|Year : 2016 | Volume
| Issue : 6 | Page : 339-346
Quality of acute asthma care in two tertiary hospitals in a state in South Western Nigeria: A report of clinical audit
Olufemi Olumuyiwa Desalu1, Adekunle Olatayo Adeoti2, Olarinde Jeffrey Ogunmola3, Joseph Olusesan Fadare4, Tolutope Fasanmi Kolawole3
1 Department of Medicine, University of Ilorin Teaching Hospital, Ilorin, Nigeria
2 Department of Medicine, Ekiti State University Teaching Hospital, Ado-Ekiti, Nigeria
3 Department of Medicine, Federal Teaching Hospital, Ido-Ekiti, Nigeria
4 Department of Pharmacology, Ekiti State University Teaching Hospital, Ado-Ekiti, Nigeria
|Date of Web Publication||11-Nov-2016|
Olufemi Olumuyiwa Desalu
Department of Medicine, University of Ilorin Teaching Hospital, PMB 1459, Ilorin, Kwara State
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: To audit the quality of acute asthma care in two tertiary hospitals in a state in the southwestern region of Nigeria and to compare the clinical practice against the recommendations of the Global Initiative for Asthma (GINA) guideline. Patients and Methods: We carried out a retrospective analysis of 101 patients who presented with acute exacerbation of asthma to the hospital between November 2010 and October 2015. Results: Majority of the cases were females (66.3%), <45 years of age (60.4%), and admitted in the wet season (64.4%). The median duration of hospital stay was 2 days (interquartile range; 1-3 days) and the mortality was 1.0%. At admission, 73 (72.3%) patients had their triggering factors documented and 33 (32.7%) had their severity assessed. Smoking status, medication adherence, serial oxygen saturation, and peak expiratory flow rate measurement were documented in less than half of the cases, respectively. Seventy-six (75.2%) patients had nebulized salbutamol, 89 (88.1%) had systemic corticosteroid, and 78 (77.2%) had within 1 h. On discharge, 68 (67.3%) patients were given follow-up appointment and 32 (31.7%) were reviewed within 30 days after discharge. Less than half were prescribed an inhaled corticosteroid (ICS), a self-management plan, or had their inhaler technique reviewed or controller medications adjusted. Overall, adherence to the GINA guideline was not satisfactory and was very poor among the medical officers. Conclusion: The quality of acute asthma care in our setting is not satisfactory, and there is a low level of compliance with most recommendations of asthma guidelines. This audit has implicated the need to address the non-performing areas and organizational issues to improve the quality of care.
Keywords: Asthma, audit, emergencies, guidelines, management
|How to cite this article:|
Desalu OO, Adeoti AO, Ogunmola OJ, Fadare JO, Kolawole TF. Quality of acute asthma care in two tertiary hospitals in a state in South Western Nigeria: A report of clinical audit. Niger Med J 2016;57:339-46
|How to cite this URL:|
Desalu OO, Adeoti AO, Ogunmola OJ, Fadare JO, Kolawole TF. Quality of acute asthma care in two tertiary hospitals in a state in South Western Nigeria: A report of clinical audit. Niger Med J [serial online] 2016 [cited 2017 Sep 21];57:339-46. Available from: http://www.nigeriamedj.com/text.asp?2016/57/6/339/193860
| Introduction|| |
Asthma affects about 235 million people worldwide.  The incidence of asthma has been growing over the past 30 years due to changing environmental factors, greater awareness of this condition, and changes in diagnostic practice, particularly in the low- and middle-income countries that are least able to absorb its impact. , Fifty years ago, asthma was uncommon in Nigeria; however, recent reports from different parts of Nigeria have shown a prevalence of adolescent and adult asthma in excess of 10%. ,, Data reported from phases 1 and 3 of the International Study of Asthma and Allergies in Childhood found a rising trend in the prevalence of asthma.  Asthma causes an estimated 250,000 deaths annually (1 in 250 deaths worldwide).  Asthma is also the second leading cause of respiratory disease-related morbidity and third leading cause of respiratory disease-related emergency room visit and mortality within 24 h of admission in Ekiti State, Southwestern Nigeria. , Smith et al. reported that a substantial proportion of the direct costs of asthma in the USA are due to hospitalization and emergency department (ED) visits.  Several national and international thoracic societies have produced the management guidelines to standardize asthma care and achieve the goals of therapy. , In Nigeria, there is no national asthma treatment guideline , and most asthma care providers rely on the Global Initiative for Asthma (GINA) guideline which is a Global Strategy for Asthma Management and Prevention, developed by the World Health Organization and the National Heart, Lung, and Blood Institute. The guideline was issued in 1995 and regularly revised to date.  Despite the effort to standardize asthma care using the GINA guideline, several Nigerian studies dating back to more than a decade have shown that there is under-treatment of asthma and poor adherence to the guideline by doctors. ,,,,, The reduction of burden and outcome of asthma depend largely on achieving asthma control, adequate prevention, and treatment of an acute attack. It is therefore important to assess the adequacy of such treatment in our practice and plan changes to improve care; hence, the need for a clinical audit. To the best of our knowledge, there is only one study on clinical audit of acute asthma in the emergency room in Nigeria, which was done in the pediatric age group  and none in the adult population. Assessment of the quality of asthma care in developing countries is imperative because of its increasing prevalence, huge socioeconomic and psychosocial burden, and under-treatment, which leaves much room for improvement.  This study was carried out to audit the quality of acute asthma care in two tertiary hospitals in a state in the southwestern region of Nigeria and compare the clinical practice against the GINA guidelines.
| Methods|| |
This study was a retrospective analysis of 101 patients who presented with acute exacerbation of asthma to the hospital between November 2010 and October 2015 carried out at two tertiary hospitals in Southwestern Nigeria. The hospitals serve as a referral hospital for the state and its adjoining states. These hospitals also provide an internship and postgraduate training programs in both internal and family medicine. The hospitals have consultant pulmonologist who runs the pulmonary clinic, resident doctors, and several other internists. In terms of infrastructure, both centers have desktop spirometers, pulse oximeters, peak flow meters, and intensive care units. In addition, they provide a combination of primary, secondary, and tertiary health-care services. This is because they have departments of family medicine and community medicine that provide primary health care (PHC).
Asthma patients presenting with attack were previously receiving their care in PHC/private hospital in the state, some were known patients of the hospitals, while some were newly diagnosed cases presenting with acute asthma. They were seen on the first contact by casualty/medical officers, residents in family, and internal medicine undergoing emergency clerkship rotation. The attending doctor in the casualty evaluates, institutes therapy and discharges the patient when the condition has improved or referred to the internist for further treatment. The internists then referred the patient to the pulmonologist after discharge for follow-up or seek an urgent pulmonology consult depending on the severity of the disease, patients' preference, and associated comorbidity.
We retrieved and reviewed the medical case files of all the patients who had a clinical diagnosis of asthma in the two hospitals. The cases that had complete information and met the clinical criteria for diagnosis of acute exacerbation of asthma were studied. Nine cases of chronic obstructive pulmonary disease (COPD) and one case of asthma-COPD overlap syndrome (ACOS ) were excluded from the chart review. An audit proforma was used to collect (1) sociodemographic information, (2) clinical profile: Clinical features, month and season of admission, comorbid conditions, emergent investigations and asthma medications, duration of hospitalization, outcome of management, (3) standard of care recommended by GINA. 
The GINA guidelines specify that the initial assessment on admission should (1) include functional assessments such as spirometry, peak expiratory flow (PEF) measurement, and oxygen saturation measurements with oximetry and (2) assess the severity of an asthma exacerbation using brief history and physical examination pertinent to the exacerbation and functional assessments. Such assessments are recommended to be repeated 1 h after the initial treatment and then at 1-2-h intervals until there is a clear response to the treatment and a decision is reached about the patient clinical state. The GINA guidelines also recommended the following treatments: (1) Supplemental oxygen therapy, (2) repeated administration of rapid-acting inhaled β2-agonists with or without an anticholinergic before the use of theophylline, (3) systemic glucocorticosteroids in all but the mildest exacerbations, and (4) discouraging the use of sedatives and anxiolytics. On discharge, the care of patients should include (1) a minimum 3-7-days course of oral corticosteroids (OCSs); (2) initial or continued use of controller therapy; (3) review of inhaler technique and use of peak flow meter; (4) identification of potential triggers of exacerbations; (5) provision of a written action plan for prevention of future exacerbations; (6) encouragement to contact a physician within 1 week after discharge for a follow-up appointment.
In medicolegal term, the absence of documentation implies the absence of process in data collection.
Asthma was defined by the history of variable respiratory symptoms such as wheeze, shortness of breath, chest tightness, and cough and airflow limitation that has an immediate response to bronchodilator (BD) or to inhaled corticosteroids (ICSs) over week. In addition, presence of family history of asthma, and other allergic conditions (allergic rhinitis or eczema) 
Exacerbations of asthma (asthma attacks or acute asthma) were defined as episodes of progressive increase in shortness of breath, cough, wheezing, or chest tightness, or some combination of these symptoms and decrease in lung function (PEF or forced expiratory volume in 1 second [FEV1]) from the patient's usual status. 
Asthma-chronic obstructive pulmonary disease overlap syndrome was defined as persistent airflow limitation with several features usually associated with asthma and several features usually associated with COPD. 
The data were analyzed using the Statistical Package for the Social Sciences (SPSS), version 17 (SPSS Inc., Chicago, IL, USA). Results were expressed for all cases in the audit, usually as percentages for the variables of interest. Chi-square test was used to test for statistical significance between categorical variables. A P < 0.05 was considered statistically significant.
| Results|| |
A total of 111 patients were admitted during the study period, of which only 101 patients met the GINA diagnostic criteria. The age of the patients ranged from 16 to 85 years, with a mean age of 43 ± 19 years. Sixty-one (60.4%) of the asthma patients were aged <45 years, and 67 (66.3%) were females with a male to female ratio of 1:2. Fifty-one (50.5%) patients were diagnosed to have asthma for a duration <5 years. Sixty-two (61.4%) patients were admitted at night and 65 (64.4%) were admitted in the rainy (cold) season. Only 8 (7.9%) patients were regularly using ICS and 69 (68.3%) were not on any medication before admission. Almost 60% of the patients were admitted and managed by the casualty officer while 16 (15.8%) were managed by the internist. The median duration of illness before the presentation was 3 days (interquartile range [IQR]; 2-6 days) and the median length of hospital stay was 2 days (IQR; 1-3 days) and the mortality was 1.0%. The other characteristics of the patients are shown in [Table 1].
At admission, assessment of severity of attack was performed in 33 (32.7%) patients, smoking status recorded in 30 (29.7%), attack triggering factors documented in 73 (72.3%), and level of drug adherence recorded in 18 (17.8%). The oxygen saturation of the patients at admission was measured in 5 (5.0%) and continuous or serial oxygen saturation was measured in 5 (5.0%) of the patients. Six (5.9%) patients had peak expiratory flow rate (PEFR) measured at admission, and none had their post-BD PEFR measured after nebulization or intravenous medication. Chest radiography was performed in 16 (15.8%) of the patients [Table 2].
Nebulized salbutamol was the initial BD used for attack in the 76 (75.2%) of patients and the remaining had intravenous theophylline. For airway inflammation, 89 (88.1%) patients were given a corticosteroid (CS), with 29 (28.7%) receiving optimal CSs dose, 75 (74.3%) had intravenous corticosteroid and within 1 h, respectively. OCS was given to 61 (60.4%) patients and 23 (22.8%) had it within 1 h of admission. Supplemental O 2 was given to 31 (30.7%) and out of the 31 given oxygen, none of the oxygen administration was based on measured SpO2. Intravenous fluid was administered to 56 (55.4%) patients, 30 (29.7%) had antibiotics, while 4 (4.0%) had mucolytic agent [Table 3].
Twenty-five patients (24.8%) had their controller medication stepped/adjusted before the time of discharge, 37 (36.6%) were discharged on ICS/long-acting β2-agonist combination inhaler, 10 (9.9%) were given written action, 36 (35.5%) had their inhaler technique reviewed, and 25 (24.8%) retrained on it. Specific follow-up appointment was documented in 68 (67.3%) of the discharge and 32 (31.7%) were reviewed within 30 days [Table 4].
To determine the level of adherence to the 15 major recommendations of the GINA guideline by their category, we stratified the doctors into three categories; these include (1) internist, (2) family physician, and (3) casualty/medical officers. In this study, we defined "medical officers" as doctors who have a basic medical degree , currently performing general medical duties and are not in specialist training. The pulmonologists were merged with the internists because they managed very few cases that did not allow for separate in-depth analysis. There was no significant difference among the internist, family physician, and casualty/medical officers in the level of compliance to 10 of 15 GINA recommendations. There were low levels of compliance by casualty/medical officers to 4 out of 5 remaining recommendations. We also observed that the internists were significantly giving follow-up appointment than other categories of doctors [Table 5].
|Table 5: Adherence to GINA guideline recommendations by doctors category|
Click here to view
| Discussion|| |
This audit of the management of acute asthma cases admitted to the two tertiary hospitals in the southwestern region of Nigeria has demonstrated marked deficiencies in standards of care measured against the GINA management guidelines. At admission, less than one-third of patients had an assessment of severity, smoking status, inhaler technique, and medication adherence documented. Furthermore, the baseline and serial oxygen saturation, baseline PEFR, and post-BD PEFR were not documented in more than 90% of cases, respectively. Majority received nebulized salbutamol, systemic CS within 1 h, and follow-up appointment on discharge; however, only 35.7% came for follow-up within 30 days. A significant proportion of patients were not prescribed ICS and given the self management plan on discharge.
The clinical profile of patients showed that most of them were females and below the age of 45 years. This is in keeping with findings in other studies. ,,,, Female sex is a risk factor for severe asthma which is associated with increased hospital admissions. This association has been linked to several factors including menarche, menstrual cycle, pregnancy, hormone genetics, and obesity.  Women have also been associated with high level of atopy, bronchial hyperresponsiveness, and exposure to indoor pollutant. 
In the initial assessment of acute asthma admission, the GINA guideline recommended history and physical examination (auscultation, use of accessory muscles, heart rate, respiratory rate, PEF or FEV1, oxygen saturation, arterial blood gas if patient in extremis) for assessing asthma severity to determine the site of therapy, forms of treatment, and monitoring of treatment. The assessment of severity was poor as only 32.7% were documented; it is more than 3.3% in the audit of childhood asthma in Lagos,  but it is less than 42.1-82.2% in other parts of the world.  Functional assessment components such as oxygen saturation and PEFR were measured in 5.9% and 5.0% of the cases, respectively; these indices are comparatively <93.0% and 20% in Spain  and 96.1% and 81.0% in the UK,  respectively. PEFR is less commonly assessed in Mexico and Italy and more commonly assessed in Australia and France.  None of the cases had their post-BD PEFR and this is in contrast to 38.0% reported in the UK which is also a disappointing result.  The implication of not measuring post-BD PEFR is that most patients were treated and discharged without objective evaluation of airflow limitation and response to therapy. It is unimaginable that the hospitals have all the required facilities, but it was not optimally used. The reasons for nonutilization of available instruments are multifactorial. These include lack of knowledge and awareness of its usefulness  and systemic problems such as delay in replacing consumables such as battery of the oximeter and spirometry and PEF mouthpiece and repairing faulty components of the instruments.
Smoking status was recorded in 29.7% of cases and this finding is in contrast to 91.8% reported in the UK audit. 
This is a serious omission on the part of the admitting doctors. This observation may be ascribed to physicians' poor knowledge of smoking as risk factors for severe asthma and its blunting of the anti-inflammatory action of CSs. , Other factor responsible for poor recording of smoking is the perception by doctors that the most women do not smoke and is not a cause of serious morbidity among women who are mostly affected by asthma. ,,,
Majority of the patients had their asthma triggering factors documented (72.3%) which is similar to 73.3% in a previous study.  The level of drug adherence recorded was also disappointing as only 17.8% were documented to adhere to inhaled corticosteroids (ICSs). A study in Nigeria has shown that the lack of controller medication adherence is strongly associated with poor asthma control.  Proper assessment of adherence would have afforded the managing team to prescribe the optimal therapy and address the cause of poor medication compliance.
Majority (75.2%) of the patients received nebulized salbutamol as BD during asthma emergency; this result is an improvement on three other studies carried out in Nigeria about a decade ago where most patients were given theophylline. ,, Rapid-acting β2-agonists are more effective than theophylline in the management of acute asthma. Its use is associated with less severe and potentially fatal side effects.  We also found an encouraging result in the use of CSs as 88.1% of the patients were given systemic CS and 77.2% were given within 1 h of admission. The rate of steroids administration in our study is similar to other studies. ,,, In terms of time of steroid administration, our data are far better than the one in the UK where 95.0% were given systemic CS, but 40.0% were given within 1 h of admission.  The similarities in the results of this study with the previous audit might likely be due to doctors' good knowledge and belief about the efficacy of CS in reversing and resolving chronic airway inflammation of asthma. In addition, OCSs and intravenous corticosteroids are widely affordable and available in hospitals and private pharmacy during periods of hospital workers' strike and their prescription are rarely affected by systemic or organization problems.  Systemic glucocorticosteroids speed resolution of exacerbations and should be utilized in the all, but the mildest exacerbations and the benefits are greatest in patients with life-threatening asthma and those not currently receiving steroids.  Significant benefit with systemic steroid therapy is observed within 4 h of administration.  Hence, systemic steroids take several hours to exert their anti-inflammatory effect, and therefore, prompt administration after presentation is important.
Concurrently, 30.7% of the patients received supplemental oxygen; this statistic is lower than 60% reported in a Spanish study.  A multi-national study on acute asthma management, burden, and outcomes also revealed that <60% of the patients received guideline-recommended therapy with a BD, CS, and supplemental oxygen.  Oxygen administration is low in this study because there is a lack of assessment of the oximetry status and indication for acute oxygen administration during the initial assessment on admission. The poor assessment of oxygen level may be due to an unavailability of a regularly functioning pulse oximeter. There is a possibility of direct relation between knowing a patient's oxygen status and correction of hypoxemia. Furthermore, the poor administration may also be due to physician's lack of awareness of its usefulness in cases that were not life-threating or presenting with central cyanosis. Hypoxemia in asthma emergency can be detected using clinical signs, blood gas analysis, or pulse oximetry.  Cyanosis has poor sensitivity because it is possible to have hypoxemia despite the lack of cyanosis.  Systemic problems such as delay in replacing empty oxygen cylinders and repairing faulty concentrator oxygen delivery components and electrical power failure may all have roles to play in a resource-limited setting. Although, we did not evaluate the knowledge of , perception and barrier to oxygen therapy among the doctors in this study, our findings may implicate future research on oxygen therapy among health-care workers and the general populace.
On discharge, nearly one out of three patients had a prescription of inhaled corticosteroid while most patients were not prescribed ICS; this result is in contrast to other studies on asthma audit. , The use of intravenous corticosteroids is associated with good asthma control and reduced risk of asthma-related hospitalization and ED visit in Nigeria. , Furthermore, majority of the patients did not have their inhaler technique reviewed, despite recent studies showing that most patients use their inhalers incorrectly.  Also, in the UK, <50% of patients had their inhaler technique reviewed on discharge.  The findings in our study may be due to poor awareness of the clinical consequences of improper inhaler technique.
About 10% were given asthma action plan and this pattern has also been observed in other studies. ,, In a multicenter study in Nigeria to determine the unmet needs in asthma treatment, 33% of patients received asthma action plan.  This result study is a reflection of the poor partnership between asthma patient and health-care professional and poor knowledge of the asthma guidelines.
Most (67.3%) of the patients were given specific follow-up appointment; however, only 35.7% were reviewed within 30 days of discharge. This is similar to 66.8% reported in the UK asthma audit.  Lack of follow-up is a common problem among asthma patients; other studies have reported low rates of follow-up visits in their patients after they were discharged from ED. , The frequency of follow-up visits may help to build doctor and patients partnership, to predict medication adherence, and to ensure adequate monitoring of their lung function.
In assessing the doctors' adherence to the guidelines, our results showed that the level of adherence was not generally satisfactory among all the categories of doctors, with the medical/casualty officers having the lowest level adherence. We also observed that the performance of doctors increased with their level of training as specialists tended to perform better than nonspecialists. This finding is comparable to other previous studies in Nigeria. ,
This study has reflected the performance of two tertiary hospitals in Southwestern Nigeria, using the recommended standard of care, and not that of individuals, a group of professionals or specialties. This form of benchmarking has highlighted areas of deficiencies in acute asthma management that can be easily understood by medical and nonmedical staff. Poorly performing areas of the management would be examined and organizational issues as well as management protocols and clinical competence would be addressed. A second audit would be carried in 12-16 months after addressing the observed deficiencies and management challenges.
We are limited by some inaccuracies from the medical write-up of patients by doctors, missing medical record files, and periods of industrial unrest by health-care workers where instruments were locked up and some vital measurements could not be done. In view of the fact that this study was conducted in two tertiary hospitals, we are very cautious in generalizing result our findings to the whole country. However, this study may serve as template for future study on national asthma audit and reason for nonadherence to asthma guidelines before formulating the national asthma guideline.
| Conclusion|| |
The result from this first audit reveals that the acute management of asthma in our setting is suboptimal and there is a low level of compliance with most recommendations of the GINA guideline. This audit has implicated the need to address the nonperforming areas, knowledge gaps, clinical competence, and organizational issues before the second audit.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
The Global Asthma Report 2011. Paris, France: The International Union Against Tuberculosis and Lung Disease, 2011. Available from: http://www.globalasthm
areport.org/2011/images/files/Global_Asthma_Report_2011.pdf. [Last accessed on 2016 Sep 13].
Global Initiative for Asthma. Global Strategy for Asthma Management and Prevention - 2012 Updated. Geneva: Global Initiative for Asthma; 2013. Available from: http://www.ginasthma.org
. [Last accessed on 2013 Jul 17].
Desalu OO, Oluboyo PO, Salami AK. The prevalence of bronchial asthma among adults in Ilorin, Nigeria. Afr J Med Med Sci 2009;38:149-54.
Ibeh CC, Ele PU. Prevalence of bronchial asthma in adolescent in Anambra State, Nigeria. Niger J Intern Med 2002;5:23-6.
Desalu OO, Ojo OO, Busari OA, Fadeyi A. Pattern of respiratory diseases seen among adults in an emergency room in a resource-poor nation health facility. Pan Afr Med J 2011;9:24.
Ogunmola OJ, Olamoyegun MA. Patterns and outcomes of medical admissions in the accident and emergency department of a tertiary health center in a rural community of Ekiti, Nigeria. J Emerg Trauma Shock 2014;7:261-7.
Smith DH, Malone DC, Lawson KA, Okamoto LJ, Battista C, Saunders WB. A national estimate of the economic costs of asthma. Am J Respir Crit Care Med 1997;156(3 Pt 1):787-93.
National Heart Lung and Blood Institute. National Asthma Education and Prevention Program. Expert Panel Report 3: Guidelines for the Diagnosis and Management of Asthma. National Institutes of Health; 2007.
Available from: https://www.brit-thoracic.org.uk/document-library/clinical-information/asthma/btssign-asthma-guideline-2009/. [Last accessed on 2016 Sep 13].
Desalu OO, Onyedum CC, Iseh KR, Salawu FK, Salami AK. Asthma in Nigeria: Are the facilities and resources available to support internationally endorsed standards of care? Health Policy 2011;99:250-4.
Onyedum C, Ukwaja K, Desalu O, Ezeudo C. Challenges in the management of bronchial asthma among adults in Nigeria: A systematic review. Ann Med Health Sci Res 2013;3:324-9.
Umoh VA, Ukpe IE. Knowledge of the asthma guidelines among doctors in a tertiary hospital in Nigeria. Indian J Allergy Asthma Immunol 2012;26:77-82.
Ayuk A, Iloh K, ObumnemeAnyim I, Ilechukwu G, Oguonu T. Practice of asthma management among doctors in SouthEast Nigeria. Afr J Respir Med 2010;6:14-7.
Okoromah CA, Renner JK, Oduwole AO, Adenuga AO. Acute asthma in a children′s emergency room: A clinical audit and management guideline proposal. Niger Postgrad Med J 2006;13:348-53.
Desalu OO, Onyedum CC, Adeoti AO, Ozoh OB, Fadare JO, Salawu FK, et al.
Unmet needs in asthma treatment in a resource-limited setting: Findings from the survey of adult asthma patients and their physicians in Nigeria. Pan Afr Med J 2013;16:20.
Erhabor GE, Adigun AO. Analysis of intra-hospital deaths from acute severe asthma. Niger J Health Sci 2001;1:22-5.
Salami AK, Oluboyo PO. Bronchial asthma in Ilorin: A five year review. Trop J Health Sci 2004;11:19-23.
Lindsay J, Heaney L. British Thoracic Society. Adult Asthma Audit; 2012. Available from: https://www.brit-thoracic.org.uk/document-library/audit-and-quality-improvement/audit-reports/bts-adult-asthma-audit-report-2012/. [Last accessed on 2016 Sep 13].
Schatz M, Clark S, Camargo CA Jr. Sex differences in the presentation and course of asthma hospitalizations. Chest 2006;129:50-5.
Gibbison B, Griggs K, Mukherjee M, Sheikh A. Ten years of asthma admissions to adult critical care units in England and Wales. BMJ Open 2013;3:e003420.
ENFUMOSA Study Group. The ENFUMOSA cross-sectional European multicentre study of the clinical phenotype of chronic severe asthma. Eur Respir J 2003;22:470-7.
Leynaert B, Bousquet J, Henry C, Liard R, Neukirch F. Is bronchial hyperresponsiveness more frequent in women than in men? A population-based study. Am J Respir Crit Care Med 1997;156:1413-20.
Fitzgerald JM, O′Byrne PM, McFetridge JT, Demuth D, Allen-Ramey FC. Pulmonary function testing in the emergency department and medications prescribed at discharge: Results of the Multinational Acute asthma Management, Burden, and Outcomes (MAMBO) study. Prim Care Respir J 2010;19:155-62.
Linares T, Campos A, Torres M, Reyes J. Medical audit on asthma in an emergency department. Allergol Immunopathol (Madr) 2006;34:248-51.
Desalu OO, Busari OA, Onyedum CC, Salawu FK, Obateru OA, Nwogu KC, et al.
Evaluation of current knowledge, awareness and practice of spirometry among hospital -based Nigerian doctors. BMC Pulm Med 2009;9:50.
de Marco R, Marcon A, Jarvis D, Accordini S, Almar E, Bugiani M, et al.
Prognostic factors of asthma severity: A 9-year international prospective cohort study. J Allergy Clin Immunol 2006;117:1249-56.
Adcock IM, Ito K, Barnes PJ. Glucocorticoids: Effects on gene transcription. Proc Am Thorac Soc 2004;1:247-54.
Erhabor GE, Agbroko SO, Bamigboye P, Awopeju OF. Prevalence of asthma symptoms among university students 15 to 35 years of age in Obafemi Awolowo University, Ile-Ife, Osun State. J Asthma 2006;43:161-4.
Desalu OO, Fawibe AE, Salami AK. Assessment of the level of asthma control among adult patients in two tertiary care centers in Nigeria. J Asthma 2012;49:765-72.
Duke T, Graham SM, Cherian MN, Ginsburg AS, English M, Howie S, et al.
Oxygen is an essential medicine: A call for international action. Int J Tuberc Lung Dis 2010;14:1362-8.
Desalu OO, Fadare JO, Adeoti AO, Adekoya AO. Risk factors for asthma hospitalization and emergency department visit in Nigeria: The role of symptoms frequency and drug utilization. Indian J Allergy Asthma Immunol 2013;27:129-33.
Onyedum C, Desalu O, Nwosu N, Chukwuka C, Ukwaja K, Ezeudo C. Evaluation of inhaler techniques among asthma patients seen in Nigeria: An observational cross sectional study. Ann Med Health Sci Res 2014;4:67-73.
Wiener-Ogilvie S, Pinnock H, Huby G, Sheikh A, Partridge MR, Gillies J. Do practices comply with key recommendations of the British Asthma Guideline? If not, why not? Prim Care Respir J 2007;16:369-77.
Mash B, Rhode H, Pather M, Ainslie G, Irusen E, Bheekie A, et al.
Quality of asthma care: Western Cape province, South Africa. S Afr Med J 2009;99:892-6.
Smith SR, Jaffe DM, Highstein G, Fisher EB, Trinkaus KM, Strunk RC. Asthma coaching in the pediatric emergency department. Acad Emerg Med 2006;13:835-9.
Zorc JJ, Chew A, Allen JL, Shaw K. Beliefs and barriers to follow-up after an emergency department asthma visit: A randomized trial. Pediatrics 2009;124:1135-42.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]