Factors Affecting Adherence to Antiretroviral Therapy

1.

Margaret A. Chesney
+Author Affiliations

1.

1.

School of Medicine, University of California San Francisco

Reprints or correspondence: Dr. Margaret A. Chesney, University of California San Francisco, Center for AIDS
Prevention Studies, 74 New Montgomery St., Suite 600, San Francisco, CA 94105 (mchesney@psg.ucsf.edu).
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Abstract
In both clinical trials and clinical practice, nonadherence to medications is widespread among patients
with chronic diseases. The shift to combination therapies for treating human immunodeficiency virus
(HIV)-infected individuals has increased adherence challenges for both patients and health-care
providers. Estimates of average rates of nonadherence to antiretroviral therapy range from 50% to
70%. Adherence rates of <80% are associated with detectable viremia in a majority of patients. The
principal factors associated with nonadherence appear to be patient-related, including substance and
alcohol abuse. However, other factors may also contribute, such as inconvenient dosing frequency,
dietary restrictions, pill burden, and side effects; patient-health-care provider relationships; and the
system of care. We discuss the major reasons reported by HIV-infected individuals for not taking their
medications. Improving adherence probably requires clarifying the treatment regimen and tailoring it
to patient lifestyles.
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Measurement of Adherence
The shift to the use of highly active antiretroviral therapy (HAART) for treating human
immunodeficiency virus (HIV) disease has led to increasingly complex drug regimens. These present
significant challenges to both patients and health-care providers with respect to adherence. Without
adequate adherence, antiretroviral agents are not maintained at sufficient concentrations to suppress
HIV replication in infected cells and to lower the plasma viral load. In addition to being associated
with poor short-term virological response, poor adherence to antiviral medication accelerates
development of drug-resistant HIV. Therefore, identifying and overcoming the factors that reduce
adherence to combination antiretroviral agents is of utmost importance for prolonged viral load
suppression.
There are a number of key issues in the study of adherence to antiretroviral therapy, including
accurate measurement of adherence, assessment of the impact of adherence on viral load and
clinical outcome, determination of the factors that affect adherence, and the development of
interventions. Addressing these issues may provide valuable information about which patients are
most at risk for nonadherence and about how adherence might be improved. The critical factors that
influence adherence fall into 4 main groups: (1) patient factors, such as drug use, alcohol use, age,
sex, or ethnicity; (2) medication regimen, such as dosing complexity, number of pills, or food
requirements; (3) the patient-health-care provider relationship; and (4) the system of care.
Adherence to therapy is difficult to measure accurately. Four basic techniques have been developed
for quantifying adherence, all of which have limitations. First and most common are patient selfreports. These have the advantages of low cost and flexibility of design (questionnaires suit individual
language abilities). The data are easily collected and can help to determine the reasons why patients
are nonadherent. They assume, however, that patients can accurately recall their behavior and are
providing honest answers. A major limitation of self-reports is that they reflect only short-term or
average adherence and may often overestimate it. Nevertheless, some studies show significant
relationships between data from self-reports and viral load [1, 2]. Other studies that compare data
from self-reports to pill counts or electronic measurements found differences, suggesting that selfreports provide inflated estimates of adherence behavior [3, 4].
Second are patients' reports of missing pills, which are almost always reliable [5], so self-reports can
be helpful for understanding the dynamics surrounding missed medication. Pill counts have been
widely used. The return of excess pills provides tangible evidence of nonadherence. However, pill

counts require patients to return the medication packaging to the clinician. Even in clinical trial
situations, patients tend to forget the packages or inadvertently discard them. There have also been
reports that patients other than those with HIV, aware that pill counts are being conducted, engage in
pill dumping to appear adherent. As a result, pill counts typically overestimate adherence.
Third, assays of drug levels have been used in clinical trials to measure the last dose taken; however,
these assays are often impractical because of their expense and lack of general availability. In
addition, serum concentrations of nucleoside analogues may not reflect intracellular concentration of
the active triphosphates. Furthermore, these assays typically measure only recent doses and thus
provide limited data. Adherence may be overestimated if patients are more conscientious about
taking their medication before a clinic visit.
Fourth, electronic monitoring systems, such as the Medication Event Monitoring System (MEMS), are
inserted into medication bottle caps; they contain a computer chip that records the date and time of
opening and closing of the bottle. Interpretation of these data assumes that a single dose is taken
each time the bottle is opened, and may lead to inaccuracies if multiple doses are removed at once.
Despite the limitations of these measurement techniques, adherence data are providing valuable
insight into the association between drug taking and viral load, as well as approaches that may be
useful for improving adherence.
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Adherence to HIV Therapy

Large-scale studies of the impact of adherence on viral load and clinical outcome in HIV therapy are
underway within the AIDS Clinical Trials Group (ACTG) and at clinical sites in the United States and
abroad. However, findings have not yet been reported. A small study by Paterson et al. [6] examined
patient adherence to protease inhibitor therapy by use of MEMS. The investigators found that poor
adherence correlated with clinical and virological failure at 3 months of follow-up (table 1). These
results suggest that a high degree of adherence is necessary for maintenance of drug efficacy. Further
similar studies are needed to corroborate these data and to establish whether adherence
requirements vary for different drugs.

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Table 1

Poor medication adherence correlates with virologic failure: a study of 45 HIV-infected patients.
Although very little published information is available on medication adherence of HIV-infected
patients, new data from a number of studies were presented at numerous conferences, including the
12th World AIDS Conference in Geneva and the 38th Annual Interscience Conference on Antimicrobial
Agents and Chemotherapy (ICAAC) in San Diego. Because the study of adherence is in its infancy,
study designs and end points vary widely, making study comparisons difficult. Self-reported
adherence, as defined in research studies, has been reported to range from 0% to 100% [6-13].
Although the results of some of these studies appear to conflict, important information is emerging
about the extent of and factors associated with adherence. The earliest reports of nonadherence
suggested that slightly >10% of patients missed 1 dose of medication each day [1, 14]. Rates of
nonadherence may be as high as 50% when averaged over time and with an arbitrary cutoff point of
<80% of medication taken [8]. This figure is supported by observations from 2 larger studies: an
international multicenter study of 235 HIV-infected patients and a United States study of 244 HIVinfected Medicaid-insured patients. The reported rates of patients who take <80% of doses in these
studies were 46% and 40%, respectively [9, 10]. It is interesting to note that these results are
consistent with estimates of adherence in other chronic diseases and support the view that
nonadherence is a common behavior that should be expected, even with a serious disease such as
HIV infection.

In order to implement measures to improve adherence, it is first essential to identify the principal
factors that contribute to the inability of patients to take their medication. Those factors identified to
date are summarized in table 2.

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Table 2

Factors reported to negatively affect adherence in HIV-infected patients.

A published study of adherence by Eldred et al. [10] required 244 patients who were receiving
antiretroviral therapy and Pneumocystis cariniipneumonia (PCP) prophylaxis to report the medications
they were taking, their pattern of use, and their knowledge and attitudes about HIV therapies [10].
Most of the patients in the study were receiving monotherapy. Eldred et al. found that 60% of patients
reported >80% adherence to treatment regimens in the previous 7 days. When PCP prophylaxis was
analyzed by assaying urinary sulfamethoxazole levels, a correlation of 80% was found between self-report
and levels of sulfamethoxazole in the urine. This leads to the conclusion that at least 40% of patients were getting <80% of
their antiviral medication. Good adherence was associated with dosing twice a day or less, the
likelihood that patients take medication when away from home, and self-efficacy (i.e., patients' belief
in their ability to take their medication). The major factor associated with nonadherence was active
illicit drug use. In particular, patients who had used crack cocaine were significantly less adherent.
These findings, although not directly applicable to combination therapy, may shed light on adherence
issues for patients who are receiving HAART.
Preliminary data from a number of studies of adherence to antiretroviral agents have been presented
in abstract form [4, 6, 12, 15, 19-22]. Specific findings vary from study to study, due at least in part to
the different samples and measures used. In general, it appears that the most important factors that
affect adherence are patient-related. The most common reasons given by patients for nonadherence
are summarized intable 3; the principal reasons are that they forgot or were busy. Data from a large
cohort of HIV-infected patients (1322 persons living with HIV/AIDS) who were receiving antiviral
combination therapies demonstrated that characteristics that predict non-adherence included youth,
government-subsidized health insurance, extreme anxiety or pain, and no perceived change in health
status as a result of drug therapy [15]. These data suggest that vulnerable subgroups of HIV-infected
patients need to be identified and targeted [15].

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Table 3

Frequent causes for medication nonadherence by HIV- infected patients who are receiving highly
active antiretroviral therapy.

Reduction of the administration frequency of current drug regimens may be limited by the relatively
short half-lives of the nonnucleoside reverse transcriptase inhibitors (NNRTIs) and protease inhibitors.
Although it has been assumed that reducing dosing frequency or pill burden will increase adherence,
it is important to note that this may not be the case. In the above-mentioned trial of 179 patients and
in another smaller trial of 45 patients, there was no association between dose frequency or pill
burden and nonadherence [6, 10]. There are indications from a number of other studies that meal
restrictions and other factors, and not simply pill burden, are predictors of nonad-herence
[2, 4, 10, 13, 19]. It is worth noting that the pharmaceutical industry is investing considerable effort
to develop new compounds or regimens with longer half-lives in order to reduce pill count and dosing
frequency and is also trying to find other ways to simplify drug regimens. The simplification of
existing regimens may prove worthwhile as therapies continue to fail in nonadherent patients and
even more medications are added to regimens.
A good patient-health-care provider relationship may be an important motivating factor for taking and
adhering to complex combination drug therapies [20]. A qualitative study of homosexual youths
showed that primary-care providers exhibited judgmental behavior, stereotyping, homophobia, and
failure to address cultural issues when administering care [17]. Such experiences are likely to lead
some people with HIV infection to avoid the health care system. On the other hand, factors that have
been identified as strengthening patient-health-care provider relationships include perceptions of
health-care provider competence, communication quality and clarity, compassion, willingness to
include patients in treatment decisions, adequacy of referrals, and convenience of visiting the doctor
[21]. Conversely, frustration for health-care providers is associated with lack of patient adherence to
treatment, miscommunication, missed appointments, complexity of treatment regimens, and
medication side effects [21, 23]. In light of these problems, it is heartening to find that initiatives are
underway to encourage health-care providers to work with patients as partners in care and to
involve representatives from the entire HIV community [24].
Other important adherence issues have arisen, particularly with regard to economically
disadvantaged patients with multiple social problems. Many clinicians feel that lifestyle factors, such
as homelessness, substance abuse, lack of education, and mental illness, are predictors of
nonadherence and therefore are withholding HAART from these patients. A review of these studies
indicates that some, but not all, have found an association between nonadherence and youth, female
sex, less edu-cation, or a current or past history of substance abuse [25]. Therefore, health-care
providers should be cautious in making assumptions about patients' likelihood to encounter problems.
It is of interest that results of trials show that health-care providers are not very good at predicting
which patients will be adherent to medication [6, 22, 26]. For example, a comparison of health-care
providers' opinions and self-reports from 193 HIV-infected patients revealed that the health-care
providers overestimated the influence of social factors on adherence [22]. In this study, social factors
made no significant difference. Results of another study of 45 patients indicated that health-care
providers predicted adherence of patients poorly: 33% of nonadherent patients were identified by
health-care providers as adherent, and 36% of patients with better than 95% adherence (measured
by MEMS Caps) were identified as being poorly adherent [3]. In addition, the results of a recent study
of 31 HIV-infected youths found that homelessness, current living situation, years of education,
clinical depression, and substance abuse did not predict adherence to combination therapy [26].
These data do not support the routine withholding of HAART from specific social groups, since
adherence cannot reliably be predicted on the basis of patient characteristics [27].
Special issues with adherence exist for HIV-infected children and adolescents. Infants and young
children are dependent on adults for administration of their medications, which means that their
adherence is only as good as that which their caregivers are able to achieve. Unfortunately, liquid
formulations are often not particularly palatable, and food requirements for some anti-retroviral
agents make therapies difficult to administer to infants who require frequent formula feeding. These
factors can affect the willingness of the caregiver to administer the medication and the willingness of
the child to take it. Another barrier to adherence for children and adolescents with HIV may be their
families' desire for secrecy about the condition. For example, parents may be unwilling to fill
prescriptions at local pharmacies and/or may send their child to school without their medication to
hide the fact that the child is HIV-infected. Adolescents find adherence particularly challenging as
they enter a stage of life when they are particularly self-conscious and do not want to be different
from their peers. A detailed assessment of the barriers to adherence should be implemented for all
minors who require antiretroviral therapy. Case managers and counselors may often be able to work
with families to resolve specific issues.

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The Way Ahead

A variety of methods for improving adherence have been suggested, and descriptions from clinicians,
pilot studies, and 1 trial [28] provide encouraging positive results. A study by Workman et al. [18]
describes a practice that implemented a number of patient management interventions aimed at
improving adherence. These included extended consultation time to explain and to reinforce
medication instructions, tailoring the choice of drug regimen to patient lifestyle, frequent follow-up
when initiating or changing drug regimens, rapid viral load feedback, and the use of reminder calls
and alarms [18]. Adherence rates of 80%-100% (with 73% reporting 100% adherence) were reported
by 99% of 77 HIV-infected patients [18]. The authors concluded that the interventions significantly
enhanced adherence, compared with mean adherence rates reported in the literature [6, 8-10]. The
effectiveness of an alarm set to alert patients when their drugs should be taken was tested in another
study of 49 HIV-infected patients [29]. After 3 months, the frequency of 100% pill adherence was
89%; 80% adherence was observed in 99% of patients. The patients also exhibited good adherence to
timing and diet requirements. All the patients were enthusiastic about the alarm device; however,
concerns were raised as to its durability, since malfunctions occurred in the devices issued to half of
the patients. Managed social support and perceived health-care provider support for promoting
adherence have also been investigated. In 2 separate studies, patient support systems were found to
enhance adherence and were particularly helpful with regard to enabling patients to better follow
advice and instructions [30, 31].
As the previous review demonstrates, the major factors associated with nonadherence are related to
patient behavior, and a variety of strategies by health care professionals are beginning to yield
improved adherence. Some of the interventions that have been studied are listed in table 4. Of
particular importance is the tailoring of medication to the patient's lifestyle [18, 25, 28]. This can be
illustrated by consideration of dosing requirements and the need for special instructions that take into
account the life patterns of patients. For some patients, certain dosing intervals might be easier to
adhere to; for others, lack of ready access to refrigeration or water may prove problematic. Moreover,
if a patient's treatment fails, the patient should be approached to review adherence before the
regimen is changed. This should help ensure that patients begin a new regimen with optimal
adherence.

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Table 4

Strategies for enhancing adherence to antiretroviral therapy.

Future clinical trials that study safety and efficacy of anti-retroviral agents with respect to virologic
and immunologic endpoints may be considered deficient if they do not include at least 1 acceptable
measure of adherence to therapy. Indeed, simultaneous measurement of adherence by 2 different
methods may be the best approach. In addition, there is a need for studies that directly assess
strategies that are designed to increase adherence.
Finally, important lessons can be drawn from studies of adherence among patients with other chronic
diseases, where there is a larger body of published literature. Both the factors related to adherence
and many of the interventions to improve adherence to other medications may largely overlap with
those important to antiretrovirals [27]. For example, a recent review of hypertension stated the
following: Once-daily dosing should be coupled with selection of a drug with long duration of action
to overcome problems of missed doses. Widespread adoption of simple compliance enhancement

methods could lead to decreased morbidity and mortality [32]. Incomplete compliance with any
long-term medication is a multifactorial problem, but it is a problem that can and must be addressed.
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Summary
It is important to recognize that some degree of nonadherence is common and should be expected in
all patients who are receiving antiretroviral therapy. The first step toward addressing the problem of
medication nonadherence is to accurately identify patients whose risk of nonadherence is sufficient to
undermine clinical outcomes. However, a number of studies have demonstrated that health-care
providers cannot accurately identify those patients likely to be nonadherent. Studies of large samples
suggest that substance abuse is associated with nonadherence. Therefore, health-care providers may
want to be careful to ask patients with histories of substance abuse about adherence. It does not
follow, however, that all patients who abuse substances will be nonadherent. Similarly, homelessness,
lack of education, and mental illness are not necessarily predictors of nonadherence, but might
warrant extra attention and support. Furthermore, the absence of alcohol and drug abuse does not
predict good adherence. Steps to maximize adherence, therefore, should be reviewed with all
patients. Although self-reports tend to overestimate adherence, they are inexpensive and fairly
accurate for providing an indication of problems. In particular, reports of nonadherence are reliable
and call for action. Such reports also help to determine why HIV-infected patients are nonadherent. Of
the available methods, self-reports are the most practical for routine use in the clinic. Once
nonadherent patients are identified, health-care providers may want to implement a variety of
interventions to enhance adherence. Strategies for intervention are likely to be based on tailoring the
drug regimen to the lifestyle of the patient and assessing adherence as part of a follow-up program.
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Footnotes

Financial support for this research was provided by National Institutes of Health grants to the
Center for AIDS Prevention Studies (MH42459) and the Center for AIDS Research (MH59037).

2000 by the Infectious Diseases Society of America

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Table 4

Strategies for enhancing adherence to antiretroviral therapy.

Table 1

Poor medication adherence correlates with virologic failure: a study of

45 HIV-infected patients.