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(Chest. 2006;130:436-441.)
© 2006 American College of Chest Physicians

Is There a Link Between the Qualitative Descriptors and the Quantitative Perception of Dyspnea in Asthma?

Claudia Coli, MD; Monica Picariello, MD; Loredana Stendardi, MD; Michela Grazzini, MD; Barbara Binazzi, MD; Roberto Duranti, MD and Giorgio Scano, MD, FCCP

* From the Department of Internal Medicine (Drs. Coli, Picariello, Scano, and Duranti), Section of Immunology and Respiratory Medicine, University of Florence; and Fondazione Don C. Gnocchi (Drs. Stendardi, Grazzini, and Binazzi), Section of Respiratory Rehabilitation, Pozzolatico (Firenze), Firenze, Italy.

Correspondence to: Giorgio Scano, MD, Department of Internal Medicine, Section of Respiratory Medicine, Clinica Medica 3, Policlinico di Careggi, Careggi, Viale Morgagni 87, 50134 Firenze, Italy; e-mail: gscano{at}unifi.it

Abstract

Background: There is no obvious link between qualitative descriptors and overall intensity of dyspnea during bronchoconstriction in patients with asthma.

Aims: To determine whether qualitative and quantitative perception of methacholine-induced bronchoconstriction independently contribute to characterizing clinically stable asthma.

Material and methods: We assessed changes in inspiratory capacity, and quantitative (by Borg scale) and qualitative (by a panel of eight dyspnea descriptors) sensations of dyspnea at 20 to 30% fall in FEV1 during methacholine inhalation in 49 asthmatics. Furthermore, we calculated the level of perception of bronchoconstriction at 20% fall in FEV1 (PB20).

Results: Descriptors selected by patients during methacholine inhalation allowed us to define three language subgroups: (1) chest tightness (subgroup A, n = 21); (2) work/effort (subgroup B, n = 7); and (3) both descriptors (subgroup C, n = 13). Eight of the 49 patients (subgroup D) were not able to make a clear-cut distinction among descriptors. The subgroups exhibited similar function at baseline and during methacholine inhalation. Most importantly, patients selected chest tightness to a greater extent (42.85%), and work/effort (14.3%) and both descriptors (26.5%) to a lesser extent at the lowest level of bronchoconstriction (FEV1 fall < 10%) as at 20% fall in FEV1. Thirty-two patients were normoperceivers (PB20 ≥ 1.4 to < 5 arbitrary units [au]), 7 patients were hyperperceivers (PB20 ≥ 5 au), and 10 patients were hypoperceivers (PB20 < 1.4 au). Language subgroups were equally distributed across the perceiver subgroups.

Conclusions: In patients with clinically stable asthma, PB20 and language of dyspnea independently contribute to defining the condition of the disease. However, the possibility that this independence may be due to a ß-error should be taken into account.

Key Words: bronchoconstriction • chest tightness • dyspnea • respiratory work/effort

Studies12 have shown that patients with acute or stable asthma have resolution of their dyspnea despite minimal improvement in lung function and the persistence of significant airflow obstruction. Rubinfeld and Pain3 showed that 10% of their asthmatic patients had FEV1 < 50% of predicted when they had no symptoms at baseline. These patients have been described as poor perceivers. These studies123 suggest that patients’ perception of their dyspnea in response to change in lung function is nonspecific and that assessment directed at the intensity of dyspnea alone may not accurately reflect the level of persistent airway obstruction. In this connection, by using the language of dyspnea,4567 Moy et al8 found that descriptors of dyspnea are more specifically associated with change in lung function than overall intensity of dyspnea. In a further study, Moy et al9 found that the initial sensation of chest tightness reflected the breathing discomfort resulting from mild bronchoconstriction; with more severe FEV1 fall and hyperinflation, selection of chest tightness decreased, whereas selection of work or effort progressively increased. In turn, the available data suggest that multiple mechanisms are likely to lead to several distinct sensations of dyspnea in patients with asthma.45678910

The intensity of the perception of bronchoconstriction during a provocation test may provide information on how a given subject perceives asthma symptoms. Low perception, even when asthma is stable, may potentially be a risk factor of worsening severe asthma because of delay of rescue medication. Based on quantitative assessment of perception of bronchoconstriction at 20% fall in FEV1 (PB20), patients with asthma have been stratified into three groups of perceivers: hypoperceivers, normoperceivers, and hyperperceivers.111213

Because different types of dyspnea exist in patients with a variety of cardiopulmonary abnormalities—with the quality of sensation, not the intensity, appearing to be the distinguishing features—we hypothesized that in clinically stable asthma, intensity and quality of dyspnea during bronchoconstriction may provide independent information on the state of the disease. To our knowledge, no study has addressed whether the pattern of language descriptors differs among perceiver categories of asthma. This was the aim of the present study where we assessed qualitative (using dyspnea language) and quantitative (using the Borg scale) perception of bronchoconstriction in clinically stable patients with asthma.

Materials and Methods

Forty-nine patients with persistent stable bronchial asthma according to the criteria of the National Heart, Lung, and Blood Institute14 with a significant response to ß2-agonists participated in the study. Asthma in these patients had been diagnosed for at least 1.8 years. Asthma was classified as either mild or mild to moderate according to the frequency of symptoms, the requirement of ß2-agonists for the treatment of symptoms, baseline airway function, and a provocative concentration of methacholine causing a 20% fall in FEV1 (PC20) < 8 mg/mL (Table 1 ). No patient had a history of smoking, and at the time of the study there was no clinical or laboratory evidence of any other cardiorespiratory disease. Each patient received inhaled corticosteroids at a daily dose of 125 mg (mild asthma), to 250 to 375 µg (mild-to-moderate asthma). The use of a bronchodilator was withheld for at least 24 h before each visit. Informed consent was given by patients, and the study was approved by the local ethics committee.


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  		Table 1. Anthropometric and Lung Function Data at Baseline*

 
Study Design
Patients were studied on two occasions 1 to 2 days apart. At the first screening visit, patients were familiarized with dyspnea questionnaires and the Borg scale. On the study day, dyspnea was measured and spirometry performed at baseline after inhalation of nebulized saline solution and after each progressive dose of methacholine.

Lung Function
Baseline pulmonary function testing was performed by measuring static and dynamic (FEV1) volumes with a water-sealed spirometer (Pulmonet Godart; SensorMedics; Yorba Linda, CA), as reported previously.15 The normal values for lung volumes are those proposed by the European Community for Coal and Steel.16

Bronchial Challenge
Each patient was administered a methacholine aerosol inhalation test according to a standardized tidal breathing procedure.17 Increasing concentrations of methacholine-chlorhydrate in normal phosphate-buffered saline solution (prepared by the University Hospital Pharmacy) were inhaled from a nebulizer (model 646; DeVilbiss; Somerset, PA), resulting in an output of 0.13 mL/min. With this method, 4 mL of solution was placed in the nebulizer, and inhalation continued during tidal breathing for 2 min. Methacholine solution was stored at 4°C and was nebulized at room temperature. Normal phosphate-buffered saline solution was inhaled first, followed at 5-min intervals by methacholine in twofold increasing concentrations from 0.015 to 8 mg/mL. The test was stopped at the PC20 from baseline. FEV1 was measured 1 to 1.5 min after the inhalation of each concentration of methacholine. Two measurements of FEV1 were performed, and the best value was used. PC20 was noted from the log dose-response curve.

Dyspnea Evaluation
The perception of dyspnea was evaluated by asking the patients to score the intensity of the dyspnea on the Borg scale. The Borg scale is a vertical list with labeled categories (0 to 10) describing increasing intensities of dyspnea.18 Subjects were asked to rank the overall sensation of respiratory discomfort; they were instructed that 0 signified no sensation at all, and 10 signified the most severe sensation that they could imagine. The quality of the dyspnea was evaluated by asking patients to select one to three descriptors of dyspnea from a panel of eight descriptors before inhalation of saline solution and at each concentration of methacholine, before FEV1 measurements. Questionnaires regarding descriptors of dyspnea during spontaneous episodes of asthma were filled out retrospectively during the first screening visit (Table 2 ). Thus, we chose eight descriptors that the same patients were familiar with during spontaneous asthma. In keeping with Mahler et al,6 descriptors were arranged by clusters: descriptors 3, 4, and 6 (Table 2) defined work/effort, whereas descriptors 7 and/or 8 described chest tightness. Descriptors 1, 2, and 5 were never selected. On the day of the study, the same questionnaire was employed to describe the sensation experienced during methacholine-induced bronchoconstriction, before the Borg rating.


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  		Table 2. Descriptors of Dyspnea

 
Data Analysis
Changes in inspiratory capacity (IC) and FEV1 were measured immediately after inhalation of each concentration of methacholine. Values are given as mean ± SD. Least-squares linear regression was used to analyze the dose-response curves and the relationship between changes in Borg score and fall in FEV1, expressed as percent of control; from this relationship slope ({Delta}Borg/{Delta}FEV1) and intercept (Borg arbitrary units [au]) were obtained. The Borg score at 20% fall in FEV1 was determined by interpolation (PB20). In line with previous studies,111213 three groups of perceivers were selected: normoperceivers (PB20 ≥ 1.4 to < 5 au), hyperperceivers (PB20 ≥ 5 au), and hypoperceivers (PB20 < 1.4). Differences in IC and fall in FEV1, and in Borg were assessed among subgroups by using univariate analysis of variance.19 At each methacholine step, patients were asked to select one or more language descriptors. The association between categories of dyspnea sensation and dyspnea severity were analyzed by frequency tables; statistics included Pearson {chi}2, likelihood-ratio {chi}2, linear-by-linear association test, and Fisher exact test. The conventional level of statistical significance was set at p < 0.05.

Results

The two descriptors selected by patients at 20 to 30% fall in FEV1 allowed us to define the language subgroups: subgroup A, chest tightness (n = 21); subgroup B, work/effort (n = 7); and subgroup C, both descriptors (n = 13). Eight patients (subgroup D) were not able to understand question about their breathlessness or were extremely confused about their symptoms during the screening visit; they were not given the option not to select any descriptor. As shown in Table 3 , language subgroups exhibited similar function at baseline; at methacholine end point, FEV1 fall and Borg score were similar in the subgroups, whereas the level of hyperinflation, as assessed in terms of IC fall, was greater in subgroup C (analysis of variance p < 0.016) than in subgroups A, B, or D. Most importantly, we found a greater selection of chest tightness, and a lower selection of work/effort at the lowest degree of airway obstruction (FEV1 fall < 10%) without any hyperinflation: 42.85% selected chest tightness, whereas 14.3% selected work/effort, and 26.5% selected both descriptors. In particular, the corresponding average values of fall in FEV1 were 5.65 ± 4.6%, 7.7 ± 5.4%, and 9.36 ± 7%, respectively (p = not significant [NS]). The data indicate that the perception of chest tightness did not anticipate the perception of work/effort. Last but not least, in no case did patients modify their initial descriptor(s) during the test.


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  		Table 3. Function Data in the Language Subgroups*

 
Change in Borg score regressed to a fall in FEV1 (mean slope {Delta}Borg/{Delta}FEV1 percentage fall of 0.13 ± 0.08 au/%; r2 = 0.53 to 0.98), but not to fall in IC. Group (PB20) was 3.66 ± 2 au. As shown in Table 4 , the vast majority of subjects (32 of 48 patients) were normoperceivers (PB20 ≥ 1.4 to < 5 arbitrary units [au]), 7 patients were hyperperceivers (PB20 ≥ 5 au), and 10 patients were hypoperceivers (PB20 < 1.4 au). Most importantly, as shown in Table 4, no association was detected between categories of dyspnea sensation and dyspnea severity (Pearson {chi}2, p = 0.78; likelihood-ratio {chi}2, p = 0.794; linear-by-linear association test, p = 0.50; Fisher exact test, p = 0.77). The average dose of inhaled corticosteroids did not differ among perceiver categories (p = NS).


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  		Table 4. Perception of Bronchoconstriction as Assessed in Terms of Borg Score at 20% Fall in FEV1 in the Language Subgroups*

 
Discussion

We studied patients who were naïve to the protocol and the descriptors of dyspnea. This made it unlikely that the results represent a selection bias. Our data show that patients scored the intensity of perceived bronchoconstriction (PB20) regardless of the selected descriptors of dyspnea. Patients selected chest tightness to a greater extent and work/effort to a lesser extent at the lowest level of airway obstruction without any hyperinflation as at 20% fall in FEV1.

Qualitative Perception of Asthma
Killian et al7 hypothesized that acute bronchoconstriction generates several stimuli activating different sensory receptors that elicit several sensations that are described by different expressions or symptoms. They found that symptoms that can be reliably distinguished imply different neural processes; symptoms that cannot be reliably differentiated imply a similar neural process.7 Chest tightness and work effort were reliably distinguished in their article.

Chest tightness, a frequently reported descriptor by asthmatic patients during acute bronchoconstriction,4567 may arise from stimulation of sensory receptors within the lungs mediated through vagal and autonomic pathways.910 Rapidly adapting (irritant) receptors and C-fibers may respond to local inflammation of the airways and may contribute to dyspnea.2021 Descriptors comprised in the work/effort cluster are associated with increased motor command to ventilatory muscles relayed2223 by interneurons high in the CNS to the sensory cortex (corollary discharge).24 The intensity of the motor command alone or in combination with the generation of force and contraction of the respiratory muscles may be consciously appreciated as difficult in breathing or effort.24 Moy et al9 found that an initial sensation of chest tightness reflected the breathing discomfort resulting from mild bronchoconstriction; with more severe FEV1 fall and hyperinflation, selection of tightness decreased, whereas selection of work or effort progressively increased.9 The progressive increase in work/effort could reflect the more persistent airway obstruction related to the inflammatory component of asthma,22 and the associated mechanical load on the ventilatory muscles.2325 Unlike the data by Moy et al,9 the present data show that subjects selected the same descriptors at the lowest levels of obstruction and at 20% fall in FEV1. Moreover, for a similar fall in FEV1, regardless of the level of hyperinflation, subgroups C and B selected work/effort (Table 3), indicating that in the range of the values in the present study, reason(s) other than hyperinflation/obstruction underlie the sensation of work/effort. In line with this view is the finding that asthmatics describe work/effort without hyperinflation during incremental exercise testing.26 This is consistent with the hypothesis that multiple mechanisms lead to distinct sensations of dyspnea in asthma.45678910 Clinical differences between series (persistent asthma, exercise asthma, upper respiratory infection, and steroid treatment as in the present study) might be the reason for the discrepant results between the present study and that of Moy et al.9

The observation that eight patients were not able to differentiate one descriptor from another seems also to indicate that although it is clear that some patients rate at least two dimensions of respiratory discomfort,6 subjects may have difficult time making a clear-cut distinction.10 The difference between the experience of patients in this study and that of patients who selected different descriptors of dyspnea (perception of inspiratory difficulty, expiratory difficulty, difficulty in taking a deep breath, or an awareness of unsatisfied inspiratory effort)5 are most likely due to a difference in the severity of airway obstruction and the level of dynamic hyperinflation achieved.

Quantitative vs Qualitative Perceptions
Low perception of bronchoconstriction even when asthma is stable may be a potential risk factor of severe asthma because of delayed rescue medication. In line with our previous study12 and that of others,111213 the present study shows that stable asthmatic patients can be either moderate perceivers, hypoperceivers, or hyperperceivers to an acute change in airway caliber with methacholine. This simply means that poor perceivers have the lowest perception value compared to the rest of the study population.12 Acute perception of bronchoconstriction (Borg score) was related, to a varying extent, to the percentage of fall in FEV1 ({Delta}Borg/{Delta}FEV1). Unlike other studies,527 change in IC, which is the mirror image of the changes in end expiratory lung volume, did not contribute significantly to the variance in Borg ratings. Nonetheless, the decrease in IC in this study was lower than that in our previous study,27 where, however, the level of bronchoconstriction was remarkably more severe.

Moy et al8 found that acute patients discharged from the emergency department after intensive nebulization therapy with FEV1 < 60% of predicted had an overall dyspnea intensity < 1.5. While these patients could be considered "poor perceivers," it was remarkable that half of them continued to select phrases that described breathing as "tight" or requiring work/effort. Moy et al8 suggested that "use of language of dyspnea to supplement global ratings of dyspnea intensity may help identify these patients." They also underlined the need to examine whether patterns of language descriptors differ among patients who are poor perceivers of overall dyspnea.

The present study was designed to define the link between qualitative and quantitative assessment of the perception of bronchoconstriction in clinically stable patients with asthma. As it is evident, patients selected descriptors regardless of the quantitative perception of bronchoconstriction (PB20) [Table 4]. For example, cluster A was shared by the three perceiver subgroups. Likewise, normoperceivers were equally distributed among the language groups. Note that for similar levels of FEV1, and IC decrease in subgroups A and B (Table 3), a greater number of each perceiver category (normoperceiver, hypoperceiver, and hyperperceiver) was present in subgroup A than in subgroup B. Moreover, although subgroup D patients were unable to provide a qualitative descriptor of their dyspnea, they were able to make a quantitative estimate of its intensity. The observation that the perception of chest tightness did not anticipate the perception of work/effort during the test (see "Results" section) indicates that, if however the fall in FEV1 increased the score of dyspnea quantitatively ({Delta}Borg/{Delta}FEV1 slopes), it did not appear to determine the perception of dyspnea qualitatively. In turn, the data suggest that PB20 and language of dyspnea are independent dimensions.

In summary, patients select descriptors of dyspnea regardless of the quantitative level of perception of bronchoconstriction (PB20). Quantity and quality independently characterize dyspnea in asthma supporting the validity of routine assessment of both. The data also suggest that various qualities of dyspnea may result from the association of different pathophysiologic abnormalities. Studies on a larger series aimed at defining the association of language descriptors with either low or high levels of perception of bronchoconstriction are needed in patients with asthma. As yet, we should not disregard the possibility that the lack of an obvious link between qualitative and quantitative perception of dyspnea intensity may be due to a ß-error.

Footnotes

Abbreviations: au = arbitrary unit; IC = inspiratory capacity; NS = not significant; PB20 = perception of bronchoconstriction at 20% fall in FEV1; PC20 = provocative concentration of methacholine causing a 20% fall in FEV1

The authors state that they have no potential or financial conflicts related to this article.

Received for publication September 21, 2005. Accepted for publication February 1, 2006.

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