Hospitalizations for asthma: impact of a program for the control of asthma and allergic rhinitis in Feira de Santana, Brazil

Brandão, Heli Vieira; Cruz, Constança Margarida Sampaio; Santos Junior, Ivan da Silva; Ponte, Eduardo Vieira; Guimarães, Armênio; Cruz, Álvaro Augusto

doi:10.1590/S1806-37132009000800002

Abstracts

OBJECTIVE: To evaluate the impact of the Programa de Controle da Asma e Rinite Alérgica em Feira de Santana (ProAR-FS, Program for the Control of Asthma and Allergic Rhinitis in Feira de Santana) on the frequency of hospitalizations for asthma in patients monitored at a referral center for one year. METHODS: This was a historical control study involving 253 consecutive patients with asthma, ages ranging from 4 to 76 years. We compared the frequency of hospital admissions and visits to the emergency room (ER) in the 12 months prior to and after their admission to the ProAR-FS. During the program, patients received free treatment, including inhaled medications and education on asthma. Demographic and socioeconomic aspects were also assessed. RESULTS: There was a significant reduction in the number of hospitalizations (465 vs. 21) and of visits to the ER (2,473 vs. 184) after their admission to ProAR-FS (p < 0.001 for both). Of the 253 patients who had been hospitalized and had had ER visits within the year prior to the admission to ProAR-FS, only 16 were hospitalized and 92 visited the ER during the follow-up year, representing a reduction of 94% and 64%, respectively. CONCLUSIONS: Implementing a referral center for the treatment of asthma and rhinitis in the Unified Health Care System, with the free distribution of inhaled corticosteroids and the support of an education program, is a highly effective strategy for the control of asthma.

Hospitalization; Asthma; Rhinitis; Health services; Public health

OBJETIVO: Avaliar o impacto do Programa de Controle da Asma e Rinite Alérgica em Feira de Santana (ProAR-FS) na frequência de hospitalizações por asma em pacientes acompanhados por um ano em um centro de referência. MÉTODOS: Estudo de controle histórico de 253 pacientes com asma, entre 4 e 76 anos idade, e admitidos consecutivamente. Comparou-se a frequência de internações e de atendimentos em emergência nos doze meses anteriores e posteriores à sua inclusão no ProAR-FS. Durante o programa, os pacientes receberam atendimento gratuito, incluindo medicação inalatória e educação em asma. Os aspectos demográficos e socioeconômicos também foram avaliados. RESULTADOS: Houve redução significativa no número de internações (463 vs. 21) e de atendimentos em emergência (2.473 vs. 184) após a matrícula no ProAR-FS (p < 0,001 para ambos). Dos 253 pacientes internados e atendidos na emergência no ano anterior à participação no ProAR-FS, apenas 16 foram novamente internados e 92 foram atendidos na emergência durante o ano de acompanhamento, correspondendo a uma redução de 94% e 64%, respectivamente. CONCLUSÕES: A implementação de um ambulatório de referência para o tratamento de asma e rinite no Sistema Público de Saúde, com o fornecimento de corticoide inalatório e o suporte de um programa de educação, é uma estratégia muito efetiva para o controle da asma.

Hospitalização; Asma; Rinite; Serviços de saúde; Saúde pública

ORIGINAL ARTICLE

Hospitalizations for asthma: impact of a program for the control of asthma and allergic rhinitis in Feira de Santana, Brazil^*

Heli Vieira Brandão^I; Constança Margarida Sampaio Cruz^II; Ivan da Silva Santos Junior^III; Eduardo Vieira Ponte^VI; Armênio Guimarães^V; Álvaro Augusto Cruz^VI

^IAssistant Professor. Department of Pediatrics, Feira de Santana State University, Feira de Santana, Brazil

^IIAdjunct professor. Graduate Course in Medicine and Human Health. Bahia School of Medicine and Public Health, Salvador, Brazil

^IIIPhysician. Bahia State Health Department, Salvador, Brazil

^VIPhysician. Program for the Control of Asthma and Allergic Rhinitis, Feira de Santana, Brazil

^VFull Professor. Graduate Course in Medicine and Human Health. Bahia School of Medicine and Public Health, Salvador, Brazil

^VIAdjunct Professor. Federal University of Bahia School of Medicine, Salvador, Brazil

Correspondence to

ABSTRACT

OBJECTIVE: To evaluate the impact of the Programa de Controle da Asma e Rinite Alérgica em Feira de Santana (ProAR-FS, Program for the Control of Asthma and Allergic Rhinitis in Feira de Santana) on the frequency of hospitalizations for asthma in patients monitored at a referral center for one year.

METHODS: This was a historical control study involving 253 consecutive patients with asthma, ages ranging from 4 to 76 years. We compared the frequency of hospital admissions and visits to the emergency room (ER) in the 12 months prior to and after their admission to the ProAR-FS. During the program, patients received free treatment, including inhaled medications and education on asthma. Demographic and socioeconomic aspects were also assessed.

RESULTS: There was a significant reduction in the number of hospitalizations (465 vs. 21) and of visits to the ER (2,473 vs. 184) after their admission to ProAR-FS (p < 0.001 for both). Of the 253 patients who had been hospitalized and had had ER visits within the year prior to the admission to ProAR-FS, only 16 were hospitalized and 92 visited the ER during the follow-up year, representing a reduction of 94% and 64%, respectively.

CONCLUSIONS: Implementing a referral center for the treatment of asthma and rhinitis in the Unified Health Care System, with the free distribution of inhaled corticosteroids and the support of an education program, is a highly effective strategy for the control of asthma.

Keywords: Hospitalization; Asthma; Rhinitis; Health services; Public health.

Introduction

Frequent hospitalizations for asthma reflect elevated morbidity and indicate a relevant public health problem.^(1,2)The lack of appropriate control of the disease has led to an increased number of emergency room visits, hospitalizations and deaths. Appropriate asthma treatment, with the use of inhaled corticosteroids, allows the control of the disease and avoids exacerbations, hospitalizations and deaths.^(3,4)Studies show that there is still a lack of strategies and planning in public policies related to asthma outpatient care within the Brazilian Unified Health Care System,^(5,6)which has disastrous consequences for the health care system and for the patients.

Despite of the unfavorable scenario, health programs have reduced the number of hospitalizations for asthma attack, by offering appropriate diagnostic and therapeutic approach, complemented by educational activity and rehabilitation measures.^(7,12)Education programs on asthma associated to medication represent one of the pillars of the success of the effectiveness of the asthma program and have been proven to reduce exacerbations and hospitalizations for asthma, as well as reducing the expenses with the disease.⁽¹³⁾The Programa de Controle da Asma e Rinite Alérgica em Feira de Santana (ProAR-FS, Program for the Control of Asthma and Allergic Rhinitis in the city of Feira de Santana, Brazil) was evaluated using data from the Information Technology Department of the Unified Health Care System after the first year of the program in the city, and a reduction of 42% in hospitalizations for asthma was observed.⁽¹²⁾

The present study aimed at evaluating the impact of the implementation of the ProAR-FS on hospitalizations for asthma in patients monitored for a year in the referral center of the program.

Methods

Implemented in 2004, ProAR-FS has offered inhaled medication free of charge and an asthma education program to the asthma patient, as well as training to health professionals, with the objective of providing control of mild and moderate asthma in the primary health care clinics and in the Family Health Program. Severe asthma patients are referred to a referral center, where they received specialized monitoring and treatment.

This was an observational, longitudinal, retrospective and prospective study with historical controls. The same patients were used in order to evaluate the effectiveness of the medical care provided to the asthma patient by comparing data related to the number of emergency room visits for asthma attacks and to the number of hospitalizations in the 12 months preceding the monitoring in the ProAR-FS with the number of hospitalizations and emergency room visits in the 12 months following enrollment in the ProAR-FS. We evaluated all 253 consecutive patients who were residents of Feira de Santana and were admitted to the referral center.

Patients diagnosed with asthma who had been hospitalized for an asthma attack at least once in the 12 months preceding admission to the program were included. Smokers and patients with a pulmonary disease other than asthma were excluded. The patients were monitored for a period of 12 months.

Data referring to the period preceding admission to the referral center in Feira de Santana were obtained retrospectively according to the standardized treatment protocol implemented upon the foundation of the outpatient clinic. During the 12 months of prospective monitoring, specific questionnaires of the study were applied, with questions related to the following aspects: demographic data (gender, age at admission to the program, place of birth and residence); socioeconomic status (family income and level of education); anthropometric data (weight, height); asthma history (age at first attack, severity and frequency of hospitalizations/emergency room visits in the 12 months preceding admission to the outpatient clinic); medical care (use of prophylactic medication, number of follow-up visits during monitoring and respiratory therapy); and overall health status (including comorbidities, such as allergic rhinitis, arterial hypertension and diabetes).

The diagnosis and classification of asthma severity were carried out by a pulmonologist at the first ProAR-FS patient visit and were performed according to the Global Initiative for Asthma criteria.⁽¹⁴⁾The diagnosis of allergic rhinitis was made based in the criteria established in the World Health Organization "Allergic Rhinitis and its Impact on Asthma" workshop.⁽¹⁵⁾Severe asthma was characterized by the following criteria: continuous daytime symptoms and nearly daily nighttime symptoms; limitation of activities; frequent exacerbations; and FEV₁or PEF < 60% of predicted.⁽¹⁶⁾

During the 12-month monitoring period, a standard outpatient form was used in order to obtain data related to emergency room visits and hospitalizations for asthma. Patients with severe rhinitis were referred to an otolaryngologist. All of the patients monitored (or their parents) were included in an asthma education program, which provides information on the disease, its triggering factors, the appropriate use of medications, the identification of attacks and the use of an action plan for asthma exacerbations. Patients with moderate or severe asthma were referred to a physical therapist, who aided them in the performance of lung deflation maneuvers and in the appropriate use of the respiratory muscles, as well as giving them a refresher course in the correct use of the inhaled medication. Medication for asthma and allergic rhinitis were dispensed at the treatment facility and consisted of inhaled corticosteroids (beclomethasone or budesonide), bronchodilators (albuterol or formoterol), topical nasal corticosteroids (beclomethasone or budesonide), antihistamines and oral corticosteroids, in the doses recommended by the attending physician. The medication was distributed via the pharmacy, after the completion of a form containing identification, type of medication, date, quantity dispensed, and the subsequent units dispensed upon the return of the empty flask.

The project was approved by the Research Ethics Committee of the Bahia Foundation for Science Development.

Statistical analysis

For the calculation of the sample, we used PEPI (Sagebush Press, Salt Lake City, UT, USA). The study indicators of the benefit of the intervention were measured by the comparison of the frequencies and the absolute numbers of hospitalizations and emergency room visits within the 12 months prior to and following the monitoring at the ProAR-FS referral center. In order to compare the frequencies and the absolute numbers of hospitalizations and emergency room visits before and after the ProAR-FS, we used McNemar's test and Wilcoxon test, respectively. Statistical analyses were carried out using the Statistical Package for the Social Sciences, version 14.0 (SPSS Inc., Chicago, IL, USA).

Results

Demographic and clinical characteristics of the population are shown in Table 1. The sample comprised 253 patients (107 children, 44 adolescents and 102 adults). The male/female ratio among the children and adolescents was 2.6:1 (63.6% vs. 36.4%), whereas, among the adults, females predominated at a ratio of 4:1 (80.4% vs. 19.6%). The majority (78.2%) of the adult asthma patients had at least 9 years of schooling, as did most (64.7%) of the mothers of the children and adolescents evaluated. Family incomes were typically low, being less than or equal to the national minimum wage in 75.5% of the cases. Severe asthma was significantly more common in adults (66.7%), and only 7.5% of the patients had used inhaled corticosteroid prior to enrolling in the program. There were 219 patients (86.3%) who presented with concomitant allergic rhinitis/asthma, and 139 (63.5%) of those patients used medication for the treatment of rhinitis (a topical nasal corticosteroid or an antihistamine).

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All 253 patients had been hospitalized and had visited the emergency room for an asthma attack before enrollment in the ProAR-FS. The decrease in the number of hospitalizations was 95.5% (465 vs. 21), and the decrease in the number of emergency room visits was 92.6% (2,473 vs. 184). There was a significant decrease in the number of hospitalizations and emergency room visits, regardless of patient age (p < 0.001; Table 2). We also observed a significant decrease in the number of hospitalizations and emergency room visits, regardless of the degree of asthma severity, hospitalizations for asthma dropping from 215 to 13 and emergency room visits dropping from 1,515 to 116 (p < 0.001; Table 3). In a patient-by-patient analysis of the study period, we found that, of the 253 patients who had been hospitalized or treated in the emergency room in the 12 months preceding enrollment in the ProAR-FS, only 16 were hospitalized and 96 visited the emergency room, which represents a decrease of 93.7% and 62.1%, respectively (p < 0.001).

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Discussion

The decrease in hospitalizations for asthma is the principal goal of asthma control programs. Previous experiences in some countries, including Brazil, indicate that the access to treatment offered by programs of this nature reduces the number of hospitalizations.^(9-12)In one study, it was demonstrated that appropriate asthma patient treatment policies can reduce the rates of asthma-related mortality.⁽¹⁷⁾In the present study, we observed a considerable decrease in the number of hospitalizations and emergency room visits in the 12 months following enrollment in the ProAR-FS, in all age brackets, reflecting the great impact that appropriate management has the control of the asthma symptoms.

The limited access to appropriate medication and the irregular monitoring of asthma patients within the Unified Health Care System have been implicated in the overuse of the emergency room and the great number of hospitalizations for asthma. In the present study, the percentage of patients using inhaled corticosteroids for asthma control before enrollment in the ProAR-FS (7.5%) was lower than that observed in other national studies.^(5,18)After the medication for asthma and rhinitis came to be distributed free of charge, the proportion of patients using inhaled corticosteroid increased to 94.7%, contributing to a 94.0% decrease in hospitalizations, a value similar to that found in a case-control study involving children with asthma using inhaled corticosteroid and enrolled in an asthma education program.⁽¹⁹⁾One of the differences between the ProAR-FS and other asthma control programs is the concomitant treatment of rhinitis (providing patients with topical nasal corticosteroids), as well as the fact that the ProAR-FS serves all age brackets and treats all patients with asthma or rhinitis, regardless of the degree of severity.

In this study, the combination of asthma and allergic rhinitis was seen in over 80% of the patients in the two age brackets, which is in accordance with studies indicating that nasal symptoms occur in 30-80% of all patients with asthma and in up to 99% of those who are atopic.⁽²⁰⁾Studies have shown that rhinitis and asthma are interrelated, and that the appropriate treatment of allergic rhinitis improves asthma control, decreasing symptoms and reducing the risk of emergency room visits and hospitalizations.^(21-25)Indeed, 35 children in the ProAR-FS with mild asthma (23.6% of the sample of children and adolescents) and persistent rhinitis, using exclusively nasal corticosteroid, were not hospitalized, and there was a decrease of 84.2% in the frequency of emergency room visits during monitoring in the ProAR-FS. Scientific evidence suggests that treatment of rhinitis with topical nasal corticosteroids prevents bronchial hyper-responsiveness associated with the exposure to allergens and can avoid the exacerbations of symptoms in patients with mild asthma.⁽²³⁾

Another important observation of our study was the predominance of hospitalizations among male children and among female adults. Although there was predominance of hospitalizations among female adults, there was no statistically significant difference between the two genders in terms of the number of hospitalizations during the ProAR-FS monitoring period. Another important point is the great positive impact this program has had on a region in which the majority of resident have no more than 9 years of schooling and family incomes rarely surpass the national minimal wage, establishing its efficiency and its feasibility among those who most need support from health policies.

The present study had a retrospective component, being subject to memory and measurement biases in relation to the events that occurred before enrollment in the ProAR-FS, as well as to biases common to interventional observational studies, due to the lack of control of other potentially confounding variables, such as in randomized clinical trials. However, we attempted to verify the verbal information on the basis of the hospital discharge register.

We conclude that the activities at the outpatient clinic of the ProAR-FS referral center, with the care of the health team, distribution of nasal and inhaled corticosteroids, in combination with an asthma education program for patients and their relatives, was associated with a pronounced decrease in the use of health resources due to asthma in an cohort of outpatients with a history of hospitalization.

Acknowledgments

We wish to thank the Feira de Santana Municipal Department of Health, the State Coordination of the ProAR in Bahia and the professionals at the referral center: Vera Gardênia Ferreira, Camila Portugal, Daniela do Amaral, Isabela Caribé, Fabiana Dias, Rosa Argentina Sarkis, Luciana Alves Amorim, Maria Raimunda Palmeira, Edgar Adolfo Costa and Murilo Cerqueira.

References

1. Bousquet J, Bousquet PJ, Godard P, Daures JP. The public health implications of asthma. Bull World Health Organ. 2005;83(7):548-54.
2. Blais L, Suissa S, Boivin JF, Ernst P. First treatment with inhaled corticosteroids and the prevention of admissions to hospital for asthma. Thorax. 1998;53(12):1025-9.
3. Suissa S, Ernst P. Inhaled corticosteroids: impact on asthma morbidity and mortality. J Allergy Clin Immunol. 2001;107(6):937-44.
4. Björ O, Bråbäck L. A retrospective population based trend analysis on hospital admissions for lower respiratory illness among Swedish children from 1987 to 2000. BMC Public Health. 2003;3:22.
5. Sarinho E, Queiroz GR, Dias ML, Silva AJ. Asthma-related hospitalizations and lack of outpatient follow-up treatment. J Bras Pneumolol. 2007;33(4):365-71.
6. Rio EM, Galo PR, Siqueira AA. Mortalidade por asma no Município de São Paulo, Brasil. Rev Saude Publica. 2002;36(2):149-54.
7. Haahtela T, Tuomisto LE, Pietinalho A, Klaukka T, Erhola M, Kaila M, et al. A 10 year asthma programme in Finland: major change for the better. Thorax. 2006;61(8):663-70.
8. Ventura RN, Naspitz C, Puccini RF, Silva EM. Avaliação do programa de atenção a crianças asmáticas acompanhadas nas unidades de saúde do Município do Embu, São Paulo, no período de 1988 a 1993. Cad Saude Publica. 1998;14(1):117-28.
9. Ponte E, Franco RA, Machado AS, Machado CS, Cruz AA. Impact that a program to control severe asthma has on the use of Unified Health System resources in Brazil. J Bras Pneumol. 2007;33(1):15-9.
10. Lasmar LM, Calazans GC, Fontes MJ, Camargos PA. Programa Criança que Chia - Belo Horizonte - MG - Experiência Mineira com um Programa Municipal de Atendimento a Criança Asmática. In: Cerci Neto A, editor. Asma em Saúde Pública. Barueri: Manole; 2007. p. 93-101
11. Cerci Neto A, Ferreira-Filho OF, Bueno T, Talhari MA. Reduction in the number of asthma-related hospital admissions after the implementation of a multidisciplinary asthma control program in the city of Londrina, Brazil. J Bras Pneumol. 2008;34(9):639-45.
12. Cruz AA, Moreira E, Brandão HV, Silva-Junior I. Programa de Controle da Asma e Rinite Alérgica de Feira de Santana ProAR-FS. In: Cerci Neto A, editor. Asma em Saúde Pública. Barueri: Manole; 2007. p. 133-9.
13. Oliveira MA, Muniz MT, Santos LA, Faresin SN, Fernandes AL. Custo-efetividade de programa de educação para adultos asmáticos atendidos em hospital-escola de instituição pública. J Pneumol. 2002;28(2):71-6.
¹⁴
Global Initiative for Asthma - GINA [homepage on the Internet]. Bethesda: National Heart, Lung and Blood Institute. National Institutes of Health, US Department of Health and Human Services; c2000 [updated 2007 Sep; cited 2008 Dec 2]. Available from: http://www.ginasthma.org
» link
15. Bousquet J, Van Cauwenberge P, Khaltaev N; Aria Workshop Group; World Health Organization. Allergic rhinitis and its impact on asthma. J Allergy Clin Immunol. 2001;108(5 Suppl):S147-334.
16. Sociedade Brasileira de Pneumologia e Tisiologia. IV Diretrizes Brasileiras para o Manejo da Asma. J Pneumol. 2006;32(Suppl 7):447-74.
17. Sin DD, Tu JV. Inhaled corticosteroid therapy reduces the risk of rehospitalization and all-cause mortality in elderly asthmatics. Eur Respir J. 2001;17(3):380-5.
18. Lasmr LM, Camargos PA, Goulart EM, Sakurai E. Risk factors for multiple hospital admissions among children and adolescents with asthma. J Bras Pneumol. 2006;32(5):391-9.
19. Cabral AL, Carvalho WA, Chinen M, Barbiroto RM, Boueri FM, Martins MA. Are International Asthma Guidelines effective for low-income Brazilian children with asthma? Eur Respir J. 1998;12(1):35-40.
20. Sears MR, Burrows B, Flannery EM, Herbison GP, Holdaway MD. Atopy in childhood. I. Gender and allergen related risks for development of hay fever and asthma. Clin Exp Allergy. 1993;23(11):941-8.
21. Lasmar LM, Camargos PA, Ordones AB, Gaspar GR, Campos EG, Ribeiro GA. Prevalence of allergic rhinitis and its impact on the use of emergency care services in a group of children and adolescents with moderate to severe persistent asthma. J Pediatr (Rio J). 2007;83(6):555-61.
22. Cruz AA, Popov T, Pawankar R, Annesi-Maesano I, Fokkens W, Kemp J, et al. Common characteristics of upper and lower airways in rhinitis and asthma: ARIA update, in collaboration with GA(2)LEN. Allergy. 2007;62 Suppl 84:1-41.
23. Corren J, Manning BE, Thompson SF, Hennessy S, Strom BL. Rhinitis therapy and the prevention of hospital care for asthma: a case-control study. Allergy Clin Immunol. 2004;113(3):415-9.
24. Crystal-Peters J, Neslusan C, Crown WH, Torres A. Treating allergic rhinitis in patients with comorbid asthma: the risk of asthma-related hospitalizations and emergency department visits. J Allergy Clin Immunol. 2002;109(1):57-62.
25. Adams RJ, Fuhlbrigge AL, Finkelstein JA, Weiss ST. Intranasal steroids and the risk of emergency department visits for asthma. J Allergy Clin Immunol. 2002;109(4):636-42.

Endereço para correspondência:

Heli Vieira Brandão

Rua Milão, 742

CEP 44062-170 Feira de Santana, BA, Brasil

Tel 55 75 3221-9331

E-mail:

helivb@terra.com.br

*

Trabalho realizado na Fundação Bahiana para Desenvolvimento das Ciências, Salvador (BA) Brasil.

Publication Dates

Publication in this collection
09 Sept 2009
Date of issue
Aug 2009

History

Accepted
17 Mar 2009
Received
02 Dec 2008

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] 1. Bousquet J, Bousquet PJ, Godard P, Daures JP. The public health implications of asthma. Bull World Health Organ. 2005;83(7):548-54.

[2] 2. Blais L, Suissa S, Boivin JF, Ernst P. First treatment with inhaled corticosteroids and the prevention of admissions to hospital for asthma. Thorax. 1998;53(12):1025-9.

[3] 3. Suissa S, Ernst P. Inhaled corticosteroids: impact on asthma morbidity and mortality. J Allergy Clin Immunol. 2001;107(6):937-44.

[4] 4. Björ O, Bråbäck L. A retrospective population based trend analysis on hospital admissions for lower respiratory illness among Swedish children from 1987 to 2000. BMC Public Health. 2003;3:22.

[5] 5. Sarinho E, Queiroz GR, Dias ML, Silva AJ. Asthma-related hospitalizations and lack of outpatient follow-up treatment. J Bras Pneumolol. 2007;33(4):365-71.

[6] 6. Rio EM, Galo PR, Siqueira AA. Mortalidade por asma no Município de São Paulo, Brasil. Rev Saude Publica. 2002;36(2):149-54.

[7] 7. Haahtela T, Tuomisto LE, Pietinalho A, Klaukka T, Erhola M, Kaila M, et al. A 10 year asthma programme in Finland: major change for the better. Thorax. 2006;61(8):663-70.

[8] 8. Ventura RN, Naspitz C, Puccini RF, Silva EM. Avaliação do programa de atenção a crianças asmáticas acompanhadas nas unidades de saúde do Município do Embu, São Paulo, no período de 1988 a 1993. Cad Saude Publica. 1998;14(1):117-28.

[9] 9. Ponte E, Franco RA, Machado AS, Machado CS, Cruz AA. Impact that a program to control severe asthma has on the use of Unified Health System resources in Brazil. J Bras Pneumol. 2007;33(1):15-9.

[10] 10. Lasmar LM, Calazans GC, Fontes MJ, Camargos PA. Programa Criança que Chia - Belo Horizonte - MG - Experiência Mineira com um Programa Municipal de Atendimento a Criança Asmática. In: Cerci Neto A, editor. Asma em Saúde Pública. Barueri: Manole; 2007. p. 93-101

[11] 11. Cerci Neto A, Ferreira-Filho OF, Bueno T, Talhari MA. Reduction in the number of asthma-related hospital admissions after the implementation of a multidisciplinary asthma control program in the city of Londrina, Brazil. J Bras Pneumol. 2008;34(9):639-45.

[12] 12. Cruz AA, Moreira E, Brandão HV, Silva-Junior I. Programa de Controle da Asma e Rinite Alérgica de Feira de Santana ProAR-FS. In: Cerci Neto A, editor. Asma em Saúde Pública. Barueri: Manole; 2007. p. 133-9.

[13] 13. Oliveira MA, Muniz MT, Santos LA, Faresin SN, Fernandes AL. Custo-efetividade de programa de educação para adultos asmáticos atendidos em hospital-escola de instituição pública. J Pneumol. 2002;28(2):71-6.

[14] ¹⁴
Global Initiative for Asthma - GINA [homepage on the Internet]. Bethesda: National Heart, Lung and Blood Institute. National Institutes of Health, US Department of Health and Human Services; c2000 [updated 2007 Sep; cited 2008 Dec 2]. Available from: http://www.ginasthma.org
» link

[15] 15. Bousquet J, Van Cauwenberge P, Khaltaev N; Aria Workshop Group; World Health Organization. Allergic rhinitis and its impact on asthma. J Allergy Clin Immunol. 2001;108(5 Suppl):S147-334.

[16] 16. Sociedade Brasileira de Pneumologia e Tisiologia. IV Diretrizes Brasileiras para o Manejo da Asma. J Pneumol. 2006;32(Suppl 7):447-74.

[17] 17. Sin DD, Tu JV. Inhaled corticosteroid therapy reduces the risk of rehospitalization and all-cause mortality in elderly asthmatics. Eur Respir J. 2001;17(3):380-5.

[18] 18. Lasmr LM, Camargos PA, Goulart EM, Sakurai E. Risk factors for multiple hospital admissions among children and adolescents with asthma. J Bras Pneumol. 2006;32(5):391-9.

[19] 19. Cabral AL, Carvalho WA, Chinen M, Barbiroto RM, Boueri FM, Martins MA. Are International Asthma Guidelines effective for low-income Brazilian children with asthma? Eur Respir J. 1998;12(1):35-40.

[20] 20. Sears MR, Burrows B, Flannery EM, Herbison GP, Holdaway MD. Atopy in childhood. I. Gender and allergen related risks for development of hay fever and asthma. Clin Exp Allergy. 1993;23(11):941-8.

[21] 21. Lasmar LM, Camargos PA, Ordones AB, Gaspar GR, Campos EG, Ribeiro GA. Prevalence of allergic rhinitis and its impact on the use of emergency care services in a group of children and adolescents with moderate to severe persistent asthma. J Pediatr (Rio J). 2007;83(6):555-61.

[22] 22. Cruz AA, Popov T, Pawankar R, Annesi-Maesano I, Fokkens W, Kemp J, et al. Common characteristics of upper and lower airways in rhinitis and asthma: ARIA update, in collaboration with GA(2)LEN. Allergy. 2007;62 Suppl 84:1-41.

[23] 23. Corren J, Manning BE, Thompson SF, Hennessy S, Strom BL. Rhinitis therapy and the prevention of hospital care for asthma: a case-control study. Allergy Clin Immunol. 2004;113(3):415-9.

[24] 24. Crystal-Peters J, Neslusan C, Crown WH, Torres A. Treating allergic rhinitis in patients with comorbid asthma: the risk of asthma-related hospitalizations and emergency department visits. J Allergy Clin Immunol. 2002;109(1):57-62.

[25] 25. Adams RJ, Fuhlbrigge AL, Finkelstein JA, Weiss ST. Intranasal steroids and the risk of emergency department visits for asthma. J Allergy Clin Immunol. 2002;109(4):636-42.