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Patient Factors and Medication Guideline Adherence Among Older Women With Asthma
R. Graham Barr, MD, MPH;
Samuel C. Somers, MD;
Frank E. Speizer, MD;
Carlos A. Camargo, Jr, MD, DrPH
Arch Intern Med. 2002;162:1761-1768.
ABSTRACT
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Background Asthma guidelines are well established but often followed poorly. Determinants
of adherence among older persons may differ from younger persons and have
not been well characterized.
Objectives To assess adherence to asthma medication guidelines among older women
with asthma and evaluate predictors of adherence with emphasis on asthma characteristics,
comorbid medical conditions, work-related factors, social supports, caregiving,
and emotional well-being.
Methods We assessed adherence to the National Asthma Education and Prevention
Program medication guidelines among participants in the Nurses' Health Study
who reported a physician diagnosis of asthma and reconfirmed the diagnosis
on a separate questionnaire, excluding those with chronic obstructive pulmonary
disease.
Results Among 121 700 participants in the Nurses' Health Study, 5107 reported
physician-diagnosed asthma meeting inclusion criteria. Mean ± SD age
was 63 ± 7 years in 1998. Adherence with asthma medication guidelines
was 57% for mild persistent, 55% for moderate persistent, and 32% for severe
persistent asthma (P = .001). In multivariate analysis,
nonadherence was associated with severe asthma, increasing age, lower socioeconomic
status, current smoking, earlier onset of asthma, and number of comorbid medical
conditions. Measures of social isolation, caregiving, and emotional well-being
were not associated with nonadherence.
Conclusions Asthma is undertreated among older women, even those who are health
care professionals. Women with advanced age and severe asthma were particularly
at risk. Given that the greatest increase in asthma mortality has occurred
among older women, further research is needed to examine physician prescribing
patterns and patient beliefs in this vulnerable population.
INTRODUCTION
APPROPRIATE USE of asthma medications reduces morbidity and mortality
from asthma1-2 and improves quality
of life.3 The National Asthma Education and
Prevention Program (NAEPP) has distilled the literature on the effectiveness
of asthma control medications into severity-based guidelines, which were originally
published in 19914 and were updated in 1997.3 Adherence to these guidelines has been noted to be
low, ranging from 20% to 72% among various groups in the United States.5-12
Studies have suggested that younger age,5-6,12
male sex,6 minority status,5-6
low socioeconomic status,7 severe asthma,6, 8 and nonspecialist care5-6,9, 12-13
are associated with nonadherence; however, these studies have been limited
by poor response rates,5 ecological7 and cross-sectional design,6, 9
and small sample size.10
Most studies on asthma guideline adherence have focused on children
and young adults. However, asthma also is an important problem among elderly
patients. Nationwide, the largest increases in asthma mortality have occurred
among older women.14 Research in cardiovascular
disease suggests that medication adherence may be especially low and have
different causes among elderly patients.15-16
Similar low adherence seems to be true among elderly patients with asthma11, 17; for example, fewer than one third
of 92 nonsmoking, elderly patients with asthma in the Cardiovascular Health
Study received inhaled corticosteroids.18
Clark et al19 have hypothesized that
physical factors, such as comorbid conditions, and a variety of psychosocial
factors, including social isolation and caregiving responsibilities, may contribute
to poor adherence among older patients with asthma. However, few data are
available to assess these ideas. Sin and Tu13
recently reported that increasing age, comorbidity, and physician specialty
predicted poor adherence among older patients hospitalized for asthma; however,
they were unable to evaluate other factors owing to reliance on administrative
data.
We therefore assessed overall adherence to NAEPP medication guidelines
among older women with asthma in the Nurses' Health Study, a prospective cohort
study with high follow-up. We further evaluated the impact of physical factors,
such as asthma severity, and psychosocial factors, such as social isolation
and caregiving, on adherence to NAEPP medication guidelines among these older
women.
PARTICIPANTS AND METHODS
STUDY SAMPLE
In 1976, the Nurses' Health Study enrolled 121 700 married, female
registered nurses, aged 30 to 55 years, who resided in 1 of 11 US states and
responded to a 2-page questionnaire.20 Participants
have been followed biennially via questionnaire to allow evaluation of a large
number of lifestyle and psychosocial exposures and various disease outcomes.
Follow-up of the original cohort in 1998 was greater than 90%.
All participants were asked biennially about a physician diagnosis of
asthma from 1988 onward. A supplemental asthma questionnaire detailing asthma
symptoms, medication use, and exacerbation-related health care use was sent
in 1998 to all participants who reported a physician diagnosis of asthma through
1996 (N = 10 496) except those who died or withdrew from the study before
1998 (n = 657). Women were included in the present study if they reported
a physician diagnosis of asthma on an original form and reiterated a physician
diagnosis of asthma on the supplemental form 2 to 10 years later. Women were
excluded if they reported a physician diagnosis of chronic obstructive pulmonary
disease (COPD) or alternative pulmonary condition or if they declined to provide
information on asthma severity or medication use. Validity of the case definition
of asthma and a case definition of physician diagnosis of COPD has been previously
established in the Nurses' Health Study.21-22
Asthma symptoms, severity, and medication use were assessed on the 1998
supplemental questionnaire. Other variables were ascertained by prior questionnaires
sent to all participants in the Nurses' Health Study in 1992 (socioeconomic
status and confidante items only), 1996, and 1998. The most recent information
(ie, from 1998) was used for variables in which inferences were unlikely to
be subject to reverse causality. That is, data from 1998 were used for variables
such as age and menopausal status that were unlikely to be affected by adherence
with asthma medications. Prospectively collected data were used for variables
in which inferences might otherwise be attributable to reverse causality.
For example, caregiving was ascertained in 1996 and prospectively compared
with asthma medication adherence in 1998.
EXPOSURE MEASURES
Physical Factors
Asthma severity was classified according to NAEPP guidelines,3 modified slightly to match items on the supplemental
questionnaire (Table 1). Classification
was based on symptoms at the time of the questionnaire; respondents continued
to take asthma medications at the time of symptom report. Since all participants
in the Nurses' Health Study belong to the same profession and have, in most
cases, a similar educational background, variability in socioeconomic status
was approximated by participants' husbands' educational attainment. The number
of comorbid conditions was calculated as the number of other major diseases
reported by the participant, such as cardiovascular disease (including hyperlipidemia),
diabetes, and cancer. The number of nonasthma regular medications included
daily aspirin or other nonsteroidal anti-inflammatory drug use.
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Table 1. Classification Criteria for Asthma Severity in the Nurses'
Health Study Based on National Asthma Education and Prevention Program Recommendations3
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Psychosocial Factors
Caregiving was assessed with the question, "Outside of your employment,
do you provide regular care for any of the following: disabled or ill spouse,
parent, or other person, and non-ill child or grandchild?" Participants were
also asked, "How stressful would you say it is to provide care to the individuals
mentioned above?"
Subcategories of the Medical Outcomes Study 36-Item Short-Form Health
Survey23 (SF-36) were used to estimate depressive
symptoms, vitality, social function, and role limitations due to emotional
problems. These subcategories were picked for likely relevance to medication
adherence. The SF-36 has been used in clinical and epidemiologic studies and
is internally consistent, reliable, and predictive of health outcomes in a
variety of populations.24-26
Subcategories were assessed and calculated using standard methods.27
MEDICATION GUIDELINE ADHERENCE
Adherence to NAEPP medication guidelines was estimated by medication
use in the year preceding administration of the supplemental questionnaire.
Participants were asked, "Which medication(s) have you taken for asthma within
the past year," followed by a list of medication types along with generic
and proprietary names of medications. Table
2 summarizes the NAEPP guidelines as used for classification in
this study. Individuals were considered adherent if they reported medication
use concordant with their asthma severity step. Long-acting bronchodilator
use was defined as long-acting inhaled  -agonist, theophylline, or oral -agonist.
Dose of inhaled corticosteroid was not assessed; therefore, use of any inhaled
corticosteroid satisfied our definition of adherence for mild-moderate persistent
disease (Table 2). In contrast,
the NAEPP guidelines recommend ascending dose of inhaled corticosteroid with
worsening asthma severity.
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Table 2. Classification of Medication Use Fulfilling Criteria for Adherence
Based on National Asthma Education and Prevention Program Recommendations3
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STATISTICAL ANALYSIS
Data are presented as proportions and means ± SDs. Proportions
of participants adherent with steps 2 through 4 of the NAEPP guidelines were
calculated by dividing the number taking appropriate medications by the number
of participants reporting symptoms consistent with a given guideline step.
These analyses excluded women who denied a physician visit in the preceding
2 years. Adherence was not estimated for step 1 (mild intermittent) because
control medications are not recommended for this step.
The association between guideline adherence and other factors was examined
with the  2 test. All analyses were repeated within strata
of asthma severity. Clinically relevant variables, such as age, and variables
associated with adherence at P .10 were evaluated
for inclusion in multivariate logistic regression models. Logistic regression
was used to model the association between guideline nonadherence and various
predictors after adjustment for covariates. Continuous variables were categorized
into indicator variables to avoid assumptions of linear relationships in logistic
regression models. When bivariate analyses suggested that associations differed
within strata of asthma severity, multiplicative interaction terms were tested
in the regression models. Results of all interaction testing are reported.
Odds ratios are presented with 95% confidence intervals (CIs). All P values are 2-tailed, with P<.05 considered
statistically significant. Analyses were performed using SAS statistical software
version 6.12 (SAS Institute, Cary, NC).
RESULTS
Of 9839 participants in the Nurses' Health Study who reported a physician
diagnosis of asthma and were sent the supplemental asthma questionnaire, 8197
responded and 53 died, yielding overall follow-up of 84%. Among respondents,
2356 also reported COPD or other pulmonary condition. An additional 647 did
not reconfirm a physician diagnosis of asthma (usually reporting a one-time
episode of "asthmatic bronchitis" associated with an infection), and 87 did
not provide adequate information on asthma severity or medication use. After
these exclusions, 5107 participants remained in the analysis.
The characteristics of the study population are described in Table 3 and Table 4 (first columns). The mean ± SD age was 63 ±
7 years. Forty-two percent had mild intermittent asthma, 28% had mild persistent,
25% had moderate persistent, and 5% had severe persistent asthma. Ninety-two
percent reported a physician visit in the preceding 2 years and 1% denied
such a visit; the remaining 7% had characteristics similar to participants
who reported a visit and were therefore treated as having had a visit.
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Table 3. Characteristics of Women in the Nurses' Health Study With
Physician-Diagnosed Asthma and Physical Factors Related to Adherence Among
Women With Persistent Asthma
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Table 4. Characteristics in Women in the Nurses' Health Study With
Physician-Diagnosed Asthma and Psychosocial Factors Related to Adherence Among
Women With Persistent Asthma
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Among all participants, use of asthma medications increased with asthma
severity (Figure 1) (P<.001). Fifty-one percent of women with mild persistent asthma
reported use of inhaled corticosteroids, compared with 53% with moderate persistent
and 79% with severe persistent asthma.
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Asthma medication use categorized by the National Asthma Education
and Prevention Program severity step among all participants.3 P for trend, <.001 for all medications.
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Overall adherence to NAEPP guidelines among women with persistent asthma,
excluding those who denied a physician visit in the preceding 2 years, was
55% (Table 3, third column). Adherence
varied by NAEPP severity classification. The proportion of women with mild
and moderate persistent asthma who reported taking the recommended medications
was 57% and 55%, respectively, whereas only 32% of women with severe persistent
asthma reported medication use consistent with NAEPP guidelines (P<.001). This decrement among the severe persistent group resulted
from underuse of long-acting bronchodilators (46% reported inhaled corticosteroid
and long-acting bronchodilator use) in addition to underuse of oral steroids
(49% reported inhaled corticosteroid and oral corticosteroid use).
Adherence with NAEPP guidelines was inversely associated with age and
current smoking (Table 3). Socioeconomic
status, measured by husband's educational attainment, was positively associated
with adherence, and retired women were less likely to adhere to guidelines
than working women.
Asthma characteristics predicted adherence; women who developed asthma
before age 18 years were less adherent than women with onset of symptoms after
age 45 years, whereas histories of hospitalization and hospitalization in
the preceding year were associated with higher adherence (Table 3).
Participants without comorbidities were more adherent than participants
with multiple comorbid conditions (Table
3). Other physical factors, such as menopausal status, number of
other medications taken, and obesity, were unrelated to adherence.
Few psychosocial factors were associated with adherence, despite the
relatively large number of participants in the study. Aspects of social support,
included living situation, marital status, religious heritage, and frequency
of contact with a confidante, were not associated with adherence (Table 4, third column). Adherence was higher
among participants with daily contact with a confidante than with no confidante
(44% vs 18%, respectively; P = .01) among participants
with severe persistent asthma; however, the interaction term was not statistically
significant (P = .27).
Amount of care for an ill spouse was associated with considerable reductions
in adherence (P = .02, Table 4). Other job-related potential stressors were not associated
with adherence. Categories of well-being on the SF-36 were generally not statistically
associated with guideline adherence, with the exception of role limitations
due to emotional problems (P = .03).
In multivariate analyses, the strongest predictor of nonadherence was
severe asthma (Table 5). Age was
positively and monotonically associated with nonadherence. Age and retirement
were collinear; retirement predicted nonadherence when age was removed from
the model (P<.001). Other asthma characteristics
were associated with nonadherence: women with more contact with the health
care system because of asthma exacerbations were less likely to be nonadherent
with guidelines, whereas women with younger age of onset of asthma symptoms
were more likely to be nonadherent.
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Table 5. Multivariate Predictors of Nonadherence With National Asthma
Education and Prevention Program3 Guidelines for Asthma Medication
Use Among Participants With Persistent Asthma
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Socioeconomic status, smoking, and number of comorbid medical conditions
remained significant in the multivariate analysis; however, number of hours
of caregiving and emotional role were not. The overall explanatory power of
the logistic regression model was moderate (c statistic
= 0.70). Restricting the analysis to women 60 years and older, lifelong nonsmokers,
and confirmed physician visits produced similar results.
COMMENT
In the Nurses' Health Study, a relatively socioeconomically advantaged
and medically knowledgeable population of older women, adherence to NAEPP
guidelines for the treatment of asthma was low. Overall adherence was comparable
to results from a national sample of patients with asthma.12
Participants with the most severe asthma were least likely to report use of
the appropriate array of asthma control medications. Nonadherence was best
predicted by asthma characteristics, age, and comorbid medical conditions.
Severe asthma was the strongest predictor of nonadherence in our study,
matching findings in younger populations.6, 8
The much lower compliance with NAEPP guidelines among older women with severe
asthma is alarming in light of a recent study14
that found that the greatest increase in asthma mortality in the United States
was among older women. Although most participants reported use of inhaled
corticosteroids, other long-acting medications were underused. Although we
had suspected that low adherence among women with severe disease would be
due to reticence on the part of participants and their physicians to use systemic
corticosteroids, we found that both systemic corticosteroids and long-acting
bronchodilators were underused.
We investigated predictors of adherence to NAEPP guidelines and found
that older and retired women were less likely to take appropriate asthma medications
compared with their younger, working colleagues. Both older age and retirement
predicted nonadherence independent of asthma severity, comorbidity, and other
covariates; however, these factors were collinear (overlapping) in regression
models. Therefore, the independent effect of age was hard to differentiate
from retirement. Age has been previously shown to predict nonadherence with
inhaled corticosteroids among Canadians 65 years or older, few of whom presumably
were working.13
Most physicians recognize that treating medical conditions appropriately
becomes harder as the number of conditions increases. Comorbidities were measured
and adjusted in the Canadian study and our study, and both studies found a
positive association between the number of comorbid conditions and nonadherence.
This relationship, however, did not account for the association of age and
nonadherence.
Despite the occupational similarity of participants, variation in socioeconomic
status, marked by participants' husbands' educational attainment, was independently
associated with guideline adherence. This result matches findings from other
studies encompassing wider socioeconomic gradients,7
but it did not confound the association of age and nonadherence.
Another possible explanation for the observed age gradient is increasing
social isolation among older patients.19 We
explored this factor and found that contact with a confidante was only related
to adherence among participants with severe persistent asthma. This is a potentially
important finding, but it requires confirmation given the lack of statistical
significance of the interaction of isolation and asthma severity. Other measures
of social support, including marital status and living situation, were not
associated with adherence in our study.
Greater caregiving responsibilities also have been hypothesized to affect
adherence among older patients.19 Women caring
for ill spouses were more likely to be nonadherent with asthma medications;
however, because of the small number of affected participants, this factor
did not reach statistical significance in the multivariate model. Caregiving
for other individuals, such as grandchildren, was not associated with adherence
(data not shown).
Other psychosocial factors did not contribute materially to the association
of age and adherence in this study. Role limitation due to emotional problems
on the SF-36 was associated with nonadherence in bivariate analyses, but not
in multivariate analyses. Depression is often associated with nonadherence28; however, in this study, this effect was not apparent,
possibly because we were not able to explicitly separate patient factors from
physician practice patterns.
An alternative explanation for the age gradient in care is that older
age and retirement are markers of changing insurance status. Most health plans
offered to nurses cover prescription medications, whereas Medicare does not
currently pay for prescription drugs.29 However,
a similar inverse association between age and adherence among elderly patients
( 65 years) hospitalized for asthma was noted in Ontario, where government
health insurance covers medication costs for the entire elderly population.13 We were therefore not able to account for the age
gradient in adherence with information on psychosocial factors and must conclude
that physician practice patterns or patient preferences caused the strong
gradient in guideline adherence with advancing age.
Interpretation of these results should consider that our criteria for
fulfillment of NAEPP guidelines were lenient. A report of medication use at
any time in the prior year was sufficient to fulfill criteria, as was use
of any dose of inhaled corticosteroids. No penalty was levied for overuse
of a medication (eg, short-acting -agonist) or use of a medication that
is not among medications recommended for management of chronic asthma (eg,
ipratropium bromide). Also, we underestimated NAEPP asthma severity step by
classifying participants by symptoms at treatment and without information
on nocturnal symptoms, peak expiratory flow rates, and forced expiratory volume
in 1 second.
This study is unique in assessing guideline adherence and its predictors
among older women with asthma in a well-characterized cohort with excellent
response rates and reliability. A limitation is the cross-sectional assessment
of asthma severity and medication use. This design makes it possible that
treatment caused women with severe disease to be classified as moderate and
so on. However, guideline adherence was similar for moderate persistent asthma
and mild persistent asthma, and use of all asthma control medications increased
monotonically with severity. Participants in this study are not representative
of all older patients with asthma; however, as noted herein, the proportion
adherent was similar to that in a representative sample of Americans.
Somewhat paradoxically, participants who reported an urgent office or
emergency department visit or a hospitalization were more likely to be adherent
with guidelines. Adherence with asthma medication guidelines may have caused
emergency department visits and hospitalizations; however, this reasoning
seems unlikely given extensive documentation of the beneficial effects of
inhaled corticosteroids.1-2 A
more probable explanation is that such visits highlighted underlying asthma
severity, prompting physicians to prescribe the appropriate medications and
participants to take them.
In conclusion, asthma is undertreated among older women, even among
health care professionals. Undertreatment is particularly marked among older
women with the most severe asthma and multiple comorbid medical conditions.
Physicians should make greater efforts to evaluate asthma severity and to
step-up therapy when indicated. In addition, further research is needed to
examine the role of physician prescribing patterns and patient preferences
regarding use of asthma medications among older women.
AUTHOR INFORMATION
Accepted for publication January 17, 2002.
This study was supported by grants HL-07427, PE-11001, HL-63841, HL-03533,
and CA-87969 from the National Institutes of Health, Bethesda, Md.
We thank Karen Corsano, LMS, and Gary Chase, BSc, for invaluable assistance
with the implementation of the study and Ichiro Kawachi, MD, PhD, for helpful
comments on the manuscript.
Corresponding author and reprints: Carlos A. Camargo, Jr, MD, DrPH,
Channing Laboratory, 181 Longwood Ave, Boston, MA 02115 (e-mail: carlos.camargo{at}channing.harvard.edu).
From the Channing Laboratory, Department of Medicine, Brigham and Women's
Hospital (Drs Barr, Somers, Speizer, and Camargo), and General Medicine Division
(Dr Barr) and Department of Emergency Medicine (Dr Camargo), Massachusetts
General Hospital, Harvard Medical School, Boston.
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