AIDS Behav DOI 10.1007/s10461-014-0780-5
ORIGINAL PAPER
Evolving Understanding of the Epidemiology of HIV and Prevention Needs among Men Who Have Sex with Men in Ulaanbaatar, Mongolia Iliza Azyei • Bulbul Aumakhan • Baigalmaa Jantsansengee • Sergelen Munkhbaatar • Erdenetuya Gombo • Unenchimeg Puntsag • Davaalkham Jagdagsuren • Sosthenes Ketende • Susanne Stromdahl • Stefan Baral • Tugsdelger Sovd • Oyunbileg Amindavaa
Ó Springer Science+Business Media New York 2014
Abstract This study describes HIV and syphilis biobehavioral survey conducted among 200 men who have sex with men (MSM) recruited via respondent-driven sampling (RDS) between January 4 and February 1, 2012 in Ulaanbaatar, Mongolia. Participants were administered a structured questionnaire and data were analyzed with RDSnetwork program in STATA. Of 196 participants who agreed to be tested for HIV and syphilis, 21 (10.7 %; weighted 7.5; 95 % CI: 4.9, 11.4) and 8 (4.1 %; weighted 3.4; 95 % CI: 1.7, 6.7) were positive for HIV and syphilis,
Iliza Azyei and Bulbul Aumakhan contributed equally to the manuscript. I. Azyei S. Munkhbaatar O. Amindavaa Global Fund Supported Projects on HIV/AIDS and TB, Ministry of Health, Ulaanbaatar, Mongolia B. Aumakhan (&) E. Gombo U. Puntsag D. Jagdagsuren HIV/AIDS and STI Surveillance and Research Department, National Center for Communicable Diseases, Ministry of Health, Ulaanbaatar, Mongolia e-mail: [email protected] B. Jantsansengee Mongolian Field Epidemiology Training Program, Ulaanbaatar, Mongolia E. Gombo ’’Together Center’’ NGO, Bayanzurkh, Mongolia S. Ketende S. Stromdahl S. Baral Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA T. Sovd Monitoring and Evaluation, and Internal Auditing Department, Ministry of Health, Ulaanbaatar, Mongolia
respectively. Exposure to HIV prevention programs in the last 12 months was reported by 51.8 % (weighted 33.6; 95 % CI: 27.6, 40.1) of participants. This study found high HIV prevalence and limited uptake of HIV prevention services among MSM in Mongolia. Given the concentrated HIV epidemic among MSM in Mongolia, HIV prevention, treatment and care services should focus on MSM as the population group most affected by HIV.
Resumen Este estudio reporta una encuesta de VIH y sı´filis conducido en 200 hombres que tienen sexo con hombres (HSH) los cuales fueron enrolados a trave´s un muestreo guiado por los participantes entre enero 4 y febrero 1 del 2012 en Ulaanbaatar, Mongolia. Los participantes recibieron un cuestionario estructurado y la informacio´n se analizo con el programa Stata. De los 196 participantes quienes estuvieron de acuerdo en ser testeados para el VIH y sı´filis, 21 (10.7 %; tasa ajustada 7.5; 95 % IC: 4.9, 11.4) and 8 (4.1 %; tasa ajustada 3.4; 95 % IC: 1.7, 6.7) fueron positivos para VIH y sı´filis, respectivamente. Exposicio´n a los programas de prevencio´n del VIH en los u´ltimos 12 meses fue reportado por 51.8 % (tasa ajustada 33.6; 95 % IC: 27.6, 40.1) de los participantes. Este estudio ha documentado que HSH tienen una alta prevalencia de VIH y limitado servicios de prevencio´n para VIH. Dada la concentrada epidemia del VIH en HSH en Mongolia, la prevencio´n y tratamiento del VIH ası´ como servicios de asistenciales deberı´an focalizarse en HSH debido a que este grupo es la ma´s afectada por la epidemia del VIH.
Keywords Mongolia HIV Respondent-driven sampling Men who have sex with men Asia
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Introduction Mongolia is a landlocked country situated in Northern Central Asia bordering Russia to the north and China to the south. It is the 19th largest country in the world in territory and most sparsely populated with a population of about 2.8 million people [1]. Nearly half of the population resides in the capital city Ulaanbaatar. With only 150 cases reported as of December 31, 2013, Mongolia remains a country with a very low HIV prevalence (\0.1 %) among the general population (unpublished data, National Center for Communicable Diseases, Ulaanbaatar, Mongolia). However, there are signs that HIV spread may be accelerating in the country, particularly among men who have sex with men (MSM). Over 80 % (n = 121) of all cumulative cases are men among whom MSM constitute the overwhelming majority (n = 99, 82 %). Except the first 5 cases, all (n = 145/150, 97 %) were reported since 2005. MSM in Mongolia are largely hidden due to low public awareness and widespread prejudice about MSM and issues related to sexual minorities [2, 3]. Stigma and discrimination are common, and given the small population, disclosure of sexual orientation is major concern for MSM. As has been documented in other settings, social and family pressures often force MSM to marry and lead ‘‘double lives’’ with both male and female sexual partners [4]. The stigma and discrimination faced by MSM also pose significant barriers to health service access, employment and social acceptance. In terms of legal environment, male-to-male sex has been legal since 2002, but there are no laws protecting the rights of sexual minorities [5, 6]. Civil society is a relatively new concept in Mongolia with the first MSM community based organization (CBO) formed in 2003. Currently there are three CBOs serving MSM, all based in Ulaanbaatar, providing outreach, peer education, counseling, condom distribution and referrals to HIV and STI testing and treatment services. However, the outreach, community engagement and empowerment capacity of these organizations remain limited. Given the context, monitoring HIV trends among MSM in Mongolia has been challenging due to difficulties of recruiting MSM and limited data on MSM population size and distribution. Bi-annual second generation surveillance (SGS) surveys have been employed since 2005 to study HIV prevalence and trends among MSM. Previous SGS surveys used convenience sampling methods and accounted only for new HIV infections. The SGS survey conducted in 2007 found 1 new HIV infection among 118 MSM (0.8 %), and the survey in 2009 found 3 new HIV infections among 167 MSM (1.8 %) recruited in the capital city of Ulaanbaatar [7]. A cross-sectional study conducted in 2011 by UNAIDS Mongolia in collaboration with the Johns Hopkins School of Public Health, USA, found an
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adjusted self-reported HIV prevalence of 6.3 % among MSM in Ulaanbaatar [8]. The latter study used respondentdriven sampling (RDS) for the first time in Mongolia and successfully recruited over 300 MSM, but did not collect biological samples to validate the self-reported HIV status. Here, we describe a bio-behavioral survey of 200 MSM recruited via RDS in Ulaanbaatar between January 4 and February 1, 2012. The objective of this study was to determine the prevalence of HIV and syphilis among MSM in Ulaanbaatar and factors associated with HIV positive status.
Methods The survey received approval from the Scientific Committee of the National Center for Communicable Disease (NCCD), Ulaanbaatar, Mongolia and the Ethical Committee of the Ministry of Health. Written consent was obtained from all participants prior to enrollment into the survey. Sampling Strategy, Population and Questionnaire RDS method was chosen to recruit participants because it was proven to be successful in recruiting MSM, a highly hidden and hard to reach population group in Mongolia [8]. In addition, RDS is an approximation of probability-based sampling methods and allows characterization of unbiased estimates of outcomes of interest. When certain theoretical assumptions are met, RDS produces weighted estimates that adjust for the difference between the composition of the survey sample and the likely composition of MSM population overall. Details of this method have been described elsewhere [9]. To start recruitment we selected 5 seeds through referral from three local non-governmental organizations (NGOs) working with the MSM population. Seeds were selected based on their varying socio-demographic characteristics (e.g. age, education), level of interest in participation, range of social networks and likelihood of referring three participants. Each participant was given 3 coupons to recruit additional participants until the target sample size was reached. Seeds and participants had to meet the following criteria to be eligible for participation in the survey: (1) age between 15 and 49 years old; (2) have had sexual intercourse (anal or oral) in the last 12 months with another man; (3) able to provide adequate informed consent; and (4) have not been interviewed for this study in the past 3 months. Participants received dual incentives as per RDS method [9]. The incentive amount was equivalent to the local cost of round trip transportation and an average meal. A structured questionnaire eliciting information on demographics, sexual behavior with male and female partners, drug and alcohol use history, sexually transmitted
AIDS Behav
infections (STI) and treatment history, knowledge of HIVtransmission related issues and HIV voluntary counseling and testing (VCT) experiences was administered to participants. The questionnaire was developed and pre-tested in previous rounds of SGS surveys, but included new questions related to social networking as required by RDS method. The survey was administered face-to-face in Mongolian language by trained interviewers and lasted approximately 30 min. A unique identifier was created for each participant as an 8-digit code consisting of the first two letters of father’s first name (Mongolians go by single name and father’s first name is used as a last name), the first two letters of mother’s first name, two-digit year and month of birth. Each participant was also asked if he wanted a reminder call to receive test results, and if the participant agreed, his phone number was recorded in the laboratory journal. Information used for this reminder phone call was not recorded on a specific survey or test results to maintain anonymity. The unique codes and phone numbers were subsequently used to verify HIV positive participants against the cases registered in the national HIV case database. Sample Size The sample size was calculated using the module for determining a population proportion in OpenEpi software [10]. Assuming 2 % of men in Ulaanbaatar age between 15 and 49 years are MSM, 5.4 % syphilis prevalence observed during SGS 2009 as anticipated frequency of outcome factor, design effect of 2 [11] and confidence limits of ±5 %, the target sample size was estimated to be 156. Allowing 80 % response rate for blood collection among behavioral survey respondents, the sample size was 187 participants. In the end, the survey enrolled 200 MSM. Laboratory Procedures Blood samples were kept at a room temperature for no more than 4 h before being delivered to NCCD laboratory for HIV and syphilis testing. Blood samples were tested for HIV using ‘‘SD HIV 1/2 Rapid 3.0’’ (Standard Diagnostics Inc, Korea) rapid tests. Reactive specimens were confirmed using Enzyme-linked immunosorbent assay (ELISA) and Western blot. Syphilis testing was conducted using Rapid plasma reagin (RPR) and Treponema pallidum haemagglutination assay (TPHA) test kits (New Market Laboratories Ltd. Kentford, Newmarket, CB 8 & PN-UK) according to manufacturer’s instructions. Sample was considered positive for syphilis if both TPHA and RPR tests were reactive with RPR titer C1:2. Quality control was performed in compliance with the internal quality control standards with 10 % of randomly selected negative
and all positive samples retested at NCCD laboratory. All participants received pre- and post-test counseling according to national standards. Participants with laboratory evidence of STI were managed free of charge per national STI diagnosis and treatment guidelines. Data management and Analysis RDS Coupon Manager Software was used to keep track of recruitment process and respondent compensation. The following three questions were used to determine social network size: (1) How many people do you know who have sex with men? (2) Of those MSM without overlapping, how many have you met or talked with over the past 6 months? (3) In the following 3 weeks (coupon’s validity period) how many MSM can you meet with? The third question was used to measure network size for the purpose of RDS weighting. If the response was ‘‘zero’’ or ‘‘don’t know’’ the response value to the second question was used as a network size. Variable specific weights were estimated to obtain weighted prevalence estimates. Weighted estimate adjusts for the difference between the composition of the survey sample and the likely composition of the population from which the sample is drawn and thus, theoretically represents the overall MSM population in Ulaanbaatar. If no weighted estimates were produced due to estimation convergence problems, or when a group recruited exclusively from within their own group, the results were marked as ‘‘not determined’’. Bivariate and multivariate analyses were weighted using HIV as the outcome. Bivariate categorical associations were tested using corrected weighted Pearson Chi square converted into F-statistic for complex survey data [12]. Variables associated with HIV infection at p \ 0.20 were entered into multivariate logistic regression that included condom use, type of sexual intercourse, HIV testing history, participation in HIV prevention programs, drinking history, sex with female and correct answer to all HIV knowledge questions. Socio-demographic variables such as age and marital status were included in logistic regression models regardless of p value to account for potential association of socio-demographic factors with HIV infection. Seeds were excluded from multivariate regression analysis as recommended per RDS-method [9]. We considered p values less than 0.1 as statistically significant. Analyses were conducted using RDS network program [13] in STATA statistical software (STATA/IC Version 12.1, Stata Corporation, College Station, Texas, USA). The RDS network program allows an easy implementation of RDS analysis in STATA. It produced point estimates that were identical to those produced by RDS Analysis Tool
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Fig. 1 Referral networks by HIV status (n = 200). Key: large square seed; red square HIV positive (n = 21); blue square HIV negative (n = 175); black square refused testing (n = 4) (Color figure online)
(RDSAT) software but with slightly differing confidence intervals due to use of different bootstrapping algorithms for obtaining confidence intervals. As in RDSAT, RDS network program in STATA incorporates recruitment network structure and adjusts for homophily and oversampling of people with large networks. The RDS network program for analysis of RDS data in STATA is described in detail elsewhere [13]. The network graph was generated using Netdraw program [14].
(Fig. 1). The longest chain reached eight waves and 68 referrals. In 85 % of cases participants were recruited by sexual partners, friends and MSM acquaintances they know well. The remaining 15 % were recruited by NGO outreach workers, peer educators and other MSM. The homophily values for most variables were around zero indicating mostly random recruitment among participants. However, some degree of homophilous recruitment (degree of homophily *0.4) was observed among men age under 25, men of similar educational attainment and those exposed to HIV prevention programs.
Results Demographic Characteristics Recruitment Characteristics The five seeds selected to start recruitment process were age between 23 and 50 years old, three had college and two completed secondary education. None reported drug use, three had regular partners, one was HIV-infected and one syphilis sero-positive. All seeds were effective recruiters
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Participants had a mean age of 30 (median 29, range: 17–50, Table 1). Over half of participants (62.5 %; weighted 54.4; 95 % CI: 47.2, 61.4) had college and/or university level education. Eight percent (weighted 13.2; 95 % CI: 8.3, 20.4) of participants reported being married and currently living with a spouse.
AIDS Behav Table 1 Crude and RDS-weighted demographic characteristics of MSM, Ulaanbaatar, Mongolia, 2012 Characteristic
Crude% (N)
Wt% (95 % CI)
Age Mean/median (range)
30/29 (17, 50)
Age groups 15–24
35.5 (200)
38.8 (32.3, 46.0)
25–34
36.0 (200)
32.1 (26.2, 38.7)
35–44
23.5 (200)
23.7 (18.2, 30.1)
C45 Education
5.0 (200)
5.4 (2.9, 9.8)
Bcomplete secondary
37.5 (200)
45.6 (38.6, 52.8)
College/university
62.5 (200)
54.4 (47.2, 61.4)
Marital status Married living with spouse
8.0 (200)
13.2 (8.3, 20.4)
Not married, living with male permanent partner
32.0 (200)
24.1 (19.0, 30.0)
Not married, no permanent partner Separated/widowed/divorced
43.0 (200)
41.6 (34.8 , 48.7)
17.0 (200)
21.1 (34.8 , 48.7)
Network size Mean/median (range)
11/4 (1, 200)
Sexual Practices and Risk Behaviors Mean and median age at first sexual experience was 18 (range: 8–36, Table 2). Receptive intercourse was reported as the dominant sexual role by 15.6 % (weighted 14.4; 95 % CI: 10.3, 19.8) of participants. Sexual behavior with male partners shows that less than half (47.5 %; weighted 47.4; 95 % CI: 40.5, 54.4) of participants used condom consistently in the last 12 months while condom use at last sex was 70.2 % (weighted 71.0; 95 % CI: 64.3, 76.9). Sexual contact with females was common and reported roughly by 40 % (36.0 %; weighted 45.8; 95 % CI: 38.7, 53. 0) of participants. Only two participants reported having sex with female sex workers in the last 12 months. Reports of genital discharge and genital ulcers in the last 12 months were infrequent. Alcohol was the most commonly used substance with more than 80 % reporting that they drank at least once per month. Non-injectable illicit drug use was 11.5 % (weighted 6.5; 95 % CI: 4.3, 9.7) and none reported injection drug use in the last 12 months. Types of drugs used were not asked but smoking and sniffing were the most common routes of drug use (data not shown). HIV Knowledge, HIV Testing and Prevention Coverage Over 90 % responded correctly to at least one of the five HIV transmission-related knowledge questions (Table 3).
However, the percentage of those who knew correct answer to all 5 questions was 60.2 % (weighted 58.9; 95 % CI: 51.4, 66.0). About 67 % (66.5 %; weighted 54.6; 95 % CI: 47.2, 61.8) were tested for HIV in the last 12 months of whom 97 % (weighted 97.7; 95 % CI: 93.9, 99.1) received test results. The overall percentage of those both tested and received the results was 64.5 % (weighted 55.3; 95 % CI: 48.0, 62.4). The crude percentage for exposure to HIV prevention activities was 51.8 % but weighted was only 33.6 % (95 % CI: 27.6, 40.1), indicating inadequate reach of HIV prevention programs. When disaggregated by type of HIV prevention program, inadequate coverage rates were observed for participation in VCT (57.8 %; weighted 43.6; 95 % CI: 34.5, 53.3), focus group (48.0 %; weighted 33.2; 95 % CI: 25.2, 42.2), community empowerment activities (34.3 %; weighted 28.8 %; 95 % CI: 21.2, 37.9) and STI diagnostics (22.6 %; weighted 12.3; 95 % CI: 8.1, 18.3). HIV and Syphilis Prevalence and Factors Associated with HIV Positive Status HIV and syphilis testing was performed on 196 MSM (4 refused testing). Twenty one participants (10.7 %; weighted 7.5; 95 % CI: 4.9, 11.4, Table 2) were sero-positive for HIV and 8 (4.1 %; weighted 3.4; 95 % CI: 1.7, 6.7) had reactive tests for syphilis. One person was positive for both HIV and syphilis. Graphical representation of HIV among participants is shown in Fig. 1. All 21 HIV cases were previously known cases. This was determined through an 8-digit unique codes and phone numbers of HIV positive cases and verifying it against the corresponding information on patient files and the data in the national HIV case registry. No new infections were detected. Factors associated with HIV positive status were further explored via bivariate (Table 4) and multivariate (Table 5) analyses. HIV prevention coverage (50.1 vs. 76.2 %, p = 0.024), consistent condom use both in the last 12 months (42.3 vs. 81 %, p = 0.007) and condom use at last sex (68 vs. 86 %, p = 0.091) were all significantly lower among HIV uninfected than among HIV infected MSM. Among HIV uninfected MSM reporting exposure to HIV prevention activities in the last 12 months only half (49.5 %) used VCT services. Twice more HIV infected (28.6 %) than HIV uninfected men (13.8 %) practiced receptive intercourse (p = 0.073). Significantly fewer HIV infected men (14.3 vs. 37.7 %) reported having sex with females in the last 12 months (p = 0.035). Two variables, consistent condom use (OR = 10.42, p \ 0.0001) and responding correctly to all 5 knowledge questions (OR = 8.83, p = 0.021), were statistically significantly associated with HIV infection in the multivariate logistic regression analysis.
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AIDS Behav Table 2 Crude and RDSweighted risk characteristics, and prevalence of HIV and syphilis among MSM, Ulaanbaatar, Mongolia, 2012
Characteristic
Crude% (N)
Wt% (95 % CI)
Age at 1st sex Mean/median (range)
18/18 (8, 36)
Sexual behavior with male partners No. of male partners (last 12 months) Mean/median (range)
3/2 (1, 25)
1
39.7 (199)
2–4
43.2 (199)
50.0 (42.9, 57.2) 38.7 (32.1, 45.7)
C5
17.1 (199)
11.3 (8.0,15.6)
Insertive
44.2 (199)
49.5 (42.5, 56.5)
Receptive
15.6 (199)
14.4 (10.3, 19.8)
Universal
40.2 (199)
36.1 (29.8, 43.0)
Always
47.5 (200)
47.4 (40.5,54.4)
Most of the time Sometimes
26.5 (200) 15.5 (200)
23.1 (17.9,29.2) 17.5 (12.6,23.8)
Dominant sexual role
Frequency of condom use (last 12 months)
Rarely
3.5 (200)
3.5 (1.7,7.2)
Never
7.0 (200)
8.6 (5.1, 13.9)
Condom use at last sex
70.2 (198)
Received payment for sex with male partner
4.0 (200)
71.0 (64.3, 76.9) 2.8 (1.4, 5.5)
Sexual behavior with female partners Sex with female
36.0 (200)
45.8 (38.7 , 53.0)
No. of female partners (last 12 months) Mean/median (range)
2/1 (1,20)
1
63.4 (71)
68.9 (57.4,78.4)
C2
36.6 (71)
31.1 (21.6, 42.6)
Sex with non-regular non-commercial female partner
50.7 (71)
41.4 (30.5,53.2)
Condom use at last sex with non-regular female partner
75% (36)
62.5 (43.0,78.6)
2.9 (70)
Not determined
Sex with commercial female partner Substance use Frequency of alcohol use At least once a week
40.0 (200)
33.7 (27.6 , 40.3)
At least once a month
44.0 (200)
47.6 (40.6, 54.6)
Rarely or never
16.0 (200)
18.7 (13.6, 25.3)
11.5 (200)
6.5 (4.3, 9.7)
Ever used drugs Injected drugs in the past 12 months
0.0 (23)
Not determined
Sexually transmitted infections Had genital discharge
7.5 (199)
5.0 (3.0,8.2)
Had ulcers/sores
3.0 (199)
Not determined
Had treatment
50.0 (26)
36.7 (20.3, 56.9)
10.7 (196)
7.5 (4.9, 11.4)
4.1 (196)
3.4 (1.7, 6.7)
Prevalence of HIV and syphilis HIV seropositive Syphilis seropositive
Discussion A cross-sectional bio-behavioral survey of HIV and syphilis recruited 200 MSM via RDS approach in Ulaanbaatar,
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Mongolia and found a 7.5 % adjusted (crude 10.7 %) prevalence of HIV. This is higher than the 1.8 % prevalence reported in 2009 [7], and it exceeds the 5 % cut-off in a high risk group that defines per UNAIDS criteria a concentrated
AIDS Behav Table 3 HIV knowledge, testing and prevention characteristics of MSM, Ulaanbaatar, Mongolia, 2012 Characteristic
Crude% (N)
Wt% (95 % CI)
Having one and faithful sex partner can reduce transmission risk of HIV infection
92.7 (192)
92.9 (88.3, 95.8)
Using condom properly in all sexual intercourses can prevent HIV infection
95.5 (199)
93.8 (88.6, 96.8)
Healthy looking person can be infected with HIV
95.2 (189)
96.7 (93.8, 98.3)
Mosquito bites do not transmit HIV
72.2 (176)
67.0 (59.3, 73.9)
Handshaking and sharing food with HIV infected person do not transmit HIV
92.9 (196)
93.0 (88.4, 95.8)
Responded correctly to all above questions
60.2 (176)
58.9 (51.4, 66.0)
Tested for HIV
66.5 (200)
54.6 (47.2, 61.8)
If tested, received results back
97.0 (133)
97.7 (93.9, 99.1)
Tested and received test results
64.5 (200)
55.3 (48.0, 62.4)
Participated in HIV prevention
51.8 (199)
33.6 (27.6, 40.1)
Training
78.4 (102)
75.3 (66.2,82.6)
Focus group
34.3 (102)
28.8 (21.2,37.9)
HIV-related knowledge
HIV testing and prevention
Voluntary counseling and testing
57.8 (102)
43.6 (34.5,53.3)
Community empowerment activities
48.0 (102)
33.2 (25.2,42.2)
Received condoms lubricants
65.7 (102)
44.9 (35.4,54.8)
STI diagnostics Know where to get HIV test
22.6 (102)
12.3 (8.1,18.3)
87.0 (200)
80.0 (72.5, 88.5)
HIV epidemic. However, the prevalence found in this survey should not be interpreted directly as a sharp increase in HIV prevalence among MSM in Mongolia. Rather, interpretation should take into consideration several factors. First, the 2009 survey counted only new HIV positive cases and excluded known positive cases, whereas HIV positive status was not an exclusion criterion in this survey. Second, the surveys employed different sampling strategies, RDS in the current survey and convenient sampling in 2009 survey. Third, it was subsequently determined that all 21 HIV positive cases detected in this survey were known infections registered with HIV/AIDS and STI Surveillance and Research Department, NCCD. Finally, the survey only sampled MSM in the capital city, Ulaanbaatar, and thus, it is not representative of HIV prevalence among MSM nationwide. The 7.5 % HIV prevalence, however, is comparable to 6.3 % self-reported HIV prevalence estimate observed in the earlier mentioned survey of MSM in Ulaanbaatar that
was implemented with the support of UNAIDS Mongolia in collaboration with the Johns Hopkins School of Public Health, USA, in 2011 [8]. The main purpose of the latter survey was to establish baseline data on HIV risk status, access to services and human rights contexts among MSM in Mongolia. The finding that all 21 HIV cases were known infections already registered in the national HIV case database at NCCD indicates, that these cases may have come from a single or few networks, or that HIV has not been introduced into other sexual networks. This is supported by the epidemiological risk profile data of cases registered in the national HIV case registry. Specifically, all HIV suspected cases around the country are confirmed with Western Blot at NCCD. Upon confirmation all newly identified cases undergo detailed epidemiologic investigation including contact tracing. Consequently, HIV clinicians and epidemiologists at NCCD have long suspected that many cases among MSM are epidemiologically linked with each other. This was confirmed in a study published in 2011 which reported results of a phylogenetic tree analysis of viral sequences isolated from the sera of 38 (out of 56 total reported by the time of study, May 2009) HIV infected cases [15]. The phylogenetic study identified two clusters of HIV subtype B infections among MSM and determined that there was a rapid expansion of HIV transmission with the same ancestor virus from these clusters starting around early 2000s. Graphical representation of HIV referral networks also shows existence of potentially several clusters of HIV infections among social networks of MSM in Ulaanbaatar. On the other hand, this finding could also indicate that recruitment did not reach all MSM networks. All seeds were identified with the help of three local NGOs that collaborate in their work with MSM. Therefore, MSM not involved in NGO activities and unaware of these organizations may have been missed. In addition, it is possible that because the target sample size was relatively small and reached quickly (in less than a month), members of other MSM networks may not have been given a chance to enroll into the study. The fact that all HIV cases were known infections also explains the results of multivariate regression analyses, whereby consistent condom use and knowledge of HIV transmission issues were associated with positive HIV status. HIV infected men knew their status prior to participation in the study which means that they have been through the NCCD system and received risk reduction counseling. Exposure to the system and risk reduction counseling make these cases understandably more aware of HIV and associated risks compared to HIV negative men. Also, the survey had a cross-sectional design and hence, temporality of the observed association, i.e. whether the
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123 85 33
Not married, no permanent partner
Separated/widowed/divorced
9.5 (2)
31 21
Sometimes
105 68
Yes
No
Knew correct answer to all HIV questions
69 127
2.9 (2)
17.1 (18)
14.4 (18)
4.4 (3)
5.1 (3)
59
No
13.3 (18)
12.8 (10)
20 (6)
5.8 (5)
135
Yes
Sex with female (last 12 months)
No
Yes
78
30
Receptive
Both Condom use at last sex with male partner
87
Insertive
Dominant sexual ‘‘role’’
Rarely/Never
3.2 (1)
53
1.9 (1)
91
Most of the time
18.7 (17)
16/5 (2, 60)
21.2 (7)
10.6 (9)
6.3 (4)
7.1 (1)
16.4 (9)
7.0 (5)
10.0 (7)
33/33 (22, 50)
2.0 (0.5, 7.8)
12.3 (7.8, 19.0)
10.1 (6.3, 15.6)
3.0 (1.0, 9.0)
3.5 (1.1, 10.5)
9.4 (5.9, 14.7)
9.1 (4.9, 16.3)
14.5 (6.4, 29.5)
4.0 (1.6, 9.3)
6.7 (1.6, 23.7)
2.2 (0.3, 14.4)
1.3 (0.2, 8.8)
13.5 (8.4, 21.0)
15.4 (7.3, 29.8)
7.4 (3.8, 13.9)
4.3 (1.6, 11.2)
5.0 (0.7, 28.9)
11.7 (6.1, 21.4)
4.9 (2.0, 11.4)
7.0 (3.3, 14.2)
97.1 (66)
82.9 (87)
85.8 (109)
95.7 (66)
94.9 (56)
86.7 (117)
87.2 (68)
80.0 (24)
94.3 (82)
90.5 (19)
96.8 (30)
98.1 (52)
81.3(74)
10/4 (1, 200)
78.8 (26)
89.4 (76)
93.8 (60)
92.9 (13)
83.6 (46)
93.0 (66)
90.0 (63)
30/29 (17, 49)
Crude% (n)
Crude% (n)
Wt% (95 % CI)
HIV-negative
HIV-positive
Always
Condom use (last 12 months)
Mean/median (range)
196
64
Not married, with permanent partner
Network size
14
Married living with spouse
54
71
C35 Marital status
70
25–34
196
N
15–24
Age groups
Mean/median (range)
Age
Characteristic
98.0 (92.2, 99.5)
87.7 (81.0, 92.3)
89.9 (84.4, 93.7)
97.0 (91.0, 99.2)
96.5 (89.5, 98.9)
90.6 (85.3, 94.1)
90.9 (83.7, 95.1)
85.5 (70.5, 93.6)
96.0 (90.7, 98.4)
93.3 (76.3, 98.4)
97.8(85.6, 99.7)
98.7 (91.2, 99.8)
86.5 (79.0, 91.6)
84.6 (70.2, 92.8)
92.6 (86.1, 96.2)
95.7 (88.9, 98.4)
95.0 (71.1, 99.3)
88.3 (78.6, 93.9)
95.1 (88.6, 98.0)
93.0 (85.8, 96.7)
Wt% (95 % CI)
Table 4 Selected crude and RDS-weighted demographic and risk characteristics by HIV status among MSM, Ulaanbaatar, Mongolia, 2012
8.205
4.518
2.891
2.634
4.112
4.803
1.440
–
F-statistic
0.005
0.035
0.091
0.073
0.007
0.146
0.238
0.058
P-value
AIDS Behav
0.080 100 (26)
91.3 (86.8, 94.3) 87.7 (149) 8.7 (5.7, 13.2)
0.0 0.0 (0) No
12.4 (21) 170
26
Yes
Knew where to get HIV test
100
3.102
0.024 5.169 96.3 (91.2, 98.5)
88.9 (82.4, 93.2) 84.5 (87)
94.6 (87) 3.8 (1.5, 8.8)
11.1 (6.8, 17.6)
No
15.5 (16) 103
92
Yes
5.4 (5)
99.0 (92.9, 99.9) 98.5 (65) 1.0 (0.1, 7.1) 1.5 (1) 66 No
Participated in HIV prevention
84.6 (111) 15.4 (20) 131
11.0 (7.1, 16.6) Tested for HIV
N Characteristic
Table 4 continued
Yes
Crude% (n) Crude% (n)
Wt% (95 % CI)
HIV-negative HIV-positive
Wt% (95 % CI)
89.0 (83.4, 92.9)
8.874
F-statistic
0.003
P-value
AIDS Behav
cases had the knowledge or have consistently used condoms before becoming infected, or became more knowledgeable and altered behavior subsequent to infection cannot be determined. One of the disconcerting findings of the survey is the low coverage of MSM by HIV prevention activities. Only a third of MSM (weighted 33.6 %, crude 51.8 %) have been reached with HIV prevention programs. Among HIV negative MSM reporting exposure to HIV prevention activities in the last 12 months, only about half used VCT services. Thus, less than a quarter of MSM at risk for HIV acquisition have been tested for HIV. VCT programs have been shown to be an effective means of sexual behavior change [16] and therefore, the observed low use of these programs is of particular concern. Suboptimal use of VCT was mentioned in several other reports as well [2, 8]. Specifically, negative attitude of health providers in public health-care settings, a limited variety of VCT service models, lack of pharyngeal and ano-rectal checks as well as structural factors, including human rights violations stemming from stigma and discrimination, were mentioned as major barriers for accessing VCT services. Addressing these barriers and increasing the uptake of HIV testing services is particularly important today, given the increasing evidence for early antiretroviral therapy as an effective HIV prevention tool [17]. NCCD has recently started offering antiretroviral treatment to anyone identified HIV infected, and who is willing to adhere to treatment regimen as prescribed, regardless of their current CD4 count. Therefore, substantial increase in testing and counseling among MSM will be needed to reap the benefits of early antiretroviral therapy and achieve meaningful reduction in HIV transmission. In addition to low HIV prevention coverage and low uptake of VCT services, consistent condom use both in the last 12 months and at last sex were significantly lower among HIV negative MSM than among HIV infected MSM. Results on risk factors such as alcohol and drug use are consistent with previous reports. Alcohol use is widespread but drug use, particularly injection drug use, is still very rare. No questions were asked to elucidate the extent of alcohol abuse or alcohol use in the context of sexual risk behavior. However, an earlier study found that about twothirds reported having a few drinks before or during sex, and about 20 % engage in this behavior often or all the time [8]. Regarding drug use, there is limited reliable data available on the extent and types of illicit drug use in Mongolia. Nevertheless, injection drug use appears to not be widespread and no cases of HIV transmission occurring through injection drug use have been reported to date. Taken together, these data indicate that HIV negative MSM in Mongolia are at high risk for HIV acquisition. The values for key indicators such as HIV prevention coverage
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AIDS Behav Table 5 Multivariate analysis of the association between risk factors and HIV among MSM, Ulaanbaatar, Mongolia, 2012 Characteristic
Unweighted OR (95 % CI)
Z-score
P
Weighted OR (95 % CI)
t-statistic
P
Age 15–24
1.00
25–34
0.48 (0.09, 2.46)
-0.88
0.376
1.00 0.45 (0.08, 2.38)
-0.95
0.345
C35
3.02 (0.63, 14.52)
1.38
0.168
2.88 (0.73, 11.4)
1.52
0.129
1.08
0.279
1.11
0.267
3.56
ORIGINAL PAPER
Evolving Understanding of the Epidemiology of HIV and Prevention Needs among Men Who Have Sex with Men in Ulaanbaatar, Mongolia Iliza Azyei • Bulbul Aumakhan • Baigalmaa Jantsansengee • Sergelen Munkhbaatar • Erdenetuya Gombo • Unenchimeg Puntsag • Davaalkham Jagdagsuren • Sosthenes Ketende • Susanne Stromdahl • Stefan Baral • Tugsdelger Sovd • Oyunbileg Amindavaa
Ó Springer Science+Business Media New York 2014
Abstract This study describes HIV and syphilis biobehavioral survey conducted among 200 men who have sex with men (MSM) recruited via respondent-driven sampling (RDS) between January 4 and February 1, 2012 in Ulaanbaatar, Mongolia. Participants were administered a structured questionnaire and data were analyzed with RDSnetwork program in STATA. Of 196 participants who agreed to be tested for HIV and syphilis, 21 (10.7 %; weighted 7.5; 95 % CI: 4.9, 11.4) and 8 (4.1 %; weighted 3.4; 95 % CI: 1.7, 6.7) were positive for HIV and syphilis,
Iliza Azyei and Bulbul Aumakhan contributed equally to the manuscript. I. Azyei S. Munkhbaatar O. Amindavaa Global Fund Supported Projects on HIV/AIDS and TB, Ministry of Health, Ulaanbaatar, Mongolia B. Aumakhan (&) E. Gombo U. Puntsag D. Jagdagsuren HIV/AIDS and STI Surveillance and Research Department, National Center for Communicable Diseases, Ministry of Health, Ulaanbaatar, Mongolia e-mail: [email protected] B. Jantsansengee Mongolian Field Epidemiology Training Program, Ulaanbaatar, Mongolia E. Gombo ’’Together Center’’ NGO, Bayanzurkh, Mongolia S. Ketende S. Stromdahl S. Baral Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA T. Sovd Monitoring and Evaluation, and Internal Auditing Department, Ministry of Health, Ulaanbaatar, Mongolia
respectively. Exposure to HIV prevention programs in the last 12 months was reported by 51.8 % (weighted 33.6; 95 % CI: 27.6, 40.1) of participants. This study found high HIV prevalence and limited uptake of HIV prevention services among MSM in Mongolia. Given the concentrated HIV epidemic among MSM in Mongolia, HIV prevention, treatment and care services should focus on MSM as the population group most affected by HIV.
Resumen Este estudio reporta una encuesta de VIH y sı´filis conducido en 200 hombres que tienen sexo con hombres (HSH) los cuales fueron enrolados a trave´s un muestreo guiado por los participantes entre enero 4 y febrero 1 del 2012 en Ulaanbaatar, Mongolia. Los participantes recibieron un cuestionario estructurado y la informacio´n se analizo con el programa Stata. De los 196 participantes quienes estuvieron de acuerdo en ser testeados para el VIH y sı´filis, 21 (10.7 %; tasa ajustada 7.5; 95 % IC: 4.9, 11.4) and 8 (4.1 %; tasa ajustada 3.4; 95 % IC: 1.7, 6.7) fueron positivos para VIH y sı´filis, respectivamente. Exposicio´n a los programas de prevencio´n del VIH en los u´ltimos 12 meses fue reportado por 51.8 % (tasa ajustada 33.6; 95 % IC: 27.6, 40.1) de los participantes. Este estudio ha documentado que HSH tienen una alta prevalencia de VIH y limitado servicios de prevencio´n para VIH. Dada la concentrada epidemia del VIH en HSH en Mongolia, la prevencio´n y tratamiento del VIH ası´ como servicios de asistenciales deberı´an focalizarse en HSH debido a que este grupo es la ma´s afectada por la epidemia del VIH.
Keywords Mongolia HIV Respondent-driven sampling Men who have sex with men Asia
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AIDS Behav
Introduction Mongolia is a landlocked country situated in Northern Central Asia bordering Russia to the north and China to the south. It is the 19th largest country in the world in territory and most sparsely populated with a population of about 2.8 million people [1]. Nearly half of the population resides in the capital city Ulaanbaatar. With only 150 cases reported as of December 31, 2013, Mongolia remains a country with a very low HIV prevalence (\0.1 %) among the general population (unpublished data, National Center for Communicable Diseases, Ulaanbaatar, Mongolia). However, there are signs that HIV spread may be accelerating in the country, particularly among men who have sex with men (MSM). Over 80 % (n = 121) of all cumulative cases are men among whom MSM constitute the overwhelming majority (n = 99, 82 %). Except the first 5 cases, all (n = 145/150, 97 %) were reported since 2005. MSM in Mongolia are largely hidden due to low public awareness and widespread prejudice about MSM and issues related to sexual minorities [2, 3]. Stigma and discrimination are common, and given the small population, disclosure of sexual orientation is major concern for MSM. As has been documented in other settings, social and family pressures often force MSM to marry and lead ‘‘double lives’’ with both male and female sexual partners [4]. The stigma and discrimination faced by MSM also pose significant barriers to health service access, employment and social acceptance. In terms of legal environment, male-to-male sex has been legal since 2002, but there are no laws protecting the rights of sexual minorities [5, 6]. Civil society is a relatively new concept in Mongolia with the first MSM community based organization (CBO) formed in 2003. Currently there are three CBOs serving MSM, all based in Ulaanbaatar, providing outreach, peer education, counseling, condom distribution and referrals to HIV and STI testing and treatment services. However, the outreach, community engagement and empowerment capacity of these organizations remain limited. Given the context, monitoring HIV trends among MSM in Mongolia has been challenging due to difficulties of recruiting MSM and limited data on MSM population size and distribution. Bi-annual second generation surveillance (SGS) surveys have been employed since 2005 to study HIV prevalence and trends among MSM. Previous SGS surveys used convenience sampling methods and accounted only for new HIV infections. The SGS survey conducted in 2007 found 1 new HIV infection among 118 MSM (0.8 %), and the survey in 2009 found 3 new HIV infections among 167 MSM (1.8 %) recruited in the capital city of Ulaanbaatar [7]. A cross-sectional study conducted in 2011 by UNAIDS Mongolia in collaboration with the Johns Hopkins School of Public Health, USA, found an
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adjusted self-reported HIV prevalence of 6.3 % among MSM in Ulaanbaatar [8]. The latter study used respondentdriven sampling (RDS) for the first time in Mongolia and successfully recruited over 300 MSM, but did not collect biological samples to validate the self-reported HIV status. Here, we describe a bio-behavioral survey of 200 MSM recruited via RDS in Ulaanbaatar between January 4 and February 1, 2012. The objective of this study was to determine the prevalence of HIV and syphilis among MSM in Ulaanbaatar and factors associated with HIV positive status.
Methods The survey received approval from the Scientific Committee of the National Center for Communicable Disease (NCCD), Ulaanbaatar, Mongolia and the Ethical Committee of the Ministry of Health. Written consent was obtained from all participants prior to enrollment into the survey. Sampling Strategy, Population and Questionnaire RDS method was chosen to recruit participants because it was proven to be successful in recruiting MSM, a highly hidden and hard to reach population group in Mongolia [8]. In addition, RDS is an approximation of probability-based sampling methods and allows characterization of unbiased estimates of outcomes of interest. When certain theoretical assumptions are met, RDS produces weighted estimates that adjust for the difference between the composition of the survey sample and the likely composition of MSM population overall. Details of this method have been described elsewhere [9]. To start recruitment we selected 5 seeds through referral from three local non-governmental organizations (NGOs) working with the MSM population. Seeds were selected based on their varying socio-demographic characteristics (e.g. age, education), level of interest in participation, range of social networks and likelihood of referring three participants. Each participant was given 3 coupons to recruit additional participants until the target sample size was reached. Seeds and participants had to meet the following criteria to be eligible for participation in the survey: (1) age between 15 and 49 years old; (2) have had sexual intercourse (anal or oral) in the last 12 months with another man; (3) able to provide adequate informed consent; and (4) have not been interviewed for this study in the past 3 months. Participants received dual incentives as per RDS method [9]. The incentive amount was equivalent to the local cost of round trip transportation and an average meal. A structured questionnaire eliciting information on demographics, sexual behavior with male and female partners, drug and alcohol use history, sexually transmitted
AIDS Behav
infections (STI) and treatment history, knowledge of HIVtransmission related issues and HIV voluntary counseling and testing (VCT) experiences was administered to participants. The questionnaire was developed and pre-tested in previous rounds of SGS surveys, but included new questions related to social networking as required by RDS method. The survey was administered face-to-face in Mongolian language by trained interviewers and lasted approximately 30 min. A unique identifier was created for each participant as an 8-digit code consisting of the first two letters of father’s first name (Mongolians go by single name and father’s first name is used as a last name), the first two letters of mother’s first name, two-digit year and month of birth. Each participant was also asked if he wanted a reminder call to receive test results, and if the participant agreed, his phone number was recorded in the laboratory journal. Information used for this reminder phone call was not recorded on a specific survey or test results to maintain anonymity. The unique codes and phone numbers were subsequently used to verify HIV positive participants against the cases registered in the national HIV case database. Sample Size The sample size was calculated using the module for determining a population proportion in OpenEpi software [10]. Assuming 2 % of men in Ulaanbaatar age between 15 and 49 years are MSM, 5.4 % syphilis prevalence observed during SGS 2009 as anticipated frequency of outcome factor, design effect of 2 [11] and confidence limits of ±5 %, the target sample size was estimated to be 156. Allowing 80 % response rate for blood collection among behavioral survey respondents, the sample size was 187 participants. In the end, the survey enrolled 200 MSM. Laboratory Procedures Blood samples were kept at a room temperature for no more than 4 h before being delivered to NCCD laboratory for HIV and syphilis testing. Blood samples were tested for HIV using ‘‘SD HIV 1/2 Rapid 3.0’’ (Standard Diagnostics Inc, Korea) rapid tests. Reactive specimens were confirmed using Enzyme-linked immunosorbent assay (ELISA) and Western blot. Syphilis testing was conducted using Rapid plasma reagin (RPR) and Treponema pallidum haemagglutination assay (TPHA) test kits (New Market Laboratories Ltd. Kentford, Newmarket, CB 8 & PN-UK) according to manufacturer’s instructions. Sample was considered positive for syphilis if both TPHA and RPR tests were reactive with RPR titer C1:2. Quality control was performed in compliance with the internal quality control standards with 10 % of randomly selected negative
and all positive samples retested at NCCD laboratory. All participants received pre- and post-test counseling according to national standards. Participants with laboratory evidence of STI were managed free of charge per national STI diagnosis and treatment guidelines. Data management and Analysis RDS Coupon Manager Software was used to keep track of recruitment process and respondent compensation. The following three questions were used to determine social network size: (1) How many people do you know who have sex with men? (2) Of those MSM without overlapping, how many have you met or talked with over the past 6 months? (3) In the following 3 weeks (coupon’s validity period) how many MSM can you meet with? The third question was used to measure network size for the purpose of RDS weighting. If the response was ‘‘zero’’ or ‘‘don’t know’’ the response value to the second question was used as a network size. Variable specific weights were estimated to obtain weighted prevalence estimates. Weighted estimate adjusts for the difference between the composition of the survey sample and the likely composition of the population from which the sample is drawn and thus, theoretically represents the overall MSM population in Ulaanbaatar. If no weighted estimates were produced due to estimation convergence problems, or when a group recruited exclusively from within their own group, the results were marked as ‘‘not determined’’. Bivariate and multivariate analyses were weighted using HIV as the outcome. Bivariate categorical associations were tested using corrected weighted Pearson Chi square converted into F-statistic for complex survey data [12]. Variables associated with HIV infection at p \ 0.20 were entered into multivariate logistic regression that included condom use, type of sexual intercourse, HIV testing history, participation in HIV prevention programs, drinking history, sex with female and correct answer to all HIV knowledge questions. Socio-demographic variables such as age and marital status were included in logistic regression models regardless of p value to account for potential association of socio-demographic factors with HIV infection. Seeds were excluded from multivariate regression analysis as recommended per RDS-method [9]. We considered p values less than 0.1 as statistically significant. Analyses were conducted using RDS network program [13] in STATA statistical software (STATA/IC Version 12.1, Stata Corporation, College Station, Texas, USA). The RDS network program allows an easy implementation of RDS analysis in STATA. It produced point estimates that were identical to those produced by RDS Analysis Tool
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Fig. 1 Referral networks by HIV status (n = 200). Key: large square seed; red square HIV positive (n = 21); blue square HIV negative (n = 175); black square refused testing (n = 4) (Color figure online)
(RDSAT) software but with slightly differing confidence intervals due to use of different bootstrapping algorithms for obtaining confidence intervals. As in RDSAT, RDS network program in STATA incorporates recruitment network structure and adjusts for homophily and oversampling of people with large networks. The RDS network program for analysis of RDS data in STATA is described in detail elsewhere [13]. The network graph was generated using Netdraw program [14].
(Fig. 1). The longest chain reached eight waves and 68 referrals. In 85 % of cases participants were recruited by sexual partners, friends and MSM acquaintances they know well. The remaining 15 % were recruited by NGO outreach workers, peer educators and other MSM. The homophily values for most variables were around zero indicating mostly random recruitment among participants. However, some degree of homophilous recruitment (degree of homophily *0.4) was observed among men age under 25, men of similar educational attainment and those exposed to HIV prevention programs.
Results Demographic Characteristics Recruitment Characteristics The five seeds selected to start recruitment process were age between 23 and 50 years old, three had college and two completed secondary education. None reported drug use, three had regular partners, one was HIV-infected and one syphilis sero-positive. All seeds were effective recruiters
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Participants had a mean age of 30 (median 29, range: 17–50, Table 1). Over half of participants (62.5 %; weighted 54.4; 95 % CI: 47.2, 61.4) had college and/or university level education. Eight percent (weighted 13.2; 95 % CI: 8.3, 20.4) of participants reported being married and currently living with a spouse.
AIDS Behav Table 1 Crude and RDS-weighted demographic characteristics of MSM, Ulaanbaatar, Mongolia, 2012 Characteristic
Crude% (N)
Wt% (95 % CI)
Age Mean/median (range)
30/29 (17, 50)
Age groups 15–24
35.5 (200)
38.8 (32.3, 46.0)
25–34
36.0 (200)
32.1 (26.2, 38.7)
35–44
23.5 (200)
23.7 (18.2, 30.1)
C45 Education
5.0 (200)
5.4 (2.9, 9.8)
Bcomplete secondary
37.5 (200)
45.6 (38.6, 52.8)
College/university
62.5 (200)
54.4 (47.2, 61.4)
Marital status Married living with spouse
8.0 (200)
13.2 (8.3, 20.4)
Not married, living with male permanent partner
32.0 (200)
24.1 (19.0, 30.0)
Not married, no permanent partner Separated/widowed/divorced
43.0 (200)
41.6 (34.8 , 48.7)
17.0 (200)
21.1 (34.8 , 48.7)
Network size Mean/median (range)
11/4 (1, 200)
Sexual Practices and Risk Behaviors Mean and median age at first sexual experience was 18 (range: 8–36, Table 2). Receptive intercourse was reported as the dominant sexual role by 15.6 % (weighted 14.4; 95 % CI: 10.3, 19.8) of participants. Sexual behavior with male partners shows that less than half (47.5 %; weighted 47.4; 95 % CI: 40.5, 54.4) of participants used condom consistently in the last 12 months while condom use at last sex was 70.2 % (weighted 71.0; 95 % CI: 64.3, 76.9). Sexual contact with females was common and reported roughly by 40 % (36.0 %; weighted 45.8; 95 % CI: 38.7, 53. 0) of participants. Only two participants reported having sex with female sex workers in the last 12 months. Reports of genital discharge and genital ulcers in the last 12 months were infrequent. Alcohol was the most commonly used substance with more than 80 % reporting that they drank at least once per month. Non-injectable illicit drug use was 11.5 % (weighted 6.5; 95 % CI: 4.3, 9.7) and none reported injection drug use in the last 12 months. Types of drugs used were not asked but smoking and sniffing were the most common routes of drug use (data not shown). HIV Knowledge, HIV Testing and Prevention Coverage Over 90 % responded correctly to at least one of the five HIV transmission-related knowledge questions (Table 3).
However, the percentage of those who knew correct answer to all 5 questions was 60.2 % (weighted 58.9; 95 % CI: 51.4, 66.0). About 67 % (66.5 %; weighted 54.6; 95 % CI: 47.2, 61.8) were tested for HIV in the last 12 months of whom 97 % (weighted 97.7; 95 % CI: 93.9, 99.1) received test results. The overall percentage of those both tested and received the results was 64.5 % (weighted 55.3; 95 % CI: 48.0, 62.4). The crude percentage for exposure to HIV prevention activities was 51.8 % but weighted was only 33.6 % (95 % CI: 27.6, 40.1), indicating inadequate reach of HIV prevention programs. When disaggregated by type of HIV prevention program, inadequate coverage rates were observed for participation in VCT (57.8 %; weighted 43.6; 95 % CI: 34.5, 53.3), focus group (48.0 %; weighted 33.2; 95 % CI: 25.2, 42.2), community empowerment activities (34.3 %; weighted 28.8 %; 95 % CI: 21.2, 37.9) and STI diagnostics (22.6 %; weighted 12.3; 95 % CI: 8.1, 18.3). HIV and Syphilis Prevalence and Factors Associated with HIV Positive Status HIV and syphilis testing was performed on 196 MSM (4 refused testing). Twenty one participants (10.7 %; weighted 7.5; 95 % CI: 4.9, 11.4, Table 2) were sero-positive for HIV and 8 (4.1 %; weighted 3.4; 95 % CI: 1.7, 6.7) had reactive tests for syphilis. One person was positive for both HIV and syphilis. Graphical representation of HIV among participants is shown in Fig. 1. All 21 HIV cases were previously known cases. This was determined through an 8-digit unique codes and phone numbers of HIV positive cases and verifying it against the corresponding information on patient files and the data in the national HIV case registry. No new infections were detected. Factors associated with HIV positive status were further explored via bivariate (Table 4) and multivariate (Table 5) analyses. HIV prevention coverage (50.1 vs. 76.2 %, p = 0.024), consistent condom use both in the last 12 months (42.3 vs. 81 %, p = 0.007) and condom use at last sex (68 vs. 86 %, p = 0.091) were all significantly lower among HIV uninfected than among HIV infected MSM. Among HIV uninfected MSM reporting exposure to HIV prevention activities in the last 12 months only half (49.5 %) used VCT services. Twice more HIV infected (28.6 %) than HIV uninfected men (13.8 %) practiced receptive intercourse (p = 0.073). Significantly fewer HIV infected men (14.3 vs. 37.7 %) reported having sex with females in the last 12 months (p = 0.035). Two variables, consistent condom use (OR = 10.42, p \ 0.0001) and responding correctly to all 5 knowledge questions (OR = 8.83, p = 0.021), were statistically significantly associated with HIV infection in the multivariate logistic regression analysis.
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AIDS Behav Table 2 Crude and RDSweighted risk characteristics, and prevalence of HIV and syphilis among MSM, Ulaanbaatar, Mongolia, 2012
Characteristic
Crude% (N)
Wt% (95 % CI)
Age at 1st sex Mean/median (range)
18/18 (8, 36)
Sexual behavior with male partners No. of male partners (last 12 months) Mean/median (range)
3/2 (1, 25)
1
39.7 (199)
2–4
43.2 (199)
50.0 (42.9, 57.2) 38.7 (32.1, 45.7)
C5
17.1 (199)
11.3 (8.0,15.6)
Insertive
44.2 (199)
49.5 (42.5, 56.5)
Receptive
15.6 (199)
14.4 (10.3, 19.8)
Universal
40.2 (199)
36.1 (29.8, 43.0)
Always
47.5 (200)
47.4 (40.5,54.4)
Most of the time Sometimes
26.5 (200) 15.5 (200)
23.1 (17.9,29.2) 17.5 (12.6,23.8)
Dominant sexual role
Frequency of condom use (last 12 months)
Rarely
3.5 (200)
3.5 (1.7,7.2)
Never
7.0 (200)
8.6 (5.1, 13.9)
Condom use at last sex
70.2 (198)
Received payment for sex with male partner
4.0 (200)
71.0 (64.3, 76.9) 2.8 (1.4, 5.5)
Sexual behavior with female partners Sex with female
36.0 (200)
45.8 (38.7 , 53.0)
No. of female partners (last 12 months) Mean/median (range)
2/1 (1,20)
1
63.4 (71)
68.9 (57.4,78.4)
C2
36.6 (71)
31.1 (21.6, 42.6)
Sex with non-regular non-commercial female partner
50.7 (71)
41.4 (30.5,53.2)
Condom use at last sex with non-regular female partner
75% (36)
62.5 (43.0,78.6)
2.9 (70)
Not determined
Sex with commercial female partner Substance use Frequency of alcohol use At least once a week
40.0 (200)
33.7 (27.6 , 40.3)
At least once a month
44.0 (200)
47.6 (40.6, 54.6)
Rarely or never
16.0 (200)
18.7 (13.6, 25.3)
11.5 (200)
6.5 (4.3, 9.7)
Ever used drugs Injected drugs in the past 12 months
0.0 (23)
Not determined
Sexually transmitted infections Had genital discharge
7.5 (199)
5.0 (3.0,8.2)
Had ulcers/sores
3.0 (199)
Not determined
Had treatment
50.0 (26)
36.7 (20.3, 56.9)
10.7 (196)
7.5 (4.9, 11.4)
4.1 (196)
3.4 (1.7, 6.7)
Prevalence of HIV and syphilis HIV seropositive Syphilis seropositive
Discussion A cross-sectional bio-behavioral survey of HIV and syphilis recruited 200 MSM via RDS approach in Ulaanbaatar,
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Mongolia and found a 7.5 % adjusted (crude 10.7 %) prevalence of HIV. This is higher than the 1.8 % prevalence reported in 2009 [7], and it exceeds the 5 % cut-off in a high risk group that defines per UNAIDS criteria a concentrated
AIDS Behav Table 3 HIV knowledge, testing and prevention characteristics of MSM, Ulaanbaatar, Mongolia, 2012 Characteristic
Crude% (N)
Wt% (95 % CI)
Having one and faithful sex partner can reduce transmission risk of HIV infection
92.7 (192)
92.9 (88.3, 95.8)
Using condom properly in all sexual intercourses can prevent HIV infection
95.5 (199)
93.8 (88.6, 96.8)
Healthy looking person can be infected with HIV
95.2 (189)
96.7 (93.8, 98.3)
Mosquito bites do not transmit HIV
72.2 (176)
67.0 (59.3, 73.9)
Handshaking and sharing food with HIV infected person do not transmit HIV
92.9 (196)
93.0 (88.4, 95.8)
Responded correctly to all above questions
60.2 (176)
58.9 (51.4, 66.0)
Tested for HIV
66.5 (200)
54.6 (47.2, 61.8)
If tested, received results back
97.0 (133)
97.7 (93.9, 99.1)
Tested and received test results
64.5 (200)
55.3 (48.0, 62.4)
Participated in HIV prevention
51.8 (199)
33.6 (27.6, 40.1)
Training
78.4 (102)
75.3 (66.2,82.6)
Focus group
34.3 (102)
28.8 (21.2,37.9)
HIV-related knowledge
HIV testing and prevention
Voluntary counseling and testing
57.8 (102)
43.6 (34.5,53.3)
Community empowerment activities
48.0 (102)
33.2 (25.2,42.2)
Received condoms lubricants
65.7 (102)
44.9 (35.4,54.8)
STI diagnostics Know where to get HIV test
22.6 (102)
12.3 (8.1,18.3)
87.0 (200)
80.0 (72.5, 88.5)
HIV epidemic. However, the prevalence found in this survey should not be interpreted directly as a sharp increase in HIV prevalence among MSM in Mongolia. Rather, interpretation should take into consideration several factors. First, the 2009 survey counted only new HIV positive cases and excluded known positive cases, whereas HIV positive status was not an exclusion criterion in this survey. Second, the surveys employed different sampling strategies, RDS in the current survey and convenient sampling in 2009 survey. Third, it was subsequently determined that all 21 HIV positive cases detected in this survey were known infections registered with HIV/AIDS and STI Surveillance and Research Department, NCCD. Finally, the survey only sampled MSM in the capital city, Ulaanbaatar, and thus, it is not representative of HIV prevalence among MSM nationwide. The 7.5 % HIV prevalence, however, is comparable to 6.3 % self-reported HIV prevalence estimate observed in the earlier mentioned survey of MSM in Ulaanbaatar that
was implemented with the support of UNAIDS Mongolia in collaboration with the Johns Hopkins School of Public Health, USA, in 2011 [8]. The main purpose of the latter survey was to establish baseline data on HIV risk status, access to services and human rights contexts among MSM in Mongolia. The finding that all 21 HIV cases were known infections already registered in the national HIV case database at NCCD indicates, that these cases may have come from a single or few networks, or that HIV has not been introduced into other sexual networks. This is supported by the epidemiological risk profile data of cases registered in the national HIV case registry. Specifically, all HIV suspected cases around the country are confirmed with Western Blot at NCCD. Upon confirmation all newly identified cases undergo detailed epidemiologic investigation including contact tracing. Consequently, HIV clinicians and epidemiologists at NCCD have long suspected that many cases among MSM are epidemiologically linked with each other. This was confirmed in a study published in 2011 which reported results of a phylogenetic tree analysis of viral sequences isolated from the sera of 38 (out of 56 total reported by the time of study, May 2009) HIV infected cases [15]. The phylogenetic study identified two clusters of HIV subtype B infections among MSM and determined that there was a rapid expansion of HIV transmission with the same ancestor virus from these clusters starting around early 2000s. Graphical representation of HIV referral networks also shows existence of potentially several clusters of HIV infections among social networks of MSM in Ulaanbaatar. On the other hand, this finding could also indicate that recruitment did not reach all MSM networks. All seeds were identified with the help of three local NGOs that collaborate in their work with MSM. Therefore, MSM not involved in NGO activities and unaware of these organizations may have been missed. In addition, it is possible that because the target sample size was relatively small and reached quickly (in less than a month), members of other MSM networks may not have been given a chance to enroll into the study. The fact that all HIV cases were known infections also explains the results of multivariate regression analyses, whereby consistent condom use and knowledge of HIV transmission issues were associated with positive HIV status. HIV infected men knew their status prior to participation in the study which means that they have been through the NCCD system and received risk reduction counseling. Exposure to the system and risk reduction counseling make these cases understandably more aware of HIV and associated risks compared to HIV negative men. Also, the survey had a cross-sectional design and hence, temporality of the observed association, i.e. whether the
123
123 85 33
Not married, no permanent partner
Separated/widowed/divorced
9.5 (2)
31 21
Sometimes
105 68
Yes
No
Knew correct answer to all HIV questions
69 127
2.9 (2)
17.1 (18)
14.4 (18)
4.4 (3)
5.1 (3)
59
No
13.3 (18)
12.8 (10)
20 (6)
5.8 (5)
135
Yes
Sex with female (last 12 months)
No
Yes
78
30
Receptive
Both Condom use at last sex with male partner
87
Insertive
Dominant sexual ‘‘role’’
Rarely/Never
3.2 (1)
53
1.9 (1)
91
Most of the time
18.7 (17)
16/5 (2, 60)
21.2 (7)
10.6 (9)
6.3 (4)
7.1 (1)
16.4 (9)
7.0 (5)
10.0 (7)
33/33 (22, 50)
2.0 (0.5, 7.8)
12.3 (7.8, 19.0)
10.1 (6.3, 15.6)
3.0 (1.0, 9.0)
3.5 (1.1, 10.5)
9.4 (5.9, 14.7)
9.1 (4.9, 16.3)
14.5 (6.4, 29.5)
4.0 (1.6, 9.3)
6.7 (1.6, 23.7)
2.2 (0.3, 14.4)
1.3 (0.2, 8.8)
13.5 (8.4, 21.0)
15.4 (7.3, 29.8)
7.4 (3.8, 13.9)
4.3 (1.6, 11.2)
5.0 (0.7, 28.9)
11.7 (6.1, 21.4)
4.9 (2.0, 11.4)
7.0 (3.3, 14.2)
97.1 (66)
82.9 (87)
85.8 (109)
95.7 (66)
94.9 (56)
86.7 (117)
87.2 (68)
80.0 (24)
94.3 (82)
90.5 (19)
96.8 (30)
98.1 (52)
81.3(74)
10/4 (1, 200)
78.8 (26)
89.4 (76)
93.8 (60)
92.9 (13)
83.6 (46)
93.0 (66)
90.0 (63)
30/29 (17, 49)
Crude% (n)
Crude% (n)
Wt% (95 % CI)
HIV-negative
HIV-positive
Always
Condom use (last 12 months)
Mean/median (range)
196
64
Not married, with permanent partner
Network size
14
Married living with spouse
54
71
C35 Marital status
70
25–34
196
N
15–24
Age groups
Mean/median (range)
Age
Characteristic
98.0 (92.2, 99.5)
87.7 (81.0, 92.3)
89.9 (84.4, 93.7)
97.0 (91.0, 99.2)
96.5 (89.5, 98.9)
90.6 (85.3, 94.1)
90.9 (83.7, 95.1)
85.5 (70.5, 93.6)
96.0 (90.7, 98.4)
93.3 (76.3, 98.4)
97.8(85.6, 99.7)
98.7 (91.2, 99.8)
86.5 (79.0, 91.6)
84.6 (70.2, 92.8)
92.6 (86.1, 96.2)
95.7 (88.9, 98.4)
95.0 (71.1, 99.3)
88.3 (78.6, 93.9)
95.1 (88.6, 98.0)
93.0 (85.8, 96.7)
Wt% (95 % CI)
Table 4 Selected crude and RDS-weighted demographic and risk characteristics by HIV status among MSM, Ulaanbaatar, Mongolia, 2012
8.205
4.518
2.891
2.634
4.112
4.803
1.440
–
F-statistic
0.005
0.035
0.091
0.073
0.007
0.146
0.238
0.058
P-value
AIDS Behav
0.080 100 (26)
91.3 (86.8, 94.3) 87.7 (149) 8.7 (5.7, 13.2)
0.0 0.0 (0) No
12.4 (21) 170
26
Yes
Knew where to get HIV test
100
3.102
0.024 5.169 96.3 (91.2, 98.5)
88.9 (82.4, 93.2) 84.5 (87)
94.6 (87) 3.8 (1.5, 8.8)
11.1 (6.8, 17.6)
No
15.5 (16) 103
92
Yes
5.4 (5)
99.0 (92.9, 99.9) 98.5 (65) 1.0 (0.1, 7.1) 1.5 (1) 66 No
Participated in HIV prevention
84.6 (111) 15.4 (20) 131
11.0 (7.1, 16.6) Tested for HIV
N Characteristic
Table 4 continued
Yes
Crude% (n) Crude% (n)
Wt% (95 % CI)
HIV-negative HIV-positive
Wt% (95 % CI)
89.0 (83.4, 92.9)
8.874
F-statistic
0.003
P-value
AIDS Behav
cases had the knowledge or have consistently used condoms before becoming infected, or became more knowledgeable and altered behavior subsequent to infection cannot be determined. One of the disconcerting findings of the survey is the low coverage of MSM by HIV prevention activities. Only a third of MSM (weighted 33.6 %, crude 51.8 %) have been reached with HIV prevention programs. Among HIV negative MSM reporting exposure to HIV prevention activities in the last 12 months, only about half used VCT services. Thus, less than a quarter of MSM at risk for HIV acquisition have been tested for HIV. VCT programs have been shown to be an effective means of sexual behavior change [16] and therefore, the observed low use of these programs is of particular concern. Suboptimal use of VCT was mentioned in several other reports as well [2, 8]. Specifically, negative attitude of health providers in public health-care settings, a limited variety of VCT service models, lack of pharyngeal and ano-rectal checks as well as structural factors, including human rights violations stemming from stigma and discrimination, were mentioned as major barriers for accessing VCT services. Addressing these barriers and increasing the uptake of HIV testing services is particularly important today, given the increasing evidence for early antiretroviral therapy as an effective HIV prevention tool [17]. NCCD has recently started offering antiretroviral treatment to anyone identified HIV infected, and who is willing to adhere to treatment regimen as prescribed, regardless of their current CD4 count. Therefore, substantial increase in testing and counseling among MSM will be needed to reap the benefits of early antiretroviral therapy and achieve meaningful reduction in HIV transmission. In addition to low HIV prevention coverage and low uptake of VCT services, consistent condom use both in the last 12 months and at last sex were significantly lower among HIV negative MSM than among HIV infected MSM. Results on risk factors such as alcohol and drug use are consistent with previous reports. Alcohol use is widespread but drug use, particularly injection drug use, is still very rare. No questions were asked to elucidate the extent of alcohol abuse or alcohol use in the context of sexual risk behavior. However, an earlier study found that about twothirds reported having a few drinks before or during sex, and about 20 % engage in this behavior often or all the time [8]. Regarding drug use, there is limited reliable data available on the extent and types of illicit drug use in Mongolia. Nevertheless, injection drug use appears to not be widespread and no cases of HIV transmission occurring through injection drug use have been reported to date. Taken together, these data indicate that HIV negative MSM in Mongolia are at high risk for HIV acquisition. The values for key indicators such as HIV prevention coverage
123
AIDS Behav Table 5 Multivariate analysis of the association between risk factors and HIV among MSM, Ulaanbaatar, Mongolia, 2012 Characteristic
Unweighted OR (95 % CI)
Z-score
P
Weighted OR (95 % CI)
t-statistic
P
Age 15–24
1.00
25–34
0.48 (0.09, 2.46)
-0.88
0.376
1.00 0.45 (0.08, 2.38)
-0.95
0.345
C35
3.02 (0.63, 14.52)
1.38
0.168
2.88 (0.73, 11.4)
1.52
0.129
1.08
0.279
1.11
0.267
3.56
