Abstract
Purpose: People with neck pain are likely to have negative respiratory findings. The purpose of this study was to investigate the relationship between neck pain and dysfunctional breathing and to examine their relationship to stress. Method: This cross-sectional study included 49 participants with neck pain and 49 age- and sex-matched controls. We measured neck pain using the numeric rating scale (NRS); neck disability using the Neck Disability Index (NDI); dysfunctional breathing using the Nijmegen Questionnaire (NQ), Self-Evaluation of Breathing Questionnaire (SEBQ), breath hold time, and respiratory rate (RR); and stress using the Perceived Stress Scale (PSS). Results: Participants with neck pain scored higher on the NQ (p < 0.01) and the SEBQ (p < 0.01) than controls. NQ and SEBQ scores correlated moderately with NDI scores (r > 0.50; 95% CI: 0.25, 0.68 and 0.33, 0.73, respectively) and PSS scores (r > 0.50; 95% CI: 0.29, 0.78 and 0.31, 0.73, respectively). SEBQ scores showed a fair correlation with NRS scores and RR a fair correlation with NDI scores. Conclusions: Participants with neck pain had more dysfunctional breathing symptoms than participants without neck pain, and dysfunctional breathing was correlated with increased neck disability and increased stress. The NQ and SEBQ can be useful in assessing dysfunctional breathing in patients with neck pain.
Key Words: anxiety, dysfunctional breathing, hyperventilation, neck disability, neck pain, stress
Abstract
Objectif : les personnes qui éprouvent des douleurs cervicales sont susceptibles d’avoir des problèmes respiratoires. La présente étude visait à examiner le lien entre les douleurs cervicales et une respiration dysfonctionnelle, de même que leur lien avec le stress. Méthodologie : la présente étude transversale incluait 49 participants ayant des douleurs cervicales et 49 sujets témoins appariés. Les chercheurs ont mesuré la douleur cervicale au moyen de l’échelle d’évaluation numérique (ÉÉN); les incapacités cervicales au moyen de l’indice d’incapacité cervicale (IIC); la respiration dysfonctionnelle au moyen du questionnaire de Nijmegen (QN), du questionnaire d’autoévaluation de la respiration (QAÉR), de la durée de retenue de la respiration et de la fréquence respiratoire (FR); et le stress au moyen de l’échelle de perception du stress (ÉPS). Résultats : les participants qui éprouvaient des douleurs cervicales obtenaient des résultats plus élevés que les sujets témoins au QN (p < 0,01) et au QAÉR (p < 0,01). Les scores du QN et du QAÉR avaient une corrélation modérée avec les scores de l’IIC (r > 0,50; IC à 95 %, 0,25, 0,68 et 0,33, 0,73, respectivement) et les scores de l’ÉPS (r > 0,50; IC à 95 %, 0,29, 0,78 et 0,31, 0,73, respectivement). Les scores du QAÉR ont révélé une corrélation claire avec les scores de l’ÉÉN et la FR, ainsi qu’avec les scores de l’IIC. Conclusions : les participants qui éprouvaient des douleurs cervicales avaient plus de symptômes de respiration dysfonctionnelle que les participants sans douleur cervicale, et la respiration dysfonctionnelle était corrélée avec une incapacité cervicale et un stress accrus. Le QN et le QAÉR peuvent être utiles pour évaluer la respiration dysfonctionnelle chez les patients éprouvant des douleurs cervicales.
Mots-clés : : douleur cervicale, incapacité cervicale, respiration dysfonctionnelle, stress
Chronic neck pain is common in the general population.1 It has a high global prevalence2 and generally a poor prognosis.3 Research has suggested that neck pain is related to altered breathing biomechanics and hypocapnia.4,5
The neck is connected to the thorax through many muscular, fascial, and neural structures.6 Therefore, movement of the thorax impacts the neck and vice versa. Research has correlated respiratory weakness with neck weakness,5,7 and people with neck pain are more likely to have a chest-dominant breathing pattern,8,9 putting strain on the neck accessory muscles.10
Breathing is multidimensional, comprising biomechanical, biochemical, and psychological dimensions;11 dysfunctional breathing is breathing function that is compromised in any one of these dimensions.11,12 Hyperventilation is one example of dysfunctional breathing.11 Hyperventilation reduces pain perception of an acute painful stimulus13 and is thought to be a normal coping response to pain.14 However, persistent hyperventilation results in alkalosis, which is associated with muscle tension, muscle spasm, and muscle ischaemia.15 If the respiratory system does not correct the alkalosis, metabolic compensation occurs that partially corrects pH by increasing the excretion of calcium in the urine,16 further exaggerating muscle and nerve dysfunction. This process may explain why people with chronic neck pain are more likely to have reduced CO2 levels.17,18
Hyperventilation is also associated with anxiety-related disorders.13,19 Feelings of anxiety and stress cause an increase in sympathetic activity, leading to changes in breathing rate and depth and increased muscle tension.13,16 This increase in sympathetic activity may also be related to the finding that anxiety and depression are more common in people with neck pain and increased neck disability.5,20
To our knowledge, no research has investigated the presence of dysfunctional breathing in participants with neck pain and how dysfunctional breathing and neck pain relate to stress. The objectives of this study were to investigate differences in dysfunctional breathing measures between participants with and without neck pain, the association of neck pain and neck disability with measures of dysfunctional breathing and stress, and the association of dysfunctional breathing with stress in participants with and without neck pain.
Methods
Design and setting
This study had a quantitative cross-sectional analytical design. We conducted assessments in a private physiotherapy practice in Johannesburg, South Africa, between July and December 2019.
Participants
We used convenience sampling to recruit participants from the physiotherapy practice where the first author worked and from the public. Participants in the study group had neck pain of insidious onset and were between ages 20 and 60. Participants in the control group were pain free in the neck, shoulder, and thorax and had not experienced neck pain in the preceding 6 months; they were matched in age (± 5 years) and sex to the study group. Exclusion criteria for the study group were neck trauma; previous surgery of the spine, thorax, or upper abdomen; pathology of the lung, heart, or neuromuscular system (excluding asthma); one or more asthma attacks in the preceding 6 months; current acute infection; and current smoking.
We determined that 49 participants in each group would be sufficient using a two-sample t-test based on the mean differences in maximum voluntary ventilation (study group, 92.2 L/min; control group, 104.4 L/min) with an estimated within-group SD of 21.2,7 and the assumption of a 5% significance level and a power of 80%. Maximum voluntary ventilation gives a general indication of respiratory function.7
Outcome measures and instruments
Neck pain and neck disability
The numeric rating scale (NRS) is a quick, easy-to-use tool to evaluate pain intensity in adults.21 Respondents rate their pain as a whole number from 0 (no pain) to 10 (worst pain imaginable).21 The NRS is able to detect change in neck condition, and previous research reported intra-class correlation coefficients (ICCs) for test–retest reliability in stable patients of 0.7622 for those with mechanical neck pain and 0.58−0.8823for those with cervical radiculopathy. For the current study, scores of 0–5 represent mild pain, 6–7 moderate pain, and 8–10 severe pain.24
The Neck Disability Index (NDI) is a self-report questionnaire containing 10 sections; it assesses the extent to which neck pain affects everyday activities.25 For each section, respondents choose 1 of 6 response options that are scored from 0 to 5.26 Many studies have reported test-retest reliability coefficients above 0.90,25 and test re-test reliability is reported to be better (ICCs > 0.90) when clients are tested on one occasion but in different languages or presented in a different order25 than when repeated tests occur over longer periods (ICCs = 0.50−0.55).22,23 The NDI is internally consistent and has strong convergent and divergent validity with other tests used to assess neck pain.27 It has good construct validity and responsiveness for neck pain of various presentations and populations.25 We interpreted NDI scores as Vernon27 recommended: 0–4, no disability; 5–14, mild disability; 15–24, moderate disability; 25–34, severe disability; and 35–50, complete disability.
Dysfunctional breathing
The Nijmegen Questionnaire (NQ) consists of 16 symptom-related questions patients answer using a 5-point scale from 0 (never) to 4 (very often). Researchers have used a cutoff score of 23 for the diagnosis of hyperventilation.28,29 On the basis of symptoms reported by clinicians and patients with experience with hyperventilation, researchers have found that the NQ has good content validity for hyperventilation but poor structural validity.30 Reports of NQ scores corresponding with hypocapnia have been inconsistent.31,32 The NQ has an ICC test-retest reliability of 0.87 and good responsiveness to change after treatment for a range of respiratory and non-respiratory complaints.33
The Self-Evaluation of Breathing Questionnaire (SEBQ) contains 25 questions that relate to symptoms of dysfunctional breathing.34 Clients rate each statement on a 4-point scale from 0 (never or not true at all) to 3 (very frequently or very true)35; scores greater than 11 indicate dysfunctional breathing.32 In the general population, the SEBQ’s test-retest reliability (ICC) is 0.89 and internal consistency (Cronbach’s α) is 0.93.35
Breath hold time (BHT) tests the length of breath hold at functional residual capacity. BHTs less than 20 seconds are mildly suggestive and less than 10 seconds strongly suggestive of dysfunctional breathing.36 The use of BHT as a diagnostic tool for measuring hyperventilation is inconsistent in the literature,37,38 and no significant correlation has been found between BHT and end-tidal CO2.32,39
Respiratory rate (RR) is the number of breaths per minute, and elevated RR may be associated with acute hyperventilation, pain, or anxiety.13,12 Tachypnoea is defined as an RR of more than 20 breaths per minute in adults.40
Perceived stress
The Perceived Stress Scale (PSS) is a measure of general distress and coping ability.41–43 The questionnaire has 10 statements, and the client rates each statement on a 5-point scale from 0 (never) to 4 (very often). The test has good internal consistency reliability and test-retest reliability, with average Cronbach’s αs greater than 0.70 for both.44
Procedure
We obtained permission to conduct the study from the associated institutions’ ethics review boards, and we conducted all procedures in accordance with institutional and national ethical standards and the Helsinki Declaration. We provided participants with details about the study, and they signed an informed consent form. To minimize bias, we administered the assessments in the same order using the same instructions for all participants.
Questionnaires
All participants completed the NQ, SEBQ, and PSS, as well as a questionnaire we developed for this study that contained the numeric rating scale and questions about the inclusion and exclusion criteria. The study group also completed the NDI. Control group participants did not fill in the NRS section of the study questionnaire or complete the NDI.
Breath hold time
To measure BHT, we asked participants to be seated. We instructed them to breathe in, then breathe out to a comfortable exhale, and then hold their breath at the volume at which they would normally breathe in again. We used a stopwatch to measure the hold time in seconds and recorded the average of three measurements.
Respiratory rate
We measured RR by observing participants’ chest and abdomen as they sat facing forward. We recorded the number of breaths observed in 1 minute.
Data analysis
We used SAS Version 9.4 (SAS Institute, Cary, NC) for data analysis. We used the two-sample t-test to compare dysfunctional breathing and perceived stress in participants with neck pain to those without, and we used Fisher’s exact test to compare percentages of participants with dysfunctional breathing according to the NQ and SEBQ. To evaluate the association of neck pain and neck disability with measures of dysfunctional breathing and perceived stress, we used Spearman correlation coefficients, and we applied the Satterthwaite correction because of the heterogeneity of variances. Our null hypothesis was that we would find no difference in measures of dysfunctional breathing between groups and no correlations between variables.
Results
Study participants
The sample consisted of 98 participants, 49 with neck pain (study group) and 49 without (control group). Both groups had 38 female and 11 male participants. Participants’ mean ages were 36.5 (SD 11.49) years in the study group and 36.2 (SD 11.92) years in the control group.
Assessment results
Neck pain and neck disability
Most study group participants had mild pain; the mean score on the NRS was 4.37 (SD 2.06). Most also had mild disability; the mean NDI score was 10.98 (SD 3.19). (See table 1).
Table 1 .
Neck Pain and Disability in the Study Group (n = 49)
| No. (%) of participants
|
||||||
|---|---|---|---|---|---|---|
| Measure | Mean (SD) | Median (1stQ, 3rd Q) | None | Mild | Moderate | Severe |
| Pain—NRS | 4.4 (2.1) | 4 (3,6) | 0 | 31 (63.3) | 16 (32.7) | 2 (4.1) |
| Neck disability—NDI | 11 (5.2) | 10 (7,13) | 3 (6.1) | 36 (73.5) | 10 (20.4) | 0 |
Q = quartile; NRS = numeric rating scale (mild pain, 0-5; moderate pain, 6-7; severe pain, 8-10); NDI = Neck Disability Index (no disability, 0-4; mild disability, 5-14; moderate disability, 15-24).
Dysfunctional breathing
NQ and SEBQ scores were higher in participants with neck pain than in those without (p < 0.01). BHT and RR were similar in both groups (Table 2). NQ (p = 0.09) and SEBQ (p < 0.01) scores showed that more participants in the study group than in the control group had dysfunctional breathing (using Fisher’s exact test and cutoff scores of 23 and 11 respectively; Table 3).
Table 2 .
Measures of Dysfunctional Breathing
| Measure | Study group; n = 49
|
Control group; n = 49
|
Two-sample t -test
|
Between-groups difference (SE) | |||
|---|---|---|---|---|---|---|---|
| Mean (SD) | Min-Max | Mean (SD) | Min-Max | t -value | p -value | ||
| Nijmegen Questionnaire | 17.6 (10.3) | 0–42 | 11.2 (7.5) | 0–3 | 0–3.5088 | < 0.01 | 6.4 (1.8) |
| Self-Evaluation of Breathing Questionnaire | 17.1 (12.5) | 0–51 | 8.9 (7.2) | 0–3 | −3.9677 | < 0.01 | 8.2 (2.1) |
| Breath hold time, s | 26.9 (9.2) | 11.9–53.9 | 30.3 (10.9) | 14.3–70.6 | 1.7096 | 0.09 | −3.4 (2.0) |
| Respiratory rate, breaths × min | 15.0 (3.6) | 9–24 | 14.7 (3.1) | 7–20 | −0–4396 | 0.67 | 0.3 (0.7) |
Table 3 .
Normal and Dysfunctional Breathing in the Study Group (n = 49) and Control Group (n = 49) According to Scores on the Nymegen Questionnaire and Self-Evaluation of Breathing Questionnaire
| Breathing function | Nijmegen Questionnaire
|
Self-Evaluation of Breathing Questionnaire
|
||||
|---|---|---|---|---|---|---|
| No. (%)
|
No. (%)
|
|||||
| Study group | Control group | p -value | Study group | Control group | p -value | |
| Normal | 34 (69.4) | 45 (91.8) | 0.61 | 18 (36.7) | 34 (69.4) | < 0.01 |
| Dysfunctional | 15 (30.6) | 4 (8.2) | 31 (63.3) | 15 (30.6) | ||
Perceived stress
PSS mean scores were similar for the study group, 17.16 (SD 7.38), and the control group, 16.04 (SD 7.72; p = 0.46).
Analysis results
Table 4 summarises the association of pain intensity and neck disability with measures of dysfunctional breathing and perceived stress. SEBQ scores (dysfunctional breathing) correlated with NRS scores (pain intensity), and NDI scores (neck disability) correlated with NQ and SEBQ scores (dysfunctional breathing). NDI scores (neck disability) also correlated with respiratory rate and, to some degree, with PSS scores (perceived stress). In addition, Table 5 shows that PSS scores (stress) correlated with NQ and SEBQ scores (dysfunctional breathing) but not with breath hold time or respiratory rate.
Table 4 .
Correlations of Neck Pain and Disability with Dysfunctional Breathing and Perceived Stress in the Study Group (n = 49)
| Measure | Pain (NRS)
|
Neck disability (NDI)
|
||
|---|---|---|---|---|
| r(95% Cl) | p -value | r(95% Cl) | p -value | |
| Nijmegen Questionnaire | 0.21 (−0.08, 0.46) | 0.16 | 0.50 (0.25, 0.68) | < 0.01 |
| Self-Evaluation of Breathing Questionnaire | 0.29 (0.01, 0.53) | 0.04 | 0.56 (0.33, 0.73) | < 0.01 |
| Breath hold time, s | −0.06 (−0.34, 0.22) | 0.67 | −0.15 (−0.41, 0.14) | 0.23 |
| Respiratory rate, breaths × min | 0.10 (−0.19, 0.37) | 0.51 | 0.44 (0.18, 0.64) | < 0.01 |
| Perceived Stress Scale | 0.12 (−0.17, 0.39) | 0.41 | 0.26 (−0.03, 0.50) | 0.07 |
NRS = numeric rating scale; NDI = Neck Disability Index.
Table 5 .
Correlations of Perceived Stress Scores with Measures of Dysfunctional Breathing
| Measure | Perceived Stress Scale scores
|
|||
|---|---|---|---|---|
| Study group (n = 49)
|
Control group (n = 49)
|
|||
| r (95% Cl) | p -value | r (95% Cl) | p -value | |
| Nijmegen Questionnaire | 0.54 (0.29, 0.71) | < 0.01 | 0.65 (0.44, 0.78) | < 0.01 |
| Self-Evaluation of Breathing Questionnaire | 0.55 (0.31, 0.72) | < 0.01 | 0.57 (0.33, 0.73) | < 0.01 |
| Breath hold time, s | −0.20 (−0.46, 0.09) | 0.17 | −0.02 (−0.30, 0.27) | 0.92 |
| Respiratory rate, breaths × min | 0.08 (−0.21, 0.35) | 0.61 | < 0.01 (−0.28, 0.29) | 0.97 |
Discussion
In this study, participants with neck pain reported more symptoms of dysfunctional breathing than those without neck pain on the NQ and SEBQ. In addition, their NQ and SEBQ scores correlated with scores on measures of neck pain and neck disability. These results are unique; no previous study has evaluated dysfunctional breathing in people with neck pain using the NQ and SEBQ.
Study participants
There were more female than male participants in each group; 38 (77.6%) of the participants with neck pain were female. The literature has reported a higher prevalence of neck pain and higher recurrence in women,>2,45 perhaps because of hormone differences.46
The average age in this study was approximately 36 years, whereas the reported peak prevalence of neck pain occurs at ages 40 to 49 years1; in addition, mean pain intensity and neck disability in the study group were mild. The relatively young age of the participants and mild levels of pain and disability can likely be attributed to the inclusion of participants who were not seeking physiotherapy or medical intervention for their neck pain.
Dysfunctional breathing
The NQ contains questions relating to symptoms of hypocapnia resulting from hyperventilation, breathing difficulty, and the psychological component of dysfunctional breathing.31 Thus, the NQ assesses the biochemical and psychological dimensions of dysfunctional breathing, whereas the SEBQ addresses primarily the biochemical and biomechanical components of dysfunctional breathing.34 In this study, the SEBQ had a stronger correlation with neck disability and pain intensity than the NQ, suggesting that the biochemical and biomechanical components of dysfunctional breathing were more strongly present in our sample of participants with mild neck pain.
Average BHT was only slightly longer in the control group than the study group (p = 0.09) and was not correlated with neck pain or disability. Reports of the relationship between BHT and hypocapnia have been inconsistent, and although BHT can be used to diagnose dysfunctional breathing, it is not necessarily related to other tests of dysfunctional breathing.32,38
Our findings that RR was similar in participants with and without neck pain (p = 0.67) and that RR did not correlate with pain is contrary to studies reporting an increase in RR in response to pain.13 The reason for the differing findings may be that breathing responses to pain vary14 and depend on a variety of factors, including the context and individual emotional response to pain.13 Therefore, resting RR alone may not be sufficient to determine respiratory response to pain. Furthermore, most participants in this study reported only mild pain, which may have minimised their body’s response.
Negative thoughts and emotions also influence RR,13,47 and psychosocial factors have been strongly linked to neck disability.48 We found a stronger correlation between RR and NDI scores than between RR and PSS scores, however, indicating that perhaps our participants’ related more to psychological factors surrounding disability-related activity limitations than to general distress or coping, which the PSS measures.
Correlations between perceived stress and neck pain and disability
Our findings of a lack of association between perceived stress and neck pain and a weak relationship between stress and neck disability were unexpected, considering the literature that supports the link between neck pain and psychosocial factors.20,48,49 Our results may suggest that general distress and coping difficulty as assessed by the PSS are less prevalent in people with neck pain than depression or anxiety, which previous studies measured.5,20,48 In addition, depression and anxiety are more likely to occur in people with high levels of neck pain,48 and many of our participants had only mild neck pain. Dimitriadis and colleagues20 reported that participants with chronic neck pain of mild to moderate intensity and mild disability had levels of anxiety and depression similar to those of participants without neck pain.
Correlations between perceived stress and dysfunctional breathing
The correlations between PSS scores and NQ and SEBQ scores suggest a relationship between dysfunctional breathing and stress. Other studies have reported high NQ scores in people with anxiety disorders.29 Both stress and anxiety stimulate the sympathetic nervous system, which affects breathing, and they likely contribute to increased symptoms of breathing dysfunction.50
A study of people with panic disorder found they had shorter BHTs than healthy controls.51 We found no association between BHT and PSS, perhaps because of differences in the presentation of stress and panic disorder or because the participants in our study reported only low to moderate stress levels.
This study had several limitations. We recruited participants by convenience, resulting in narrow population diversity; therefore, generalizability of the results is limited. We based the sample size on differences in maximum voluntary ventilation (an outcome measure we did not assess in the current study) as this gave a general indication of respiratory function. Our participants included people with neck pain who were not attending a health care facility, which may have contributed to the mild levels of reported pain and disability in our sample. All testing was done by one researcher, a potential source of bias.
Conclusion
This study confirms previous research on negative respiratory findings in people with neck pain. Participants with neck pain in our study reported more symptoms of dysfunctional breathing, as reflected in NQ and SEBQ scores, than participants without neck pain. NQ and SEBQ scores were moderately to strongly correlated with neck disability and perceived stress in the study group. In addition, SEBQ scores correlated at a fair level with pain intensity. The results of this study suggest that the NQ and SEBQ can serve as useful assessment and outcome measures in screening for and treating dysfunctional breathing in patients with neck pain. The SEBQ may be especially useful in assessing dysfunctional breathing in patients with mild neck pain. The NQ and SEBQ are more accessible and easier to use than spirometry, respiratory strength, or capnography, which have been used in previous studies.17,52
Key Messages
What is already known on this topic
People with neck pain are more likely to differ in breathing biomechanics, respiratory weakness, and hypocapnia from people without neck pain.5,7 Dysfunctional breathing and neck pain are both associated with psychological factors.5,20
What this study adds
This study supports use of the Nijmegen Questionnaire and the Self-Evaluation of Breathing Questionnaire as easy-to-use assessment tools for the diagnosis and management of dysfunctional breathing in patients with neck pain. The study also confirms that dysfunctional breathing is positively correlated both to neck disability and stress, and sheds light on the relationships between dysfunctional breathing, neck pain, and stress, which had not previously been examined in one sample group.
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