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Adherence to Antiretroviral Therapy and Virologic Suppression among HIV-Infected Persons Receiving Care in Private Clinics in Mumbai, India

  1. Bijal Shah1,
  2. Louise Walshe2,
  3. Dattary G. Saple4,
  4. Shruti H. Mehta3,
  5. Jeetender P. Ramnani3,
  6. R. D. Kharkar4,
  7. Robert C. Bollinger2,3, and
  8. Amita Gupta2
  1. 1Department of Emergency Medicine, Carolinas Medical Center, Charlotte, North Carolina
  2. 2School of Medicine, Baltimore, Maryland
  3. 3Bloomberg School of Public Health, Johns Hopkins University, Baltimore, Maryland
  4. 4Human Healthcare and Research Foundation, Mumbai, India
  1. Reprints or correspondence: Dr. Amita Gupta, Div. of Infectious Diseases, Center for Clinical Global Health Education, Johns Hopkins School of Medicine, 600 N. Wolfe St., Phipps 540B, Baltimore, MD 21287 (agupta25{at}jhmi.edu).

  1. Presented in part: 16th International AIDS Conference, Toronto, Canada, August 2006 (abstract THPE0194).

 
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Abstract

Background. Adherence to antiretroviral therapy (ART) and correlates of adherence and virologic suppression among human immunodeficiency virus (HIV)—infected persons receiving ART in private, outpatient clinics in India is unknown.

Methods. Between December 2004 and April 2005, persons receiving ART at 3 private clinics in Mumbai, India, were interviewed regarding HIV care and adherence to ART. Physicians also completed a survey for each participant. Quantitative HIV-1 RNA level was determined for 200 participants.

Results. Of 279 participants, 73% reported ⩾95% adherence to ART. Adherence was positively associated with age ⩾50 years (adjusted odds ratio [aOR], 3.90), presence of comorbid conditions (aOR, 1.92), medication self-efficacy (aOR, 4.01), absence of pain in the past month (aOR, 2.14), and support from family and friends (aOR, 2.57). Lack of reminders from family members to take medication (aOR, 0.27) was negatively associated with adherence. Of 200 participants, 127 (63.5%) had virologic suppression (RNA level, <400 copies/mL). Independent correlates of suppression were a regimen containing ⩾3 ART drugs (aOR, 5.52), first ART regimen (aOR, 3.28), adherence to therapy ⩾95% (aOR, 5.70), female sex (aOR, 3.19), and a physical component score ⩾50 (aOR, 1.07).

Conclusion. Self-reported adherence to ART in a sample of patients attending Mumbai's private clinics was relatively high. However, the fact that a detectable viral level was found in nearly 40% of patients suggests that second-line ART regimens, as well as an emphasis on adherence and appropriate ART regimens in India, is needed.

Antiretroviral therapy (ART) has significantly reduced rates of morbidity and mortality among HIV-infected persons in both resource-rich and resource-limited environments [1–3]. ART treatment success—defined by sustained virologic suppression, immunologic recovery, and clinical benefit—depends on many factors, including patient adherence, appropriate ART regimens, laboratory monitoring, physician knowledge, and biologic factors that include measurement of pretreatment viral load and CD4 cell count [4–6]. Suboptimal adherence and/or suboptimal ART regimens lead to inadequate viral suppression and the emergence of drug-resistant strains of HIV-1 [7], resulting in treatment failure, disease progression, and the potential for transmission of resistant virus—a major obstacle to the long-term efficacy of ART [6, 8–11]. Therefore, promoting optimal adherence to ART and optimal treatment regimens is critical to maintaining virologic suppression and thereby ensuring the global success of treatment of HIV infection.

An estimated 5.7 million persons live with HIV infection in India. Of these, an estimated 0.7 million have AIDS and require ART [12]. Although free ART is increasingly available in government clinics, many patients still choose to pay out-of-pocket for ART and are treated in the private sector, a fee-for-service health care system consisting of clinics and hospitals that are unregulated, vary in quality, and account for ∼80% of all health care expenditure in India [13].

Despite the importance of understanding the determinants of ART adherence and determining what proportion of patients receiving ART in India have virological suppression, there are little published data. Our objective was to assess ART adherence and virologic suppression and to identify their correlates among HIV-infected individuals who were receiving ART in a sample of private, outpatient clinics in Mumbai, India, an urban epicenter of HIV infection.

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Methods

We conducted a cross-sectional study among HIV-infected patients who were receiving ART in 3 private outpatient clinics in Mumbai from December 2004 through April 2005. The study design and methods were approved by Johns Hopkins University School of Medicine Institutional Review Board and a local Mumbai ethics committee. Informed consent was obtained from all participants in the study. Human experimentation guidelines of the US Department of Health and Human Services and the participating institutions were followed in the conduct of this research. Informed consent procedures were reviewed and approved by independent ethical committees in Mumbai, India, and the United States.

Clinic Sites and Provider Characteristics

Clinic sites were located in 3 geographically distinct areas of Mumbai: the central region (Dadar), the northern region (Malad), and the eastern region (Ulhasanagar). Each physician had a local reputation for treating patients with HIV infection and prescribing ART. The size of practice varied from 150–2500 patients with HIV infection, and an estimated 14%–60% of these patients were receiving ART. Physicians had 6–16 years of HIV experience.

Study Participants

Of 283 patients approached, 279 (98.6%) completed the survey. Patients were considered to be eligible for inclusion in the study if they were ⩾18 years of age and had been receiving ART for at least 3 months. Patients were excluded from the study if they had an acute illness, were unaware of their HIV infection status, or were unable to provide informed consent. All participants paid out-of-pocket for their ART except for 3 individuals whose ART expenses were reimbursed by a nongovernmental organization.

Data Collection

All materials used for participant interactions (including informed consent, participant survey, and response cards) were translated and back-translated from English to Marathi or Hindi. At each clinic, patients were consecutively sampled each day during morning office hours for the duration of the study period or until all consenting, eligible patients were interviewed, whichever came first.

Participant interviews. Structured interviews were conducted by local, trained interviewers in a private room, prior to each participant's visit with their physician. Each participant completed a 45-min, 145-question administered survey that included questions regarding medication adherence and adverse effects, social support, use of alternative therapies, comorbidities, counseling, health care satisfaction, health-related quality of life, substance use, health beliefs, assessment of economic burden (e.g., household income and monthly cost of ART), and sociodemographic characteristics.

Adherence was assessed using the Adult AIDS Clinical Trials Group questionnaire, responses to which have been shown to correlate with plasma viremia [14]. Adherence was defined as having taken ⩾95% of the prescribed doses over the past 4 days. To mitigate participant concerns regarding disclosure of nonadherence, we followed suggestions made by Paterson et al. [15], including having the questioner not be the physician and inserting a preamble before the adherence questions to help the participant understand that they were not being judged and that honest answers were being sought.

Medication reminders, social support, and substance use were assessed using items from the Adult AIDS Clinical Trials Group Baseline Adherence questionnaire II [14], and health care satisfaction was assessed using items from the Utilization of Services section of the Quality of Life Instrument [16]. Health-related quality of life was assessed using the 12-question Medical Outcomes Survey (MOS-SF12) [17]. To facilitate local understanding, minor modifications were made to 2 role-functioning questions that assessed perceived ability to work and perform daily tasks (e.g., “flights of stairs” was changed to “couple of floors [18–28 steps]”).

Provider survey. A 16-question survey was completed by the physician on the same day as the participant's interview. Data gathered included World Health Organization (WHO) clinical stage [18], WHO performance scale, duration of ART, past and current ART regimen(s), and prior CD4 cell count and viral load results.

Laboratory Assessments

Laboratory measurements included a complete blood count, CD4 cell count, and quantitative HIV-1 RNA level using the Amplicor Monitor Standard Assay, version 1.5 (Roche Molecular Systems) validated for subtype C. Given the high cost of HIV-1 RNA testing, 200 of 279 participants were tested. The lab that performed the testing had no clinical information regarding the patients and took samples from the storage box without any specific application of a selection criteria. A detection limit of 400 copies/mL was used for the measurement of HIV-1 RNA level; patients with a level <400 copies/mL were defined as having virologic suppression. Results of laboratory measurements were forwarded to the participant's physician.

Statistical Methods

Characteristics of adherent and nonadherent participants were compared using the χ2 and Fisher's exact tests for categorical variables and the Mann-Whitney tests for continuous variables. Multiple logistic regression was used to identify factors that were independently associated with adherence to ART. Factors that were significantly associated with adherence in univariate analysis at the P < .10 level were considered in the final model. In addition, variables associated with adherence in the published literature were forced into the model, regardless of statistical significance. The same approach was taken to assess correlates of virologic suppression. Interactions between age, sex, and other covariates were examined by including appropriate interaction terms in the model. Data analyses were performed using SAS software, version 9.1.3 (SAS Institute), and STATA software, version 9.0 (Stata Corporation).

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Results

Sociodemographic and clinical characteristics.Characteristics of participants are summarized in table 1. Median time since receipt of HIV diagnosis was 42 months (interquartile range [IQR], 22–66). The reported reasons given by the physician for initiating ART were low CD4 cell count (in 40.9% of patients), observation of symptoms of disease or advanced WHO stage (in 29.8% of patients), or a combination of both (in 24.0% of patients). Median total duration of ART was 21 months (IQR, 10–32). Of 51 participants (18.3%) with a CD4 cell count <200 cells/mm3, 22 (43.1%) were not receiving optimal prophylaxis for opportunistic infections. Seventy-one participants (25.5%) were receiving concurrent treatment for tuberculosis. Only 10 participants (3.6%) reported seeking care from an alternative health care provider, but 61 participants (22.1%) reported using alternative treatments for HIV infection. Of 167 participants (59.9%) who had ever drunk alcohol, 127 (76.0%) reported having no drinks in the past month, and only 6 (3.6%) reported drinking at least 3–4 times per week in the past month.

Table 1
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Table 1

Sociodemographic and clinical characteristics of 279 HIV-infected persons receiving antiretroviral therapy (ART) at 3 private clinics in Mumbai, India.

Of the 279 total participants, 225 (80.6%) were receiving ⩾3 ART medications, and 269 (96.4%) had a twice-a-day dosing schedule. The median number of pills per day was 3 (IQR, 2–4 pills per day). Two hundred forty participants (86.0%) purchased ART medications at the clinic where treatment was received; of these, 84.6% purchased a 30-day supply. The median travel time to the clinic was 45 min (IQR, 30–90 min), and 36 participants (12.9%) traveled >5 h. The majority (95.3%) had disclosed their HIV infection status to friends or family, and 62 (22.2%) lived in a household with another HIV-infected person.

The median reported monthly cost of ART (in Indian rupees [INR]), INR2000 (US$44), was 60% of the median reported monthly income of INR3333 (US$74). One hundred fifty participants (53.8%) stated they had done at least 1 of the following to pay for their ART medications: spent less on clothes (79.3%) or food (36.4%), borrowed money from others (77.1%), sold personal items (37.9%), or changed where they lived (10.0%).

The majority (98.2%) of patients believed that ART improves health; 188 participants (67.4%) disagreed with discontinuation of ART after improvement of symptoms, 167 (59.9%) agreed that missing doses may allow for viral rebound, 19 (6.8%) believed that alternative therapies can improve their HIV infection condition, and 165 (59.1%) agreed that HIV-infected people experience discrimination.

Self-reported adherence and its correlates. By self report, 205 participants (73.5%) reported having taken ⩾95% of their prescribed doses in the past 4 days, 45 (16.1%) took 70%–94% of their prescribed doses, and 29 (10.4%) took <70% of their prescribed doses. Common reasons for missing doses were “ran out of pills” (in 26.2% of participants), “traveling away from home” (in 15.4% of participants), “felt sick or ill” (in 11.5% of participants), “simply forgot” (in 9.3% of participants), and “busy with other things” (in 8.2% of participants).

Significant univariate correlates of adherence were age, higher health-related quality of life, and having the perception that people with HIV infection experience discrimination (table 2). Significant regimen-related correlates of adherence were cost of ART per month, having a regimen with ⩾3 antiretroviral drugs, and taking ⩾3 pills per day. Correlates negatively associated with adherence were lack of medication reminders from family or friends, confusion regarding medication regimen, adverse effects of medication (any gastrointestinal-related or ⩾2 other adverse effects), and presence of pain during the past month. Sociodemographic factors (such as sex, education, marital status, employment, travel time to clinic, or number of sexual partners) and clinical factors (such as WHO clinical stage, concurrent treatment for tuberculosis or opportunistic infection, duration of treatment, number of prior regimens, number of doses per day, substance use, or use of alternative therapies) were not associated with adherence (P > .10).

Table 2
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Table 2

Correlates of adherence among 279 HIV-infected persons receiving antiretroviral therapy (ART) at 3 private clinics in Mumbai, India.

In multivariate logistic regression, patient age ⩾50 years (aOR, 3.90), presence of comorbid conditions (aOR, 1.92), medication self-efficacy (aOR, 4.01), absence of pain in the past month (aOR, 2.14), and satisfaction with overall support from family and friends (aOR, 2.57) were independently associated with adherence. Lack of reminders from family members to take medication (aOR, 0.27) was negatively associated with adherence. Higher adherence was observed in 1 of the 3 clinics, but adjustment for clinic site did not change the relationship to adherence or the statistical significance of other correlates (data not shown).

Correlates of virologic suppression. Of the 200 participants for whom HIV-1 load data were obtained, 127 (63.5%) had virologic suppression. Although these 200 participants did not differ sociodemographically from the 79 participants for whom viral load was not determined (data not shown), participants for whom viral load was determined were less likely to be adherent than those for whom no viral load was determined (adherence rate, 69% vs. 85%; P = .007).

Compared with nonadherent participants, adherent participants were 3 times more likely to have virological suppression (table 3). Of 139 participants who were receiving a WHO-approved nonnucleoside reverse-transcriptase inhibitor—containing regimen, 104 (74.8%) had virological suppression, compared with 14 (32.6%) of 43 patients who were receiving a dual nucleoside reverse-transcriptase inhibitor regimen and 5 (45.5%) of 11 who were receiving a boosted protease inhibitor regimen. In univariate analysis, level of adherence, receiving ⩾3 ART drugs, a higher physical health score on the MOS-SF12 (⩾50), and cost of ART were significantly associated with virologic suppression, whereas lifetime duration of ART (i.e., >24 months) and clinic site were associated with a detectable viral load (table 4).

Table 3
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Table 3

Immunologic and virologic correlates of adherence among HIV-infected persons receiving antiretroviral therapy at private clinics in Mumbai, India.

Table 4
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Table 4

Characteristics associated with HIV suppression for 200 patients receiving antiretroviral therapy (ART) at 3 private clinics in Mumbai, India.

In multivariate analysis, virologic suppression was independently associated with a regimen containing ⩾3 ART drugs (aOR, 5.52), first ART regimen (aOR, 3.28), adherence to ART regimen of ⩾95% (aOR, 5.70), female sex (aOR, 3.19), and a physical component score ⩾50 (aOR, 1.07). There was a trend (P = .08) that a monthly cost of ART of INR1200–INR1999 was associated with virologic suppression.

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Discussion

Little is known about adherence to ART and virologic suppression in India, where many HIV-infected patients pay out-of-pocket for care and treatment [13, 19]. In our study, we determined that the adherence rate among persons paying out-of-pocket for ART is 73.5%—higher than the pooled estimate of 55% adherence from North American studies (which includes data for complex protease inhibitor regimens), but similar to the 77% pooled estimated adherence data in studies from Africa, where fixed-dose nonnucleoside reverse-transcriptase inhibitor—containing regimens predominate [20]. Second, we determined that overall virologic suppression was 63.5% and that 75% of patients who were receiving a WHO-approved nonnucleoside reverse-transcriptase inhibitor—containing regimen had virologic suppression. Third, we found that self-reported adherence, as determined by the Adult AIDS Clinical Trials Group instrument, is correlated with virologic suppression, with 71.5% of adherent participants having virologic suppression. Last, we observed that social support, such as reminders by family members to take medication, and medication self-efficacy are among the modifiable factors that significantly influence adherence levels, whereas regimen type and adherence were modifiable factors associated with virologic suppression.

Few studies have identified correlates associated with adherence to ART in India. Social support is a well-established correlate of adherence in the West [5, 21, 22] and has been reported as being important in a qualitative study in Chennai, India [23, 24]. We also found that social support from family and friends, including reminders to take medication, was associated with optimal adherence. In addition, we found patient age, adverse effects, comorbidities, and medication self-efficacy to be significant correlates of adherence. We postulate that the associations between adherence and age and between adherence and comorbidities may be related to greater familiarity with the health care system and/or an already-established habit of taking daily medications. Several of these determinants have been found to be significant in other studies [25–28].

Studies in resource-rich countries have shown that, in clinical trials, combination ART reduces HIV-1 RNA load to <400 copies/mL in 22%–89% of treatment-naive patients, depending on the regimen used [29–32]. Treatment outcomes with combination ART outside of clinical trials have been less successful, with 15%–60% of patients achieving sustained virologic suppression at 1 year after initiation of therapy [33, 34]. In resource-limited areas, even with high adherence and simple ART regimens, many studies have shown that only 50%–85% of patients achieve viral loads of <400 copies/mL at 1 year [1, 2, 35, 36]. In our study, 63.5% had virologic suppression. The group with the highest rate of virologic suppression was those who were receiving WHO-approved regimens containing nonnucleoside reverse-transcriptase inhibitors, which are more convenient and tolerable than protease inhibitors. As expected, persons who were receiving suboptimal dual nucleoside reverse-transcriptase inhibitor regimens were least likely to have virologic suppression (35.6%). Such regimens threaten the long-term success of treatment of HIV infection. We did not formally assess why suboptimal prescribing was occurring, but studies have shown that this can occur when physicians perceive a patient's inability to pay or when physicians have limited experience with or knowledge of the management of HIV infection [37–39].

Cost is a well-documented barrier to adherence and, thus, to virologic suppression in many resource-limited areas [5, 24, 40, 41]. We found that 54% of participants reported payment for ART to be an economic burden, and that 60% of median monthly income is spent on ART. Although we did not find cost to be an independent predictor of adherence or virologic suppression, economic burdens on the household caused by the cost of ART and care of an HIV-infected person are likely to shift a proportion of families into poverty, as has been described in other studies in India, where costs of medical care have been substantial [42]. Furthermore, with >30% of our sample population experiencing virologic failure, effective and affordable second-line regimens are essential. Because protease inhibitors remain substantially more costly in India than nonnucleoside reverse-transcriptase inhibitors (currently, they are >4 times the cost of the least expensive nonnucleoside reverse-transcriptase inhibitor, nevirapine), many persons continue to receive failing regimens because the costs of second-line therapies are prohibitive.

Of interest, although it was not the focus of our study, we found that 43% of patients with a CD4 cell count <200 cells/mm3 were not receiving Pneumocystis jiroveci infection prophylaxis. The reasons for this are unclear, but it may be the result of a lack of physician or patient awareness of CD4 cell count or the result of patient noncompliance. Although emphasis on ART access and adherence is critical, appropriate prophylaxis against opportunistic infection must not be overlooked as an important strategy for the optimal management of HIV infection. Furthermore, we identified a high proportion of participants who were receiving both ART and tuberculosis therapy. The complexities of managing the cases of persons who are dually affected by HIV infection and by tuberculosis remains one of the most important challenges in resource-limited areas.

Our study is cross-sectional in design and, therefore, does not reflect the dynamic nature of adherence. We based our adherence assessments on patient self-report using a validated instrument; although this is commonly done, it does not perfectly correlate to actual adherence rates. We attempted to enroll all eligible patients who presented to our clinics; however, because we chose a convenience sample of clinics, our results do not necessarily reflect treatment practices at other private clinics in Mumbai or elsewhere. Furthermore, because our participant group was urban, relatively well-educated, and of middle income, our results may not be generalizable to persons who are seeking treatment in rural or public clinics, where persons are generally of lower educational and economic status. Larger studies that sample a variety of clinic sites, as well as longitudinal studies that assess adherence across multiple regimen types (including once-daily ART, diverse geographies, and varying socioeconomic levels in India), are needed to better understand adherence correlates and develop appropriate intervention strategies to improve adherence.

With limited affordable second-line regimens in India and limited laboratory monitoring, optimal adherence to appropriate first-line regimens is an essential strategy to ensure treatment success in India and in other resource-limited areas. Further understanding of factors associated with optimal adherence and virologic suppression in India is required. Continued education of patients, their families, and health care providers regarding adherence and antiretroviral regimens, as well as the development of validated low-cost interventions that optimize adherence and viral load monitoring, are essential for India. As government programs in India expand access to free ART for HIV-infected patients, lessons learned from India's private sector regarding the ART experience may optimize the success of public programs.

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Acknowledgments

We thank the study interviewers and participants. We thank Metropolis Laboratories in Mumbai, India, and Dr. Balakrishnan at the Y. R. Gaitonde Centre for AIDS Research and Education, Chennai, India.

Financial support. Human Healthcare and Research Foundation (Mumbai, India) and National Institutes of Health–Johns Hopkins University K12 Junior Faculty Scholars Program (support to A.G.).

Potential conflicts of interest. All authors: no conflicts.

  • Received November 6, 2006.
  • Accepted January 20, 2007.
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  1. Clin Infect Dis. (2007) 44 (9): 1235-1244. doi: 10.1086/513429
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