Skip to main content
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2018 Sep 1.
Published in final edited form as: J Acquir Immune Defic Syndr. 2018 Sep 1;79(1):e7–e16. doi: 10.1097/QAI.0000000000001756

Individual and Network Factors Associated with HIV Care Continuum Outcomes Among Nigerian MSM Accessing HealthCare Services

Habib O Ramadhani 1, Nicaise Ndembi 1,2, Rebecca G Nowak 1, Uchenna Ononaku 2, Jerry Gwamna 3, Ifeanyi Orazulike 4, Sylvia Adebajo 5, Trevor A Crowell 6,7, Hongjie Liu 8, Stefan D Baral 9, Julie Ake 7, Man E Charurat 1, For the TRUST/RV368 Study Group
PMCID: PMC6092228  NIHMSID: NIHMS966531  PMID: 29781881

Abstract

Background and setting

As data on the determinants of the HIV care continuum from key populations such as men who have sex with men (MSM) in resource-limited, settings (RLS) are limited, the study aimed to characterize HIV care continuum outcomes and assess individual and network barriers to progression through the HIV care continuum among MSM in Abuja and Lagos, Nigeria.

Methods

TRUST/RV368 study used respondent-driven-sampling to accrue MSM into community-based clinics in Nigeria. Participants received HIV testing at enrollment. HIV-infected participants were offered antiretroviral therapy (ART) with HIV RNA testing every three months (Abuja) or six months (Lagos). Multiple logistic regression models were used to calculate adjusted odds ratios for factors associated with each point in the HIV care continuum, including HIV testing, ART initiation, and six-month viral suppression.

Results

A total of 1506 MSM were recruited, 1178 (78.2%) tested for HIV and 369 (31.3%) were HIV positive newly diagnosed. Of these, 188 (50.1%) initiated ART, 136 (72.3%) completed six months and 96 (70.6%) were virally suppressed. Larger network size and stronger social network support were positively associated with HIV testing uptake. Factors associated with ART initiation were higher education and stronger social network support. Having stronger social network support was associated with increased odds of viral suppression at six months.

Conclusions

Social determinants of health potentiated increased HIV Care Continuum outcomes. Integration of HIV prevention, HIV Counselling and Testing services and universal coverage of ART into a community-based clinic is critical in achieving better hig HIV Care Continuum outcomes.

Keywords: Men who have Sex with Men, Sexual network, HIV testing, ART initiation, Viral suppression

Introduction

The UNAIDS 90-90-90 targets challenge healthcare systems to diagnose 90% of people living with HIV (PLHIV), link 90% of those diagnosed to care and treatment, and to achieve viral suppression in 90% of those in care1. Data on the determinants of the HIV care continuum from key populations such as men who have sex with men (MSM) in resource-limited settings (RLS) are needed to inform targeted interventions in these populations in order to achieve the UNAIDS targets.

Prior studies focused on individual characteristics associated with HIV testing, ART initiation and viral suppression 27. Besides individual characteristics, sexual network factors may affect HIV testing and downstream engagement in health services8. MSM face challenges in accessing health care that may be alleviated by culturally competent care providers, peer health navigators, and/or integrated healthcare services 9,10. For example, in Nigeria, same-sex practices are criminalized and MSM are highly stigmatized 11,12. For this reason, it remains challenging to effectively engage MSM living with HIV in Nigeria given that they are less likely to access health care services and are at risk of uncontrolled viral load. MSM are disproportionately affected by HIV with prevalence of HIV among Nigerian MSM ranging from 44% to 66 % compared to 3.2% in general population13,14. Similarly, incidence and prevalence of sexually transmitted infections (STI) among Nigerian MSM are high 13,15, posing the risk of adverse clinical outcomes and also onward HIV transmission. Understanding the multi-level barriers and enhancers is key to designing and implementing more effective treatment and prevention programs. In this study, we characterized the HIV care continuum within the context of test and treat among MSM in Nigeria.

Methods

Study design and population

MSM were recruited into a prospective combination HIV prevention and treatment study (TRUST/RV368) using respondent driven sampling (RDS) in two clinics in Abuja and Lagos, Nigeria as previously described16,17. In brief, eligible participants were born male, age ≥16 years (Abuja) or ≥18 years (Lagos), engaged in receptive or insertive anal intercourse in the past year, and provided informed consent in English or Hausa. Through community based convenient sampling, 12 individuals (seeds) who are highly connected within the target population were recruited. Seeds recruited up to three of their social and/or sexual eligible partners through the distribution of coupons. Recruitment chains ranged in length from 0 to 28 waves as of August 2017. Seeds and subsequent recruits were included in these analyses. The study was approved by the University of Maryland Baltimore Institutional Review Board (IRB); the Federal Capital Territory Health Research Ethics Committee, Abuja; and Walter Reed Army Institute of Research IRB.

Data collection

In these analyses, study participants (egos) provided information on up to 5 of their partners (alters) from the past year. Face-to-face interviews using a structured questionnaire were administered to each ego at baseline and every 3 months for up to 18 months. The questionnaire captured demographic characteristics as well as other information such as, receiving information about HIV prevention and participation in HIV prevention meetings in the past 12-months, sexual orientation, fear of seeking health care, avoiding seeking care, blackmail, network size, network density, and disclosure of MSM status to family or health care workers. Information collected about alters included age, education, marital status, socio economic status, HIV status, regular or casual partnership, and sexual orientation.

Clinical data and blood samples were collected at baseline and at each follow up visit. Blood samples were tested for HIV infection using rapid HIV antibody tests following the parallel testing algorithm for high-risk individuals according to national guidelines in Nigeria18. Plasma viral load (VL) tests were conducted every three months (Abuja) or six months (Lagos) using COBAS TaqMan HIV-1 Test (Roche Molecular Diagnostics, California).

Definition of Variables

The outcome variables of interest were HIV testing, ART initiation, and viral suppression. HIV diagnosed participants underwent HIV treatment preparation counselling and initiated ART. Those who initiated ART and had HIV-RNA ≤1000 copies/ml at 6-months post ART initiation were considered virally suppressed in accordance with WHO guidelines19.

Network size was defined as the number of MSM the study participant knew and/or had seen or communicated with in the last six months. Network density was defined as degree of connection in the network and was calculated as the total number of actual ties divided by the total number of potential ties20. Network density scores were dichotomized; < 50% indicating smaller network density and ≥ 50% indicating larger network density. To understand the effect of social support on HIV Care Continuum, participants answered the following five questions: “Can you count on other MSM in your group of friends if you need to borrow money”, “Can you count on other MSM in your group of friends to accompany you to a doctor or hospital”, “Can you count on other MSM in your group of friends if you need to talk about your problems”, “Can you count on other MSM in your group of friends if you need somewhere to stay” and “Can you count on other MSM in your group of friends to help deal with a violent or difficult situation”. Responses were measured using a Likert scale ranging from (0) strongly disagree to (3) strongly agree. Scores were summed (score range: 0–15) and the Cronbach’s alpha was 0.82. Scores were dichotomized at the median, < 10 indicating weaker social support and ≥ 10 indicating stronger social support. Strength of partner’s information was based on the ego’s rating from 0 (not sure at all) to 10 (100% sure) about the information he provided on his alter. Rating scores were dichotomized at the median, < 8 indicating weaker strength of partner’s information and ≥ 8 indicating stronger strength of partner’s information. Strength of partner’s relationship was based on the ego’s rating of his friendship with his alter on a scale of 0 to 10. Rating scores were dichotomized at the median, < 6 indicating weaker relationship and ≥ 6 indicating stronger relationship.

Statistical analysis

Frequencies of categorical variables were calculated as the proportions of participants sampled. At the ego level, correlates of HIV testing were assessed using bivariate and multiple logistic regression models. From the list of alters we created ego-alter pair data which consisted of one data record for each sexual partner that included participant characteristics and ART initiation and viral suppression outcomes. For the paired data analysis, logistic regression with generalized estimating equations were used to account for the correlations of the ego in each ego-alter relationship. Since participants who did not test for HIV did not have alters’ information collected, logistic regression models using paired data were fit to assess ego and alter predictors of ART initiation and viral suppression. For the analyses of paired data, three hierarchical models were performed. Model 1 included only ego characteristics. In model 2, alter characteristics were added to model 1. The final model, model 3, cross level differences and interaction terms were added to model 2. Akaike’s information criterion (AIC), − 2Log likelihood (–2LL) and likelihood ratio test were used to assess the fitness of hierarchical models. Multivariate models included pre-specified, biologically plausible factors of interest and variables with p-value of less than 0.2 in bivariate models. In hierarchical models, variables were sequentially added in a stepwise manner while checking the model fit. Dummy variables were created for the missing data. All associations were presented as adjusted odds ratios (aORs) with 95% confidence intervals (CIs). Statistical analyses were conducted using SAS version 9.3 (SAS Institute Inc., Cary, NC).

Results

Study population

Between March 2013 and August 2017, a total of 2024 MSM were recruited and those who had a known HIV positive status were excluded (n=518). Of the remaining 1506 MSM with unknown HIV status, 1178 (78.2%) were tested for HIV and 369 (31.3%) were HIV-infected (figure 1). Of these newly diagnosed individuals, 188 (50.9%) initiated ART. Of 136 individuals who reached 6 months in care after ART initiation, 96 (70.6%) achieved viral suppression. Table 1 presents baseline ego and alter characteristics.

Figure 1.

Figure 1

HIV testing, ART initiation and six-month viral suppression among MSM in Abuja and Lagos, Nigeria

Table 1.

Individual and Network Characteristics at various stages of HIV Cascade among MSM at HIV Prevention Clinics, Abuja and Lagos, Nigeria 2013 – 2017

Characteristic Ego (n = 1506) Alter (n = 3370)
N % n %
Age
 ≤ 19 years 259 17.2 359 10.7
 20 – 29 years 1033 68.6 1930 57.3
 ≥ 30 years 214 14.2 776 23.0
 Missing/ Don’t know 0 0.0 305 9.0
Education
 < Senior secondary school 264 17.5 224 6.6
 Senior secondary school 765 50.8 1153 34.2
 > Senior secondary school 451 30.0 1671 49.6
 Missing / Don’t know 26 1.7 322 9.6
Religion
 Christian 983 65.3
 Moslem 497 33.0
 Missing 25 1.7
Marital status
 Single 1308 86.8 2708 80.4
 Married 104 6.9 528 15.7
 Divorced/separated/ widow 31 2.1 38 1.1
 Missing/ Don’t know 63 4.2 96 2.9
SES of Alters compared to that of Ego’s
 Lower 779 23.1
 Same 682 20.2
 Higher 1839 54.6
 Do not know 70 2.1
Sex orientation
 Bisexual 971 64.5 1817 53.9
 Homosexual 507 33.7 1356 40.2
 Missing / Don’t know 28 1.9 197 5.8
Sexual relationship
 Regular 1255 37.2
 Casual 2107 62.5
 Missing 8 0.2
HIV status
 Negative 809 53.7 1599 47.4
 Positive 369 24.5 87 2.6
 Missing / Don’t know 328 21.8 1684 50.0
Received information about HIV prevention for MSM
 No 710 47.1
 Yes 194 12.9
 Missing/Defaulted/Non response 602 40.0
Participate in HIV prevention meetings
 No 557 37.0
 Yes 345 22.9
 Missing/Defaulted/Non response 604 40.0
Network size
 1 – 10 1028 68.3
 11 – 20 208 13.8
 21 – 30 83 5.5
 31+ 153 10.2
 Missing 34 2.3
Network density
 < 50 % 369 24.5
 ≥ 50 % 478 31.7
 Missing/Defaulted/Non response 659 43.8
Have fear of seeking health care
 No 1034 68.7
 Yes 431 28.6
 Missing 40 2.7
Ever being blackmailed
 No 1179 78.2
 Yes 305 30.3
 Missing 22 1.5
Ever tested for HIV
 No 519 34.5
 Yes, once 944 62.7
 Missing 43 2.8
Disclosed MSM to family
 No 1291 85.7
 Yes 195 13.0
 Missing 20 1.3
Disclosed MSM to health care workers
 No 1142 75.8
 Yes 364 24.2
 Missing 0 0.0
Social support score
 < Median 378 25.1
 ≥ Median 436 29.0
 Missing/Defaulted/Non response 692 46.0
Can count on friends to get money
 Disagree/strongly disagree 278 18.5
 Agree/strongly agree 586 38.9
 Missing/Defaulted/Non response 314 42.6
Can count on friends to accompany to the hospital
 Disagree/strongly disagree 241 16.0
 Agree/strongly agree 645 42.8
 Missing/Defaulted/Non response 620 41.2
Can count on friends to talk about your problems
 Disagree/strongly disagree 212 14.1
 Agree/strongly agree 675 44.8
 Missing/Defaulted/Non response 619 41.1
Wave
 0 – 12 890 59.1
 13 – 27 616 40.9
Site
 Lagos 433 28.7 1093 32.4
 Abuja 1073 71.3 2277 67.6
Strength of partners information
 <Median 1607 47.7
 ≥Median 1733 51.4
 Missing 30 0.9
Partners strength of relationship with ego
 <Median 1296 38.5
 ≥Median 2055 61.0
 Missing 19 0.5

Abbreviations: HIV, Human immune deficiency Virus; SES, Socio economic status; MSM, Men who have sex with men.

Ego characteristics

The median age of egos was 24 (IQR, 21–27) years. The majority of egos were between 20 and 29 years old (n=1033, 68.6%), had senior secondary school education (n=765, 50.8%), were Christian (n = 983, 65.3) and were bisexual (n=971, 64.5%). One hundred and ninety four (12.9%) received information about HIV prevention in the past 12-months and participated in HIV prevention meetings (n=345, 22.9%). Most, (n =1028, 68.3%) had a network size between 1–10 partners, had a network density ≥ 50% (n=478, 31.7%) and reported avoiding seeking health care (n=431, 28.6%). Nearly a quarter (24.2%) reported disclosing sexual orientation to health care providers and never had a prior HIV test (n = 519, 34.5%). The median social support score was 10 (IQR, 8 –11) and nearly a third had social support score ≥ median (n = 436, 29.0%).

Alter characteristics

The median age of alters was 25 (IQR, 22–30) years. Of 3370 alters, 1930 (57.3%) were between 20 and 29 years old and 1671 (49.6%) had more than senior secondary school education. Based on the egos’ responses, 1839 (54.6%) alters had social economic status higher than ego’s and 1817 (53.9%) were bisexual. Eight seven alters (2.6%) were HIV positive and 2107 (62.5%) were casual relationships. The median score measuring egos’ confidence in alters information was 8 (IQR, 6–9).

HIV testing

Multivariate analyses of ego characteristics (Table 2) showed that higher education, senior secondary school vs. < senior secondary school (aOR =2.4; 95% CI, 1.7 – 3.4), > senior secondary school vs. < senior secondary school (aOR = 2.6; 95% CI, 1.7 – 4.0) and having a large network density ≥ 50% vs. < 50% (aOR = 1.8; 95% CI, 1.1 – 3.0) were significantly associated with increased odds of HIV testing. Having a large network size, 11–20 vs. 1–10 (aOR =1.7; 95% CI, 1.1 – 2.5), 21–30 vs.1–10 (aOR = 3.5; 95% CI, 1.5 – 7.8) and disclosing being an MSM to health care workers (aOR =1.5; 95% CI, 1.1 – 2.2) were also associated with increased odds of HIV testing. Furthermore, participants who have stronger social support from friends within their networks (aOR = 6.4.; 95% CI, 1.1 – 37.2) and those who reported prior HIV test (aOR = 1.5.; 95% CI, 1.1 – 2.0) had increased odds of HIV testing. Younger age, ≤ 19 vs. ≥ 30 years (aOR =0.7; 95% CI, 0.5 – 0.9), 20 – 29 vs. ≥ 30 years (aOR =0.6; 95% CI, 0.4 – 1.0), religion, Moslem vs Christian (aOR =0.4; 95% CI, 0.3 – 0.6) and blackmail (aOR = 0.9, 95% CI, 0.8 – 1.0) were associated with decreased odds of HIV testing.

Table 2.

Association Between Ego Characteristics and HIV testing among MSM at HIV Prevention Clinics, Abuja, and Lagos, Nigeria 2013 – 2017.

Characteristics Tested
N = 1178
Bivariate Multivariate
n (%)* OR 95% CI aOR 95% CI
Age
 ≤ 19 years 172(56.3) 0.5 (0.4 – 0.7) 0.7 (0.5 – 0.9)
 20 – 29 years 823(79.7) 0.3 (0.2 – 0.5) 0.6 (0.4 – 1.0)
 ≥ 30 years 183(85.5) 1.0 1.0
Education
 < Senior secondary school 145(54.9) 1.0 1.0
 Senior secondary school 620(81.0) 3.5 (2.6 – 4.7) 2.4 (1.7– 3.4)
 > Senior secondary school 392(86.9) 5.4 (3.8 – 7.9) 2.6 (1.7 – 4.0)
 Missing 21(80.8)
Religion
 Christian 806(82.0) 1.0 1.0
 Moslem 347(69.8) 0.5 (0.4 – 0.6) 0.4 (0.3 – 0.6)
 Missing 25(96.2)
Sex orientation
 Bisexual 778(80.1) 1.0 1.0
 Homosexual 373(73.6) 1.4 (1.1 – 1.7) 1.1 (0.9 – 1.5)
 Missing / Don’t know 27(396.4)
Participate in HIV prevention meetings
 No 480(86.2) 1.0 1.0
 Yes 335(97.1) 3.4 (1.9 – 7.4) 4.1 (2.7 – 6.2)
 Missing 363(60.0)
Received information on HIV prevention
 No 618(87.0) 1.0 1.0
 Yes 169(96.0) 3.4 (1.7 – 7.3) 4.9 (2.9 – 8.2)
 Missing 374(62.1)
Network size
 1 – 10 771(75.0) 1.0 1.0
 11 – 20 171(82.2) 1.5 (1.0 – 2.2) 1.7 (1.1 – 2.5)
 21 – 30 76(91.6) 3.5 (1.6 – 7.8) 3.5 (1.5 – 7.8)
 31+ 130(85.0) 1.8 (1.2 – 2.9) 1.9 (1.1 – 3.1)
 Missing 30(88.2)
Network density
 < 50 % 332(90.1) 1.0 1.0
 ≥ 50 % 450(94.2) 1.8 (1.1 – 3.0) 2.1 (1.2 – 3.7)
 Missing 396(60.0)
Ever being blackmailed
 No 935(79.3) 1.0 1.0
 Yes 223(73.1) 0.7 (0.5 – 0.9) 0.9 (0.8 – 1.0)
 Missing 20(9.1)
Disclosed MSM to family
 No 991(76.7) 1.0 1.0
 Yes 168(86.2) 1.8 (1.2 – 2.8) 1.2 (0.9 – 2.0)
 Missing 19(95.0)
Disclosed MSM to health care workers
 No 858(75.1) 1.0 1.0
 Yes 320(87.9) 2.4 (1.7 – 3.4) 1.5 (1.1 – 2.2)
 Missing 0(0.0)
Social support score
 < Median 368(97.1) 1.0 1.0
 ≥ Median 434(99.5) 5.9 (1.3 – 27.1) 6.4 (1.1 – 37.2)
 Missing 376(54.3)
Ever tested for HIV
 No 337(34.5) 1.0 1.0
 Yes 799(84.6) 2.7 (2.1 – 3.4) 1.5 (1.1 – 2.0)
 Missing 42(97.7)
Wave
 0 – 12 709(79.7) 1.0 1.0
 13 – 27 469(76.1) 0.8 (0.6 – 1.0) 1.0 (0.8 – 1.4)

Abbreviations: OR, Odds ratio; aOR, adjusted odds ratio; CI, Confidence intervals; HIV, Human immune deficiency Virus;

*

Percentage denote proportion of HIV testing using n from this table with N from Table 1.

Bolded denotes p < 0.05

Multilevel modelling

Ego characteristics and ART Initiation (Model 1)

Having higher education, > senior secondary school vs. < senior secondary school (aOR = 2.4; 95% CI, 1.5 – 4.0) was associated with increased odds of ART Initiation (Table 3). Participants having stronger social network support (aOR = 1.4; 95% CI, 1.0 – 1.8) also had increased odds of ART Initiation. Younger partcipants, 20 – 29 vs. ≥ 30 years (aOR =0.5; 95% CI, 0.3 – 0.9) and Moslems (aOR = 0.5; 95% CI, 0.3 – 0.6) had decreased odds of ART initiation.

Table 3.

Association Between Individual, Structural and Network Characteristics and ART Initiation Among MSM at HIV Prevention Clinics, Abuja and Lagos, Nigeria 2013 – 2016: Multilevel Logistic Regression Models Using Paired Data

Characteristic Model1 Model2 Model3



aOR 95% CI aOR 95% CI aOR 95% CI
Ego factors
Age
 ≤ 19 years 1.1 (0.6 – 2.0) 1.5 (0.6 – 3.1) 0.9 (0.5 – 1.8)
 20 – 29 years 0.5 (0.3 – 0.9) 0.5 (0.3 – 0.8) 0.5 (0.3 – 0.8)
 ≥ 30 years 1.0 1.0 1.0
Education
 < Senior secondary school 1.0 1.0 1.0
 Senior secondary school 1.3 (0.8 – 2.2) 2.0 (1.2 – 3.6) 1.9 (1.1 – 3.6)
 > Senior secondary school 2.4 (1.5 – 4.0) 4.3 (2.4 – 7.6) 4.2 (2.3 – 7.9)
Religion
 Christian 1.0 1.0 1.0
 Moslem 0.5 (0.3 – 0.6) 0.4 (0.3 – 0.7) 0.5 (0.3 – 0.7)
Participate in HIV prevention meetings
 No 1.0 1.0 1.0
 Yes 1.1 (0.8 – 1.5) 1.2 (0.8 – 1.7) 1.1 (0.7 – 1.5)
Network size
 1 – 10 1.0 1.0 1.0
 11 – 20 0.6 (0.3 – 0.9) 0.8 (0.2 – 0.6) 0.5 (0.3 – 0.7)
 21 – 30 1.5 (0.8 – 3.1) 1.8 (0.9 – 3.7) 1.3 (0.8 – 2.1)
 31+ 0.8 (0.5 – 1.3) 0.9 (0.5 – 1.4) 0.8 (0.5 – 1.3)
Disclosed MSM to health care workers
 No 1.0 1.0 1.0
 Yes 1.2 (0.9 – 1.8) 1.4 (0.9 – 2.2) 1.4 (1.0 – 2.3)
Social support score
 < Median 1.0 1.0 1.0
 ≥ Median 1.4 (1.0 – 1.8) 1.4 (1.1 – 1.9) 1.3 (1.1 – 1.9)
 Missing
Wave
 0 – 12 1.0 1.0 1.0
 13 – 27 1.1 (0.8 – 1.5) 1.0 (0.8 – 1.4) 0.9 (0.7 – 1.3)
Alter factors
Partner education
 < Senior secondary school 1.0 1.0
 Senior secondary school 1.5 (0.7 – 3.2) 1.4 (0.5 – 3.9)
 > Senior secondary school 2.0 (1.0 – 4.1) 1.9 (1.1 – 3.3)
Partner HIV status
 No 1.0 1.0
 Yes 1.2 (0.6 – 2.8) 1.3 (0.6 – 3.0)
 Don’t know 1.3 (0.9 – 1.7) 1.5 (1.1 – 2.0)
Social economic status of the alters relative to the ego
 Lower 1.0 1.0
 The same 1.9 (1.2 – 3.0) 1.8 (1.1 – 3.0)
 Higher 1.4 (0.9 – 2.1) 1.7 (1.1 – 2.8)
Cross level differences/Interaction
Age difference
 Same age 1.0
 Ego older 1.6 (0.9 –3.0)
 Alter older 1.3 (0.7 –2.4)
Network size*social support
 Smaller network size and social support 1.0
 Large network size and social support 1.4 (1.0 – 2.2)
Site
 Lagos 1.0
 Abuja 2.2 (1.1 – 4.4)
Model Fit
 AIC 1463.4 1342.7 1225.7
 − 2LL 1461.4 1340.7 1223.7
p Value likelihood ratio test Model 2 vs. 1: p < 0.01 Model 3 vs. 2: p < 0.01

Abbreviations: aOR, adjusted Odds ratio; CI, Confidence Intervals.

HIV, Human immune deficiency Virus;

Bolded denotes p < 0.05

Alter characteristics and ART Initiation (Model2)

Compared to participants whose sex partners have less than senior secondary school education, those whose partners have more than senior secondary school (aOR = 2.0; 95% CI, 1.0 – 4.1) were significantly associated with increased odds of ART Initiation. The odds of participants initiating ART is higher when alters and ego have similar level of social economic status compared to when alters have lower social economic status relative to ego (aOR = 1.9; 95% CI, 1.2 – 3.0).

Cross level differences/Interactions and ART initiation (Model 3)

Participants with larger network size and stronger social support had increased odds of ART initiation compared to those with smaller network size and weaker social support (aOR = 1.4; 95% CI, 1.0 – 2.2).

Ego characteristics and viral suppression (Model 1)

Multivariate associations of ego and alter characteristics and six months viral suppression are presented in table 4. Younger age, 20 – 29 vs. ≥ 30 years (aOR =0.3; 95% CI, 0.1 – 0.8) and having a large network size 11–20 vs. 0–10 (aOR = 0.6; 95% CI, 0.3 –0.9) were associated with decreased odds of viral suppression. Moslems (aOR = 1.8; 95% CI, 1.0 – 3.1), those who disclosed MSM status to health care workers (aOR = 1.8; 95% CI, 1.1 – 3.2) and participants with stronger social support from other friends within their networks (aOR = 2.8; 95% CI, 1.9 – 4.2) had increased odds of viral suppression.

Table 4.

Association Between Individual and Network Characteristics and Six Months Viral Suppression Among MSM at HIV Prevention Clinics, Abuja and Lagos, Nigeria 2013 – 2017: Multilevel Logistic Regression Models Using Paired Data

Characteristics Model1 Model2 Model3



aOR 95% CI aOR 95% CI aOR 95% CI
Ego factors
Age
 ≤ 19 years 0.7 (0.3 – 1.5) 0.6 (0.3 – 1.7) 0.7 (0.2 – 2.1)
 20 – 29 years 0.3 (0.1 – 0.8) 0.3 (0.1 – 0.9) 0.2 (0.0 – 0.9)
 ≥ 30 years 1.0 1.0 1.0
Education
 < Senior secondary school 1.0 1.0 1.0
 Senior secondary school 0.8 (0.3 – 1.9) 0.8 (0.3 – 3.3) 0.6 (0.2 – 2.5)
 > Senior secondary school 0.6 (0.2 – 1.4) 0.7 (0.2 –2.4) 0.5 (0.1 – 1.8)
Religion
 Christian 1.0 1.0 1.0
 Moslem 1.8 (1.0 – 3.1) 3.4 (1.5 – 7.8) 2.4 (1.0 – 5.9)
Participate in HIV prevention meetings
 No 1.0 1.0 1.0
 Yes 1.5 (0.9 – 2.5) 1.9 (0.9 – 2.9) 2.2 (1.1 – 4.2)
Network size
 1 – 10 1.0 1.0 1.0
 11 – 20 0.6 (0.3 – 0.9) 0.4 (0.2 – 0.7) 0.7 (0.4 – 1.9)
 21 – 30 1.9 (0.7 – 5.0) 1.1 (0.3 – 3.6) 0.9 (0.2 – 3.8)
 31+ 0.7 (0.3 – 1.3) 0.2 (0.1 – 0.4) 0.4 (0.2 – 1.0)
Disclosed MSM to family
 No 1.0 1.0 1.0
 Yes 1.5 (0.8 – 3.0) 1.3 (0.6 – 2.8) 2.1 (0.9 – 5.1)
Disclosed MSM to health care workers
 No 1.0 1.0 1.0
 Yes 1.8 (1.1 – 3.2) 2.0 (1.0 – 4.3) 2.0 (1.0 – 4.2)
Social support score
 < Median 1.0 1.0 1.0
 ≥ Median 2.8 (1.9 – 4.2) 2.9 (1.5 – 5.8) 5.8 (2.6 – 13.2)
Alter factors
Partner HIV status
 No 1.0 1.0
 Yes 2.7 (0.9 – 8.1) 2.5 (0.5 – 14.0)
 Don’t know
Social economic status of the alters relative to the ego
 Lower 1.0 1.0
 The same 2.3 (1.1 – 4.5) 3.4 (1.4 – 8.0)
 Higher 1.1 (0.1 – 9.6) 1.4 (0.7 – 3.5)
Cross level differences/Interaction
Age difference
 Same age 1.0
 Ego older 0.4 (0.1 – 1.8)
 Alter older 0.4 (0.1 – 1.7)
Network size*social support
 Smaller network size and social  support 1.0
 Large network size and social support 3.0 (1.1 – 8.2)
AIC 823.1 614.2 553.6
− 2LL 823.1 612.2 551.6
p Value likelihood ratio test Model 2 vs. 1: p < 0.01 Model 3 vs. 2: p < 0.01

Abbreviations: aOR, adjusted Odds ratio; CI, Confidence Intervals

Bolded denotes p < 0.05

Alter characteristics viral suppression (Model 2)

The odds of participants achieving viral suppression is higher when alters and ego have similar level of social economic status compared to when alters have lower social economic status relative to ego (aOR =2.3; 95% CI, 1.1 – 4.5).

Cross level differences/Interactions and viral suppression (Model 3)

Participants with larger network size and stronger social support had increased odds of achieving viral suppression compared to those with smaller size density and weaker social support (aOR = 3.0; 95% CI, 1.1 – 8.2).

Discussion

The provision of MSM friendly health care services by integrating universal coverage of ART into community-based clinics facilitated the achievement of moderate levels of the HIV Care Continuum outcomes in this population. Approximately 78% of the study participants tested for HIV, and of those infected, slightly over half initiated ART. These proportions are far less than the UN targets suggesting more work is needed in order to achieve the UN goals. Achieving moderate level of viral suppression at 6-months of follow up is promising, suggesting high level of medication adherence among those retained in care. Our findings also indicate having stronger social network support is an important factor in succeeding in all points in the HIV Care Continuum pathway.

There is consistent evidence that social networks exert strong social influence on the engagement of network members in the HIV Care Continuum 2123. In addition to stigma affecting HIV infection, MSM often are affected by stigma related to sexual practices and sexual orientation 24,25. Stigma is a fundamental barrier to engagement into HIV care and negatively impacts patient outcomes 11,12. Social support systems reduce stigma, improve individual acceptability of HIV infection, as well as successful navigation throughout the HIV Care Continuum pathway 23,26. Instrumental support such as provision of financial assistance, emotional support such as comfort, and informational support such as advice on dealing with difficult situation may have facilitated the uptake of HIV testing, initiation of ART and eventual viral suppression in this cohort. Previous research among Ghanaian MSM demonstrated that family and friend’s social support and positive experiences at the health care setting facilitated HIV care27. We observed an interaction between network size and social support in that, those with both a larger network and higher social support were more likely to initiate ART and achieve viral suppression compared to participants with smaller network size and social support. The larger the network size the higher the likelihood of receiving social support to positively influence HIV care outcomes. Structured social support systems tailored to key population (KP) are critical to engaging MSM into care, improving health and prevention of HIV infection.

Younger MSM were less likely to test for HIV compared to older participants. Globally, adolescents and young MSM are at increased risk for HIV due to the many developmental, psychological, social, and structural transitions that converge in this period of the lifespan28. The starting point for all interventions must still be HIV counseling and testing. Innovative ways to promote testing have shown promise including incentivization, self-testing, and mobile health 29,30 but more evaluation to show effectiveness in this age group is required. Comparison of those who tested and those who did not test demonstrated that a higher proportion of those who did not test 36% had less than senior secondary school education compared to 12% for those who tested, suggesting the importance of education on HIV testing. Furthermore, among those who did not test for HIV at study entry and never sought HIV testing before, 34% were 19 years or younger compared to 6% who were 30 years or older, emphasizing the need to improve HIV testing and engagement in care among young MSM.

These analyses demonstrated that a fair proportion of participants did not initiate treatment. As previously documented, the shock of new HIV diagnosis, fear of being discriminated by the peer or family 18,31 may explain the moderate rate of ART initiation. Because of marginalization and high mobility, approximately one-third of HIV newly diagnosed MSM who did not initiate ART in this study moved to a different location. Interventions to alleviate stigma and strengthening of drop-in centers with culturally competent health care providers to better serve mobile KP is critical.

The achieved moderate level of viral suppression in this cohort of MSM suggests that provision of MSM friendly clinical services is effective. Although viral load suppression rate among MSM is lacking in Nigeria, prior data among heterosexual individuals showed suppression rates that are comparable to our data 32,33. Younger MSM had a decreased odds of achieving viral suppression. Successful viral suppression requires optimal adherence to ART. Prior data on MSM showed levels of ART adherence ranging from 16 to 74% with younger MSM having lower adherence rates 34,35. Interventions to improve adherence among young MSM such as treatment support and reminders from network members 36 are essential in order to improve sustained viral suppression.

Religion was a significant predictor at all points of HIV care cascade. Compared to Christians, Muslims had decreased odds of HIV testing and ART initiation. Prior research showed overwhelming opposition of homosexuality by Islamic society37, which could explain the low uptake of HIV testing and treatment among Muslim gay men in this study. Although Muslim lag behind Christians in HIV testing and treatment, a few of those engaged in care tended to have better viral suppression outcome, indicating that with better support, good health care outcomes could be achieved among Muslim gay men.

The main strength of these analyses is the characterization of HIV Care Continuum using a well-established cohort of MSM as opposed to the use of cross sectional data. However, our study is not without limitations. Alter sexual behaviors data were reported by the ego, reporting bias cannot be eliminated although we assessed the confidence in egos’ recall on information about alters. In addition, lost to follow is high. Since participants who were lost to follow up tended to have lower level of education and less exposure to HIV education, our effects size on HIV care cascade outcomes might be underestimated. It is also important to acknowledge that the time period following HIV diagnosis may entail restructuring of social support networks, and these dynamics may vary. Our ongoing research will establish a baseline understanding of these dynamics and patterns.

Conclusions

In conclusion, this report represents a rigorous multi-level characterization of the HIV Care Continuum for MSM from a sub-Saharan Africa, where information have been limited thus far. Our finding underscores that, within the context of achieving epidemic control through universal coverage of ART, MSM still lag behind other men and women of similar reproductive age. However, integration of HIV prevention, HIV Counselling and Testing services and universal coverage of ART into a community-based setting is necessary and critical in achieving high levels of HIV Care Continuum outcomes. Interventions that harness the social support network, especially of the young MSM to improve HIV care outcomes, offer promise for long-term efficacy for the 90-90-90 targets.

Acknowledgments

Source of funding: This work was supported by a cooperative agreement between the Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., and the U.S. Department of Defense [W81XWH-11-2-0174]; the National Institutes of Health [R01 MH099001, R01 AI120913]; Fogarty AITRP [D43TW01041]; and the President’s Emergency Plan for AIDS Relief through a cooperative agreement between the Department of Health and Human Services/Centers for Disease Control and Prevention, Global AIDS Program, and the Institute for Human Virology-Nigeria [U2G IPS000651].

The TRUST/RV368 Study Group includes Principal Investigators: Manhattan Charurat (IHV, University of Maryland, Baltimore, MD, USA), Julie Ake (MHRP, Walter Reed Army Institute of Research, Silver Spring, MD, USA); Co-Investigators: Sylvia Adebajo, Stefan Baral, Erik Billings, Trevor Crowell, George Eluwa, Abiola Fasina, Charlotte Gaydos, Sosthenes Ketende, Afoke Kokogho, Hongjie Liu, Jennifer Malia, Nelson Michael, Nicaise Ndembi, Jean Njab, Rebecca Nowak, Oluwasolape Olawore, Zahra Parker, Sheila Peel, Habib Ramadhani, Merlin Robb, Cristina Rodriguez-Hart, Eric Sanders-Buell, Sodsai Tovanabutra; Institutions: Institute of Human Virology at the University of Maryland School of Medicine (IHV-UMB), University of Maryland School of Public Health (UMD SPH), Johns Hopkins Bloomberg School of Public Health (JHSPH), Johns Hopkins University School of Medicine (JHUSOM), U.S. Military HIV Research Program (MHRP), Walter Reed Army Institute of Research (WRAIR), Henry M. Jackson Foundation for the Advancement of Military Medicine (HJF), Henry M. Jackson Foundation Medical Research International (HJFMRI), Institute of Human Virology Nigeria (IHVN), International Centre for Advocacy for the Right to Health (ICARH), The Initiative for Equal Rights (TIERS), Population Council (Pop Council), Nigeria.

Footnotes

Conflicts of interest: No conflicts of interest to report

Disclaimer: The views expressed are those of the authors and should not be construed to represent the positions of the U.S. Army, the Department of Defense, or the Department of Health and Human Services. The investigators have adhered to the policies for protection of human subjects as prescribed in AR-70.

References

  • 1.UNAIDS 90-90-90. An ambitious treatment target to help end the AIDS epidemic. 2014 Oct; Available at: http://www.unaids.org/sites/default/files/media_asset/90-90-90_en_0.pdf.
  • 2.McFall AM, Mehta SH, Srikrishnan AK, et al. Getting to 90: linkage to HIV care among men who have sex with men and people who inject drugs in India. AIDS Care. 2016;28(10):1230–1239. doi: 10.1080/09540121.2016.1168915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Park JN, Papworth E, Billong SC, et al. Correlates of prior HIV testing among men who have sex with men in Cameroon: a cross-sectional analysis. BMC Public Health. 2014;14:1220. doi: 10.1186/1471-2458-14-1220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Mikolajczak J, Hospers HJ, Kok G. Reasons for not taking an HIV-test among untested men who have sex with men: an Internet study. AIDS Behav. 2006;10(4):431–435. doi: 10.1007/s10461-006-9068-8. [DOI] [PubMed] [Google Scholar]
  • 5.Horth RZ, Cummings B, Young PW, et al. Correlates of HIV Testing Among Men Who have Sex with Men in Three Urban Areas of Mozambique: Missed Opportunities for Prevention. AIDS Behav. 2015;19(11):1978–1989. doi: 10.1007/s10461-015-1044-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Hightow-Weidman L, LeGrand S, Choi SK, Egger J, Hurt CB, Muessig KE. Exploring the HIV continuum of care among young black MSM. PLoS One. 2017;12(6) doi: 10.1371/journal.pone.0179688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Tanner Z, Lachowsky N, Ding E, et al. Predictors of viral suppression and rebound among HIV-positive men who have sex with men in a large multi-site Canadian cohort. BMC Infect Dis. 2016:16. doi: 10.1186/s12879-016-1926-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Fuqua V, Chen YH, Packer T, et al. Using social networks to reach Black MSM for HIV testing and linkage to care. AIDS Behav. 2012;16(2):256–265. doi: 10.1007/s10461-011-9918-x. [DOI] [PubMed] [Google Scholar]
  • 9.Shangani S, Escudero D, Kirwa K, Harrison A, Marshall B, Operario D. Effectiveness of peer-led interventions to increase HIV testing among men who have sex with men: a systematic review and meta-analysis. AIDS Care. 2017;29(8):1003–1013. doi: 10.1080/09540121.2017.1282105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Cange CW, LeBreton M, Billong S, et al. Influence of stigma and homophobia on mental health and on the uptake of HIV/sexually transmissible infection services for Cameroonian men who have sex with men. Sex Health. 2015;12(4):315–321. doi: 10.1071/SH15001. [DOI] [PubMed] [Google Scholar]
  • 11.Schwartz SR, Nowak RG, Orazulike I, et al. The immediate eff ect of the Same-Sex Marriage Prohibition Act on stigma, discrimination, and engagement on HIV prevention and treatment services in men who have sex with men in Nigeria: analysis of prospective data from the TRUST cohort. Lancet HIV. 2015;2(7):e299–306. doi: 10.1016/S2352-3018(15)00078-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Risher K, Adams D, Sithole B, et al. Sexual stigma and discrimination as barriers to seeking appropriate healthcare among men who have sex with men in Swaziland. J Int AIDS Soc. 2013;16(3 Suppl 2):18715. doi: 10.7448/IAS.16.3.18715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Keshinro B, Crowell TA, Nowak RG, et al. High prevalence of HIV, chlamydia and gonorrhoea among men who have sex with men and transgender women attending trusted community centres in Abuja and Lagos, Nigeria. J Int AIDS Soc. 2016;19(1):21270. doi: 10.7448/IAS.19.1.21270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Bashorun A, Nguku P, Kawu I, et al. A description of HIV prevalence trends in Nigeria from 2001 to 2010: what is the progress, where is the problem? Pan Afr Med J. 2014;18(Suppl 1):3. doi: 10.11694/pamj.supp.2014.18.1.4608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Ramadhani HO, Liu H, Nowak RG, et al. Sexual partner characteristics and incident rectal Neisseria gonorrhoeae and Chlamydia trachomatis infections among gay men and other men who have sex with men (MSM): a prospective cohort in Abuja and Lagos, Nigeria. Sex Transm Infect. 2017;93(5):348–355. doi: 10.1136/sextrans-2016-052798. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Charurat ME, Emmanuel B, Akolo C, et al. Uptake of treatment as prevention for HIV and continuum of care among HIV-positive men who have sex with men in Nigeria. J Acquir Immune Defic Syndr. 2015;68(Suppl 2):S114–123. doi: 10.1097/QAI.0000000000000439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Baral SD, Ketende S, Schwartz S, et al. Evaluating respondent-driven sampling as an implementation tool for universal coverage of antiretroviral studies among men who have sex with men living with HIV. Journal of acquired immune deficiency syndromes (1999) 2015;68(Suppl 2):S107–113. doi: 10.1097/QAI.0000000000000438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Obi SN, Ifebunandu NA. Consequences of HIV testing without consent. Int J STD AIDS. 2006;17(2):93–96. doi: 10.1258/095646206775455649. [DOI] [PubMed] [Google Scholar]
  • 19.WHO. Consolidated guidelines on the use of antiretroviral drugs for treating and preventing HIV infection. Recommendations for a public health approach. (2) 2016 Available at: http://apps.who.int/iris/bitstream/10665/208825/1/9789241549684_eng.pdf?ua=1. [PubMed]
  • 20.Guida J, Hu L, Liu H. The Impact of Occupational Stigma on the Social Networks of Older Female Sex Workers: Results from a Three-Site Egocentric Network Study in China. AIDS Patient Care STDS. 2016;30(1):1–3. doi: 10.1089/apc.2015.0137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Scott HM, Pollack L, Rebchook GM, Huebner DM, Peterson J, Kegeles SM. Peer social support is associated with recent HIV testing among young black men who have sex with men. AIDS Behav. 2014;18(5):913–920. doi: 10.1007/s10461-013-0608-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Liu Y, Osborn CY, Qian HZ, et al. Barriers and Facilitators of Linkage to and Engagement in HIV Care Among HIV-Positive Men Who Have Sex with Men in China: A Qualitative Study. AIDS Patient Care STDS. 2016;30(2):70–77. doi: 10.1089/apc.2015.0296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Friedman MR, Coulter RW, Silvestre AJ, et al. Someone to count on: social support as an effect modifier of viral load suppression in a prospective cohort study. AIDS Care. 2017;29(4):469–480. doi: 10.1080/09540121.2016.1211614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Crowell TA, Keshinro B, Baral SD, et al. Stigma, access to healthcare, and HIV risks among men who sell sex to men in Nigeria. J Int AIDS Soc. 2017;20(1):21489. doi: 10.7448/IAS.20.01.21489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Rodriguez-Hart C, Nowak RG, Musci R, et al. Pathways from sexual stigma to incident HIV and sexually transmitted infections among Nigerian men who have sex with men. AIDS. 2017 doi: 10.1097/QAD.0000000000001637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Daniel Kelly J, Hartman C, Graham J, Kallen MP, Giordano T. Social Support as a Predictor of Early Diagnosis, Linkage, Retention, and Adherence to HIV Care: Results From The Steps Study. 2014;25 doi: 10.1016/j.jana.2013.12.002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Ogunbajo A, Kershaw T, Kushwaha S, Boakye F, Wallace-Atiapah ND, Nelson LE. Barriers, Motivators, and Facilitators to Engagement in HIV Care Among HIV-Infected Ghanaian Men Who have Sex with Men (MSM) AIDS Behav. 2017 doi: 10.1007/s10461-017-1806-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Mofenson LM, Cotton MF. The challenges of success: adolescents with perinatal HIV infection. J Int AIDS Soc. 2013;16:18650. doi: 10.7448/IAS.16.1.18650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Lee R, Cui RR, Muessig KE, Thirumurthy H, Tucker JD. Incentivizing HIV/STI testing: a systematic review of the literature. AIDS Behav. 2014;18(5):905–912. doi: 10.1007/s10461-013-0588-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Ren XL, Wu ZY, Mi GD, McGoogan J, Rou KM, Zhao Y. Uptake of HIV Self-testing among Men Who have Sex with Men in Beijing, China: a Cross-sectional Study. Biomed Environ Sci. 2017;30(6):407–417. doi: 10.3967/bes2017.054. [DOI] [PubMed] [Google Scholar]
  • 31.UNAIDS. HIV and AIDS-related stigmatization, discrimination and denial: forms, contexts and determinants. Research studies from Uganda and India. 2000 Jun; Available at: http://data.unaids.org/publications/irc-pub01/jc316-uganda-india_en.pdf.
  • 32.Babajide K, Ojor A, Kene T, et al. Virological Suppression and Patterns of Resistance Amongst Patients on Antiretroviral Therapy at 4 Nigerian Military Hospitals. Curr HIV Res. 2017 doi: 10.2174/1570162X15666170517103704. [DOI] [PubMed] [Google Scholar]
  • 33.Ugbena R, Aberle-Grasse J, Diallo K, et al. Virological response and HIV drug resistance 12 months after antiretroviral therapy initiation at 2 clinics in Nigeria. Clin Infect Dis. 2012;54(Suppl 4):S375–380. doi: 10.1093/cid/cir1064. [DOI] [PubMed] [Google Scholar]
  • 34.Risher K, Mayer KH, Beyrer C. HIV treatment cascade in MSM, people who inject drugs, and sex workers. Curr Opin HIV AIDS. 2015;10(6):420–429. doi: 10.1097/COH.0000000000000200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Zanoni BC, Mayer KH. The adolescent and young adult HIV cascade of care in the United States: exaggerated health disparities. AIDS Patient Care STDS. 2014;28(3):128–135. doi: 10.1089/apc.2013.0345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Holloway IW, Tan D, Dunlap SL, Palmer L, Beougher S, Cederbaum JA. Network support, technology use, depression, and ART adherence among HIV-positive MSM of color. AIDS Care. 2017;29(9):1153–1161. doi: 10.1080/09540121.2017.1325435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Hamdi N, Lachheb M, Anderson E. Muslim gay men: identity conflict and politics in a Muslim majority nation. Br J Sociol. 2017 doi: 10.1111/1468-4446.12334. [DOI] [PubMed] [Google Scholar]

RESOURCES