Recent Patterns in Population-Based HIV Prevalence in Swaziland

Background The 2011 Swaziland HIV Incidence Measurement Survey (SHIMS) was conducted as part of a national study to evaluate the scale up of key HIV prevention programs. Methods From a randomly selected sample of all Swazi households, all women and men aged 18-49 were considered eligible, and all consenting adults were enrolled and received HIV testing and counseling. In this analysis, population-based measures of HIV prevalence were produced and compared against similarly measured HIV prevalence estimates from the 2006-7 Swaziland Demographic and Health. Also, measures of HIV service utilization in both HIV infected and uninfected populations were documented and discussed. Results HIV prevalence among adults aged 18-49 has remained unchanged between 2006-2011 at 31-32%, with substantial differences in current prevalence between women (39%) and men (24%). In both men and women, between since 2006-7 and 2011, prevalence has fallen in the young age groups and risen in the older age groups. Over a third (38%) of the HIV-infected population was unaware of their infection status, and this differed markedly between men (50%) and women (31%). Of those aware of their HIV-positive status, a higher percentage of men (63%) than women (49%) reported ART use. Conclusions While overall HIV prevalence remains roughly constant, age-specific changes strongly suggest both improved survival of the HIV-infected and a reduction in new HIV infections. Awareness of HIV status and entry into ART services has improved in recent years but remains too low. This study identifies opportunities to improve both HIV preventive and care services in Swaziland.


Introduction
HIV is the leading public health concern in Swaziland. Swaziland's Demographic and Health Survey (SDHS), conducted in 2006-7, demonstrated a generalized epidemic with an HIV prevalence of 26% among of 15-49 year olds [1]. Faced with the highest HIV prevalence rate in the world, the Swaziland Ministry of Health (MOH) has expanded access to key HIV services: HIV testing and counseling, HIV care and antiretroviral therapy (ART), and prophylaxis for the prevention of mother-to-child transmission (PMTCT) of HIV [2]. In 2011 based on randomized control trials showing the potent effect of medical male circumcision (MMC) in reducing risk of HIV acquisition from heterosexual exposure in men [3,4,5], the MOH launched a national campaign to increase the uptake of voluntary MMC among HIV-uninfected men ages 15-49. The current study, the Swaziland HIV Incidence Measurement Survey (SHIMS), was designed to assess the impact of this national combination HIV prevention strategy on HIV incidence in Swaziland. In this paper, we describe the cross-sectional (2011) estimates of HIV prevalence as well as HIV testing history and ART use among the Swaziland population and compare these estimates from SHIMS with data from the 2006-07 SDHS to assess trends.

Study design
The overall design of SHIMS was based on the direct measurement of HIV incidence at the population level before and after the scale-up of the national combination HIV prevention strategy. To identify eligible participants for the first incidence cohort, a nationally representative, household-based cross-sectional survey was conducted from December 2010 to June 2011, with key epidemiologic and bio-demographic information collected from Swaziland adults, 18 to 49 years of age. At ages 50+ years, recent (incident) HIV infections are very infrequent.
The household sample size was calculated at 14,927 to permit 80% power to detect a 45% reduction in HIV incidence in men from pre-to post-national scale up of the national combination HIV prevention strategy, assuming a baseline HIV incidence of 2.0% among men. We assumed a design effect of 1.25 (based on previous similar DHS surveys), a retention rate of 90%, a household vacancy rate of 13% and a household refusal rate of 5%; and that 10% of men would not be contactable, 23% would be HIV infected and 5% would refuse to participate in the survey. The households were selected using a two-stage cluster sampling procedure, similar in design to that used by the SDHS. In the first stage, a systematic random sample of 575 of the country's 2076 enumeration areas (EAs) was drawn. In the second stage, a full listing of all households was conducted within each of the 575 EAs. This household listing provided the sampling frame from which a random sample of 26 households was drawn from each EA. Field teams contacted the selected households, and conducted a census of household residents with the head of household (or other available responsible adult household member).
Survey eligibility criteria included residing in or sleeping in the household the night before, reporting an age between 18-49 years inclusive, and the ability to provide informed consent in either SiSwati or English. Further information contributing to the SHIMS sampling methodology and weighting are provided elsewhere [6].

Data Collection and Analysis
Interviewers administered questionnaires in SiSwati or English to survey participants on demographic, clinical and behavioral topics, including self-reported male circumcision status. HIV testing, including pre-and post-test counseling, was conducted in a private location in or just outside of the home. Blood samples were collected by venipuncture and rapid HIV testing was performed using Determine™ HIV-1/2Ag/Ab Combo (Alere, Japan). Determine reactive samples were confirmed with Uni-Gold™ HIV Test (Trinity Biotech, Ireland), following the country's serial testing algorithm. Internal and external quality assurance procedures were implemented throughout the survey. Indeterminate test results were resolved by a two HIV EIA testing algorithm (Genscreen HIV-1/2 Version 2 Assay, Bio-Rad Laboratories, California, USA; and Vironostika HIV Uni-Form II plus O, bioMerieux Inc., France), and final HIV status based on the EIA results were returned to participants in the context of high quality post-test counseling including referral to prevention and, if indicated, HIV care services (pre-ART, CD4+ testing).
Survey weights were applied to the data, accounting for differential probability of selection in the cluster sampling procedure and survey non-response rates. Given N's (with the exception of Table 1) are estimated for SHIMS-sized population. HIV prevalence was based on testing positive in the survey; self-reported HIV status was not used. Illustrations of a circumcised and uncircumcised penis were provided to assist participants in correctly identifying their own (men) or their partner's (women) circumcision status. Analyses were performed with SAS version 9.2 (SAS Institute, Cary, NC).

Ethical considerations
All study participants provided written informed consent prior to the collection of data and blood samples. Ethical approval was obtained from the Swaziland Scientific and Ethics Committee, Columbia University Institutional Review Board (IRB) and U.S. Centers for Disease Control and Prevention IRB before initiation of field work.

Response Rates
The 14,891 selected households were approached, 13,335 were found occupied, and of these, 12,571 households participated in the baseline cross-sectional survey, resulting in a household response rate of 94.3% (Table 1). Urban and rural household response rates did not differ substantially. Among participating households, 13,508 women and 11,048 men aged 18-49 were identified as eligible. Despite up to 9 repeated visits to obtain individual interviews, some eligible person were either not contacted or when contacted refused to participate or make themselves available for interview. Eighty-one (81) % of women (11,042) and 65% of men (7,130) took part in the survey, having agreed to both the HIV test and a face-to-face interview. Urban men had a higher response rate than their rural counterparts (68% versus 63%). No significant differences in response rates were observed by age category or region (data not shown).

Socio-demographic Characteristics of the Study Population
Over half (56%) of the population was under age 30 and most (70%) lived in rural areas of the country (Table 2), a finding which mirrors the population distribution reflected in the most recent National Census (2007) [7]. Over a quarter (29%) of adults reported ever attending only primary school, 50% reported attending secondary school, and 14% reported attending tertiary education. Seven percent of participants reported never attending school. Education-related differentials between surveyed men and women were minimal.
Nearly one-half of women and nearly two-thirds of men age 18-49 reported not being married, and more unmarried men than women reported never having had sex (16 % versus 6%). More women (22%) than men (11%) reported having a marital partner who either lived in a different household or whose living/sleeping arrangements were unknown. Seven (7) percent of women reported being pregnant.
Overall, 22% of participants reported having no sexual partners in the prior six months, 27% of men and 18% of women. Two-thirds (67%) reported having one partner in the past 6 months, 54% of men and 78% of women; while 10% of participants reported having two or more partners, 18% of men and 4% of women. One in 6 (17%) of men reported that they were circumcised.

HIV Prevalence: Levels and Trends
HIV prevalence was 32% among adults aged 18-49 years (Table 3), 24% among men and 39% among women. In both men and women, HIV prevalence increased steeply with age and peaked before age 40 ( Figure 1). Peak HIV prevalence was lower for men (47%) than women (54%) and occurred at an older age (35-39 versus 30-34). The difference in HIV prevalence by sex was most pronounced among young adults: HIV prevalence among <25 year olds was five times higher among women than men (26% versus 5%), a pattern commonly observed in sub-Saharan Africa associated with earlier age at first sex and exposure to HIV in women. The

HIV Prevalence by Socio-demographic characteristics
HIV prevalence was similar in urban and rural areas, and across the four regions of Swaziland, ranging from 31% in Shiselweni and Hhohho to 34% in Manzini (Table 3). HIV prevalence varied substantially by education attainment, with higher HIV prevalence observed among both men and women with less education. In men, HIV prevalence among non-school attenders was more than double (41% versus 16%) that of those who attended a tertiary institution (college, university).
Unmarried men and women who reported never having had sex had relatively low HIV prevalence rates (4% women, 1% men). Infections in men and women reporting having had no previous sexual activity is likely due to underreporting associated with prevailing social unacceptability of early sexual debut, especially among girls. Another possible explanation is that coerced sex and rape was not understood and reported as sexual activity. The prevalence of HIV was substantially higher in sexually active unmarried women (43%) compared to sexually active unmarried men (20%). HIV prevalence among women did not vary by pregnancy status (38% for pregnant; 39% for non-pregnant). Among married men and women, HIV prevalence varied little by whether living with partner or not. In both women and men, higher reported numbers of sexual partners (last 6 months) were associated with higher HIV prevalence. In men, HIV prevalence was markedly higher among those reporting one partner in the last six months compared to those reporting no partners (31% versus 9%). There was however little difference in HIV prevalence between men reporting one versus two or more partners (31% versus 28%). Uncircumcised men had a 26 percent HIV prevalence rate compared to 16 percent among circumcised men, although this can be explained in part by the preponderance of circumcised men being younger (i.e. less cumulative exposure to HIV risk).

HIV Testing History, Awareness of Serostatus and ART Uptake
Overall, 71% of adults in Swaziland reported having received HIV testing services in the past (Table 4). More women (84%) than men (55%) reported prior HIV testing, regardless of current serostatus. Among all HIV-infected adults, 62% were already aware of their positive serostatus while 38% were unaware, either because they had not tested previously (17%) or because they did not receive a positive result in an earlier test (21%).
HIV-infected men were far more likely (50%) than infected women (31%) to be unaware of their positive serostatus, but among those who were aware of their positive status, a larger proportion of men (60%) than women (46%) reported ART use (Figure 3). This prevailing pattern of service utilization results in nearly twice as many HIV infected women (35%) than men (19%) knowing their HIV positive status but not using ART. Age-related differentials in knowledge of HIV serostatus and HIV service utilization are striking. Nearly 4 in 5 (78%) HIV infected men under age 25 were not aware of their serostatus, compared to about one-third (38%) of infected men age 45+ years. Comparable figures for women were 46% and 23%, respectively. Of note, knowledge of HIV serostatus and ART use among the HIV-infected did not vary substantially between urban and rural areas in Swaziland (data not shown).

Discussion
In this cross-sectional survey of a household-based, nationally representative sample of adults (age 18-49) in Swaziland, HIV prevalence was 32%, representing the national adult HIV prevalence in 2011. The substantial inter-survey prevalence declines observed during 2006 to 2011 in the young age cohorts (particularly men) and prevalence rises in the older age groups (particularly women) suggest (1) a reduction in HIV incidence in the past four to five years, resulting in lower prevalence at young ages (fewer recent infections), and (2) improved survival among HIV positive people, resulting in higher prevalence in older age groups. These changing age-related patterns in HIV prevalence are not wholly unexpected. The past two rounds of the antenatal clinicbased HIV surveillance have shown declines in HIV prevalence among young pregnant women (ages 15-24) [8]. That prevalence rates for young men and non-pregnant women are here also displaying consistent downwards trends is encouraging and further support previous interpretation of reductions in new infections.
Another key finding is that since the 2006-7 SDHS, gains have been made in the proportion of persons who have accessed HIV testing and counseling services (HTC) and are aware of their HIV status. In the SDHS 75% of men and 53% of women ages 18-49 reported having never been tested for HIV,  compared to 45% and 16% in men and women, respectively, in SHIMS 2011. Despite the gains, a still substantial proportion of men (50%) and women (31%) with a positive HIV test in SHIMS were unaware of their HIV status at the time of their test. These findings highlight the need for a sustained effort to increase HTC frequency and coverage levels in the general population of Swaziland, with a particular emphasis on increasing access in men and improving linkage of both men and women to now widely available HIV prevention and care services.
Swaziland has shown progress in responding to the growing need for ART, from 2004 when very few Swazis were receiving the benefit of ARVs to end-2011 when 81% of the eligible population (at CD4+ level below 350 cells/mm 3 ) are estimated to have received ART through the national program [9]. A recent national ART program evaluation has underscored the importance of bringing ARVs closer to those in need through decentralization of care services [10]. Efforts to document expected declines in HIV-related mortality have not yet not been implemented. The rise observed here in HIV prevalence at ages above age 30 for women and age 35 for men is supportive evidence of improved survival as a result of ART. That this effect is especially pronounced in women, who represent 65% of adult ART users in the country, further bolsters this interpretation. Increases in HIV incidence in the older population, while a less parsimonious explanation, cannot be wholly discounted.  The pattern of low/late uptake of HTC by men especially is consistent with late entry into care. Data from the National ART program evaluation demonstrate that men initiate ART at a lower CD4+ level (mean = 114) than women (mean = 158) and that the percentage of men who are already WHO stage 4 at initiation is almost double that amongst women (18% versus 10%) [10]. this emphasizes the need to strengthen programs targeting male involvement in HTC and subsequent linkage to care.
While reduced prevalence and indications of falling infection rates in young persons indicate progress in slowing the epidemic, it is apparent that both young men and women (ages <25) are underutilizing HIV services. This has important implications for HIV prevention programs as youth represent a generally receptive target group for adoption of medical male circumcision and efforts to reduce early sexual debut. For youth already infected, timely entry into care services and positive prevention programs would be expected to have a long-lasting positive impact in reducing new infections and mitigating health and social costs. Given the very large proportion of HIV-infected males (78%) and females (46%) under 25 who do not know their status, it is recommended that efforts to increase the coverage and frequency of HIV testing and counseling in this group be intensified.
The relatively high uptake of HTC services among women has resulted in a large pool of women who know they are HIV-positive but have not yet accessed care services. Current rates of linkage to care for Swaziland are not known, although current research in the country has this focus. The estimated retention rate of ART patients in HIV care at 12 months in Swaziland is 82% [10], which is above the median level of 75% found in a multi-country study of ART retention in sub-Saharan Africa [11]. In addition to HIV testing and care, establishing and maintaining one's HIV-negative status through enhanced preventative services is also a principle objective of the Swaziland's public health leadership. According to SHIMS, 61% of Swazi women and 76% of Swazi men age 18-49 are HIV-negative. In a country that continues to experience the highest national HIV prevalence in the world, our challenge remains to support uninfected men and women in accessing high quality prevention services , including voluntary medical male circumcision for men, HIV risk counseling, and widespread access to condoms.