Protective effect of heart rate variability biofeedback on stress-induced lung function impairment in asthma

https://doi.org/10.1016/j.resp.2019.01.011Get rights and content

Highlights

  • Stress decreased the spirometry performance in asthmatic patients.

  • HRV-BF had a protective effect on stress-induced airway constriction.

  • HRV-BF modulated heart rate dynamics in asthmatic patients.

Abstract

Psychological stress can provoke airway constriction in asthmatic patients, which may be because of autonomic nervous system dysfunction in asthma. We investigated the effect of enhancing respiratory sinus arrhythmia using heart rate variability biofeedback (HRV-BF) on spirometry performance and HRV indices during stress induced by Stroop Color-Word interference test in asthmatic patients and healthy volunteers. Stress caused decrease in FEV1%, FVC%, and PEF% compared to baseline in asthmatic patients, but not in healthy subjects. A single short duration episode of HRV-BF not only had a protective effect on stress-induced airway constriction, but also significantly augmented the level of FEV1% and FVC% as compared with their own baseline. Also, there was a significant correlation between HRV changes and the augmentation of spirometry performance in asthmatic patients receiving HRV-BF. Our findings indicated that even a single short duration episode of HRV-BF can decrease susceptibility to stress-induced lung function impairment in patients with asthma, which may be through the modulation of respiratory sinus arrhythmia.

Introduction

Asthma is one of the most common chronic disorders in the world, characterized by reversible airway obstruction and heightened airway reactivity (Global Initiative For Asthma (GINA), 2017). Although asthma can be commonly affected by allergens, exercise, and infection, growing numbers of evidence suggest an association between psychological stress and the aggravation of asthma symptoms, more frequent exacerbations, and increased use of emergency and general health services (Lavoie et al., 2005; Martínez-Moragón et al., 2003; Ten Brinke et al., 2001). Psychological stress can provoke airway constriction in asthmatic patients. For instance, experimental stress induction is associated with a reduction in forced expiratory volume in 1 s (FEV1) and respiratory resistance in patients with asthma compared to healthy controls (Janssens et al., 2017; Kullowatz et al., 2008; Rietveld and van Beest, 2007; Ritz et al., 2012). In addition, sustained stress-induced airway constriction may make patients susceptible to experiencing more asthma attacks in their daily lives (Ritz et al., 2012). There is evidence indicating that exacerbation occurs in 20–35% of asthmatic patients during periods of stress (Isenberg et al., 1992) and 10–15% of the asthma exacerbation is caused by psychological stress (Koyanagi et al., 2009).

Chronic stressors lead to the releasing of stress hormones such as catecholamines and cortisol by activating the sympathetic–adrenal–medullary axis (SAM) and hypothalamus-pituitary-adrenal (HPA) axis respectively, which may be related to the subsequent exacerbation in asthma (Kullowatz et al., 2008). Moreover, long-term stress could elevate T-helper2 cells, which may cause airway inflammation and exacerbated asthma (Kullowatz et al., 2008). However, these processes are activated by long-term stress and the underlying mechanism of short-term stress-induced airway constriction is not clear.

There is evidence that an autonomic imbalance in asthma might be an important contributing factor for these exacerbations (Isenberg et al., 1992; Lehrer et al., 2002). It has been suggested that psychological stress influences asthma by altering the activity of the autonomic nervous system (ANS). Pharmacological blockade of airway cholinergic receptors significantly attenuates emotion-induced airway constriction (Ritz et al., 2010). Additionally, increase in high-frequency heart rate variability, which is suggestive of vagal activity, is associated with greater airway resistance measured after the presentation of a distressing film (Miller et al., 2009). Moreover, increased stress activates the HPA axis and the sympathetic nervous system, possibly leading to immune-regulatory changes such as the production of cytokine type 2 (Kullowatz et al., 2008). Organs of the immune system are innervated by sympathetic postganglionic neurons that express adrenergic receptor subtypes. Norepinephrine regulates immune cell activity through these adrenergic receptors (Kullowatz et al., 2008). It appears that stress-induced airway constriction has been observed to be more pronounced in patients with asthma compared to healthy subjects (Ritz et al., 2012), because of ANS dysfunction in asthma (Garcia-Araújo et al., 2015; Garrard et al., 1992; Souza et al., 2010). Therefore, improving ANS activity may be a protective strategy against stress-induced asthma attack.

Heart rate variability biofeedback (HRV-BF) is a behavioral method that causes subjects to breath approximately 6 times per minute (˜0.1 Hz) in order to maximize respiratory sinus arrhythmia (RSA), which reflects vagus nerve function (Lehrer et al., 2013, 2003; Vaschillo et al., 2006, 2002). This approach has been used to modulate vagal and sympathetic modulation in a variety of clinical disorders, such as anxiety and hypertension (Lehrer et al., 2003). There are reports indicating that HRV-BF has clinically significant effects on pulmonary function and asthma symptoms. Asthmatic patients receiving long-term HRV-BF as a complementary treatment have displayed improved spirometry performance and respiratory resistance, as well as a decrease in the frequency of exacerbations, while receiving a lower dose of asthma medications (Lehrer et al., 2004, 2018; Lehrer et al., 2000a,b). However, no study has investigated the effect of HRV-BF on emotion-induced airway constriction in asthma so far.

Taken together, since autonomic imbalance is considered as an important contributing factor in airway constriction during psychological stress and that previous reports have demonstrated that even a single short duration episode of HRV-BF (Prinsloo et al., 2013) can improve autonomic reactivity, we hypothesized that HRV-BF may modulate RSA and decrease susceptibility to stress-induced lung function impairment in patients with asthma. To examine this hypothesis, we aimed to investigate the effect of a single HRV-BF on HRV indices during stress induction using the Stroop Color-Word interference test, and on spirometry performance in the immediate post-stress period in asthmatic patients and healthy volunteers.

Section snippets

Participants

Forty four age-matched women, including 22 healthy volunteers and 22 asthmatic patients, 20–35 years of age with disease duration of 8–15 years, referred to the outpatient clinic of Masih Daneshvari Lung Hospital (Tehran, Iran), were enrolled in this study. Asthma was diagnosed by pulmonologists based on clinical symptoms and pulmonary function. All patients in this study had atopic mild asthma as indicated by an FEV1 between 60 and 85% of predicted values (National Asthma Education and

Baseline characteristics

General characteristics, baseline spirometry parameters, and HRV indices in healthy and asthmatic subjects have been depicted in Table 1. There were no significant differences in age, BMI, menstrual cycle, stress level, SpO2, and respiratory rate among groups. Evaluation of the lung function revealed that asthmatic patients exhibit significantly lower FEV1% (p = 0.045), FEV1/FVC% (p = 0.002), and PEF% (p = 0.005) compared to healthy subjects. Group comparison of HRV showed higher values of HR

Discussion

In the present study, stress induced by Stroop test decreased FEV1%, FVC%, and PEF% compared to baseline in asthmatic patients, but not in healthy subjects. A single short duration episode of HRV-BF not only had a protective effect on stress-induced alteration of lung function, but also significantly augmented the level of FEV1% and FVC% as compared with baseline. Moreover, patients with asthma showed deterioration in the HRV indices during the baseline period. Stress significantly affected HRV

Funding

This study was supported by grants from Tarbiat Modares University to Niloofar Taghizadeh.

References (51)

  • J.P. Delaney et al.

    Effects of short-term psychological stress on the time and frequency domains of heart-rate variability

    Percept. Mot. Skills

    (2000)
  • G. Ernst

    Heart-Rate Variability-More than Heart Beats?

    Front. Public Health

    (2017)
  • A.S. Garcia-Araújo et al.

    Increased sympathetic modulation and decreased response of the heart rate variability in controlled asthma

    J. Asthma

    (2015)
  • C.S. Garrard et al.

    Spectral analysis of heart rate variability in bronchial asthma

    Clin. Auton. Res.

    (1992)
  • P. Gayrard et al.

    Mechanisms of the bronchoconstrictor effects of deep inspiration in asthmatic patients

    Thorax

    (1979)
  • A.G. Gift

    Visual analogue scales: measurement of subjective phenomena

    Nurs. Res.

    (1989)
  • Global Initiative For Asthma (GINA)

    Global Strategy For Asthma Management and Prevention. Global Initiative for Asthma

    (2017)
  • D.S. Goldstein et al.

    Low-frequency power of heart rate variability is not a measure of cardiac sympathetic tone but may be a measure of modulation of cardiac autonomic outflows by baroreflexes

    Exp. Physiol.

    (2011)
  • S.A. Isenberg et al.

    The effects of suggestion and emotional arousal on pulmonary function in asthma: a review and a hypothesis regarding vagal mediation

    Psychosom. Med.

    (1992)
  • A. Kullowatz et al.

    Stress effects on lung function in asthma are mediated by changes in airway inflammation

    Psychosom. Med.

    (2008)
  • P.M. Lehrer et al.

    Respiratory sinus arrhythmia versus neck/trapezius EMG and incentive inspirometry biofeedback for asthma: a pilot study

    Appl. Psychophysiol. Biofeedback

    (1997)
  • P.M. Lehrer et al.

    Resonant frequency biofeedback training to increase cardiac variability: rationale and manual for training

    Appl. Psychophysiol. Biofeedback

    (2000)
  • P. Lehrer et al.

    Respiratory sinus arrhythmia biofeedback therapy for asthma: A report of 20 unmedicated pediatric cases using the Smetankin method

    Appl. Psychophysiol. Biofeedback

    (2000)
  • P. Lehrer et al.

    Psychological aspects of asthma

    J. Consult. Clin. Psychol.

    (2002)
  • P.M. Lehrer et al.

    Heart rate variability biofeedback increases baroreflex gain and peak expiratory flow

    Psychosom. Med.

    (2003)
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