1.

Introduction

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Chronic neck pain is a musculoskeletal disease associated with remarkable functional disabilities,

with approximately 23% overall prevalence (Hoy et al. , 2010). Patients may present with chronic local

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symptoms with various compensatory adaptations developed in other associated regions, e.g., dysfunction

of the thoracic spine and upper limb (Kahlaee et al. , 2017). Due to the close relationship between cervical

and thoracic spine in terms of anatomy and biomechanics, neuromusculoskeletal adaptations including

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dysfunction of mobility manifested with smaller craniovertebral angle i.e., forwarded head posture, and

greater thoracic curvature, and impairment of strength as well as motor control between muscles at the

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cervical and thoracic region had been reported (Falla and Farina, 2008, Kapreli et al. , 2008, KAYA and

ÇELENAY, 2017, Lau et al. , 2010a).

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Classical manifestations of the impairment reported in chronic neck pain population including neck

range of motion restriction, muscle weakness and fatigability, recruitment alternations expressed in delayed

onset of the deep stabilizers and over- or under-activity of the prime movers of the cervical spine, head-
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neck posture mal-alignment, proprioceptive deficits, and psychological dysfunctions (Dimitriadis et al. ,

2013b, Falla et al. , 2004a, Falla et al. , 2003, Gogia and Sabbahi, 1994, Kim et al. , 2018, Mäntyselkä et
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al. , 2010, Silva et al. , 2009). Meanwhile, the respiratory function is predominantly dependent on the

capacity of the primary respiratory muscles, i.e., diaphragm (DF), intercostal muscles and abdominal
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muscles, meanwhile, the cervical muscles namely the scalene, sternocleidomastoid (SCM) and trapezius

muscles serve as the accessory muscles to assist in respiratory function when necessary (de Paleville et al. ,

2011, De Troyer and Boriek, 2011, Ratnovsky et al. , 2008). With the aforementioned impairments
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developed in individuals with chronic neck pain, further demand on these cervical muscles in response to

augmented respiratory requirement associated with strenuous physical activity may have a negative impact
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on the health of the cervical spine (Kahlaee, Ghamkhar, 2017, Kapreli, Vourazanis, 2008).

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 Respiratory muscles deficits may further contribute to low lungs volume, hypoventilation, and

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limited exercise capacity, which had been found in some patients with chronic neck pain (Dimitriadis et al.

, 2014, Yalcinkaya et al. , 2017). Maximal inspiratory and expiratory pressures (MIP and MEP) are

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commonly used to quantify the respiratory muscle strength and force production non-invasively (Clanton

and Diaz, 1995). To further investigate the respiratory muscle activation pattern in chronic neck pain

patients, surface electromyography (EMG) has been frequently applied to reveal the recruitment pattern

and fatigability (Ludin, 1995, Weiss, 2016). Previous studies showed that reduced respiratory function

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reflected by MIP and MEP, faulty breathing pattern and higher fatigability of accessory muscles including

SCM, anterior scalene (AS) and upper trapezius (UT), were detected in chronic neck pain patients at resting

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conditions (Dimitriadis, Kapreli, 2013b, Falla, Rainoldi, 2003, Gogia and Sabbahi, 1994). At rest, primary

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respiratory muscles played the major role for respiration while the abdominal muscles, as the expiratory

pressure generator, are responsible for forceful expiration during exercise (Aliverti, 2016, Welch et al. ,
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2019). The increase in rib cage expandability enables the lung volume increment for meeting the additional

requirement of the respiratory function related to exercise exertion. Compensatory recruitment of the

accessory muscles may occur if the primary respiratory muscles fail to fulfill the escalated demand (Aliverti,
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2016, Welch, Kipp, 2019). However, changes of respiratory function and activation pattern of those

involved muscles as well as the potential impact of chronic neck pain for meeting the respiration demand
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during submaximal exercise are yet to be examined.

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This study aimed to investigate the alteration of respiratory function in chronic neck pain patients

during submaximal exercise test. The hypotheses of this study were:

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 Participants with chronic neck pain display

1. a higher level of activity and/or greater fatigability in the accessory respiratory muscles (including
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AS, SCM and UT), but a lower activity and/or fatigability in the primary respiratory muscles

(including DF, and external intercostals (EI)); and

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 2. a reduction in respiratory muscle strength measured by MIP and MEP;

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throughout the submaximal exercise test, compared to health controls.

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2. Methods

2.1. Study Design

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A cross-sectional comparative study was conducted with ethical approval obtained from the Human

Subject Ethics Review Committee of the Hong Kong Polytechnic University (Reference no.:

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HSEARS20201208003, Appendix 1). Declaration of Helsinki followed in this study and written informed

consent was obtained from each participant (Appendix 2) and risk stratification of exercise testing

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(Appendix 3) was performed prior to the data collection.
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2.2. Participants

Fifteen adults with chronic neck pain more than 3 months and aged between 18 to 40 years
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old (as neck pain, NP group) and fourteen age- and gender-match healthy controls (those reported to be

asymptomatic for more than 1 year) were recruited voluntarily from the local community using poster
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advertisements. All participants were able to read Chinese and to complete the self-administered

questionnaires included in this study. Individuals were excluded if they had any of the followings: (i) known
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cardiopulmonary diseases including chronic obstructive cardiopulmonary disease, uncontrolled

hypertension, heart failure, lung cancer etc.; (ii) current or ex-smoker; (iii) any known congenital

musculoskeletal abnormalities (Lau, 2013); (iv) rib cage deformity of congenital, traumatic or operational
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cause; (v) acute infection; (vi) not compliant to submaximal exercise; (vii) neuromuscular disorder; (viii)

history of neck or cardiopulmonary surgery or any acquired comorbid disability that would preclude the
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 assessment; (ix) contraindicated to exercise test as recommended in ACSM guideline of exercise testing

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(Riebe and American College of Sports Medicine, 2018).

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2.3. Instrumentation and procedures

2.3.1. Baseline measurements

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The participants’ demographics, daily physical activity level by International Physical Activity

Questionnaire-Chinese version (IPAQ-C) (Committee, 2016) , neck pain intensity by 11-point Numeric

Pain Rating Scale (NPRS 0-10) and the Nijmegen Questionnaire for detection of the hyperventilation

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syndrome (HVS) (van Dixhoorn and Duivenvoorden, 1985) were assessed at baseline. The forward head

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posture and thoracic spine kyphotic changes were assessed by the craniovertebral angle (CV angle) and

occiput-to-wall distance respectively (Lau et al. , 2010b, Suwannarat et al. ). The mobility and curvature
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of the thoracic spine (1st to 12th Thoracic vertebrae level) were derived from the sagittal profile scanning

between C7 and S2 using the spinal goniometry (The Spinal Mouse®, Idiag, Fehraltorf, Switzerland), a

handheld non-invasive electromechanical device and customized algorithm was used to assess the sagittal
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curvature and ROM of the thoracic spine of each participant (Mannion et al. , 2004). The scanning

procedures was conducted in three positions including natural standing, forward flexion to maximum and
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extension to maximum of the trunk in standing (KAYA and ÇELENAY, 2017). The sagittal thoracic spinal

curvature and mobility (between 1st to 12th Thoracic vertebrae level) were then be computed based on the
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differences measured between the data captured in these three specified positions (Mannion, Knecht, 2004).

Excellent intra-tester and inter-tester reliability of the Spinal Mouse device was demonstrated in the

previous study with ICC > 0.8 and 0.95 respectively (Mannion, Knecht, 2004, Post and Leferink, 2004).
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2.3.2. Submaximal exercise testing

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 A lower limb ergometry submaximal testing using the MONARK 894 E was selected in this study

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as to minimize the effect of exercise task nature to the neck muscles recruitment. The exercise testing was

conducted with adherence to the guidelines recommended by ACSM and the termination criteria of exercise

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test reported in previous literature (Gappmaier, 2012, Riebe and American College of Sports Medicine,

2018). The seat height was adjusted individually, and participants were asked to rest their arms on the arm-

support positioned on the sides of the ergometer to minimize the activation of their neck muscles caused by

unrelated upper limb movements during the exercise test.

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Firstly, the participants started with a 2-minute warm up phase and were required to achieve 60

revolution per minute. The participants were asked to reach the submaximal heartrate (HR) zone [(50-85%

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of the maximum heartrate (HRmax)] before the end the warm up phase. The loading discs, 1kg per time,

was added if the participant was unable to reach the target zone within the 2-minute warm up phase. Then,
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the participants were asked to perform the ergometry within the submaximal exercise HR zone for 6 minutes

after the warm up phase, which defined as submaximal phase. A 2-minute cool down phase was commenced

immediately after the submaximal exercise testing at their comfortable pace. A 2-minute static recovery
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phase was continued after cool down phase with complete rest on the ergometry.
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2.3.3. Primary outcome measures

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Respiratory Muscle Strength

The respiratory muscle strength was measured by MIP and MEP for revealing the underlying
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impairment of the respiratory function associated with physical exertion. MIP and MEP measurements

using a handheld respiratory pressure meter (±300cm H2O) (MicroRPM®; Micro Medical, Chantham, UK),
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were performed before the exercise testing as baseline (T1), the start of the submaximal phase (T2), the

termination of submaximal phase (T3), post-cool down phase (T4) and post-static recovery phase (T5) of

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 the exercise test (refers to Fig. 1). Three trials were performed at each of the 5 specified time intervals and

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the maximum value was recorded for comparison (Kapreli et al. , 2009). In assessing MIP, the participants

were asked to give maximal inspiratory effort after starting from maximal exhalation, whereas MEP was

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measured after starting from maximal inhalation. One-off disposable mouthpiece with an inbuilt filter was

used by each participant for infectious control measures.

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Surface Electromyography

Besides the MIP and MEP described above, surface EMG of AS, SCM, UT, DF, and EI muscles were

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recorded bilaterally at a sampling frequency of 1000Hz and bandwidth of 10-500Hz (MyoMuscle, Noraxon

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Inc., USA). The EMG electrodes for the selected muscles were placed according to previous research

(Table 1)(Aliverti, 2016, Welch, Kipp, 2019)< 10kΩ using standardized skin preparation procedures
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(cleaning and light abrasion of skin with medical sandpaper before electrode attachment) with the inter-

electrode distance of 2cm. Two assessors placed all the electrodes for all participants. The EMG was

recorded continuously during the submaximal exercise test for assessing the changes in the amplitude and
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fatigability of the primary and accessory respiratory muscles, and 2 minutes after the test ended (defined as

static recovery phase) as primary outcome measures.

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2.3.4. Secondary outcome measures and vital sign monitoring

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For monitoring of the physiological responses of the participants, the Rate of Perceived Exertion

(RPE) and neck pain intensity in terms of NPRS were recorded at every minute of the exercise protocol to
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determine the level of exertion and changes in neck pain towards submaximal exercise respectively

throughout the submaximal exercise testing protocol as secondary outcome measures (Scherr et al. , 2012).
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Meanwhile, vital signs including the HR and peripheral oxygenation (SpO2) were recorded in specific time-

point in every minute; while BP was recorded in the 0, 3, 9 and 11-minute (without interfering the EMG

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 measurements) to establish the cardiovascular changes within the submaximal exercise challenge and

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monitor the safety of the testing protocol.

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2.4. Data Processing and Statistical Analysis

A customized program was used for all the data processing and analysis (MyoMuscle, Noraxon

Inc., USA). EMG was processed by standardized steps which include the full wave rectification and

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filtering with band pass of 10-500Hz. For amplitude analysis, the EMG signals was normalized to the

percentage of maximum voluntary contraction (%MVC) of the corresponding muscle for enabling

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comparison of the level of effort between muscles and across time. A 3-second window of the filtered

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signals of the targeted muscles from participants at the 5 specified time intervals during the test for

unraveling the various phases of the exercise testing, i.e., the during the 1st minute of warm up phase (T1),
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the 1st half-minute of the submaximal phase (T2), the last half-minute of submaximal phase (T3), the during

the 1st minute of cool down phase (T4) and static recovery phase (T5) were selected for data evaluation

(refers to Fig. 1). For fatigability analysis of the muscles, the median frequency was calculated during the
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whole exercise testing (Allison and Fujiwara, 2002).

Data was analysed by the IBM SPSS statistical software (version 26.0). Levene’s test and
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Kolmogorov-Smirnov test were applied to test for the homogeneity of variance and fitness of normality of

all the data, respectively. Mauchly’s test was used to test for sphericity. Independent T-test and Chi-square
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test were used to detect the between group difference depends on the nature of the data. Two-way repeated

measure ANOVA was used to detect the difference in the surface EMG amplitude, respiratory muscle

strength (MIP & MEP), neck pain intensity and RPE across the submaximal exercise testing protocol and
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between two groups of participants across different measurements with assumption that satisfied the

parametric analysis. Paired-t test with Bonferroni correction was conducted as post-hoc analysis if any
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significant difference was detected. For those data were not normally distributed, the Friedman test was

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 applied; and post-hoc analysis, using Wilcoxon signed-ranks tests, was performed if any significance

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difference was detected. The level of significance was set at 0.05 for all analysis except 0.01 for analysis

between and within group post-hoc analysis across the 5 intervals.

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[Insert Table 1 here]

[Insert Fig. 1 here]

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3. Results

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A total of 29 participants (15 in NP group and 14 in control group) with mean age of 26±3.16 years

and 26.14±1.92 years respectively were recruited in this study. Participants in NP group and control group

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were comparable with no significant between-group differences found in the demographics at baseline

(Table 2). Participants in both groups reported similar level of physical activity, hyperventilation symptoms,
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cervical posture, and curvature as well as mobility of their thoracic spines. Participants in NP group reported

neck pain intensity ranging from 2 to 8 of 10 on the NPRS, and duration of 4 to 96 months. Locations of

their neck pain were reported as over the left (n=9), right (n=3) and central (n=3) area of the cervical region.
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All the participants were right-hand dominant and were able to complete the submaximal exercise testing
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without termination with their heart rate maintained within the targeted zone during submaximal phase.

[Insert Table 2 here]

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3.1. Respiratory muscle strength (MIP and MEP)

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No significant difference in MIP or MEP was found between two groups at each time-point

(p>0.05). Two-way repeated ANOVA revealed that there was no significant time effect, group effect for
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both MIP and MEP (p>0.05) (Fig. 2).

[Insert Fig. 2 here]

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3.2. Electromyography amplitude analysis

3.2.1. Anterior scalene (AS)

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A significantly higher EMG amplitude was observed over AS in the NP group at T3 for right side

(p<0.01). There were also significant time effects and group effects for both sides (right: p=0.011; left

p=0.010) (Fig. 3a). Post-hoc analysis revealed significant differences in AS EMG amplitude between T3

and T1 for right AS (p=0.007), T3 and T2 (right: p=0.003; left: p=0.005), and T4 and T3 (right: p=0.005;

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left: p=0.006) bilaterally.

[Insert Fig. 3 a-f here]

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3.2.2. Sternocleidomastoid (SCM)
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No significant difference was retrieved between two groups at each interval for both sides (p>0.01).
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There were no significant time effects and group effects for SCM EMG amplitude for both sides (Fig. 3b).

3.2.3. Upper Trapezius (UT)

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No significant difference in UT EMG amplitude was observed between two groups for both sides
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at each interval (p>0.01). There were no significant time effects and group effects for UT EMG amplitude

in both sides (Fig. 3c).

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3.2.4. External intercostals (EI)

There was no significant difference in right EI EMG amplitude between two groups at each interval
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(p>0.01). There was no significant time effects and group effects for right EI EMG (Fig. 3d). Data analysis

for left EI was excluded in view of trace of available data.

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3.2.5. Diaphragm (DF)

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 No significant difference in right DF EMG amplitude was revealed between two groups at each

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interval (p>0.01). No significant time effects and group effects was found for right DF EMG amplitude as

well (Fig. 3e). There was a trace of available data for left DF EMG amplitude, data analysis was thus

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excluded.

3.3. Muscle fatigue analysis

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There was significant difference in left AS and left SCM EMG median frequency between two

groups. (Table 3). The NP group was more prone to fatigue when compared with control group in left AS

and SCM significantly during the submaximal exercise testing protocol. All the muscle listed demonstrated

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an observable difference that NP group were more prone to fatigue with a smaller median frequency, the

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results of other muscle group however yet to reach statistical significance.

[Insert Table 3 here]

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3.4. Rate of Perceived Exertion and neck pain

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The NP group reported a higher RPE level throughout the test, the difference was however

statistically insignificant (p>0.01) (Fig. 4a). No neck pain was reported from the control group throughout
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the test (Fig.4b). The values of the neck pain intensity reported by the NP group ranged from 0.53 to 0.8/10

on Numeric Pain Rating Scale 0-10 throughout the submaximal exercise test.
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[Insert Fig. 4 here]

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3.5. Vital Sign Monitoring

Monitoring of blood pressure (BP), heart rate (HR) and saturation of oxygenation (SpO2) was
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fulfilled the guidelines recommended by ACSM and no participant was required to terminate the exercise

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 test in both groups. The trend of both groups was similar. Generally, all the value of BP and HR started to

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increase after the commence of the exercise test, peak value for both outcomes were reached within the

submaximal phase. While the value of SpO2 was generally stable throughout the study. The HR of two

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groups were maintained within the targeted submaximal zone (50-85% HRmax) during submaximal phase.

The HR of both groups reached the highest at the 9th minute (1 minute after the start of cool down phase)

of the testing protocol, with the peak mean 132 and 121 beats per minute (bpm) for the NP group and

control, respectively. The HR started to return to the resting level for both groups after the peak reached.

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4. Discussion

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The present findings revealed that individuals with mild degree of neck pain reported a higher level

of perceived exertion and with higher HR compared to healthy individuals but a stable intensity of their
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neck pain during the submaximal exercise testing. Participants in both neck pain and healthy groups showed

the comparable levels of respiratory strength measured by the MIP and MEP during various phases of the

exercise test. Greater degree of recruitment of the inspiratory accessory muscles i.e., AS, SCM and UT of
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both sides were observed for participants in NP group, in which the between-group difference in the EMG

amplitude was particularly higher during submaximal phase (T2 to T3). Meanwhile in NP group, higher
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EMG amplitude was found in left AS, right UT and bilateral SCM at the static recovery phase compared to

the warm up phase. Such findings imply that these accessory respiratory muscles indeed required a longer
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recovery after stress related to the increased physical exertion. It is critical to observe the contrary response

displayed in the NP group with the compromised recruitment level of the primary inspiratory and expiratory

muscles, i.e., right EI and right DF throughout the exercise test. In addition, both accessory muscles and
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primary inspiratory muscles were found to be having a higher fatigability towards endurance type of

physical exertion, as expressed in the lower value of median frequency analysis compared to the healthy
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individuals. These novel findings on the adaptations of the recruitment pattern between the primary and

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 accessory muscles involved in respiration upon the augmented physical exertion may have a critical role in

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contributing to the chronicity and recurrence of neck pain.

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4.1. Respiratory muscle strength during and after submaximal exercise test

The normal reference values for MIP and MEP among Asians were 92.9 and 100.8 cmH2O

respectively (Sriboonreung et al. , 2021). Our NP group showed a marked deficit in their MIP (28% lower)

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and MEP (14% lower) performance at rest when compared with these norm values. Previous studies

demonstrated that MIP and MEP were indirect methods of gross respiratory muscle strength assessments

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with different degrees of primary and accessory respiratory muscles involvement during the MIP and MEP.

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The primary inspiratory muscles could be activated in both measurements, while abdominal muscles were

more activated in MEP and accessory inspiratory muscles such as SCM were more activated in MIP(Aslan
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et al. , 2019, Nava et al. , 1993, Walterspacher et al. , 2018). During the physical exertion in the submaximal

ergometry task (T1 to T3), healthy controls were able to achieve a higher level of the MIP and MEP

performance while the neck pain participants failed to do so. The rib cage is expected to contribute more
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through the increase in its expansion capacity to assist in the increment of tidal volume required under the

circumstance of physical exertion. Therefore, the recruitment of accessory inspiratory muscles would assist
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the diaphragm in achieving the respiratory demand (Welch, Kipp, 2019). In our NP group, the accessory

inspiratory muscles (e.g., AS, SCM and UT) demonstrated a higher level of recruitment and greater

susceptibility to fatigue in AS and SCM over the left side. Such manifestations suggested that these
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accessory respiration muscles were not able to spare additional reserve in performing the MIP tasks during

the submaximal exercise. This phenomenon can partly be explained by the inability of these cervical
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muscles to serve efficiently their dual roles i.e., as the prime movers of the cervical and accessory respiration

muscles in the presence of the coexisting neuromuscular impairment commonly found in chronic neck pain
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population.

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 Previous studies reported that MEP was more related to the neck pain intensity and disability than

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MIP (Dimitriadis et al. , 2013a, Dimitriadis, Kapreli, 2013b). In our study, the MEP of NP group showed a

trend to decline during the warm up phase and it returned to the baseline level during the end of submaximal

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phase. In contrast, an opposite trend was observed in control group. Although there was no statistically

significant difference in time-and-group interaction on MEP during the submaximal testing, the reverse

pattern of MEP performance after submaximal exertion observed in NP group concurs the previous findings

for which the neck pain intensity is associated with the reduction in MEP. The imbalance of superficial and

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deep neck muscle strength may further compromise the thoracic spine stability. The changes in rib cage

mechanics may induce compensatory pattern for forceful expiratory work. This deficit may not affect our

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expiration at rest substantially since expiration task is achieved by elastic recoil of the lung (Aliverti, 2016).

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However, when stress to the respiratory function reaches the threshold as the physical task is in place, the

recruitment of expiratory muscles at forceful level would be needed to address the increased demands. The
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expiratory muscles were not capable in maintaining the MEP generation when additional demand was

needed for submaximal breathing task. Unfortunately, the EMG data of RA failed to provide insight to this

specific finding of MEP, possibly due to the disturbance on the EMG signals on RA related to the repetitive
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hip knee flexions near the inner range during the lower limb ergometry test (Kelly et al. , 2007).
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Moreover, since the value of minimal clinical importance difference (MCID) of MIP and MEP has

not been well established in the literatures, it remains impossible to interpret the clinical significance of the
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difference in measurement obtained in the present study (IWAKURA et al. , 2020). However, this new set

of norms identified here would be useful for comparison of the findings emerge from forthcoming research.
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4.2. Electromyography analysis during and after submaximal exercise test

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 Study of the EMG amplitude helps reflect the relative effort of muscles involved in the task

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execution. Meanwhile, the median frequency analysis is defined as division of the power density spectrum

into two ranges i.e., higher versus lower frequency spectrum. The decrease in median frequency revealed

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from the spectrum analysis of the EMG signals is a validated method to objectively determine the fatigue

profile (high frequency) during sustained muscle contraction (Allison and Fujiwara, 2002). Researches have

indicated that a combination of a decrease in median frequency and an increase in amplitude were widely

accepted to imply the fatigability of muscle (Mannion et al. , 1998, Schiaffino and Reggiani, 2011).

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Muscles are composed of muscle fibers for which they are further classified into slow- and fast-

twitch fibers depending on their metabolism required for specific functions (Schiaffino and Reggiani, 2011).

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Majority of muscles in human are formed by combinations of muscle fibers at varied levels of composition.

Slow-twitch fibers (also known as Type I fibers) are mainly for performance of endurance task and fast-
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twitch fibers (also known as Type II fibers) are mainly for rapid and powerful task. Previous study revealed

that smaller proportion of slow-twitch fibers tended to have a greater slope of median frequency, which

was less resistant to muscle fatigue (Mannion, Dumas, 1998). Evidence showed that the superficial cervical
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flexors (predominantly the AS and SCM) were commonly found to be overactive in chronic neck pain
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patients (Falla et al. , 2004b). It was hypothesized that overactivity of AS and SCM compensate the

underlying delayed or inactivity of the deep cervical flexors. Moreover, previous study revealed that greater

percentage of Type II fibers were found in SCM and AS in chronic neck pain participants (Falla, Rainoldi,
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2003). For UT, histochemical study showed that Type II fibers were the main component of the muscle

which implied its primary function for supporting non-endurance type of tasks (Lindman et al. , 1990, 1991).
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The amplitudes of AS, SCM and UT were generally higher in NP group, and the between-group
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difference became profound shortly after the submaximal exercise commenced. This could be related to the

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 functional deficiency of these accessory respiratory muscles to assist the overall increase in respiratory

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demand in NP group, towards a prolonged increase in physical exertion. Moreover, amplitude of AS, SCM

and UT in general failed to return to baseline during the static-recovery phase was found only in NP group.

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Such altered functional capacities reflected by the discrepancy in physiological responses between the

symptomatic and healthy individuals warrant study to further investigate the reversibility as well as

effective interventions to optimize the dual functions of these cervical muscles involved in the neck region

and respiration for sufferers of chronic neck pain.

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Since the recruitment of AS, SCM and UT increased during submaximal exercise, and these

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muscles were mainly composed by Type II fiber, these muscles were more prone to fatigue. This may

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explain the median frequency of theses muscle in NP group were generally lower in our study. Only the

median frequency of left AS and left SCM were significantly lower in NP group, which could reflect the
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underlying endurance deficiency displayed in the cervical muscles ipsilateral to the side of the neck pain,

driven by the higher percentage of left sided neck pain (60%) in our NP group. Our results coincided with

previous study that chronic neck pain patient may have lower neuromuscular efficiency of the SCM and
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AS in neck pain patients during upper limbs fine motor task in 2.5 minutes (Falla, Bilenkij, 2004a).
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Combining the known evidence of decreased neuromuscular efficiency and increased fatigability

of AS, SCM and UT in chronic neck pain participants in static posture (Falla, Bilenkij, 2004a), our present
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findings proved that such clinical manifestation generalized to and became more explicit when neck pain

participants undergo the submaximal exercise. With the overactivity of AS and SCM which compensates
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the underactivity of the deep cervical flexors (Falla, Jull, 2004b), it helps promote the adoption of forward

head posture (i.e., upper cervical extension and lower cervical flexion) in symptomatic individuals. Previous

study stated that cervical flexion increases the loading and anteroposterior shearing force to the cervical
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 spine (Barrett et al. , 2020), and hence, the overactivation of these superficial muscles may speed up the

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degeneration of the cervical spine.

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Owing to the poor quality of EMG signals collected from the DF and EI possibly caused by the

restraints of the surface EMG and movements of the lower limbs during exercise test, only a limited

numbers of EMG datasets were included for comparison. Therefore, interpretation of the recruitment of

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these muscle groups would require additional caution. The amplitude of DF and EI muscles of NP group

were smaller at initial phase of testing when compared with control group. These findings support the notion

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hypothesized by previous research that changes in rib cage mechanic would lead to change in the length

tension curve of DF, abdominal and intercostal muscles and hence these muscles would become weaker

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(Kahlaee, Ghamkhar, 2017). Although, the between-group difference in amplitude analysis was statistically

insignificant, the power analysis was found to be relatively low for these comparisons. The inadequate
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quality of EMG signals has also limited the conclusion to be made in terms of the median frequency of

these primary respiratory muscles. Future studies are recommended to further examine the responses of

these muscles when advanced technology becomes feasible to accurately assess the EMG recruitment and
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fatigue analysis along with the improvement of the method to carry out the exercise test without causing
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the white noise to the EMG signals over the abdominal region (Kelly, Podoll, 2007).
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4.3. Intensity of neck pain and physiological responses during submaximal exercise test

The pain intensity levels of our NP group were along similar throughout the submaximal exercise
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test. The pain intensity of our neck pain participants was mild to moderate (mean NPRS score 3.47±1.77).

According to previous study, the MCID of pain intensity in chronic neck pain participants was -8mm in

Visual Analogue Scale (VAS) scale, which equals to -0.8 on the NPRS 0–10 (Lauche et al. , 2013). In our
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This preprint research paper has not been peer reviewed. Electronic copy available at: https://ssrn.com/abstract=4093327
 study, the pain intensity of NP group was varied within the small range (<0.8), which was unable to meet

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the MCID suggested mentioned above.

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The between-group difference found in HR remains inconclusive since the submaximal exercise

intensity was standardized to be 50-85% HRmax in our study, hence, the HR differences between two groups

may be inherently caused by the wide range of targeted HR. In order to investigate the actual changes of

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HR, a narrower range of targeted HR should be adopted. Moreover, monitor the HR variability may also

be considered for assessing the autonomic modulation in future studies (Kang et al. , 2012).

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Previous studies stated that there were moderate to strong relationships between perceived ratings

and muscle fatigue (Iridiastadi and Nussbaum, 2006, Law et al. , 2010, Rashedi and Nussbaum, 2016, Rose
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et al. , 2014). At the static recovery phase, the between group difference in RPE became minimal, implying

the recovery time of the perceived exertion was similar in NP group and control group in a subjective aspect.

By considering all these physiological responses, our results showed that lower limbs ergometry exercise
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in submaximal level could be performed safely without causing an exacerbation in mild to moderate chronic

neck pain people.

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4.4. Limitations
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The EMG data of the targeted muscles was incomplete as some of the EMG data did not pass the

quality control. Future study with better-quality EMG signals on respiratory muscles (DF, EI) could be
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performed to obtain a more precise data for analysis. Future study with larger sample size may provide

evidence with higher level of statistical power.

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This preprint research paper has not been peer reviewed. Electronic copy available at: https://ssrn.com/abstract=4093327
 5. Conclusions

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This study pioneered to investigate the changes of respiratory function towards submaximal

exercise in patients with chronic neck pain. Altered activation pattern between the primary and accessory

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respiratory muscles and greater fatigability of the accessory respiratory muscles were observed in neck pain

patients during the submaximal level of physical exertion. The present findings indicated that patients with

chronic neck pain showed an impaired recruitment efficiency for both primary inspiratory and expiratory

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muscles under physical exertion at submaximal intensity, compared to healthy individuals. While patients

with chronic neck pain were capable to maintain a comparable level of respiratory strength during the

exercise test, a compensatory pattern with the significant increase in recruitment of the inspiratory accessory

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muscles, AS and SCM were revealed. The long-term impact of such compensatory recruitment of the

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inspiratory accessory muscles during submaximal exercise in neck pain patients is yet to be investigated.

Meanwhile, our findings indicated that submaximal exercise did not cause a substantial increase in pain
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intensity for individuals with chronic neck pain. However, clinicians should carefully monitor the extent of

the compensation of respiratory muscle recruitment in individuals with chronic neck pain, particularly for

that of the accessory respiration muscles at the cervical region, for their over-activity in responses to the
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physical exertion (e.g., exercise training) in order to avoid the negative impact on the neck dysfunction

associated with muscle overuse.

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Declaration of Competing Interest

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The authors declare that they have no known competing financial interests or personal relationships that

could have appeared to influence the work reported in this paper.

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This preprint research paper has not been peer reviewed. Electronic copy available at: https://ssrn.com/abstract=4093327
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 Compensatory respiratory muscle recruitment strategy adopted in people with chronic neck pain

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during submaximal exercise

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Authors

Michelle T.K. Chung1, Louis W.L. Tam1, Edwin S.L. Wu1, Sam C.S. Yeung1, Sharon M.H. Tsang1

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Department of Rehabilitation Sciences, The Hong Kong Polytechnic University, Hong Kong

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Keywords: Neck pain, respiratory muscle, maximal respiratory pressure, electromyography, submaximal

exercise.
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Corresponding author: Sharon M.H. Tsang
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Address: Room ST535, Department of Rehabilitation Sciences, The Hong Kong Polytechnic University,

Hunghom, Kowloon, Hong Kong.

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Email address: Sharon.Tsang@polyu.edu.hk

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This preprint research paper has not been peer reviewed. Electronic copy available at: https://ssrn.com/abstract=4093327