less than .05 was considered statistically significant. Intragroup effect sizes (ESs) for all quantitative variables were calculated using Cohen d coefficient.60 The periods evaluated were paired as following: baseline 2-baseline 1, follow-up-baseline 1, and follow-up-baseline 2. An ES greater than 0.8 was considered large, around 0.5 moderate, and less than 0.2 small. The ES was very small between baseline 2 and 1 and very similar between the follow-up and both baselines. Based on this result, the Cohen d coefficients presented later are only between the follow-up and baseline 2. Results The descriptive data of the individuals are shown in Table 1. The average stretching protocol compliance was 41.20 9.22 days (5.9 weeks) and 40.32 8.28 days (5.8 weeks) for the healthy and shoulder pain groups, respectively. This variability in compliance was due primarily to personal schedules of the individuals. Some subjects performed more than 42 days of stretching to match their schedule with the follow-up appointment. Figure 1 shows that 27 subjects did not complete the stretching protocol. The main reasons given by subjects for dropping out were pain during stretching, improvement in pain before the end of the 6 weeks’ protocol, and personal factors. Table 2 shows the results for the DASH and length of the PM for both groups at each assessment. The healthy group did not demonstrate statistically significant differences (P > .016) across assessments for the DASH. The ES was small for this questionnaire (Cohen d, 0.06). The shoulder pain group showed reduced DASH score at followup compared with baselines 1 and 2 (P ¼ .001 and .004, respectively) and a large (Cohen d, 0.83) ES were observed for the questionnaire. Neither statistically significant interactions between group and evaluation were observed nor a statistically significant main effect of group and evaluation for PM length in the resting (F ¼ 0.18 and P ¼ .84; F ¼ 0.71 and P ¼ .40; F ¼ 8.65 and P ¼ .05, respectively, Table 2) or retraction positions (F ¼ 0.88 and P ¼ .39; F ¼ 0.76 and P ¼ .38; F ¼ 1.39 and P ¼ .25, respectively, Table 2) was observed. Cohen d coefficients showed small effects of the stretch protocol (Cohen d, 0.006-0.21) for both groups in all comparisons. Scapular kinematics Healthy group For the healthy group, neither a statistically significant interaction between angle and time was observed nor a statistically significant
Table 1 Descriptive data of the individuals Variable
Healthy group (n ¼ 25)
Shoulder pain group (n ¼ 25)
P
Gender Age (y)a Height (m)a Weight (kg)a BMI (kg/m2)a Evaluated shoulder
13 women; 12 men 25.76 6.95 1.69 0.08 64.12 10.76 22.30 2.56 13 dominant; 12 nondominant d
14 women; 11 men 26.96 5.79 1.69 0.07 67.54 9.68 24.42 5.75 18 dominant; 7 nondominant 42.32 64.54
d .51 .80 .24 .09 d
Duration of pain (mo)a
BMI ¼ body mass index. a Values are mean standard deviation.
d
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main effect of time for scapular IR (Fig. 4A) (F ¼ 0.32 and P ¼ .95; F ¼ 1.37 and P ¼ .26, respectively) or scapular UR (Fig. 4B) (F ¼ 1.20 and P ¼ .32; F ¼ 2.61 and P ¼ .08, respectively) during arm elevation was observed. A statistically significant angle time interaction effect was determined (F ¼ 2.97 and P ¼ .003) for scapular PT (Fig. 4C), where at 90 of arm elevation, there was decreased scapular PT at follow-up when compared with baseline 2 (P ¼ .02). The ESs in the healthy group were small for IR (Cohen d, 0.05 to 0.10). For scapular UR, the ESs were moderate (Cohen d, w0.50). For scapular PT, this group showed small ES at rest, 30 , and 60 of arm elevation (Cohen d, 0.30 to 0.09) and moderate ES at 90 and 120 of arm elevation (Cohen d, 0.50). Shoulder pain group For the shoulder pain group, there were no statistically significant interaction effects between angle and time and no main effect of time for scapular IR (Fig. 4A) (F ¼ 1.21 and P ¼ .32; F ¼ 2.94 and P ¼ .06, respectively), scapular UR (Fig. 4B) (F ¼ 0.51 and P ¼ .84; F ¼ 1.50 and P ¼ .24, respectively), or PT of the scapula (Fig. 4C) (F ¼ 0.83 and P ¼ .58; F ¼ 0.42 and P ¼ .66, respectively) during arm elevation. The ESs for scapular rotations in the shoulder pain group were small for IR (Cohen d, 0.32 to 0.21). For scapular UR, the ESs were small (Cohen d, 0.20) except at 30 of arm elevation with moderate ES (Cohen d, w0.50). For scapular PT, the group showed small ES (Cohen d, 0.36 to 0.002).
Discussion This study evaluated the effects of a daily stretching protocol for the PM on muscle length, function, and scapular kinematics in individuals with and without shoulder pain. Our results showed that PM stretching decreased pain and improved function in subjects with shoulder pain but was not effective at changing the PM length or scapular kinematics. Different techniques to stretch the PM are used in clinical practice, but the most effective technique is unknown. Borstad and Ludewig50 compared 3 techniques and concluded that the unilateral self-stretch was better than the supine or sitting manual stretch techniques to increase the distance between the origin and insertion of the PM.48 The DASH questionnaire revealed a decrease in pain and improvement in function in the shoulder pain group, despite the low scores reported at the beginning of the study. Although the DASH score decreased 10.37 points in the present study, it was just shy of reaching the 10.7-point minimal detectable change (MDC) reported by Franchignoni et al.61 However, the large ES after the intervention suggests that stretching contributed to the change in pain and function of the upper limbs. Decreased muscle length may lead to loss of extensibility due to decreased number of sarcomeres in series, fewer actin-myosin crossbridges,21 the type of titin protein, and shortening of connective tissue.62-64 Shortening of connective tissue has been described as a possible cause of pain.47 We propose that the stretching protocol applied in the present study may have positively affected pain by decreasing muscle passive resistance,3,65 improving connective tissue extensibility,66 and influencing neural activation patterns.67 The PM shortening was determined as previously described by Borstad and Ludewig,11 and it has been used in some recent studies.28,51,68-73 A threshold of shortening has not been determined yet, so it is recommended that it should be calculated for the sample in each study.11 In the present study, 85% of the sample presented muscle shortening. Although this number seems to be high, it is believed that the PMI adopted was appropriate to classify
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Table 2 Results of DASH questionnaire and pectoralis minor length for healthy and shoulder pain groups Outcome measure Healthy group (n ¼ 25) DASH Muscle lengthdrest (cm) Muscle lengthdretraction (cm) Shoulder pain group (n ¼ 25) DASH Muscle lengthdrest (cm) Muscle lengthdretraction (cm)
Baseline 1
Baseline 2
Follow-up
3.46 4.22 (1.72-5.21) 15.99 1.35 (15.44-16.56) 17.33 1.47 (16.73-17.94)
2.63 4.02 (0.97-4.29) 16.19 1.45 (15.59-16.79) 17.43 1.48 (16.81-18.03)
2.86 3.90 (1.25-4.47) 16.38 1.46 (15.78-16.98) 17.44 2.33 (16.47-18.40)
17.36 11.68 (13.49-22.76) 16.36 1.57 (15.72-17.01) 17.65 2.03 (16.81-18.48)
15.83 12.30 (11.18-21.08) 16.47 1.75 (15.75-17.20) 17.68 1.74 (16.96-18.40)
7.94 7.82a (4.71-11.17) 16.87 1.90 (6.08-17.65) 18.26 1.86 (17.49-19.03)
DASH ¼ Disabilities of the Arm, Shoulder, and Hand. Results are mean standard deviation (95% confidence interval). a P < .016, when compared with baselines 1 and 2.
individuals with muscle shortening, considering that the groups were very similar for all baseline variables. The mean change in PM resting length after the stretching protocol in individuals with shoulder pain was þ0.51 cm, with a small ES. This change in length is close to the SEM (0.41 cm) for measurements between days in individuals with shoulder pain determined in a previous study. The MDC (1.14 cm) was also determined in the previous study,70 with the intent of identifying the change in PM length that represents a real change. Because the mean change of 0.51 cm is smaller than the MDC, the increase in PM
length measured at follow-up does not represent a real alteration in muscle length after stretching. Changes in scapular kinematics were not observed after the intervention in the present study. This result does not support our hypothesis that scapular ER, UR, and PT would be increased after the stretching protocol in those with a relatively short PM. Other studies have assessed scapular kinematics after an intervention combining PM stretching with scapular and rotator cuff muscle strengthening and manual therapy techniques in individuals with SIS,30,36,39,43 but the results are equivocal. One possible
Fig. 4. Mean of scapular (A) internal and (B) upward rotations and (C) posterior tilt. During arm elevation for (left) healthy and (right) shoulder pain groups at all assessments. The error bars are standard error of mean. *P ¼ .02, when compared with baseline 1.
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explanation for the lack of change in kinematics in the present study is that the home-based intervention may not have maximized PM muscle elongation as much as a therapist-applied stretch may have. It is also possible that PM length has only a minor contribution to kinematics so that stretching can only impart a limited effect on motion. Because scapular kinematics represent a complex combination of muscle activation, motor control, and soft tissue variables, an intervention to alter only 1 variable may not be sufficient to change kinematics perceptibly. It is possible that adding the right strengthening exercises to the stretching protocol may positively alter scapular kinematics. Our purpose was to evaluate the effect of PM stretching independent of other interventions, and the results suggest that stretching PM alone is not enough to modify kinematics. Borstad and Ludewig11 reported scapula kinematic differences for IR and PT only in subjects distinguished by relatively short and long PM length. The lack of change in scapula UR in the present study suggests that the PM length has minimal influence on scapula UR during arm elevation. Borstad and Ludewig50 also suggested that the stretching technique performed in this study may favor increased PT of the scapula. However, the present study showed only decreased PT at 90 of arm elevation for the healthy group after stretching, whereas no differences were observed in the shoulder pain group. This change was not considered clinically relevant because the ES was moderate (Cohen d, w0.50), and the w3 change was below the clinically meaningful angular change adopted in this study (5 ). Other studies have reported similar changes in scapular tilt after interventions in subjects with and without pain. Haik et al37 reported increased scapular AT after thoracic manipulation in healthy subjects with a small ES. A recent randomized controlled trial also showed more AT in subjects with shoulder pain after a strengthening and stretching intervention, with a small ES for scapular tilting also reported.74 It is important to note that the lack of change in PM muscle length in the retraction position also helps explain the lack of scapular kinematic changes. This result suggests that PM length change during a dynamic motion was not influenced by stretching, implying that passive resistance from PM during arm elevation continues to influence scapular kinematics.11,13,28 As the present study is the first study to evaluate the independent effects of PM stretching on scapular kinematics, additional studies are necessary to determine the real influence of PM length on scapular motion. The placebo effect may have contributed to the decreased pain and increased function reported in this study. When the potential benefits of an intervention are explained to participants, their expectations about these benefits may influence postintervention assessments.75 Although incomplete information about the objectives of this study was given to participants, expectations for improvement may have influenced the results. Specifically, a placebo effect may explain the significant decrease in pain and improved function in the patient group, despite the lack of meaningful biomechanical changes. Although the hypothesized biomechanical changes were not observed, the present study demonstrates an important finding relative to clinical practice. This study demonstrated that a simple stretching protocol performed daily at home can significantly decrease pain and improve the function in subjects with shoulder pain. This stretch intervention can be easily prescribed to individuals with shoulder pain. The mechanism whereby a simple stretch decreases pain and improves function does not appear directly related to PM muscle length or scapula kinematics, suggesting that other neuromuscular mechanisms or improved
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subjective tolerance76 are involved. Of note is that the mean duration of pain in the patient group was 42 months, and perhaps stretching alters mechanoreception such that pain intensity is modified in individuals with chronic musculoskeletal symptoms. It is possible that the participants may not have maximally elongated PM during the stretch, either by ineffective shoulder positioning or by pain avoidance. A therapist-applied stretch may have been more effective at ensuring that PM length was optimal and that forces were maintained during stretching. A recognized limitation is that linear measurements such as the one used to quantify PM length in this study cannot represent real structural changes of muscle after a stretching protocol. Similarly, the PM length may be influenced by a subject’s posture during the measurements. Between-day reliability estimates are excellent for this measurement and should minimize this concern. Subjects with shoulder pain in this study reported a mean pain duration of 42 months, limiting the application of these findings to a more acute clinical population. Future investigations should evaluate the effects of other PM stretch techniques on PM length, shoulder function, and pain. Considering that linear measurements may not represent real structural changes in muscle after stretching, it would be beneficial to incorporate imaging that can evaluate these potential tissue adaptations in future studies. The randomized controlled trial is also needed to confirm the results from the present study. Conclusion The findings of this study showed that daily PM stretching performed at home was effective in decreasing pain and improving function in individuals with shoulder pain but did not change PM length or scapular kinematics during arm elevation in subjects with or without shoulder pain. Acknowledgments The authors thank the volunteers who participated in this study and Rafael Foroni Luchesi and Letícia Bergamin Januário for helping in data collection. References 1. Bruls VE, Bastiaenen CH, de Bie RA. Non-traumatic arm, neck and shoulder complaints: prevalence, course and prognosis in a Dutch university population. BMC Musculoskelet Disord. 2013;14:8. 2. van der Windt DA, Koes BW, de Jong BA, Bouter LM. Shoulder disorders in general practice: incidence, patient characteristics, and management. Ann Rheum Dis. 1995;54:959e964. 3. Taylor DC, Dalton Jr JD, Seaber AV, Garrett Jr WE. Viscoelastic properties of muscle-tendon units. The biomechanical effects of stretching. Am J Sports Med. 1990;18:300e309. 4. Lukasiewicz AC, McClure P, Michener L, Pratt N, Sennett B. Comparison of 3dimensional scapular position and orientation between subjects with and without shoulder impingement. J Orthop Sports Phys Ther. 1999;29:574e583. discussion 584-576. 5. Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther. 2000;80:276e291. 6. Laudner KG, Myers JB, Pasquale MR, Bradley JP, Lephart SM. Scapular dysfunction in throwers with pathologic internal impingement. J Orthop Sports Phys Ther. 2006;36:485e494. 7. Lin JJ, Lim HK, Yang JL. Effect of shoulder tightness on glenohumeral translation, scapular kinematics, and scapulohumeral rhythm in subjects with stiff shoulders. J Orthop Res. 2006;24:1044e1051. 8. McClure PW, Michener LA, Karduna AR. Shoulder function and 3-dimensional scapular kinematics in people with and without shoulder impingement syndrome. Phys Ther. 2006;86:1075e1090.
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9. Ogston JB, Ludewig PM. Differences in 3-dimensional shoulder kinematics between persons with multidirectional instability and asymptomatic controls. Am J Sports Med. 2007;35:1361e1370. 10. Ludewig PM, Reynolds JF. The association of scapular kinematics and glenohumeral joint pathologies. J Orthop Sports Phys Ther. 2009;39:90e104. 11. 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;35:227e238. 12. Bach HG, Goldberg BA. Posterior capsular contracture of the shoulder. J Am Acad Orthop Surg. 2006;14:265e277. 13. Phadke V, Camargo P, Ludewig P. Scapular and rotator cuff muscle activity during arm elevation: a review of normal function and alterations with shoulder impingement. Rev Bras Fisioter. 2009;13:1e9. 14. Ribeiro A, Pascoal AG. Resting scapular posture in healthy overhead throwing athletes. Man Ther. 2013;18:547e550. 15. Muraki T, Aoki M, Izumi T, Fujii M, Hidaka E, Miyamoto S. Lengthening of the pectoralis minor muscle during passive shoulder motions and stretching techniques: a cadaveric biomechanical study. Phys Ther. 2009;89:333e341. 16. Warner JJ, Micheli LJ, Arslanian LE, Kennedy J, Kennedy R. Scapulothoracic motion in normal shoulders and shoulders with glenohumeral instability and impingement syndrome. A study using Moire topographic analysis. Clin Orthop Relat Res. 1992;285:191e199. 17. Endo K, Ikata T, Katoh S, Takeda Y. Radiographic assessment of scapular rotational tilt in chronic shoulder impingement syndrome. J Orthop Sci. 2001;6:3e10. 18. Tabary JC, Tabary C, Tardieu C, Tardieu G, Goldspink G. Physiological and structural changes in the cat’s soleus muscle due to immobilization at different lengths by plaster casts. J Physiol. 1972;224:231e244. 19. Goldspink G, Tabary C, Tabary JC, Tardieu C, Tardieu G. Effect of denervation on the adaptation of sarcomere number and muscle extensibility to the functional length of the muscle. J Physiol. 1974;236:733e742. 20. Williams PE, Goldspink G. Changes in sarcomere length and physiological properties in immobilized muscle. J Anat. 1978;127:459e468. 21. McHugh MP, Kremenic IJ, Fox MB, Gleim GW. The role of mechanical and neural restraints to joint range of motion during passive stretch. Med Sci Sports Exerc. 1998;30:928e932. 22. Page P. Current concepts in muscle stretching for exercise and rehabilitation. Int J Sports Phys Ther. 2012;7:109e119. 23. Weppler CH, Magnusson SP. Increasing muscle extensibility: a matter of increasing length or modifying sensation? Phys Ther. 2010;90:438e449. 24. Kendall FP, Provance P, McCreary EK. Muscles: Testing and Function. 4th ed. Baltimore, MD: Lippincott Williams & Wilkins; 1993. 25. Sahrmann S. Diagnosis and Treatment of Movement Impairment Syndromes. St. Louis, MO: Mosby; 2002. 26. Griegel-Morris P, Larson K, Mueller-Klaus K, Oatis CA. Incidence of common postural abnormalities in the cervical, shoulder, and thoracic regions and their association with pain in two age groups of healthy subjects. Phys Ther. 1992;72:425e431. 27. Kibler WB. The role of the scapula in athletic shoulder function. Am J Sports Med. 1998;26:325e337. 28. Borstad JD. Resting position variables at the shoulder: evidence to support a posture-impairment association. Phys Ther. 2006;86:549e557. 29. Ludewig PM, Borstad JD. Effects of a home exercise programme on shoulder pain and functional status in construction workers. Occup Environ Med. 2003;60:841e849. 30. McClure PW, Bialker J, Neff N, Williams G, Karduna A. Shoulder function and 3dimensional kinematics in people with shoulder impingement syndrome before and after a 6-week exercise program. Phys Ther. 2004;84:832e848. 31. Tate AR, McClure PW, Young IA, Salvatori R, Michener LA. Comprehensive impairment-based exercise and manual therapy intervention for patients with subacromial impingement syndrome: a case series. J Orthop Sports Phys Ther. 2010;40:474e493. 32. Camargo PR, Haik MN, Ludewig PM, Filho RB, Mattiello-Rosa SM, Salvini TF. Effects of strengthening and stretching exercises applied during working hours on pain and physical impairment in workers with subacromial impingement syndrome. Physiother Theory Pract. 2009;25:463e475. 33. Portney LG, Watkins MP. Foundations of Clinical Research: Applications to Practice. 3rd ed. Upper Saddle River, NJ: Pearson/Prentice Hall; 2008. 34. Haik MN, Alburquerque-Sendin F, Camargo PR. Reliability and minimal detectable change of 3-dimensional scapular orientation in individuals with and without shoulder impingement. J Orthop Sports Phys Ther. 2014;44:341e349. 35. Hegedus EJ, Goode AP, Cook CE, et al. Which physical examination tests provide clinicians with the most value when examining the shoulder? Update of a systematic review with meta-analysis of individual tests. Br J Sports Med. 2012;46:964e978. 36. Struyf F, Nijs J, Mollekens S, et al. Scapular-focused treatment in patients with shoulder impingement syndrome: a randomized clinical trial. Clin Rheumatol. 2013;32:73e85. 37. Haik MN, Alburquerque-Sendin F, Silva CZ, Siqueira-Junior AL, Ribeiro IL, Camargo PR. Scapular kinematics pre- and post-thoracic thrust manipulation in individuals with and without shoulder impingement symptoms: a randomized controlled study. J Orthop Sports Phys Ther. 2014;44:475e487.
38. Camargo PR, Avila MA, Alburquerque-Sendin F, Asso NA, Hashimoto LH, Salvini TF. Eccentric training for shoulder abductors improves pain, function and isokinetic performance in subjects with shoulder impingement syndrome: a case series. Rev Bras Fisioter. 2012;16:74e83. 39. Worsley P, Warner M, Mottram S, et al. Motor control retraining exercises for shoulder impingement: effects on function, muscle activation, and biomechanics in young adults. J Shoulder Elbow Surg. 2013;22:e11ee19. 40. Neer 2nd CS. Anterior acromioplasty for the chronic impingement syndrome in the shoulder: a preliminary report. J Bone Joint Surg Am. 1972;54:41e50. 41. Jobe FW, Moynes DR. Delineation of diagnostic criteria and a rehabilitation program for rotator cuff injuries. Am J Sports Med. 1982;10:336e339. 42. Phadke V, Ludewig PM. Study of the scapular muscle latency and deactivation time in people with and without shoulder impingement. J Electromyogr Kinesiol. 2013;23:469e475. 43. Heyworth BE, Williams 3rd RJ. Internal impingement of the shoulder. Am J Sports Med. 2009;37:1024e1037. 44. Hung CJ, Jan MH, Lin YF, Wang TQ, Lin JJ. Scapular kinematics and impairment features for classifying patients with subacromial impingement syndrome. Man Ther. 2010;15:547e551. 45. Ludewig PM, Cook TM. Translations of the humerus in persons with shoulder impingement symptoms. J Orthop Sports Phys Ther. 2002;32:248e259. 46. Alburquerque-Sendin F, Camargo PR, Vieira A, Salvini TF. Bilateral myofascial trigger points and pressure pain thresholds in the shoulder muscles in patients with unilateral shoulder impingement syndrome: a blinded, controlled study. Clin J Pain. 2013;29:478e486. 47. Alter MJ. Science of Flexibility. 3rd ed. Champaign, IL: Human Kinetics; 2004. 48. Neer 2nd CS, Foster CR. Inferior capsular shift for involuntary inferior and multidirectional instability of the shoulder. A preliminary report. J Bone Joint Surg Am. 1980;62:897e908. 49. Rowe CR, Zarins B. Recurrent transient subluxation of the shoulder. J Bone Joint Surg Am. 1981;63:863e872. 50. Borstad JD, Ludewig PM. Comparison of three stretches for the pectoralis minor muscle. J Shoulder Elbow Surg. 2006;15:324e330. 51. Borstad JD. Measurement of pectoralis minor muscle length: validation and clinical application. J Orthop Sports Phys Ther. 2008;38:169e174. 52. Orfale AG, Araujo PM, Ferraz MB, Natour J. Translation into Brazilian Portuguese, cultural adaptation and evaluation of the reliability of the Disabilities of the Arm, Shoulder and Hand Questionnaire. Braz J Med Biol Res. 2005;38: 293e302. 53. Hudak PL, Amadio PC, Bombardier C. Development of an upper extremity outcome measure: the DASH (Disabilities of the Arm, Shoulder and Hand). The Upper Extremity Collaborative Group (UECG). Am J Ind Med. 1996;29:602e608. 54. Gummesson C, Atroshi I, Ekdahl C. The Disabilities of the Arm, Shoulder and Hand (DASH) outcome questionnaire: longitudinal construct validity and measuring self-rated health change after surgery. BMC Musculoskelet Disord. 2003;4:11. 55. Aytar A, Baltaci G, Uhl T, Tuzun H, Oztop P, Karatas M. The effects of scapular mobilization in patients with subacromial impingement syndrome: a randomized, double-blind, placebo-controlled clinical trial. J Sport Rehabil. 2015;24:116e129. 56. Rothbart MK, Sheese BE, Rueda MR, Posner MI. Developing mechanisms of selfregulation in early life. Emot Rev. 2011;3:207e213. 57. Wu G, van der Helm FC, Veeger HE, et al. ISB recommendation on definitions of joint coordinate systems of various joints for the reporting of human joint motiondpart II: shoulder, elbow, wrist and hand. J Biomech. 2005;38:981e992. 58. Folpp H, Deall S, Harvey LA, Gwinn T. Can apparent increases in muscle extensibility with regular stretch be explained by changes in tolerance to stretch? Aust J Physiother. 2006;52:45e50. 59. McHugh MP, Cosgrave CH. To stretch or not to stretch: the role of stretching in injury prevention and performance. Scand J Med Sci Sports. 2010;20:169e 181. 60. Cohen J. The concepts of power analysis. In: Statistical Power Analysis for the Behavioral Sciences. Hillsdale, NJ:: Lawrence Erlbaum Associates; 1988:1e17. 61. Franchignoni F, Vercelli S, Giordano A, Sartorio F, Bravini E, Ferriero G. Minimal clinically important difference of the Disabilities of the Arm, Shoulder and Hand Outcome Measure (DASH) and its shortened version (QuickDASH). J Orthop Sports Phys Ther. 2014;44:30e39. 62. Ehler E, Gautel M. The sarcomere and sarcomerogenesis. Adv Exp Med Biol. 2008;642:1e14. 63. Granzier H, Labeit S. Structure-function relations of the giant elastic protein titin in striated and smooth muscle cells. Muscle Nerve. 2007;36:740e755. 64. Kontrogianni-Konstantopoulos A, Ackermann MA, Bowman AL, Yap SV, Bloch RJ. Muscle giants: molecular scaffolds in sarcomerogenesis. Physiol Rev. 2009;89:1217e1267. 65. Magnusson SP, Simonsen EB, Aagaard P, Gleim GW, McHugh MP, Kjaer M. Viscoelastic response to repeated static stretching in the human hamstring muscle. Scand J Med Sci Sports. 1995;5:342e347. 66. Purslow PP. Strain-induced reorientation of an intramuscular connective tissue network: implications for passive muscle elasticity. J Biomech. 1989;22: 21e31. 67. Fowles JR, Sale DG, MacDougall JD. Reduced strength after passive stretch of the human plantarflexors. J Appl Physiol. 2000;89:1179e1188.
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Contents lists available at ScienceDirect
Journal of Hand Therapy journal homepage: www.jhandtherapy.org
Scientific/Clinical Article
Effects of a stretching protocol for the pectoralis minor on muscle length, function, and scapular kinematics in individuals with and without shoulder pain Dayana P. Rosa PT, MS a, John D. Borstad PT, PhD b, Lívia S. Pogetti PT, MS c, Paula R. Camargo PT, PhD c, * a
Physical Therapist, Master of Physical Therapy Program, Methodist University of Piracicaba, Piracicaba, SP, Brazil Associate Professor, Physical Therapy Division, The Ohio State University, Columbus, OH, USA c Physical Therapist, Adjunct Professor, Physical Therapy Department, Federal University of São Carlos, São Carlos, SP, Brazil b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 April 2015 Received in revised form 9 May 2016 Accepted 17 June 2016 Available online xxx
Study Design: Parallel-group intervention with repeated measures. Introduction: Shortening of the pectoralis minor (PM) may contribute to alterations in scapular kinematics. Purpose of the Study: To evaluate the effects of a stretching protocol on function, muscle length, and scapular kinematics in subjects with and without shoulder pain. Methods: A sample of 25 patients with shoulder pain and 25 healthy subjects with PM tightness performed a daily stretching protocol for 6 weeks. Outcome measures included Disabilities of the Arm, Shoulder, and Hand questionnaire, PM length, and scapular kinematics. Results: Disabilities of the Arm, Shoulder, and Hand scores decreased (P < .05) in the patient group at post-intervention. No differences (P > .05) were found for PM length in both groups. Scapular anterior tilt increased (P < .05) at 90 of flexion in the healthy group. Discussion: This study demonstrated that a daily home stretching protocol significantly decreases pain and improves function in subjects with shoulder pain. The mechanism responsible for these improvements does not appear directly related to PM muscle length or scapula kinematics, suggesting that other neuromuscular mechanisms are involved. Conclusion: The PM stretching protocol did not change the PM length or scapular kinematics in subjects with or without shoulder pain. However, pain and function of the upper limbs improved in patients with shoulder pain. Level of Evidence: 2b. Ó 2016 Hanley & Belfus, an imprint of Elsevier Inc. All rights reserved.
Keywords: Physical therapy Scapula Shortening Shoulder impingement syndrome
Introduction Shoulder impingement syndrome (SIS) represents 44%-65% of all cases of shoulder pain1,2 and may be related to abnormal shoulder kinematics.3-10 In individuals with SIS, alterations in scapular kinematics have been described as a possible consequence Funding: This study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (2012/20305-8 and 2013/50363-2). Conflict of interest: All named authors affirm that they have no financial affiliation or involvement with any commercial organization that has a direct financial interest in any matter included in this article, except as disclosed in an attachment and cited in the article. Any other conflict of interest (ie, personal associations or involvement as a director, officer, or expert witness) is also disclosed in the attachment. This study was registered at ClinicalTrials.gov: identifier NCT01956240. * Corresponding author. Universidade Federal de São Carlos, Departamento de Fisioterapia, Rodovia Washington Luís, Km 235, 13565-905 São Carlos, SP, Brazil. Tel.: þ55 16 3306 6696; fax: þ55 16 3361 2081. E-mail address: [email protected] (P.R. Camargo).
of pectoralis minor (PM) tightness,5,11 posterior capsule tightness,7,12 changes in activity of the scapular and rotator cuff muscles,5,13 and/or repetitive overhead activity.6,14 The PM is the only scapulothoracic muscle with both origin and insertion anterior to the scapula.11,15 The fiber orientation of the PM muscle favors scapular internal rotation (IR), downward rotation, and anterior tilt (AT), and for this reason, it is considered an antagonist to the necessary scapular motions during arm elevation.3,5,11,13 Relative to subjects with greater PM length, healthy subjects with a short PM had increased scapular IR and decreased scapular posterior tilt (PT) during arm elevation,11 similar to the alterations described in subjects with SIS.4,5,16,17 These scapular kinematic alterations support a potential relationship between PM shortening and SIS. Muscle length will decrease through loss of sarcomeres in series when immobilized at a shorter length.18-21 A shortened muscle will also demonstrate increased passive tension as it elongates,22,23 limiting full joint motion.11,22 There is also a
0894-1130/$ e see front matter Ó 2016 Hanley & Belfus, an imprint of Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jht.2016.06.006
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greater percentage of connective tissue in immobilized muscle that further increases passive tension.23 Changes in posture that approximate the origin and insertion of muscle may also result in decreased length,22,24,25 although empirical evidence for this phenomenon is lacking. Based on these muscle adaptations, it is hypothesized that the forward shoulder posture commonly observed in the clinical setting may lead to decreased PM length.26-28 With increased passive tension in the PM secondary to decreased resting length, the normal scapular motions of upward rotation (UR), external rotation (ER), and PT that occur during arm elevation may be restricted and contribute to shoulder dysfunction.11,28 As such, people with shoulder pain and PM tightness may benefit from interventions to improve PM muscle flexibility. PM stretching is often included in comprehensive rehabilitation strategies for individuals with SIS.29-32 However, because PM stretching is typically one of many techniques applied, it is difficult to determine the direct beneficial effect it has on movement, function, and symptoms in subjects with SIS. Therefore, the purpose of this study was to evaluate the effects of a standard PM stretching protocol on muscle length, pain, function, and scapular kinematics in subjects with PM tightness with or without shoulder pain. We hypothesized that PM stretching would increase PM resting length and scapular UR, ER, and PT during arm elevation in all subjects. We also hypothesized that PM stretching would decrease pain and improve function in subjects with shoulder pain.
Methods A total of 100 subjects with or without shoulder pain were initially recruited and evaluated for eligibility, and 78 subjects with PM tightness were included in the study. Fifty subjects (25 patients with shoulder pain and 25 healthy subjects) completed the study (Fig. 1). The participation of all subjects was voluntary, and no incentives were given to encourage enrollment. Each group was considered separately using a within-group repeatedmeasures design. To detect clinically meaningful angular change of 5 in scapular kinematics and achieve a statistical significance level of .05 with a power of 0.80, 25 subjects per group were required.11,33 The clinically meaningful angular change of 5 was selected to be larger than the standard measurement error for scapular kinematics from a recent study in our laboratory, with between-day error ranging from 2.7 to 4.9 in asymptomatic subjects and from 3.1 to 3.8 in subjects with SIS.34 Fliers posted in the local university setting and surrounding community were used to recruit individuals with shoulder pain. Healthy individuals were recruited through personal contacts of the investigators. A healthy group was included to determine the effect of stretching on PM length and scapular kinematics without the additional influence of pain. Individuals with shoulder pain were required to present with at least 1 week of symptoms consistent with SIS using a combination of criteria shown to maximize diagnostic accuracy.35 Subjects were also required to have active arm elevation close to 150 as
Fig. 1. Flow diagram representing enrollment, allocation, procedures, and analysis for both groups.
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determined by digital inclinometer to ensure that scapular kinematic data were captured over the painful arc for impingement.34,36,37 The diagnosis for SIS was made based on a clinical examination and self-reported history.29,34,35,37 SIS was considered to be present when at least 3 of the following signs or symptoms were noted29,32,34,37-39: positive Neer test,40 positive Hawkins test,30 positive Jobe test,41 pain with passive or isometric resisted shoulder ER,31,42,43 pain with active shoulder elevation,44 and pain in the anterolateral shoulder region.5,8,29,45,46 Healthy subjects were excluded if they had any of the positive signs and symptoms for SIS noted previously. Individuals from either group were excluded if they were pregnant; demonstrated glenohumeral joint ligamentous laxity based on a positive sulcus,47,48 an apprehension,49 or an anterior drawer test8; reported a history of traumatic shoulder pathology, fracture, or shoulder surgery; had a history of adhesive capsulitis, scoliosis, or systemic illnesses; had a body mass index of greater than 28 kg/m2 because higher indexes may increase error through skin motion artifact during kinematics data collection; were allergic to transpore tape; or had received physical therapy treatment in the last 6 months, to have no influence from recent interventions.32 Individuals from both groups also had to present with shortened PM muscle length as determined with the pectoralis minor index (PMI) and the methods described by Borstad and Ludewig.11 Pilot data from 12 healthy subjects (6 women and 6 men; 26.58 4.5 years; 66.58 11.86 kg; 1.69 0.08 m) were used to determine the PMI for the present study using an established formula ([(muscle length [cm]/height [cm]) 100]).11 PM length was measured with a tape measure and considered relatively short when the PMI was less than 1 standard deviation below the mean PMI (10.54 cm) calculated using pilot data.11,28,50,51 Thus, in the present study, individuals were classified with shortened PM if their PMI was below 9.93. The study was approved by the Ethics Committee of the University (protocol number 100/12) and registered at ClinicalTrials.gov (registration number, NCT01956240). The data collection was performed in the Laboratory of Analysis and Intervention of the Shoulder Complex at Federal University of São Carlos. All subjects gave their written and informed consent to participate in this study, which was conducted according to the Helsinki statement. Only the symptomatic shoulder was evaluated in the shoulder pain group. For healthy participants with bilateral shortening, the side evaluated was randomly determined using a computergenerated randomization list.
PM length assessment PM length was measured in both the resting and shoulder retraction positions using a tape measure with 0.10-cm resolution. All measurements were taken by the primary investigator who was
3
blinded to the result by covering the side of the tape measure facing them with adhesive tape. A second examiner then read the result and recorded the measurement values. The caudal edge of the fourth rib at the sternum and the inferomedial aspect of the coracoid process were palpated, marked with a pencil, and used to represent PM length, as suggested by Borstad and Ludewig.11 The distance between these landmarks was measured twice with 2 minutes between trials. During the resting position measurements (Fig. 2A), participants were asked to remain in a relaxed posture with the arms at the side in a neutral position, avoid postural correction, and exhale just before the measurement. The pencil marks were removed after each measurement. The intrarater reliability (intraclass correlation coefficient [ICC] ¼ 0.950.97; standard error of measurement [SEM] ¼ 0.31-0.42 cm), interrater reliability (ICC ¼ 0.86-0.87; SEM ¼ 0.70-0.84 cm), and between-days reliability (ICC ¼ 0.95; SEM ¼ 0.40-0.41 cm) of this measurement was established in a previous study for subjects with and without shoulder pain.32 To evaluate the PM length in the retraction position, individuals performed scapular retraction and held this position as the primary investigator measured the muscle length (Fig. 2B). The measurement in this position was also taken twice, and the second examiner recorded the values.
Disabilities of the Arm, Shoulder, and Hand questionnaire The Brazilian version of the Disabilities of the Arm, Shoulder, and Hand (DASH) questionnaire was used to evaluate upper limb physical function and symptoms.52 The DASH self-assessment questionnaire contains 30 questions, and a maximum score of 100 indicates the worst possible condition.53 This questionnaire is reliable, valid, and responsive52,54 and has been widely used in individuals with SIS.34,38,55
Three-dimensional scapular kinematics For 3-dimensional scapular kinematics, Flock of Birds (miniBird) hardware (Ascension Technology Corporation, Burlington, VT) integrated with MotionMonitor software (Innovative Sports Training, Inc, Chicago, IL) was used for data capture and analysis.11,34,37,56 The tridimensional position and orientation of 3 sensors were tracked simultaneously at a sampling rate of 100 Hz. Sensors were secured to subjects’ skin with double-sided adhesive tape and transpore tape to the sternum, the acromion of the scapula, and a thermoplastic cuff secured to the distal humerus. The subject stood with the arms relaxed at the side in a neutral position with the transmitter directly behind the shoulder tested, whereas bony landmarks on the thorax, scapula, and humerus were palpated and
Fig. 2. Measurement of pectoralis minor length: distance between coracoid process (white arrow) and fourth rib (black arrow) taken with a tape measure on (A) resting and (B) retraction positions.
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digitized to allow transformation of the sensor data to local anatomically based coordinate systems. Local coordinate systems were established for the trunk, scapula, and humerus as recommended by the International Society of Biomechanics.57 For all local coordinate systems, the z-axis pointed laterally, x-axis anteriorly, and y-axis superiorly. The YX0 Z00 Euler sequence57 was used to describe scapular motions relative to the trunk in the sequence of IR/ER, UR/downward rotation, and AT/PT. Humeral orientation with reference to the trunk was determined using the YX0 Y00 Euler sequence, which defines the plane of elevation, elevation, and IR/ER.
Procedure Kinematic data were collected with the subjects in a relaxed standing position. Subjects elevated their arm from a dependent position through their full range of motion at a speed such that it took around 3 seconds to elevate their arm and 3 seconds to lower it. Subjects maintained light fingertip contact with a flat planar surface, and their thumb pointed superiorly during these motions to maintain a consistent positioning of the arm in the sagittal plane. Data were collected during 3 consecutive repetitions. This procedure has been shown to be reliable in healthy subjects and subjects with shoulder impingement symptoms.34 All measurements were taken by the primary investigator.
Intervention Both groups performed a daily PM stretching protocol for 6 weeks.58,59 The protocol consisted of 4 repetitions of 1-minute stretches with a 30-second interval between repetitions.58,59 A minimum of 4 minutes of stretching to decrease muscle passive resistance is recommended.59 The subjects were instructed by a physical therapist to perform a unilateral corner stretch using a wall (Fig. 3). The starting position for this stretch is with the individual in the standing position, 90 of arm abduction, 90 of elbow flexion, and the palmar surface of the hand on the wall. The contralateral leg to the shoulder being stretched was positioned forward of the other leg. To apply the stretch, the trunk is shifted forward and rotated opposite to the side being stretched.50 This stretch position resulted in the largest separation between the fourth rib and coracoid process landmarks when compared with sitting and supine manual PM stretches.50 The stretching protocol was performed at home. The physical therapist was available to answer questions or clarify procedures during the intervention period and contacted the individuals weekly to remind them to do the protocol. A daily exercise log to record compliance and a picture of the stretch were given to participants. At the end of the 6 weeks, all participants returned the log to the investigators. Individuals were included in the data analysis if they performed at least 4 weeks of stretching as this time is described as the minimal period to achieve a decrease in muscle passive resistance.59 Two baseline evaluations were performed 1 week apart before the intervention. The follow-up evaluation was performed immediately after completion of the 6-week stretch protocol (evaluation 3). The double baseline design was used to assure stability of the dependent variables before the intervention. DASH, PM muscle length, and scapular kinematics were assessed at each evaluation. The DASH was also evaluated in the healthy group to evaluate whether PM stretching, as would be done preventively, could provoke shoulder region irritation.
Fig. 3. Unilateral corner stretch.
Statistical analysis Adherence was quantified as the number of days in which a participant performed the stretching protocol, and descriptive data were calculated. The data were analyzed using the SPSS statistical package (17.0 version; SPSS, Chicago, IL). Normality was evaluated by Kolmogorov-Smirnov test, and it was violated for DASH questionnaire (P < .05). Thus, the Friedman test with Wilcoxon post hoc tests was used to verify differences between evaluations within each group for the questionnaire. If significant differences were revealed, a Bonferroni adjustment to the a level was calculated. As 3 comparisons were performed, a P value of less than .016 (0.05/3) was adopted to be more conservative in identifying differences between evaluations for the questionnaire score. For PM length in both the resting and retraction positions, a 2way repeated-measures analysis of variance was used to test interactions of group (healthy and shoulder pain) evaluation (1, 2, and 3) and for main effects of group or evaluation. Scapular kinematic data at rest and at humerothoracic elevation angles of 30 ,
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60 , 90 , and 120 were selected for analysis. For scapular IR, UR, and PT, separate 2-way repeated-measures analyses of variance with Bonferroni post hoc tests were used to test for interactions of angle (rest, 30 , 60 , 90 , and 120 ) evaluation (1, 2, and 3), and for main effects of evaluation. For scapula kinematics, the groups were analyzed separately. A P value of less than .05 was considered statistically significant. Intragroup effect sizes (ESs) for all quantitative variables were calculated using Cohen d coefficient.60 The periods evaluated were paired as following: baseline 2-baseline 1, follow-up-baseline 1, and follow-up-baseline 2. An ES greater than 0.8 was considered large, around 0.5 moderate, and less than 0.2 small. The ES was very small between baseline 2 and 1 and very similar between the follow-up and both baselines. Based on this result, the Cohen d coefficients presented later are only between the follow-up and baseline 2. Results The descriptive data of the individuals are shown in Table 1. The average stretching protocol compliance was 41.20 9.22 days (5.9 weeks) and 40.32 8.28 days (5.8 weeks) for the healthy and shoulder pain groups, respectively. This variability in compliance was due primarily to personal schedules of the individuals. Some subjects performed more than 42 days of stretching to match their schedule with the follow-up appointment. Figure 1 shows that 27 subjects did not complete the stretching protocol. The main reasons given by subjects for dropping out were pain during stretching, improvement in pain before the end of the 6 weeks’ protocol, and personal factors. Table 2 shows the results for the DASH and length of the PM for both groups at each assessment. The healthy group did not demonstrate statistically significant differences (P > .016) across assessments for the DASH. The ES was small for this questionnaire (Cohen d, 0.06). The shoulder pain group showed reduced DASH score at followup compared with baselines 1 and 2 (P ¼ .001 and .004, respectively) and a large (Cohen d, 0.83) ES were observed for the questionnaire. Neither statistically significant interactions between group and evaluation were observed nor a statistically significant main effect of group and evaluation for PM length in the resting (F ¼ 0.18 and P ¼ .84; F ¼ 0.71 and P ¼ .40; F ¼ 8.65 and P ¼ .05, respectively, Table 2) or retraction positions (F ¼ 0.88 and P ¼ .39; F ¼ 0.76 and P ¼ .38; F ¼ 1.39 and P ¼ .25, respectively, Table 2) was observed. Cohen d coefficients showed small effects of the stretch protocol (Cohen d, 0.006-0.21) for both groups in all comparisons. Scapular kinematics Healthy group For the healthy group, neither a statistically significant interaction between angle and time was observed nor a statistically significant
Table 1 Descriptive data of the individuals Variable
Healthy group (n ¼ 25)
Shoulder pain group (n ¼ 25)
P
Gender Age (y)a Height (m)a Weight (kg)a BMI (kg/m2)a Evaluated shoulder
13 women; 12 men 25.76 6.95 1.69 0.08 64.12 10.76 22.30 2.56 13 dominant; 12 nondominant d
14 women; 11 men 26.96 5.79 1.69 0.07 67.54 9.68 24.42 5.75 18 dominant; 7 nondominant 42.32 64.54
d .51 .80 .24 .09 d
Duration of pain (mo)a
BMI ¼ body mass index. a Values are mean standard deviation.
d
5
main effect of time for scapular IR (Fig. 4A) (F ¼ 0.32 and P ¼ .95; F ¼ 1.37 and P ¼ .26, respectively) or scapular UR (Fig. 4B) (F ¼ 1.20 and P ¼ .32; F ¼ 2.61 and P ¼ .08, respectively) during arm elevation was observed. A statistically significant angle time interaction effect was determined (F ¼ 2.97 and P ¼ .003) for scapular PT (Fig. 4C), where at 90 of arm elevation, there was decreased scapular PT at follow-up when compared with baseline 2 (P ¼ .02). The ESs in the healthy group were small for IR (Cohen d, 0.05 to 0.10). For scapular UR, the ESs were moderate (Cohen d, w0.50). For scapular PT, this group showed small ES at rest, 30 , and 60 of arm elevation (Cohen d, 0.30 to 0.09) and moderate ES at 90 and 120 of arm elevation (Cohen d, 0.50). Shoulder pain group For the shoulder pain group, there were no statistically significant interaction effects between angle and time and no main effect of time for scapular IR (Fig. 4A) (F ¼ 1.21 and P ¼ .32; F ¼ 2.94 and P ¼ .06, respectively), scapular UR (Fig. 4B) (F ¼ 0.51 and P ¼ .84; F ¼ 1.50 and P ¼ .24, respectively), or PT of the scapula (Fig. 4C) (F ¼ 0.83 and P ¼ .58; F ¼ 0.42 and P ¼ .66, respectively) during arm elevation. The ESs for scapular rotations in the shoulder pain group were small for IR (Cohen d, 0.32 to 0.21). For scapular UR, the ESs were small (Cohen d, 0.20) except at 30 of arm elevation with moderate ES (Cohen d, w0.50). For scapular PT, the group showed small ES (Cohen d, 0.36 to 0.002).
Discussion This study evaluated the effects of a daily stretching protocol for the PM on muscle length, function, and scapular kinematics in individuals with and without shoulder pain. Our results showed that PM stretching decreased pain and improved function in subjects with shoulder pain but was not effective at changing the PM length or scapular kinematics. Different techniques to stretch the PM are used in clinical practice, but the most effective technique is unknown. Borstad and Ludewig50 compared 3 techniques and concluded that the unilateral self-stretch was better than the supine or sitting manual stretch techniques to increase the distance between the origin and insertion of the PM.48 The DASH questionnaire revealed a decrease in pain and improvement in function in the shoulder pain group, despite the low scores reported at the beginning of the study. Although the DASH score decreased 10.37 points in the present study, it was just shy of reaching the 10.7-point minimal detectable change (MDC) reported by Franchignoni et al.61 However, the large ES after the intervention suggests that stretching contributed to the change in pain and function of the upper limbs. Decreased muscle length may lead to loss of extensibility due to decreased number of sarcomeres in series, fewer actin-myosin crossbridges,21 the type of titin protein, and shortening of connective tissue.62-64 Shortening of connective tissue has been described as a possible cause of pain.47 We propose that the stretching protocol applied in the present study may have positively affected pain by decreasing muscle passive resistance,3,65 improving connective tissue extensibility,66 and influencing neural activation patterns.67 The PM shortening was determined as previously described by Borstad and Ludewig,11 and it has been used in some recent studies.28,51,68-73 A threshold of shortening has not been determined yet, so it is recommended that it should be calculated for the sample in each study.11 In the present study, 85% of the sample presented muscle shortening. Although this number seems to be high, it is believed that the PMI adopted was appropriate to classify
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Table 2 Results of DASH questionnaire and pectoralis minor length for healthy and shoulder pain groups Outcome measure Healthy group (n ¼ 25) DASH Muscle lengthdrest (cm) Muscle lengthdretraction (cm) Shoulder pain group (n ¼ 25) DASH Muscle lengthdrest (cm) Muscle lengthdretraction (cm)
Baseline 1
Baseline 2
Follow-up
3.46 4.22 (1.72-5.21) 15.99 1.35 (15.44-16.56) 17.33 1.47 (16.73-17.94)
2.63 4.02 (0.97-4.29) 16.19 1.45 (15.59-16.79) 17.43 1.48 (16.81-18.03)
2.86 3.90 (1.25-4.47) 16.38 1.46 (15.78-16.98) 17.44 2.33 (16.47-18.40)
17.36 11.68 (13.49-22.76) 16.36 1.57 (15.72-17.01) 17.65 2.03 (16.81-18.48)
15.83 12.30 (11.18-21.08) 16.47 1.75 (15.75-17.20) 17.68 1.74 (16.96-18.40)
7.94 7.82a (4.71-11.17) 16.87 1.90 (6.08-17.65) 18.26 1.86 (17.49-19.03)
DASH ¼ Disabilities of the Arm, Shoulder, and Hand. Results are mean standard deviation (95% confidence interval). a P < .016, when compared with baselines 1 and 2.
individuals with muscle shortening, considering that the groups were very similar for all baseline variables. The mean change in PM resting length after the stretching protocol in individuals with shoulder pain was þ0.51 cm, with a small ES. This change in length is close to the SEM (0.41 cm) for measurements between days in individuals with shoulder pain determined in a previous study. The MDC (1.14 cm) was also determined in the previous study,70 with the intent of identifying the change in PM length that represents a real change. Because the mean change of 0.51 cm is smaller than the MDC, the increase in PM
length measured at follow-up does not represent a real alteration in muscle length after stretching. Changes in scapular kinematics were not observed after the intervention in the present study. This result does not support our hypothesis that scapular ER, UR, and PT would be increased after the stretching protocol in those with a relatively short PM. Other studies have assessed scapular kinematics after an intervention combining PM stretching with scapular and rotator cuff muscle strengthening and manual therapy techniques in individuals with SIS,30,36,39,43 but the results are equivocal. One possible
Fig. 4. Mean of scapular (A) internal and (B) upward rotations and (C) posterior tilt. During arm elevation for (left) healthy and (right) shoulder pain groups at all assessments. The error bars are standard error of mean. *P ¼ .02, when compared with baseline 1.
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explanation for the lack of change in kinematics in the present study is that the home-based intervention may not have maximized PM muscle elongation as much as a therapist-applied stretch may have. It is also possible that PM length has only a minor contribution to kinematics so that stretching can only impart a limited effect on motion. Because scapular kinematics represent a complex combination of muscle activation, motor control, and soft tissue variables, an intervention to alter only 1 variable may not be sufficient to change kinematics perceptibly. It is possible that adding the right strengthening exercises to the stretching protocol may positively alter scapular kinematics. Our purpose was to evaluate the effect of PM stretching independent of other interventions, and the results suggest that stretching PM alone is not enough to modify kinematics. Borstad and Ludewig11 reported scapula kinematic differences for IR and PT only in subjects distinguished by relatively short and long PM length. The lack of change in scapula UR in the present study suggests that the PM length has minimal influence on scapula UR during arm elevation. Borstad and Ludewig50 also suggested that the stretching technique performed in this study may favor increased PT of the scapula. However, the present study showed only decreased PT at 90 of arm elevation for the healthy group after stretching, whereas no differences were observed in the shoulder pain group. This change was not considered clinically relevant because the ES was moderate (Cohen d, w0.50), and the w3 change was below the clinically meaningful angular change adopted in this study (5 ). Other studies have reported similar changes in scapular tilt after interventions in subjects with and without pain. Haik et al37 reported increased scapular AT after thoracic manipulation in healthy subjects with a small ES. A recent randomized controlled trial also showed more AT in subjects with shoulder pain after a strengthening and stretching intervention, with a small ES for scapular tilting also reported.74 It is important to note that the lack of change in PM muscle length in the retraction position also helps explain the lack of scapular kinematic changes. This result suggests that PM length change during a dynamic motion was not influenced by stretching, implying that passive resistance from PM during arm elevation continues to influence scapular kinematics.11,13,28 As the present study is the first study to evaluate the independent effects of PM stretching on scapular kinematics, additional studies are necessary to determine the real influence of PM length on scapular motion. The placebo effect may have contributed to the decreased pain and increased function reported in this study. When the potential benefits of an intervention are explained to participants, their expectations about these benefits may influence postintervention assessments.75 Although incomplete information about the objectives of this study was given to participants, expectations for improvement may have influenced the results. Specifically, a placebo effect may explain the significant decrease in pain and improved function in the patient group, despite the lack of meaningful biomechanical changes. Although the hypothesized biomechanical changes were not observed, the present study demonstrates an important finding relative to clinical practice. This study demonstrated that a simple stretching protocol performed daily at home can significantly decrease pain and improve the function in subjects with shoulder pain. This stretch intervention can be easily prescribed to individuals with shoulder pain. The mechanism whereby a simple stretch decreases pain and improves function does not appear directly related to PM muscle length or scapula kinematics, suggesting that other neuromuscular mechanisms or improved
7
subjective tolerance76 are involved. Of note is that the mean duration of pain in the patient group was 42 months, and perhaps stretching alters mechanoreception such that pain intensity is modified in individuals with chronic musculoskeletal symptoms. It is possible that the participants may not have maximally elongated PM during the stretch, either by ineffective shoulder positioning or by pain avoidance. A therapist-applied stretch may have been more effective at ensuring that PM length was optimal and that forces were maintained during stretching. A recognized limitation is that linear measurements such as the one used to quantify PM length in this study cannot represent real structural changes of muscle after a stretching protocol. Similarly, the PM length may be influenced by a subject’s posture during the measurements. Between-day reliability estimates are excellent for this measurement and should minimize this concern. Subjects with shoulder pain in this study reported a mean pain duration of 42 months, limiting the application of these findings to a more acute clinical population. Future investigations should evaluate the effects of other PM stretch techniques on PM length, shoulder function, and pain. Considering that linear measurements may not represent real structural changes in muscle after stretching, it would be beneficial to incorporate imaging that can evaluate these potential tissue adaptations in future studies. The randomized controlled trial is also needed to confirm the results from the present study. Conclusion The findings of this study showed that daily PM stretching performed at home was effective in decreasing pain and improving function in individuals with shoulder pain but did not change PM length or scapular kinematics during arm elevation in subjects with or without shoulder pain. Acknowledgments The authors thank the volunteers who participated in this study and Rafael Foroni Luchesi and Letícia Bergamin Januário for helping in data collection. References 1. Bruls VE, Bastiaenen CH, de Bie RA. Non-traumatic arm, neck and shoulder complaints: prevalence, course and prognosis in a Dutch university population. BMC Musculoskelet Disord. 2013;14:8. 2. van der Windt DA, Koes BW, de Jong BA, Bouter LM. Shoulder disorders in general practice: incidence, patient characteristics, and management. Ann Rheum Dis. 1995;54:959e964. 3. Taylor DC, Dalton Jr JD, Seaber AV, Garrett Jr WE. Viscoelastic properties of muscle-tendon units. The biomechanical effects of stretching. Am J Sports Med. 1990;18:300e309. 4. Lukasiewicz AC, McClure P, Michener L, Pratt N, Sennett B. Comparison of 3dimensional scapular position and orientation between subjects with and without shoulder impingement. J Orthop Sports Phys Ther. 1999;29:574e583. discussion 584-576. 5. Ludewig PM, Cook TM. Alterations in shoulder kinematics and associated muscle activity in people with symptoms of shoulder impingement. Phys Ther. 2000;80:276e291. 6. Laudner KG, Myers JB, Pasquale MR, Bradley JP, Lephart SM. Scapular dysfunction in throwers with pathologic internal impingement. J Orthop Sports Phys Ther. 2006;36:485e494. 7. Lin JJ, Lim HK, Yang JL. Effect of shoulder tightness on glenohumeral translation, scapular kinematics, and scapulohumeral rhythm in subjects with stiff shoulders. J Orthop Res. 2006;24:1044e1051. 8. McClure PW, Michener LA, Karduna AR. Shoulder function and 3-dimensional scapular kinematics in people with and without shoulder impingement syndrome. Phys Ther. 2006;86:1075e1090.
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