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Correspondence and reprint requests: Professor Karl Peltzer Human Sciences Research Council Private Bag X41 Pretoria 0001 South Africa Email: [email protected]

INTRODUCTION

The clinical efficacy of antiretroviral therapy (ART) in suppressing the HIV virus and improving sur- vival rates for those living with HIV has been well- documented (1-3). However, successful antiretrovi- ral therapy is dependent on sustaining high levels of adherence (correct dosage, taken on time, and in the correct way—either with or without food). The minimum level of adherence required for antiretro-

viral drugs to work effectively is 95% (4). Although more potent antiretroviral regimens can allow for effective viral suppression at moderate levels of adherence, no or partial adherence can lead to the development of drug-resistant strains of the virus (5-7). Adherence to ART is influenced by factors as- sociated with the patient, the disease, the therapy, and the relationship of the patient with healthcare provider (8-10). Patient-related factors include so- cioeconomic status (SES) (8,10).

A review of studies since 2005 on SES and adher- ence to ART primarily in high-income countries, did not provide conclusive support for a clear asso- ciation between SES and adherence (8). However, it is not clear what effect socioeconomic factors have on adherence to ART in low- and middle-income

REVIEW ARTICLE

Socioeconomic Factors in Adherence to HIV Therapy in Low- and Middle-income Countries

Karl Peltzer1,2,3, Supa Pengpid2,3

1HIV/AIDS/SIT/and TB (HAST), Human Sciences Research Council, Pretoria, South Africa; 2 Department of Psychology,

University of Limpopo, Turfloop, South Africa; 3ASEAN Institute for Health Development, Madidol University, Salaya,

Phutthamonthon, Nakhonpathom, Thailand 73170

ABSTRACT

It is not clear what effect socioeconomic factors have on adherence to antiretroviral therapy (ART) among patients in low- and middle-income countries. We performed a systematic review of the association of socioeconomic status (SES) with adherence to treatment of patients with HIV/AIDS in low- and middle- income countries. We searched electronic databases to identify studies concerning SES and HIV/AIDS and collected data on the association between various determinants of SES (income, education, occupation) and adherence to ART in low- and middle-income countries. From 252 potentially-relevant articles ini- tially identified, 62 original studies were reviewed in detail, which contained data evaluating the associa- tion between SES and adherence to treatment of patients with HIV/AIDS. Income, level of education, and employment/occupational status were significantly and positively associated with the level of adherence in 15 studies (41.7%), 10 studies (20.4%), and 3 studies (11.1%) respectively out of 36, 49, and 27 studies reviewed. One study for income, four studies for education, and two studies for employment found a nega- tive and significant association with adherence to ART. However, the aforementioned SES determinants were not found to be significantly associated with adherence in relation to 20 income-related (55.6%), 35 education-related (71.4%), 23 employment/occupational status-related (81.5%), and 2 SES-related (100%) studies. The systematic review of the available evidence does not provide conclusive support for the exis- tence of a clear association between SES and adherence to ART among adult patients infected with HIV/ AIDS in low- and middle-income countries. There seems to be a positive trend among components of SES (income, education, employment status) and adherence to antiretroviral therapy in many of the reviewed studies.

Keywords: Antiretroviral therapy, highly active; Education; Employment; Income; Occupations; Social class

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countries. A possible association between SES and adherence to ART among HIV patients may have an impact on the success of their treatment (8,10).

MATERIALS AND METHODS

Literature search

We performed a systematic search of the litera- ture to identify reviews and original studies that reported data on the impact of SES on adherence to ART. The relevant studies were identified by the use of electronic databases, such as MEDLINE, EMBASE, SCI Web or Science, NLM Gateway, and Google Scholar. The last search was conducted in November 2011. In addition, relevant articles from the list of references of the initially-retrieved papers were identified. Studies conducted only in low- and middle-income countries were included, according to World Bank classifications (11). Five different search strategies using the follow- ing key words were employed: (i) Socioeconomic status AND (HIV OR AIDS) AND (compliance OR adherence), (ii) (Compliance OR adherence) AND (HIV OR AIDS) AND determinants, (iii) (AIDS OR HIV) AND (compliance OR adherence) AND edu- cation AND/OR income AND/OR occupation, (iv) (AIDS OR HIV) AND (compliance OR adherence) AND determinants, and (v) (AIDS OR HIV) AND (compliance OR adherence).

Defining socioeconomic status (SES) is difficult because a single, consistent unit of measurement was not used in the studies reviewed. Further, a debate exists in the public-health arena on the appropriate components of socioeconomic sta- tus and methods of measurement (12). Krieger et al. (13) have argued that it is important to dis- tinguish two different components of socioeco- nomic position (actual resources and prestige or rank-related characteristics), and they preferred the use of the term ‘socioeconomic position’ in- stead of ‘socioeconomic status’. In addition, they argued that it is important to collect data at the individual, household and neighbourhood level (12,13). Additional points emphasized included that data on individuals supported from ‘annual family income’ should be collected, measure- ments should incorporate the recognition that socioeconomic position can change over a life- time, and measures of socioeconomic position may perform differentially based on racial/eth- nic group and gender background (12,13). Most of the reviewed articles did not attend to these complexities, rather used one to three mea- sures of SES, most often simplistic measures of

income, education, and occupation or employ- ment status. The reviewed articles were analyzed with the understanding that the complexities present in SES highlighted by Krieger et al. (13) should ideally be incorporated in future studies designed to tease out the relationship between SES and adherence to ART in low- and middle- income populations. Meanwhile, the term SES is used in this article rather than socioeconomic position, simply because this is how these mea- sures were discussed by the authors in the pa- pers reviewed (12). SES reflects different aspects of social stratification, and the traditional indi- cators at the individual level have been income, education, and occupation (14,15). There is no single-best indicator of SES suitable for all study objectives and applicable at all time-points in all settings. Each indicator measures different, often related aspects of socioeconomic stratifi- cation and may be more or less relevant to dif- ferent health outcomes and at different stages in the course of life (15). Galobardes et al. (16) described the theoretical basis of the following three indicators used for measuring SES:

(a) Education attempts to capture the knowledge- related assets of a person. As formal education is normally completed in young adulthood and is strongly determined by parental char- acteristics, it can be conceptualized within a course of life framework as an indicator that, in part, measures socioeconomic position (SEP) in early life (16).

(b) Income is the indicator of SEP that most di- rectly measures the material resources com- ponent (16).

(c) Occupation represents Weber’s notion of SEP as a reflection of a person’s place in soci- ety relating to their social standing, income, and intellect (16).

Selection of studies

The inclusion and exclusion criteria used for the reviewed studies were set before the literature search. Studies included in our study concerned only individual HIV-infected adult patients and their adherence to antiretroviral therapy. Re- views and editorials were not included in our systematic review. Studies that focused on HIV- infected illicit and/or licit drug-users and/or those with severe mental illness were excluded since such persons may need more creative ap- proaches than other patients to ART adherence that differentiates them from the general popu-

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lation (8,17-19). Two authors of the present ar- ticle evaluated the eligibility studies obtained from the literature search using a predefined protocol. The two authors worked independently to scan all ab- stracts and obtained full-text articles. In cases of dis- crepancy, agreement was reached by consensus.

Data extraction

Two authors of the present article independently extracted and compiled the data. For each identified study that met the selection criteria, details were extracted on study design, characteristics of study population, data relevant to SES, the measure of adherence, the overall adherence, and findings re- garding the association between determinants of SES and adherence on to an Excel spreadsheet. In this review, three parameters as major factors con- tributing to SES were assessed, namely income, ed- ucation, occupation/employment status and their association with adherence to ART.

The following diagram presents the various steps in the process of selecting studies.

RESULTS AND DISCUSSION

The literature search identified 252 potentially- relevant studies, from which we further reviewed 62 studies with original data. In Annexure A-F, the characteristics of 62 studies that were in- cluded in the systematic review are presented by region and country. The year of publication of the studies ranged from 2002 to 2011. There was considerable variability across the studies in setting and patient population, largely because these were conducted in different low-resource settings, with different cultures, incomes, and education levels (Table 1).

Regarding the study design, 44 cross-sectional (21,24,26,28-31,33-37,41,42,47-49,53,55,56,58-72, 74-76,78-82), 19 longitudinal (22,25,27,32,38- 40, 43-46,50-52,54,57,77), and two case-control (23,73) studies were included in the review. The average number of patients was 400 per study in the total of 62 studies (ranging from 53 to 2,381, depending on the study setting).

252 Potential relevant articles identified and screened for retrieval

Figure. Flow-diagram of reviewed studies

105 potentially appropriate studies regarding antiretroviral

treatment adherence were further reviewed

147 studies were excluded because these

were not relevant to this study

100 studies included data relevant to the association between SES and

adherence to antiretroviral treatment

5 studies were excluded because these were reviews

73 studies remained for further analysis

27 studies were excluded because of the following: • Health literacy (exclusively) and its influence on adherence (5) • HIV knowledge, ARV knowledge (3) • SES only descriptive information (17) • SES not disaggregated in analysis (e.g. vulnerability, including SES and other variables) (3)

62 original studies remained for further analysis and were

included in this review

11 studies were excluded because of the following: • These referred to illicit and licit drug-users infected with HIV (6) • These referred to persons with serious mental illness

infected with HIV (2) • These referred to HIV-TB co-infected persons • Inmates (3)

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Table 2. Summary of studies on the association between the main components of socioeconomic status and adherence to antiretroviral therapy

SES component Number of

studies N

Positive association

N (%)

Negative association

N (%)

No association

N (%) Education 49 10 (20.4) 4 (8.2) 35 (71.4) Income 36 15 (41.7) 1 (2.8) 20 (55.6) Occupation/employment 27 3 (11.1) 2 (7.4) 22 (81.5) SES 2 0 0 2 (100)

Studies varied in the measurement of adherence (pills per dose, doses per day, days of treatment per week, time schedule for pill-refill, etc.) and used different cutoff points of adherence (from 80% to 100% of dosage) to dichotomize the patients be- tween adherence and non-adherence to ART. Two studies focused directly on the association between SES or its main determinants analyzed as a group and adherence (40,78). The available reported data

regarding the method, with which adherence to an- tiretroviral treatment was measured, and the data on overall adherence are presented in Annexure A-F. In 50 out of 62 studies included in the review, self-report by the patients was the main measure of adherence to treatment (21,22,24,26,27,29-32,34- 37,39,41,42,44-49,51,53,56,58-69,70-82); six stud- ies used pill counts, MEMS, pharmacy refills as the main measures (23,40,43,54,55,57), and in six

Table 1. Education and income (country indicators) in study countries

Country

Education Income

Adult literacy (%)

Primary school enrollment rate:

Male/Female

Gross national income per capita

(PPP int. $)

Living on <1$ (PPP int. $) a

day (%) Botswana 83 86/88 12,840 – Brazil 90 95/93 10,200 5.2 Burkina Faso 29 67/59 1,170 56.5 Cameroon 76 97/86 2,190 32.1 China 94 – 6,890 15.9 Columbia 93 93/80 8,600 16.0 Costa Rica 96 – 10,930 2.0 Cuba 100 99/99 – – Dominican Republic 88 92/82 8,110 4.4 Ethiopia 36 85/80 930 39.0 India 63 91/88 3,250 41.6 Ivory Coast 55 62/52 1,640 23.3 Jamaica 86 82/79 7,230 <2.0 Kenya 87 82/83 1,570 19.7 Mali 26 79/66 1,190 51.4 Nigeria 60 64/58 2,070 64.4 Papua New Guinea 60 – 2,260 – Rwanda 70 95/97 1,060 76.6 Senegal 42 72/74 1,810 33.5 South Africa 95 87/88 10,050 26.2 The Gambia 45 67/71 1,330 34.3 Thailand 94 91/89 7,640 <2.0 Uganda 75 96/99 1,190 51.5 United Republic of Tanzania 73 96/97 1,350 88.5 Zambia 71 96/92 1,280 64.3 Source: World health statistics 2011 (20)

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studies both self-report and objective adherence measures (25,28,33,38,50,52) were used.

The main parameters affecting SES (income, educa- tion, occupation) were only examined as a group comprising SES in two studies but, in 61 studies, these were rather regarded as socioeconomic char- acteristics. Therefore, many studies lacked data concerning some of the parameters. There were insufficient data regarding income in 26 stud- ies (22,28,29,31,33,37,38,41,47,48,50,51,53,54, 56,60,68-70,72,74,75,80-82) and educational level in 14 (26,28,30,37,39-41,46,59,61,62,65,68) of the 62 reviewed studies (Some of the studies had data on income but not on education, and others had the reverse). Employment and/or oc- cupational status was assessed in 28 studies (22- 24,28,29,31,34-37,39-42,44,45,53,54,58,59,61,67- 69,70,77,78,81,82). However, no data were given on occupational status or working position in 18 of those 28 studies.

The main findings regarding the analysis of the as- sociation of SES or the various components of SES and adherence were as follows: income, level of education, and employment/occupational sta- tus were significantly and positively associated with the level of adherence in 15 studies (41.7%) (21,24,26,32,39,43,46,49,62,63,65-67,76,78), 10 studies (20.4%) (33,35,53,66,69,71-73,75,77), and three studies (11.1%) (28,29,77) respectively out of 36, 49, and 27 studies reviewed. Most significant findings refer to a positive associa- tion between levels of SES components and lev- els of adherence to antiretroviral treatment, al- though one for income (59), four for education (21,31,43,63) and two for employment (59,77) of the reviewed studies suggest an inverse asso- ciation with adherence. However, the aforemen- tioned SES determinants were not found to be sig- nificantly associated with adherence in relation to 20 income-related studies (71,73,23,24,25,30,34- 36,42,43,45,57,61,77), 35 education-related stud- ies (22-25,27,29,32,34,36,38,42,44,45,47-52, 60,64,67,70,74,76,78-81,82), 22 employment/ occupational status-related studies (22-24,34- 36,41,42,44,45,49,53,54,58,67-70,78,79,81,82) and two SES-related studies (40,78) (Table 2).

Limitations

This systematic review has several limitations. First, it was not possible to make a synthesis of the data, using the principles of meta-analysis due to the fact that there was considerable heterogeneity among the reviewed studies. Adherence was measured by different methods in each of the studies and the

cutoff percentage of adherence to treatment be- tween ‘adherent’ and ‘non-adherent’ varied among the studies. Another limitation was that the ma- jority of the studies examined the used unreliable measures of adherence (self-report, in particular) as the adherence outcome measure. In addition, SES was not focused upon as a homogenous group of specific factors in most of the reviewed studies but was rather dispersed among its components, which were regarded as socioeconomic informa- tion. Therefore, partial data had to be collected re- garding the association of such SES components, and adherence to antiretroviral therapy, where and if such an association was assessed. Occupation was mainly assessed in terms of employment status because often no data were given on status of oc- cupation or working position of the patients (8).

Conclusions

The systematic review of the available evidence found a positive trend among components of SES (income, education, occupation/employment) and adherence to antiretroviral therapy in many of the reviewed studies. However, we found inconclusive support for a clear association between SES and ad- herence among patients infected with HIV/AIDS in low- and middle-income countries. The association between SES and adherence may differ depend- ing on the cultural/economic/geographic context of the countries studied, and results emphasize a site-specific approach to adherence studies and programmes. Future studies should measure socio- economic factors more accurately and, thus, may further explain the different impacts of SES to ART adherence. In the absence of a gold standard for measure of adherence, future studies should assess many outcomes.

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Peltzer K and Pengpid SSocioeconomic factors in adherence to HIV therapy

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