Comprehensive corrective exercise program improves alignment, muscle activation and movement pattern of men with upper crossed syndrome: randomized controlled trial

Upper crossed syndrome (UCS) refers to the altered muscle activations and movement patterns in scapulae along with some abnormal alignment in the upper quarter, which may contribute to the dysfunction of the cervicothoracic and glenohumeral joints. The present study aimed to investigate the effectiveness of a comprehensive corrective exercise program (CCEP) and subsequent detraining on alignment, muscle activation, and movement pattern in men with the UCS. This randomized controlled trial included 24 men. The intervention group conducted CCEP (8 weeks), followed by four weeks of detraining and the control group maintained normal daily activities. Electromyography of selected muscles, scapular dyskinesis test, head, shoulder, and thoracic spine angle were measured at baseline, post-test, and follow-up. There were significant differences for Group x time interaction and also for within-group from pre-test to post-test and follow-up in all outcomes. Also, significant differences were observed in three outcomes at post-test and follow-up between the CCEP and control group in favor of the CCEP. In Conclusion, the present study demonstrates that the CCEP for individuals with UCS is feasible and effective, improving muscle activation imbalance, movement patterns, and alignment. Importantly, these improvements were maintained after four weeks of detraining, suggesting lasting neuromuscular re-training adaptations.


Results
shows the baseline demographic and all variable characteristics for each group. There was no significant difference between the two groups for any of demographic and outcome variables. Although some outcome variables varied between CCEP and control groups, they were not significantly different. Repeated-measures ANOVAs were used to compare alignment, muscle activation, and movement pattern of UCS subjects at both post-test and follow-up between the CCEP and control groups ( Table 2). There was a significant group by time interaction (p < 0.05) for each outcome (except the onset of muscle activities); that is, the CCEP and control groups changed differently over time.
Within-group comparison for the CCEP and control group. Table 2 shows that there were significantly different (p < 0.05) for all three outcomes (alignment, muscle activation, and movement pattern) in the CCEP from pre-test to post-test and follow-up. In this regards, the alignment outcomes (including FHA, FSA, TKA) and some muscle activation outcomes (including UT, UT/MT, UT/LT, UT/SA) were decreased, and movement patterns (scapular dyskinesis) and muscle activation in MT, LT, and SA were increased in the CCEP. Interestingly, there were significantly different (p < 0.05) levels of UT, LT, and SA activations in the control group from pre-to post-test and follow-up, with increasing UT activation and decreasing LT and SA activations. The onset of muscle activations did not change significantly for either group over time ( Table 2).
Considering the pairwise comparisons for the participants in the CCEP group, the alignment, muscle activations (except the onset), and movement patterns significantly improved from pre-test to both post-test and follow-up (p < 0.05). However, the same changes were not statistically significant from post-test to follow-up (between the end of the program training and after 4-weeks detraining) ( Table 2).
Between-group comparison at posttest and follow-up. Significant differences were observed between the CCEP and control group in all three outcomes (alignment, muscle activation, and movement pattern) at the post-test and follow-up to the favor of the CCEP (Table 3). No significant differences were noted concerning the onset of muscle activations. (η 2 ≥ 0.14) improvement in all three outcomes, including alignment, muscle activation (except the onset), and movement pattern at the post-test when compared to the control group. Also, the demonstrated changes in the outcomes from baseline to follow-up were more than MCIDs that were calculated by the mentioned formula ( Fig. 1).

Discussion
This study evaluated the effects of the CCEP compared with a control condition on alignment, muscle activation patterns of the main scapular stabilizers, and related movement patterns among young men with the UCS. Mean EMG amplitude and onset of the UT, MT, LT, and SA, as well as alignment factors including FHA, FSA, and TKA, along with related movement pattern (scapular dyskinesis), were measured for both the CCEP and control groups at baseline (pre-test), week 8 (post-test), and week 12 (follow-up). The research hypothesis was that the CCEP would significantly improve the selected muscle activation, movement patterns, and alignment of the head, shoulder, and thoracic spine. We also hypothesized that the effects following the CCEP would be maintained after four weeks of detraining. According to our results, the CCEP used in this study appears to have an acceptable effect on restoring balance in the scapula stabilizer muscles. This is one of the main findings of the present study because, according to the chain reactions expressed by Janda, the scapula is considered as the key-stone and source of complications in the UCS 7 . It is plausible that one of the main reasons for the restoring muscle activity of the scapular stabilizer Table 2. Within-group differences in alignment, muscle activation, and movement pattern in the CCEP and control group, P < 0.05. www.nature.com/scientificreports/ Table 3. Between-group differences in alignment, muscle activation, and movement pattern in the CCEP and control group, P < 0.05.

Outcomes measures
Post-test  www.nature.com/scientificreports/ following the implementation of the CCEP was the emphasis on cognition as a part of neuromuscular rehabilitation, especially in the initial phase. The role of neuromuscular rehabilitation is to change movement patterns or motor behavior. Furthermore, cognition can modify or facilitate motor behavior and control 24 ; therefore, having chronic musculoskeletal pain patients mentally focus on muscle contraction during corrective exercises may be beneficial. To utilize these cognitive benefits, the participants in the CCEP group used an internal focus of attention to contract underactive scapular muscles or to relax overactive muscles for normalization of scapular position and, if needed, the therapist gave verbal or tactile feedback. Researchers in the field of scapular rehabilitation have previously described this type of exercise as "scapular orientation exercises" 25 . Mottram et al. showed that individuals could be trained to position the scapula in upward rotation and posterior tilt by creating appropriate contractions in the three parts of the trapezius muscle 25,26 .
Restoring motor control and balance of scapular muscle activations are more critical than increasing strength in these muscles 27 . Therefore, some researchers have used EMG biofeedback to learn the correct contractions of the scapular muscles during neuromuscular exercises. These previous studies showed that conscious exercises with feedback have immediate effects on controlling movement and kinematics of the scapulae 27,28 . Holterman et al. showed that after one hour of biofeedback by EMG, all subjects learned to activate parts of the trapezius muscle (such as the lower part) while simultaneously relaxing the other part (upper part) 29 . Moreover, researchers have shown that musculoskeletal disorders can be associated with reorganization of the cerebral cortex 30 . Therefore, retraining muscle activity using motor learning principles and neuromuscular function can restore proper muscle application patterns in the early stages of the training program 24,29 .
At the end of the initial phase of CCEP, the participants gradually gained the ability to create concentric and eccentric contractions while performing the movement in different positions of the exercise. The logic of exercise progression (from isometric to dynamic) has been confirmed in previous studies 31 . Our results showed an improvement in selected muscle activations in all three phases of concentric, isometric, and eccentric, which can be due to training in all contraction phases.
Another reason for the improvement in selected muscle activations was probably related to the use of targeted exercises in CCEP for scapular dyskinesis rehabilitation, which increased the activity of the MT, LT, and SA and reduced the activity of the UT 32 . All of these exercises have been mentioned as exercises that can create the preferred activation ratio between the scapular stabilizer muscles 33,34 . The present study showed a clinically-desired, significant decrease in the ratio of the UT/MT, UT/LT, and UT/SA after the end of the CCEP.
Although there was no significant change in the onset of muscle activation following the CCEP, our study suggests the timing of muscle activation seems to be closer to normal. The timing of muscle activation is an essential factor in the coordination between the scapula and arm movement 35,36 . The timing of the experimental group before performing CCEP was as follows: first, the UT (− 0.20 ms), then the MT (− 0.13 ms), the LT (− 0.12 ms), and then the SA (0.26 ms) was activated. Theoretically, the middle and lower parts of the trapezius muscle play a more stabilizing role; the delay in their activation compared to the UT, as seen in this study, can lead to a relative dominance of the UT 35 . This relative dominance at the onset, along with the higher level of activity of the UT than the MT, LT, and SA, creates muscle imbalance around the scapula, and ultimately leads to dysfunction in the rhythm and movement of the scapula (scapular dyskinesis) 21,37 . The results showed that despite the lack of significant differences, the timing of scapular muscle activations was changed after CCEP as following: first, the MT (0.05 ms), the SA (0.12 ms), the LT (0.19 ms), and finally the UT (0.24 ms) were activated. This could indicate that the upper part of the trapezius muscle was not superior to other parts after performing CCEP.
Our results demonstrated that the CCEP can improve the movement patterns (scapular dyskinesis) and the alignments of the head, shoulder, and thoracic spine in people with UCS. It seems that improving in scapular dyskinesis and alignment would be followed by improvement in neuromuscular factors created by cognition and conscious control of experimental participants after CCEP. Previous evidence has shown that people with scapular dyskinesis can obtain a proper position and movement of the scapula by consciously controlling the scapula 26,38 . Cools et al. also noted the importance of the correct alignment of the head and spine during scapular rehabilitation exercises 39 ; the authors stated that this strategy of simultaneous correction of the posture should be noted in all phases of the rehabilitation program. After using internal focus of attention and regaining sufficient control over scapular muscles in the CCSP, participants then focused externally on correcting related segments through chin tuck, retraction of shoulders, and straightening the upper thoracic spine 18 . We believe the improvement in postural deviations and scapular position and rhythm in the CCEP group was due to the interaction of improved muscle activity, movement pattern and alignment.
For the secondary purpose of the current study, the results showed that the positive effects following the CCEP were maintained after four weeks of detraining. The present study is the first we are aware of to investigate the effect of a short-term detraining on the scapula stabilizer muscle activations and movement patterns, as well as related postural deviations after applying an 8-week training intervention. Previous research suggests there should be an increase in muscle function at the beginning of an exercise program related to physiological and neurological adaptations. Prior to hypertrophic gains, early muscular adaptations to resistance training include applying more motor units, learning more effective and economical use of active motor units, and reducing inhibitory inputs for alpha motor neurons 40,41 . Optimal neuromuscular changes in the initial and improvement phases of CCEP followed by maintenance of these changes after a month of detraining support the lasting positive effects of corrective exercise on muscle activations, movement patterns and alignment in participants with UCS.
Our study had some limitations, including the recruitment of only young males; therefore, the results of this study may not be generalizable to all groups (e.g., women or men aged ≥ 28 years) with the UCS. Also, the study was performed on a relatively small sample size; however, the effect sizes of the differences in outcome measures between the CCEP and control groups suggest that the findings are less likely to be affected by sample size. Another limitation is the lack of a double-blind design, which is not feasible with exercise interventions.

Conclusion
This study demonstrated that the CCEP for individuals with UCS is feasible and results in improvement of muscle imbalance, movement patterns, and postural alignment that are maintained after short-time detraining. Therefore, our approach to improving the UCS could represent a fundamental paradigm shift in exercise intervention strategies to improve postural malalignments and their consequences. This study may assist practitioners in individualized clinical decision-making; however, our results may have a limited generalizability to all individuals with UCS.

Methods
Study design. The current study was a parallel-group randomized, controlled trial comparing the 8-week CCEP, followed by four weeks of detraining to a control group without any intervention. The study has been registered at the Iranian Registry of Clinical Trials on 26 October 2018 (IRCT20181004041232N1), and the ethical approval was obtained by the Ethics Committee on Research at the University of Tehran, Iran (IR. UT.REC.1395026). The study was conducted at the Laboratory of Health and Sports Medicine Department, University of Tehran, Tehran, Iran. The study was reported in accordance with the rigor of the CONSORT guideline, and all experimental conditions conformed to the Declaration of Helsinki. The study protocol has been published elsewhere 18 . Participants. The participants consisted of 24 men aged 18 to 28 years with the UCS. The process of recruiting and screening is reported elsewhere 18 . All participants completed and signed the informed consent form. The inclusion criteria were having any abnormality in the position and rhythm of the scapula, as measured by the scapular dyskinesis test, having postural changes such as excessive thoracic kyphosis (≥ 42°), forward head (≥ 44°) or round shoulder (≥ 49°) as measured by flexicurve and photogrammetry, respectively 17 . Exclusion criteria were having any visible malalignment in the pelvis or lower extremities, have a rotation higher than 5 degrees on the forward bending test because of scoliosis, which was measured with a scoliometer 17 , have a history of joint diseases in the spine, shoulder, and pelvis, fracture, surgery, and have a bodyweight outside the normal range (BMI between 18 and 25) 42 .
Randomization. Participants were randomized using computer-generated block randomization in a 1:1 ratio, followed by a concealed allocation through opening the sequentially numbered, opaque and sealed envelopes, and a card inside indicated the group into which the participant was randomly allocated, i.e., the intervention or the control group. After randomization, participants took part in the baseline assessment process, and then the treatment group received the interventions for eight weeks, while the control group did not receive any intervention. All the measurements were repeated after ending the intervention. Finally, a follow-up assessment was performed after a 4-week detraining period. The study flowchart is shown in Fig. 2.
Intervention. The duration of the exercise protocol was eight weeks and three sessions per week, and each session was about an hour. Each exercise session began with 10 min of warm-up activity, ended with 5 min of cool-down, and all exercises were performed under supervision. The participants did not conduct any extra exercises at home; however, it was essential to avoid sustaining poor postures. The control group did their ordinary daily activities and did not participate in any exercise programs. After the study was completed, the control group received the exercise intervention protocol for ethical considerations. The specific intervention protocol has been described in detail elsewhere 18 and is briefly summarized below. Although there was a framework for the CCEP, shown in Table 4, exercises were progressed by considering individual characteristics of each participant.
Comprehensive Corrective Exercises Program (CCEP). The CCEP was designed in three phases, including initial, improvement, and maintenance. Exercises are progressed in frequency and intensity during these phases, as long as the movements are performed in a good quality. The exercises in the initial phase were characterized with a cognitive focus on scapular muscles (i.e., the internal focus of attention). Subjects were instructed to contract underactive muscles isometrically and relax overactive muscles for normalization of scapular position and motion 25,31 . After restoring the muscle balance in the static conditions, participants added upper extremity movements in various training positions (Fig. 3: exercises 1-5).
Once the participants could contract appropriate muscles in correct alignment during the movement pattern, the protocol focused on improving sustained postures. This goal was addressed in the improvement phase when necessary tissue adaptations occurred by increasing the load of exercises (Fig. 3: exercises 6-13) 43,44 . In the maintenance phase, the participant continued to do the exercises and maintain the training adaptations for two weeks 44 . The exercises were the same as the improvement phase without any progression in intensity and frequency.
Outcome measures. Demographic characteristics (i.e., age, weight, height, BMI) were measured at baseline. All outcome measurements were performed by the main researcher at the baseline, eight weeks (posttest), and 12 weeks (follow-up).
Electromyography measurement. Surface electromyography of the selected muscles, including the upper trapezius (UT), middle trapezius (MT), lower trapezius (LT), and serratus anterior (SA) were performed using a ME-6000 Megawin (MegaWin, Finland) www.nature.com/scientificreports/ three phases (concentric, isometric, and eccentric) lasting for 3 s each. They had already been trained to achieved the reliable reproduction of the movement at the required velocity. A synchronized electrogoniometer and a metronome were used to control the three phases. Speed was standardized to a count of 3 s in the concentric phase, a second at full range abduction (isometric phase) and 3 s in the eccentric phase of abduction motion. Therefore, they performed the movement five times, and the rest time lasted 3 s in-betweens. Disposable Ag-AgCl electrodes with a diameter of 2 cm and a 2 cm spacing between two poles of electrodes were used, and data were recorded at a frequency of 1000 Hz. The location of the electrodes was determined using the SENIAM protocol and based on valid scientific papers 45,46 . The maximum voluntary isometric contraction (MVIC) was recorded to normalize the signals 18 . The data from the mean square root (RMS) was used in the process of meas-  www.nature.com/scientificreports/ uring muscle activation. Muscle activation ratios were also calculated for the mean EMG amplitude; a ratio less than one indicates higher MT, LT, or SA activation than UT, and an amount greater than one indicates greater UT activation than MT, LT, or SA 46 . Only the concentric phase of the motion was used to determine the onset of muscle activity, and it was based on the onset of the deltoid muscle. Moreover, the onset of muscle activation was from the point where the level of muscle activity reached three standard deviations above the rest of the muscle activity 46 .
Scapular dyskinesis. The dynamic scapular dyskinesis test, according to the procedure described by McClure et al. 47 , was used to assess the scapular movement pattern. The position and motion of scapula were characterized by dyskinesis as a "yes" (presence of deviation or dysrhythmia/asymmetry bilaterally) or "no" (no presence). This method has been shown to be reliable among observers and has acceptable clinical utility 47,48 .
Forward head and shoulder angles. The forward head and shoulder angles were measured using the photogrammetry method according to the procedure described elsewhere 17,49 . The validity and reliability of this method have been established in previous studies 50,51 .
Thoracic kyphosis angle. The Flexicurve method was used to measure the static alignment of the thoracic spine, which is a well-established, valid, and reliable technique 52,53 . A detailed description of the procedure can be found in previous studies 17,42 . , and military press (exercise 5). Improvement phase exercises: side-lying external rotation with dumbbell (exercise 6), side-lying forward flexion with dumbbell (exercise 7), standing diagonal flexion with dumbbell (exercise 8), standing external rotation with Thera-band (exercise 9), standing diagonal flexion with Thera-band (exercise 10), abduction in sitting on a training ball (exercise 11), lying prone V, T, and W exercises (exercise 12), and abduction in standing on the balance board (exercise 13).