The timely initiation of antiretroviral therapy (ART) is required to lower the risk of HIV-related morbidity and mortality . Criteria for initiating ART include both clinical staging and consideration of the CD4 cell count, as a marker of the severity of immunodeficiency . The threshold value, below which the risk of opportunistic infections starts to increase substantially, has long been considered to be 200 CD4 cells/μl . Clinical research in high resource settings, however, tends to encourage initiating therapy in ART-naive adults before the CD4 cell count drops below 350 cells/μl or even at an earlier stage [3–5].
In the case of resource-limited settings, where access to CD4 testing is not widespread, treatment guidelines from the World Health Organization (WHO)  underline that clinical parameters prevail over immunological markers when deciding on ART initiation. These guidelines also stipulate that, when available, the CD4 cell level must also be considered as additional relevant information that can guide the final decision on whether to initiate ART or not, the benchmark threshold being 200 cells/μl. The WHO public health approach to ART delivery in resource-limited settings, characterized by standardized and simplified antiretroviral regimens , has been shown to result in individual immunological and virological outcomes comparable with those obtained in high-resource countries [7,8]. However, the two different standards currently used for initiating ART in high and resource-limited settings are controversial both for ethical  and public health reasons  and the implications of their use have not yet been addressed at the individual level. Moreover, despite the fact that perceived health is known to influence risky behaviours, including unprotected sex [11–14], it has not been well documented for patients in low-resource settings who are not eligible for treatment according to current guidelines.
In this study, we aimed at evaluating the effect of non access to ART on health-related quality of life (HRQoL), unsafe sexual behaviours, self-reported symptoms and disclosure of HIV status to relatives or friends in a population of HIV-infected outpatients with different CD4 cell levels living in Cameroon. This country, severely hit by the AIDS epidemic , has developed a large national programme of ART scaling up with treatment guidelines based on the WHO recommendations [16,17].
Study design and patients
Since 2001, Cameroon has developed a large national programme for access to ART for people living with HIV and AIDS (PLWHA). The cornerstone of this programme is the progressive decentralization of HIV care, through the creation of specialized healthcare facilities outside the capital cities of Yaoundé and Douala (central level of health care). To that end, HIV care centres were first created in each of the 10 provinces of the country (provincial level), and then at the most decentralized level, within districts (district level). In this context, the national cross-sectional multicentre survey EVAL (ANRS 12-116) was conducted in 27 HIV care centres in Cameroon between September 2006 and March 2007, among a random sample of 3151 PLWHA, aged 21 years or older and diagnosed HIV positive for at least 3 months. Clinical data were collected using medical questionnaires filled in by care providers, whereas sociodemographic, economic and psychosocial data were collected during face-to-face interviews of participants performed by trained interviewers. The EVAL research project was funded by the French National Agency for Research on AIDS and Viral Hepatitis (ANRS) and was approved by the Ministry of Public Health in Cameroon and the Cameroonian National Ethics Committee. Its complete design is detailed elsewhere .
National guidelines for HIV treatment in Cameroon [16,17] recommend ART initiation in: patients with AIDS clinical stage [Centers for Disease Control and Prevention (CDC) stage C] whatever their CD4 cell count; all patients with CD4 cell counts lower than 200 cells/μl; patients with CDC stage B2 and CD4 cell counts between 200 and 350 cells/μl who have recurrent infections.
In decentralized healthcare facilities, with limited access to CD4 cell testing equipment, national guidelines recommend the use of the WHO classification to evaluate patients' clinical stage and the use of the total lymphocyte count to evaluate their immunodeficiency (1200 lymphocytes/μl roughly corresponding to 200 CD4 cells/μl). ART must be initiated in patients at WHO clinical stage 3 or 4 and in patients at WHO clinical stage 2 who have a total lymphocyte count below 1200 cells/μl.
Health-related quality of life
Patient HRQoL was assessed using the 12-item medical outcomes study short-form general health survey (SF-12) . This generic questionnaire, which has been validated in the specific context of HIV infection , enables the computation of eight HRQoL subscores, on the basis of patient responses to 12 items concerning their perceptions and feelings during the previous 4 weeks. Each subscore corresponds to one of the following dimensions of HRQoL: physical functioning, role limitations as a result of physical health, bodily pain, general health perceptions, vitality, social functioning, role limitations as a result of emotional problems and mental health. Two aggregate component summary scores – physical (PCS) and mental (MCS) – each ranging from 0 to 100, can be derived from these subscores, with higher score values corresponding to better HRQoL.
Inconsistent condom use
Patients were asked about sexual activity and condom use during the previous 3 months. For the purpose of the present analysis, unsafe sexual behaviours were defined as reporting inconsistent condom use with one's steady partner (either HIV-negative or of unknown HIV status) or with one's casual partners. Patients who reported they used condoms ‘almost always’, ‘sometimes’ or ‘never’ during the previous 3 months were considered as reporting inconsistent condom use.
Number of self-reported disease symptoms
Patients were asked about the occurrence of 18 listed disease-related symptoms during the previous 4 weeks. This list was based on the HIV symptom index developed by Justice et al.  and included symptoms such as headaches, fatigue and diarrhoea .
Disclosure of HIV status
Patients were asked if they had disclosed their HIV status to a member of their family or a friend, as well as the total number of persons to whom they had disclosed their status, this latter being recorded as follows: no one apart from medical staff; only one person; between one and five persons; more than five persons. For the present analysis, the outcome variable that was used was whether or not the respondent reported to have disclosed her/his HIV status to at least one person apart from medical staff (described hereafter as disclosure to relatives or friends).
Propensity scores matching
The main characteristics of patients receiving ART or not, at the time of the survey, were compared using chi-square and Wilcoxon rank-sum tests for categorical and continuous variables, respectively. These characteristics included sex, age and time since HIV diagnosis, as well as the following known correlates of access to ART: CD4 cell count and experience of AIDS-defining events (CDC C clinical stage). ART and non ART-treated patients were also compared according to the characteristics of the healthcare facility in which they were taken care of: level of decentralization in service delivery (central, provincial, or district level)  and size of the facility (small, i.e. less than 80 hospital beds; medium, i.e. 80–220 hospital beds; large, i.e. more than 220 hospital beds). Propensity score matching was then used to adjust for treatment selection bias as a result of the differences observed. Since its presentation in the work of Rosenbaum and Rubin , this statistical method has been extensively used in observational studies, particularly in the context of cardiovascular pathologies [25,26]. In the present study, it consisted of calculating for each patient the predicted probability of not receiving ART (the propensity score) using a logistic regression model adjusted for the characteristics cited above. Patients with the same propensity score therefore had the same probability of not receiving ART, based on sex, age, time since diagnosis, CD4 cell count, CDC stage, as well as the level of healthcare structure decentralization and size of the hospital. Patients not receiving ART (cases) were then matched on propensity score with those receiving ART (controls) using the nearest available pair matching method. All cases were matched with a control.
Modelling of the effect of not receiving antiretroviral therapy on psychosocial outcomes
In a first step, the effect of receiving ART or not on psychosocial outcomes was estimated using univariate regression models. Logistic regression was used to model the two following binary outcomes: disclosure to more than one person except medical staff and unsafe sexual behaviours during the previous 3 months. To model the impact of ART on continuous HRQoL scores (PCS and MCS), analysis of variance was used, after normalization using a transformation based on the normal density curve . Finally, negative binomial regression was used to model the impact of ART on the number of self-reported disease-related symptoms, because this variable had a positive discrete distribution and the sample variance exceeded the sample mean.
Adjusted odds ratios and coefficients were then calculated for the effect of receiving ART after introducing into the models the following sociodemographic and HIV-related factors already known to be associated with patient psychosocial outcomes: age; sex and social living conditions; educational level; living in a couple; living under the poverty line (defined as earning less than 20 000 FCFA (francs de la communauté financière Africaine) per equivalent adult and per month) ; CD4 cell count at last assessment (below or above 200 cells/μl); time since HIV diagnosis; hospitalization during the previous 6 months; number of self-reported symptoms (except of course for the model dealing with the number of self-reported symptoms as the outcome variable) and, finally, knowledge of the HIV status of the respondent's main sexual partner.
Finally, in order to evaluate the effect of receiving ART or not on psychosocial outcomes for different CD4 cell levels and clinical stage, the obtained multivariate models were re-run after dividing the sample of non-treated patients into the following three subcategories: individuals with CD4 cell counts less than 200 cells/μl or AIDS stage (which corresponds to the current WHO criteria for initiating ART in resource-limited settings), individuals with CD4 cell counts between 200 and 350 cells/μl and individuals with CD4 cell counts greater than 350 cells/μl.
The significance level was fixed at α = 0.05 for all tests. Statistical analyses were performed using the SPSS version 15.0 (SPSS Inc, Chicago, Illinois, USA) and Intercooled Stata 9 (StataCorp LP, College Station, Texas, USA) software packages.
Patients' characteristics at the time of the survey
Most of the 3151 PLWHA (71.1%) participating in the EVAL survey were women (Table 1). A total of 2466 patients (78.3%) was receiving ART at the time of the survey, whereas 685 (21.7%) were not receiving it. Among patients who were receiving ART, the median [interquartile range (IQR)] time since ART initiation was 10.4 (2.0–23.9) months. Approximately 81% of these patients had a CD4 cell count below 200 cells/μl at the time of ART initiation. Patients who were not receiving ART were significantly younger than their ART-treated counterparts (Table 1). In addition, they had been diagnosed HIV positive for a shorter period of time, they had experienced AIDS-defining events less frequently, and had a significantly lower CD4 cell count at the time of the survey. Finally, they were more frequently followed up in a HIV centre located at the district level, and less frequently followed up in medium-sized hospitals. The breakdown of non-treated patients into categories combining CD4 cell count and clinical stage was as follows: a total of 265 (8.4% of the participants in the EVAL survey) had less than 200 CD4 cells/μl or were at the AIDS stage, 156 (5.0%) had a CD4 cell count between 200 and 350 cells/μl, and 264 (8.4%) had a count greater than 350 cells/μl. Among this latter group of patients, CD4 cell median (IQR) was 498 (396–691) cells/μl. Fifty-nine per cent of the 265 not-treated patients with less than 200 CD4 cells/μl or AIDS stage reported they may start therapy soon (patients with ongoing examinations or waiting for the therapeutic committee's decision). In addition, 16% were currently being treated for tuberculosis, which may have deferred treatment initiation. As logically expected, differences between ART-treated and non-treated patients were less pronounced after matching by propensity analysis (Table 1). There remained statistically significant differences in CD4 cell count and time since HIV diagnosis. These differences were not, however, of clinical relevance (in median 345 versus 318 cells/μl and 14 versus 12 months).
The distribution of psychosocial outcomes after matching by propensity analysis (n = 1370) is presented in Table 2. HRQoL data were available for a total of 1366 patients. Median (IQR) value for SF-12 PCS and MCS scores were respectively 49.2 (40.3–55.1) and 44.1 (37.2–50.7). Among the 650 patients (47.4%) who reported sexual intercourse during the previous 3 months, a total of 453 reported it with their main partner of either serodiscordant or unknown HIV status or with casual partners. Inconsistent condom use was reported by 48.1% of these patients. In addition, the median (IQR) number of self-reported symptoms was five (3–8) and approximately three-quarters of patients reported having disclosed their HIV status to relatives or friends.
Models for the effect of receiving antiretroviral therapy or not on psychosocial outcomes
After adjustment for sociodemographic and HIV-related factors, as well as characteristics of healthcare delivery centres, multivariate regression models showed that impaired physical HRQoL, greater risk of inconsistent condom use, higher number of self-reported disease symptoms and less frequent disclosure of HIV status to relatives or friends were all significantly associated with not receiving ART (Table 3). These results were confirmed after stratifying non-treated patients according to their CD4 cell level and clinical stage (Table 3), with all categories of non-treated patients revealing significantly poorer psychosocial outcomes than treated patients.
This study clearly highlights that HIV-infected outpatients not yet receiving ART in Cameroon significantly differ from their ART-treated counterparts in terms of major outcomes: they engage more frequently in unsafe sexual behaviours and experience an impaired quality of life – as expressed by physical HRQoL, self-reported symptoms and difficulties with HIV disclosure to relative and friends. These results, obtained after matching treated and non-treated patients for the clinical and healthcare-related characteristics used when deciding on ART initiation, still held after multivariate analysis adjusted for sociodemographic and HIV-related factors. It is interesting to note that impaired quality of life and higher inconsistent condom use frequency were observed for all categories of non-treated patients, irrespective of their CD4 cell count and clinical stage. Indeed, even non-treated patients with high CD4 cell counts (>350 cells/μl) reported significantly impaired physical HRQoL, were at greater risk of inconsistent condom use and reported to have disclosed their HIV status to relatives or friends less frequently when compared with ART-treated patients. These results suggest that access to ART is correlated not only with improved wellbeing, but also with better experience with HIV disease at the individual level. Overall, these results bring additional evidence for the urgent need to readjust CD4 cell guidelines for ART initiation in resource-limited settings in order to improve HIV care  and to lower the risk of HIV transmission. Most HIV-infected patients in resource-limited settings tend to get access to ART when they have advanced symptomatic disease , which leads in turn to high early mortality rates . Indeed, improved HIV care through timely access to ART can only be possible if combined with increased access to HIV testing facilities and counselling .
In the present study, non-treated patients had lower levels of physical HRQoL than their ART-treated counterparts. Few studies have addressed the issue of HIV-infected patients' HRQoL in the context of ART scaling up in Africa [32–34]. One study conducted among 371 HIV-infected patients in South Africa showed significant improvements in physical quality of life in the initial months of ART [32,33]. Another study conducted among 947 HIV-infected patients in rural Uganda highlighted significant gains in both physical and mental HRQoL over the first year of ART, with most of the gains being achieved by the third month of therapy . In the present study, treated patients were receiving ART for a median of 10 months, which appeared to be a sufficiently long enough period to observe a significant improvement in physical HRQoL in comparison with non-treated patients.
This higher level of HRQoL was correlated with better experience of the HIV disease, as expressed by a lower number of self-reported disease symptoms. Information about symptom prevalence in the context of ART in resource-limited settings remains limited. A recent study in South Africa showed that being treated with ART was not associated with lower HIV symptom levels . Two-thirds of patients included in that study reported having been diagnosed with an AIDS-defining event, whereas this was the case for only one-third of the patients in our study group.
The present study also highlights the positive effect of access to ART on safe sexual behaviours of HIV-infected patients, and rather contradicts the familiar psychosocial a priori hypothesis that access to treatment may induce a relapse into unprotected behaviours [36,37]. Most studies in high-resource settings have already concluded that the risk of unsafe sex is not higher among patients receiving ART, as shown in the meta-analytic review by Crepaz et al. . This has also been confirmed by several studies conducted in African countries [39–45]. In the present study, patients not receiving ART were from one and a half to three times more likely to report unsafe sexual behaviours than their ART-treated counterparts. Although the non-ART-treated subsample in the EVAL survey included PLWHA who were aware of their serostatus and were already followed up for HIV care, they may have a poorer access to HIV prevention and counselling as positive prevention is often delivered in health facilities on the occasion of ART initiation. Counselling interventions for supporting adherence to ART may also play a key role in preventing unsafe behaviours in general, including inconsistent condom use .
Finally, access to ART appears to encourage disclosure of seropositivity to family members and friends. This may be partly explained by the fact that, when initiating ART, caregivers encourage patients to do so in order to facilitate adherence. Obviously, this may also be a ‘forced’ disclosure, in order to explain to family members why the patient has to take drugs every day and make frequent visits to hospital. Several recent studies in the African context point out the positive outcomes of disclosure of HIV status, notably to sexual partners, in terms of risk reduction behaviour and greater social support [46–48].
The present study is limited by its cross-sectional design, which made it impossible to evaluate pre to post-ART changes in patients' psychosocial outcomes. To our knowledge, however, this is the first study to document the effect of access to ART on a set of psychosocial outcomes evaluated on a given population in a resource-limited setting. In addition, this study was conducted on a national sample representative of HIV outpatients followed up in the Cameroonian health system.
Our results suggest that access to ART in resource-limited settings has a positive effect on HIV-infected patients' wellbeing, even for patients with high CD4 cell levels. Findings also underline the need for offering specific psychosocial support to non-ART-treated patients, who are often left to their own devices. Finally, in light of recent data from clinical research in high-resource settings, our results strongly argue for a reconsideration of CD4 cell threshold values currently used in treatment guidelines for resource-limited settings in order to maximize the impact of ART programmes on public health and individual wellbeing .
The authors would like to thank the hospitals that participated in the survey and their medical teams, as well as all the patients who agreed to take part in the study. Their thanks also go to Professor Jason Barabas, from Florida State University, for his availability and his methodological support on the use of propensity scores matching. The authors would also like to thank Jude Sweeney for the English revision and editing of the manuscript.
Members of the EVAL Study Group
S. Koulla-Shiro (Central Hospital, Yaoundé, Cameroon), P. Ongolo-Zogo (Ministry of Public Health, Division of Health Operations Research, Yaoundé, Cameroon), J. Blanche, A.-D. Bouhnik, S. Boyer, M.-P. Carrieri, A. Dia, F. Eboko, S. Loubière, F. Marcellin, J.-P. Moatti, Y. Obadia, C. Protopopescu, B. Spire (INSERM, IRD, University of the Mediterranean UMR 912, Marseilles, France), S.-C. Abega, C. Abé, P.C. Bilé, C. Bios, R.-C. Bonono, Y. Mehe, M.T. Mengue, H. Mimcheu, F. Mounsade, L.M. Ngaba, J. Ngo Mbog, S. Ngo Yebga, H. Nkwidjan (IRSA, Catholic University of Central Africa, Yaoundé, Cameroon), R. Nantchouang (GERCIS, Catholic University of Central Africa, Yaoundé, Cameroon).
Sponsorship: The French National Agency for Research on AIDS and Viral Hepatitis (ANRS) funded the EVAL survey (ANRS 12-116) research programme and the Cameroonian Ministry of Public Health supported its execution.
Conflicts of interest: None.
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