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Factors Affecting Adherence to Antiretroviral Therapy

Margaret A. Chesney From the School of Medicine,University of California San Francisco

In both clinical trials and clinical practice, nonadherence to medications is widespreadamong patients with chronic diseases. The shift to combination therapies for treating humanimmunodeficiency virus (HIV)–infected individuals has increased adherence challenges forboth patients and health-care providers. Estimates of average rates of nonadherence to an-tiretroviral therapy range from 50% to 70%. Adherence rates of !80% are associated withdetectable viremia in a majority of patients. The principal factors associated with nonadher-ence appear to be patient-related, including substance and alcohol abuse. However, otherfactors may also contribute, such as inconvenient dosing frequency, dietary restrictions, pillburden, 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 med-ications. Improving adherence probably requires clarifying the treatment regimen and tailoringit to patient lifestyles.

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. Thesepresent significant challenges to both patients and health-careproviders with respect to adherence. Without adequate adher-ence, antiretroviral agents are not maintained at sufficient con-centrations to suppress HIV replication in infected cells and tolower the plasma viral load. In addition to being associatedwith poor short-term virological response, poor adherence toantiviral medication accelerates development of drug-resistantHIV. Therefore, identifying and overcoming the factors thatreduce adherence to combination antiretroviral agents is of ut-most importance for prolonged viral load suppression.

There are a number of key issues in the study of adherenceto antiretroviral therapy, including accurate measurement ofadherence, assessment of the impact of adherence on viral loadand clinical outcome, determination of the factors that affectadherence, and the development of interventions. Addressingthese issues may provide valuable information about whichpatients are most at risk for nonadherence and about howadherence might be improved. The critical factors that influenceadherence fall into 4 main groups: (1) patient factors, such asdrug use, alcohol use, age, sex, or ethnicity; (2) medicationregimen, such as dosing complexity, number of pills, or food

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

Reprints or correspondence: Dr. Margaret A. Chesney, University of Cal-ifornia San Francisco, Center for AIDS Prevention Studies, 74 New Mont-gomery St., Suite 600, San Francisco, CA 94105 (mchesney@psg.ucsf.edu).

Clinical Infectious Diseases 2000;30(Suppl 2):S171–6q 2000 by the Infectious Diseases Society of America. All rights reserved.1058-4838/2000/3006S2-0010$03.00

requirements; (3) the patient–health-care provider relationship;and (4) the system of care.

Adherence to therapy is difficult to measure accurately. Fourbasic techniques have been developed for quantifying adher-ence, all of which have limitations. First and most commonare patient self-reports. These have the advantages of low costand flexibility of design (questionnaires suit individual languageabilities). The data are easily collected and can help to deter-mine the reasons why patients are nonadherent. They assume,however, that patients can accurately recall their behavior andare providing honest answers. A major limitation of self-reportsis that they reflect only short-term or average adherence andmay often overestimate it. Nevertheless, some studies show sig-nificant relationships between data from self-reports and viralload [1, 2]. Other studies that compare data from self-reportsto pill counts or electronic measurements found differences,suggesting that self-reports provide inflated estimates of ad-herence behavior [3, 4].

Second are patients’ reports of missing pills, which are almostalways reliable [5], so self-reports can be helpful for under-standing the dynamics surrounding missed medication. Pillcounts have been widely used. The return of excess pills pro-vides tangible evidence of nonadherence. However, pill countsrequire patients to return the medication packaging to the cli-nician. Even in clinical trial situations, patients tend to forgetthe packages or inadvertently discard them. There have alsobeen reports that patients other than those with HIV, awarethat pill counts are being conducted, engage in “pill dumping”to appear adherent. As a result, pill counts typically overesti-mate adherence.

Third, assays of drug levels have been used in clinical trialsto measure the last dose taken; however, these assays are oftenimpractical because of their expense and lack of general avail-ability. In addition, serum concentrations of nucleoside ana-logues may not reflect intracellular concentration of the active

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Table 1. Poor medication adherence correlates with virologic failure:a study of 45 HIV-infected patients.

Medication adherence, % of patients Virologic failure, % of patients

!80 8780–90 47195 10

NOTE. Seventy-two percent of patients were treated with a single proteaseinhibitor (nelfinavir, 65%; indinavir, 26%; other inhibitors, 9%); 28% received acombination of saquinavir and ritonavir. Adapted from [6].

Table 2. Factors reported to negatively affect adherence in HIV-infected patients.

Patient factorsActive substance abuse (drugs and/or alcohol)Male sexYouthActive depressionLower level of educationLack of self-efficacya

Extreme anxietyExtreme painNo change in health statusNon-white

Medication factorsDose frequency of more than twice a dayPill burdenType of drugInability to take medication when away from homeFood requirementSide effectsPoor doctor–health-care provider relationship

System of careDissatisfaction with past experience of health-care system, leading

to avoidance

NOTE. Based on data from [2, 6–8, 12, 13, 15–19].a “Self-efficacy” refers to patients’ belief in their ability to take medication

as prescribed.

triphosphates. Furthermore, these assays typically measureonly recent doses and thus provide limited data. Adherencemay be overestimated if patients are more conscientious abouttaking their medication before a clinic visit.

Fourth, electronic monitoring systems, such as the Medi-cation Event Monitoring System (MEMS), are inserted intomedication bottle caps; they contain a computer chip that re-cords the date and time of opening and closing of the bottle.Interpretation of these data assumes that a single dose is takeneach time the bottle is opened, and may lead to inaccuracies ifmultiple doses are removed at once. Despite the limitations ofthese measurement techniques, adherence data are providingvaluable insight into the association between drug taking andviral load, as well as approaches that may be useful for im-proving adherence.

Adherence to HIV Therapy

Large-scale studies of the impact of adherence on viral loadand clinical outcome in HIV therapy are underway within theAIDS Clinical Trials Group (ACTG) and at clinical sites in theUnited States and abroad. However, findings have not yet beenreported. A small study by Paterson et al. [6] examined patientadherence to protease inhibitor therapy by use of MEMS. Theinvestigators found that poor adherence correlated with clinicaland virological failure at 3 months of follow-up (table 1). Theseresults suggest that a high degree of adherence is necessary formaintenance of drug efficacy. Further similar studies are neededto corroborate these data and to establish whether adherencerequirements vary for different drugs.

Although very little published information is available onmedication adherence of HIV-infected patients, new data froma number of studies were presented at numerous conferences,including the 12th World AIDS Conference in Geneva and the38th Annual Interscience Conference on Antimicrobial Agentsand Chemotherapy (ICAAC) in San Diego. Because the studyof adherence is in its infancy, study designs and end points varywidely, making study comparisons difficult. Self-reported ad-herence, as defined in research studies, has been reported torange from 0% to 100% [6–13]. Although the results of someof these studies appear to conflict, important information isemerging about the extent of and factors associated with ad-herence. The earliest reports of nonadherence suggested thatslightly 110% of patients missed >1 dose of medication each

day [1, 14]. Rates of nonadherence may be as high as 50% whenaveraged over time and with an arbitrary cutoff point of !80%of medication taken [8]. This figure is supported by observationsfrom 2 larger studies: an international multicenter study of 235HIV-infected patients and a United States study of 244 HIV-infected Medicaid-insured patients. The reported rates of pa-tients who take !80% of doses in these studies were 46% and40%, respectively [9, 10]. It is interesting to note that theseresults are consistent with estimates of adherence in otherchronic diseases and support the view that nonadherence is acommon behavior that should be expected, even with a seriousdisease such as HIV infection.

In order to implement measures to improve adherence, it isfirst essential to identify the principal factors that contributeto the inability of patients to take their medication. Those fac-tors identified to date are summarized in table 2.

A published study of adherence by Eldred et al. [10] required244 patients who were receiving antiretroviral therapy andPneumocystis carinii pneumonia (PCP) prophylaxis to reportthe medications they were taking, their pattern of use, and theirknowledge and attitudes about HIV therapies [10]. Most of thepatients in the study were receiving monotherapy. Eldred et al.found that 60% of patients reported 180% adherence to treat-ment regimens in the previous 7 days. When PCP prophylaxiswas analyzed by assaying urinary sulfamethoxazole levels, acorrelation of ∼80% was found between self-report and levelsof sulfamethoxazole in the urine. This leads to the conclusionthat at least 40% of patients were getting !80% of their antiviralmedication. Good adherence was associated with dosing twicea day or less, the likelihood that patients take medication whenaway from home, and self-efficacy (i.e., patients’ belief in their

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Table 3. Frequent causes for medication nonadherence by HIV-infected patients who are receiving highly active antiretroviral therapy.

Reason for nonadherence Prevalence, % of patients

Forgot or busy 34–52Away from home 27–42Change in daily routine 40Side effects 19–25Depression or illness 9–23Lack of interest or drug “holidays” 4–19

NOTE. Based on data from [4, 11, 19].

ability to take their medication). The major factor associatedwith nonadherence was active illicit drug use. In particular,patients who had used crack cocaine were significantly less ad-herent. These findings, although not directly applicable to com-bination therapy, may shed light on adherence issues for pa-tients who are receiving HAART.

Preliminary data from a number of studies of adherence toantiretroviral 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 affectadherence are patient-related. The most common reasons givenby patients for nonadherence are summarized in table 3; theprincipal reasons are that they forgot or were busy. Data froma large cohort of HIV-infected patients (1322 persons livingwith HIV/AIDS) who were receiving antiviral combinationtherapies demonstrated that characteristics that predict non-adherence included youth, government-subsidized health in-surance, extreme anxiety or pain, and no perceived change inhealth status as a result of drug therapy [15]. These data suggestthat vulnerable subgroups of HIV-infected patients need to beidentified and targeted [15].

Reduction of the administration frequency of current drugregimens may be limited by the relatively short half-lives of thenonnucleoside reverse transcriptase inhibitors (NNRTIs) andprotease inhibitors. Although it has been assumed that reducingdosing frequency or pill burden will increase adherence, it isimportant to note that this may not be the case. In the above-mentioned trial of 179 patients and in another smaller trial of45 patients, there was no association between dose frequencyor pill burden and nonadherence [6, 10]. There are indicationsfrom a number of other studies that meal restrictions and otherfactors, and not simply pill burden, are predictors of nonad-herence [2, 4, 10, 13, 19]. It is worth noting that the pharma-ceutical industry is investing considerable effort to develop newcompounds or regimens with longer half-lives in order to reducepill count and dosing frequency and is also trying to find otherways to simplify drug regimens. The simplification of existingregimens may prove worthwhile as therapies continue to failin nonadherent patients and even more medications are addedto regimens.

A good patient–health-care provider relationship may be animportant motivating factor for taking and adhering to com-plex combination drug therapies [20]. A qualitative study ofhomosexual youths showed that primary-care providers exhib-ited judgmental behavior, stereotyping, homophobia, and fail-ure to address cultural issues when administering care [17]. Suchexperiences are likely to lead some people with HIV infectionto avoid the health care system. On the other hand, factorsthat have been identified as strengthening patient–health-careprovider relationships include perceptions of health-care pro-vider competence, communication quality and clarity, com-passion, willingness to include patients in treatment decisions,

adequacy of referrals, and convenience of visiting the doctor[21]. Conversely, frustration for health-care providers is asso-ciated with lack of patient adherence to treatment, miscom-munication, missed appointments, complexity of treatment reg-imens, and medication side effects [21, 23]. In light of theseproblems, it is heartening to find that initiatives are underwayto encourage health-care providers to work with patients as“partners” in care and to involve representatives from the entireHIV community [24].

Other important adherence issues have arisen, particularlywith regard to economically disadvantaged patients with mul-tiple social problems. Many clinicians feel that lifestyle factors,such as homelessness, substance abuse, lack of education, andmental illness, are predictors of nonadherence and therefore arewithholding HAART from these patients. A review of thesestudies indicates that some, but not all, have found an asso-ciation 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 makingassumptions about patients’ likelihood to encounter problems.It is of interest that results of trials show that health-care pro-viders are not very good at predicting which patients will beadherent to medication [6, 22, 26]. For example, a comparisonof health-care providers’ opinions and self-reports from 193HIV-infectedpatients revealed that the health-care providers overestimatedthe influence of social factors on adherence [22]. In this study,social factors made no significant difference. Results of anotherstudy of 45 patients indicated that health-care providers pre-dicted adherence of patients poorly: 33% of nonadherent pa-tients were identified by health-care providers as adherent, and36% of patients with better than 95% adherence (measured byMEMS Caps) were identified as being poorly adherent [3]. Inaddition, the results of a recent study of 31 HIV-infected youthsfound that homelessness, current living situation, years of ed-ucation, clinical depression, and substance abuse did not predictadherence to combination therapy [26]. These data do not sup-port the routine withholding of HAART from specific socialgroups, since adherence cannot reliably be predicted on thebasis of patient characteristics [27].

Special issues with adherence exist for HIV-infected childrenand adolescents. Infants and young children are dependent onadults for administration of their medications, which means

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Table 4. Strategies for enhancing adherence to antiretroviral therapy.

Strategy Remarks

Directly observe therapy Ensures adherenceLabor intensiveExpensiveEncourage family member to observe

Clarify instructions using personal treatment plan Helps patients to be better organizedHelps patients understand dosing schedules

Tailor drug regimen to suit patients’ lifestyles Identify daily activities that patients can link with takingmedication

Show patients how to keep medication diary Helps establish a routineEncourage pill sorting and convenient placement

of pillsHelps establish a routine of thinking about the practicalities

of taking medicationEncourage planning ahead for changes in daily

routine (weekends and holidays)Helps patients to avoid missing doses

Make clinic appointments convenient and pleas-ant, provide educational materials, etc.

Encourages patients to keep appointmentsPromotes self-efficacya

Encourages patients to learn about medicationsRefer patients for social support, treatment of

substance abuse, and for stressCounseling may help patients cope with drug and/or alcohol

abuse or with medication-related food requirementsSocial support promotes self-efficacya

a “Self-efficacy” refers to patients’ beliefs in their ability to take medication as prescribed.

that their adherence is only as good as that which their care-givers are able to achieve. Unfortunately, liquid formulationsare often not particularly palatable, and food requirements forsome antiretroviral agents make therapies difficult to administerto infants who require frequent formula feeding. These factorscan affect the willingness of the caregiver to administer themedication and the willingness of the child to take it. Anotherbarrier to adherence for children and adolescents with HIVmay be their families’ desire for secrecy about the condition.For example, parents may be unwilling to fill prescriptions atlocal pharmacies and/or may send their child to school withouttheir medication to hide the fact that the child is HIV-infected.Adolescents find adherence particularly challenging as they en-ter a stage of life when they are particularly self-conscious anddo not want to be different from their peers. A detailed as-sessment of the barriers to adherence should be implementedfor all minors who require antiretroviral therapy. Case man-agers and counselors may often be able to work with familiesto resolve specific issues.

The Way Ahead

A variety of methods for improving adherence have beensuggested, and descriptions from clinicians, pilot studies, and1 trial [28] provide encouraging positive results. A study byWorkman et al. [18] describes a practice that implemented anumber of patient management interventions aimed at im-proving adherence. These included extended consultation timeto explain and to reinforce medication instructions, tailoringthe choice of drug regimen to patient lifestyle, frequent follow-up when initiating or changing drug regimens, rapid viral loadfeedback, and the use of reminder calls and alarms [18]. Ad-herence rates of 80%–100% (with 73% reporting 100% adher-ence) were reported by 99% of 77 HIV-infected patients [18].

The authors concluded that the interventions significantly en-hanced adherence, compared with mean adherence rates re-ported in the literature [6, 8–10]. The effectiveness of an alarmset to alert patients when their drugs should be taken was testedin another study of 49 HIV-infected patients [29]. After 3months, the frequency of 100% pill adherence was 89%; 80%adherence was observed in 99% of patients. The patients alsoexhibited good adherence to timing and diet requirements. Allthe patients were enthusiastic about the alarm device; however,concerns were raised as to its durability, since malfunctionsoccurred in the devices issued to half of the patients. Managedsocial support and perceived health-care provider support forpromoting adherence have also been investigated. In 2 separatestudies, patient support systems were found to enhance adher-ence and were particularly helpful with regard to enabling pa-tients to better follow advice and instructions [30, 31].

As the previous review demonstrates, the major factors as-sociated with nonadherence are related to patient behavior, anda variety of strategies by health care professionals are beginningto yield improved adherence. Some of the interventions thathave been studied are listed in table 4. Of particular importanceis the tailoring of medication to the patient’s lifestyle [18, 25,28]. This can be illustrated by consideration of dosing require-ments and the need for special instructions that take into ac-count the life patterns of patients. For some patients, certaindosing intervals might be easier to adhere to; for others, lackof ready access to refrigeration or water may prove problematic.Moreover, if a patient’s treatment fails, the patient should beapproached to review adherence before the regimen is changed.This should help ensure that patients begin a new regimen withoptimal adherence.

Future clinical trials that study safety and efficacy of anti-retroviral agents with respect to virologic and immunologicendpoints may be considered deficient if they do not include

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at least 1 acceptable measure of adherence to therapy. Indeed,simultaneous measurement of adherence by 2 different methodsmay be the best approach. In addition, there is a need for studiesthat directly assess strategies that are designed to increaseadherence.

Finally, important lessons can be drawn from studies of ad-herence among patients with other chronic diseases, where thereis a larger body of published literature. Both the factors relatedto adherence and many of the interventions to improve ad-herence to other medications may largely overlap with thoseimportant to antiretrovirals [27]. For example, a recent reviewof hypertension stated the following: “Once-daily dosing shouldbe coupled with selection of a drug with long duration of actionto overcome problems of missed doses. Widespread adoptionof simple compliance enhancement methods could lead to de-creased morbidity and mortality” [32]. Incomplete compliancewith any long-term medication is a multifactorial problem, butit is a problem that can and must be addressed.

Summary

It is important to recognize that some degree of nonadher-ence is common and should be expected in all patients who arereceiving antiretroviral therapy. The first step toward addressingthe problem of medication nonadherence is to accurately iden-tify patients whose risk of nonadherence is sufficient to un-dermine clinical outcomes. However, a number of studies havedemonstrated that health-care providers cannot accuratelyidentify those patients likely to be nonadherent. Studies of largesamples suggest that substance abuse is associated with non-adherence. Therefore, health-care providers may want to becareful to ask patients with histories of substance abuse aboutadherence. It does not follow, however, that all patients whoabuse substances will be nonadherent. Similarly, homelessness,lack of education, and mental illness are not necessarily pre-dictors of nonadherence, but might warrant extra attention andsupport. Furthermore, the absence of alcohol and drug abusedoes not predict good adherence. Steps to maximize adherence,therefore, should be reviewed with all patients. Although self-reports tend to overestimate adherence, they are inexpensiveand fairly accurate for providing an indication of problems. Inparticular, reports of nonadherence are reliable and call foraction. Such reports also help to determine why HIV-infectedpatients are nonadherent. Of the available methods, self-reportsare the most practical for routine use in the clinic. Once non-adherent patients are identified, health-care providers may wantto implement a variety of interventions to enhance adherence.Strategies for intervention are likely to be based on tailoringthe drug regimen to the lifestyle of the patient and assessingadherence as part of a follow-up program.

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