https://orcid.org/0000-0002-6447-8586
Figures
Abstract
Background
Excessive alcohol intake has been associated with poor adherence to antiretroviral therapy (ART). The impact of alcohol on viral suppression is particularly important among groups at high risk of HIV transmission, such as female sex workers (FSWs). Few studies have directly evaluated the association between alcohol use and HIV viral load. We hypothesized that hazardous or harmful alcohol use is associated with detectable plasma viral load among HIV-positive FSWs.
Methods
A prospective cohort study was conducted among HIV-positive FSWs in Mombasa, Kenya. Hazardous or harmful alcohol use was assessed yearly and defined as an Alcohol Use Disorders Identification Test (AUDIT) score ≥7. Detectable viral load was assessed every six months and defined as ≥180 c/mL. Adherence measures were collected monthly and included late ART refill (>48 hours) and self-reported adherence, using both a validated self-rating scale of ability to take medication and visual analog scale (VAS) of ART use in the last month. Generalized estimating equations were used to estimate adjusted relative risks (aRR) and 95% confidence intervals (CI).
Results
This analysis included 366 participants followed monthly between October 2012 and March 2018. At baseline, AUDIT scores indicated hazardous alcohol use (AUDIT 7–15) in 14.3%, harmful alcohol use (AUDIT 16–19) in 1.4%, and alcohol dependency (AUDIT ≥20) in 1.4% of participants. After adjusting for potential confounders, a combined exposure including hazardous, harmful, and dependent alcohol use was not associated with detectable viral load (aRR 1.10, 95%CI 0.63–1.92) or late ART refill (aRR 1.13, 95%CI 0.82–1.56), but was associated with lower self-rated ability to take medication (aRR 2.38, 95%CI 1.42–3.99) and a lower rate of self-reported perfect ART adherence by VAS (aRR 2.62, 95%CI 1.84–3.71).
Conclusions
In this FSW cohort, while participants reporting hazardous, harmful, or dependent alcohol use were not more likely to have a detectable viral load, they were more likely to report lower ART adherence. These results suggest that interventions targeting alcohol use among this population of FSWs may not have a large impact on viral suppression.
Citation: Long JE, Richardson BA, Wanje G, Wilson KS, Shafi J, Mandaliya K, et al. (2020) Alcohol use and viral suppression in HIV-positive Kenyan female sex workers on antiretroviral therapy. PLoS ONE 15(11): e0242817. https://doi.org/10.1371/journal.pone.0242817
Editor: Joel Msafiri Francis, University of the Witwatersrand, SOUTH AFRICA
Received: June 19, 2020; Accepted: November 10, 2020; Published: November 24, 2020
Copyright: © 2020 Long et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: This study was conducted with approval from the Kenyatta National Hospital - University of Nairobi Ethics and Research Committee (KNH-UON ERC), which requires that we release data from Kenyan studies (including de-identified data) only after they have provided their written approval for additional analyses. As such, data for this study will be available from the authors upon request, with written approval for the proposed analysis from the KNH/UON ERC. Their application forms and guidelines can be accessed at http://erc.uonbi.ac.ke/. To request these data, please contact KRTC Administrator at kenyares@uw.edu.
Funding: This work was supported by the National Institutes of Health (R01HD072617) awarded to RSM (https://www.nih.gov/). Infrastructure and logistics support for the Mombasa research site was provided by the University of Washington’s Center for AIDS Research (CFAR), an NIH funded program (P30 AI027757) which is supported by the following centers: NIAID, NCI, NIMH, NIDA, NICHD, NHLBI, NCCAM. RSM receives funding for mentoring through National Institute of Child Health and Human Development K24 HD88229 (https://www.nichd.nih.gov/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: I have read the journal’s policy and the authors of this manuscript have the following competing interests: RSM receives research funding for a study of high-risk HPV collection methods, paid to the University of Washington, from Hologic Corporation. This does not alter our adherence to PLOS ONE policies on sharing data and materials. All other authors declared that no competing interests exist.
Introduction
Suppression of HIV viral replication is critical to maintain health and prevent HIV transmission. Viral suppression requires adherence to daily antiretroviral therapy (ART), which can be difficult due to multiple psychosocial and structural barriers such as fear of disclosure of HIV status, stigma, and difficulty in following a daily regimen [1]. Studies in high- and low-income countries have demonstrated that alcohol use is associated with poor ART adherence [1–4]. Fewer studies have examined the association between alcohol use and viral suppression, particularly in low-income settings, and these provide conflicting results [5–11]. With modern ART regimens, adherence >80% is sufficient to maintain viral suppression [12]. In this context, it is important to examine not only the association between alcohol use and adherence, but also the relationship between alcohol and viral suppression.
Female sex workers (FSWs) in sub-Saharan Africa are disproportionately affected by both HIV and alcohol use [7]. Based on data from the National AIDS and STI Control Programme, 29% of FSWs in Kenya are living with HIV [13]. In addition, HIV-seropositive FSWs face greater barriers to ART adherence compared to those who don’t sell sex, with evidence suggesting that ART adherence is lower among FSWs than non-sex workers in sub-Saharan Africa [7, 14–16]. A systematic review and meta-analysis reported the prevalence of current use of ART was 23% among FSWs living with HIV in Kenya [15]. Sex work is often conducted in bars and nightclubs, and FSWs may use alcohol to cope with the stress of sex work [7, 17]. Understanding and addressing barriers to ART adherence in this key population is important for achieving the 95-95-95 target of having 95% of those on ART virally suppressed by 2030 [18].
This prospective cohort study tested the hypothesis that alcohol use is associated with a lower likelihood of viral suppression in FSWs receiving ART.
Methods
Population and procedures
Data were collected from HIV-positive FSWs in Mombasa, Kenya. Detailed methods have been published [19]. Briefly, women were recruited using community outreach in FSW workplaces. Eligibility criteria included age ≥16 years, laboratory confirmed HIV infection, receiving ART, and reporting exchanging sex for money or in-kind payment.
All participants provided written informed consent, then completed a baseline standardized face-to-face interview. Self-reported data were collected on socio-demographics, reproductive and sexual health, and history of violence. Depression was assessed using the Patient Health Questionnaire-9 (PHQ-9) [18]. Blood samples were collected for viral load testing and CD4 counts. A physical examination including pelvic examination with sample collection for STI testing was performed.
Alcohol use was measured at baseline through the Alcohol Use Disorder Identification Test (AUDIT), an internationally validated tool to screen for alcohol use in the prior 12 months [20, 21]. Among women, AUDIT scores of 0–6 indicate abstinence or non-hazardous alcohol use, 7–15 hazardous alcohol use (drinking that increases risk of future harm), 16–19 harmful alcohol use (drinking that impairs physical, mental, or social health), and 20–40 alcohol dependency [21]. In this population, few women had AUDIT scores in the harmful or dependent range, so scores were dichotomized, comparing scores of 0–6 to scores ≥7. Antiretroviral therapy adherence was evaluated through three measures. First, self-reported ability to take ART was assessed using a validated 5-point self-rating scale of excellent, good, fair, poor, or very poor [22]. For analysis, this was transformed to a binary score of “excellent” or “less than excellent”. Second, women were asked to mark a visual analog scale (VAS) representing the percent of ART doses taken in the past month. In this population, the majority of VAS responses indicated 100% of doses taken, so this variable was dicohtomized to compare 100% versus <100% adherence [23, 24]. Third, pharmacy data were used to identify late ART refills, defined as refills occurring >48 hours after medications from the prior refill would have run out, assuming perfect adherence [25].
Women were asked to return for monthly follow-up visits to collect data on ART adherence. Every three months CD4 counts were repeated. Participants completed the PHQ-9 and viral load testing every six months. AUDIT score and history of violence were assessed annually. Participants were compensated 250 Kenyan shillings (approximately USD $2.50) for travel at each visit. Ethics approval was obtained from the Kenyatta National Hospital Ethics and Research Committee and the University of Washington Human Subjects Research Committee.
Laboratory procedures
Detectable plasma viral load was measured as plasma HIV RNA ≥180 copies/milliliter (Hologic, San Diego, CA). This cut point was higher than the lower limit of detection for the assay (<30 c/mL) because some 100 mL samples had to be diluted 6-fold, to a final volume of 600 mL before testing. Only viral loads collected after ≥3 months of ART use were included [26]. Testing for STIs was performed using the Hologic Aptima detection system (Hologic, San Diego, CA). Vaginal swabs were tested for prostate-specific antigen (PSA) using ABAcard p30 (Abacus Diagnostics, West Hills, CA). Positive PSA indicates semen exposure in the past 24–48 hours [27]. The BD FACSCount (BD Biosciences, San Jose, CA) was used to measure CD4+ T-cell count.
Statistical analysis
The AUDIT was administered annually, and scores were carried forward for analyses until the next assessment. To account for repeated measures from individual participants, associations between AUDIT score ≥7 and viral suppression (primary outcome) and ART adherence (secondary outcomes) were evaluated using generalized estimated equations with log link, Poisson family distribution, independence working correlation structure, and robust standard errors. After estimating unadjusted associations, a multivariable model was built using a forward manual selection process. All models were adjusted for age based on consistent prior findings of associations with alcohol use and adherence [28, 29]. Additional covariates including PHQ-9 score, intimate partner violence, and sexual behavior, were selected as potential confounders based on published associations [30–32]. These variables were modelled as time-varying in analyses. Variables were retained if they shifted the effect estimate for the association between AUDIT score ≥7 and the outcome by ≥10%. Sensitivity analyses were conducted to fully fit each model with all covariates found to be associated with the outcome examined in that model.
Collinearity between AUDIT score ≥7 and additional variables was evaluated by calculating change in the standard error of the model when each variable was added. When collinearity was suspected (>10% change in standard error when variable is added to the model), correlation between the variables was evaluated using Spearman’s rank correlation coefficient; if a variable was highly correlated (r ≥0.6) it would be removed from analysis. To assess whether the effect of alcohol on viral suppression differed by age group, regression analyses were conducted including an interaction term between AUDIT score ≥7 and age category (20–29, 30–39, 40–49, and ≥50 years of age), then were repeated stratifying by age. All analyses were conducted in Stata version 15.1 (College Station, TX, USA, 2017).
Results
Sample characteristics
There were 481 FSWs enrolled between October 2012 and April 2017, with follow-up through March 2018. Of the enrolled women, 115 were excluded from this analysis. Seventy had no plasma HIV RNA result after >3 months on ART, 44 were not on ART, and one had no AUDIT score. The remaining 366 participants contributed a total of 11,482 visits (1,131 person-years of follow-up). The median number of visits per participant was 48 (interquartile range [IQR] 39–59).
Baseline characteristics are presented in Table 1. The median age was 40 years (IQR 34, 44). Half the cohort reported a regular partner who was not a client in the prior three months (N = 191, 52.3%). A quarter of participants reported either mild (N = 67, 18.3%) or moderate to severe (N = 30, 8.2%) depressive symptoms. Intimate partner violence in the previous 12 months was reported by 20.2% (N = 74). AUDIT scores at baseline indicated hazardous alcohol use (score 7–15) in 14.3% (N = 52) of participants, harmful use (16–19) in 1.4% (N = 5), and alcohol dependency in 1.4% (N = 5). Of the 207 women who had been prescribed ART for at least three months and had baseline viral load measured, 15.9% (N = 33) were detectable.
Alcohol use and detectable viral load
AUDIT score was collected at 1,066 visits, of which 100 (9.4%) were scores ≥7. A total of 1,925 visits included viral load testing after ≥3 months on ART. Of these, 291 (15.1%) had a detectable viral load. In univariate analyses, AUDIT score ≥7 was associated with a 1.59-fold higher relative risk of having a detectable viral load (95% confidence interval [CI] 0.93–2.69) compared to AUDIT score <7 (p = 0.084) (Table 2). This association was attenuated when adjusted for age (adjusted relative risk [aRR] 1.10, 95%CI 0.63–1.92, p = 0.74). Other variables, including PHQ-9 score, history of intimate partner violence, and indicators of sexual behavior had statistically significant associations with AUDIT score ≥7 but were not retained in the final multivariable model after stepwise regression was performed.
Alcohol use and adherence
Participants refilled ART at 9,751 visits, of which 1,968 (20.2%) were refilled late. In univariate analysis, AUDIT score ≥7 was associated with late refill (RR 1.38, 95%CI 0.99–1.93, p = 0.056). This association was attenuated in the multivariable model adjusted for age (aRR 1.13, 95%CI 0.82–1.56, p = 0.442).
Participants completed the ART adherence self-rating scale at 9,780 visits, during which 371 (3.2%) indicated less than excellent perceived ability to take ART. In univariate analysis, compared to visits with AUDIT score <7, AUDIT score ≥7 was significantly associated with a 3.68-fold (95%CI 2.48–5.44) higher relative risk of reporting less than excellent ability to take ART. This association was somewhat attenuated (aRR 2.42, 95%CI 1.48–3.92, p<0.001) but remained highly significant in adjusted analyses that included age and number of sex acts in the last week (a proxy for current level of engagement in sex work).
The VAS of ART adherence was conducted at 10,085 visits, of which 613 (6.1%) indicated <100% adherence. AUDIT score ≥7 was significantly associated with a 3.44-fold (95%CI 2.44–4.85, p<0.001) higher risk of reporting <100% adherence. Similar to the self-rating scale, this association was attenuated (aRR 2.41, 95%CI 1.71–3.38, p<0.001) but remained highly significant with adjustment for age. For all outcomes, sensitivity analyses that fully fit each model with all variables associated with the outcome did not substantially change the inference of the results. These data are provided as S1 File.
Age and alcohol use
Age was the only variable for which there was evidence of collinearity with alcohol use, resulting in a >10% increase in the standard error when added to each model. However, the correlation between age and AUDIT score was weak (Spearman’s rank correlation coefficient ρ = -0.26, p-value <0.001), so it was retained in the primary models. Given the large attenuating effect of age on the association between alcohol use and detectable viral load in these analyses, as well as this evidence of collinearity, the association between AUDIT score ≥7 and detectable viral load was further evaluated through stratification by age group. The percentage of visits with AUDIT score ≥7 and detectable viral load decreased dramatically with increasing age (Fig 1). No statistically significant evidence of effect modification was found when examining interaction between AUDIT score ≥7 and age category, suggesting that the relationship between AUDIT score and detectable viral load did not significantly differ by age group (all p-values for interaction ≥0.10).
This figure displays the percent of all study visits in which the AUDIT score was ≥7 and viral load was detectable (plasma HIV RNA load ≥180 copies/milliliter), stratified by age group. During the analysis period, 579 study visits were conducted with participants age 20–29 years, 3,387 with those age 30–39, 5,722 with those age 40–49, and 1,794 with those age 50–61 years.
To further explore the effects of age, the primary analyses were repeated without inclusion of age as a covariate, and instead stratifying by age. Due to sparse data in age categories, age was dichotomized at the median (age 42 years). These results did not differ substantially from the primary findings (Table 3). An AUDIT score ≥7 was not significantly associated with detectable viral load in either age group (Age 20–41: RR 1.12, 95%CI 0.61–2.08, p = 0.706; Age 42–61: RR 1.61 95%CI 0.58–4.46, p = 0.361).
Discussion
In this longitudinal study of HIV-seropositive FSWs receiving ART, the overall prevalence of hazardous, harmful, or dependent alcohol use was low and was not associated with having a detectable viral load. Both alcohol use and detectable viral load decreased with older age, but the relationship between alcohol use and viral load was similar across age groups. Interestingly, while self-report of lower adherence using two validated methods was uncommon, women with hazardous, harmful, or dependent alcohol use were significantly more likely to report lower ART adherence using both a validated adherence self-rating scale and VAS.
The prevalence of hazardous, harmful, or dependent alcohol use, measured through AUDIT score, was lower in this cohort than in other cohorts of FSWs, both in Kenya [33] and in various parts of Asia and Latin America [34–36]. The effect of alcohol use on self-reported ART adherence in this study is consistent with previous research in other populations. A recent systematic review and meta-analysis of studies in sub-Saharan Africa, including male and female populations, found a consistent association between alcohol use and varied measures of lower ART adherence or ART non-use, with a pooled effect estimate of 2.25 (95%CI 1.87–2.69) [2]. The review identified only one study conducted among FSWs [7]. In this cross-sectional study from Malawi, non-use of ART was 1.9-fold higher (95%CI 1.0–3.8) in FSWs with AUDIT score ≥16 (harmful or dependent alcohol use) compared to those with scores <16.
The association between alcohol use and detectable viral load has been examined in a number of studies in high-income settings, with mixed results [37–42]. Fewer studies have examined this association in sub-Saharan Africa, and both exposure definitions and results have varied in differing contexts. The only study of African FSWs, conducted in Malawi, found no significant association between harmful or dependent alcohol use and detectable viral load (aPR 1.7, 95%CI 0.5–5.5) [7]. Studies of general population clinic attendees in South Africa, Lesotho, and Morocco also found no association between alcohol use and detectable viral load [6–9]. In contrast, alcohol consumption was associated with detectable viral load among those on ART in a clinic-based cohort study in Botswana (aOR 1.7, 95%CI 1.0–3.0) [5] and a Ugandan cohort study (aOR 3.14, 95%CI 0.95–10.34) [11]. Similarly, a South African study reported that drinking >20 units of alcohol per week, compared to no alcohol use, was associated with detectable viral load (aOR 7.53, 95%CI 1.04–54.55) [10].
In this cohort of Kenyan FSWs, hazardous, harmful, or dependent alcohol use was independently associated with lower self-reported adherence, but not with detectable viral load. In people taking modern ART regimens, adherence as low as 80% may be sufficient to maintain viral suppression [12], providing a potential explanation for these seemingly inconsistent findings. The low percentage of women reporting harmful alcohol use or alcohol dependency in this cohort could also partially explain these results, as previous research has suggested that non-adherence increases with increasing levels of alcohol use [3]. Alternatively, it is possible that women who are comfortable reporting heavier alcohol use are also willing to report lower ART adherence. Over half of women in this cohort were over 40 years old, and older age was associated with lower alcohol use. Exploring the association between alcohol use and viral load in a younger FSW population that has higher alcohol intake could be an avenue for future research.
This study had several strengths. The research was conducted in a population for which we have minimal data on this topic. The longitudinal design provided repeated measures of both exposure and outcome variables. This design also allowed for evaluation of temporal relationships between alcohol use and measures of viral load and ART adherence. Collecting both self-reported adherence and viral load enabled us to observe how each was associated with alcohol use within the same population. Finally, the AUDIT score provided a standardized and validated measure, allowing comparison to other studies [21].
This analysis also had a number of limitations. First, the AUDIT score is focused on 12-month recall of alcohol use. This measure was chosen because of its feasibility for implementation in HIV care settings, but does not provide information about event-level associations between alcohol use and non-adherence. Second, alcohol use and poor ART adherence are both sensitive topics, and subject to under-reporting due to social desirability bias. Third, this was an older cohort, with a median age of 42 years. While this is reflective of the aging of the HIV-positive population in Africa [43], it limits the ability of these analyses to examine the association between AUDIT score and detectable viral load in younger women. Finally, most alcohol use in this cohort was moderate, with few AUDIT scores indicating harmful alcohol use or alcohol dependency. As a result, we were not able to examine associations with these categories separately.
Conclusions
This study adds to the limited literature on the relationship between alcohol use and HIV viral load suppression in ART-treated African FSWs. The results of this study suggest that targeted interventions to address alcohol use could impact ART adherence, but this effect may not be large enough to improve viral suppression, particularly in populations like this one, where few women reported harmful or dependent alcohol use.
Acknowledgments
We are grateful to our study participants and our research, clinical, laboratory, outreach and administrative staff for making this study possible.
References
- 1. Shubber Z, Mills EJ, Nachega JB, Vreeman R, Freitas M, Bock P, et al. Patient-Reported Barriers to Adherence to Antiretroviral Therapy: A Systematic Review and Meta-Analysis. PLoS Med. 2016;13(11):e1002183. pmid:27898679
- 2. Velloza J, Kemp CG, Aunon FM, Ramaiya MK, Creegan E, Simoni JM. Alcohol Use and Antiretroviral Therapy Non-Adherence Among Adults Living with HIV/AIDS in Sub-Saharan Africa: A Systematic Review and Meta-Analysis. AIDS Behav. 2019; 24(6):1727–1742.
- 3. Hendershot CS, Stoner SA, Pantalone DW, Simoni JM. Alcohol use and antiretroviral adherence: review and meta-analysis. J Acquir Immune Defic Syndr. 2009;52(2):180–202. pmid:19668086
- 4. Azar MM, Springer SA, Meyer JP, Altice FL. A systematic review of the impact of alcohol use disorders on HIV treatment outcomes, adherence to antiretroviral therapy and health care utilization. Drug Alcohol Depend. 2010;112(3):178–93. pmid:20705402
- 5. Gross R, Bellamy SL, Ratshaa B, Han X, Steenhoff AP, Mosepele M, et al. Effects of Sex and Alcohol Use on Antiretroviral Therapy Outcomes in Botswana: A Cohort Study. Addict Abingdon Engl. 2017;112(1):73–81.
- 6. Cichowitz C, Maraba N, Hamilton R, Charalambous S, Hoffmann CJ. Depression and alcohol use disorder at antiretroviral therapy initiation led to disengagement from care in South Africa. PloS One. 2017;12(12):e0189820. pmid:29281681
- 7. Lancaster KE, Lungu T, Mmodzi P, Hosseinipour MC, Chadwick K, Powers KA, et al. The association between substance use and sub-optimal HIV treatment engagement among HIV-infected female sex workers in Lilongwe, Malawi. AIDS Care. 2017;29(2):197–203. pmid:27442009
- 8. Hicham T, Ilyas E, Tarik H, Noureddine B, Omar B, Rachid F, et al. Risk factors associated with unsuppressed viral load in HIV-1 infected patients at the first antiretroviral therapy in Morocco. Int J Mycobacteriology. 2019;8(2):113–7. pmid:31210151
- 9. Cerutti B, Broers B, Masetsibi M, Faturiyele O, Toti-Mokoteli L, Motlatsi M, et al. Alcohol use and depression: link with adherence and viral suppression in adult patients on antiretroviral therapy in rural Lesotho, Southern Africa: a cross-sectional study. BMC Public Health. 2016;16:947. pmid:27608764
- 10. Dahab M, Charalambous S, Karstaedt AS, Fielding KL, Hamilton R, La Grange L, et al. Contrasting predictors of poor antiretroviral therapy outcomes in two South African HIV programmes: a cohort study. BMC Public Health. 2010;10:430. pmid:20649946
- 11. Kazooba P, Mayanja BN, Levin J, Masiira B, Kaleebu P. Virological failure on first-line antiretroviral therapy; associated factors and a pragmatic approach for switching to second line therapy–evidence from a prospective cohort study in rural South-Western Uganda, 2004–2011. Pan Afr Med J. 2018;29.
- 12. Byrd KK, Hou JG, Hazen R, Kirkham H, Suzuki S, Clay PG, et al. Antiretroviral Adherence Level Necessary for HIV Viral Suppression Using Real-World Data. J Acquir Immune Defic Syndr. 2019;82(3):245–51. pmid:31343455
- 13. Bhattacharjee P, Musyoki HK, Becker M, Musimbi J, Kaosa S, Kioko J, et al. HIV prevention programme cascades: insights from HIV programme monitoring for female sex workers in Kenya. J Int AIDS Soc. 2019;22(S4):e25311. pmid:31328436
- 14. Baral S, Beyrer C, Muessig K, Poteat T, Wirtz AL, Decker MR, et al. Burden of HIV among female sex workers in low-income and middle-income countries: a systematic review and meta-analysis. Lancet Infect Dis. 2012;12(7):538–49. pmid:22424777
- 15. Mountain E, Mishra S, Vickerman P, Pickles M, Gilks C, Boily M-C. Antiretroviral therapy uptake, attrition, adherence and outcomes among HIV-infected female sex workers: a systematic review and meta-analysis. PloS One. 2014;9(9):e105645. pmid:25265158
- 16. Diabaté S, Zannou DM, Geraldo N, Chamberland A, Akakpo J, Ahouada C, et al. Antiretroviral Therapy among HIV-1 Infected Female Sex Workers in Benin: A Comparative Study with Patients from the General Population. World J AIDS. 2011 Sep 29;1(3):94–9.
- 17. Mbonye M, Rutakumwa R, Weiss H, Seeley J. Alcohol consumption and high risk sexual behaviour among female sex workers in Uganda. Afr J AIDS Res AJAR. 2014;13(2):145–51. pmid:25174631
- 18.
Joint United Nations Programme on HIV/AIDS (2014) Fast track: ending the AIDS epidemic by 2030 [Internet]. Geneva, Switzerland: UNAIDS; http://www.unaids.org/sites/default/files/mediaasset/JC2686_WAD2014report_en.pdf
- 19. Wilson KS, Deya R, Yuhas K, Simoni J, Vander Stoep A, Shafi J, et al. A Prospective Cohort Study of Intimate Partner Violence and Unprotected Sex in HIV-Positive Female Sex Workers in Mombasa, Kenya. AIDS Behav. 2016;20(9):2054–64. pmid:27094785
- 20. Monahan PO, Shacham E, Reece M, Kroenke K, Ong’or WO, Omollo O, et al. Validity/reliability of PHQ-9 and PHQ-2 depression scales among adults living with HIV/AIDS in western Kenya. J Gen Intern Med. 2009;24(2):189–97. pmid:19031037
- 21.
Babor T, Higgins-Biddle J, Saunders J. AUDIT, The Alcohol Use Disorders Identification Test: guidelines for use in primary care. World Health Organization; 2001.
- 22. Saunders JB, Aasland OG, Babor TF, de la Fuente JR, Grant M. Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO Collaborative Project on Early Detection of Persons with Harmful Alcohol Consumption—II. Addict Abingdon Engl. 1993;88(6):791–804.
- 23. Feldman B, Fredericksen R, Crane P, Safren S, Mugavero M, Willig JH, et al. Evaluation of the Single-Item Self-Rating Adherence Scale for Use in Routine Clinical Care of People Living with HIV. AIDS Behav. 2013;17(1):307–18. pmid:23108721
- 24. Oyugi JH, Byakika-Tusiime J, Charlebois ED, Kityo C, Mugerwa R, Mugyenyi P, et al. Multiple validated measures of adherence indicate high levels of adherence to generic HIV antiretroviral therapy in a resource-limited setting. J Acquir Immune Defic Syndr. 2004;36(5):1100–2. pmid:15247564
- 25. Graham SM, Jalalian-Lechak Z, Shafi J, Chohan V, Deya RW, Jaoko W, et al. Antiretroviral Treatment Interruptions Predict Female Genital Shedding of Genotypically Resistant HIV-1 RNA. J Acquir Immune Defic Syndr. 2012;60(5):511–8. pmid:22592588
- 26. Xia Q, Coeytaux K, Braunstein SL, Torian LV, Daskalakis DC. Proposing a New Indicator for the National Human Immunodeficiency Virus/AIDS Strategy: Percentage of Newly Diagnosed Persons Achieving Viral Suppression Within 3 Months of Diagnosis. J Infect Dis. 2019;219(6):851–5. pmid:30304520
- 27. Macaluso M, Lawson L, Akers R, Valappil T, Hammond K, Blackwell R, et al. Prostate-specific antigen in vaginal fluid as a biologic marker of condom failure. Contraception. 1999;59(3):195–201. pmid:10382083
- 28. Kendagor A, Gathecha G, Ntakuka MW, Nyakundi P, Gathere S, Kiptui D, et al. Prevalence and determinants of heavy episodic drinking among adults in Kenya: analysis of the STEPwise survey, 2015. BMC Public Health. 2018;18(Suppl 3). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6219062/ pmid:30400910
- 29. Mukui IN, Ng’ang’a L, Williamson J, Wamicwe JN, Vakil S, Katana A, et al. Rates and Predictors of Non-Adherence to Antiretroviral Therapy among HIV-Positive Individuals in Kenya: Results from the Second Kenya AIDS Indicator Survey, 2012. PloS One. 2016;11(12):e0167465. pmid:27907114
- 30. Conner KR, Pinquart M, Gamble SA. Meta-analysis of depression and substance use among individuals with alcohol use disorders. J Subst Abuse Treat. 2009;37(2):127–37. pmid:19150207
- 31. Devries KM, Child JC, Bacchus LJ, Mak J, Falder G, Graham K, et al. Intimate partner violence victimization and alcohol consumption in women: a systematic review and meta-analysis. Addict Abingdon Engl. 2014;109(3):379–91. pmid:24329907
- 32. Scott-Sheldon LAJ, Carey KB, Cunningham K, Johnson BT, Carey MP. Alcohol Use Predicts Sexual Decision-Making: A Systematic Review and Meta-Analysis of the Experimental Literature. AIDS Behav. 2016;20(0 1):19–39. pmid:26080689
- 33. Chersich MF, Bosire W, King’ola N, Temmerman M, Luchters S. Effects of hazardous and harmful alcohol use on HIV incidence and sexual behaviour: a cohort study of Kenyan female sex workers. Glob Health. 2014 Apr 3;10(1):22. pmid:24708844
- 34. Zhang C, Li X, Hong Y, Stanton B, Chen Y, Liu W, et al. Pro-Alcohol-Use Social Environments and Alcohol Use among Female Sex Workers in China: Beyond the Effects of Serving Alcohol. World Health Popul. 2012;13(4):15–27. pmid:23089725
- 35. Semple SJ, Pitpitan EV, Chavarin CV, Strathdee SA, Zavala RI, Aarons GA, et al. Prevalence and Correlates of Hazardous Drinking among Female Sex Workers in 13 Mexican Cities. Alcohol Alcohol. 2016 Jul 1;51(4):450–6. pmid:26546017
- 36. Witte SS, Batsukh A, Chang M. Sexual Risk Behaviors, Alcohol Abuse, and Intimate Partner Violence among Sex Workers in Mongolia: Implications for HIV Prevention Intervention Development. J Prev Interv Community. 2010 Apr;38(2):89–103. pmid:20391057
- 37. Wu ES, Metzger DS, Lynch KG, Douglas SD. Association between Alcohol Use and HIV Viral Load. J Acquir Immune Defic Syndr. 2011;56(5):e129–30. pmid:21532918
- 38. Baum MK, Rafie C, Lai S, Sales S, Page JB, Campa A. Alcohol Use Accelerates HIV Disease Progression. AIDS Res Hum Retroviruses. 2010;26(5):511–8. pmid:20455765
- 39. Cook RL, Zhou Z, Kelso-Chichetto NE, Janelle J, Morano JP, Somboonwit C, et al. Alcohol consumption patterns and HIV viral suppression among persons receiving HIV care in Florida: an observational study. Addict Sci Clin Pract. 2017;12(1):22. pmid:28950912
- 40. Samet JH, Cheng DM, Libman H, Nunes DP, Alperen JK, Saitz R. Alcohol Consumption and HIV Disease Progression. J Acquir Immune Defic Syndr. 2007;46(2):194–9. pmid:17667330
- 41. Nolan S, Walley AY, Herren TC, Patts GJ, Ventura AS, Sullivan MM, et al. HIV-infected individuals who use alcohol and other drugs, and virologic suppression. AIDS Care. 2017;29(9):1129–36. pmid:28513200
- 42. Kalichman SC, Grebler T, Amaral CM, McNerney M, White D, Kalichman MO, et al. Viral Suppression and Antiretroviral Medication Adherence Among Alcohol Using HIV Positive Adults. Int J Behav Med. 2014;21(5):811–20. pmid:24085706
- 43. Autenrieth CS, Beck EJ, Stelzle D, Mallouris C, Mahy M, Ghys P. Global and regional trends of people living with HIV aged 50 and over: Estimates and projections for 2000–2020. PLoS ONE 2018;13(11). Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6264840 pmid:30496302