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Journal of Asthma, 29(5), 323-330 (1992)

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Perception of Bronchoconstriction in Chronic Asthma A. L. Boner,* G . De Stefano,? G . L. Piacentini,* C. Bonizzato,* L. Sette,’ F. Banfi,$ and M. C. Hindi-Alexander1 *Pediatric Department University of Verona, Verona Italy tlstituto P w XII Misurina (Belluno), Italy SGlaxo Italy Bwstatistics 1University of Buffalo Buffalo, New York ABSTRACT Twenty-nine asthmatic children were studied to assess their ability to detect the severity of their bronchoconstriction. First (STEP 0): each child was asked if he “felt asthma,” inviting him to give a selfestimated obstruction score (SEOS) from 0 (no asthma) to 3 (severe asthma) and a baseline FEVl was recorded. Then (STEP 1): methacholine was administered to all except 9 children with an FEVl < 80% of predicted who received saline nebulization and a second SEOS was recorded. Finally: salbutamol aerosol was administered and a third SEOS and FEVl were obtained (STEP 2). Spearman’s correlation coeff icients r between SEOS and FEVl were for the overall population -0.602, -0.51 7, and -0.104 at STEP 0, STEP 1 , and STEP 2, respectively. The r values reduction during the trial can be due either to a decrease of children’s concentration during the study or to a real difficulty in

Address reprint requests to: Prof. Attilio Boner, Clinica Pediatrica, Policlinico Borgo Roma, 37124 Verona, Italy.

323 Copyright Q 1992 by Marcel Dekker, Inc.

Boner et al.

324

recognizing repeated changes in airway status. Some children tend to underestimate their bronchospasm. For these patients an accurate assessment of the severity of the bronchoconstriction requires an objective measurement during acute changes in asthmatic children.

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INTRODUCTION Many studies have assessed the reliability of the perception of bronchoconstriction in adult asthmatic patients. Some authors studied the perception of externally hindered breathing (1-5). Although this method may provide information about the reflex control of respiration, it is of limited value if extrapolated to a clinical situation (6). Rubinfeld and Pain (6) demonstrated that controlled bronchial provocation with methacholine mimics asthma sufficiently well to allow this technique to be used in the study of sensations associated with obstructed breathing. At present, to our knowledge, there are few studies on perception of airway tone by asthmatic children (7-10) and one project studied adults and children together (11). Couriel et al. (10)studied children who had very frequent or persistent symptoms in a clinical setting. The aim of the present work was to assess the ability of children of different ages with less severe symptoms to detect the severity of their "natural" bronchoconstriction and also to recognize the instantaneous changes in airway status induced by drugs.

PATIENTS Twenty-nine children, 19 boys and 10 girls aged 6-14 years (mean 10.7 k 2.2), participated in the study. All patients had asthma as defined by the American Thoracic Society (12) and were skin test and RAST positive for house dust mite Dermatophagoides pteronyssinus andor common grass pollen. At the time of the study they had been admitted, at least for three months, to a residential house for asthmatic children in the Italian Alps (Istituto Pi0 XII-Misurina, located at 1756 m above sea level).

A positive response to salbutamol inhalation with a n increase in FEV, L 15% of baseline was observed at admission to the residential house. All the children were used to the procedures (pulmonary function tests and inhalation of drugs by aerosol) employed in the study. Considering the environmental conditions (no mites and no grass pollen) (13), some children were relatively symptom free during the study period and were not receiving any treatment. All the drugs currently used (Table 1) were stopped 3 days before the study. Patient characteristics are shown in Table 1.

METHODS The study was performed in three consecutive steps (STEP 0-1-2) represented in Figure 1. STEP 0: Each child was asked if he/she felt any bronchoconstriction and to attribute a self-estimated obstruction score (SEOS) from 0 (no asthma) to 3 (severe asthma) to reflect the bronchoconstriction experienced at that time. Children were also allowed to give intermediate values in the established range. Only the children who clearly understood the scoring system well enough to give an independent score without requiring adult supervision were admitted to the study. Then, baseline forced expiratory volume in 1 s (FEV,) was recorded using a Vitalograph spirometer, without revealing to the child hidher airway status. The best of three efforts was recorded. STEP 1: If FEVl was lower than 80% of predicted value (14) saline aerosol was administered to evaluate a n eventual placebo effect; then another SEOS and FEVl were obtained. On the other hand, if the FEVl was greater than or equal to 80% of predicted U4), nebulized methacholine was

Perception of Bronchoconstriction in Chronic Asthma

325

Table 1. Patient Characteristics BASELINE

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PATtE NT

GENDER

AGE

DURATION OF ASTHMA (yrs)

CURRENT THERAPY

1

M

11

4

T-iB-BDP

2

M

13

7

-

3

M M

13 14 13 13 13 10 10 12 9

5.5 8 6.5 6 4 3 3.5 4.5 2.5

iB

4

9 7 12 11 9 11 13 11 12 12 13 12 6

3 2.5 2.5 5 6 4 7 5 3 5 4 3 1.5

M

7 7 8 11

M

9

3 2.5 3 3 2

5

M

6

M

7 8

M

9

F

10

M

11

M

F

12

M

13

M

14

F

15

F

16

hi

17 18 19 20 21 22 23 24 25 26 27 28 29

F

F F

F F F M M

M M M

10.7 f 2.2

MEAN

4.12

FNl % PREDICTED

73 70

-

95 71 103 80 80

iB

89

T

74 88 87

iB iB

T

-

iB C-i B T T-iB

C iB iB

T-BW

T -

84 86 88 86 90 87

74 62 94 59 84 95 86

-

108 80 76 83

-

75

C C iB

* 1.7

Abbreviations: T = theophylline; iB = intermittent p2-stirnulants; BDP = beclomethasone dipropionate; C = crornolyn.

9 STEP 0

(Q pts.) STEP 1

STEP 2

0 Figure 1. Experimental design. SEOS = self-estimated obstruction score; FEVl P = placebo; M = methacholine; S = salbutamol.

=

forced expiratory volume in 1 s;

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326

Boner et al.

administered and both SEOS and FEVl were obtained again. STEP 2: The child was then given aerosolized salbutamol and the SEOS and FEVl were recorded once more. All the treatments were administered by aerosol and the nature of the inhaled drug was not revealed either to the nurse who treated the children or to the patients. They were told only that each aerosol could make their breathing worse, better, or unchanged. Aerosols were generated by MeFar nebulizers (MeFar, Brescia, Italy) driven by compressed air at 6 L/min. Salbutamol and methacholine were administered as 0.5% and 0.31 mg/ml solutions, respectively. The inhalations were interrupted every 30 seconds for a 30-second period to assess the patients’ condition by clinical examinations. Nebulizations were in each case stopped after a cumulative 120 s of inhalations or earlier, if wheezing, cough, hand trembling, or any other unpleasant side effect was noted (0.75 ml of solution were nebulized in cumulative 120 s; this volume is equal to 0.23 mg of methacholine and 3.7 mg of salbutamol). At the end of each 120 s nebulization both the SEOS and FEVl were obtained again. At the end of the study the child was informed on the nature of the aerosol and on hisher performance. Informed consent was obtained from each child and the respective parents, and the protocol was approved by the Hospital Ethical Committee. Statistical evaluations were performed by Spearman’s rank correlation coefficient T .

and received placebo aerosol (saline) which never resulted in improved pulmonary function; then all 9 children received salbutamol aerosol (Fig. 1).Distribution of patients by FEVl and SEOS at all steps together is reported in Table 2 and is graphically represented in Figure 2 for step 0 and Figure 3 for all steps tagether in which FEVl values are plotted against their relative SEOS with the estimated regression line. As can be seen, no child ever gave a SEOS greater than 1.5 (mild/moderatebronchoconstriction)although five values of FEVl were < 60% of predicted (Table 2, Fig. 3). The Spearman’s rank correlation coefficients T between SEOS and FEV, are reported in Table 3. As can be seen, it was -0.502 for the overall population studied at all steps. For the 16 children aged more than 11 years the correlation coefficient r was -0.678, while for those aged 11 or less the correlation coefficient T was only -0.345. The correlation coefficientscalculated at each step of the design ranged from -0.602 at baseline to -0.104 at STEP 2. In order to evaluate the ability of the children to recognize changes in their airway status (bronchodilation or bronchoconstriction), a correlation was made between differences in FEV, observed at step 1 and step 0 (FEVI/STEP 1-FEV1/STEP 0) and corresponding SEOS (SEOS/STEP 1-SEOS/STEP 0)( r = -0.632) and again, between STEP 2 and STEP 1 (FEVI/STEP 2-FEVIISTEP 1) and SEOS/STEP 2-SEOSISTEP 1)( r = -0.332).

RESULTS

Table 2. Distribution of Patients at All STEPS Together: FEV, by SEOS

Twenty patients had a baseline value of FEVl 2 80% of predicted (Table 1) and therefore received methacholine first, followed by a salbutamol challenge (Fig. 1). There were either no changes or insignificant decreases in FEV1% of predicted values after methacholine inhalation when compared with baseline values in 6 patients (Nos. 8,12, 13, 25, 26, 28). Nine patients had a n FEVl baseline value < 80% of predicted (Table 1)

SEOS

Oh

FEVl OF PREDICTED

0

0.5

1

1.5

n

50-59

1

1

3

0

5

60-69

0

1

6

2

9

70-79

15

6

5

0

26

80-89

27

4

1

0

32

t 90

12

1

2

0

15

n

55

13

17

2

87

327

Perception of Bronchoconstriction in Chronic Asthma

n

90 a0 .-i, -0 70 a, L c l 60 v0 50 x 40 > 30 w LL 20 73

6,

u

W

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r

SEOS =O

SEOS =0.5

SEOS = 1

SEOS =1.5

Figure 2 . Distribution of patients by FEVl and SEOS, STEP 0 0 3 = severe.

In all cases, the patients tested were able to recognize instantaneous variations in airway tone both when bronchoconstriction occurred after methacholine (STEP 1-STEP 0) and when bronchodilatation occurred after salbutamol (STEP 2-STEP 11, even though the SEOS was frequently out of proportion with the actual measured FEV1, particularly

=

SEOS =2.5

SEOS =2

no bronchoconstriction;1

=

mild; 2 = moderate;

after salbutamol. There was no statistically significant relationship between the symptom perception and the length of history of asthma; though, there was a greater tendency toward underestimating the severity of the bronchoconstriction in those children with a longer history of disease. No child showed side effects from either

.:

'100 lo$ I

0'

1

.....

I

SEOS =O

I

I SEOS =0.5 1

I

SEOS =1

I

1 SEOS =1.5 1

Figure 3 . Distribution of patients by FEV, and SEOS. All Steps together: 0 2 = moderate; 3 = severe.

=

I

SEOS

=2

1

no bronchoconstriction;1

=

mild;

Boner et al.

328 Table 3. Spearman’s Correlation Coefficient r Between FEV, and SEOS SPEARMAN’S CORR. COEFFICIENT

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STEP 0 (n. 29) STEP 1 (n. 29) STEP 2 (n. 29) All STEPS (n. 87) All STEPS age 5 1 1 yrs (n. 48) All STEPS age > 1 1 yrs (n. 39)

methacho-line or mlbutamol of such entity to induce both the interruption of the study or the unblind of the drug administered.

DISCUSSION Our study was conducted at high altitude in environmental conditions associated with the absence of common antigens. This results in a reduction of bronchial hyperreactivity (15) and may explain the fact that some children experienced either no changes or insignificant decreases in FEVl percent of predicted values after methacholine (230pg) inhalation and the fact that 9 patients were receiving no treatment and that 8 of these 9 subjects had baseline FEVl > 80% of the predicted value (Table 1). However, the children who did not show any reaction to the dose of methacholine administered in this study were reactive to a greater dose of methacholine when they were discharged from the residential house. Therefore, the lack of the responsiveness during the study may be also explained by the low dose used. The results of this study show that, although the perception of the airway status was generally good,there are some children who tend to underestimate their bronchoconstriction. Some studies have found similar results in adults (16-18) and children (8-10) while others found the opposite, that is that adults are more reliable in their perception of bronchoconstriction (11,19). Our concern lies obviously with underestimation of bronchoconstriction, because those patients could

-0.602 -0.51 7 -0.104 -0.502 -0.345 -0.678

99% CONFIDENCE INTERVALS (-0.819; (-0.773; (-0.508; (-0.667; (-0.609; (-0.838;

-0.236) -0.1 15) 0.338) -0.290) -0.013) -0.412)

S S

NS S

S S

be at risk of death from asthma (20-22).These rates have been increasing, in both children and adults even though the tmatment for this disease has p a t l y improved (20-22).As an example, in our study a 9-year-oldmale child gave a SEOS d 1(mild bronchoconstriction) with an FEVl = 56%of predicted, a 12-yearold girl gave a SEOS = 1 with a FEVl = 55% of predicted and a SEOS = 0 when her FEVl was 59%of predicted; another 12-yearold female gave a SEOS = 1with a FEVl = 59% and 0.5 with a FEVl = 58%of predicted (Table 2; Fig. 3). Silverman and co-workers (11)found that for asthmatic patients aged 7 to 43 years, an estimated PEFR is a much more accurate and reliable subjective indicator of airway obstruction than is a verbal obstructed breathing score; however, because of the lower mean age of our study population, we thought it was best to use a verbal obstructed breathing score which, in our opinion, is more intuitive for children. As can be seen in Table 3, r absolute values tend to decrease in the process of the trial. At present we cannot establish if this is due to a decrease of the power of concentration of the children or to a real difficulty in recognizing repeated changes in their airway status. It also may be possible that the perception of bronchodilation (STEP2-STEP 1)is more difficult than the perception of bronchoconstriction (STEP 1-STEP 0). In our study those children whose asthma was more severe and of longer duration had a greater tendency to underestimate their bronchoconstriction as previously observed (9). The reason for this is the fact that probably the principle of temporal sensory

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Perception of Bronchoconstriction in Chronic Asthma adaptation can be applied to breathlessness just as to any other sensation. Temporal adaption implies that prolonged stimulation results in consistent reduction of perceived magnitude (18).In the presence of chronic asthma, patients may become adapted to their pulmonary dysfunction. In this connection, McNicol and Williams (23) suggested that much of childhood chest deformity due to asthma may be due to lack of perception of the severity of the disease by the patients or their parents. Furthermore it has been shown that those patients with the more severe bronchial hyperreactivity are the least aware of dyspnea since they are able to adjust respiratory muscle performance to suit varying airflow obstruction (24). This situation is dangerous in view of the risk for asthma death, the major causes of which seem to be underestimation of the severity of an episode of bronchoconstridion, delay or underuse of appropriate care and, especially for children, disregard of symptoms and inadequate self-management (20-22). Shim and Williams (19) found that asthmatics were more accurate than physicians in assessing the severity of their airway obstruction and that even experienced physicians were quite inaccurate in estimating the actual peak expiratory flow rate (PEFR) when examining patients. According to other studies (9,111, overestimation of the severity of symptoms by patients was less frequent, but it nevertheless is dangerous, since it may be associated with an increase in medication-taking,resulting in unpleasant side effects. From all these observations, it is clear that accurate assessment of the severity of bronchoconstriction requires, when possible, an objective measurement of airway obstruction. For this reason it is recommended that children who tend t o greatly underestimate their asthma be identified and be encouraged to record the objective measurement, of their pulmonary function with the use of a portable peak expiratory flow meter. They should be given guidelines to follow and a decisionmaking protocol for acute situations. This has been shown to result in improvement in the early detection of bronchoconstriction and in the general asthma management (9,251.

329

Furthermore, personal profile batteries adapted to use in children (26) may be useful to identify patients who may underestimate their asthma (e.g., patients with low panicfear thresholds) and thus would be good candidates for peak flow monitoring.

REFERENCES 1. Campbell EJM, Bennett ED, Rubenstein D. The ability to distinguish between added elastic and resistive loads to breathing. Clin Sci Mol Med

24~201-207, 1963. 2. Campbell EJM,Freedman S, Smith PS, Taylor ME. The ability of man to detect added elastic loads to breathing. Clin Sci Mol Med 20:223-231,1961. 3. Bennett ED,Jayson MI, Rubenstein D, Campbell EJM. The ability of man to detect added non elastic loads to breathng. Clin Sci Mol Med 23:155-162, 1962. 4. Wiley RL, Zechman FW.Perception of added airflow resistance in humans. Resp Phys 273-83, 1966. 5. Burki NK, Mitchell K, Chaudhary BA, Zechman FW. The ability of asthmatics to detect added resistive loads. A m Reu Resp Dis 11 771-75,1978. 6. Rubinfeld AR, Pain MCF. Bronchial provocation in the study of sensations associated with disordered breathing. Clin Sci Mol Med 52:423-428,1977. 7. Harver A, Kotses H. Perception of static respiratory forces in young and old subjects. Percept Psychophys 41 :449-454,1987. 8. Sly PD, Landau LI, Weymouth R. Home recording of peak expiratory flow rates and perception of asthma. A m J Dis Child 139:479-482,1985. 9. Konig P, Rejent A. Subjective and objective means of assessing cystic fibrosis and asthma. Ann Allergy 49236-92,1982. 10. Couriel JM,Demis T, Olinsky A. The perception of asthma. Aust Paediatr J 22:4547,1986. 11. Silverman BA, Mayer D, Sabinsky R, WilliamsAkita A, Feldman J, Schneider AT, Chiaramonte LT. Training perception of airflow obstruction in asthmatics. Ann Allergy 59:350-354,1987. 12. American Thoracic Society. Chronic bronchitis, asthma, and pulmonary emphysema. A m Reu Resp Dis 85:762-768,1962. 13. Verloet D,Penaud A, Razzouk H, e t al. Altitude and house dust mite. J Allergy CLin Immunol 69~290-296, 1982. 14. Polgar G , Promadhat V. Pulmonary Function Testing in Children; Techniques and Standards. WB Saunders, Philadelphia, 1971,pp 42-86. 15. Boner AL,Niero E, Antolini I, Valletta EA, Gaburro D. Pulmonary function and bronchial hyperreactivity in asthmatic children with house dust mite allergy during prolonged stay in the Italian Alps 1985. (Misurina, 1756 m). Ann Allergy 54~42-45,

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330 16. Rubidield AR, Pain MCF. Perception of asthma. Lancet 1:882684, 1976. 17. Ellis ME, Friend JAR. How well do asthma clinic patients understand their asthma? Br J Dis Chest 7943-48, 1985. 18. Editorial. Peroeption of breathlessness in asthma. Lancet 1:912-913, 1983. 19. Shim CS, Williams MH Jr. Evaluation of the eeverity of asthma: patients versus physician. A m J Med 68:ll-13, 1980. 20. Sly RM.Increase in death from asthma.Ann Alkrgy 53:20-25, 1984. 21. William AJ, Church SE. A near fatal asthma attack in a patient unaware of deteriorating lung function. Eur J Resp Dis 71:259-262, 1987. 22. Hindi-Alexander MC, Middleton E Jr. Asthma deaths: are they preventable? NER Allergy Proc 7462-466, 1986.

Boner et al. 23. Mc Nicol KM, Williams HB.Spectrum of asthma in childhood :l. Clinical and physiological components. Br Med J4:7, 1973. 24. Burdon JGW, Juniper EF, Killian KJ, Hargreave FE, Campbell EJM. The perception of breathlessness in asthma. A m Rev Resp Dis 126825-828, 1982. 25. Wigal JK, Katses H, Rawson JC, Creer TL. The effecta of suggestionon the total respiratory resistance of nonasthmatic female subjects. J Psychosom Res 32(4/5):409416, 1988. 26. Jones NF, Kinsman RA, Dirks JF, Dahlem NW. Psychological contributionsto chronicity in asthma: patient responae styles influencing medical treatment andits outcome. Med Care17(11):1103-1118, 1979.

Perception of bronchoconstriction in chronic asthma.

Twenty-nine asthmatic children were studied to assess their ability to detect the severity of their bronchoconstriction. First (STEP 0): each child wa...
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