Ventilatory adaptation during eccentric cycling in patients with severe COPD: Potential implications for exercise training

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Highlights

  • Ventilatory adaptation during eccentric exercise in patients with severe COPD is poorly understood.

  • Patients with severe COPD had a more hyperpneic ventilatory pattern during eccentric cycling than during concentric exercise.

  • In addition, they had a lower inspiratory capacity and a poorer ventilatory efficiency during eccentric exercise.

  • Eccentric exercise training should be decided with caution in patients with severe COPD.

Abstract

Introduction

Eccentric (ECC) cycling is viewed as an alternative to concentric (CON) cycling for exercise training in patients with severe COPD as it induces a much lower ventilatory demand for a given mechanical load than CON cycling. However, a more hyperpneic breathing pattern (i.e., higher fB and lower tidal volume (VT)) during ECC than during CON has been reported in healthy subjects.

Research question

Do patients with severe COPD develop a more hyperpneic breathing pattern during ECC than during CON cycling, and is it associated with differences in dynamic hyperinflation, ventilatory efficiency and cardiometabolic adaptation?

Methods

Fourteen patients with severe COPD performed incremental CON and ECC cardiopulmonary exercise tests (CPET). Several physiological parameters including VT, fB, inspiratory capacity (IC) and oxygen consumption (V̇O2) were recorded at each workload increment during CPET.

Results

At the highest identical minute ventilation (V̇E) achieved during ECC and CON (28.6 ± 4.6 L.min−1), VT was lower (1010 ± 218 vs. 1100 ± 233 mL; p = 0.02), fB was higher (29.0 ± 5.1 vs. 27.0 ± 5.5 min−1; p = 0.03), IC(% baseline) was lower (84 ± 10 vs. 78 ± 9; p < 0.01) and markers of ventilatory efficiency were poorer during ECC than during CON. Similar results were found at the highest identical V̇O2 achieved during ECC and CON.

Conclusion

The finding of a more hyperpneic ventilatory pattern during ECC cycling together with a lower IC and a poorer ventilatory efficiency suggests that ECC exercise training should be decided with caution in patients with severe COPD.

Introduction

Pulmonary rehabilitation is considered indispensable in the management of patients with chronic obstructive pulmonary disease (COPD) and provides significant improvements in quality of life and exercise capacity (McCarthy et al., 2015). Exercise training is the main component of pulmonary rehabilitation and usually involves concentric (CON) muscle contractions, typically during walking or cycling (Troosters et al., 2001). Skeletal muscle overload is an important training principle, and patients who develop significant contractile muscle fatigue (CMF) during endurance exercise training are those who are the most likely to improve functional exercise capacity (Burtin et al., 2012). Some COPD patients, especially those with severe airflow obstruction, may however have limited potential to sustain high-intensity load during CON exercise because of a limitation of the ventilatory system (Spruit et al., 2015): in these patients, the tidal volume (VT) may be unable to expand appropriately in response to the metabolic demand during CON muscle contraction because of the occurrence of dynamic hyperinflation (O’Donnell et al., 2001).

Exercise training with eccentric (ECC) muscle contractions has been reliably shown to induce CMF at a lower metabolic cost compared with CON exercise (Perrey et al., 2001; Camillo et al., 2020). ECC exercise training may therefore represent an interesting alternative to CON training in patients who are limited by their respiratory system, i.e., COPD patients with severe airflow obstruction (Camillo et al., 2020; Bourbeau et al., 2020). Nevertheless, this potential might be hampered by the finding that during ECC exercise, healthy subjects developed a more hyperpneic breathing pattern (i.e., lower VT and higher breathing frequency [fB]) for a given minute ventilation than during CON exercise (Lechauve et al., 2014). The breathing pattern during ECC cycling exercise has not been studied in detail, but a hyperpneic pattern may contribute per se to the occurrence of dynamic hyperinflation and to exercise limitation by the ventilatory system in patients with severe COPD. We therefore aimed to study ventilatory adaptations during ECC cycling in patients with severe COPD and to compare these adaptations with those measured during CON exercises.

Section snippets

Trial design

Ventilatory adaptation to concentric (CON) versus eccentric (ECC) exercise in patients with severe COPD (CONVEX trial - NCT03923660) was an investigator-initiated, monocenter, prospective, randomized, cross-over, open-label trial, conducted in the University hospital of Besançon, France, from June 2019 through March 2020.

The study protocol was approved by an ethics committee (Comité de Protection des Personnes Sud Méditerranée P/2018/374) according to French law.

Participants

Patients with severe COPD

Subject characteristics

Among the sixteen patients included, fourteen completed the study (Fig. 1). One patient withdrew after the initial assessment because of a musculoskeletal problem secondary to the familiarization session and one patient due to medical reasons unrelated to the study.

Subject characteristics are summarized in Table 1, Table 2. Among the fourteen patients who completed the study, four had a FEV1 below 30 % of predicted value. All had lung hyperinflation at rest (functional residual capacity [FRC]

Discussion

The main finding of this prospective randomized study was that in patients with severe COPD, ventilatory adaptation during cycling exercise performed in a semi-recumbent position was different between the ECC and CON exercise modalities: for a given minute ventilation (V̇E), breathing frequency (fB) was higher, tidal volume (VT) was lower, inspiratory capacity (IC) was lower and markers of ventilatory efficiency were poorer during ECC than during CON. In addition, electromyographic recruitment

Conclusion

Even if ECC exercise is considered a promising and feasible exercise modality in patients with severe COPD, we observed that ECC cycling induces a more hyperpnoeic breathing pattern, a more severe decrease in inspiratory capacity and more pronounced ventilatory inefficiency than CON cycling in these patients. We therefore suggest that ECC exercise training for severe COPD patients should be decided with caution. Whether or not the observed ventilatory pattern has an impact on the use and the

Author contributions

B.D. conceived and designed the study; O.N and O.R performed the experiments; T.S. and O.N. analyzed data; O.N., Y.S., B.D. and T.S. interpreted the results of experiments; T.S. prepared figures; O.N and T.S. drafted the manuscript; O.R. and B.D. edited and revised the manuscript; All authors approved final version of manuscript.

Funding

This study was supported by a grant from the associations Le Nouveau Souffle and Don du Souffle.

Declaration of Competing Interest

The authors declare that they have no conflict of interest for the submitted work.

Acknowledgements

We express our appreciation to the patients who participated in the study. We also thank the clinical staff who contributed to the measurements. We are indebted to Dr. Pierre Decavele for valuable support. We thank Dr. Alison Foote (Grenoble Alpes University Hospital) for critically editing the manuscript.

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    These authors contributed equally to the work.

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