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Published in final edited form as: Clin Biomech (Bristol). 2021 Sep 21;90:105485. doi: 10.1016/j.clinbiomech.2021.105485

EVIDENCE FOR INCREASED NEUROMUSCULAR DRIVE FOLLOWING SPINAL MANIPULATION IN INDIVIDUALS WITH SUBACROMIAL PAIN SYNDROME

Amy K Hegarty 1, Melody Hsu 2, Jean-Sébastien Roy 3, Joseph R Kardouni 4, Jason J Kutch 1, Lori A Michener 5
PMCID: PMC8793937  NIHMSID: NIHMS1742952  PMID: 34571486

Abstract

Background:

Thoracic spinal manipulation can improve pain and function in individuals with shoulder pain; however, the mechanisms underlying these benefits remain unclear. Here, we evaluated the effects of thoracic spinal manipulation on muscle activity, as alteration in muscle activity is a key impairment for those with shoulder pain. We also evaluated the relationship between changes in muscle activity and clinical outcomes, to characterize the meaningful context of a change in neuromuscular drive.

Methods:

Participants with shoulder pain related to subacromial pain syndrome (n=28) received thoracic manipulation of low amplitude high velocity thrusts to the lower, middle and upper thoracic spine. Electromyographic muscle activity (trapezius-upper, middle, lower; serratus anterior; deltoid; infraspinatus) and shoulder pain (11-point scale) was collected pre and post-manipulation during arm elevation, and normalized to a reference contraction. Clinical benefits were assessed using the Pennsylvania Shoulder Score (Penn) at baseline and 2–3 days post-intervention.

Findings:

A significant increase in muscle activity was observed during arm ascent (p=0.002). Using backward stepwise regression analysis, a specific increase in the serratus anterior muscle activity during arm elevation explained improved Penn scores following post-manipulation (p<0.05).

Interpretation:

Thoracic spinal manipulation immediately increases neuromuscular drive. In addition, increased serratus anterior muscle activity, a key muscle for scapular motion, is associated with short-term improvements in shoulder clinical outcomes.

Keywords: shoulder pain, subacromial impingement, electromyography, spinal manipulation, persistent pain, shoulder

INTRODUCTION

Shoulder pain is a common condition, often chronic and affecting the ability to perform everyday tasks (Johannes et al., 2010, Luime et al., 2004). Subacromial pain syndrome (SPS) is defined as shoulder pain related to the structures within the subacromial space, and accounts for 44–65% of musculoskeletal shoulder pain complaints during a physician office visit (van der Windt et al., 1996, Saltychev et al., 2015, Tekavec et al., 2012). The prognosis of SPS can be poor, with 40–50% of patients reporting persistent pain 6 to 12 months after an initial consultation (Croft et al., 1996, van der Windt et al., 1996). Deficits in shoulder muscle activity may be important factors in the development and chronicization of SPS, and targeted motor training can reduce pain and improve function (Ager et al., 2019, de Oliveira et al., 2017, Østerås et al., 2009, Worsley et al., 2013). The question remains, do other conservative treatments such as spinal manipulation (SM) also have the ability to improve shoulder function by modifying shoulder muscle activity? Understanding the mechanism by which SM provides a clinical benefit can enable directed use in the treatment of patients with SPS.

Increased muscle activity has been commonly reported following SM, in both muscles directly contiguous to the spine (e.g., paraspinals and lower trapezius) and those distal to the site of manipulation at the spine (e.g., ankle plantar flexors and biceps brachii) (Bicalho et al., 2010, Christiansen et al., 2018, Cleland and Caron, 2004, Dishman et al., 2008, Dunning and Rushton, 2009, Haavik and Murphy, 2012, Niazi et al., 2015, Nougarou et al., 2013). For individuals with SPS, there are therapeutic benefits of thoracic SM when used alone and combined with exercise (Pieters et al., 2020); however, underlying mechanisms associated with clinical outcomes are unclear. Evidence suggests SM increases shoulder muscle activity during arm elevation (Muth et al., 2012); however, these results were limited by small sample size and a lack of connection between motor control changes and clinical symptoms. Previous work from our lab suggests SM has minimal effects on spinal motion, and pain sensitivity for individuals with SPS (Kardouni et al., 2015a, Kardouni et al., 2015b). We propose SM provides a therapeutic benefit by: (1) inducing central changes in sensorimotor processing to increase muscle activity necessary for active control of the shoulder, and (2) improving short-term shoulder function and pain associated with SPS (Figure 1).

Figure 1.

Figure 1.

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Theoretical model identifying the mechanism of shoulder pain development for individuals with subacromial pain syndrome (SPS) and the mechanism by which spinal manipulation may intercede in this cycle. Spinal manipulation is hypothesized to affect sensorimotor processing in the central nervous system, leading to measurable changes in muscle activity using electromyography (EMG). Dashed arrows represent a broken or reduced connection after the application of spinal manipulation (SM).

Altered shoulder muscle activity has been observed in those with SPS (Kinsella and Pizzari, 2017, Michener et al., 2016), and during evoked (acute) painful stimuli in healthy individuals (Diederichsen et al., 2009, Stackhouse et al., 2013). Decreased shoulder muscle activity of the upper trapezius, anterior deltoid, and infraspinatus (Diederichsen, Winther, 2009) and balance between the serratus and lower trapezius (Michener, Sharma, 2016) in particular may relate to impaired shoulder function (Figure 1). Mechanistically, SM may alter aberrant shoulder muscle activity by targeting direct motor pathways or indirectly by altering pain modulatory effects.

Here we evaluate the effects of thoracic SM on shoulder muscle activity for individuals with SPS. We hypothesize that SM will lead to an increase in muscle activity, and that change in EMG activity will be associated with a short-term improvement in self-report shoulder pain and function.

METHODS

1.1. Participants

This study evaluated individuals with SPS (n=28) to evaluate the effects of spinal manipulation in individuals with SPS performed between November 2012 and April 2013. Inclusion criteria were: 1) pain ≥ 6 weeks, 2) average shoulder pain ≥ 2/10 on an 11-point scale, 3) be 18–60 years, 4) 3 of 5 positive signs of SPS: Hawkins Test, Neer Test, pain during active elevation, pain or weakness with the Jobe/Empty Can test, and pain or weakness with resisted shoulder external rotation with the arm at the side of the body (Michener et al., 2009). Exclusion criteria were: 1) history of shoulder, cervical spine, or thoracic spine surgery, 2) primary complaint of neck or thoracic pain, 3) signs of central nervous system involvement such as sensory disturbances within the hands or face, unsteadiness during walking or pathological reflexes, 4) signs of cervical nerve root involvement, 5) contraindications to manipulative therapy including hypermobility, instability or severe arthrosis of the thoracic spine, 6) primary diagnosis of adhesive capsulitis, 7) primary instability of the shoulder, or 8) reproduction of shoulder or arm pain with cervical rotation to the ipsilateral side, axial compression, or Spurling’s Test. Data collection was conducted under the approval of the University’s Institutional Review Board (#HM13363). Participants were provided verbal and written explanations of the study, and signed an informed consent to participate.

1.2. Procedures

Participants underwent thoracic SM therapy (n=28), with 1 participant removed from analysis due to poor muscle activity signal quality, resulting in n=27 participants. Participants completed the Pennsylvania Shoulder Score, a self-reported questionnaire on shoulder function (Penn, 0–100, with 100=no pain, full satisfaction, and full function), at baseline and 2–3 days post-intervention. The Penn has been shown to be reliable and valid, with a minimum clinically important difference of 11.4 points (Leggin et al., 2006). Numeric pain rating scale (NPRS, 0= no pain, 10= extreme pain), which is reliable and responsive in patients with shoulder pain (Mintken et al., 2010), was also completed at baseline to assess current shoulder pain. Muscle activity was recorded during arm elevation tasks prior to and immediately following the SM intervention. The SM intervention was applied by a physical therapist to the thoracic spine as depicted in Figure 2 (Kardouni, Pidcoe, 2015a). Each technique was applied two times to the lower, middle, and upper (cervico-thoracic junction) thoracic spine, for 6 total SM applications.

Figure 2.

Figure 2.

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Methodology of spinal manipulation techniques and electromyography placement. Thoracic spinal manipulation was administered to the cervicothoracic junction (A) with the patient in a seated position, and to the middle (B) and lower (C) thoracic spine with the patient in a prone position. Placement of all electromyography sensors (D) over muscle bellies of the superficial rotator cuff and periscapular muscles are also shown. The middle deltoid electrode was placed at the point midway between the acromion process and the insertion of the deltoid muscle, in line with the posterior acromion process and insertion of the deltoid. The infraspinatus electrode was placed 1 inch inferior to the scapular spine at a point midway between the root of the scapular spine and posterior acromion process. The upper trapezius electrode was placed at the midpoint of line connecting the spinous process of the first thoracic vertebra and the acromion process. The middle trapezius electrode was placed lateral of the midpoint between the spinous process of the third thoracic vertebra and the root of the scapular spine. The lower trapezius electrode was placed immediately lateral to the midway point between the spinous process of the seventh thoracic vertebra and the inferior angle of the scapula, along a line connecting the posterior acromion process and seventh thoracic vertebra. The serratus anterior electrode was placed along the mid-axillary line over rib six for the lower portion of the serratus anterior, with the participants arm at 90° of elevation in the scapular plane. Confirmation was made that the serratus anterior electrode was not placed over the latissimus dorsi with a muscle test for the latissimus dorsi. A reference electrode was affixed with adhesive tape on the contralateral olecranon process.

1.3. Surface Electromyography

Muscle activity was recorded using dual silver bar pre-amplified surface EMG electrodes (Bagnoli-8; Delsys Inc, Boston, MA) with a 10 mm inter-electrode distance, amplification factor of 10,000, and a common mode rejection ratio >92 dB at 60 Hz. Raw EMG data were collected at 960Hz using a 16-bit analog to digital converter and synced with kinematic data within Motion Monitor (Innovative Sports Training, Inc, Chicago, IL). Surface electrodes were affixed on the skin over 6 muscles: middle deltoid, upper, lower, and middle trapezius, infraspinatus, and serratus anterior (Figure 2) (Ekstrom et al., 2004, Ludewig et al., 1996, Perotto, 1994).

EMG was processed via Motion Monitor and MATLAB software (The MathWorks, Inc; Natick, MA). A researcher blinded to group (pre or post measures) analyzed all data. EMG signals were bandpass filtered with a second order zero-lag butterworth filter from 20Hz-400Hz and notch filtered with a 0.5Hz width notch at 60 Hz within Motion Monitor. EMG signals were then rectified and smoothed using a 50 ms moving average window within MATLAB 2019a. The average EMG amplitude within each muscle was calculated during two time periods: (1) humeral ascending phase of 30° to 120°; and (2) humeral descending phase of 120° to 30°. EMG amplitude values were normalized by a single maximal effort contraction (MVC) verified to activate the targeted muscles (Burden, 2010), prior to the SM intervention.

MVC-contraction was performed at 90° of elevation, with the participant pushing maximally upward via their wrist against a stabilized device for 5 seconds (Cram J, 1998), and repeated twice to ensure maximal effort. In pilot testing, 6 separate muscle tests resulted in increased shoulder pain and fatigue, therefore a single MVC task was chosen for EMG normalization. EMG signals were filtered as described above, rectified, and smoothed using a moving average window of 250 ms. A 3 second window was manually defined to capture a window of maximal effort from each muscle during the MVC. The maximum EMG value recorded during the interval of interest was used as each muscle’s reference value.

Three dimensional kinematics of the humerus were measured with an electromagnetic tracking system (Polhemus 3Space Fastrak electromagnetic-based motion capture system (Polhemus, Colchester, VT)) integrated with Motion Monitor software. The thoracic sensor was placed on the sternum, and the humeral sensor on the distal posterior arm (Wu and Cavanagh, 1995, Wu et al., 2005). Bony landmarks were digitized per International Society of Biomechanics (ISB) protocol (Wu, Van der Helm, 2005). Kinematic data were sampled at 30 Hz and humeral elevation angles, measured as the relative angle between the humerus and trunk, were used to define event markers for the EMG analysis. Humeral elevation velocity was calculated using backward stepping numerical differentiation, and an average velocity was calculated during the ascending phase (30°–120° humeral elevation) and descending phase (120°–30° humeral elevation) to match analysis of EMG.

Active arm elevation task was performed with a 1.36 kg (3 lbs) hand-held weight for participants weighing less than 68 kg, or 2.27 kg (5 lbs) for those more than 68 kg. Five repetitions of active arm elevation in the scapular plane were performed at a standard rate of 3 seconds up, 3 seconds down with a verbal count for velocity. A visual cue of a guide pole maintained the plane of motion. Dynamic EMG and humeral elevation data were averaged for each participant across the 3 middle repetitions of arm elevation prior to and after intervention, resulting in a single scalar value for each participant before and after intervention.

Before beginning EMG analysis, we estimated the sample size needed based on effect sizes from previous SM studies. Previous studies suggest changes in electromyography and maximum force production, which is closely tied to EMG magnitude, following SM range from effect sizes of 0.5 – 2.0 (Christiansen, Niazi, 2018, Holt et al., 2019, Niazi, Turker, 2015). Using a conservative effect size of 0.5, and estimated power of 82% for a two tailed paired t-test, a sample size of 27 participants was needed.

Data from this study are available upon request. Suitability of a data request and access to the data will be made on an individual basis.

1.4. Data Analysis

All statistical analyses were performed in MATLAB 2019a. The change in Penn shoulder score, was assessed using a paired t-test (ɑ=0.05). The immediate change in muscle activity for each muscle was assessed separately during the ascending phase (30°–120° humeral elevation), and the descending phase (120°–30° humeral elevation) using a linear regression model (ɑ=0.05). Change in muscle activity over time (post-pre) was the dependent variable (Y), with independent categorical variables for muscle and a confounding variable of no interest of arm velocity. Arm velocity was an important confound of no interest as muscle contraction velocity is directly tied to excitation amplitude and only partially controlled in the study using a verbal metronome (e.g. Komi et al., 1987). The overall treatment effect (model intercept) and muscle main effect (differing effect at any measured muscle) were tested using an anova F-test (ɑ=0.05). Finally, a linear regression model was used to explore potential important explanatory variables for the observed short term (2–3 day) change in Penn score. A backward stepwise model selection method was used to identify the significant explanatory variables, where change in Penn over time was the dependent variable (Y) and change in muscle activity following intervention from each muscle (i.e. trapezius-upper, middle, lower; serratus anterior; deltoid; infraspinatus) were entered as independent variables (X1 – X6) and baseline shoulder pain was entered as a confound of no interest. Baseline shoulder pain was an important confound of no interest as pain intensity is often a strong predictor of symptom resolution. A separate backward selection model was used for muscle activity during arm descent (ɑ=0.05).

Reliability of EMG was assessed in a subset of SPS study participants (n=43, n=21 from this study) with consistent collection methods, using two repeated trials of the arm elevation tasks with no intervention provided between assessments. Intraclass correlation coefficients (ICC) were calculated using EMG for each muscle both during arm ascent and descent elevation consistent with procedures performed in this study. Repeated measures were taken within the same testing session without removal of the EMG sensors. The standard error of EMG amplitude during arm ascent and arm descent for each muscle was calculated as follows [SEM = standard deviation × (1-ICC)1/2]. The minimum detectable change was calculated as [MDC = SEM × (2)1/2]. The overall reliability of EMG amplitude measurements was high. The ICC(3,2) ranged from 0.94–0.99 across all muscles and task conditions; with the MDC ranging from 0.4–3.2 %MVC.

RESULTS

Participant demographics are in Table 1 that include baseline shoulder pain. Thoracic SM led to a significant increase in the Penn score, assessed 2–3 days after intervention (p<0.0001, CI95%: [4.7, 12.2], Table 1). A summary of EMG muscle activity measured during the ascending phase and descending phase immediately prior to, and following SM are shown in Table 2 (A–C). Average velocity of arm elevation, relative to the trunk was higher during the ascending phase after the intervention (p<0.046, Table 2D). There was an overall increase in muscle activity during the ascending phase of arm elevation following the intervention (p=0.002) irrespective of arm velocity changes, but there was no significant effect of muscle suggesting all instrumented muscles had a similar response to SM. No significant increase in muscle activity was found during the descending phase of arm elevation after controlling for arm velocity (p>0.05). The number of participants with EMG changes larger than the MDC ranged from 3 (11%, lower trapezius descending phase) to 15 (58%, deltoid ascending and descending phase); see Supplemental Table.

Table 1.

Demographics and physical measures for all participants. Unless otherwise specified, all values are reported as group mean (standard deviation).

Baseline Follow Up 48–27 hours later
Age (years) 31.0 (11.9)
BMI (kg/m2) 26.1 (5.99)
Dominant shoulder tested, n (%) 14 (50%)
Male, n (%) 12 (43%)
Shoulder Pain (NPRS, 0–10, 0=no pain, 10=severe pain) 3.5 (1.3)
Penn Shoulder Score (0–100; 100 = no pain, full satisfaction and function) 70.9 (11.0) 79.4 (11.9)
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Table 2.

Muscle activity during the ascending phase (A) and descending phase (B) of arm elevation reported before (pre) and immediately following (post) thoracic spinal manipulation, adjusted for changes in arm velocity. Unless otherwise specified, all values are reported as group mean (standard deviation) with units %MVC. Adjusted and unadjusted means, adjusted mean differences (post-pre), 95% confidence interval (CI), and p-values are reported. Humeral elevation velocity is reported as the average velocity while the humerus is between 30°–120° of elevation during the ascending and descending phases. n.s. - not significant.

Un-Adjusted Pre (%MVC) Un-Adjusted Post (%MVC) Adjusted Pre (%MVC) Adjusted Post (%MVC) Adjusted Mean Difference (95% CI), P Value
A. Ascending Phase (30°–120°)
Grand Mean (Overall Treatment Effect) 33.5 (15.2) 35.9 (15.9) 33.5 (15.2) 35.0 (15.9) 1.50 (0.58, 2.43) p=0.002
 Deltoid 30.2 (10.4) 32.6 (11.0) 30.2 (10.4) 31.5 (11.0) -
 Upper Trapezius 44.2 (12.9) 48.4 (16.3) 44.2 (12.9) 46.7 (15.6) -
 Infraspinatus 29.9 (12.0) 33.2 (14.6) 29.9 (12.0) 31.6 (13.9) -
 Serratus Anterior 42.4 (22.4) 44.2 (19.9) 42.4 (22.4) 43.5 (20.8) -
 Middle Trapezius 26.8 (11.8) 27.9 (12.0) 26.8 (11.8) 26.6 (11.6) -
 Lower Trapezius 26.8 (8.9) 28.7 (9.2) 26.8 (8.9) 27.9 (9.0) -
B. Descending Phase (120°–30°)
Grand Mean (Overall Treatment Effect) 16.6 (7.0) 17.5 (8.0) 16.6 (7.0) 16.2 (7.8) −0.44 (−4.0, 3.1) p n.s.
 Deltoid 16.2 (6.7) 18.0 (7.6) 16.2 (6.7) 16.6 (7.7) -
 Upper Trapezius 18.3 (6.8) 18.5 (6.8) 18.3 (6.8) 16.9 (6.7) -
 Infraspinatus 18.5 (6.8) 19.1 (8.5) 18.5 (6.8) 17.4 (8.4) -
 Serratus Anterior 18.6 (9.2) 18.5 (8.5) 18.6 (9.2) 17.2 (8.7) -
 Middle Trapezius 13.5 (5.4) 15.2 (7.3) 13.5 (5.4) 13.8 (7.3) -
 Lower Trapezius 14.4 (5.5) 15.4 (7.4) 14.4 (5.5) 14.3 (7.5) -
C. Humeral Velocity
Humeral Elevation Velocity (°/s) Ascending phase 82.5 (18.2) 88.2 (16.5) - - 5.8 (0.86, 10.7) p=0.023
Humeral Elevation Velocity (°/s) Descending phase 65.0 (10.6) 69.0 (13.6) - - −4.0 (−7.8, −0.08) p=0.046
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Short term increases in Penn score was predicted by increased serratus anterior muscle activity both during ascending phase (p=0.049) and descending phase (p=0.035) after controlling for baseline pain (Figure 4).

Figure 4.

Figure 4.

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Relationship between clinical outcome and muscle activity response to spinal manipulation (SM). Positive differences indicate an increase in clinical outcomes score and increase in muscle activity after intervention. Panel A shows the relationship between change in Penn Shoulder Score and change in surface electromyography (EMG) following intervention, for the serratus anterior during arm ascent (30° to 120° humeral elevation). Panel B shows the relationship between change in Penn and change in EMG following intervention, for the serratus anterior during arm descent (120° to 30° humeral elevation).

DISCUSSION

One proposed mechanism of SM is facilitation of muscle activity. Motor facilitation may be brought on by changes in sensorimotor processing (Bialosky et al., 2018, Haavik and Murphy, 2012), which may be particularly important for individuals with SPS with demonstrated deficits in activation of both glenohumeral and scapulothoracic muscle (de Oliveira, Bouyer, 2017, Kinsella and Pizzari, 2017). In this study, we identified a widespread immediate increase in shoulder muscle activity following the SMT intervention, with a subsequent improvement in patient-reported functional outcomes 2 to 3 days after SM.

The increases in EMG amplitude was not specific to those muscles contacted by the therapist during the intervention or attached to the thoracic spine, suggesting direct touch or mechanical effect on the thoracic spine were not responsible for the observed changes in muscle activity. Interestingly, all muscles demonstrated a relative increase in muscle activity after the SM intervention during the ascending phase, with no specific effects for any of the individual instrumented muscles. There was no significant overall change in muscle activity during the descending phase. The higher demand during the ascending phase may explain the overall larger treatment effect on EMG in the ascending phase compared to the descending phase. The low magnitude of EMG changes may reflect the immediate transient changes in neuromuscular drive associated with manual interventions.

We identified increased muscle activity following SM independent of increases in arm velocity, therefore, increases in EMG are likely not the result of a learning effect from shoulder elevation task repetition, but rather reflect changes induced by SM. Further, observed relationships between change in patient-reported outcomes measured 2 to 3 days after the SM intervention and muscle activity changes immediately following intervention suggest the changes in muscle activity may be one mechanism leading to short term improvement in shoulder function.

The serratus anterior is a key muscle to stabilize the scapula, and contributes and controls scapular upward/downward rotation during arm elevation. Patients with SPS display dysfunctional scapular upward rotation and serratus muscle activity deficits (Ratcliffe et al., 2014, Struyf et al., 2014, Timmons et al., 2012). In particular, deficits in the ratio between the serratus and the trapezius muscle activity (Michener, et al., 2016). The serratus anterior dysfunction is thought to directly contribute to SPS, as scapular control and stability is important to reduce both the potential for compression and overload of the rotator cuff tendons (Seitz et al., 2011). This study presents an exciting link between supplemented neuromuscular drive among many shoulder muscles, and a direct link between the increase in serratus anterior activity and the positive short-term clinical benefit in shoulder symptoms and function.

Pain inhibition within the central nervous system is also a supported mechanism explaining the benefits of manual therapy (Bialosky, Beneciuk, 2018, Bialosky et al., 2009, Coronado et al., 2012). SM can impact brain function within areas where pain is processed (Gay et al., 2014, Maiers et al., 2014, Sparks et al., 2013, Weber II et al., 2019). Further, interference of voluntary muscle activity via pain is commonly reported (Diederichsen, Winther, 2009, Stackhouse, Eisennagel, 2013), and related to deficits in arm motion and function in people with shoulder pain (De Mey et al., 2012, Michener, Sharma, 2016). Previous studies have also identified motor facilitation with SM, suggesting SM does not simply restore aberrant processing but may also augment sensorimotor integration even in healthy individuals (Bicalho, Setti, 2010, Cardinale et al., 2015, Christiansen, Niazi, 2018, Cleland and Caron, 2004, Niazi, Turker, 2015). Both motor facilitation and changes in pain perception may play critical roles in improved muscle activity and patient-reported function observed in this study.

A strength of this study is the delivery of SM to a body region free from pain. This allowed us to examine the mechanism of SM independent of the effect on pain at the site of delivery of the SM. This study enables us to begin to disentangle the effects of SM including that of pain inhibition and motor facilitation.

This study demonstrated that thoracic SM leads to an immediate increase in muscle activity, linked to short term changes in patient reported shoulder pain, function and satisfaction. Participants did not have ultrasound imaging, which can be beneficial to confirm the diagnosis of SPS and rule out other competing causes of shoulder pain. Moreover, participants had a moderate to low level of pain, which may have dampened the response to treatment. Further, the study is limited by the lack of a comparator group. While changes in EMG and shoulder function were not compared against a no-treatment control group, we are confident the present study provides evidence that changes in neuromuscular control may be one component of short term improvement in shoulder pain. It is well supported in the literature that SM both leads to increased motor drive in healthy individuals (e.g. Bicalho et al., 2010, Christiansen et al., 2018, Cleland and Caron, 2004, Niazi et al., 2015, Nougarou et al., 2013)., and can reduce clinical symptoms (e.g. Pieters et al., 2020) in musculoskeletal pain conditions. Our study provides evidence that neuromuscular drive may be increased for individuals with SPS following SM, and that the muscle activity changes are related to clinical symptoms. Future studies should consider the inclusion of a no-treatment or no-touch control group, with special consideration for the challenges of assessing a centrally mediated therapy. In this study we addressed this main limitation by determining if our findings were greater than measurement error as determined by the included test-retest reliability. Because we aimed to determine central changes of SM, a comparator of the contralateral painless shoulder or a sham manipulation involving touch that can facilitate muscle activity was not possible.

CONCLUSION

Thoracic SM induced immediate widespread increase in shoulder muscle activity irrespective of arm velocity, suggesting an increase in neuromuscular drive following treatment. Immediate increase in muscle activity of the serratus anterior, a key muscle in scapular motion, was related to clinical improvement of shoulder symptoms and function following treatment. These findings support the use of thoracic SM as a therapy to immediately induce increased muscle activity even for body regions distal to the site of manipulation. Further, this study contributes to the overarching hypothesis that thoracic manipulation works by inducing centrally mediated changes in neuromuscular drive and pain inhibition.

Supplementary Material

1

Figure 3.

Figure 3.

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Change in surface electromyography (EMG) immediately following spinal manipulation (SM) adjusted for change in arm elevation velocity. Positive differences indicate an increase in muscle activity after intervention. Main effect of the grand mean change in muscle activity (collapsed across muscles) are shown as gray dashed lines. Each muscle EMG’s average response and 95% confidence interval is depicted in the red diamond marker, and each dot represents each individual participant response. Panel A shows differences during the ascending phase of arm elevation between 30° and 120° humeral elevation. Panel B shows differences during the descending phase of arm elevation between 120° and 30° of humeral elevation. All EMG differences are normalized by a single maximal effort reference contraction (MVC).

Highlights.

  • Shoulder muscle activity is a key deficit in those individuals with shoulder pain

  • Spinal manipulation increased shoulder muscle activity in patients with shoulder pain

  • Shoulder muscle activity was related to improved shoulder pain and function.

  • Neuromuscular drive mechanism may optimize use of manipulation

Funding / Statement of the sources of grant support

This work was supported by the Charles D. and Mary Bauer Foundation, and the National Institute of Diabetes and Digestive and Kidney Diseases R01 DK110669.

Footnotes

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Conflict of Interests

All authors declarations of interest: None

Statement of financial disclosure and conflict of interest

Authors of this work have no financial disclosures or conflicts of interest to disclose

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