Post COVID REspiratory mechanisms and the efficacy of a breathing exercise intervention for DYsregulated breathing (Remedy): A feasibility RCT study

Abstract

Background

Dysregulated breathing is a major cause of persisting breathlessness for many people following acute COVID-19 illness. There is little evidence to support the use of breathing interventions within this population.

Methods

A feasibility study was conducted to investigate the potential role of supervised, remote online yogic breathing as an intervention, compared to usual care. The intervention was a six-week group programme, in which they were encouraged to attend bi-weekly. Primary outcomes of attendance, completion and acceptability were recorded and a survey following the intervention. Secondary measures of breathlessness and physical function were collected.

Results

Of 122 people invited who had reported dysregulated breathing at the time of clinical consult, 40 consented and 34 were randomised (Intervention n=17, usual care n=17), 33 had initial assessment (n=16 and n=17) and with post-intervention outcomes available in n=13 and n=14, respectively. Of the 13 in the intervention arm, 5 people completed >75% of sessions and the post intervention assessment. The median number of sessions attended per participant was 7. No safety issues were recorded. The survey (n=13) of the actual intervention highlighted it was well received but there was limited options for attending. Although some breathlessness measures improved in the people receiving the intervention, there was no significant difference when comparing the intervention to usual care arms.

Conclusions

The feasibility of the study was limited in this select population of people after COVID-19 with dysregulated breathing. The intervention was well received, but attendance at all the sessions was challenged by the limited options for the sessions.

Keywords

COVID-19 dysregulated breathing breathing pattern disorder breathing control long COVID yoga

Introduction

Dysregulated breathing, or breathing pattern disorder, are terms describing chronic changes in a person’s breathing pattern and can be characterised by dyspnoea,¹ reduced exercise tolerance and air hunger.² Whilst it has been recognised in other lung conditions including in asthma² for some time, it is now recognised as a common cause of persisting breathlessness following acute COVID-19 illness.^3,4

Previously, there has been limited focus on identifying and managing people with dysregulated breathing. Traditionally, where addressed, management of dysregulated breathing in asthma has included breathing retraining, positioning, relaxation and education,⁵ often as a one-off physiotherapy consult, but there is little robust scientific evidence to support these interventions.⁶ Different breathing retraining programmes, along with yoga breathing techniques, have been proposed for various patient populations, including COVID-19 Breathlessness.^7–9 In particular, yoga-based pranayama breathing exercises improve respiratory function due to a number of underlying mechanistic factors, including expanding the lungs, relaxing chest muscles, increasing respiratory stamina, raising energy levels, and calming the body.^9,10 Unfortunately, these benefits are largely anecdotal due to study limitations/design of these trials which have limited generalisability to those surviving COVID-19.

A multidisciplinary diagnostic assessment respiratory clinic in Nottingham for those with persisting breathlessness following COVID-19 illness identified a high prevalence of dysregulated breathing in this population⁴ highlighting a need for interventions that would benefit this population.

This study is a feasibility randomised controlled trial (RCT) study exploring a physiotherapy-led, group-based, remote yogic breathing intervention for those with dysregulated breathing and persistent breathlessness following COVID-19 illness.

Methods

Trial design and setting

This was a single centre prospective feasibility study RCT design. Participants with clinically evident dysregulated breathing following COVID-19, and with persistent breathlessness were invited to participate. Ethical approval was awarded (22/LO/0642; IRAS 314769) and was prospectively registered on ClinicalTrials.gov: NCT05732571. Participants were approached i) at the time of review at the post-COVID respiratory diagnostic assessment clinic or ii) a post hospital clinic attendance at the Nottingham University Hospitals (NUH) from January 2023 until December 2023. Additionally, invitations were sent to people who had previously been reviewed in a post COVID clinic, with dysregulated breathing and expressed interest in future research. Written informed consent was sought. All study visits were completed in the Nottingham Health Recovery Research Facility (NHRRF) or Clinical Research Facility at Nottingham City Hospital.

Eligibility was based on a persisting (>12 weeks) self-reported breathlessness following COVID-19; comprehensive clinical respiratory assessment; confirmed dysregulated breathing (including a Nijmegen Questionnaire score (NQ) >23) at time of assessment; aged 18 – 80 years of age; ability to give informed consent and speak English language.

Exclusion criteria were severe mood disturbance, no access to online delivery and/or IT illiterate. Pre-existing myalgic encephalitis, fibromyalgia or chronic fatigue syndrome or a diagnosis of asthma or another chronic lung disease prior to COVID-19 were also exclusions.

Randomisation and blinding

Participants were randomised in a 1:1 ratio (Intervention: usual care (UC)) using a sealed envelope block randomisation process. The study was single-blinded and managed through the use of two separate teams: an intervention team who managed the randomisation, the intervention session and planning and a blinded outcome team who performed the assessments in all subjects. Unblinding of the outcomes team occurred at study end and after initial statistical analysis.

Duration of the trial/study and participant involvement

Participants agreeing to enter the study attended the NHRRF on up to three separate occasions for assessment (see study schedule, Figure 1). This was one week prior to starting and one week after completion of the intervention or usual care. (This was then followed by the 6-week cross over phase and a third visit where the person stayed in the study – not reported here as numbers dwindled further).

Figure 1.

Study schedule and duration.

Intervention

A six-week, twice weekly, on-line breathing exercises intervention was delivered by a trained physiotherapist, lasting 40-50 minutes, via “DoctorDr” online software.

Participants were called prior to intervention start date, to ensure they could correctly access and navigate online sessions.

Intervention sessions began with an introduction, followed by review of previous session and then measuring pre-session BS and RPE. A warmup (gentle yoga-based stretches to mobilise shoulder girdle and thoracic cage) of 5 minutes preceded a 30-minute intervention including breathing training, yogic breathing practice including pranayama and meditation techniques. Participants were able to choose from a variety of seated, standing or lying positions according to their ability. All sessions concluded with a gentle five-minute cool down replicated from the warmup. End session measures of BS and RPE were repeated after the cooldown. Please refer to Supplemental Material for detailed script of the intervention.

Participants not initially allocated to the intervention were offered it after visit 2.

Study outcomes

Primary objective: To evaluate the feasibility (attendance and completion) of a 6-week online, remote breathing intervention using yogic techniques in a population of people with persisting breathlessness due to confirmed dysregulated breathing after COVID-19. Acceptable completion of the intervention was classed as >75% attendance and a visit 2 assessment post intervention.

Other key study outcomes to guide future studies were a) change in breathlessness, measured using the Chronic Respiratory Disease Questionnaire-Dyspnoea domain (CRQ-D),¹¹ (with a minimal clinically important difference (MCID) of 0.5¹²) and b) change in function using the five-repetition chair to stand test (5RCTS)³(MCID of 1.7 seconds¹³). Additionally, the change in Dyspnoea-12 (D-12),¹⁴ NQ,¹⁵ Borg Scale of Breathlessness (BS),¹⁶ perceived exertion (RPE),¹⁷ breath hold (BH) time,¹⁸ four-metre gait speed (4MGS),¹⁹ Modified Minnesota Physical Activity (PA) Questionnaire,²⁰ Chalder fatigue scale (CFQ)³ and the EuroQual-5 (EQ-5D-5L)³ were collected alongside patient demographics. Outcome data was collected at 7 weeks and again at 14 weeks (Figure 1).

Originally capnography was planned but could not be completed due to limited availability of operators and equipment (when it came to study delivery).

All participants who attended the intervention session in the first phase were invited to complete a brief self-reported survey capturing satisfaction, strengths and weaknesses of the intervention. This consisted of six compulsory satisfaction statements that were rated as 1-5 (where 1=poor, 3=average and 5=excellent) and a further six optional text responses focusing on improvements, modifications required and general feedback.

Safety

Any adverse safety events at assessment or during the intervention were captured and reported in the site file and intervention visit schedule case report form. Mitigations of risk included ensuring participants kept their cameras on throughout the online session so that the practitioner delivering the session could observe any untoward incidents and provide timely feedback if appropriate. Functional measures at assessment were designed to be low-level intensity and therefore acceptable.⁴ Study-stopping rules and discontinuation criteria were monitored for poor recruitment, safety concerns relating to the intervention, lack of resources, or any concerns relating to the feasibility of the study intervention.

Statistical analysis

Per protocol analyses was set out as the primary analyses to gain a better understanding of the effect of the intervention on outcomes, however intention to treat analyses was also undertaken to gain understanding of the effect if used in future practice.

Paired t-test was completed to compare the pre and post treatment at weeks 0 (visit 1) and 7 (visit 2) within each treatment group. The mean differences (post-pre) were reported alongside 95% confidence interval (CI). A t-test was used to determine the difference in mean differences between the usual care and intervention for each of the key outcomes stated above.

Intergroup difference

Cohen’s D was calculated to determine the magnitude of differences between two groups with 95%CI to estimate the precision of mean differences and information regarding statistical significance. The means were interpreted as 0.2 small effect, 0.5 medium effect and 0.8 large effect.²¹

In addition, for those who underwent the intervention originally, the difference from baseline (visit 1), at 14 weeks (visit 3) was also compared using paired t-test to determine if there was any lasting benefit of the intervention.

A sample size of up to n=60 was proposed after discussion across the study team but the protocol recognised the lack of existing information. It was felt that up to 60 people would inform future power calculations of a full RCT. All analysis was performed using StataCorp. (2023) Stata Statistical Software: Release 18. StataCorp LLC. The level of significance was set p<0.05.

Results

Patient characteristics

There were 122 people invited to take part from the clinics and registry, who had dysregulated breathing at the time of their assessment. There were 52 pre-screened and 40 were consented and underwent further eligibility tests (Figure 2). There were 34 randomised but one person did not attend the baseline visit 1 assessment, hence 16 went forward for intervention and 17 to usual care. There were 3 participants lost to both groups following the intervention (Consort diagram, Figure 2). Both intervention and usual care groups had more females than males, but mean age was similar between the groups (Table 1).The participants, predominantly, did not need hospitalisation for the acute COVID-19.

Figure 2.

Consort diagram.

Table 1.

Patient characteristics.

Characteristics	Active intervention	Usual care	Total
Number	16	17	33
Gender
Male	4 (25.0%)	2 (11.8%)	6 (18.2%)
Female	12 (75.0%)	15 (88.2%)	27 (81.8%)
Age (years)	47.3 (12.31)	49.5 (11.56)	48.4 (11.79)
BMI (Kg/m²)	29.9 (6.53)	30.6 (6.38)	30.3 (6.36)
Ethnicity
White/White British	11 (68.8%)	16 (94.1%)	27 (81.8%)
Asian/Asian British	1 (6.2%)	1 (5.9%)	2 (6.1%)
Black/Black British	2 (12.5%)	0 (0.0%)	2 (6.1%)
Mixed Race	1 (6.2%)	0 (0.0%)	1 (3.0%)
Other	1 (6.2%)	0 (0.0%)	1 (3.0%)
Hospitalised with the initial COVID-19
No	14 (87.5%)	17 (100.0%)	31 (93.9%)
Yes	2 (12.5%)	0 (0.0%)	2 (6.1%)
Smoke status
Never smoked	12 (75.0%)	11 (64.7%)	23 (69.7%)
Current smoker	1 (6.2%)	0 (0.0%)	1 (3.0%)
Ex-smoker	3 (18.8%)	6 (35.3%)	9 (27.3%)
Vaping
Never Vaped	15 (93.8%)	16 (94.1%)	31 (93.9%)
Currently Vape	1 (6.2%)	1 (5.9%)	2 (6.1%)
Breath hold (secs)	10.3 (4.64)	11.2 (6.06)	10.7 (5.36)
Breathhold (<30 seconds)	16 (100.0%)	17 (100.0%)	33 (100.0%)
Work-pre COVID
Employed	14 (87.5%)	15 (88.2%)	29 (87.9%)
Self-Employed	1 (6.2%)	2 (11.8%)	3 (9.1%)
Receiving State Support	1 (6.2%)	0 (0.0%)	1 (3.0%)
Back to work
No	2 (13.3%)	6 (35.3%)	8 (25.0%)
Yes - Same hours as before	5 (33.3%)	8 (47.1%)	13 (40.6%)
Yes - But less hours	8 (53.3%)	3 (17.6%)	11 (34.4%)

Feasibility of intervention

Sixteen participants started the intervention, attending a median of 7 sessions [2-11 sessions], of which 5 participants completed >75% attendance of the intervention sessions and the post intervention assessment. No serious adverse events were reported. 4 participants reported intermittent technological difficulties with accessing “DoctorDr” online software.

Per protocol analysis

There were no statistically significant intergroup differences (Table S1). However, at visit 2 clinical improvements in the CRQ-D of 0.71 (95% CI; 0.14, 1.28; p=0.02), and a reduction in the NQ of -2.36 (-5.40, 0.67; p=0.11) were observed in the completers (n=5), but not in the usual care group (n=14) which remained stable or deteriorated (Table S1).

Intention to treat analysis

There were no intergroup statistically significant difference (Table 2). However, as shown in the per-protocol analyses, a clinical improvement was found in CRQ-D scores in the intervention group, with a mean difference of 0.77 (95%CI 0.29, 1.25; p=<0.001) but not in usual care 0.27 (95%CI -0.31, 0.85; p=0.33). Neither group showed an improvement in the 5RCTS 2.48 (95%CI -2.16, 7.11; p=0.26) and 1.69 (95%CI -4.52, 1.15; p=0.22), respectively. The NQ clinically improved with the intervention: -2.69 (95%CI -5.26, -0.12; p=0.04) but not in the usual care -1.60 (95%CI -4.69, 1.49; p=0.29). There was no significant change for dyspnoea (D12), Borg scale, RPE, breath-hold, fatigue, 4MGS, physical activity score or EQ5D for both within or between group analysis.

Table 2.

Mean differences at six weeks for all participants – Intention to Treat.

	Active intervention (n=13)				Usual care (n=14)				Intergroup difference
	Week 0	Week 7	Mean difference (95%CI	p-value	Week 0	Week 7	Mean difference (95%CI	p-value	Mean, (95% CI)
Primary Outcomes
CRQ-D	2.48, (0.72)	3.25 (1.18)	0.77 (0.29, 1.25)	<0.001	2.61, (0.88)	2.89 (1.33)	0.27 (-0.31, 0.85)	0.33	0.55 (-0.26, 1.35)
5RCTS (secs)	14.66 (4.85)	17.14 (9.91)	2.48 (-2.16, 7.11)	0.26	14.94, (7.17)	13.26 (4.92)	1.69 (-4.52, 1.15)	0.22	0.69, (-0.19, 1.56)
Secondary Outcomes
D-12	17.69 (2.51)	17.38 (8.20)	-0.31 (-3.95, 3.33)	0.86	16.67, (7.21)	17.00, (6.64)	0.33 (-2.62, 3.29)	0.81	-0.11 (-0.89, 0.67)
NQ Score	35.38 (13.44)	32.69 (14.40)	-2.69 (-5.26, -0.12)	0.04	35.00, (13.42)	33.4, (11.69)	-1.60 (-4.69, 1.49)	0.29	-0.22 (-1.00, 0.56)
Borg scale of breathlessness	3.92 (2.47)	3.69 (1.97)	-0.23 (-1.92, 1.46)	0.77	3.50, (2.67)	2.57, (1.34)	-0.93 (-2.39, 0.53)	0.19	0.26 (-0.54, 1.06)
Breath holds (secs)	10.81 (5.45)	9.25 (4.75)	-1.56 (-4.90, 1.77)	0.33	7.94, (4.37)	9.90, (3.91)	1.95 (-0.51, 4.41)	0.11	-0.72 (-1.54, 0.10)
4MGS in secs	3.83 (0.73)	4.44 (1.51)	0.61 (0.00-1.22)	0.05	3.66, (1.01)	3.54, (0.72)	-0.12 (-0.51, 0.27)	0.52	0.86 (0.03, 1.69)
Modified Minnesota PA: (mins)	459. 46 (490.74)	558. 38 (808.76)	98.92 (-277.72, 475.57	0.58	393.73, (348.50)	403.87, (356.07)	10.13 (-143.60, 163.86	0.89	0.19 (-0.59, 0.97)
Fatigue	25.62 (5.99)	21.62 (7.34)	-4.00 (-7.37, -0.63)	0.02	26.00, (5.78)	24.00, (6.82)	-2.00 (-4.56, 0.56)	0.12	-0.39 (-1.18, 0.39)
EQ5D	50.38 (18.31)	53.54 (19.18)	3.15 (-5.98, 12.29)	0.00	46.33 (24.16)	54.67 (20.57)	8.33 (-2.53, 19.19)	0.12	-0.29 (-1.08, 0.49)

CRQ-D: Chronic Respiratory Disease Questionnaire – Dyspnoea; 5RCTs: Five Repetition Chair to Stand Test; D12; Dyspnoea 12; NQ Nijmegen score; 4MGS: 4M Gait Speed Test; EQ-5D-5l: EuroQual-5 dimensions version; SD: standard deviation; CI: confidence interval.

Baseline to 14 weeks in the people originally randomised to the Intervention

Only 1 outcome between baseline and 14 weeks demonstrated a significant change in the 13 participants. There was a mean difference in the intervention group of -5.08 (95%CI -8.74 to -1.42) p=0.01 in the NQ score.

Survey

The survey was completed in 13 intervention participants. Statements of satisfaction are shown in Table 3.

Table 3.

Post intervention survey satisfaction results: Median and Interquartile range (IQR).

Question	Median	IQR
The training itself	5	3-5
The group environment for the training	5	4-5
The online nature of training	5	4-5
The “in-person” assessments	5	4-5
The preparation and administration	5	3-5
How Confident to continue on your own	4	3-5

One respondent reported being unconfident to continue the techniques on their own unsupervised.

Strengths of the intervention highlighted that staff were supportive and encouraging, that the group dynamic was supportive and engaging and highlighted the importance of shared experiences with others. Challenges in completing the intervention suggested that greater scheduling flexibility would have increased completion/attendance, and the addition of a video or handbook would help with ongoing continuation/self-management.

Optional participant feedback included reports of feeling improvements in breathing, feeling more relaxed, improved exercise tolerance improved anxiety management. One respondent reported “While doing the sessions I noticed an improvement” while another reflected “During the yoga sessions I felt most in control of my breathing.” Other comments included wishing for earlier access to the intervention, use of mindfulness and benefits of peer support from the group environment. Only one participant commented about fatigue reporting “It felt like exercising again but at a level I could manage without a major flare up in fatigue”. 11 respondents would recommend the intervention to others.

Discussion

We describe how feasible a physiotherapist-led remote, online yogic breathing intervention is for dysregulated breathing causing persistent breathlessness following COVID-19 illness, the vast majority of the patients not requiring hospitalisation for the acute illness. Feasibility of the intervention was challenging in this population, in particular the limited number of symptomatic volunteers by the time the study commenced. There is however useful data gathered that could be utilised if considering a trial across other underlying lung diseases with dysregulated breathing.

The lack of an intervention for the significant number of people experiencing dysregulated breathing and persisting breathlessness after COVID-19 was identified early in 2021. However, the inevitable delays in securing funding, processing regulatory aspects, and starting the intervention led to many people who had struggled for a long time feeling better by the time they were approached for help. Further, the number of people presenting with persisting breathlessness after COVID-19 diminished over time given the success of vaccination programmes. We had set out as a single-site study as it was directly linked to the post-COVID service we offered at that time and in response to local clinical needs.

The outcome measures did not show intergroup statistical significance, however it was not powered and the per-protocol sample size in the intervention group was small. The study was exploratory to determine patient experience of the outcome and whether online breathing sessions could occur. The intervention was well received by those who could attend the sessions but the main barrier to full attendance was inflexibility of session schedules and, occasionally, IT failure. The intervention was informed using pranayama breathing techniques which focused primarily on breathing technique rather than any postural or positional strengthening. This may account for the disparity in clinical signals between measures of breathlessness and function and can be supported by the subjective feedback from participants on the post-intervention survey. The survey highlighted a consensus on feelings of improvement in breathlessness, kinesiophobia, and reduced episodes of panic, while showing little recognition of changes in physical function. There was a mention of improved fatigue management in one reply. Encouragingly, the intervention was well received, and participants liked the group nature and construct of the sessions, with many participants requesting self-directed material for continuation and self-management.

Recent primary care guidance²² highlighted a lack of robust evidence for individuals with dysregulated breathing and persistent breathlessness after COVID-19 and acknowledged a need to develop interventions that improve breathlessness, physical function, and psychosocial wellbeing. This is the first feasibility study to explore the use of yogic breathing interventions in this population. Other interventions have also observed clinical benefits, encompassing broader reasons for breathlessness such as pulmonary rehabilitation^23–25 A remote breathing intervention for people living with dysregulated breathing and persistent breathlessness, whether organic or not, remains a possible intervention for those struggling to attend traditional routes.

There is currently no additional evidence supporting a dedicated breathing intervention for those suffering from persistent breathlessness due to dysregulated breathing following COVID-19 illness. Further, there is a dearth of evidence for any intervention in the management of dysregulated breathing across other chronic respiratory conditions. The data presented in this feasibility study provides insightful indicators that may well be transferable to other populations, such as those with asthma or COPD-related dysregulated breathing. A timely James Lind Alliance publication has identified the 10 research priorities in the management of breathlessness, and self-management for people living with chronic respiratory disease²⁵ and highlights non drug treatments and how best the breathless person can be supported.

Delivery of the intervention was challenging due to staff availability with relevant skills to deliver the intervention. Respiratory physiotherapists have the knowledge and skills to treat breathlessness and therefore proved to be an ideal professional for intervention delivery. Respiratory physiotherapists are however few, and this impacted the scheduling of the sessions. This is an important consideration for any future RCT or clinical implementation. In addition, the timing of the sessions for the participants needs to be considered as only a small percentage were able to attend >75% of the session in the intervention.

A future, fully powered RCT may be of use in understanding the benefits of this intervention across a range of respiratory conditions where individuals present with dysregulated breathing leading to persistent breathlessness. Given the changes and feedback observed in this feasibility study, a measure of breathlessness seems the most appropriate. Implementation factors to be considered include session scheduling preferences of the population, capacity and skill mix of the intervention delivery workforce (inclusive of funding), robust communication strategies including remote infrastructure support, and responsive mechanisms for sustainability and patient safety.

Several factors limited the feasibility of a remote, yogic breathing intervention delivered over six weeks for those with dysregulated breathing following COVID-19 illness. Key limitations were the diminishing number of eligible patients as the COVID-19 pandemic evolved, invitation limitations, and the limited flexibility of yoga sessions.

These preliminary findings, in this select population, highlight the gap in clinical management of people impacted by persistent breathlessness due to dysregulated breathing. Whilst this study amongst people recovering with COVID-19 was not feasible, there remains an opportunity for a future clinical trial of an intervention for people with dysregulated breathing associated with a wider range of lung conditions.

Supplemental material

Supplemental material - Post COVID REspiratory mechanisms and the efficacy of a breathing exercise intervention for DYsregulated breathing (Remedy): A feasibility RCT study

Supplemental material for Post COVID REspiratory mechanisms and the efficacy of a breathing exercise intervention for DYsregulated breathing (Remedy): A feasibility RCT study by Harvey-Dunstan TC, Chikuri S, Kaur J, Porte J, Middleton S, Moffatt F, McKeever TM and Bolton CE in Chronic Respiratory Disease

Footnotes

Acknowledgements

Many thanks to Sabrina Prosper, Liz Simpson, Prof Ian Hall, Aline Nixon and Eleanor Douglas for supporting various aspects of the protocol, development of the intervention or clinical visits.

Ethical considerations

Ethical approval was awarded (22/LO/0642; IRAS 314769) and was prospectively registered on ClinicalTrials.gov: NCT05732571. Informed consent to participate was written and in line with ethical approval.

Author contributions

THD helped develop the protocol, wrote the first draft of paper and assisted in the delivery of the intervention. TMM was overall statistical advisor and with JK led on the statistical analysis. SC recruited, consented and conducted the assessments in the volunteers. She was blinded to the intervention. JK contributed to analysis. SM contributed to the protocol design and running of the study. FM contributed to development and delivery of the intervention. JP contributed to trial management and randomisation of participants. CEB conceived the idea, sought funding and oversaw the overall development of the protocol. CEB is the overall custodian of the study. All authors have reviewed and inputted to the writing of the paper.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by a Charitable Donation to the University of Nottingham; NIHR Nottingham BRC; Senior Investigator Award (IPH). The work was also supported by the NIHR Nottingham Biomedical Research Centre.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. CEB acknowledges grant support to the institution for this work (from a charitable donation), and for other COVID-19 research from Nottingham University Hospitals Charity and UKRI/NIHR. No other author has any conflicts to declare.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author, Professor Charlotte Bolton, upon reasonable request.*

Supplemental material

Supplemental material for this article is available online.

References

Boulding

Stacey

Niven

, et al. Dysfunctional breathing: a review of the literature and proposal for classification. Eur Respir Rev 2016; 25(141): 287–294. https://doi.org/10.1183/16000617.0088-2015

Morgan

. Dysfunctional breathing in asthma: is it common, identifiable and correctable? Thorax 2002; 57(Suppl 2): II31-II35. PMID: 12364708; PMCID: PMC1765996.

Evans

McAuley

Harrison

, et al. Physical, cognitive, and mental health impacts of COVID-19 after hospitalisation (PHOSP-COVID): a UK multicentre, prospective cohort study. The Lancet Respiratory medicine 2021; 9(11): 1275–1287. https://doi.org/10.1016/s2213-2600(21)00383-0

Frésard

Genecand

Altarelli

, et al. Dysfunctional breathing diagnosed by cardiopulmonary exercise testing in ‘long COVID’ patients with persistent dyspnoea. BMJ Open Respir Res 2022; 9(1): e001126. https://doi.org/10.1136/bmjresp-2021-001126

Bradley

. Physiotherapy breathing rehabilitation strategies. In: Chaitlow

LBD

Gilbert

(eds). Multidisciplinary approaches to breathing pattern disorders: Churchill Livingstone, 2002, pp. 173–195.

Jones

Harvey

Marston

, et al. Breathing exercises for dysfunctional breathing/hyperventilation syndrome in adults. Cochrane Database Syst Rev 2013; 5: Cd009041. https://doi.org/10.1002/14651858.CD009041.pub2

Smyth

CME

Winter

Dickinson

. Novel Real-Time OEP Phase Angle Feedback System for Dysfunctional Breathing Pattern Training-An Acute Intervention Study. Sensors (Basel, Switzerland) 2021; 21(11): 3714. https://doi.org/10.3390/s21113714

Bondarenko

Burge

Bremner

, et al. Nonpharmacological Interventions for Dysfunctional Breathing in Adults: A Systematic Review. The Journal of Allergy and Clinical Immunology: In Practice 2025; 13: 2062–2074. https://doi.org/10.1016/j.jaip.2025.04.053

Saoji

Raghavendra

Manjunath

. Effects of yogic breath regulation: A narrative review of scientific evidence. Journal of Ayurveda and integrative medicine 2019; 10(1): 50–58. https://doi.org/10.1016/j.jaim.2017.07.008

10.

Telles

Singh

. A review of the use of yoga in breathing disorders. In: Chaitow

Bradley

Gilbery

(eds). Recognizing and Treating Breathing Disorders: a Multidsiciplinary Approach. 2nd ed: Elsevier, 2014, pp. 275–282.

11.

Williams

Singh

Sewell

, et al. Health status measurement: sensitivity of the self-reported Chronic Respiratory Questionnaire (CRQ-SR) in pulmonary rehabilitation. Thorax 2003; 58(6): 515–518. https://doi.org/10.1136/thorax.58.6.515

12.

Schünemann

Puhan

Goldstein

, et al. Measurement Properties and Interpretability of the Chronic Respiratory Disease Questionnaire (CRQ). COPD: Journal of Chronic Obstructive Pulmonary Disease 2005; 2(1): 81–89. https://doi.org/10.1081/COPD-200050651;05

13.

Jones

Kon

Canavan

, et al. The five-repetition sit-to-stand test as a functional outcome measure in COPD. Thorax 2013; 68(11): 1015–1020. https://doi.org/10.1136/thoraxjnl-2013-203576

14.

Williams

Lewthwaite

Paquet

, et al. Dyspnoea-12 and Multidimensional Dyspnea Profile: Systematic Review of Use and Properties. Journal of Pain and Symptom Management 2022; 63(1): e75–e87. https://doi.org/10.1016/j.jpainsymman.2021.06.023

15.

Grammatopoulou

Skordilis

Georgoudis

, et al. Hyperventilation in asthma: a validation study of the Nijmegen Questionnaire--NQ. The Journal of asthma : official journal of the Association for the Care of Asthma 2014; 51(8): 839–846. https://doi.org/10.3109/02770903.2014.922190

16.

Borg

. Perceived exertion as an indicator of somatic stress. Scandinavian journal of rehabilitation medicine 1970; 2(2): 92–98.

17.

Borg

Ljunggren

Ceci

. The increase of perceived exertion, aches and pain in the legs, heart rate and blood lactate during exercise on a bicycle ergometer. European journal of applied physiology and occupational physiology 1985; 54(4): 343–349. https://doi.org/10.1007/BF02337176

18.

Courtney

Cohen

. Investigating the claims of Konstantin Buteyko, M.D., Ph.D.: the relationship of breath holding time to end tidal CO2 and other proposed measures of dysfunctional breathing. Journal of alternative and complementary medicine (New York, NY) 2008; 14(2): 115–123. https://doi.org/10.1089/acm.2007.7204

19.

Kon

Canavan

Nolan

, et al. The 4-metre gait speed in COPD: responsiveness and minimal clinically important difference. Eur Respir J 2014; 43(5): 1298–1305. Epub 2013 Oct 31. PMID: 24177002.

20.

Richardson

Leon

Jacobs

, et al. Comprehensive evaluation of the Minnesota leisure time physical activity questionnaire. Journal of Clinical Epidemiology 1994; 47(3): 271–281. https://doi.org/10.1016/0895-4356(94)90008-6

21.

Lakens

. Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs. Front Psychol 2013; 4: 863. https://doi.org/10.3389/fpsyg.2013.00863

22.

Evans

Pick

Lardner

, et al. Breathing difficulties after covid-19: a guide for primary care. Breathing difficulties after Covid-19: a guide for primary care BMJ 2023; 381: e074937. https://doi.org/10.1136/bmj-2023-074937

23.

Daynes

Evans

Greening

, et al. Post-Hospitalisation COVID-19 Rehabilitation (PHOSP-R): A randomised controlled trial of exercise-based rehabilitation. Eur Respir J 2025; 65(5): https://doi.org/10.1183/13993003.02152-2024

24.

Fugazzaro

Contri

Esseroukh

, et al. Rehabilitation Interventions for Post-Acute COVID-19 Syndrome: A Systematic Review. Int. J. Environ. Res. Public Health 2022; 19: 5185. https://doi.org/10.3390/.ijerph19095185

25.

Evans

Loa

Reilly

, et al. Top ten research priorities for breathlessness research: UK James Lind Alliance priority setting partnership. The Lancet Respiratory Medicine 2024; 13(Issue 1): e1–e2. https://doi.org/10.1016/S2213-2600(24)00376-X

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