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Original Research: Asthma |

Has Asthma Medication Use Caught Up With the Evidence?: A 12-Year Population-Based Study of Trends FREE TO VIEW

Mohsen Sadatsafavi, MD, PhD; Hamid Tavakoli, MD; Larry Lynd, PhD; J. Mark FitzGerald, MD
Author and Funding Information

FUNDING/SUPPORT: This study was funded by an arm’s length research contract with AstraZeneca Canada, mediated through and approved by the University-Industry Liaison Office at the University of British Columbia.

aCollaboration for Outcomes Research and Evaluation, Faculty of Pharmaceutical Sciences, University of British Columbia, Vancouver, Canada

bInstitute for Heart and Lung Health, Department of Medicine, University of British Columbia, Vancouver, Canada

cCentre for Clinical Epidemiology and Evaluation, University of British Columbia, Vancouver, Canada

dCentre for Health Evaluation and Outcomes Research, University of British Columbia, Vancouver, Canada

CORRESPONDENCE TO: Mohsen Sadatsafavi, MD, PhD, Room 4110, Faculty of Pharmaceutical Sciences, 2405 Wesbrook Mall, Vancouver, BC, Canada V6T1Z3


Copyright 2016, American College of Chest Physicians. All Rights Reserved.


Chest. 2017;151(3):612-618. doi:10.1016/j.chest.2016.10.028
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Published online

Background  The importance of balance between controller and reliever medications in asthma is recognized. However, to our knowledge, the extent to which real-world practice has caught up with evidence-based guidelines has not been studied.

Methods  This was a retrospective cohort study of individuals 15 to 67 years of age who satisfied a validated case definition of asthma in the administrative health database of British Columbia, Canada between 2002 and 2013. Each patient-year was assessed for inappropriate and excessive prescription of short-acting beta-agonists (SABAs) and the balance between controller and reliever medications. Trends on three time axes were evaluated: calendar time, time course of asthma, and age. Poisson regression was used to test for a linear trend.

Results  Three hundred fifty-six thousand, one hundred twelve patients (56.5% female sex; mean age, 30.5 years) contributed 2.6 million patient-years. In 7.3% of the patient-years, SABAs were prescribed inappropriately. This proportion dropped by a relative rate of 5.3% per year (P < .001). In the first year of asthma, 6.3% of patients had indicators of inappropriate SABA use, which dropped within the first 3 years but increased thereafter. Excessive prescription of SABAs increased rapidly during the time course of asthma (change of 23.3% per year; P < .001) and by age (change of 5.1% per year; P < .001).

Conclusions  Despite overwhelming evidence regarding the risks, inappropriate prescription for SABAs was prevalent. Excessive SABA use might explain high asthma mortality in older patients. Inappropriate prescriptions declined over the study period but increased over the time course of asthma. These trends might have contributed to the declining asthma hospitalization rates in British Columbia, but there remain gaps in care and potential for improvement in asthma outcomes.

Figures in this Article

The balance between controller and reliever medication use in asthma has been a topic of historical and active interest. With suppression of symptoms but generally no effect on the underlying inflammation, reliever medications such as short-acting beta-agonists (SABAs) without concomitant antiinflammatory therapy such as inhaled corticosteroids (ICS) can result in poor asthma control with an increased risk of morbidity and mortality.

Multiple different studies have demonstrated that a low ratio of controller to reliever medication is associated with adverse outcomes.,,,,, The recognition of such increased risk has resulted in significant changes in guidelines and best practice recommendations in asthma management, such as the influential Global Initiative for Asthma. Although there is substantial historical evidence in this regard, evidence is lacking on the current state of the problem. Understanding recent trends enables one to quantify the current, and project the future, avoidable burden due to a departure from evidence-based asthma medication use. Given the strong emphasis of contemporary asthma guidelines on the appropriate use of asthma medications, the persistence of inappropriate reliever use would indicate that other solutions besides advocating guideline-based treatments are required. The purpose of the present study was to use 12 years of data from the entire population of a well-defined geographic area to study the extent and trends of inappropriate or excessive use of asthma reliever medications.

We used administrative health databases of British Columbia, a Canadian province with a population of 4.67 million (as of 2015) between January 2002 and December 2013. We had access to all inpatient records, all outpatient services records, birth and death data, and basic demographics and longitudinal status of individuals within the health-care system., Finally, we had access to the database of filled prescription records of all legal residents. Data were linkable at the individual level and have shown excellent reliability, with a very low rate of missing or incorrect data. All inferences, opinions, and conclusions drawn from this research are those of the authors and do not reflect the opinions or policies of the data stewards. This study was approved by the University of British Columbia’s Human Ethics Board (H15-00062).

From these data, we created a cohort of patients with asthma using a validated case definition based on satisfying at least one of three criteria in a rolling 12-month window (patients were between 15 and 55 years). The criteria included (1) the use of three asthma-related medications (e-Tables 1, 2) or (2) two outpatient visits or (3) one hospitalization with the main code for asthma. The index date was the first date of any asthma-related resource use after a person's 15th birthday. We applied an upper age criterion of 55 years in the case definition to avoid misclassification of patients with obstructive lung disease. However, once selected, we followed patients as long as they were in the database. Given the 12-year data, this would result in an upper age of 67 years. To evaluate the pattern of prescriptions since the inception of asthma (time course of asthma) within this “full cohort,” we created a secondary “incident cohort,” which was defined as individuals who had at least 5 years of data before their index date during which no asthma-related records could be found. Follow-up time started on the index date and ended at the earliest of the following: date of death, last resource use of any type, or the end of the study period (December 12, 2013). Follow-up time was divided into juxtaposing 12-month periods. If the last follow-up period was < 12 months, it was excluded.

Exposure Variables

Three metrics were defined: inappropriate prescription of SABAs, excessive prescription of SABAs, and the ratio of ICS to total asthma-related prescriptions. These variables were calculated for each follow-up patient-year. We used a previously published definition for associating each patient-year with appropriate or inappropriate prescription of SABAs. Inappropriate prescription was defined as greater than two puffs of a SABA per week if no ICS was used and nine or more canisters of SABA and no more than 100 μg (beclomethasone equivalent) per day of ICS. Appropriate prescription was defined as receiving fewer than two puffs per week in the absence of ICS or filling prescriptions for four or fewer SABA canisters per year and at least 400 μg per day of ICS. Individuals could fall into a “gray zone,” in which the definition for either appropriate or inappropriate prescription was not satisfied. Excessive SABA prescription was defined as filling prescriptions for 12 or more canisters during a year, regardless of ICS use. Finally, we calculated the ratio of ICS to total asthma prescriptions as described by Laforest et al. This ratio is validated in claims-based and electronic medical records and is shown to be negatively associated with adverse asthma outcomes. We used the proposed cutoff of 50% to mark each patient-year as having a satisfactory ratio. In calculating these metrics, both controller and reliever medications were adjusted for defined daily doses.

Statistical Analysis

The unit of observation was the patient-year. We conducted three trend analyses for each of the three metrics: over calendar time, over the time course of asthma (since the inception of asthma; this analysis was restricted to the incident asthma cohort), and over age. Trends were tested using Poisson regression, with the counts of the variable as the dependent variable and time axis of interest as the independent variable. For the trend analysis of inappropriate and excessive SABA prescription, total patient-years was the denominator; for the ICS to total prescription ratio, the number of patient-years in which the patient had filled prescriptions for at least one ICS or SABA was the denominator; this was necessary, as periods with no filled ICS or SABA prescriptions would result in 0:0 ratios. SAS, version 9.3 (SAS Institute) was used for all analyses. Statistical significance was defined at two-tailed P = .05.

The case definition of asthma was satisfied by 343,520 individuals who had at least one follow-up period. Average age on the index date was 30.5 years; 55.9% were women. Average follow-up time was 7.46 years. At least 5 years of data without any asthma-related records prior to the index date was satisfied by 126,896 individuals, who composed the incident asthma cohort. Table 1 provides the baseline characteristics of the cohorts.

Table Graphic Jump Location
Table 1 Baseline Characteristics and Follow-Up Statistics of the Study Population

Neighborhood income quintiles based on postal codes.

ICS = inhaled corticosteroids; SABA = short-acting beta-agonist.

Overall Findings

In 7.6% of patient-years (190,364) in the full cohort, SABAs were prescribed inappropriately (Table 1). The proportion of follow-up time associated with inappropriate SABA prescription was lower in the incident cohort (6.3%). When we removed patient-years in which no asthma-related prescriptions were filled, the proportion of patient-years associated with inappropriate SABA prescription increased to 11.9% in the full cohort and to 9.7% in the incident cohort. In 0.9% of patient-years in the full cohort, SABAs were prescribed excessively. This was lower in the incident cohort (0.3%). Finally, in 29.6% of patient-years in the full cohort, ICS to total prescription ratio was > 0.5. This proportion was 28.4% in the incident cohort.

Trends Over Calendar Time

Results are provided in Figure 1. In 2002, 8.7% of patients were prescribed SABAs inappropriately. This value declined to 4.6% in 2013. The average annual relative rate of change was 5.1% per year (P < .001). Similarly, the excessive prescription of SABAs declined during the study period. In 2002, 1.1% of patients filled prescriptions for more than 12 SABA canisters, which fell to 0.4% in 2013. The relative rate of decline was 9.2% per year (P < .001). The proportion of patient-years with a satisfactory ICS to total prescription ratio was 44.2% in 2002, increasing to 55.5% in 2013 (change of 1.7% per year; P < .001).

Figure 1
Figure Jump LinkFigure 1 Trends over calendar year. All annual rates of change were significant (P < .01). ICS = inhaled corticosteroids; SABAs = short-acting beta-agonists.Grahic Jump Location
Trends Over Time Course of Asthma

The results of trends over the time course of asthma are provided in Figure 2. The rate of inappropriate SABA prescription was highest in the incident year (6.8%). It declined for the next 3 years and steadily increased afterward, reaching 6.0% by the 12th year. The overall trend was compatible with a 1.4% increase per year (P < .001). Excessive prescription of SABAs increased sharply over the time course of asthma. It was lowest (< 0.1%) in the incident year but increased to 0.6% in the 12th year, corresponding to an increase of 23.3% per year (P < .001). The proportion of individuals with a satisfactory ICS to total prescription ratio remained largely constant around 50%. This was the only trend that was not statistically significant (P = .324).

Figure 2
Figure Jump LinkFigure 2 Trends over time course of asthma. Annual rates of change for inappropriate use of SABAs were significant (P < .001). Annual trend for the ICS to total medication rate was not significant (P = .324). See Figure 1 legend for expansion of abbreviations.Grahic Jump Location
Trends Over Age

Trends over age results are presented in Figure 3. Inappropriate SABA prescription decreased between 15 and 19 years of age, reaching a minimum of 3.0% in patients 19 years of age. It increased until the early 30s, reaching a maximum of 5.9% at age 31 years; remained mainly constant among subjects in their late 40s; and declined thereafter (overall relative change of 0.2% per year of age). The picture was very different for excessive SABA prescription. It generally remained < 0.2% to the mid-40s but quickly increased, passing the 1.0% point among individuals 64 years of age. The trend after this age was considered noninterpretable given the small sample size in these groups. Overall, excessive SABA prescription increased by 5.1% per year of age (P < .001). Finally, the proportion of individuals with a satisfactory ICS to total prescription ratio decreased from 49% to 41% from the age of 15 years to the mid-20s but gradually increased to 55% after the age of 50 years (relative rate of change, 1.1% per year of age; P < .001).

Figure 3
Figure Jump LinkFigure 3 Trends over age. All annual rates of change were significant (P < .01). See Figure 1 legend for expansion of abbreviations.Grahic Jump Location

Using population-based data from a well-defined geographic area, this study demonstrated that > 7% of patients with asthma had indicators of inappropriately using reliever medications based on their filled prescription records. Not considering patient-years in which patients did not take any asthma-related medications (which might indicate dormant asthma) increased this value to 12%. Only a small proportion (< 1%) of patients had indicators of excessive SABA use. In more than half of patient-years, the ratio of controller to reliever medications was less than the recommended threshold. Given the high prevalence of asthma, the cumulative time in which patients were potentially exposed to a dangerous combination of asthma medications was very high: more than 190,000 patient-years of data in a 12-year span were associated with inappropriate reliever prescriptions.

There were encouraging trends, however. Inappropriate prescription of SABAs halved from 2002 to 2013, whereas excessive SABA prescription declined by more than 60%. This might represent gradual adoption of guidelines among care providers and patients. It may also reflect increasing access to and use of effective medications that have gradually improved asthma control. Previous analyses have shown a 176% increase over 6 years in the use of combination ICS and long-acting beta agonist (LABA) therapy in British Columbia, which more than offset the decline in monotherapy with ICS. Higher ICS + LABA use can also result in lower use of SABAs, regardless of asthma control. Physicians prescribing LABAs and patients taking such medications might be wary of the total beta-agonist intake and cut the use of SABAs irrespective of symptoms. There might well be other reasons beyond the generally opposing direction of inappropriate/excessive SABA use and high controller to total medication use. For example, a post hoc analysis (results not shown) revealed a higher prevalence of use of ICS as well as a higher total dose of ICS among users of ICS over calendar time (thus reducing the prevalence of inappropriate SABA users).

In the first year after asthma diagnosis, patients had the highest risk of inappropriate SABA prescription—higher than that present in the subsequent 12 years. This likely relates to the “as-needed” use of SABAs without any controller medication when the physician is not yet certain of an asthma diagnosis or in patients with intermittent asthma at the onset of their disease (step 1 in the Global Initiative for Asthma treatment algorithm). Patients and care providers need to be vigilant about maintaining the use of relievers at low levels in the absence of ICS. Aside from the postdiagnosis period, we documented an increasing trend in inappropriate or excessive SABA prescriptions over the time course of asthma. This may reflect behavioral aspects of treatment—for example, increasing reliance on reliever medications over time. This can also indicate gradual worsening of asthma (eg, development of fixed airflow obstruction) or the increasing burden of comorbid conditions that might deviate attention from appropriate management of asthma. Trends over age were more complex, with inappropriate SABA use being highest in young to middle-aged patients, with excessive use rapidly increasing in the older population. Asthma mortality is highest among the elderly. The novel insights into the age-related increase in excessive reliever use highlights a potentially causal mechanism that warrants further assessment.

Although there have been multiple studies on the outcomes associated with inappropriate use of reliever medications, there has been a scarcity of evidence on the extent and trends of the phenomenon. Stafford et al analyzed 25 years (1978-2002) of nationally representative data on prescribing patterns by office-based US physicians. SABA use increased until the late 1990s and declined only in the last 3 years of the study period. Higashi et al estimated an 11% decline in the use of SABAs and a 37% increase in the use of ICS in the United States from 1997 to 2009 based on office-based physician audits. In contrast, a multicenter European study did not find any changes in the prevalence of SABA use between the mid-1990s and the mid-2000s. A study from the United Kingdom, however, documented an increase of 20% in the total dispensed dose of SABAs between 1994 and 1998 but also reported that the ratio of ICS to SABA increased from 0.49 to 0.73.

Our study updates the older estimates of the trends and is the first to provide insight into trends of prescriptions over the time course of asthma. A major strength of this study was access to all the data of a well-defined health jurisdiction with universal health care. The very low level of self-selection was particularly important in addressing the study objectives, as previous findings have indicated the association between socioeconomic status, a factor that influences the enrollment into commercial insurance programs, and asthma medication use. The 12 years of follow-up provides robust estimates of trends that can be a basis for the estimation of avoidable burden and projection of future outcomes.

The limitations of this study should also be acknowledged. Without information on actual drug intake, it is difficult to establish with precision the true patterns of asthma medication use. For example, it might be the case that patients stockpile their reliever medications (eg, at work and home). Although this pattern should cancel out in long-term prescription data, it might affect the trends around the time of diagnosis. An important factor to consider is that asthma, at least in Canada, is an overdiagnosed condition, which means that a proportion of our study sample did not have true airway hyperreactivity. This is not a limitation of this study per se, which aimed at capturing the reality of asthma management. However, it would be informative if future studies could also evaluate the trends in factors that can mediate the effect of controller and reliever use, such as the degree of airway reactivity, smoking status, and asthma phenotypes.

Asthma guidelines have been advocating the appropriate use of asthma medications for more than 2 decades, and the evidence is strong regarding the risks associated with overuse of reliever therapy. However, the reality of asthma care is highlighted by the departure from asthma treatment guidelines, especially for older age groups. Indeed, a recent audit of asthma deaths in the United Kingdom showed that in approximately 50% of deaths, there were avoidable factors, including overreliance on reliever medications. There are encouraging trends indicating a decline in the pattern of inappropriate use of asthma medications. This might be partially responsible for the downward trend of asthma-related hospitalizations in British Columbia. Future studies are needed to evaluate such trends in other jurisdictions and to evaluate factors that explain the variation in asthma medication use. There is also a need for studies that propose solutions toward improving asthma care.

Author contributions: M. S. and H. T. are guarantors of the manuscript. M. S., J. M. F., and L. L. are responsible for the concept of the study. M. S. and H. T. designed the study and created the data analysis plan. J. M. F. and L. L. provided feedback on the design. H. T. performed all statistical analyses. M. S. wrote the first draft of the manuscript. All authors critically commented on the manuscript and approved the final version.

Financial/nonfinancial disclosures: The authors have reported to CHEST the following: J. M. F. has served on advisory boards of Novartis, Pfizer, AstraZeneca, Boehringer-Ingelheim, ALK, and Merck. He has also been a member of speakers’ bureaus for AstraZeneca, Boehringer-Ingelheim, ALK, and Merck. He has received research funding, paid directly to the University of British Columbia, from AstraZeneca, Glaxo-SmithKline, Boehringer-Ingelheim, Merck, Sanofi, Amgen, and Genentech. J. M. F. is a member of the Global Initiative for Asthma (GINA) Executive and Science Committees. M. S. receives salary support from the Canadian Institutes of Health Research and the Michael Smith Foundation for Health Research. None declared (H. T., L. L.).

Role of sponsors: The sponsor had no role in the design of the study, the collection and analysis of the data, or the preparation of the manuscript.

Additional information: The e-Tables can be found in the Supplemental Materials section of the online article.

Laforest L. .Licaj I. .Devouassoux G. .et al Prescribed therapy for asthma: therapeutic ratios and outcomes. BMC Fam Pract. 2015;16:49- [PubMed]journal. [CrossRef] [PubMed]
 
Spitzer W.O. .Suissa S. .Ernst P. .et al The use of beta-agonists and the risk of death and near death from asthma. N Engl J Med. 1992;326:501-506 [PubMed]journal. [CrossRef] [PubMed]
 
Schatz M. .Nakahiro R. .Crawford W. .Mendoza G. .Mosen D. .Stibolt T.B. . Asthma quality-of-care markers using administrative data. Chest. 2005;128:1968-1973 [PubMed]journal. [CrossRef] [PubMed]
 
Schatz M. .Zeiger R.S. . Improving asthma outcomes in large populations. J Allergy Clin Immunol. 2011;128:273-277 [PubMed]journal. [CrossRef] [PubMed]
 
Laforest L. .Licaj I. .Devouassoux G. .et al Relative exposure to controller therapy and asthma exacerbations: a validation study in community pharmacies. Pharmacoepidemiol Drug Saf. 2014;23:958-964 [PubMed]journal. [CrossRef] [PubMed]
 
Laforest L. .Licaj I. .Devouassoux G. .Chatte G. .Martin J. .Van Ganse E. . Asthma drug ratios and exacerbations: claims data from universal health coverage systems. Eur Respir J. 2014;43:1378-1386 [PubMed]journal. [CrossRef] [PubMed]
 
Anis A.H. .Lynd L.D. .Wang X.H. .et al Double trouble: impact of inappropriate use of asthma medication on the use of health care resources. Can Med Assoc J. 2001;164:625-631 [PubMed]journal
 
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Figures

Figure Jump LinkFigure 1 Trends over calendar year. All annual rates of change were significant (P < .01). ICS = inhaled corticosteroids; SABAs = short-acting beta-agonists.Grahic Jump Location
Figure Jump LinkFigure 2 Trends over time course of asthma. Annual rates of change for inappropriate use of SABAs were significant (P < .001). Annual trend for the ICS to total medication rate was not significant (P = .324). See Figure 1 legend for expansion of abbreviations.Grahic Jump Location
Figure Jump LinkFigure 3 Trends over age. All annual rates of change were significant (P < .01). See Figure 1 legend for expansion of abbreviations.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1 Baseline Characteristics and Follow-Up Statistics of the Study Population

Neighborhood income quintiles based on postal codes.

ICS = inhaled corticosteroids; SABA = short-acting beta-agonist.

References

Laforest L. .Licaj I. .Devouassoux G. .et al Prescribed therapy for asthma: therapeutic ratios and outcomes. BMC Fam Pract. 2015;16:49- [PubMed]journal. [CrossRef] [PubMed]
 
Spitzer W.O. .Suissa S. .Ernst P. .et al The use of beta-agonists and the risk of death and near death from asthma. N Engl J Med. 1992;326:501-506 [PubMed]journal. [CrossRef] [PubMed]
 
Schatz M. .Nakahiro R. .Crawford W. .Mendoza G. .Mosen D. .Stibolt T.B. . Asthma quality-of-care markers using administrative data. Chest. 2005;128:1968-1973 [PubMed]journal. [CrossRef] [PubMed]
 
Schatz M. .Zeiger R.S. . Improving asthma outcomes in large populations. J Allergy Clin Immunol. 2011;128:273-277 [PubMed]journal. [CrossRef] [PubMed]
 
Laforest L. .Licaj I. .Devouassoux G. .et al Relative exposure to controller therapy and asthma exacerbations: a validation study in community pharmacies. Pharmacoepidemiol Drug Saf. 2014;23:958-964 [PubMed]journal. [CrossRef] [PubMed]
 
Laforest L. .Licaj I. .Devouassoux G. .Chatte G. .Martin J. .Van Ganse E. . Asthma drug ratios and exacerbations: claims data from universal health coverage systems. Eur Respir J. 2014;43:1378-1386 [PubMed]journal. [CrossRef] [PubMed]
 
Anis A.H. .Lynd L.D. .Wang X.H. .et al Double trouble: impact of inappropriate use of asthma medication on the use of health care resources. Can Med Assoc J. 2001;164:625-631 [PubMed]journal
 
Global INitiative for Asthma. GINA Report, Global Strategy for Asthma Management and Prevention, 2015.http://ginasthma.org/gina-reports/. Accessed July 7, 2016.
 
British Columbia BC Stats. Population Estimates.http://www.bcstats.gov.bc.ca/StatisticsBySubject/Demography/PopulationEstimates.aspx, 2015. Accessed July 7, 2016.
 
Population Data BC. Discharge Abstract Database (Hospital Separations). Data Extract. MOH (2014).http://www.popdata.bc.ca/data. Accessed July 7, 2016.
 
Legislative Assembly of British Columbia. Ministry of Health Services MSP fee-for-service payment analysis.http://www.llbc.leg.bc.ca/public/pubdocs/bcdocs/350351/index.htm. Accessed July 7, 2016.
 
Population Data BC. Vital Statistics Deaths. Data extract. BC Vital Statistics Agency, 2013.http://www.popdata.bc.ca/data. Accessed July 7, 2016.
 
Population Data BC. Vital Statistics Births. Data extract. BC Vital Statistics Agency, 2013.http://www.popdata.bc.ca/data. Accessed July 7, 2016.
 
Population Data BC. Consolidation file (MSP registration & premium billing). Data extract. MOH, 2014.http://www.popdata.bc.ca/data. Accessed July 7, 2016.
 
Population Data BC. PharmaNet. Data extract. Data Stewardship Committee, 2013.http://www.popdata.bc.ca/data. Accessed July 7, 2016.
 
Williams J, Adger W. Inventory of studies on the accuracy of Canadian health administrative databases. Toronto: Institute for Clinical Evaluative Sciences; 1996.
 
Prosser R.J. .Carleton B.C. .Smith M.A. . Identifying persons with treated asthma using administrative data via latent class modelling. Health Serv Res. 2008;43:733-754 [PubMed]journal. [CrossRef] [PubMed]
 
Hong S.H. .Sanders B.H. .West D. . Inappropriate use of inhaled short acting beta-agonists and its association with patient health status. Curr Med Res Opin. 2006;22:33-40 [PubMed]journal. [CrossRef] [PubMed]
 
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Bedouch P. .Marra C.A. .FitzGerald J.M. .Lynd L.D. .Sadatsafavi M. . Trends in asthma-related direct medical costs from 2002 to 2007 in British Columbia, Canada: a population based-cohort study. PloS One. 2012;7:e50949- [PubMed]journal. [CrossRef] [PubMed]
 
Gillman A. .Douglass J.A. . Asthma in the elderly. Asia Pac Allergy. 2012;2:101-108 [PubMed]journal. [CrossRef] [PubMed]
 
Stafford R.S. .Ma J. .Finkelstein S.N. .Haver K. .Cockburn I. . National trends in asthma visits and asthma pharmacotherapy, 1978-2002. J Allergy Clin Immunol. 2003;111:729-735 [PubMed]journal. [CrossRef] [PubMed]
 
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NOTE:
Citing articles are presented as examples only. In non-demo SCM6 implementation, integration with CrossRef’s "Cited By" API will populate this tab (http://www.crossref.org/citedby.html).
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  • CHEST Journal
    Print ISSN: 0012-3692
    Online ISSN: 1931-3543