Objectives Early diagnosis and treatment of HIV infection is critical to improving clinical outcomes for HIV-infected individuals. We sought to characterise the HIV care continuum and identify correlates of being unaware of one's HIV infection among men who have sex with men (MSM) in Moscow, Russia.
Methods Participants (N=1376) were recruited via respondent-driven sampling and completed a sociobehavioural survey and HIV testing from 2010 to 2013. Sample and population estimates were calculated for key steps along the HIV care continuum for HIV-infected MSM and logistic regression methods were used to examine correlates of being unaware of one's HIV infection.
Results 15.6% (184/1177; population estimate: 11.6%; 95% CI 8.5% to 14.7%) of participants were HIV infected. Of these, only 23.4% (43/184; population estimate: 13.2; 95% CI 11.0 to 15.4) were previously aware of their infection, 8.7% (16/184 population estimate: 4.7; 95% CI 1.0 to 8.5) were on antiretroviral therapy (ART), and 4.4% (8/164; population estimate: 3.0; 95% CI 0.3 to 5.6) reported an undetectable viral load. Bisexual identity (reference: homosexual; adjusted odds ratio (AOR): 3.69; 95% CI 1.19 to 11.43), having ≥5 sexual partners in the last 6 months (reference: ≤1; AOR: 4.23; 95% CI 1.17 to 15.28), and employer HIV testing requirements (reference: no; AOR: 15.43; 95% CI 1.62 to 147.01) were associated with being unaware of one's HIV infection. HIV testing in a specialised facility (reference: private; AOR: 0.06; 95% CI 0.01 to 0.53) and testing ≥2 times in the last 12 months (reference: none; AOR: 0.17; 95% CI 0.04 to 0.73) were inversely associated with being unaware of HIV infection.
Conclusions There is a steep gradient along the HIV care continuum for Moscow-based MSM beginning with low awareness of HIV infection. Efforts that improve access to acceptable HIV testing strategies, such as alternative testing facilities, and linkage to care are needed for key populations.
- ANTIRETROVIRAL THERAPY
- BEHAVIOURAL SCIENCE
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The HIV care continuum provides an excellent heuristic to guide researchers and practitioners in implementing strategies and developing new methods to treat and prevent HIV.1 For those living with HIV infection, the framework focuses on measurements of the proportion that are diagnosed, enter and are retained in care, initiate antiretroviral therapy, and reach virological suppression as a means to assess where dropouts occur and inform response.2 Such monitoring and response has important implications for treatment and improvement of morbidity and mortality of those living with HIV, but also supports secondary prevention of onward transmission.1 ,3
As one of only nine countries globally in which the burden of HIV is increasing, the Russian Federation plays an important role in global HIV epidemiology and is estimated to contribute 69% of the global number of people living with HIV.4 New HIV infections are primarily concentrated among key populations at risk for HIV infection, including people who inject drugs, men who have sex with men (MSM), and sex workers, representing more than 85% of new infections.5 ,6 There has been a major emphasis on HIV testing in the Russian Federation with over 27.8 million tests conducted among Russian citizens and 1.9 million tests reported among foreign nationals in 2014.6 HIV testing is nationally provided by Federal AIDS Centres, though it can also be accessed at a cost through private facilities or for free through other specialised facilities or programmes, such as non-governmental outreach programmes, needle and syringe programmes (NSPs), and in prisons and jails. All confirmatory testing, CD4 counts and viral load tests are publicly available to residents and conducted by the Federal AIDS Centre; however, it is not known whether HIV testing is reaching those at highest risk, and whether testing leads to knowledge of positive infection status, access to medical care and ultimately to viral suppression.
In Russia, however, research among gay, bisexual and other MSM has been relatively limited. The few studies that have consisted of samples recruited from gay-identified venues or snowball methods, limiting generalisability.4 ,7–10 Though the Federal AIDS Centres collect data on modes of acquisition among new infections, it is unclear the extent to which MSM and other key populations access HIV services or report their risk behaviours during confirmatory testing. This study used the care continuum perspective to help understand the current status of HIV testing and medical care among MSM in Moscow, Russia and identify impediments to further engagement in care as a viable strategy to address the HIV epidemic among MSM in Russia.
The analysis presented here is derived from a large NIH-funded, cross-sectional study that was conducted in Moscow, Russia.11–13 The primary objectives of that parent study sought to characterise the HIV epidemic among gay, bisexual, and other MSM living in Moscow and compare the use of respondent-driven sampling (RDS) to internet-based sampling (IBS) for recruitment of MSM into HIV testing interventions. This analysis focuses on those MSM who were recruited via RDS and, subsequently, those determined to be living with HIV.
Population and setting
Eligibility requirements for participation included: presented a valid recruitment coupon, assigned male at birth, aged ≥18 years, fluent in Russian, were residing or working in the Moscow metropolitan area, reported anal sex with another man in the last 12 months, no prior participation in this study and provided informed verbal consent to participate. Study activities were conducted in private rooms of a gay-friendly, non-governmental clinic that is centrally located in Moscow. Recruitment and interviews were implemented by a Moscow-based non-governmental HIV prevention organisation.
This analysis focuses on participants recruited by RDS, given the small sample that was produced through IBS recruitment strategies (data not shown). RDS was implemented from late October 2010 to April 2013 and study methods have been previously described.13 RDS recruitment continued in successive waves until the desired sample size of 1370 was reached.
Survey and measures
Survey measures included sociodemographic and behavioural characteristics; sexual identity and disclosure; substance use; depression symptoms; sexual relationships and practices; and HIV prevention and care. All participants were asked personal network size questions traditionally used for population estimates that account for RDS recruitment.14 ,15
Information on history of and where HIV testing (lifetime and last 12 months) was obtained was collected, with options of public (Federal AIDS Centres), private clinic or specialised facility, which included outreach, NSPs, drug treatment and/or jails/prisons. All steps of the HIV care continuum were measured by self-report. With few exceptions, the continuum measures were consistent with other literature and included: awareness of HIV infection; linkage to care; current ART use; and achievement of viral suppression.16 Awareness of one's HIV infection was defined as self-report of being previously tested, diagnosed with HIV infection and having a positive result during study HIV testing. Conversely, participants were determined to be unaware of their HIV infection if they reported that the result of their last test was negative or if they report never being tested for HIV infection, but had a positive result according to the study HIV testing algorithm. Specific data on linkage to care, which is often defined as attendance at a medication-prescribing facility, was not collected; however, because CD4 testing by the Federal AIDS Centre is required for the first step of care, we used self-report of ever having one's CD4 cell count measured as proxy for linkage to care. No data on retention in care was collected. Viral load was measured by a binary item, which asked if the participants knew their last viral load and, if so, whether it was detectable or undetectable.
HIV testing procedures have been previously described.13 Following completion of the survey, participants who had provided separate consent to HIV testing proceeded to biological testing using OraQuick Rapid HIV 1/2 test (OraSure Technologies, Bethlehem, Pennsylvania, USA). Additional blood samples from those with positive rapid results were sent for confirmatory testing by western blot at the local reference laboratory (Lages Laboratory, Moscow).
A total of 1376 MSM were recruited into the study via RDS, reaching up to 31 waves of recruitment. Of these, 1177 consented to HIV testing and 169 (14.4%) participants were identified with HIV infection through rapid and confirmatory HIV testing. An additional 15 who had a positive rapid HIV test, but reported a previous diagnosis of HIV infection and declined confirmatory testing were included in the sample as being HIV infected, yielding a total of 184 (15.6%) with a positive HIV status included in the analysis.
Descriptive statistics of the HIV care continuum and HIV testing history among HIV infected MSM were calculated. Data collected via RDS recruitment are often weighted during statistical analysis to provide population prevalence estimates. Population estimates for the care continuum were calculated using the RDS-II estimator (Volz-Heckathorn) and bootstrapping with 1000 iterations to produce 95% CIs.17 Crude sample proportions and weighted RDS population prevalence estimates are provided.
Given the large decline in the care continuum with awareness of infection, we focused on identifying correlates of undiagnosed infection to identify factors that may aid in understanding why the MSM are undiagnosed, for considerations in how the national or non-governmental organisation (NGO) AIDS response may address these gaps. χ2 tests were used to evaluate statistical significance in bivariate analysis of sample estimates. Variables that were significantly or marginally associated with being unaware of one's HIV infection (p<0.10) or considered a priori to be a potential confounder (ie, age)7 were included in the final multivariable model. Variance inflation tests were conducted to identify collinearity in the model and goodness of fit tests were used to test final model fit. For the multivariable model two sensitivity analyses were conducted. First, the multivariable model was recalculated to examine any differences in regression estimates by inclusion of participants who only had a study confirmed HIV status (N=169). Second, population multivariable analysis was also conducted using the RDS-II estimator. RDS weights, which are produced based on individual, self-reported network size, were included in the final weighted unadjusted and adjusted analyses.17 Statistical analyses were conducted using Stata V.13.0 (Stata Corporation, College Station, USA) and RDS Analyst V.0.1 for R (Los Angeles, USA).18
Table 1 provides the demographic characteristics of study participants and the RDS weighted estimates. Among the sample, 15.6% were currently living with an HIV infection (184/1177; population estimate: 11.6%; 95% CI 8.5% to 14.7%). Among participants who were HIV infected, 86.9% reported ever being tested for HIV and 69.0% had been tested within the last year (population estimate: 78.0; 95% CI 67.1 to 88.8). Among those who were HIV infected, 23.4% reported being previously diagnosed and aware of their HIV infection (population estimate: 13.2; 95% CI 11.0 to 15.4; 31.2% among those ever tested;), 16.9% reported being linked to care (population estimate: 9.0; 95% CI 0.0 to 21.9), 8.7% were currently on ART (population estimate: 4.7; 95% CI 1.0 to 8.5; 48.4% among those ever linked to care) and 4.4% reported having an undetectable viral load (population estimate: 3.0; 95% CI 0.3 to 5.6; 41.7% among those on ART). Eight per cent of those living with HIV (53.9% of those with CD4 levels measured) reported their last CD4 count to be ≥500 cells/mm3. Among those participants who were previously aware of their HIV infection, 73.8% reported ever being linked to care, 38.1% were currently on antiretroviral therapy, and 22.2% reported an undetectable viral load. Figure 1 and online supplementary table S1 display the sample and population estimates of the HIV care continuum steps for the total group of MSM living with HIV infection.
Of the 184 individuals living with HIV, 76.6% were previously unaware of their HIV infection (population estimate: 86.4%; 95% CI 80.4% to 92.5%). Among those previously unaware, 92.2% (130/141) returned to receive their HIV test results through this study and were linked to services provided by the clinic. Table 2 presents the bivariate analysis comparing characteristics of MSM who were previously aware of their HIV infection to those previously unaware. Significant differences between the two groups were related to characteristics including sexual identity and numbers of recent partnerships, alcohol use, and HIV testing patterns and motivations. Seventeen per cent of those previously unaware had not received the results of their last HIV test, higher than those who were previously aware of their infection (16.5% vs 0.0%; p<0.01). For MSM who were tested for HIV in their lifetime, the median time since last HIV test was 0.29 years (IQR: 0.1–0.7) among those previously aware of their HIV infection, compared with 0.92 years (IQR: 0.4–1.7) among those previously unaware.
Table 3 presents the unadjusted and adjusted logistic regression analyses of being unaware of one's HIV infection. Increased odds of being unaware of one's infection were associated with bisexual identity (ref: homosexual identity; AOR: 3.69; 95% CI 1.19 to 11.43; p<0.02), increased numbers of sex partners in the last 6 months (≥5 vs ≤1 sex partner; AOR: 4.23; 95% CI 1.17 to 15.28; p=0.03) and HIV testing requirements for employment (ref: not required; AOR: 15.43; 95% CI 1.62 to 147.01; p=0.02). MSM who reported being tested ≥2 times within the last 12 months were less likely to be unaware of their HIV infection (ref: not tested in last 12 months; AOR: 0.17; 95% CI 0.04 to 0.73; p=0.02) as were those who reported being tested in a setting specifically related to HIV risk behaviours (ref: public facility; AOR: 0.06; 95% CI 0.01 to 0.53; p=0.01). The sensitivity analysis of the multivariable model that assessed the inclusion of participants who only had a study confirmed HIV status (N=169) found no substantial differences in estimates (data not shown).
Online supplementary table S2 presents the corresponding unadjusted and adjusted population estimates, which were relatively similar to sample estimates, with few exceptions. The magnitude of association for bisexual identity was slightly lower than the sample estimate (ref: homosexual; AOR: 2.96; 95% CI 0.88 to 9.92; p=0.08). Employment requirements for HIV testing had a higher magnitude of association than the sample estimate, with wide CIs (ref: no; population estimate AOR: 22.04; 95% CI 2.11 to 229.92; p=0.01).
This study highlights critical losses in the HIV care continuum among these men living in Moscow city.4 Notable declines were observed in regard to awareness of one's HIV infection and subsequently losses in treatment and viral load suppression. Ultimately, less than 5% of MSM living with HIV in this sample had achieved virological suppression.
While no data exist on engagement of MSM in the HIV care continuum in the Russian Federation, nor in the wider Eastern Europe Central Asia (EECA) region, the lack of ART among this sample may be foreshadowed by national estimates that highlight inadequate treatment coverage of the general population living with HIV as of 2013.4 Prior estimates suggest that only 19% of the 668 032 HIV-infected Russian residents in the Federal AIDS Centre database were reported to have achieved viral suppression.19 While such findings highlight existing barriers along the HIV care continuum in the Russian Federation, MSM and other key populations may bear the brunt of these inequalities, particularly in light of emergent social stigma.10
Awareness of one's HIV infection is the critical barrier along the HIV care continuum among HIV-infected MSM. Despite relatively high levels of HIV counselling and testing, less than one in four HIV infected MSM in the sample were previously aware of their HIV infection (13.6% of the HIV infected MSM population), clearly inhibiting access to subsequent points along the HIV care continuum.
With respect to individual characteristics, bisexual identity and increased numbers of partners were independently associated with lack of awareness of HIV infection. Those reporting bisexual identity may have less knowledge of HIV risk related to unprotected anal intercourse, may not typically access HIV prevention information targeted to homosexually identified men, or may experience greater self-stigma and isolation that prohibits access to and use of HIV prevention programmes. Laws banning the ‘propaganda of homosexuality’ may impede provision of information on HIV risk and may increase concerns related to privacy and confidentiality.4 ,10 Having more sex partners in the last year was also associated with being unaware of one's HIV infection. Despite high levels of recent HIV testing, high-risk sexual behaviours may lead to new acquisition after testing.
HIV testing characteristics provide additional insight into issues of lack of awareness among MSM living with HIV. Participants who had been tested for HIV at least twice within the last year were significantly more likely to be aware of their infection. This lends support to CDC guidance on HIV testing and care for MSM, particularly recommendations that high-risk individuals test more than once a year.20 Improvements in awareness of HIV status were also associated with use of specialised testing programmes related to HIV risk behaviours, such as outreach and NSPs, and highlight the importance of targeted, confidential programmes for key populations. These programmes are often free of charge and are provided to key populations, may provide risk reduction counselling that is more specific to their individual risk behaviours, and may be perceived to have lower stigma and discrimination than public or even private facilities. Evidence that a substantial proportion of MSM reported use of private facilities for HIV testing (about 20%), despite generally low income levels, suggests reservations in the use of free, public facilities for HIV testing. Finally, employer HIV testing requirements were associated with being unaware of HIV infection. This may be related to practices of purchasing negative HIV test results, without actual HIV testing, when required for employment or other legal issues, as has been noted with testing requirements for migration.12 These findings also bring up questions on the quality and confidentiality of public HIV counselling and testing programmes.21
Research findings should be viewed in light of several limitations. Estimates of the HIV care continuum were based on self-report and thus may be biased by recall of CD4 levels and viral load, as these levels were not biologically confirmed during the study. Clinical measures related to linkage, retention and time from diagnosis to linkage, were not collected given resource constraints and because this was not the primary purpose of the study. Data were collected on current ART use; thus, we did not know the proportion of MSM living with HIV who may have initiated and stopped treatment or experienced treatment interruptions. RDS-weighted estimates provide population-based estimates; however, there is an ongoing debate as to which estimators are the most accurate for use and estimates should therefore be reviewed with caution.22 ,23 This is a cross-sectional study which limits temporal analysis and determination of the directionality of association; we do not know if these characteristics and behaviours represent predictors of testing and awareness or were postdiagnosis behavioural changes. Finally, the study sample is comprised of MSM recruited from Moscow city and the number of MSM living with HIV is relatively small, limiting our generalisability to MSM living in the wider Russian Federation and EECA. To our knowledge, however, these data represent the first HIV care continuum estimates for MSM in the region.
Engagement and retention in the HIV care continuum and, ultimately, reaching viral suppression is a challenge for MSM living with HIV in the Russian Federation. The recent loss of the Global Fund and lack of acknowledgement of key populations by Federal AIDS programmes mean that alternative sources of funding to support these important prevention and testing programmes are needed.24 This is further exacerbated by limitations on provision of information related to same-sex practices associated with new laws prohibiting the ‘propaganda of homosexuality’, which create ‘new obstacles and disincentives for gay men or other MSM in accessing HIV programmes and services’.4 Gaps identified along the HIV care continuum and benefits of testing characteristics highlight opportunities in which HIV testing interventions can be introduced (or improved) to further engage MSM living with HIV. HIV testing innovations, such as HIV self-testing and CD4 point-of-care tests have demonstrated success in other challenging settings and may provide improved and alternative means for increasing awareness of one's HIV infection and providing engagement in care in a stigmatised setting.25 ,26
Little data exist on engagement in the HIV care continuum among men who have sex with men (MSM), in Moscow, Russia.
There is a steep gradient in the HIV care continuum for MSM living with HIV: 76% of the population are unaware of their infection, inhibiting further access to care.
Lack of awareness of infection was associated with sexual identity and behaviours, as well as HIV testing patterns.
Ensuring access to confidential HIV testing is important to enabling early identification and engagement in care for MSM who are living with HIV in the Russian Federation.
HIV testing innovations, such as HIV self-testing and CD4 point of care, may provide alternative means for MSM to understand their infection status and engage in care.
The authors thank SANAM clinic and Tatiana Bondarenko for insight, support, and use of the SANAM clinic for conduct of qualitative research and the Be Safe study. The authors appreciate the efforts of Irina Deobald and Konstantin Dyakonov in the formative phases of this project. The authors thank the participants who contributed their time and personal experiences to this study
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
- Data supplement 1 - Online supplement
Correction notice This article has been corrected since it was published Online First. New author affiliations have been included.
Handling editor Jackie A Cassell
Twitter Follow Andrea Wirtz at @12AndreaW
Contributors CB, ALW, CEZ, NG, VM, AP and CL collaborated in the design and oversight of the overall study. PD and IK collected data. ALW conducted data analysis. SHM and CEZ reviewed and provided input to the statistical analysis. ALW wrote the initial drafts of this manuscript. All authors had full access to the data, reviewed and edited the manuscript, and take responsibility for its integrity as well as the accuracy of the analysis.
Funding Funding for this research came from the National Institute of Mental Health (NIMH R01 MH085574-01A2) ‘High Risk Men: Identity, Health Risks, HIV and Stigma’ funded from 2009–2014. This research has been facilitated by the infrastructure and resources provided by the Johns Hopkins University Center for AIDS Research, an NIH funded programme (P30AI094189), which is supported by the following NIH Co-Funding. and Participating Institutes and Centers: NIAID, NCI, NICHD, NHLBI, NIDA, NIMH, NIA, FIC, NIGMS, NIDDK and OAR. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.
Competing interests None declared.
Ethics approval Ethics Committee of the State Medical University, IP Pavlov, St. Petersburg, Russia, and Johns Hopkins Bloomberg School of Public Health Institutional Review Board, Baltimore, Maryland, USA.
Provenance and peer review Not commissioned; externally peer reviewed.