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Manual Therapy 19 (2014) 440e444

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Manual Therapy
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Original article

Respiratory dysfunction in patients with chronic neck pain e Inuence


of thoracic spine and chest mobility
B. Wirth a, *, M. Amstalden a, M. Perk b, U. Boutellier b, B.K. Humphreys c
a

Motor Control and Learning, Institute for Human Movement Sciences and Sports, ETH Zurich, Zurich, Switzerland
Exercise Physiology Lab, Institute for Human Movement Sciences and Sports, ETH Zurich, Zurich, Switzerland
c
Department of Chiropractic, Balgrist Hospital, Zurich, Switzerland
b

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 9 December 2013
Received in revised form
4 April 2014
Accepted 17 April 2014

Patients with chronic neck pain exhibit various musculoskeletal decits and respiratory dysfunction. As
there is a link between thoracic and cervical spine motion, the aim of this study was to investigate the
relationship between thoracic spine and chest mobility with respiratory function and neck disability.
Nineteen patients with chronic neck pain (7 male, 46.6  10.5 years) and 19 healthy subjects (7 male,
46.5  9.9 years) participated. Spirometry was conducted to determine maximal voluntary ventilation
(MVV), maximal inspiratory (Pimax) and maximal expiratory pressure (Pemax). Thoracic spine mobility
was measured using the Spinal Mouse. Chest expansion was assessed by subtracting chest circumference during maximal inspiration and expiration. Neck function was investigated by examining range of
motion, forward head posture, neck exor muscle synergy endurance and self-assessment (Neck
disability index (NDI)). Correlation analyses and multiple linear regression analyses were conducted
using MVV, Pimax and Pemax as independent variables. Thoracic spine mobility during exion and chest
expansion correlated signicantly to MVV (r 0.45 and 0.42), all neck motions (r between 0.39 and 0.59)
and neck muscle endurance (rS 0.36). Pemax and Pimax were related to NDI (r 0.58 and 0.46). In the
regression models, chest expansion was the only signicant predictor for MVV, and Pemax was determined by neck muscle endurance. These results suggest that chronic neck pain patients should improve
the endurance of the neck exor muscles and thoracic spine and chest mobility. Additionally, these
patients might benet from respiratory muscle endurance training, possibly by increasing chest mobility
and Pemax.
2014 Elsevier Ltd. All rights reserved.

Keywords:
Neck pain
Respiratory dysfunction
Thoracic spine

1. Introduction
Neck pain is an increasingly common disabling and costly
musculoskeletal disorder with a mean overall prevalence in the
general population of approximately 23% (Hoy et al., 2010). Its
course is characterised by periods of remission and exacerbation,
but the majority of patients do not completely recover from their
symptoms (Cote et al., 2004).
Several studies have shown that patients with chronic neck pain
present with various motor dysfunctions, such as the inhibition of
deep cervical exor muscle activation accompanied by increased
activation of the supercial neck muscles (Falla et al., 2004; Jull
et al., 2004), increased forward head posture (Yip et al., 2008)
and sensorimotor disturbances (Sjolander et al., 2008). Cervical
* Corresponding author. Institute for Human Movement Sciences and Sports,
Department of Health Sciences and Technology, ETH Zurich, Hnggerberg, Wolfgang Pauli Str. 27, 8093 Zurich, Switzerland. Tel.: 41 44 632 59 81.
E-mail address: brigitte.wirth@hest.ethz.ch (B. Wirth).
http://dx.doi.org/10.1016/j.math.2014.04.011
1356-689X/ 2014 Elsevier Ltd. All rights reserved.

spine mobility seems to be restricted (DallAlba et al., 2001; Ohberg


et al., 2003), but this nding is inconclusive (Sjolander et al., 2008).
Some newer studies have also reported impaired respiratory
function that manifested itself in reduced maximal voluntary
ventilation (MVV) as well as reduced maximal inspiratory and
expiratory pressures (Pimax and Pemax) (Kapreli et al., 2009;
Dimitriadis et al., 2013b). Isometric neck extensor muscle
strength and forward head posture were thereby mostly associated
with these respiratory parameters (Kapreli et al., 2009; Dimitriadis
et al., 2013b). It was hypothesised that the observed respiratory
dysfunction in chronic neck pain patients might be caused by the
following factors (Kapreli et al., 2008): 1) weakness of the deep
neck exor and extensor muscles, leading to the reduced stability of
the cervical and thoracic spine as well as changes in rib cage mechanics, 2) altered forceelength curves of the sternocleidomastoid
muscles (accessory breathing muscles that are active during forced
inspiration) due to muscle hyperactivity and restricted range of
motion of the cervical spine and 3) chronic pain and kinesiophobia
that leads to changes in blood chemistry (reduction of arterial

B. Wirth et al. / Manual Therapy 19 (2014) 440e444

carbon dioxide) via chronic hyperventilation (Dimitriadis et al.,


2013a).
Recently, the importance of the thoracic spine in neck kinematics and in the development of neck pain was emphasised (Lau
et al., 2010; Quek et al., 2013; Tsang et al., 2013). In asymptomatic
subjects, the thoracic spine contributed substantially to overall
neck motion (approximately 15% to rotation, 25% to lateral exion
and 35% to exion and extension) (Tsang et al., 2013). Furthermore,
the sagittal posture of the thoracic spine (greater upper thoracic
angle) was associated with forward head posture (smaller craniovertebral angle), cervical mobility (reduced exion and rotation)
and the presence of neck pain (Lau et al., 2010; Quek et al., 2013).
With regard to respiratory function, it was shown in elderly persons
that thoracic kyphosis was accompanied by dyspnoea and ventilator dysfunction (Di Bari et al., 2004). Accordingly, in young
healthy athletes, a 4 weeks respiratory muscle training decreased
thoracic and lumbar angles in the sagittal spinal curvature
(Obayashi et al., 2012). In neck patients, breathing retraining led to
clinically important changes in pain and function (McLaughlin
et al., 2011), but further studies on the impact of breathing reeducation training on chronic neck pain were advised
(Dimitriadis et al., 2013a).
Based on these ndings and on the hypotheses underlying the
observed respiratory dysfunction in chronic neck pain patients,
changes in chest expansion and thoracic spine mobility might be
hypothesised to be involved in chronic neck pain patients. This
might in turn promote the alterations observed in the mechanics of
the sternocleidomastoid muscles and in cervical spine mobility.
Thus, the aim of the present study was to investigate 1) whether
patients with chronic neck pain differ from healthy controls in
terms of thoracic spine and chest mobility and 2) whether these
parameters correlate positively with respiratory and neck function.
The results might contribute to optimising the rehabilitation of
patients with chronic neck pain, particularly when it concerns new
therapy approaches, such as breathing retraining.
2. Methods
2.1. Subjects
The participants were recruited from various medical practices
and from a sports club. The neck patients were included if they
were older than 18 years of age and had neck pain for longer than 6
months. Patients with spinal fracture or surgery as well as neurological or inammatory pathology of the cervical spine were
excluded. Chronic whiplash-associated neck pain was not an
exclusion criterion because it was advised against treating these
patients as a subgroup (Verhagen et al., 2011). To exclude all risk
factors for the lung function measurements, all of the subjects
completed a questionnaire on risk factors for performance tests
used in the exercise physiology laboratory of ETH Zurich. The level
of physical activity was assessed by the Baecke questionnaire
(Baecke et al., 1982). All of the procedures were performed in
accordance with the Declaration of Helsinki and were approved by
the ethics committee of the canton of Zurich. All of the subjects
gave written informed consent for their participation.
2.2. Experimental procedures
2.2.1. Respiratory function testing
Respiratory function was tested according to standard testing
recommendations (American Thoracic Society and European
Respiratory Society, 2002; Miller et al., 2005). All of the tests
were performed in a seated position with subjects wearing a nose
clip. Spirometry was completed using a MasterScope PC spirometer

441

(Jaeger, Hoechberg, Germany) that was calibrated prior to each


testing session. Testing parameters included vital capacity (VC),
forced vital capacity (FVC), peak expiratory ow (PEF), forced
expiratory ow in 1 s (FEV1), forced expiratory ratio (FEV1/FVC),
forced expiratory ow (FEF25%, FEF50%, FEF75%) and 12 s MVV. The
tests were repeated 3 to 5 times, depending on the standard
between-manoeuvre criteria (Miller et al., 2005). For each
manoeuvre, the largest value was recorded. Pimax and Pemax were
tested with a digital respiratory pressure meter (MicroRPM, CareFusion, Hoechberg, Germany), a hand-held device with a built-in
small air leak to prevent pressure generation by glottis closure.
For Pimax, subjects had to inhale maximally from residual volume
against a resistance for at least 1 s. For Pemax, subjects were
instructed to exhale maximally from total lung capacity against a
resistance for at least 1 s. In addition, subjects were required to
pinch their lips during Pemax to avoid air leaks around the
mouthpiece. Pimax and Pemax manoeuvres were alternated every 3
trials. A minimum of 5 and a maximum of 10 trials were performed
to ensure that the 3 largest values varied by less than 5%. The
maximum value was recorded.
2.2.2. Musculoskeletal assessments
Range of motion (ROM) of the cervical spine was measured
using Zebris CMS10 (Zebris Medical, Isny, Germany). The
ultrasound-based coordinate system measured 3 consecutive
movements of maximal exion-extension, lateral exion as well as
rotation and calculated the average value for each direction. For
rotation and lateral exion, the mean of left and right ROM was
used for further analysis. The Spinal Mouse (idiag, Fehraltorf,
Switzerland), a hand-held, non-invasive electromechanical device,
was used to determine sagittal ROM of the thoracic spine (Mannion
et al., 2004). This test was conducted in the all-fours position to
promote a greater range of motion (Edmondston et al., 2011). The
device was rolled down the spine starting with the 7th cervical
vertebra (C7) and ending at the 3rd lumbar vertebra (L3). The
measurements were performed in the neutral, maximally exed
and maximally extended positions. Mobilities between neutral and
exed position (thoracic exion) and neutral and extended position
(thoracic extension) were calculated. Chest mobility was measured
at the level of the xiphoid process (Lunardi et al., 2011). A at
measuring tape was drawn tight around the subjects chest, and the
difference in circumference between maximal inspiration and
maximal expiration for each level was measured twice. The mean of
the two values was recorded. If the difference between the two
trials was greater than 1 cm, a 3rd measurement was taken, and the
average of the 2 largest values was recorded. For the determination
of the forward head posture (craniovertebral angle), a prole
photograph of the left side of the face was taken (Raine and
Twomey, 1997) in the standing position (Kapreli et al., 2009). The
tragus of the ear and the spinal process of C7 served as anatomical
markings to calculate the angle between the horizontal line
running through C7 and the line from tragus to C7. Endurance of the
neck exor muscle synergy was tested as recommended (de Koning
et al., 2008). The subjects were in the supine position and were
instructed to lift their head approximately 2 cm while keeping their
chins tucked in (craniocervical exion). The time was measured
until the subject was no longer able to tuck the chin in. The
examiner monitored chin position visually and by a light nger
touch (Grimmer, 1994). This test could not be conducted by one
patient due to neck pain.
2.2.3. Self-assessment of neck disability
Neck disability was assessed by the German version of the NDI
(NDI-G) (Swanenburg et al., 2014). This assessment covers 10 areas
of daily living (pain intensity, personal care, lifting, reading,

442

B. Wirth et al. / Manual Therapy 19 (2014) 440e444

headache, concentration, work, driving, sleeping and recreation)


each given a score in the range of 0 (no impairment) to 5 points
(maximal impairment), resulting in a maximal possible score of 50
points (Vernon and Mior, 1991).

Table 1
Respiratory and musculoskeletal parameters in the neck patient and in the control
group.
Parameter

2.3. Data analysis and statistics


Data distribution was tested by ShapiroeWilk Tests and was
normal for all parameters apart from chest mobility, neck muscle
endurance and NDI-G score (points out of 50). Group differences
were calculated by independent t tests for parametric data and by
Mann Whitney U tests for non-parametric data. In addition,
Cohens effect sizes (ES) were calculated. ES values between 0.2 and
0.5 were regarded as small, between 0.5 and 0.8 as moderate and
greater than 0.8 as large (Cohen, 1988). Correlations between respiratory and musculoskeletal parameters were calculated in all
participants using the Pearson (parametric) and Spearman (nonparametric) correlation coefcients (r and rS). Correlation coefcients <0.25 indicated little or no relationship, coefcients between 0.25 and 0.5 were regarded as fair, between 0.5 and 0.75 as
moderate to good and coefcients greater than 0.75 as good to
excellent (Portney and Watkins, 2000). Multiple regression analyses (enter method/forced entry) were performed using MVV,
Pimax and Pemax as dependent variables. Thoracic spine mobility in
exion, chest mobility, forward head posture and endurance of the
short neck exors were selected as predictors. Because no predictive value of cervical mobility was shown (Dimitriadis et al., 2013b),
this parameter was not included in the analyses. For all analyses,
IBM SPSS Statistics 20.0 (SPSS, Chicago, IL, USA) was used and the
signicance level a was set to 0.05.
3. Results
Nineteen healthy subjects (7 male, mean age 46.5  9.9 years,
mean body mass index 24.5  4.1 kg/m2) and 19 patients with
chronic neck pain of similar age and identical gender (7 male, mean
age 46.6  10.5 years, mean body mass index 24.8  5.4 kg/m2, 7
with chronic neck pain of traumatic origin) were tested. No signicant difference in physical activity was observed comparing the
control group (9.1  1.2 points) with the patient group (8.5  1.3
points; p 0.13). The neck disability in the patient group was mild
on average (12.0  7.1 NDI-G points) (Vernon and Mior, 1991).
MVV, Pimax and Pemax were somewhat lower in the patient
group, but these differences did not reach a statistically signicant
level (Table 1). Nevertheless, ES was moderate for MVV, but small
for Pimax and Pemax. Cervical mobility was signicantly reduced in
all movements, apart from lateral exion, and the ES were

MVV [l/min]
Pimax [cmH20]
Pemax [cmH20]
VC [l]
FVC [l]
FEV1/FVC [ ]
PEF [l]
Cervical exion [ ]
Cervical extension [ ]
Cervical rotation [ ]
Cervical lateral exion [ ]
Thoracic exion [ ]
Thoracic extension [ ]
Chest mobility [cm]
Forward head posture [ ]
Neck muscle endurance [s]

Neck patients

Controls

Mean (SD)

Mean (SD)

110.3
92.3
146.6
4.2
4.0
0.8
7.4
57.0
56.0
67.7
38.4
30.2
13.3
4.8
47.7
105.7

132.4
104.2
157.1
4.5
4.3
0.8
8.2
67.0
65.8
74.6
39.7
31.2
12.7
5.8
49.1
94.3

(40.0)
(28.3)
(54.1)
(0.9)
(0.8)
(0.1)
(2.0)
(13.6)
(16.1)
(7.4)
(8.5)
(15.5)
(10.5)
(2.4)
(8.0)
(77.4)

(41.2)
(27.1)
(33.6)
(1.1)
(1.0)
(0.03)
(2.0)
(10.6)
(11.1)
(10.3)
(9.8)
(13.4)
(10.6)
(2.4)
(6.4)
(51.3)

P value

Effect size

0.106
0.194
0.478
0.331
0.394
0.375
0.231
0.016
0.034
0.023
0.674
0.819
0.867
0.242
0.562
0.893

0.54
0.43
0.23
0.32
0.28
0.29
0.40
0.82
0.71
0.78
0.14
0.07
0.05
0.39
0.19
0.18

FEV1 forced expiratory ow in 1 s.


FVC forced vital capacity.
MVV maximal voluntary ventilation.
PEF peak expiratory ow.
Pemax maximal expiratory pressure.
Pimax maximal inspiratory pressure.
VC vital capacity.
Bold indicates signicant results (p < 0.05).

moderate to large. In contrast, thoracic spine mobility did not differ


between the groups with negligible ES. Chest mobility was similar
in both groups and the ES was small. No differences between the
groups were found in forward head posture and endurance of the
neck exor muscle synergy (Table 1).
Signicant fair correlations of thoracic spine mobility in exion
and of chest mobility to MVV were found (r 0.45, and r 0.42,
respectively). All neck motions were signicantly correlated to
thoracic spine mobility in exion with fair correlation coefcients
(r 0.39e0.46) and to chest mobility with moderate to good coefcients (r 0.50e0.59), apart from neck exion (r 0.39).
Additionally, signicant fair correlations between thoracic spine
mobility in exion and neck muscle endurance (r 0.36) as well as
between chest expansion and forward head posture were found
(r 0.36) (Table 2).
The NDI-G scores showed a signicant moderate to good correlation to Pemax (r 0.58), a signicant fair correlation to Pimax
(r 0.46) and fair correlations (not signicant) to MVV, thoracic
exion mobility and endurance of the neck exor muscle synergy
(Table 3).

Table 2
Correlations of thoracic spine and chest mobility to respiratory and musculoskeletal parameters.

Respiratory parameters

Musculoskeletal parameters

MVV
Pimax
Pemax
Cervical exion
Cervical extension
Cervical rotation
Cervical lateral exion
Forward head posture
Neck muscle endurance (rS)

MVV maximal voluntary ventilation.


Pemax maximal expiratory pressure.
Pimax maximal inspiratory pressure.
r Pearson correlation coefcient.
rS Spearman correlation coefcient.
Bold indicates signicant results (p < 0.05).

Thoracic spine exion (r)

Thoracic spine extension (r)

Chest expansion (rS)

0.45
0.21
0.31
0.43
0.46
0.39
0.39
0.12
0.36

0.07
0.07
0.04
0.12
0.09
0.01
0.03
0.19
0.05

0.42
0.11
0.21
0.39
0.59
0.58
0.50
0.36
0.22

(0.005)
(0.197)
(0.058)
(0.007)
(0.004)
(0.015)
(0.015)
(0.474)
(0.029)

(0.676)
(0.676)
(0.830)
(0.480)
(0.587)
(0.939)
(0.871)
(0.248)
(0.750)

(0.008)
(0.525)
(0.210)
(0.015)
(<0.001)
(<0.001)
(0.001)
(0.027)
(0.186)

B. Wirth et al. / Manual Therapy 19 (2014) 440e444


Table 3
Correlations of self-reported neck disability (NDI-G score) to respiratory and
musculoskeletal parameters.

Respiratory
parameters
Musculoskeletal
parameters

Parameter

Correlation coefcient (rS)

MVV
Pimax
Pemax
Thoracic exion
Thoracic extension
Chest expansion
Cervical exion
Cervical extension
Cervical rotation
Cervical lateral exion
Forward head posture
Neck muscle endurance

0.42
0.46
0.58
0.37
0.04
0.15
0.16
0.25
0.09
0.04
0.06
0.41

(0.078)
(0.048)
(0.009)
(0.116)
(0.858)
(0.542)
(0.505)
(0.303)
(0.730)
(0.863)
(0.806)
(0.091)

MVV maximal voluntary ventilation.


Pemax maximal expiratory pressure.
Pimax maximal inspiratory pressure.
rS Spearman correlation coefcient.
Bold indicates signicant results (p < 0.05).

The multiple linear regression analyses (no multicollinearity


detected, independent residuals) revealed that MVV could be predicted by the regression model with chest mobility as the only
signicant predictor (Table 4). Similarly, Pemax was signicantly
predicted by endurance of the neck exor muscle synergy. The
chosen regression model could not signicantly predict Pimax
(Table 4).

4. Discussion
This study revealed no changes in thoracic spine and chest
mobility in patients with chronic neck pain and showed only a fair
relation between thoracic spine and chest mobility and MVV.
Nevertheless, the correlations of chest expansion and thoracic
spine exion mobility to cervical motion, which was substantially
reduced in the neck pain patients, underline the importance of
thoracic spine and chest mobility for neck function. Interestingly,
self-reported neck disability was mainly predicted by Pemax and
Pimax, while neck mobility was of no importance.
Respiratory function was only somewhat reduced in the patient
group and this difference was not signicant, which is in contrast to
previous studies (Kapreli et al., 2009; Dimitriadis et al., 2013b).
While MVV and Pimax compare well to data in previous studies, the
subjects in this study presented with a higher Pemax. This
discrepancy might partly be explained by the only mild neck
disability of the patients in this study (average NDI 12 points)
compared with that in other studies (average NDI 30 points
(Kapreli et al., 2009)), according to the classication of NDI scores in
the original literature (Vernon and Mior, 1991). Indeed, in accordance with the study by Dimitriadis et al. (Dimitriadis et al., 2013b),
Pemax was particularly related to the NDI-G score. The difference in

443

Pemax values might also be the result of some methodological differences. Pimax and Pemax values seem to be smaller when assessed
in the standing position (Dimitriadis et al., 2013b) compared with
the sitting position (Kapreli et al., 2009). Additionally, the test
protocol was more stringent in the present study than in previous
studies (Kapreli et al., 2009; Dimitriadis et al., 2013b) (e.g. maximal
10 instead of 5 trials were conducted).
Thoracic exion mobility and chest expansion correlated with
cervical mobility, which was signicantly reduced in the patient
group in all neck motions apart from lateral exion, which is in
accordance with other studies (Chiu and Sing, 2002; Shahidi et al.,
2012). This matches the nding in healthy subjects that thoracic
spine movement contributes substantially to neck mobility,
particularly in the sagittal plane (Tsang et al., 2013). The observed
relationship of thoracic exion and chest mobility to MVV conrms
ndings in patients with ankylosing spondylitis who present with
impaired pulmonary function (Berdal et al., 2012). The nding that
Pimax and Pemax were related to the NDI-G score corroborates the
results of the study by Dimitriadis et al. (Dimitriadis et al., 2013b).
However, in contrast to the former study, neck exor muscle synergy endurance, but not forward head posture predicted Pemax in
the present study. This discrepancy might partly be explained by
the different methodology used for testing neck exor endurance.
Dimitriadis et al. (Dimitriadis et al., 2013b) conducted the craniocervical test using a biofeedback device, which was not recommended for clinical use due to its limited reliability (de Koning
et al., 2008). Nevertheless, the subjects in this study presented
with high scores for the endurance of the neck exor muscle synergy compared with that in other studies (Grimmer, 1994; Shahidi
et al., 2012). This matches with the observed high Pemax values, but
might also reect the difculties in objectively assessing endurance
of the neck exor muscle synergy. Although the chosen assessment
was recommended in a review paper (de Koning et al., 2008), a
recent study showed a limited inter-rater reliability in neck patients
(Shahidi et al., 2012). This shows the need for further research in
this clinically important eld.
The main limitation of the present study was the small sample
size with a limited age range, which makes generalization of the
results difcult. Furthermore, the measurement of spinal mobility
by the Spinal Mouse has only been validated in the standing position (Mannion et al., 2004) and still needs to be validated for the
all-fours position. As a further limitation, isometric neck muscle
strength was not assessed in this study. Such assessments should
however be included in further studies because they have emerged
as predictors for both Pimax and Pemax (Dimitriadis et al., 2013b).
Future studies on respiratory dysfunction in patients with
chronic neck pain should focus on those patients with a higher level
of neck disability to detect more pronounced effects and should
also exclude traumatic neck patients. With the intention of developing new therapeutic strategies, there is some evidence that
breathing re-education might be benecial for chronic neck pain
patients (McLaughlin et al., 2011), but further studies on this issue

Table 4
Regression models for the prediction of the respiratory parameters.
Dependent variable

MVV
Pimax
Pemax

Model
parameters

Standardized regression coefcients (p)

R2

Thoracic spine mobility in exion

Chest mobility

Forward head posture

Neck muscle endurance

0.34
0.23
0.30

0.008
0.075
0.020

0.17 (0.344)
0.06 (0.761)
0.07 (0.692)

0.40 (0.038)
0.26 (0.207)
0.13 (0.488)

0.32 (0.052)
0.32 (0.074)
0.22 (0.186)

0.23 (0.138)
0.39 (0.026)
0.48 (0.005)

MVV maximal voluntary ventilation.


Pemax maximal expiratory pressure.
Pimax maximal inspiratory pressure.
Bold indicates signicant results (p < 0.05).

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B. Wirth et al. / Manual Therapy 19 (2014) 440e444

are needed (Dimitriadis et al., 2013a). Respiratory muscle endurance training reduced stiffness of the rib cage in healthy athletes
(Obayashi et al., 2012) and led to signicant increase in Pemax in
patients with chronic obstructive pulmonary disease (Scherer et al.,
2000) and spinal cord injury (Berlowitz and Tamplin, 2013), while
inconsistent ndings were reported in healthy subjects (Verges
et al., 2008; Walker et al., 2013). Thus, it should be investigated in
chronic neck pain patients whether respiratory training might increase chest mobility and Pemax, which both emerged from this
study as particularly important parameters with a view to neck
mobility and self-perceived neck disability, respectively. In a second
step, such training should be compared with conventional cervical
exor muscle endurance training, as conducted in physiotherapy
(Falla et al., 2012; Thoomes-de Graaf and Schmitt, 2012).
In conclusion, although thoracic spine and chest mobility were
related only to MVV and not to the maximal respiratory pressures,
the nding of the relationship to all cervical motions is of clinical
importance. Pemax was most closely related to NDI-G and was
mainly predicted by the endurance of the neck exor muscle synergy. These ndings suggest that respiratory muscle endurance
training might be a valuable addition to the rehabilitation of patients with chronic neck pain, possibly by increasing chest mobility
and Pemax.
Acknowledgements
We thank Dr. Rolf Nussbaumer, Dr. med. Hansjrg Holdener and
Adrian Sandmeier for their help with the patient recruitment.
Furthermore, we thank Anja Trepp from the idiag AG for providing
the Spinal Mouse.
References
American Thoracic Society, European Respiratory Society. ATS/ERS statement on
respiratory muscle testing. Am J Respir Crit Care Med 2002;166:518e624.
Baecke JA, Burema J, Frijters JE. A short questionnaire for the measurement of
habitual physical activity in epidemiological studies. Am J Clin Nutr 1982;36(5):
936e42.
Berdal G, Halvorsen S, van der Heijde D, Mowe M, Dagnrud H. Restrictive pulmonary function is more prevalent in patients with ankylosing spondylitis than
in matched population controls and is associated with impaired spinal
mobility: a comparative study. Arthritis Res Ther 2012;14(1):R19.
Berlowitz DJ, Tamplin J. Respiratory muscle training for cervical spinal cord injury.
Cochrane Database Syst Rev 2013;7. CD008507.
Chiu TT, Sing KL. Evaluation of cervical range of motion and isometric neck muscle
strength: reliability and validity. Clin Rehabil 2002;16(8):851e8.
Cohen J. Statistical power analysis for the behavioral sciences. 2 ed. Hillsdale, New
Jersey: Lawrence Erlbaum Associates; 1988.
Cote P, Cassidy JD, Carroll LJ, Kristman V. The annual incidence and course of neck
pain in the general population: a population-based cohort study. Pain
2004;112(3):267e73.
DallAlba PT, Sterling MM, Treleaven JM, Edwards SL, Jull GA. Cervical range of
motion discriminates between asymptomatic persons and those with whiplash.
Spine 2001;26(19):2090e4.
de Koning CH, van den Heuvel SP, Staal JB, Smits-Engelsman BC, Hendriks EJ.
Clinimetric evaluation of methods to measure muscle functioning in patients
with non-specic neck pain: a systematic review. BMC Musculoskelet Disord
2008;9:142.
Di Bari M, Chiarlone M, Matteuzzi D, Zacchei S, Pozzi C, Bellia V, et al. Thoracic
kyphosis and ventilatory dysfunction in unselected older persons: an epidemiological study in Dicomano, Italy. J Am Geriatr Soc 2004;52(6):909e15.
Dimitriadis Z, Kapreli E, Strimpakos N, Oldham J. Hypocapnia in patients with
chronic neck pain: association with pain, muscle function, and psychologic
states. Am J Phys Med Rehabil Assoc Acad Physiatrists 2013a;92(9):746e54.
Dimitriadis Z, Kapreli E, Strimpakos N, Oldham J. Respiratory weakness in patients
with chronic neck pain. Man Ther 2013b;18(3):248e53.
Edmondston SJ, Waller R, Vallin P, Holthe A, Noebauer A, King E. Thoracic spine
extension mobility in young adults: inuence of subject position and spinal
curvature. J Orthop Sports Phys Ther 2011;41(4):266e73.

Falla D, OLeary S, Farina D, Jull G. The change in deep cervical exor activity after
training is associated with the degree of pain reduction in patients with chronic
neck pain. Clin J Pain 2012;28(7):628e34.
Falla DL, Jull GA, Hodges PW. Patients with neck pain demonstrate reduced electromyographic activity of the deep cervical exor muscles during performance
of the craniocervical exion test. Spine 2004;29(19):2108e14.
Grimmer K. Measuring the endurance capacity of the cervical short exor muscle
group. Aust J Physiother 1994;40:251e4.
Hoy DG, Protani M, De R, Buchbinder R. The epidemiology of neck pain. Best Prac
Res Clin Rheumatol 2010;24(6):783e92.
Jull G, Kristjansson E, DallAlba P. Impairment in the cervical exors: a comparison
of whiplash and insidious onset neck pain patients. Man Ther 2004;9(2):89e94.
Kapreli E, Vourazanis E, Billis E, Oldham JA, Strimpakos N. Respiratory dysfunction
in chronic neck pain patients. A pilot study. Cephalalgia Int J Headache
2009;29(7):701e10.
Kapreli E, Vourazanis E, Strimpakos N. Neck pain causes respiratory dysfunction.
Med Hypotheses 2008;70(5):1009e13.
Lau KT, Cheung KY, Chan KB, Chan MH, Lo KY, Chiu TT. Relationships between
sagittal postures of thoracic and cervical spine, presence of neck pain, neck pain
severity and disability. Man Ther 2010;15(5):457e62.
Lunardi AC, Marques da Silva CC, Rodrigues Mendes FA, Marques AP, Stelmach R,
Fernandes Carvalho CR. Musculoskeletal dysfunction and pain in adults with
asthma. J Asthma Ofcial J Assoc Care Asthma 2011;48(1):105e10.
Mannion AF, Knecht K, Balaban G, Dvorak J, Grob D. A new skin-surface device for
measuring the curvature and global and segmental ranges of motion of the
spine: reliability of measurements and comparison with data reviewed from
the literature. Eur Spine J Ofcial Publ Eur Spine Soc Eur Spinal Deformity Soc
Eur Sect Cerv Spine Res Soc 2004;13(2):122e36.
McLaughlin L, Goldsmith CH, Coleman K. Breathing evaluation and retraining as an
adjunct to manual therapy. Man Ther 2011;16(1):51e2.
Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J 2005;26(2):319e38.
Obayashi H, Urabe Y, Yamanaka Y, Okuma R. Effects of respiratory-muscle exercise
on spinal curvature. J Sport Rehabil 2012;21(1):63e8.
Ohberg F, Grip H, Wiklund U, Sterner Y, Karlsson JS, Gerdle B. Chronic whiplash
associated disorders and neck movement measurements: an instantaneous
helical axis approach. IEEE Trans Inf Technol Biomed Publ IEEE Eng Med Biol Soc
2003;7(4):274e82.
Portney L, Watkins M. Foundations of clinical research. Applications to practice. 2
ed. Upper Saddle River, New Jersey: Prentice Hall International; 2000.
Quek J, Pua YH, Clark RA, Bryant AL. Effects of thoracic kyphosis and forward head
posture on cervical range of motion in older adults. Man Ther 2013;18(1):65e
71.
Raine S, Twomey LT. Head and shoulder posture variations in 160 asymptomatic
women and men. Arch Phys Med Rehabil 1997;78(11):1215e23.
Scherer TA, Spengler CM, Owassapian D, Imhof E, Boutellier U. Respiratory muscle
endurance training in chronic obstructive pulmonary disease: impact on exercise capacity, dyspnea, and quality of life. Am J Respir Crit Care Med
2000;162(5):1709e14.
Shahidi B, Johnson CL, Curran-Everett D, Maluf KS. Reliability and group differences
in quantitative cervicothoracic measures among individuals with and without
chronic neck pain. BMC Musculoskelet Disord 2012;13:215.
Sjolander P, Michaelson P, Jaric S, Djupsjobacka M. Sensorimotor disturbances in
chronic neck painerange of motion, peak velocity, smoothness of movement,
and repositioning acuity. Man Ther 2008;13(2):122e31.
Swanenburg J, Humphreys K, Langenfeld A, Brunner F, Wirth B. Validity and reliability of a German version of the Neck Disability Index (NDI-G). Man Ther
2014;19:52e8.
Thoomes-de Graaf M, Schmitt MS. The effect of training the deep cervical exors on
neck pain, neck mobility, and dizziness in a patient with chronic nonspecic
neck pain after prolonged bed rest: a case report. J Orthop Sports Phys Ther
2012;42(10):853e60.
Tsang SM, Szeto GP, Lee RY. Normal kinematics of the neck: the interplay between
the cervical and thoracic spines. Man Ther 2013;18(5):431e7.
Verges S, Boutellier U, Spengler CM. Effect of respiratory muscle endurance training
on respiratory sensations, respiratory control and exercise performance: a 15year experience. Respir Physiol Neurobiol 2008;161(1):16e22.
Verhagen AP, Lewis M, Schellingerhout JM, Heymans MW, Dziedzic K, de Vet HC,
et al. Do whiplash patients differ from other patients with non-specic neck
pain regarding pain, function or prognosis? Man Ther 2011;16(5):456e62.
Vernon H, Mior S. The Neck Disability Index: a study of reliability and validity.
J Manipulative Physiol Ther 1991;14(7):409e15.
Walker DJ, Ertl T, Walterspacher S, Schlager D, Roecker K, Windisch W, et al. Respiratory muscle function during a six-week period of normocapnic hyperpnoea
training. Respir Physiol Neurobiol 2013;188(2):208e13.
Yip CH, Chiu TT, Poon AT. The relationship between head posture and severity and
disability of patients with neck pain. Man Ther 2008;13(2):148e54.

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