Frequency of HIV-testing and factors associated with multiple lifetime HIV-testing among a rural population of Zambian men

Annual HIV-testing and counselling (HTC) in high prevalence settings is recommended for individuals at continued risk of HIV infection to support early detection of HIV-infection and initiation of anti-retroviral therapy (ART) [1]. Mathematical models suggest that the provision of “high-quality” HTC services to all individuals will increase the HIV-prevention impact of HTC service delivery [2]. In settings where annual HTC is recommended, including Zambia, men’s levels of ever HIV-testing remain lower than is needed to link men testing HIV-positive into care [3‐5]. Encouraging men to increase their lifetime frequency of HIV-testing may prove challenging [6].

Studies exploring risk factors for HIV-testing in sub-Saharan Africa highlight that age [3, 7‐10], employment [4, 11], education [8, 10, 12] and socio-economic position [4, 12], marital status [8, 10], having heard of ART [4], community-level employment and HIV-knowledge [13] are associated with men ever-testing. Whether these factors also encourage men to test more frequently deserves exploration, to determine whether the expansion of HTC services has increased the frequency of HTC among men at risk of HIV-infection. Such evidence would support the development of strategies to reach men in need of annual HIV-testing.

This study describes the frequency of HIV-testing among a rural population of Zambian men and explores the factors associated with frequent HIV-testing. We hypothesized that, relative to never-testers, the factors associated with multiple HIV-testing would be similar to ever-testing for HIV. Among men with a history of ever HIV-testing, we hypothesized that men reporting frequent HIV-testing would differ in socio-demographic characteristics from men reporting one lifetime HIV-test. We also explore whether an offer of home-based HIV-testing in a research setting increases the frequency of testing among men with a history of HIV-testing.

We analyzed data collected for a stepped-wedge cluster randomized trial (CRT): the Better Health Outcomes through Mentoring and Assessment (BHOMA) trial, which aims to strengthen the healthcare system [14]. Details of the intervention are published elsewhere [14, 15]. Briefly, BHOMA was implemented in 42 clusters, defined as a health facility and its catchment area, in three districts in Lusaka Province, Zambia. BHOMA aims to reduce age-adjusted all-cause and under-5 mortality, and is being evaluated through three rounds of household surveys [14]. Increasing HIV-testing is not a primary or secondary objective. However, health facilities were equipped with diagnostics and essential medicines [14], healthcare workers provided with protocols to guide adult visits alongside recruitment of community health workers to increase demand for health services [14]. The majority of BHOMA study sites were rural (n = 34, 81 %). Data for the present analysis were from the mid-line evaluation (February-November, 2013) after intervention implementation in all sites.

In each cluster, squares of 900 m2 were marked within a 3.8 km of the health facility [3, 14]. Computer-generated randomization was used to determine which squares would be visited and the order of visitation. All households in randomly selected squares where the survey was started were visited until 300 households were enumerated in each cluster.

In this large, population-based survey of predominantly rural men, 61 % (95 % CI: 58-64 %) of men were defined as ever-testers. Over half the men with a history of HIV-testing reported more than one lifetime HIV-test. Factors associated with multiple-testing were similar to factors associated with ever-testing [3, 8, 10, 12]. The offer of home-based HIV-testing increased the lifetime frequency of HIV-testing among half of one-time and never-testers.

Limitations of this study are that, as data were cross-sectional, temporal relationships cannot be inferred. Data were self-reported and collected retrospectively. Men may have over-reported HIV-testing and there are likely to be errors in recalling dates of HIV-tests. As a secondary analysis of data collected for an unrelated CRT, the study had limited capacity to explore whether men were HIV-testing annually as data were collected on years since first and most recent test, and number of HIV-tests. Nonetheless, most multiple-testers first tested in 2009 or later, suggesting that recent expansions of HTC services, including PITC, have increased men’s frequency of HIV-testing. In the absence of data on sexual behaviours we had limited ability to explore whether multiple-testers were at increased risk of HIV-infection. However, we found that few men living with HIV reported HIV-testing prior to diagnosis. Although this measure is subject to limitations as multiple-testing was inferred from date of first HIV-test and of HIV-diagnosis, with almost 60 % of HIV-positive men reporting one lifetime test, findings suggest that a high proportion of men continue to be diagnosed on their first HIV-test. Further exploration of multiple-testing behaviours alongside data on sexual behaviours is needed. Some 60 % of married men were linked to their spouse; associations with spousal characteristics may be biased if characteristics of spouses linked differed from those not linked. Generalisability may be limited as the health system strengthening intervention, implemented in all sites at the time of data collection, may have contributed to increased frequency of HIV-testing.

Finally, outcomes were at risk of bias due to non-participation. Studies have shown that Heckman-type selection models can be used to correct HIV-prevalence estimates where refusal to HIV-test is high [18, 20]. We used Heckman-models as we theorised that non-participation, largely due to absence, may be related to HIV-testing behaviours. The models suggested that there was no evidence for unobserved factors associated with participation and HIV-testing outcomes. However, we had limited ability to model selection due to limited individual-level data on non-participants. The selection variables were weak predictors of participation and may not be valid exclusion restrictions [21], as survey timing within clusters was not randomly determined. Aspects of survey conduct may independently affect outcomes [18]; hence our estimates of correlation (rho) between outcome and participation had little precision.

Despite limitations, this study includes a large population of rural Zambian men whose multiple-testing behaviours have been understudied to date. The study provides important insights into the contribution of expanded HIV-testing service delivery to increasing men’s lifetime frequency of HIV-testing.

To our knowledge, there are relatively few population-based surveys exploring the factors associated with multiple-testing. In a 2007 population-based survey conducted in communities in Soweto, South Africa, 50 % of male ever-testers reported more than one lifetime test [4]. Multiple-testing was higher among individuals who had heard of ART [4]. In our study, multiple-testing was higher in clusters where ART was available at the health facility suggesting that expanded ART availability contributes not only to ever-testing [22], but to increased frequency of HIV-testing. In South and Central Province, Zambia (2010/11), 36 % of men ever-tested among whom 50 % reported >1 lifetime HIV-test [23]. In a 2012 nationally representative survey, 63 % of Kenyan males aged 15–64 years ever-tested with a median of 3 tests (IQR: 2–4) per person [10].

By the time of this study, HIV-testing services had been expanded across Zambia, couples HTC was recommended in ANC [24] and there was increased service promotion. Men whose spouse ever-tested were more likely to report multiple-tests. Similar to other settings, these findings suggest that HTC in ANC has provided men with access to HTC and may provide frequent access to HTC [12, 25]. Yet, few men attend ANC [25]. Considering the risk of HIV transmission among sero-discordant cohabiting/married couples, there remains a need to strengthen the delivery of HTC services to men through ANC [26‐28].

Similar to a survey in South Africa, multiple-testers in this study were more likely to have complete secondary/higher education [4]. Employed men in this study were more likely to report multiple HIV-tests unlike in South Africa [4]. Formal employment may provide access to HTC services through the workplace thereby removing opportunity and financial costs of accessing facility-based HTC [29]. Alternatively, employed men may be encouraged by their employer or motivated by their role as providers to access health services [30]. Men of lower socioeconomic markers may face unique barriers to accessing HTC services that influence their frequency of HIV-testing. Lower health literacy likely contributes to lower levels of multiple-testing among men with less education. Other contributing factors, such as ability to access available services, stigma associated with HIV-testing within social networks or as experienced from healthcare workers, may also influence men’s frequency of HIV-testing [31]. Understanding why socioeconomic factors continue to influence men’s HIV-testing behaviors in the context of expanded service availability, the need for regular HIV-testing by socioeconomic factors and how to encourage men with lower levels of education or no formal employment to regularly test for HIV needs exploration.

Evidence suggests that men continue to access care at later stages of HIV-infection [32]. Regular-testing facilitates earlier diagnosis and opportunities to provide risk reduction counselling to HIV-negative individuals at higher risk of infection. In a facility-based cohort in South Africa, repeat-testers were less likely to be HIV-infected relative to first-time testers [33]. . In Uganda, South Africa and Zimbabwe, studies found that individuals at lower risk of HIV are more likely to ever- or repeat-test [4, 12, 34]. Conversely, in serological surveys in Tanzania, high-risk individuals were more likely to repeatedly accept VCT [35]. In this study, 40 % of ever-testers reported one-lifetime HIV-test and few men living with HIV tested before their diagnoses. With investment in delivering community-based HTC [36], there is a need to monitor whether those in greatest need of annual HIV-testing are accessing services and the effects of frequent HIV-testing on sexual behaviors [37]. Traditional “know your status” messaging may require reframing to emphasize the importance of annual HIV-testing if at ongoing risk of HIV-infection.

Home-based HIV-testing increased the lifetime frequency of HIV-testing among men in this study. As in other studies, there was little evidence that acceptance differed by markers of SEP [38, 39]. The relatively high refusal in our study relative to others [3, 40] likely reflects service delivery in the context of research, where the priority was data collection, rather than the acceptability of a home-based HTC programme [3]. In this study, multiple-testing was lower, but acceptance of home-based HIV-testing higher, in communities with higher HIV-prevention knowledge. These findings contribute to suggestions that poor accessibility influences men’s uptake of HTC services [38, 41]. Home-based HTC remains an important strategy to increase the frequency of HIV-testing among rural Zambian men with less access to services [3, 39]. However, with most men not home during household visits, a cost-effective strategy for offering regular home-based HIV-testing in rural settings requires exploration [40].

Effective strategies to reach men with HTC services are available [28], and levels of ever-testing increased among this population of men [3]. However, only 35 % of all men reported multiple HIV-tests and few men living with HIV reported HIV-testing before being diagnosed. More effective implementation and delivery of available HTC services is required to reach men in need of frequent HTC [42]. Novel alternatives to encourage never-testers to access existing HTC services should be explored [28]. These strategies could include self-testing and incentivised testing, shown to be acceptable and feasible among men [43‐45]. Additional research to investigate models for delivery, yield of these strategies and whether they are effective at increasing HIV-testing among HIV-negative men at high risk of infection is required [46, 47].