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Barriers to medication adherence in asthma
Accepted Manuscript Title: Barriers to medication adherence in asthma: the importance of culture and context Author: Elizabeth L. McQuaid PII: DOI: Reference:
S1081-1206(18)30222-9 https://doi.org/10.1016/j.anai.2018.03.024 ANAI 2512
To appear in:
Annals of Allergy, Asthma & Immunology
Received date: Revised date: Accepted date:
25-1-2018 12-3-2018 19-3-2018
Please cite this article as: Elizabeth L. McQuaid, Barriers to medication adherence in asthma: the importance of culture and context, Annals of Allergy, Asthma & Immunology (2018), https://doi.org/10.1016/j.anai.2018.03.024. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Barriers to Medication Adherence in Asthma: The Importance of Culture and Context Elizabeth L. McQuaid, PhD, ABPP Departments of Psychiatry and Human Behavior and Pediatrics Alpert Medical School, Brown University Corresponding Author: Elizabeth L. McQuaid Bradley/Hasbro Children’s Research Center Suite 204 1 Hoppin Street Providence, RI 02903 [email protected] Conflicts of interest: none
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Funding Source: Work on this manuscript was supported by the Hassenfeld Child Health Innovation Institute at Brown University.
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Trial Registration: Not applicable
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Keywords: Adherence, disparities, race, ethnicity
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Abbreviations/Acronyms: Non-Latino White (NLW); inhaled corticosteroids (ICS); leukotriene receptor agonists (LTRA); long-acting beta-agonists (LABA); Complementary and Alternative Medication (CAM); Limited English Proficiency (LEP).
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Word Count: 2828
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Figures: 2
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Tables: none
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Acknowledgment: This manuscript was supported, in part, with funds from the Hassenfeld Child Health Innovation Institute. The author would like to thank Mr. Michael Farrow for his assistance in manuscript preparation.
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Key Messages
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There are racial and ethnic disparities in the use of controller medications for asthma in
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prescription receipt, prescription initiation, and medication adherence once obtained.
35 36
symptoms play a role.
37 38
Individual factors such as culturally derived medication concerns and depressive
Patients with severe asthma or those with financial burdens may consider CAM as a supplemental or alternative strategy to traditional medications.
Patient-provider variables such as limited discussion of CAM use, difficulties
39
communicating with LEP patients, and cultural stereotypes likely influence lower levels
40
of adherence.
41
42 43 44
Office-based interventions (providing education, simplifying regimens, monitoring) may be effective if delivered in a culturally-informed manner.
Provider training in communication and cultural competence may increase patient receptivity to discussing and accepting controller medications.
45
Abstract:
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Objective. Significant disparities exist in asthma outcomes. Racial and ethnic minorities have
47
lower controller medication adherence, which may contribute to differences in asthma morbidity
48
between minority and non-minority groups. The objective of this review is to identify individual,
49
patient-provider communication, and systems issues that contribute to this pattern of medication
50
underuse and to discuss potential strategies for intervention.
51
Data Sources. Data were gathered from numerous sources, including reports of pharmacy and
52
medical records, observational studies, and trials.
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Study Selection. Studies analyzed factors contributing to patterns of asthma medication
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adherence that differ by race and ethnicity.
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Results. There is clear evidence of underuse of asthma controller medications among racial and
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ethnic minorities in prescription receipt, prescription initiation, and medication use once
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obtained. Individual factors such as medication beliefs and depressive symptoms play a role.
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Provider communication is also relevant, including limited discussion of Complementary and
59
Alternative Medicine (CAM) use, difficulties communicating with patients and caregivers with
60
limited English proficiency (LEP), and implicit biases regarding cultural differences. Systems
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issues (e.g., insurance status, cost) and social context factors (e.g. exposure to violence) also
62
present challenges. Culturally-informed strategies that capitalize on patient strengths and
63
training providers in culturally-informed communication strategies hold promise as intervention
64
approaches.
65
Conclusion. Disparities in controller medication use are pervasive. Identifying the sources of
66
these disparities is a critical step toward generating intervention approaches to enhance disease
67
management among the groups that bear the greatest asthma burden.
68 69 70
Introduction Asthma remains highly prevalent in the United States (US), affecting approximately 7.0
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million children (9.5%) and 18.7 million adults (7.7%),1 and disproportionately impacting racial
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and ethnic minorities.2 Concurrently, the demographic composition of the United States (US) is
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becoming increasingly diverse. Non-Latino whites (NLWs), the current majority group in the
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US currently comprise 62% of the population; this is expected to decline to approximately 44%
75
over the next four decades.3 Although immigration patterns are subject to cultural and political
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influences, overall the past several decades have seen first-generation immigrants in increasing
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numbers;3 it is projected that 17% of the US population will be foreign-born immigrants by
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2040.4 Accordingly, health care providers will continue to serve an increasingly diverse
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demographic over the next several decades.
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Racial and ethnic disparities in asthma prevalence, severity, and outcomes are well-
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documented.5 African Americans have higher asthma prevalence and greater health care
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utilization than NLWs.2 There is substantial heterogeneity in asthma prevalence, disease
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presentation and progression among Latino subgroups; however, with the exception of those of
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Mexican descent, Latinos have higher asthma prevalence and worse asthma outcomes relative to
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NLWs, including higher rates of urgent health care utilization and hospitalization.6,7
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One of the core features of disease management for patients with persistent asthma is
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daily use of anti-inflammatory medications, such as inhaled corticosteroids (ICS), leukotriene
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receptor agonists (LTRA), and/or medications that combine ICS and long-acting beta-agonists
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(LABA).8 Adherence to controller medications has a number of necessary components (Figure
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1).9 A health care provider must begin a prescription and clearly communicate expectations for
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use to the patient and family, the patient or caregiver must fill the prescription, and the patient
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must take the medication as directed and not discontinue it prematurely.9
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There is consistent evidence that adherence to controller medications across each of these
94
steps is suboptimal. Many patients do not initiate controller medications when prescribed,10,11
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fill medications only once after an initial prescription (e.g.12,13), or discontinue controller
96
medications prematurely, despite risk of exacerbation.14 When medications have been prescribed
97
and filled, electronic monitoring of medication use consistently yields adherence rates of less
98
than 70% of prescribed doses and often lower, in some reports ~ 60% for adult patients (e.g.,15),
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~ 50% among pediatric patients (e.g.,16), and even lower among some populations, such as low-
100
income adolescents (e.g., 33-41%,17).
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There is substantial evidence that patients from diverse racial/ethnic backgrounds have
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lower medication adherence relative to NLWs; as a result, poor medication adherence is
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considered a potential contributor to disparities in asthma course and outcomes.5 Lower rates of
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asthma medication use among minorities have been found across studies of medication
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prescription and initiation in adults18,19 and children20-22 and in actual use of medication once
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obtained in adults,15 adolescents,23,24 and children.25 The reasons for this consistent pattern of
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lower medication adherence are complex and multidetermined, and likely complicated by the
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additional effects of socioeconomic status and disadvantage commonly associated with minority
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status.5
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A recent study with adults, adolescents, and parents of children with asthma provides a
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useful framework for understanding facilitators and barriers to asthma medication adherence
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from the patient perspective.26 Qualitative analyses identified three core areas of responsibility
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for medication adherence behavior, including (1) the individual patient (factors such as
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cognition, preferences), (2) the patient-physician interaction (communication, relationship) and
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(3) the health care system (e.g., resources, insurance coverage26). In the following sections, we
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evaluate the evidence for factors that may account for racial and ethnic disparities in medication
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adherence from this framework, and conclude with recommendations for clinical practice and
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future research. Our review is focused on African American and Latino patients with asthma as
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the majority of studies have been conducted with these populations. Future work is necessary to
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identify medication adherence patterns among the numerous minority groups of increasingly
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culturally diverse US.
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Individual Patient Factors
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Medication Beliefs. Individual beliefs about medication use may be influenced by a host
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of factors, including culture, individual preference, and family experience, all of which likely
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affect patient acceptance of controller medications when prescribed. Adults have concerns about
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the use of controller medications for their asthma, such as fear of side effects and
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dependence;15,27 parents of children with asthma have similar concerns.28,29 Further, research
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with diverse samples has revealed greater negative beliefs and more concerns about asthma
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medication found among minority groups, including African American patients15,30 and
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Latinos.31,32 It is likely that these beliefs derive, at least in part, from well-documented concerns
131
among racial and ethnic minorities about participation in medical research and medical care in
132
general.33
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There is some evidence that these beliefs and concerns about controller medications play
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a role in the lower levels of medication adherence. McQuaid and colleagues found that belief in
135
medication necessity was associated with reported controller medication use in a sample of
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children with asthma, including Island Puerto Rican children, Latino children residing on the
137
mainland, and NLW children.25 In a related study from the same sample, parental belief in the
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medication necessity differed by ethnic group, and was associated with objectively monitored
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controller medication adherence.25 Le and colleagues27 evaluated the association between
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minority status, medication beliefs, and ICS use among a sample of 86 adults with asthma.
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Lower rates of adherence were found among the adults of minority status, and negative beliefs
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about asthma medications mediated the association between minority status and adherence.27
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These findings suggest that patients and parents of children with asthma have more concerns
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regarding controller medication use, which may, in turn, impact their adherence.
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Preference for Complementary and Alternative Medicine. Complementary and alternative
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medicine (CAM) refers to strategies or treatments that may complement or replace traditional
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medical treatment.34 CAM approaches for asthma include herbal remedies, as well as mind and
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body practices, such as acupuncture, relaxation/breathing exercises, and spirituality/prayer.35
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CAM use is common among patients with asthma; an estimated 26% of adults with asthma36
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report using at least one form of CAM for asthma management. Estimates of CAM use among
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children with asthma vary widely between studies, ranging from 27%37 to 65%.38 CAM use for
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asthma is more common among certain racial and ethnic groups, including both African
153
Americans38,39 and Latinos.40,41
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It is tempting to conclude that increased preference for CAM explains lower rates of
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controller medication adherence found in diverse groups; however, this relationship is not
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straightforward. In one study with inner-city adults with asthma, use of herbal remedies was
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associated with decreased self-reported adherence to ICS.42 Other studies have found no
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association between CAM use and controller medication adherence,40,42 or even positive
159
associations within some subgroups, such as NLWs.40 CAM use does appear to be more common
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among those with severe disease or poorly controlled asthma (e.g.,37,39,42), and among patients
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who experience cost barriers to obtaining medications.37,40 These findings suggest CAM is not
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necessarily a replacement for conventional medications solely due to preference, but that it may
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be used to supplement traditional care for those with severe disease, or as an alternative when
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medications are not easily obtained, highlighting the importance of asking patients and families
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about CAM use and its role in asthma management.
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Depressive Symptoms. There is evidence that symptoms of depression also contribute to increased risk for poor medication adherence. Maternal depressive symptoms have been
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correlated with adherence difficulties among young inner-city children with asthma.43
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Depressive symptoms have also been associated with poor medication adherence among
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adolescents and young adults with asthma (e.g.,44,45). Studies including diverse samples of adults
171
show a similar pattern. For example, Smith and colleagues evaluated patterns of medication
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adherence in a sample of adults (80% African American) hospitalized for asthma, and found
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lower levels of medication adherence post-discharge among those with more depressive
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symptoms.46 In another study, depressive symptoms were associated with lower self-reported
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adherence to controller medications in a diverse sample of elderly patients with asthma.47 It is
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unlikely that increased depressive symptoms completely explains disparities in controller
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medication adherence. A constellation of adverse factors such as increased stress associated with
178
difficult life circumstances likely play a role in increasing mental health issues, and in
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combination these factors may affect medication use.48
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Patient Physician Interaction
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Initial prescription of controller medications and ongoing monitoring for their use arises
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within the patient-physician encounter. There is evidence to suggest that African American and
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Latino patients with asthma are less likely to initiate a controller medication for asthma (either
184
due to not receiving a prescription from a physician or not filling one that was received). This
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finding is consistent among African American adults in managed care settings,19 Latino adults,18
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Latino children in community samples,22,32 African American and Latino children in a Medicaid
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managed care sample,20 and minority children with asthma post-hospitalization.21 Because a
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number of studies are based on either patient report or insurance claims, it is difficult to
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determine if a prescription was never written by the health care provider, or if it was provided
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and not filled by the patient or caregiver.
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Language Differences. Limited English proficiency (LEP), often associated with additional
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factors such as socioeconomic disadvantage and low levels of acculturation, may result in
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communication barriers in patient-physician interactions.48 Studies of communication patterns in
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the health care setting indicate that providers may spend less time listening and making fewer
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supportive statements when working with families with LEP, even when trained interpreters are
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used.48 There is some evidence that LEP in asthma patients is related to less effective patient
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care. Data from a four-state survey indicated that Spanish speaking Latino parents of children
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with asthma, but not African American and Latino children with English speaking parents, had
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poorer experiences with care (i.e. less communication about specific asthma management
200
practices) than white children.49 In another study with a sample of elderly Latino patients with
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asthma, LEP was associated with lower self-reported medication adherence and worse health
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outcomes.50 There are some data to indicate that, in general, underuse of professional interpreter
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services and reliance on untrained ad hoc interpreters may compromise patient care.51
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There is mounting evidence that health care providers’ unintentional or implicit biases may
205
play a role in disparities in health care,52,53 affecting communication patterns with patients,52,54 or
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even management recommendations.54 Research regarding implicit bias among providers and
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subsequent asthma management patterns is limited; in one study utilizing case vignettes,54
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pediatricians’ biases (as measured by the Implicit Association Test55) were associated with
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clinical decision making for pain medication, but not for asthma management. Given
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associations found between implicit bias and provider behavior found in other studies,52,54,56 this
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area of investigation merits further study.
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Systems Factors
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Insurance Coverage. Some research has evaluated whether public insurance coverage,
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commonly associated with minority status, is associated with lower rates of controller
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medication prescription and use than private insurance coverage. In two studies that assessed
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prescription patterns, one through chart review of Emergency Department records adults with
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asthma,57 and the other by evaluation of electronic medical record among children with asthma,58
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there were no differences in prescription rates of controller medication by insurance status
219
(public vs. private). In contrast, there are data to suggest differential patterns of controller
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medication prescription upon hospital discharge by insurance status. In a four-state study,
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Merrick and colleagues59 found that publicly insured children with asthma in each state were
222
more likely to be discharged on suboptimal medication regimens than those with private
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insurance. Similarly, a study of pediatric and adult inpatients with asthma discharged from
224
hospitals in the Chicago area found that publicly insured patients were less likely to be
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discharged on controller medications than privately insured patients.60
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Other Economic and Social Barriers. There are other broader systems factors that may
227
affect medication adherence. Some have noted that limited coverage for medications and
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additional out-of-pocket costs may affect prescription initiation and consistent medication use.61
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This “cost-related non-adherence” is an additional variable that may impact some patients from
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minority populations with limited incomes.62 There is also some evidence that for families who
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live in disadvantaged areas, exposure to violence and crime affects consistent medication use,
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even after adjusting for socioeconomic factors,63 suggesting that features of the social
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environment have links to asthma management behaviors such as medication adherence. Based
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on the limited data in this area, further investigation is warranted.
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Conclusions and Potential Intervention Strategies
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There is clear evidence of underuse of controller medications for asthma among racial
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and ethnic minorities. This occurs at many levels, including 1) the initial prescription of
238
medications in some contexts, such as at hospitalization discharge for publicly insured
239
patients,59,60 2) filling the prescription once initiated,19-21 and 3) taking medication once
240
obtained.15,25
241
There are numerous challenges to consistent adherence to controller medication for racial
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and ethnic minority patients with asthma. At the individual level, cultural differences in beliefs
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about traditional medications and mental health concerns such as depressive symptoms are
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associated with lower levels of controller medication use.27,32 Health care provider biases and
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communication patterns with culturally diverse patients, particularly those with LEP, likely
246
affect providers’ skill in communicating about controller medication use in a culturally sensitive
247
manner.49,50 Systems factors, such as health care coverage,57,58 cost,61 and features of the
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community environment such as exposure to violence,59 also present challenges to effective
249
disease management and consistent medication use. What then, can be done to address these
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disparities in medication use and subsequent outcomes? We provide an overview of potential
251
interventions in Figure 2, focusing on approaches with potential to improve medication
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prescription, initiation, and use among racial and ethnic minorities with asthma.
253
Individual interventions to increase medication adherence such as education, electronic
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tracking, and simplifying regimens have demonstrated some modest effects in increasing
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controller medication adherence for general samples of children and adults with asthma.64
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Employing a culturally tailored approach also appears to improve outcomes for asthma
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management interventions for diverse samples.65 Given the generally modest results found across
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interventions, an individualized approach that first addresses concerns about medications,
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carefully considering cultural beliefs and preferences, is the most likely to effect change. Family
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resources and routines have been found to support consistent medication use in diverse samples
261
(e.g.,25), and represent an important resource among diverse families.
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There is increasing evidence that training in both patient-centered communication and
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cultural competence can yield important effects on patient adherence. A review of the effects of
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communication training for physicians66 revealed positive effects on patient adherence across
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many medical conditions. Consistent with these findings, there is some evidence that
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interventions that emphasize shared-decision making between physicians and patients may
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improve medication adherence.67 Cultural competence training is provides health services with
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awareness of and respect for the differing health beliefs, practices, and needs of diverse patient
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groups.68 There have been fewer studies of the effects of physician cultural competence training
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on asthma medication adherence. In one early study of pediatric asthma practices in Medicaid
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health maintenance organizations, Lieu and colleagues found that practice sites with policies to
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promote cultural competence in staff were less likely to have patients underusing controller
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medications for asthma.69 Taken together, these findings suggest that providing training to
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promote effective communication with culturally diverse patient populations has the potential to
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improve patient adherence to provider recommendations.
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Increasing health care provider awareness of their patients’ use of CAM, beliefs about
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controller medications, and general health concerns may also promote more effective
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communication about asthma medications in the context of the clinical encounter, which
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arguably is the most effective channel through which to increase adherence to controller
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medications. CAM use is not regularly disclosed in medical encounters, and patients from
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minority groups are less likely to discuss self-initiated CAM approaches.70 Interestingly, in one
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recent study,71 physicians who were aware of patients’ concerns about asthma medications and
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use of CAM for asthma were more likely to initiate conversations about these issues in the
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context of a clinical encounter. Given recent data linking perceived discrimination with poor
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asthma control among African American youth with asthma,72 the area of physician-patient
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interaction, asthma management, and disparities in medication use for asthma merits further
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study. Development of interventions to increase physician awareness of cultural stereotypes and
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implicit biases that may impact communication in the patient-provider relationship is necessary.
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Systems factors such as cost and coverage are challenging to change without substantial
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advocacy. At a minimum, providers can and should monitor what is covered by patients’
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insurance to evaluate potential barriers to prescription initiation and continued medication use.
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Similarly, provider awareness of the sociocultural context in which patients reside can help
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identify pertinent stressors and challenges to effective disease management.
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Conclusion
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The sociodemographic diversity of the US is likely to continue to increase over the next
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several decades. Our research and clinical approaches must evolve to identify the most effective
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ways to support patients with asthma from diverse backgrounds to manage their disease
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effectively, including consistent medication use when indicated. It will also be increasingly
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important to promote strategies to enhance communication regarding disease management
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between providers and patients from a range of cultures. Interventions that consider not only
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patients’ cultural beliefs, but also providers’ implicit biases and methods of interacting with
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diverse patients and systems barriers to care among those at risk will be necessary to address
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disparities in asthma management and subsequent health outcomes.
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Adams SK, Koinis-Mitchell D. Perspectives on complementary and alternative therapies in asthma. Expert Rev. Clin. Immunol. 2008;4(6):703-711. Morgan W, Center H, Arms-Chavez C, LoBello SG. Complementary and alternative medicine use and asthma: Relation to asthma severity and comorbid chronic disease. Journal of Asthma. 2014;51(3):333-338. Shen J, Oraka E. Complementary and alternative medicine (CAM) use among children with current asthma. Preventive Medicine. 2012;54(1):27-31. Sidora-Arcoleo K, Yoos HL, McMullen A, Kitzman H. Complementary and alternative medicine use in children with asthma: Prevalence and sociodemographic profile of users. Journal of Asthma. 2007;44(3):169-175. George M, Birck K, Hufford DJ, Jemmott LS, Weaver TE. Beliefs About Asthma and Complementary and Alternative Medicine in Low‐Income Inner‐City African‐American Adults. Journal of General Internal Medicine. 2006;21(12):1317-1324. McQuaid EL, Fedele DA, Adams SK, et al. Complementary and alternative medicine use and adherence to asthma medications among Latino and non-Latino white families. Acad Pediatr. 2014;14(2):192-199. Pachter LM, Weller SC, Baer RD, et al. Variation in asthma beliefs and practices among mainland Puerto Ricans, Mexican-Americans, Mexicans, and Guatemalans. Journal of Asthma. 2002;39(2):119-134. Roy A, Lurslurchachai L, Halm EA, Li X-M, Leventhal H, Wisnivesky JP. Use of herbal remedies and adherence to inhaled corticosteroids among inner-city asthmatic patients. Ann Allergy Asthma Immunol. 2010;104(2):132-138. Barlett S, Krishnan J, Rickert K, Butz A, Malveaux F, Rand C. Maternal depressive symptoms and adherence to therapy in inner-city children with asthma. Pediatrics. 2004;113(2):229-237. Bender B. Risk taking, depression, adherence, and symptom control in adolescents and young adults with asthma. Am J Respir Crit Care Med. 2006;173(9):953-957. Bender B, Zhang L. Negative affect, medication adherence, and asthma control in children. J Allergy Clin Immunol. 2008;122(3):490-495. Smith A, Krishnan JA, Bilderback A, Riekert KA, Rand CS, Bartlett SJ. Depressive symptoms and adherence to asthma therapy after hospital discharge. Chest. 2006;130(4):1034-1038. Krauskopf KA, Sofianou A, Goel MS, et al. Depressive symptoms, low adherence, and poor asthma outcomes in the elderly. Journal of Asthma 2013;50(3):260-266. Thornton JD, Pham K, Engelberg RA, Jackson JC, Curtis JR. Families with limited English proficiency receive less information and support in interpreted ICU family conferences. Critical Care Medicine. 2009;37(1):89. Inkelas M, Garro N, McQuaid E, Ortega A. Race/ethnicity, language, and asthma care: Findings from a four state survey. Ann Allergy Asthma Immunol. 2008;100:120-127. Wisnivesky JP, Krauskopf K, Wolf MS, et al. The association between language proficiency and outcomes of elderly patients with asthma. Ann Allergy Asthma Immunol. 2012;109(3):179-184. Ramirez D, Engel KG, Tang TS. Language interpreter utilization in the emergency department setting: A clinical review. Journal of health care for the poor and underserved. 2008;19(2):352-362.
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52. 53. 54.
55. 56.
57.
58.
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61.
62.
63.
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65.
66. 67.
Paradies Y, Truong M, Priest N. A systematic review of the extent and measurement of healthcare provider racism. Journal of General Internal Medicine. 2014;29(2):364-387. Institute of Medicine. Unequal treatment: Confronting racial and ethnic disparities in health care. Washington, DC2002. Johnson RL, Roter D, Powe NR, Cooper LA. Patient race/ethnicity and quality of patient–physician communication during medical visits. Am J Public Health. 2004;94(12):2084-2090. Greenwald AG, McGhee DE, Schwartz JLK. Measuring individual differences in implicit cognition: the implicit association test. J. Pers. Soc. Psychol. 1998;74(6):1464. Sabin JA, Greenwald AG. The influence of implicit bias on treatment recommendations for 4 common pediatric conditions: pain, urinary tract infection, attention deficit hyperactivity disorder, and asthma. Am J Public Health. 2012;102(5):988-995. Hasegawa K, Stoll SJ, Ahn J, Kysia RF, Sullivan AF, Camargo Jr CA. Association of insurance status with severity and management in ED patients with asthma exacerbation. Western Journal of Emergency Medicine. 2016;17(1):22. Finkelstein JA, Barton MB, Donahue JG, Algatt-Bergstrom P, Markson LE, Platt R. Comparing asthma care for Medicaid and non-Medicaid children in a health maintenance organization. Archives of pediatrics & adolescent medicine. 2000;154(6):563-568. Merrick NJ, Houchens R, Tillisch S, Berlow B, Landon C. Quality of hospital care of children with asthma: Medicaid versus privately insured patients. Journal of Health Care for the Poor and Underserved. 2001;12(2):192-207. Lantner R, Brennan RA, Gray L, McElroy D, Research Outcomes Committee of the Suburban Asthma Consortium. Inpatient management of asthma in the Chicago suburbs: The Suburban Asthma Management Initiative (SAMI). Journal of Asthma. 2005;42(1):55-63. Briesacher BA, Gurwitz JH, Soumerai SB. Patients at-risk for cost-related medication nonadherence: A review of the literature. Journal of General Internal Medicine. 2007;22(6):864-871. Frankenfield DL, Wei II, Anderson KK, Howell BL, Waldo D, Sekscenski E. Prescription medication cost-related non-adherence among Medicare CAHPS respondents: Disparity by Hispanic ethnicity. Journal of Health Care for the Poor and Underserved. 2010;21(2):518-543. Williams LK, Joseph CL, Peterson EL, et al. Race-ethnicity, crime, and other factors associated with adherence to inhaled corticosteroids. J Allergy Clin Immunol. 2007;119(1):168-175. Normansell R, Kew KM, Stovold E, Mathioudakis AG, Dennett E. Interventions to improve inhaler technique and adherence to inhaled corticosteroids in children with asthma. Paediatric Respiratory Reviews. 2017;23:53-55. McCallum GB, Morris PS, Brown N, Chang AB. Culture‐specific programs for children and adults from minority groups who have asthma. The Cochrane Library. 2017;8:CD006580. Zolnierek KB, Dimatteo MR. Physician communication and patient adherence to treatment: A meta-analysis. Medical Care. 2009;47(8):826-834. Kew KM, Malik P, Aniruddhan K, Normansell R. Shared decision-making for people with asthma. Cochrane Database Syst Rev. 2017;10(8):CD012330.
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68.
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70.
71.
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Office of Minority Health. National standards for culturally linguistincally appropriate services (CLAS) in health and health care. U.S. Department of Health and Human Services, Washington, D.C. 2013. Accessed March 21, 2017. Lieu TA, Finkelstein JA, Lozano P, et al. Cultural competence policies and other predictors of asthma care quality for Medicaid-insured children. Pediatrics. 2004;114(1):e102-110. Chao MT, Wade C, Kronenberg F. Disclosure of complementary and alternative medicine to conventional medical providers: Variation by race/ethnicity and type of CAM. Journal of the National Medical Association. 2008;100(11):1341-1349. George M, Abboud S, Pantalon MV, Sommers MLS, Mao J, Rand C. Changes in clinical conversations when providers are informed of asthma patients' beliefs about medication use and integrative medical therapies. Heart & Lung: The Journal of Acute and Critical Care. 2016;45(1):70-78. Thakur N, Barcelo NE, Borrell LN, et al. Perceived discrimination associated with asthma and related outcomes in minority youth: The GALA II and SAGE II studies. Chest. 2017;151(4):804-812.
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Figure 1. Components of Medication Adherence
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Figure 2.
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Intervention Approaches to Address Disparities in Medication Use
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S1081-1206(18)30222-9 https://doi.org/10.1016/j.anai.2018.03.024 ANAI 2512
To appear in:
Annals of Allergy, Asthma & Immunology
Received date: Revised date: Accepted date:
25-1-2018 12-3-2018 19-3-2018
Please cite this article as: Elizabeth L. McQuaid, Barriers to medication adherence in asthma: the importance of culture and context, Annals of Allergy, Asthma & Immunology (2018), https://doi.org/10.1016/j.anai.2018.03.024. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
1 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Barriers to Medication Adherence in Asthma: The Importance of Culture and Context Elizabeth L. McQuaid, PhD, ABPP Departments of Psychiatry and Human Behavior and Pediatrics Alpert Medical School, Brown University Corresponding Author: Elizabeth L. McQuaid Bradley/Hasbro Children’s Research Center Suite 204 1 Hoppin Street Providence, RI 02903 [email protected] Conflicts of interest: none
16 17
Funding Source: Work on this manuscript was supported by the Hassenfeld Child Health Innovation Institute at Brown University.
18
Trial Registration: Not applicable
19
Keywords: Adherence, disparities, race, ethnicity
20 21 22
Abbreviations/Acronyms: Non-Latino White (NLW); inhaled corticosteroids (ICS); leukotriene receptor agonists (LTRA); long-acting beta-agonists (LABA); Complementary and Alternative Medication (CAM); Limited English Proficiency (LEP).
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Word Count: 2828
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Figures: 2
25
Tables: none
26 27 28 29
Acknowledgment: This manuscript was supported, in part, with funds from the Hassenfeld Child Health Innovation Institute. The author would like to thank Mr. Michael Farrow for his assistance in manuscript preparation.
30 31
Key Messages
32
There are racial and ethnic disparities in the use of controller medications for asthma in
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2 33 34
prescription receipt, prescription initiation, and medication adherence once obtained.
35 36
symptoms play a role.
37 38
Individual factors such as culturally derived medication concerns and depressive
Patients with severe asthma or those with financial burdens may consider CAM as a supplemental or alternative strategy to traditional medications.
Patient-provider variables such as limited discussion of CAM use, difficulties
39
communicating with LEP patients, and cultural stereotypes likely influence lower levels
40
of adherence.
41
42 43 44
Office-based interventions (providing education, simplifying regimens, monitoring) may be effective if delivered in a culturally-informed manner.
Provider training in communication and cultural competence may increase patient receptivity to discussing and accepting controller medications.
45
Abstract:
46
Objective. Significant disparities exist in asthma outcomes. Racial and ethnic minorities have
47
lower controller medication adherence, which may contribute to differences in asthma morbidity
48
between minority and non-minority groups. The objective of this review is to identify individual,
49
patient-provider communication, and systems issues that contribute to this pattern of medication
50
underuse and to discuss potential strategies for intervention.
51
Data Sources. Data were gathered from numerous sources, including reports of pharmacy and
52
medical records, observational studies, and trials.
53
Study Selection. Studies analyzed factors contributing to patterns of asthma medication
54
adherence that differ by race and ethnicity.
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3 55
Results. There is clear evidence of underuse of asthma controller medications among racial and
56
ethnic minorities in prescription receipt, prescription initiation, and medication use once
57
obtained. Individual factors such as medication beliefs and depressive symptoms play a role.
58
Provider communication is also relevant, including limited discussion of Complementary and
59
Alternative Medicine (CAM) use, difficulties communicating with patients and caregivers with
60
limited English proficiency (LEP), and implicit biases regarding cultural differences. Systems
61
issues (e.g., insurance status, cost) and social context factors (e.g. exposure to violence) also
62
present challenges. Culturally-informed strategies that capitalize on patient strengths and
63
training providers in culturally-informed communication strategies hold promise as intervention
64
approaches.
65
Conclusion. Disparities in controller medication use are pervasive. Identifying the sources of
66
these disparities is a critical step toward generating intervention approaches to enhance disease
67
management among the groups that bear the greatest asthma burden.
68 69 70
Introduction Asthma remains highly prevalent in the United States (US), affecting approximately 7.0
71
million children (9.5%) and 18.7 million adults (7.7%),1 and disproportionately impacting racial
72
and ethnic minorities.2 Concurrently, the demographic composition of the United States (US) is
73
becoming increasingly diverse. Non-Latino whites (NLWs), the current majority group in the
74
US currently comprise 62% of the population; this is expected to decline to approximately 44%
75
over the next four decades.3 Although immigration patterns are subject to cultural and political
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influences, overall the past several decades have seen first-generation immigrants in increasing
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numbers;3 it is projected that 17% of the US population will be foreign-born immigrants by
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4 78
2040.4 Accordingly, health care providers will continue to serve an increasingly diverse
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demographic over the next several decades.
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Racial and ethnic disparities in asthma prevalence, severity, and outcomes are well-
81
documented.5 African Americans have higher asthma prevalence and greater health care
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utilization than NLWs.2 There is substantial heterogeneity in asthma prevalence, disease
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presentation and progression among Latino subgroups; however, with the exception of those of
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Mexican descent, Latinos have higher asthma prevalence and worse asthma outcomes relative to
85
NLWs, including higher rates of urgent health care utilization and hospitalization.6,7
86
One of the core features of disease management for patients with persistent asthma is
87
daily use of anti-inflammatory medications, such as inhaled corticosteroids (ICS), leukotriene
88
receptor agonists (LTRA), and/or medications that combine ICS and long-acting beta-agonists
89
(LABA).8 Adherence to controller medications has a number of necessary components (Figure
90
1).9 A health care provider must begin a prescription and clearly communicate expectations for
91
use to the patient and family, the patient or caregiver must fill the prescription, and the patient
92
must take the medication as directed and not discontinue it prematurely.9
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There is consistent evidence that adherence to controller medications across each of these
94
steps is suboptimal. Many patients do not initiate controller medications when prescribed,10,11
95
fill medications only once after an initial prescription (e.g.12,13), or discontinue controller
96
medications prematurely, despite risk of exacerbation.14 When medications have been prescribed
97
and filled, electronic monitoring of medication use consistently yields adherence rates of less
98
than 70% of prescribed doses and often lower, in some reports ~ 60% for adult patients (e.g.,15),
99
~ 50% among pediatric patients (e.g.,16), and even lower among some populations, such as low-
100
income adolescents (e.g., 33-41%,17).
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5 101
There is substantial evidence that patients from diverse racial/ethnic backgrounds have
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lower medication adherence relative to NLWs; as a result, poor medication adherence is
103
considered a potential contributor to disparities in asthma course and outcomes.5 Lower rates of
104
asthma medication use among minorities have been found across studies of medication
105
prescription and initiation in adults18,19 and children20-22 and in actual use of medication once
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obtained in adults,15 adolescents,23,24 and children.25 The reasons for this consistent pattern of
107
lower medication adherence are complex and multidetermined, and likely complicated by the
108
additional effects of socioeconomic status and disadvantage commonly associated with minority
109
status.5
110
A recent study with adults, adolescents, and parents of children with asthma provides a
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useful framework for understanding facilitators and barriers to asthma medication adherence
112
from the patient perspective.26 Qualitative analyses identified three core areas of responsibility
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for medication adherence behavior, including (1) the individual patient (factors such as
114
cognition, preferences), (2) the patient-physician interaction (communication, relationship) and
115
(3) the health care system (e.g., resources, insurance coverage26). In the following sections, we
116
evaluate the evidence for factors that may account for racial and ethnic disparities in medication
117
adherence from this framework, and conclude with recommendations for clinical practice and
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future research. Our review is focused on African American and Latino patients with asthma as
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the majority of studies have been conducted with these populations. Future work is necessary to
120
identify medication adherence patterns among the numerous minority groups of increasingly
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culturally diverse US.
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Individual Patient Factors
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Medication Beliefs. Individual beliefs about medication use may be influenced by a host
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of factors, including culture, individual preference, and family experience, all of which likely
125
affect patient acceptance of controller medications when prescribed. Adults have concerns about
126
the use of controller medications for their asthma, such as fear of side effects and
127
dependence;15,27 parents of children with asthma have similar concerns.28,29 Further, research
128
with diverse samples has revealed greater negative beliefs and more concerns about asthma
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medication found among minority groups, including African American patients15,30 and
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Latinos.31,32 It is likely that these beliefs derive, at least in part, from well-documented concerns
131
among racial and ethnic minorities about participation in medical research and medical care in
132
general.33
133
There is some evidence that these beliefs and concerns about controller medications play
134
a role in the lower levels of medication adherence. McQuaid and colleagues found that belief in
135
medication necessity was associated with reported controller medication use in a sample of
136
children with asthma, including Island Puerto Rican children, Latino children residing on the
137
mainland, and NLW children.25 In a related study from the same sample, parental belief in the
138
medication necessity differed by ethnic group, and was associated with objectively monitored
139
controller medication adherence.25 Le and colleagues27 evaluated the association between
140
minority status, medication beliefs, and ICS use among a sample of 86 adults with asthma.
141
Lower rates of adherence were found among the adults of minority status, and negative beliefs
142
about asthma medications mediated the association between minority status and adherence.27
143
These findings suggest that patients and parents of children with asthma have more concerns
144
regarding controller medication use, which may, in turn, impact their adherence.
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Preference for Complementary and Alternative Medicine. Complementary and alternative
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medicine (CAM) refers to strategies or treatments that may complement or replace traditional
147
medical treatment.34 CAM approaches for asthma include herbal remedies, as well as mind and
148
body practices, such as acupuncture, relaxation/breathing exercises, and spirituality/prayer.35
149
CAM use is common among patients with asthma; an estimated 26% of adults with asthma36
150
report using at least one form of CAM for asthma management. Estimates of CAM use among
151
children with asthma vary widely between studies, ranging from 27%37 to 65%.38 CAM use for
152
asthma is more common among certain racial and ethnic groups, including both African
153
Americans38,39 and Latinos.40,41
154
It is tempting to conclude that increased preference for CAM explains lower rates of
155
controller medication adherence found in diverse groups; however, this relationship is not
156
straightforward. In one study with inner-city adults with asthma, use of herbal remedies was
157
associated with decreased self-reported adherence to ICS.42 Other studies have found no
158
association between CAM use and controller medication adherence,40,42 or even positive
159
associations within some subgroups, such as NLWs.40 CAM use does appear to be more common
160
among those with severe disease or poorly controlled asthma (e.g.,37,39,42), and among patients
161
who experience cost barriers to obtaining medications.37,40 These findings suggest CAM is not
162
necessarily a replacement for conventional medications solely due to preference, but that it may
163
be used to supplement traditional care for those with severe disease, or as an alternative when
164
medications are not easily obtained, highlighting the importance of asking patients and families
165
about CAM use and its role in asthma management.
166 167
Depressive Symptoms. There is evidence that symptoms of depression also contribute to increased risk for poor medication adherence. Maternal depressive symptoms have been
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8 168
correlated with adherence difficulties among young inner-city children with asthma.43
169
Depressive symptoms have also been associated with poor medication adherence among
170
adolescents and young adults with asthma (e.g.,44,45). Studies including diverse samples of adults
171
show a similar pattern. For example, Smith and colleagues evaluated patterns of medication
172
adherence in a sample of adults (80% African American) hospitalized for asthma, and found
173
lower levels of medication adherence post-discharge among those with more depressive
174
symptoms.46 In another study, depressive symptoms were associated with lower self-reported
175
adherence to controller medications in a diverse sample of elderly patients with asthma.47 It is
176
unlikely that increased depressive symptoms completely explains disparities in controller
177
medication adherence. A constellation of adverse factors such as increased stress associated with
178
difficult life circumstances likely play a role in increasing mental health issues, and in
179
combination these factors may affect medication use.48
180
Patient Physician Interaction
181
Initial prescription of controller medications and ongoing monitoring for their use arises
182
within the patient-physician encounter. There is evidence to suggest that African American and
183
Latino patients with asthma are less likely to initiate a controller medication for asthma (either
184
due to not receiving a prescription from a physician or not filling one that was received). This
185
finding is consistent among African American adults in managed care settings,19 Latino adults,18
186
Latino children in community samples,22,32 African American and Latino children in a Medicaid
187
managed care sample,20 and minority children with asthma post-hospitalization.21 Because a
188
number of studies are based on either patient report or insurance claims, it is difficult to
189
determine if a prescription was never written by the health care provider, or if it was provided
190
and not filled by the patient or caregiver.
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Language Differences. Limited English proficiency (LEP), often associated with additional
192
factors such as socioeconomic disadvantage and low levels of acculturation, may result in
193
communication barriers in patient-physician interactions.48 Studies of communication patterns in
194
the health care setting indicate that providers may spend less time listening and making fewer
195
supportive statements when working with families with LEP, even when trained interpreters are
196
used.48 There is some evidence that LEP in asthma patients is related to less effective patient
197
care. Data from a four-state survey indicated that Spanish speaking Latino parents of children
198
with asthma, but not African American and Latino children with English speaking parents, had
199
poorer experiences with care (i.e. less communication about specific asthma management
200
practices) than white children.49 In another study with a sample of elderly Latino patients with
201
asthma, LEP was associated with lower self-reported medication adherence and worse health
202
outcomes.50 There are some data to indicate that, in general, underuse of professional interpreter
203
services and reliance on untrained ad hoc interpreters may compromise patient care.51
204
There is mounting evidence that health care providers’ unintentional or implicit biases may
205
play a role in disparities in health care,52,53 affecting communication patterns with patients,52,54 or
206
even management recommendations.54 Research regarding implicit bias among providers and
207
subsequent asthma management patterns is limited; in one study utilizing case vignettes,54
208
pediatricians’ biases (as measured by the Implicit Association Test55) were associated with
209
clinical decision making for pain medication, but not for asthma management. Given
210
associations found between implicit bias and provider behavior found in other studies,52,54,56 this
211
area of investigation merits further study.
212
Systems Factors
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Insurance Coverage. Some research has evaluated whether public insurance coverage,
214
commonly associated with minority status, is associated with lower rates of controller
215
medication prescription and use than private insurance coverage. In two studies that assessed
216
prescription patterns, one through chart review of Emergency Department records adults with
217
asthma,57 and the other by evaluation of electronic medical record among children with asthma,58
218
there were no differences in prescription rates of controller medication by insurance status
219
(public vs. private). In contrast, there are data to suggest differential patterns of controller
220
medication prescription upon hospital discharge by insurance status. In a four-state study,
221
Merrick and colleagues59 found that publicly insured children with asthma in each state were
222
more likely to be discharged on suboptimal medication regimens than those with private
223
insurance. Similarly, a study of pediatric and adult inpatients with asthma discharged from
224
hospitals in the Chicago area found that publicly insured patients were less likely to be
225
discharged on controller medications than privately insured patients.60
226
Other Economic and Social Barriers. There are other broader systems factors that may
227
affect medication adherence. Some have noted that limited coverage for medications and
228
additional out-of-pocket costs may affect prescription initiation and consistent medication use.61
229
This “cost-related non-adherence” is an additional variable that may impact some patients from
230
minority populations with limited incomes.62 There is also some evidence that for families who
231
live in disadvantaged areas, exposure to violence and crime affects consistent medication use,
232
even after adjusting for socioeconomic factors,63 suggesting that features of the social
233
environment have links to asthma management behaviors such as medication adherence. Based
234
on the limited data in this area, further investigation is warranted.
235
Conclusions and Potential Intervention Strategies
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There is clear evidence of underuse of controller medications for asthma among racial
237
and ethnic minorities. This occurs at many levels, including 1) the initial prescription of
238
medications in some contexts, such as at hospitalization discharge for publicly insured
239
patients,59,60 2) filling the prescription once initiated,19-21 and 3) taking medication once
240
obtained.15,25
241
There are numerous challenges to consistent adherence to controller medication for racial
242
and ethnic minority patients with asthma. At the individual level, cultural differences in beliefs
243
about traditional medications and mental health concerns such as depressive symptoms are
244
associated with lower levels of controller medication use.27,32 Health care provider biases and
245
communication patterns with culturally diverse patients, particularly those with LEP, likely
246
affect providers’ skill in communicating about controller medication use in a culturally sensitive
247
manner.49,50 Systems factors, such as health care coverage,57,58 cost,61 and features of the
248
community environment such as exposure to violence,59 also present challenges to effective
249
disease management and consistent medication use. What then, can be done to address these
250
disparities in medication use and subsequent outcomes? We provide an overview of potential
251
interventions in Figure 2, focusing on approaches with potential to improve medication
252
prescription, initiation, and use among racial and ethnic minorities with asthma.
253
Individual interventions to increase medication adherence such as education, electronic
254
tracking, and simplifying regimens have demonstrated some modest effects in increasing
255
controller medication adherence for general samples of children and adults with asthma.64
256
Employing a culturally tailored approach also appears to improve outcomes for asthma
257
management interventions for diverse samples.65 Given the generally modest results found across
258
interventions, an individualized approach that first addresses concerns about medications,
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carefully considering cultural beliefs and preferences, is the most likely to effect change. Family
260
resources and routines have been found to support consistent medication use in diverse samples
261
(e.g.,25), and represent an important resource among diverse families.
262
There is increasing evidence that training in both patient-centered communication and
263
cultural competence can yield important effects on patient adherence. A review of the effects of
264
communication training for physicians66 revealed positive effects on patient adherence across
265
many medical conditions. Consistent with these findings, there is some evidence that
266
interventions that emphasize shared-decision making between physicians and patients may
267
improve medication adherence.67 Cultural competence training is provides health services with
268
awareness of and respect for the differing health beliefs, practices, and needs of diverse patient
269
groups.68 There have been fewer studies of the effects of physician cultural competence training
270
on asthma medication adherence. In one early study of pediatric asthma practices in Medicaid
271
health maintenance organizations, Lieu and colleagues found that practice sites with policies to
272
promote cultural competence in staff were less likely to have patients underusing controller
273
medications for asthma.69 Taken together, these findings suggest that providing training to
274
promote effective communication with culturally diverse patient populations has the potential to
275
improve patient adherence to provider recommendations.
276
Increasing health care provider awareness of their patients’ use of CAM, beliefs about
277
controller medications, and general health concerns may also promote more effective
278
communication about asthma medications in the context of the clinical encounter, which
279
arguably is the most effective channel through which to increase adherence to controller
280
medications. CAM use is not regularly disclosed in medical encounters, and patients from
281
minority groups are less likely to discuss self-initiated CAM approaches.70 Interestingly, in one
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recent study,71 physicians who were aware of patients’ concerns about asthma medications and
283
use of CAM for asthma were more likely to initiate conversations about these issues in the
284
context of a clinical encounter. Given recent data linking perceived discrimination with poor
285
asthma control among African American youth with asthma,72 the area of physician-patient
286
interaction, asthma management, and disparities in medication use for asthma merits further
287
study. Development of interventions to increase physician awareness of cultural stereotypes and
288
implicit biases that may impact communication in the patient-provider relationship is necessary.
289
Systems factors such as cost and coverage are challenging to change without substantial
290
advocacy. At a minimum, providers can and should monitor what is covered by patients’
291
insurance to evaluate potential barriers to prescription initiation and continued medication use.
292
Similarly, provider awareness of the sociocultural context in which patients reside can help
293
identify pertinent stressors and challenges to effective disease management.
294
Conclusion
295
The sociodemographic diversity of the US is likely to continue to increase over the next
296
several decades. Our research and clinical approaches must evolve to identify the most effective
297
ways to support patients with asthma from diverse backgrounds to manage their disease
298
effectively, including consistent medication use when indicated. It will also be increasingly
299
important to promote strategies to enhance communication regarding disease management
300
between providers and patients from a range of cultures. Interventions that consider not only
301
patients’ cultural beliefs, but also providers’ implicit biases and methods of interacting with
302
diverse patients and systems barriers to care among those at risk will be necessary to address
303
disparities in asthma management and subsequent health outcomes.
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Figure 1. Components of Medication Adherence
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Figure 2.
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Intervention Approaches to Address Disparities in Medication Use
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