Airflow limitation in asthmatic children assessed with a non-invasive EMG technique

doi:10.1016/S1569-9048(02)00130-1

Respiratory Physiology & Neurobiology

Volume 133, Issues 1–2, 23 October 2002, Pages 89-97

https://doi.org/10.1016/S1569-9048(02)00130-1 Get rights and content

Abstract

The aim of the study was to investigate the association between electromyography (EMG) of the diaphragm and intercostal muscles and the forced expiratory volume in 1 s (FEV₁) at different levels of histamine-induced airflow limitation, and the response to salbutamol. Moreover, we assessed the reproducibility of the EMG measurements on 2 different occasions during different levels of airflow limitation in asthmatic school children. Fourteen children with asthma performed 2 histamine challenges with a 24-h time interval and 1 child performed 1 histamine challenge. The EMG signals were derived from surface electrodes. The logarithm of the EMG-activity-ratio (log EMGAR; mean peak–bottom ratio of respiratory muscle activity) was used as EMG parameter. The log EMGAR of the diaphragm (di) and the log EMGAR of the intercostal muscles (int) associated well with the histamine-induced fall in FEV₁ at 5% steps from the baseline value. After administration of salbutamol log EMGARdi and log EMGARint returned to baseline mean peak–bottom values (for all leads P<0.001). The EMGARdi and EMGARint values were reproducible at different levels of airflow limitation. This study showed that EMGARdi and EMGARint as a parameter for a change in electrical activity of the diaphragm and intercostal muscles associated well with FEV₁, was reversible after salbutamol and was reproducible at different levels of histamine-induced airflow limitation in asthmatic school children.

Introduction

The measurement of lung function is important in clinical decision making on asthma. Lung function may provide essential information on the natural history and response to treatment (Bouchez-Buvry, 1997, Haahtela et al., 1994). Additionally, early recognition of airflow limitation and airway responsiveness in the course of asthma could provide a good opportunity for early intervention (Grol et al., 1999, Sears, 2000). Since spirometric tests require active co-operation for forced expiratory manoeuvres (FEV₁), this type of test is limited to older children (ATS, 1995). Children under 6 years and less co-operative children are generally not able to perform reproducible forced expiratory manoeuvres, making the assessment of airflow limitation in this age group difficult.

A non-invasive technique based on electromyographic (EMG) measurements of the diaphragm (di) and intercostal muscles (int) has been developed by our group for monitoring disordered respiratory behaviour in neonates and infants (Prechtl et al., 1977, O'Brien et al., 1987, Sprikkelman et al., 1998, Maarsingh et al., 2000). We investigated in a pilot study whether this method could be used for assessing bronchoconstriction responses (Sprikkelman et al., 1998). Although, surface diaphragmatic and intercostal EMG values had a close inverse relationship to a maximum fall in FEV₁ during a histamine challenge in asthmatic school children, the association with FEV₁ at different levels of airflow limitation and response to treatment is still unknown. In another study, we reported that respiratory EMG measurements appeared to be reproducible during quiet breathing in children and adults without airflow limitation (Maarsingh et al., 2000).

In the present study we investigated in asthmatic school in children: (1) the association between diaphragmatic and intercostal EMG and the FEV₁ at different levels of histamine-induced airflow limitation, (2) the response of the EMG activity after administration of salbutamol, and (3) the reproducibility of the diaphragmatic and intercostal EMG at different levels of airflow limitation.

Section snippets

Study subjects

Fifteen children (11 males, aged 10.8±3.2 years) with mild to moderate asthma participated in the study. All children attended the outpatient clinic of the Emma Children's Hospital, University Hospital of Amsterdam, The Netherlands. The children were diagnosed as having asthma according to the International Consensus Report on Diagnosis and Management of Asthma (Kay and Holgate, 1992). Children with lung diseases other than asthma, or those who were not able to perform reproducible spirometric

Results

At baseline, all children had normal lung function values on test day 1 (FEV₁=99.8±15.7% predicted, FEV₁/VC=82±10% predicted) and test day 2 (FEV₁=102.1±13.5% predicted, FEV₁/VC=83±9% predicted). Fourteen out of 15 children performed 2 histamine challenges with a time interval of 24 h, and one child performed 1 histamine challenge. The FEV₁ decreased by 20% or more in 13 children after histamine challenge on both test occasions. One child had a maximum fall in FEV₁ of 15 and 14% at the highest

Discussion

We found a good inverse association between the diaphragmatic and intercostal EMGAR values and the fall in FEV₁ in 5% steps during histamine challenge in asthmatic school children. After administration of salbutamol the EMGAR values of all leads returned significantly to baseline values and appeared to be reproducible at different levels of airflow limitation on the different measurement days.

In contrast to an earlier study (Sprikkelman et al., 1998) in which we found in asthmatic children that

Acknowledgements

This project was supported by the Netherlands Asthma Foundation (NAF project no. 3.2.97.14) and ‘Stichting Astma Bestrijding’. The authors are grateful to S.J.A. Latif-Lone for assistance in lung function testing and histamine challenging, and thank D.J. van Hoogstraten for editorial advice.

References (25)

H.F.R. Prechtl et al.
Respiratory muscle EMG in newborns: a non-intrusive method
Early Hum. Dev.
(1977)
M.R. Sears
Consequences of long-term inflammation. The natural history of asthma
Clin. Chest Med.
(2000)
Standardization of spirometry, 1994 update
Am. J. Respir. Crit. Care Med.
(1995)
A. Bouchez-Buvry
Clinical indications for lung function tests in infants, children and adolescents
Pediatr. Pulmonol.
(1997)
J.E. Butler et al.
Impaired reflex responses to airway occlusion in the inspiratory muscles of asthmatic subjects
Thorax
(1996)
A. De Troyer et al.
Neural drive to the diaphragm in patients with severe COPD
Am. J. Respir. Crit. Care Med.
(1997)
R.A. Deyo et al.
Reproducibility and responsiveness of health status measures
Control Clin. Trials
(1991)
M. Gorini et al.
Changes in neural drive (EMGd) and neuromuscular coupling during histamine-induced bronchoconstriction in patients with asthma
Eur. Respir. J.
(1988)
M.H. Grol et al.
Risk factors for growth and decline of lung function in asthmatic individuals up to age 42 years. A 30-year follow-up study
Am. J. Respir. Crit. Care Med.
(1999)
T. Haahtela et al.
Effects of reducing or discontinuing inhaled budenoside in patients with mild asthma
N. Engl. J. Med.
(1994)

A.B. Kay et al.

International consensus report on diagnosis and management of asthma

Clin. Exp. All.

(1992)

E.J.W. Maarsingh et al.

Respiratory muscle activity measured with a noninvasive EMG technique: technical aspects and reproducibility

J. Appl. Physiol.

(2000)

Cited by (21)

Identifying bronchoconstriction from the ratio of diaphragm EMG to tidal volume
2021, Respiratory Physiology and Neurobiology
Citation Excerpt :
This technique may therefore be useful in the diagnosis of asthma in patients unable to perform an FEV1 maneuver properly. This is the first study to use the EMGdi-c/VT technique to detect the changes in airway obstruction elicited by histamine challenge test and subsequent bronchodilator although EMGdi-c alone has been studied (Maarsingh et al., 2002, 2004; Sprikkelman et al., 1998). Alternative methods to indirectly assess resistance include the forced oscillation technique (FOT); however, FOT has had limited clinical acceptance probably because of difficulty in data interpretation including inaccuracy and unreliability in assessment of airway resistance (Shirai and Kurosawa, 2016; Smith et al., 2005; Wesseling et al., 1993).
A fall of ≥ 20 % in forced expiratory volume in the first second (FEV1) with a cumulative dose of histamine ≤ 7.8 μmol is considered to indicate bronchial hyperactivity, but no method exists for patients who cannot perform spirometry properly. Here we hypothesized that increases in respiratory central output measured by chest wall electromyography of the diaphragm (EMGdi-c) expressed as a function of tidal volume (EMGdi-c/VT) would have discriminative power to detect a ‘positive’ challenge test.
In a physiological study EMGdi was recorded from esophageal electrode (EMGdi-e) in 16 asthma patients and 16 healthy subjects during a histamine challenge test. In a second study, EMGdi from chest wall surface electrodes (EMGdi-c) was measured during a histamine challenge in 44 asthma patients and 51 healthy subjects. VT was recorded from a digital flowmeter during both studies.
With histamine challenge test the change in EMGdi-e/VT in patients with asthma was significantly higher than that in healthy subjects (104.2 % ± 48.6 % vs 0.03 % ± 17.1 %, p < 0.001). Similarly there was a significant difference in the change of EMGdi-c/VT between patients with asthma and healthy subjects (90.5 % ± 75.5 % vs 2.4 % ± 21.7 %, p < 0.001). At the optimal cut-off point (29 % increase in EMGdi-c/VT), the area under the ROC curve (AUC) for detection of a positive test was 0.91 (p < 0.001) with sensitivity 86 % and specificity 92 %.
We conclude that EMGdi-c/VT may be used as an alternative for the assessment of bronchial hypersensitivity and airway reversibility to differentiate patients with asthma from healthy subjects.
Second intercostal space electromyography as a measure of neural respiratory drive: Clinical utility and validity
2021, Respiratory Physiology and Neurobiology
Respiratory load perception in overweight and asthmatic children
2017, Respiratory Physiology and Neurobiology
Citation Excerpt :
To eliminate the confounding influence of changing tidal volumes on EMGpara values, EMGpara was expressed relative to the tidal volume for each breath, described as neuroventilatory efficiency (NVE) with units ml/kgPBW/μV. NVE at each resistive load was expressed as a ratio of that at baseline (NVE activity ratio (NVEAR)), similar to the method described by Maarsingh et al. (2002). Baseline recordings of EMGpara, respiratory flow, tidal volume and mouth pressure were recorded for a period of five minutes with the subject seated comfortably in a supportive chair with arms relaxed.
Overweight asthmatic children report greater symptoms than normal weight asthmatics, despite comparable airflow obstruction. This has been widely assumed to be due to heightened perception of respiratory effort.
Three groups of children (healthy weight controls, healthy weight asthmatics, overweight asthmatics) rated perceived respiratory effort throughout an inspiratory resistive loading protocol. Parasternal intercostal electromyogram was used as an objective marker of respiratory load; this was expressed relative to tidal volume and reported as a ratio of the baseline value (neuroventilatory activity ratio (NVEAR)).
Significant increases in perception scores (p < 0.0001), and decreases in NVEAR (p < 0.0001) were observed from lowest to highest resistive load. Higher BMI increased overall perception scores, with no influence of asthma or BMI-for-age percentile on the resistance-perception relationships.
These data, indicating elevated overall respiratory effort in overweight asthmatic children but comparable responses to dynamic changes in load, suggest that the greater disease burden in overweight asthmatic children may be due to altered respiratory mechanics associated with increased body mass.
Electromyographic monitoring of respiratory muscle activity in dyspneic infants and toddlers
2006, Respiratory Physiology and Neurobiology
The aim of this study was to investigate whether the changes that occurred in the clinical asthma score (CAS) correlated with the changes in the respiratory electromyographic (EMG) activity over the days during admission to hospital in dyspneic infants and toddlers. Sixteen infants and toddlers (9 males) were studied during admission and 7 days after discharge. The CAS was used to assess the severity of dyspnea and consists of five items: respiration rate, wheezing, retractions, observed dyspnea, and inspiration-to-expiration ratio. Each item was scaled 0, 1, or 2, with a maximum score of 10. Electrical activity from the diaphragm (di) and intercostal muscles (int) was derived from surface electrodes. The logarithm of the EMG-Activity-Ratio (log EMGAR; ratio of mean peak-to-bottom EMG activity during admission to the hospital, to that at baseline, 7 days after discharge) was used as EMG parameter. For assessing the association between the repeated observations of the CAS and the EMG measurements we used the quantity r² obtained with analysis of covariance. On the day of admission the patients had a mean CAS of 5.9 ± 1.2. On the day of discharge the mean CAS decreased significantly to 2.1 ± 1.6, indicating that the CAS returned to normal values. In line with this observation, a significant decrease in the log EMGARdi and log EMGARint was observed during the stay in the hospital. Over all subjects the correlation coefficient (r) of log EMGARdi versus CAS was 0.71, log EMGARint versus CAS was 0.67, and the mean log EMGAR versus CAS was 0.75 (p < 0.01, for all values). The correlation coefficients of subjects of ≤1 year seemed to be lower than those of subjects of >1 year of age (p < 0.01) and female subjects showed higher correlation coefficients than males. This study showed a moderate, but significant, relationship between the changes that occurred in the CAS and the changes in respiratory EMG activity during admission to hospital in dyspneic infants and toddlers. Moreover, the correlation coefficients of the combined leads of the intercostals and diaphragm (mean log EMGAR) were higher than those of the separate leads. The EMG measurements would extend diagnostic possibilities and would provide an objective measure to evaluate the clinical course of the disease and the efficacy of therapy in infants and toddlers with recurrent wheezing disorders.
Clinical Neurophysiology of the Motor Unit in Infants and Children
2006, Clinical Neurophysiology of Infancy, Childhood, and Adolescence
Different breathing patterns in healthy and asthmatic children: Responses to an arithmetic task
2006, Respiratory Medicine
Asthma patients have been reported to be sensitive to breathlessness, independent of the degree of airway obstruction. Paying attention and task performance may induce changes in breathing pattern and these in turn may mediate such a feeling. The present experiment investigates whether strained breathing induced by an arithmetic task was different in children with asthma compared to healthy children.
Seven healthy and eight asthmatic but symptom-free school children were equipped with electrodes for surface electromyographic (EMG) measurements of diaphragm, abdominal and intercostal (IC) muscles and with a strain gauge to monitor the pattern of breathing at rest and during an arithmetic task. The relative duration of exhalation and the relative speed of exhalation are used as measures of straining. The phase angle of maximal respiratory muscle activities relative to the maximal chest extension (MCE) are additional discriminating parameters.
Asthmatic children breathed more slowly and already at rest the phase of their respiratory muscle activity appears to be different. While in healthy children the maximal activity of the (left)abdominal muscles occurred 5±29% later than the MCE, in children with asthma the maximal activity occurred 26±30% of the cycle earlier than MCE. In children with asthma the activity of the IC muscles starts weaning already at 10±30% before MCE, in contrast to the healthy children in which intercostal muscle weaning starts only at 1±24% after MCE. During arithmetic, the significant difference between the groups in this respect disappeared.
Children with asthma show, even at rest, signs of respiratory muscle straining, probably in order to keep close control over the airflow in a similar way as healthy children during mental tasks. Such a ‘careful’ breathing pattern may work to prevent airway irritation also when they are free of symptoms.

View all citing articles on Scopus

View full text

Airflow limitation in asthmatic children assessed with a non-invasive EMG technique

Abstract

Introduction

Section snippets

Study subjects

Results

Discussion

Acknowledgements

Early Hum. Dev.

Clin. Chest Med.

Standardization of spirometry, 1994 update

Am. J. Respir. Crit. Care Med.

Clinical indications for lung function tests in infants, children and adolescents

Pediatr. Pulmonol.

Impaired reflex responses to airway occlusion in the inspiratory muscles of asthmatic subjects

Thorax

Neural drive to the diaphragm in patients with severe COPD

Am. J. Respir. Crit. Care Med.

Reproducibility and responsiveness of health status measures

Control Clin. Trials

Changes in neural drive (EMGd) and neuromuscular coupling during histamine-induced bronchoconstriction in patients with asthma

Eur. Respir. J.

Risk factors for growth and decline of lung function in asthmatic individuals up to age 42 years. A 30-year follow-up study

Am. J. Respir. Crit. Care Med.

Effects of reducing or discontinuing inhaled budenoside in patients with mild asthma

N. Engl. J. Med.

International consensus report on diagnosis and management of asthma

Clin. Exp. All.

Respiratory muscle activity measured with a noninvasive EMG technique: technical aspects and reproducibility

J. Appl. Physiol.