Journal of Asthma, 46:186–190, 2009Copyright C© 2009 Informa Healthcare USA, Inc.ISSN: 0277-0903 print / 1532-4303 onlineDOI: 10.1080/02770900802604129

ORIGINAL ARTICLE

Quality of Life in Asthmatic Adolescents: An Overall Evaluation

of Disease Control

CRISTINA GONCALVES ALVIM,1,∗ ISABELA MENDONCA PICININ,1 PAULO MOREIRA CAMARGOS,1

ENRICO COLOSIMO,2 LAURA BELIZARIO LASMAR,1 CASSIO CUNHA IBIAPINA,1 MARIA JUSSARA FONTES,1AND CLAUDIA RIBEIRO ANDRADE1

1Federal University of Minas Gerais, Pediatric, Belo Horizonte 30130100, Brazil2Federal University of Minas Gerais, Statistics, Belo Horizonte 30130100, Brazil

Objective. to evaluate the relative impact of reported symptoms, school absenteeism, hospital admission, medical visits, and the presence ofemotional and behavioral disorders on the health-related quality of life (HRQL) of low income asthmatic adolescents. Methods. Asthmatic adolescentswere randomly selected among public schools in Belo Horizonte/MG, Brazil. Asthma severity was rated according to the Global Initiative for Asthma(GINA) classification. Emotional and behavior disorders (EBDs) were evaluated through the Strengths and Difficulties Questionnaire. HRQL wasassessed through the Pediatric Asthma Quality of Life Questionnaire (PAQLQ). PAQLQ score was analyzed for each intervening variable. Multivariateregression analysis was conducted. Results. One hundred and forty-six adolescents participated in the present study, 45% being male and age rangingfrom 14 to 16 years old. Mean PAQLQ score was 5.7 ± 1.3 SD, with no significant difference regarding sociodemographic characteristics, except forgender (p = 0.001). The regression equation of the final model for the multivariate analysis was as follows: Mean PAQLQ score = 1.88 (Constant) −0.42 gender + 1.14 nighttime symptoms + 0.69 medical visits in the past 12 months + 0.95 EBDs. Therefore, if the other variables remained constant,PAQLQ score: reduced in 0.42 points for females (p = 0.01); increased in 1.14 when there were no nighttime symptoms (p < 0.01); increased in0.69 when there was no medical visit for respiratory problems within the past 12 months (p < 0.01); and increased in 0.95 when no EBDs werepresent (p < 0.01). This model was able to explain approximately half of the variation found in PAQLQ score (R-Sq = 49.4%). Conclusions. HRQLof asthmatic adolescents is influenced by the complex interaction among several factors: the severity of clinical symptoms, morbidity, gender, andthe psychological resources available so as to deal with such difficulties. A careful evaluation of HRQL is essential in order to capture feelings andsubjective perceptions, which are not investigated by the conventional evaluation of asthma control.

Keywords asthma, adolescents, quality of life, psychological adaptation, affective symptoms

INTRODUCTION

Advances in biomedical science and technology have re-sulted in dramatic improvements on the healthcare of pe-diatric chronic conditions and, thus, health-related qualityof life (HRQL) issues have become more relevant. HRQLis evocative of the World Health Organization definition ofhealth: “a state of complete physical, mental and social well-being and not merely the absence of disease or infirmity” (1).

Due to its chronic evolution, asthma affects the day-to-daylife of patients in functional, social and emotional domains.The promotion of the well-being of asthmatic patients hasbeen recommended as one of the main goals of the treatment.Therefore, there has been increasing interest in the evaluationof HRQL in asthmatic individuals.

Evidence shows that conventional methods (evaluation offrequency and severity of symptoms and pulmonary func-tion), although undeniably important, are not sufficient todetermine the impact of the disease in the life of asthmat-ics (2, 3). HRQL has been associated to symptom scores andairway inflammation as measured by exhaled nitric oxide (re-gression coefficient 0.410, p = 0.001) (4). Otherwise, Ehrset al. found no correlation between quality of life and mea-

∗Corresponding author: Dr. Cristina Goncalves Alvim1, Federal Univer-sity of Minas Gerais, Pediatric, Avenida Alfredo Balena, 190, 4o andar,Belo Horizonte, 30130100 Brazil. E-mail: cgalvim@terra.com.br

sures of asthma, such as pulmonary function, exhaled nitricoxide, and bronchial responsiveness to direct and indirectstimulis in patients with mild asthma (5). Gandhi et al. (6), ina recent review, have concluded that there is no ideal way toadequately isolate and evaluate asthma control. They suggestthat objective measurement (spirometry and peak expiratoryflow rate) be used along with inflammation markers (exhalednitric oxide and sputum eosinophils), as well as with subjec-tive measurement, such as evaluation of HRQL, in order tobetter estimate disease control.

Quality of life is usually evaluated through questionnaires,which may be unspecific or specific for a certain disease.Specific questionnaires provide higher sensitivity and candetect minute changes in HRQL of asthmatic patients. Forthat reason, they are more frequently applied (1).

Health-related quality of life is considered a major out-come of asthma treatment, but the relationship betweenHRQL and morbidity, severity and psychological disordershas not been thoroughly explored among adolescents withasthma.

HRQL reflects how individuals perceive the impact of adisease in their lives and it is expected that adequate controlof the disease results in higher levels of HRQL, as shown bysome studies (7–13). However, most of them have recruitedpatients only from general pediatric clinics, subspecialty clin-ics, and hospitals; and there is a particular lack of studies oneconomically disadvantaged populations.

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QUALITY OF LIFE IN ASTHMATIC ADOLESCENTS 187

Participating adolescents in the epidemiologicalsurvey on prevalence of asthma (ISAAC)

n=3088

Asthmaticsn=551 (17.8%)

Non-asthmaticsn=2537 (82.2%)

Randomly selectedn= 180

Completed the surveyn= 146 (81,1%)

Did not complete the surveyn= 34 (18,9%)

FIGURE 1.—Study flowchart.

The examination of adolescents as a distinct group, apartfrom children and adults, can be justified by several reasons.Adolescence is a phase of emergence of thought and inde-pendent behavior, during which stressful situations are com-monly encountered, which can affect the interpretation ofasthma symptoms and adherence to the prescribed therapy(7).

For all those reasons, the objective of this study is to eval-uate the relative impact of reported symptoms, school absen-teeism, hospital admission, medical visits, and the presenceof emotional and behavioral disorders on the quality of lifeof asthmatic adolescents in a low-income population.

METHODS

Study Design and PopulationThis is a population-based survey in which asthmatic ado-

lescents were randomly selected from public schools in BeloHorizonte/MG, Brazil. Participants were randomly selectedamong 3,088 students from 14 public schools that had par-ticipated in an epidemiological inquiry about prevalence ofasthma in Belo Horizonte/MG, based on the InternationalStudy of Asthma and Allergies in Childhood (ISAAC). Theoperational definition of asthma was a positive answer topresence of wheezing in the past 12 months, in accordancewith the ISAAC questionnaire (14), which has been shownto be a valid instrument to identify asthmatic adolescents insurveys (14–16). Participants identified as asthmatics (n =551) were consecutively numbered and 180 of them werethen randomly drawn from such listing (Figure 1). The Re-search Ethics Committee of the Federal University of MinasGerais approved the protocol, as required.

Evaluation of Morbidity and SeverityAsthma severity was rated according to the Global Initia-

tive for Asthma (GINA) classification (17). The questionsincluded symptom frequency (cough, wheezing or shortnessof breath), presence of nighttime symptoms, limitation for

physical activities, frequency of asthma or bronchitis attacks,and use of reliever medication for asthma. In order to evaluatemorbidity, there were questions about school absenteeism inthe past six months, hospital admission in the past two years,and medical visits in the past 12 months due to asthma, bron-chitis or other respiratory disorders.

Evaluation of Emotional and Behavioral DisordersThe presence of emotional and behavior disorders (EBDs)

was evaluated through the Strengths and Difficulties Ques-tionnaire – SDQ. SDQ contains 25 attributes and each can bescored as “false”, “more or less true” or “true”, respectivelyin a scale ranging from 0 to 2. Scores are added at the end anda sum equaled to 20 or more is considered altered (probablepsychiatric disorder) (18). SDQ was previously validated, isavailable in Portuguese, and is understandable, quickly ad-ministered and well accepted. (18, 19).

Evaluation of Quality of LifeAdolescents answered the Pediatric Asthma Quality of

Life Questionnaire (PAQLQ). The Asthma Quality of LifeQuestionnaire (AQLQ) was one of the first written question-naires used in the evaluation of HRQL of asthmatic adults.Through clinical experience with AQLQ and adaptations,Juniper et al. developed PAQLQ, for children and adoles-cents aged between 7 and 17 years. PAQLQ was validatedand published in 1996 in English, being later validated intwenty other languages, including Portuguese (20, 21). Sev-eral papers validating PAQLQ have been published and ithas proven to be a trustworthy instrument for adolescentswith unstable and stable asthma, in varied degrees of sever-ity (20). PAQLQ has 23 questions divided into 3 domains:activity limitation, symptoms, and emotional function. An-swers are measured according to a 7-point scale, in which 1refers to total impairment and 7 to no impairment at all (20).The final score is the arithmetic average of the sum of pointsin each item. The higher the score is, the higher is the levelof HRQL.

Data was colleted at the schools during class hours. Par-ticipants were invited to present themselves in a classroomdesignated for the research. The main author, in accordancewith Juniper’s orientations, applied all the questionnaires.

Independent VariablesDemographic and socioeconomic characteristics were also

evaluated. The family structure was classified as nuclearwhen both parents resided in the same home as the adoles-cent. The occupation of the head of the family was consideredto be stable when there was a monthly regular income.

Data AnalysisDescriptive statistics were generated using proportions

and means. For the bivariate analysis, variables were di-chotomized according to presence or absence of severity ormorbidity indicators. Other variables included the presenceor absence of EBDs and socioeconomic and demographiccharacteristics. PAQLQ score (variable of interest) was an-alyzed for each intervening variable, and then compared,through the t-test, for average equality purposes. A multi-variate regression analysis was used for the more clinically

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188 C. G. ALVIM ET AL.

TABLE 1.—Sociodemographic characteristics and PAQLQ mean scores.

Mean scoren* (%) (±SD) p-value1

Age14 years 81 (55.48) 5.54 (±1.36)15 years 56 (38.36) 5.78 (±1.27) 0.3116 years 9 (6.16) 6.15 (±1.19)

GenderMale 66 (45.21) 6.06 (±1.07) 0.001Female 80 (54.79) 5.35 (±1.42)

Mother’s schooling level≤4 years 40 (27.40) 5.86 (±1.13) 0.29>4 years 106 (72.60) 5.60 (±1.38)

Father’s schooling level≤4 years 38 (30.40) 5.66 (±1.38) 0.42>4 years 87 (69.60) 5.86 (±1.20)

Family structureNuclear 87 (60.00) 5.81 (±1.28) 0.15Others 58 (40.00) 5.49 (±1.35)

Monthly income per capita<70 dollars 29 (32.22) 5.75 (±1.20) 0.77≥70 dollars 61 (67.78) 5.66 (±1.35)

Head of the family’s occupationStable 123 (86.62) 5.72 (±1.32) 0.14Unstable 19 (13.38) 5.24 (±1.28)

Number of rooms in the house≤6 84 (58.74) 5.76 (±1.22) 0.40>6 59 (41.26) 5.57 (±1.45)

Healthcare service utilizationPrivate 45 (30.82) 5.77 (±1.36) 0.54Public 101 (69.18) 5.63 (±1.30)

1 p-value: t-test for comparison of averages.∗“n” varies due to the response option “I don’t know”.

relevant variables with p-value below 0.25 in the bivariateanalysis.

RESULTS

One hundred and forty-six (81.1%) out of the 180 randomlyselected adolescents agreed to participate in the study. Almost50% of them reported symptoms compatible with persistentasthma. Regarding the use of therapeutic drugs in the past12 months, 28.3% reported the use of bronchodilators, 9.2%recalled the use of systemic steroids, and only 13.2% reporteduse of aerosol medication.

The socio-demographic characteristics of the studied pop-ulation and PAQLQ scores are shown in Table 1. MeanPAQLQ score was 5.7 ± 1.3 standard deviation (SD). Therewas no significant difference regarding sociodemographiccharacteristics to PAQLQ score, except for gender. Girls re-ported worse HRQL, as well as higher frequency of symp-toms, nighttime symptoms, and more EBDs (p < 0.05).

Table 2 relates severity and morbidity indicators and thepresence or absence of EBDs to PAQLQ score. The analysisof the p-values obtained for the comparison of the meansshows significance for all these variables.

In the multivariate regression analysis, the following vari-ables were included: gender, family structure, head of thefamily’s occupation, nighttime symptoms, activity limitation,medical visit in the past 12 months, history of hospital ad-mittance, and presence of EBDs. Frequency of symptoms,presence of four or more asthma attacks in the last year, andschool absenteeism were not included as more than 10% ofthe participants did not know how to answer the question.The final model for this analysis is shown in Table 3. Follow-ing the residual analysis, and considering significance level

TABLE 2.—PAQLQ mean scores according to asthma morbidity, severity andpresence of EBDs.

Mean scoren* (%) (±SD) p-value1

Symptom frequency¶≥ once a week 46 (43.40) 4.74 (±1.27) 0.000< once a week 60 (56.60) 5.86 (±1.23)

Nighttime symptoms¶Present 85 (58.62) 5.05 (±1.26) 0.000Absent 60 (41.38) 6.53 (±0.80)

Activity limitationPresent 76 (52.78) 5.01 (±1.31) 0.000Absent 68 (47.22) 6.39 (±0.87)

Frequency of asthma attacks≥ 4 times a year 10 (10.53) 4.10 (±1.07) 0.000< 4 times a year 85 (89.47) 5.73 (±1.37)

Hospital admission in the past two years#

Yes 13 (8.97) 4.68 (±1.59) 0.004No 132 (91.03) 5.78 (±1.25)

School absenteeism in the past 6 months#

Yes 59 (51.75) 5.00 (±1.32) 0.000No 55 (48.25) 6.03 (±1.19)

Medical visits in the past 12 months#

Yes 55 (38.73) 5.01 (±1.39) 0.000No 87 (61.27) 6.04 (±1.10)

EBDs§Yes 30 (20.55) 4.64 (±1.46) 0.000No 116 (79.45) 5.94 (±1.14)

∗“n” varies due to the response option “I don’t know”.¶cough, wheezing or shortness of breath.# due to asthma, bronchitis other respiratory diseases.§≥20 points on the SDQ.1P-value: T Test for average comparison.

to be 1%, the regression equation of the final model for themultivariate analysis was as follows:

Mean PAQLQ score = 1.88 (Constant)

− 0.42 gender + 1.14 nighttime symptoms

+ 0.69 medical visits in the past 12 months + 0.95 EBDs

Therefore, if the other variables remained constant,PAQLQ score: reduced in 0.42 points for females (p = 0.01);increased in 1.14 when there were no nighttime symptoms(p < 0.01); increased in 0.69 when there was no medicalvisit for respiratory problems within the past 12 months (p <0.01); and increased in 0.95 when no EBDs were present(p < 0.01). This model was able to explain approximatelyhalf of the variation found in PAQLQ score (R-Sq = 49.4%).

DISCUSSION

The present study showed that HRQL of asthmatic adoles-cents is influenced by the complex interaction among several

TABLE 3.—Final model for multivariant regression analysis.

StandardVariable Coefficients error t P

Constant 1.87 0.57 3.29 0.001Gender −0.42 0.16 −2.57 0.011Nighttime symptoms 1.14 0.17 6.71 0.000Medical visits in the past 12 months 0.69 0.17 4.13 0.000EBDs 0.95 0.20 4.79 0.000

S = 0.95 R-Sq = 49.4% R-Sq (adj) = 47.9%.

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QUALITY OF LIFE IN ASTHMATIC ADOLESCENTS 189

factors: the severity of clinical symptoms, morbidity, gender,and the psychological resources available so as to deal withsuch difficulties.

Our results are consistent with a study by Okelo et al.(7), who applied PAQLQ to 185 asthmatic adolescents andobserved that a lower HRQL level was related to lack ofsymptom control, school absenteeism, and medical visits(p < 0.01). Levy et al. also found that symptom severity wasnegatively associated with asthma HRQL in children frompublic housing in Boston (8). Other studies have found similarresults (9–12). On the other hand, Kwok et al. (13), in a studywith 750 children and adolescents, showed a clinically lim-ited association between the classification of asthma severityand HRQL scores (r2 = 0.26). They suggested that isolatedseverity classification has limited value to describe the dis-ease’s global impact on the lives of children and adolescents.

One advantage of our study is that the participants wererandomly selected from schools, avoiding the bias of con-venient selection in health services or the high rates of non-respondents in the case of mailed questionnaires. Other rel-evant result was the possibility of quantifying the impact ofseverity, morbidity, gender, and emotional function on HRQLby means of a regression equation, which is not seen in otherstudies.

The mean PAQLQ score found in the present study wasrelatively high and similar to those described by other au-thors in developed countries (14, 22, 23). It suggests thatHRQL, as evaluated through PAQLQ, is more related to thedisease and its implications than to the socioeconomic con-text in which it is set. Such observation is corroborated bythe absence of association between socioeconomic variablesand PAQLQ score. However, only public schools were in-cluded, which may have represented a homogeneous socioe-conomic status. Van Dellen et al. (24) observed lower levels ofHRQL among immigrants, when compared to non-immigrantasthmatic children and adolescents. This difference was ex-plained by socioeconomic status. Other studies found similarresults, with worse HRQL among families with lower in-come (8,24–26). Another possible explanation for the highmean PAQLQ score is that most participants had intermittentasthma.

The prevalence of EBDs in asthmatic adolescents was high(20.6%) and above the one reported for non-asthmatic ado-lescents (9.0%), as discussed in a previous study (27). The as-sociation between psychopathology and HRQL for asthmaticadolescents was also found in other studies (7, 9, 28). Thereare evidences that the adolescent’s emotional state influencesthe interpretation and the perception of asthma symptoms.(29). The set of behavioral and cognitive responses designedto manage the stressors of a situation, called coping strate-gies, were found to mediate the relation between symptomseverity and HRQL in patients with chronic conditions (29–31). The high prevalence of EBDs may have contributed toan inappropriate coping strategy and to worse HRQL in ourpopulation.

Females presented a lower PAQLQ score, a result thatis compatible with other studies (32–35). According to Os-borne, women react to the disease and express it differentlyfrom men (33). This difference usually means more fre-quent report of symptoms and also more frequent medicalconsultations, and lower levels of HRQL, although this is not

indicative of more severe presentation among females (33).In our study, girls reported both higher levels of HRQL im-pairment and more frequent EBDs and asthma symptoms. Inthe multivariate analysis, gender remained statistically sig-nificant; but the clinical significance is small, as the minimalimportant difference in PAQLQ score is 0.5 (21).

There are potential limitations to the present study. Theoperational definition of asthma is one of them. We chosethe ISAAC questionnaire as a defining criterion for asthma,because it has been applied to more than 700,000 childrenand adolescents in 56 countries, which may make futurecomparisons easier (14). Jenkins et al. (16) compared theISAAC questionnaire to clinical diagnosis by a pneumol-ogist medical doctor in 361 children. They found a sensi-tivity of 85% (IC95%, 73–93%) and a specificity of 81%(IC95%, 76–86%). In addition, by using a more sensitivedefinition for asthma, it was possible to include not onlymoderate or severe forms of the disease, in which there isgeneral consensus about the negative impact on HRQL, butalso mild cases, in which such impact has not been so widelyinvestigated.

As the present study is transversal, it is not possible to statewhether lower HRQL is the cause or an effect of morbidityand severity. Since the questionnaire is specific, i.e., relatedto the impact of asthma on the individual’s life, it is moreprobable that the inadequate control of asthma is the cause forthe deterioration of HRQL. Longitudinal studies are neededin order to clarify whether a better control over asthma wouldresult in HRQL improvement.

The association between HRQL and severity/morbidityhighlights the need for improving the control over the dis-ease. Although almost half of the interviewed adolescentshad persistent symptoms, most did not report use of prophy-lactic medication, and medical visits, hospital admissions andschool absenteeism due to respiratory disorders were com-mon, pointing to lack of adequate disease control. These find-ings suggest that adolescents with asthma are frequently un-dertreated, which may contribute to the negative impact onHRQL.

A careful evaluation of HRQL is essential in order to cap-ture feelings and subjective perceptions, which are not inves-tigated by conventional assessment of asthma control. Theeffect of therapeutic and educational interventions on HRQLcan be assessed along with other clinical, functional and lab-oratorial measurements, in order to provide a broader viewof the disease control. Finally, an attempt to acquire a widerunderstanding is essential in order to identify those adoles-cents who are at higher risk for health care utilization, and todevelop a more comprehensive approach aimed at improvingtheir well being.

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