Proprioceptive changes impair balance control in individuals with chronic obstructive pulmonary disease

Lotte Janssens, Simon Brumagne, Alison K McConnell, Kurt Claeys, Madelon Pijnenburg, Chris Burtin, Wim Janssens, Marc Decramer, Thierry Troosters, Lotte Janssens, Simon Brumagne, Alison K McConnell, Kurt Claeys, Madelon Pijnenburg, Chris Burtin, Wim Janssens, Marc Decramer, Thierry Troosters

Abstract

Introduction: Balance deficits are identified as important risk factors for falling in individuals with chronic obstructive pulmonary disease (COPD). However, the specific use of proprioception, which is of primary importance during balance control, has not been studied in individuals with COPD. The objective was to determine the specific proprioceptive control strategy during postural balance in individuals with COPD and healthy controls, and to assess whether this was related to inspiratory muscle weakness.

Methods: Center of pressure displacement was determined in 20 individuals with COPD and 20 age/gender-matched controls during upright stance on an unstable support surface without vision. Ankle and back muscle vibration were applied to evaluate the relative contribution of different proprioceptive signals used in postural control.

Results: Individuals with COPD showed an increased anterior-posterior body sway during upright stance (p = 0.037). Compared to controls, individuals with COPD showed an increased posterior body sway during ankle muscle vibration (p = 0.047), decreased anterior body sway during back muscle vibration (p = 0.025), and increased posterior body sway during simultaneous ankle-muscle vibration (p = 0.002). Individuals with COPD with the weakest inspiratory muscles showed the greatest reliance on ankle muscle input when compared to the stronger individuals with COPD (p = 0.037).

Conclusions: Individuals with COPD, especially those with inspiratory muscle weakness, increased their reliance on ankle muscle proprioceptive signals and decreased their reliance on back muscle proprioceptive signals during balance control, resulting in a decreased postural stability compared to healthy controls. These proprioceptive changes may be due to an impaired postural contribution of the inspiratory muscles to trunk stability. Further research is required to determine whether interventions such as proprioceptive training and inspiratory muscle training improve postural balance and reduce the fall risk in individuals with COPD.

Conflict of interest statement

Competing Interests: AKM acknowledges a beneficial interest in an inspiratory muscle training product (POWERbreathe International Ltd.) in the form of a share of license income to the University of Birmingham and Brunel University. She also acts as a consultant to POWERbreathe International Ltd. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. LJ, SB, KC, MP, CB, WJ, MD and TT declare that they have no competing interests.

Figures

Figure 1. Experimental set-up.
Figure 1. Experimental set-up.
Standing on unstable support surface on force plate with ankle and back muscles vibration and vision occlusion.
Figure 2. Postural stability.
Figure 2. Postural stability.
Raw data of center of pressure (CoP) displacement of an individual with COPD and an age/gender-matched healthy individual while standing on unstable support surface without vision for 30 seconds. Positive values indicate an anterior body sway, negative values indicate a posterior body sway.
Figure 3. Proprioceptive control strategy.
Figure 3. Proprioceptive control strategy.
Center of pressure displacement (mean ± SD) in the control group (black) and COPD group (white) during vibration on ankle muscles, back muscles, and simultaneously on ankle and back muscles. Positive values indicate an anterior body sway, negative values indicate a posterior body sway.
Figure 4. Relative proprioceptive weighting.
Figure 4. Relative proprioceptive weighting.
Individual (left) and mean ± SD (right) relative proprioceptive weighting (RPW) ratios in the COPD group (white) and age/gender-matched control group (black). Higher values correspond to higher reliance on ankle muscle proprioception; lower values correspond to higher reliance on back muscle proprioception.

References

    1. Lawlor DA, Patel R, Ebrahim S (2003) Association between falls in elderly women and chronic diseases and drug use: cross sectional study. BMJ 327: 712–717.
    1. Roig M, Eng JJ, MacIntyre DL, Road JD, FitzGerald JM, et al. (2011) Falls in people with chronic obstructive pulmonary disease: an observational cohort study. Respir Med 105: 461–469.
    1. Lehouck A, Boonen S, Decramer M, Janssens W (2011) COPD, bone metabolism, and osteoporosis. Chest 139: 648–657.
    1. Bischoff-Ferrari HA, Conzelmann M, Stähelin HB, Carpenter MG, Adkin AL, et al. (2006) Is fall prevention by vitamin D mediated by a change in postural or dynamic balance? Osteoporos Int 17: 656–663.
    1. Roig M, Eng JJ, Road JD, Reid WD (2009) Falls in patients with chronic obstructive pulmonary disease: a call for further research. Respir Med 103: 1257–1269.
    1. Beauchamp MK, Hill K, Goldstein RS, Janaudis-Ferreira T, Brooks D (2009) Impairments in balance discriminate fallers from non-fallers in COPD. Respir Med 103: 1885–1891.
    1. Lackner JR, DiZio P (2005) Vestibular, proprioceptive, and haptic contributions to spatial orientation. Annu Rev Pshychol 56: 115–147.
    1. El-Kady MA, Durrant JD, Tawfik S, Abdel-Ghany S, Moussa AM (2006) Study of auditory function in patients with chronic obstructive pulmonary diseases. Hear Res 212: 109–116.
    1. Allum JH, Bloem BR, Carpenter MG, Hulliger M, Hadders-Algra M (1998) Proprioceptive control of posture: a review of new concepts. Gait Posture 8: 214–242.
    1. Brumagne S, Janssens L, Janssens E, Goddyn L (2008) Altered postural control in anticipation of postural instability in persons with recurrent low back pain. Gait Posture 28: 657–662.
    1. Kiers H, Brumagne S, van Dieën J, van der Wees P, Vanhees L (2012) Ankle proprioception is not targeted by exercises on an unstable surface. Eur J Appl Physiol 112: 1577–1585.
    1. Hodges PW, Gandevia SC (2000) Activation of the human diaphragm during a repetitive postural task. J Physiol 522: 165–175.
    1. Butcher SJ, Meshke JM, Sheppard MS (2004) Reductions in functional balance, coordination, and mobility measures among patients with stable chronic obstructive pulmonary disease. J Cardiopulm Rehabil 24: 274–280.
    1. Chang AT, Seale H, Walsh J, Brauer SG (2008) Static balance is affected following an exercise task in chronic obstructive pulmonary disease. J Cardiopulm Rehabil Prev 28: 142–145.
    1. Smith MD, Chang AT, Seale HE, Walsh JR, Hodges PW (2010) Balance is impaired in people with chronic obstructive pulmonary disease. Gait Posture 31: 456–460.
    1. Eisner MD, Blanc PD, Yelin EH, Sidney S, Katz PP, et al. (2008) COPD as a systemic disease: impact on physical functional limitations. Am J Med 121: 789–796.
    1. Beauchamp MK, Sibley KM, Lakhani B, Romano J, Mathur S, et al. (2012) Impairments in Systems Underlying Control of Balance in COPD. Chest 141: 1496–1503.
    1. Gosselink R, Troosters T, Decramer M (1996) Peripheral muscle weakness contributes to exercise limitation in COPD. Am J Respir Crit Care Med 153: 976–980.
    1. Baecke JA, Burema J, Frijters JE (1982) A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 36: 936–942.
    1. Rochester DF, Arora NS (1983) Respiratory muscle failure. Med Clin North Am 67: 573–597.
    1. Roll JP, Vedel JP (1982) Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res 47: 177–190.
    1. Cordo PJ, Gurfinkel VS, Brumagne S, Flores-Vieira C (2005) Effect of slow, small movement on the vibration-evoked kinesthetic illusion. Exp Brain Res 167: 324–333.
    1. Janssens L, Brumagne S, Polspoel K, Troosters T, McConnell A (2010) The effect of inspiratory muscles fatigue on postural control in people with and without recurrent low back pain. Spine 35: 1088–1094.
    1. Global strategy for diagnosis, management, and prevention of COPD. Available: . Assessed 30 November 2012.
    1. Hall LM, Brauer S, Horak F, Hodges PW (2010) Adaptive changes in anticipatory postural adjustments with novel and familiar postural supports. J Neurophysiol 103: 968–976.
    1. David P, Laval D, Terrien J, Petitjean M (2011) Postural control and ventilatory drive during voluntary hyperventilation and carbon dioxide rebreathing. Eur J Appl Physiol 112: 145–154.
    1. Hamaoui A, Gonneau E, Le Bozec S (2010) Respiratory disturbance to posture varies according to the respiratory mode. Neurosci Lett 475: 141–144.
    1. Hodges PW, Gurfinkel VS, Brumagne S, Smith TC, Cordo PC (2002) Coexistence of stability and mobility in postural control: evidence from postural compensation for respiration. Exp Brain Res 144: 293–302.
    1. Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Green M, et al. (1996) Diaphragm strength in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 154: 1310–1317.
    1. Engel R, Vemulpad S (2011) The role of spinal manipulation, soft-tissue therapy, and exercise in chronic obstructive pulmonary disease: a review of the literature and proposal of an anatomical explanation. J Altern Complement Med 17: 797–801.
    1. Kantor E, Poupard L, Le Bozec S, Bouisset S (2001) Does body stability depend on postural chain mobility or stability area? Neurosci Lett 308: 128–132.
    1. Kuznetsov NA, Riley MA (2012) Effects of breathing on multijoint control of center of mass position during upright stance. J Mot Behav 44: 241–253.

Source: PubMed

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