Respiratory weakness in patients with chronic neck pain
Zacharias Dimitriadisa,b,*, Eleni Kaprelia, Nikolaos Strimpakosa,b, Jacqueline Oldhamb
aPhysiotherapy Department, Technological Educational Institute (TEI) of Lamia, 3rd km Old National Road Lamia-Athens, 35100 Lamia, Greece
bManchester Academic Health Sciences Centre, The University of Manchester, Oxford Road, Manchester M13 9PL, UK
a r t i c l e i n f o
Received 1 April 2012
Received in revised form
24 October 2012
Accepted 30 October 2012
Chronic neck pain
Maximal expiratory pressure
Maximal inspiratory pressure
a b s t r a c t
Respiratory muscle strength is one parameter that is currently proposed to be affected in patients with
chronic neck pain. This study was aimed at examining whether patients with chronic neck pain have
reduced respiratory strength and with which neck pain problems their respiratory strength is associated.
In this controlled cross-sectional study, 45 patients with chronic neck pain and 45 healthy well-matched
controls were recruited. Respiratory muscle strength was assessed through maximal mouth pressures.
The subjects were additionally assessed for their pain intensity and disability, neck muscle strength,
endurance of deep neck flexors, neck range of movement, forward head posture and psychological states.
Paired t-tests showed that patients with chronic neck pain have reduced Maximal Inspiratory (MIP)
(r ¼ 0.35) and Maximal Expiratory Pressures (MEP) (r ¼ 0.39) (P < 0.05). Neck muscle strength (r > 0.5),
kinesiophobia (r < ?0.3) and catastrophizing (r < ?0.3) were significantly associated with maximal
mouth pressures (P < 0.05), whereas MEP was additionally negatively correlated with neck pain and
disability (r < ?0.3, P < 0.05). Neck muscle strength was the only predictor that remained as significant
into the prediction models of MIP and MEP. It can be concluded that patients with chronic neck pain
present weakness of their respiratory muscles. This weakness seems to be a result of the impaired global
and local muscle system of neck pain patients, and psychological states also appear to have an additional
contribution. Clinicians are advised to consider the respiratory system of patients with chronic neck pain
during their usual assessment and appropriately address their treatment.
? 2012 Elsevier Ltd. All rights reserved.
Chronic neck pain is one of the most frequent musculoskeletal
complaints and can lead to adaptive musculoskeletal and motor
control changes in cervical region and related structures (Falla and
Farina, 2008; Jull et al., 2008a). Although neck pain is predomi-
nantly considered and treated in clinical practice as a neuro-
musculoskeletal problem, the close anatomical connection of the
cervical region with the thoracic spine in parallel with their
musculoskeletal and neural connection have led some researchers
to believe that neck pain may lead to associated changes in thoracic
spine and rib cage and consequential changes in pulmonary func-
tion (Kapreli et al., 2008).
Cervical spine studies have shown that muscle strength and
endurance (Chiu and Lo, 2002; Harris et al., 2005), cervical mobility
(Rix and Bagust, 2001), head posture (Lau et al., 2009) and cervical
proprioception (Cheng et al., 2010) are all affected in patients with
chronic neck pain, whereas abnormal psychological states namely
anxiety, depression, kinesiophobia and catastrophizing may also be
present (Leino and Magni,1993; Hill et al., 2007; Mantyselka et al.,
2010). It has been recently theorized that all of these parameters
can have their own unique contribution for the development of
respiratory dysfunction or abnormalities in patients with chronic
neck pain (Kapreli et al., 2008) and preliminarily supported by
a previous pilot study (Kapreli et al., 2009). Changes in cervical
mobility, head posture and dysfunction of local and global muscle
system are believed that lead to changes in forceelength curves,
muscle imbalances and segmental instability (Gossman et al.,1982;
Comerford and Mottram, 2001; Key et al., 2008) potentially
affecting the function of thoracic cage and rib cage mechanics
(Kapreli et al., 2008). This dysfunction might be more apparent
during inspiration as the common muscles of cervical region and
respiration (sternocleidomastoid, scaleni and trapezius) are all
inspiratory in function (Palastanga et al., 2002). Furthermore, the
existence of psychological factors such as kinesiophobia might also
lead to movement avoidance further contributing to the dysfunc-
tion of cervical muscles and consequentially to the potential
changes in rib cage mechanics (Kapreli et al., 2008).
These changes in rib cage biomechanics could lead to associated
changes of respiratory muscles altering their forceelength curves
* Corresponding author. Physiotherapy Department, Technological Educational
Institute (TEI) of Lamia, 3rd km Old National Road Lamia-Athens, 35100 Lamia,
Greece. Tel.: þ30 22310 60176.
E-mail address: email@example.com (Z. Dimitriadis).
Contents lists available at SciVerse ScienceDirect
journal homepage: www.elsevier.com/math
1356-689X/$ e see front matter ? 2012 Elsevier Ltd. All rights reserved.
Manual Therapy 18 (2013) 248e253
and force production abilities (Gossman et al., 1982; Kapreli et al.,
2008). Piloting findings support this belief as patients with
chronic neck pain have been found to present reduction in their
maximal mouth pressures (Kapreli et al., 2009). However, existent
literature provides no other known evidence about the strength of
respiratory muscles in patients with chronic neck pain. Further-
more, the association of respiratory strength with the common
musculoskeletal and psychological manifestations of patients with
chronic neck pain remains completely unexplored. The examina-
tion of the respiratory strength and its association with the known
manifestations of neck pain could lead to a better understanding of
the changes occurring due to neck pain and to improvement of the
usual assessment and treatment provided in these patients. Given
the above, this study was aimed at investigating the possible
existence of respiratory weakness in chronic neck pain patients and
the correlations among the aforementioned factors.
The hypotheses of the present study were that:
H0: Patients with chronic neck pain have no different maximal
inspiratory and expiratory pressures from healthy controls.
H0: Maximal inspiratory and expiratory pressures of patients
with chronic neck pain are not correlated with their musculo-
skeletal (forward head posture, strength of neck muscles,
endurance of deep neck flexors, cervical range of movement,
pain intensity) and psychological (anxiety, depression, cata-
strophizing, kinesiophobia) manifestations.
In this cross-sectional study, 45 patients with chronic neck pain
and 45 healthy gender-, age-, height- and weight-matched controls
were conveniently recruited. Patients were included if they had
pain for at least 6 months with pain complaints at least once aweek
and were between 18 and 65 year old. Patients with spinal or chest
surgeries, smoking history, traumatic cervical injuries, acute or
chronic neuromusculoskeletal pain in any other non-related body
area, serious obesity (Body Mass Index (BMI) >40), clinical abnor-
malities of the thoracic cage or vertebral column, occupational
industrial exposures, serious comorbidities (neurological, neuro-
disorders), diabetes mellitus and/or malignancies were excluded
from the study.
The same eligibility criteria were applied for the healthy control
group. Healthy controls were individually matched with neck pain
patients in terms of gender, age (?5 years), height (?10 cm) and
weight (?10%). All the participants were assessed at the cardiore-
spiratory lab of the Physiotherapy Department, Technological
Educational Institute (TEI) of Lamia, Lamia, Greece during the
2009e2010 years. All the subjects had to sign an informed consent
before their participation to this study. The study was approved by
the Ethics Committee of the Department of Physiotherapy, School
of Health and Caring Professions, TEI Lamia, Greece and the
University of Manchester Ethics Committee.
Maximal Inspiratory Pressure (MIP) and Maximal Expiratory
Pressure (MEP) were assessed in a randomized order from
a standing position (Fig. 1) with a portable mouth pressure meter
(microRPM, Micro Medical Limited, Rochester, Kent, England) and
the accompanying PUMA PC software [Intraclass Correlation
Coefficient (ICC) ¼ 0.81e0.83, Standard Error of Measurement
(SEM) ¼ 12e14 cmH2O] (Dimitriadis et al., 2011). After a short
demonstration of the procedure, the volunteers were asked to
perform 5 maximal inspiratory and expiratory efforts with an at
least 30-s interval between the trials. During the measurement of
maximal mouth pressures the participants were asked to close
firmly their mouth around the flanged mouthpiece. A noseclip was
fitted to avoid any air leak. A small piece of tape was placed on the
mouth pressure meter monitor in order for the participants to be
blind to their performance. The MEP was assessed after asking the
participants to inhale as much as possible and then to exhale
maximally against the resistance of the gauge for at least 1 s. The
MIP was recorded after asking the participants to expire as much as
possible and then to inhale maximally against the resistance of the
gauge for at least 1 s. The participants were verbally encouraged
throughout the procedure for maximal performance. The best of
the inspiratory and expiratory efforts were recorded as the MIP and
The maximal voluntary isometric strength of neck flexors and
extensors was assessed in a randomized order from the Neutral
Head Position (NHP) after a short warm-up period. The measure-
ments were performed in standing position with a custom-made
Fig. 1. Positioning for assessing maximal mouth pressures.
Z. Dimitriadis et al. / Manual Therapy 18 (2013) 248e253
isometric neck dynamometer using a previously described proce-
dure (Strimpakos et al., 2004). High reliability values with small
(ICC ¼ 0.9e0.96, SEM ¼ 12.6e20.8 N) (Strimpakos et al., 2004).
The craniocervical flexion test was used for assessing the
endurance of deep neck flexors. Details about the procedure and
reliability values are provided by previous publications (ICC ¼ 0.91)
(Jull et al., 2008a, 2008b; Arumugam et al., 2011). The measure-
ments were performed from a crook lying position with a pressure
biofeedback device (Stabilizer, Chattanooga, USA), which was
placed behind participants’ neck. The device was initially inflatedto
a baseline pressure of 20 mmHg. The participants had to succes-
sively perform 310-s holds of a head nodding action at each of the 5
pressure levels (22 mmHg, 24 mmHg, 26 mmHg, 28 mmHg and
30 mmHg). Participants’ deep neck flexors were considered
fatigued when pressure decrease at the pressure sensor, apparent
activation of the superficial neck flexors or a jerky action during
holding of the pressure level were observed. The endurance of deep
neck flexors of each participant was considered the maximal
pressure that the participant was able to keep steady for three 10-s
holds without any other substitution strategy.
Cervical Range of Movement (ROM) of all neck movements was
assessed by using the Zebris ultrasound-based motion analysis
system (Zebris Meditchnic GmbH, Isny, Germany) from a standing
position, based on instructions provided by a previously published
paper (Strimpakos et al., 2005). After calibrating the Zebris in order
for the NHP tobe defined equal to 0?, the participants wereasked to
perform three repetitions for each cervical movement. For each
cervical movement the best trial was accepted. The procedure has
(ICC ¼ 0.73e0.86, SEM ¼ 6.5e8.5?) (Strimpakos et al., 2005).
The Forward Head Posture (FHP) was assessed through the
craniovertebral angle (CVA), the angle between the line extending
from the tragus of the ear to the 7th cervical vertebra (C7) spinous
process and the horizontal line through C7. For this purpose three
lateral photographs were obtained after asking the participants to
focus their vision on a predetermined reference point at the height
of their eyes. The photographs were obtained by using a digital
colour camera (HDR-SR11E, Sony, Belgium), and the values were
calculated by using a 3-D drawing software (Auto-CAD 2000,
Autodesk Inc., San Raphael, CA). The mean of the three CVAs was
used for data analysis. The procedure has been previously reported
as very reliable (ICC ¼ 0.88) (Raine and Twomey, 1997).
A numberof questionnaires weregiven toparticipants including
Visual Analogue Scales for assessing current and usual neck pain
intensity (Price et al., 1983), Neck Disability Index for assessing
pain-induced disability (Trouli et al., 2008) and the Baecke Ques-
tionnaire of Habitual Physical Activity for assessing physical activity
level (Baecke et al.,1982). Furthermore, the cross-cultural validated
Hospital Anxiety and Depression Scale (Georgoudis and Oldham,
2001), Tampa Scale for Kinesiophobia (Georgoudis et al., 2007)
and PainCatastrophizing Scale (Argyra et al., 2006) were completed
in a randomized order to reduce any potential bias and ordering
also previously published
2.3. Data analysis
Pearson correlation coefficients and paired t-tests were used for
examining the correlations between the variables and the differ-
ences between the groups, respectively. A backward stepwise
multiple regression analysis (removal ¼ 0.1) was performed for MIP
and MEP. The strength of neck extensors, endurance of deep neck
flexors, sagittal ROM, FHP, usual pain intensity, anxiety, depression,
kinesiophobia and catastrophizing were selected to be the predic-
tors of these models. When data were missing, the individual with
his/her matched participant were removed from the analysis of this
variable. One patient had missing data on left rotation and left
lateralflexion ROM due tosoftwareproblems,1 patient had missing
data on craniocervical flexion test because he had forgotten his
glasses and could not read the feedback from the pressure sensor
and 1 healthy control had missing data on FHP as the hairclip was
broken and was not possible to free the cervical area. The signifi-
cance level was defined equal to 0.05. Statistical Package of Social
Sciences (SPSS, version 17) was used for all data analysis.
The patients with chronic neck pain [32 females, age: 35.9(14.5)
years, height: 165.8(9.2) cm, weight: 71.6(16) kg, BMI: 25.9(4.5),
physical activity: 7.9(1.3)] did not differ significantly from the
healthy matched controls [32 females, age: 35.4(14) years, height:
167.1(8.7) cm, weight: 72.3(15.2) kg, BMI: 25.8(4.4), physical
activity: 7.6(1.4)] in age, height, weight, BMI and physical activity
level (P > 0.05). The patients of the study were predominantly of
mild to moderate neck pain intensity [VAS: 45.5(18.8) mm] and of
mild disability [HADS: 10.6(5.2)] and had pain chronicity of
69.6(57.6) months. Their pain intensity during the measurements
was 19.3(19.1) mm.
The patients were also found to have weak neck extensors
(P < 0.05) and trend for weak neck flexors. They were also pre-
sented with reduced mobility in all cervical movement planes and
impaired deep neck flexors (P < 0.05). However, their FHP was
similar to the control group and they were not more anxious or
depressed (P > 0.05).
Patients with chronic neck pain had a significant 13.8% and
15.4% reduction in their MIP and MEP respectively (P < 0.05)
(Fig. 2), but the MIP/MEP ratio was not significantly affected
(P > 0.05) (Table 1).
Fig. 2. Differences in Maximal Inspiratory Pressure (MIP) and Maximal Expiratory
Pressure (MEP) between patients with chronic neck pain (grey colour) and healthy
controls (white colour).
Differences in maximal mouth pressures between patients with chronic neck pain
and healthy controls.
?13.9 (?25.1, ?2.7)*
?19.5 (?33.6, ?5.5)**
0.03 (?0.05, 0.12)
*P < 0.05, **P < 0.01 MIP: Maximal Inspiratory Pressure, MEP: Maximal Expiratory
Z. Dimitriadis et al. / Manual Therapy 18 (2013) 248e253
MIP was significantly correlated with strength of neck flexors
(r ¼ 0.7, P < 0.001) and extensors (r ¼ 0.62, P < 0.001), kinesi-
ophobia (r ¼ ?0.43, P < 0.01) and catastrophizing (r ¼ ?0.3,
P < 0.05). MEP was significantly correlated with strength of neck
flexors (r ¼ 0.69, P < 0.001) and extensors (r ¼ 0.66, P < 0.001),
usual pain intensity (r ¼ ?0.33, P < 0.05), Neck Disability Index
(NDI) (r ¼ ?0.35, P < 0.05), kinesiophobia (r ¼ ?0.4, P < 0.05) and
catastrophizing (r ¼ ?0.36, P < 0.05) (Fig. 3). All the other corre-
lations were not significant and of small effect size (r < 0.3,
P > 0.05).
The regression analysis showed that the assumption of inde-
pendent errors, homoscedasticity, linearity and normally distrib-
uted errors had been met. Multicollinearity was not found to be of
concern and no influential outliers were recognized. The models
Fig. 3. Correlations between maximal mouth pressures [maximal inspiratory pressure (black dots, solid line) and maximal expiratory pressure (white dots, dashed line)] and
strength of neck extensors (upper left), strength of neck flexors (upper right), pain intensity (middle left), disability (middle right), kinesiophobia (bottom left) and catastrophizing
(bottom right) (NDI: Neck Disability Index, TSK: Tampa Scale for Kinesiophobia, PCK: Pain Catastrophizing Scale).
Z. Dimitriadis et al. / Manual Therapy 18 (2013) 248e253
revealed that strength of neck extensors is the only significant
common predictor of MIP and MEP. However, the MIP model also
included kinesiophobia and the MEP model also included FHP as
predictors (Table 2). The multiple correlation coefficients and the
generalizability of the prediction models of MIP (R ¼ 0.66,
R2¼ 0.44, adjusted R2¼ 0.41) and MEP (R ¼ 0.7, R2¼ 0.49, adjusted
R2¼ 0.46) were satisfactory.
This study was designed to investigate the potential existence of
respiratory weakness in patients with chronic neck pain and its
associations with neck pain manifestations. According to the find-
ings, patients with chronic neck pain have reduced strength of
respiratory muscles. Neck muscle strength, kinesiophobia and
catastrophizing are significantly correlated with respiratory muscle
strength, whereas pain intensity and disability are additionally
associated with strength of expiratory muscles. However, only the
strength of neck muscles remains as significant predictor of respi-
ratory weakness when all the neck pain complaints are put
together into a regression model.
The results of the study are supported by the preliminary find-
ings by Kapreli et al. (2009) where a 21.5% drop of MIP and 16.5%
drop of MEP were also observed. The fact that the MIP/MEP ratio
was not different suggests that the two respiratory indices were
similarly reduced in patients with chronic neck pain. This fact
implies that the reduction in respiratory muscle strength cannot be
attributed only to the common function of sternocleidomastoid,
scaleni and trapezius in neck movement and inspiration, since in
this case inspiratory pressures could be more affected. Thus, the
origins of this weakness should be the result of additional physical
and psychological mechanisms.
Strength of neck muscles was found to be the deficit which is
mostly associated with strength of respiratory muscles. Although
this association could be attributed to a generalized weakness of
patients with chronic neck pain, the same physical activity levels of
the two groups does not justify such a notion. Thus, this association
could be mainly based on the affected kinetic control of the cervical
Patients with chronic neck pain were found to have reduced
performance of their global and local muscles. Dysfunction of these
muscles is believed to lead to reduced respiratory performance
mainly because of a) the common function of sternocleidomastoid,
trapezius and scaleni on cervical movement and inspiration
(Palastanga et al., 2002; Legrand et al., 2003), b) changes in forcee
length curves and muscles imbalances (Gossman et al., 1982), c)
segmental instability of the cervical spine (Comerford and
Mottram, 2001) which might be also observed in thoracic spine
because of muscles such as longus colli which attach in both areas
(Palastanga et al., 2002) and d) impairment of neck proprioceptors
(Boyd-Clark et al., 2002) rendering more difficult for the patients to
find the optimal alignment of their spine (Key et al., 2008). These
changes have been proposed to lead to adapted kinetic and kine-
matic patterns of rib cage, changing the forceelength relationships
of the associated respiratory muscles and consequentially leading
to alteration of their contraction patterns (Kapreli et al., 2008).
These mechanical changes of respiratory muscles may influence
their force production abilities and can lead to a permanent
respiratory weakness due to plastic changes (Gajdosik, 2001;
The existence of psychological states seems to playan additional
role contributing to this respiratory weakness. Kinesiophobia may
directly lead to reduced respiratory strength due to poorer
performance during the pulmonary function testing (Ruppel,
2009). However, its role seems to be rather indirect through
a further deconditioning of the neck muscles because of prolonged
neck movement avoidance (Kapreli et al., 2008). Limited neck
movement can lead todeconditioningof neck musclesand adaptive
changes (Gajdosik, 2001; Bruton, 2002) further affecting the local
and global muscles and consequentially respiratory function.
Interestingly, pain intensity and disability were found to be
correlated only with MEP. If the respiratory weakness observed in
patients with neck pain was mostly dependent on the common
function of sternocleidomastoid, scaleni and trapezius in cervical
movement and respiration, MIP would be expected to have
a stronger association with this respiratory weakness. This fact
reveals that respiratory muscle weakness in patients with chronic
neck pain cannot be mainly attributed to the common function of
these muscles on both neck movement and inspiration and high-
lights that this weakness is a multidimensional dysfunction where
causes should be also sought in combination with the biome-
chanical and psychological mechanisms of other neck pain
An interesting trend was also observed in the regression models
as it was found that FHP can negatively predict MEP. This means
that an increase in FHP is associated with improved respiratory
strength. Although this association seems to be strange, it has been
also noted in a previous pilot study (Kapreli et al., 2009). Okuro
et al. (2011) have also reported that children with forward head
posture present increased MIP and MEP. Forward head posture can
be adopted by patients with poor breathing as an attempt to
increase airflow and improve respiratory function (Perri and
Halford, 2004; Okuro et al., 2011). Thus, FHP in patients with
chronic neck pain can be viewed not only as a maladaptive posture,
but it might be also a compensatory mechanism for improving
In comparison to normative data established by Evans and
Whitelaw (2009), patients with chronic neck pain had 5.5%
reduction in their inspiratory and 4.1% reduction in their expiratory
muscle strength (Evans and Whitelaw, 2009). However, in this
study patients’ respiratory strength was compared with the respi-
ratory strength of healthy matched-controls and was found to
present a higher decrease (13.8%e15.4%). This difference can be
attributed to the fact that the latter percentages derived from
comparison with a similar sample of healthy participants rather
than from predicted models based on a different population.
Although there is no objective cut-off point for defining muscle
weakness, the decrease in respiratory strength of neck patients
does not exceed 20% which is the percentage proposed by the
American Thoracic Society/European Respiratory Society for
defining considerable decline in muscle strength (American
Thoracic Society/European Respiratory Society, 2002). However,
even though this fact reveals that the respiratory weakness of
patients with chronic neck pain cannot be considered as
Regression models for the prediction of Maximal Inspiratory Pressure (MIP) and
Maximal Expiratory Pressure (MEP). This table presents the beta values (B) with
their 95% Confidence Intervals (95% CI) and their Standard Error (SE B) as well as the
standardized beta values (b) for the prediction of MIP and MEP in patients with
chronic neck pain.
B (95% CI) SE B
Strength of neck extensors
Strength of neck extensors
Forward head posture
92.14 (45.13, 139.14)***
1.98 (1.05, 2.91)***
?1.06 (?2.2, 0.09)
133.98 (46.82, 221.14)**
3.53 (2.37, 4.69)***
?1.67 (?3.5, 0.12)
**P < 0.01, ***P < 0.001.
Z. Dimitriadis et al. / Manual Therapy 18 (2013) 248e253
pathological, there is an obvious dysfunction of respiratory muscles Download full-text
which needs clinical attention. Provided that the sample of patients
used in this study was predominantly of mild neck pain and
disability, it could be stipulated that the observed respiratory
weakness may be more pronounced in patients of more severe
condition and requires further investigation.
The respiratory weakness observed in patients with chronic
neck pain can importantly influence the clinical scientists as it is
accompanied by important clinical implications about the usual
treatment of chronic neck pain. Based on the findings of this study,
it can be suggested that the respiratory function should be also
included into assessment and treatment of patients with chronic
neck pain. However, future studies should also examine the effec-
tiveness of additional respiratory exercises as complementary to
the usual treatment of patients with chronic neck pain. Electro-
myographic studies can enhance the knowledge about the activa-
tion patterns of muscles related with cervical and respiratory
function in patients with chronic neck pain. Studies by using
optoelectronic plethysmography can also offer a better under-
standingof respiratory function and respiratory kinematics in these
patients contributing to more suitable designs of therapeutic
Chronic neck pain does not seem to be a condition related only
with neuromusculoskeletal and psychological manifestations, but
it appears to have more dimensions. Respiratory function of
patients with chronic neck pain can be also affected as they present
with weakness of their respiratory muscles. Cervical muscle
dysfunction and psychological influences appear to be the factors
that are mostly associated with this respiratory dysfunction. These
conclusions suggest the incorporation of assessment and rehabili-
tation of respiratory function into the usual clinical approaches
used for patients with chronic neck pain. This can lead tochanges in
clinical reasoning with potentially more optimal therapeutic
outcomes for these chronic pain sufferers.
We would like to thank the participants for the willingness to
participate in this study, Ms Lamprini Komnianou for technical
assistance and Dr Steve Roberts for statistical advice.
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