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Infectious diseases
Research
Does antiretroviral therapy initiation increase sexual risk taking in Kenyan female sex workers? A retrospective case–control study
  1. Elysha Mawji1,
  2. Lyle McKinnon1,2,
  3. Charles Wachihi2,
  4. Duncan Chege1,
  5. Paul Thottingal2,3,
  6. Anthony Kariri2,
  7. Francis Plummer4,5,
  8. T Blake Ball4,5,
  9. Walter Jaoko2,
  10. Elizabeth Ngugi3,
  11. Joshua Kimani2,4,
  12. Lawrence Gelmon4,
  13. Nico Nagelkerke4,6,
  14. Rupert Kaul1,2,7
  1. 1Department of Medicine, University of Toronto, Toronto, Ontario, Canada
  2. 2Department of Medical Microbiology, University of Nairobi, Nairobi, Kenya
  3. 3Department of Community Health, University of Nairobi, Nairobi, Kenya
  4. 4Department of Medical Microbiology, University of Manitoba, Winnipeg, Manitoba, Canada
  5. 5National Microbiology Lab, Public Health Agency of Canada, Winnipeg, Manitoba, Canada
  6. 6Department of Community Medicine, United Arab Emirates University, Al Ain, United Arab Emirates
  7. 7Department of Medicine, University Health Network, Toronto, Ontario, Canada
  1. Correspondence to Dr Lyle McKinnon; sijuisijali{at}gmail.com

Abstract

Objectives Although antiretroviral therapy (ART) prolongs life and reduces infectiousness, in some contexts, it has been associated with increased sexual risk taking.

Design Retrospective case–control study.

Setting Nairobi-based dedicated female sex worker (FSW) clinic.

Participants HIV-infected FSWs before and after ART initiation (n=62); HIV-infected and -uninfected control FSWs not starting ART during the same follow-up period (n=40).

Intervention Initiation of ART.

Primary outcome measures Self-reported condom use, client numbers and sexually transmitted infection incidence over the study period (before and after ART initiation in cases).

Results Sexual risk-taking behaviour with casual clients did not increase after ART initiation; condom use increased and sexually transmitted infection incidence decreased in both cases and controls, likely due to successful cohort-wide HIV prevention efforts.

Conclusions ART provision was not associated with increases in unsafe sex in this FSW population.

This is an open-access article distributed under the terms of the Creative Commons Attribution Non-commercial License, which permits use, distribution, and reproduction in any medium, provided the original work is properly cited, the use is non commercial and is otherwise in compliance with the license. See: http://creativecommons.org/licenses/by-nc/2.0/ and http://creativecommons.org/licenses/by-nc/2.0/legalcode.

https://doi.org/10.1136/bmjopen-2011-000565

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    Article summary

    Article focus

    • Impact of starting ART on sexual risk-taking behaviour in FSWs, which could have an important impact on HIV transmission to clients.

    Key messages

    • ART initiation was not associated with increased risk taking or sexually transmitted infection incidence.

    • Both of these declined over time, most likely as a result of risk reduction counselling.

    Strengths and limitations of this study

    • Strengths include a relevant population, longitudinal follow-up and inclusion of biological measures of risk taking (sexually transmitted infection incidence).

    • Limitations include relatively small study groups and limited sampling time points.

    Female sex workers (FSWs) play a key role in HIV epidemic spread in sub-Saharan Africa1 during both early and late epidemic phases2 due to multiple partners, high rates of HIV and sexually transmitted infections (STIs), and in many instances, their ability to negotiate safer sex practices are compromised.1 3 4 HIV prevention in this group may be the highest impact intervention in developing countries.5 Therefore, antiretroviral therapy (ART) programmes targeting FSWs may preserve life and reduce HIV transmission at a population level. However, it will be critical to ensure that sexual disinhibition does not counteract these beneficial effects.

    ART provision appears to have contradictory effects on HIV transmission. While ART reduces blood and genital tract viral load, and therefore infectiousness,6 it has also been associated with reduced safe sex practices7–9 and increases in STI incidence in some settings.10 Reasons for behavioural disinhibition could be several, including a feeling of improved health after ART initiation. Although this increase has not been the experience to date in resource-poor countries,11 it could become an issue as access expands,2 and further studies are needed to understand the extent to which these initial observations are generalisable. Mathematical models suggest that if safe sex practices are not maintained, then HIV transmission may increase despite ART-associated reductions in genital tract virus levels.12 A recent study in Kenyan sex workers with relatively low rates of partner exchange showed no change in risk taking following ART,13 but these findings need to be confirmed in a high partner exchange setting.

    In the current study, we assessed the impact of ART on sexual behaviour within an established cohort of FSWs from Nairobi, Kenya, in a retrospective case–control study. Institutional Review Boards at Kenyatta National Hospital and the Universities of Manitoba and Toronto approved the study, and all participants gave written informed consent prior to participation. Each participant completed a standardised questionnaire and physical exam every 6 months. Self-reported risk-taking data included the number of clients (casual and regular) and condoms used per week. Percentage condom use with casual clients was calculated from reported client and condom numbers, with maximum usage arbitrarily set at 98%. Risk reduction services provided to all participants included peer- and clinic-based counselling, provision of free condoms and STI management according to Kenyan guidelines. Non-parametric statistical comparisons between groups and within an individual were performed using PASW Statistics 18.0. Self-reported sexual behaviour data were collected at two time points 6 months apart prior to ART initiation and at two time points after: means of continuous variables were calculated for each period, and changes within an individual compared by using the Wilcoxon signed-rank test. Categorical variables were compared by Mann–Whitney test.

    Results

    All HIV-infected FSWs initiating ART during 2001–2006 with ≥1 year of follow-up were included as cases (n=62). Since sexual risk taking may change over time in the cohort as a whole, HIV-infected ART naive and HIV-uninfected FSWs enrolled in the cohort for a similar duration were selected as controls (n=20 each). Cases and controls were generally comparable at baseline, but cases reported higher condom use with casual clients (mean 97.8% vs 95.7%, p=0.01) and had a trend to a lower number of unprotected sex acts over the past year (23.0 vs 34.1, p=0.14, table 1). The proportion of participants reporting a regular client was similar (cases 58% vs controls 65%, p=0.62), and condoms were rarely used with regular clients (cases 23.2% vs controls 9.6%, p=0.13).

    View this table:
    Table 1

    Baseline characteristics of study groups

    No significant change was seen in casual client numbers during the year after starting ART in cases (19.9/week pre-ART vs 21.9 post-ART, p=0.17, table 2), in condom use with casual clients (97.8% both pre-ART and post-ART, p=0.66) or in the number of unprotected sex acts with casual clients (23.7/year pre-ART vs 24.7 post-ART, p=0.26). Condom use increased in controls (mean 95.7% vs 97.6%, p=0.14), so that although casual client numbers increased over the study period from 19.4 to 24.5 per week (p=0.002), there was a trend to reduced unprotected sex acts with casual clients during the latter year (34.1 vs 29.5, p=0.10).

    View this table:
    Table 2

    Longitudinal assessment of risk taking and sexually transmitted infection prevalence in female sex workers over time

    There was some evidence to suggest an increase in condom use with regular clients in both cases (3.91 vs 3.98, p=0.06) and controls (3.80 vs 3.93, p=0.05). The mean number of regular clients remained unchanged in cases (0.64 vs 0.43, p=0.13) and controls (0.55 vs 0.60, p=0.25), although controls had more regular partners during follow-up (0.60 vs 0.43, p=0.04). It should be noted that condom use with regular partners remained infrequent in all groups; specific interventions to increase this in FSW populations could have important public health benefits.

    Social desirability or fear of being taken off ART could associate with false reporting of sexual behaviour by FSWs, and so STI rates were also examined. Combining Trichomonas vaginalis and Neisseria gonorrhoea data in all participants, 12/102 FSWs were STI positive during the year pre-ART compared with 8/102 post-ART (p=0.346). This included 6/62 cases and 6/40 controls pre-ART and 4/62 cases and 4/40 controls post-ART. The period prevalence of N gonorrhoea declined from 4.6% to 1.1% in the periods before and after ART initiation (p=0.02, Wilcoxon test); this decrease was apparent in both cases (6/78, 7.7%, pre-ART vs 1/76, 1.3%, post-ART) and controls (3/116, 2.6%, pre-ART vs 1/110, 0.9%, post-ART).

    In summary, we found no increase in sexual risk taking in FSWs who initiated ART, using either self-reported behaviour or STI rates. This was in the context of clinic- and peer-based risk reduction services offered to all participants. The latter may be important since studies in Uganda14 and Kenya13 15 showed increases in safe sex practices following ART initiation in conjunction with risk reduction services, while in Cote d'Ivoire, there was an increase in unprotected sex post-ART in their absence.16 This suggests that ART should be combined with risk reduction services where possible. A prior Kenyan FSW study also reported no increased risk after ART initiation,13 15 although in that cohort less than a third of participants reported more than one partner over the past week compared with a mean of >20 casual clients in our study.

    Several factors may potentially impact sexual practices in FSW participants, including nationwide HIV education campaigns that could be associated with national declines in HIV prevalence17 18 and a cohort-wide risk reduction programme.19 Although we found no change in HIV risk behaviour after starting ART, these factors could have masked increases in risk relative to other cohort participants after ART initiation. To rule out this possibility, we assessed a control group of 40 FSWs followed over a similar time span, both HIV-infected ART naive and HIV-uninfected FSWs, and found no evidence that this was the case.

    In conclusion, we found no evidence for alterations in sexual behaviour after starting ART in Kenyan FSWs with very high partner exchange rates. FSWs through their profession may act as an important core HIV transmission group in the region. Since ART has been shown to reduce HIV transmission,20 21 ART provision for FSWs in conjunction with risk reduction services should be considered an important strategy to reduce HIV transmission at a population level.

    Acknowledgments

    We would like to thank the staff at Majengo clinic and the Kenyan AIDS Control Project for supporting the study and the patients for their willingness to participate.

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    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

      Files in this Data Supplement:

    Footnotes

    • EM and LM contributed equally to this work.

    • To cite: Mawji E, McKinnon L, Wachihi C, et al. Does antiretroviral therapy initiation increase sexual risk taking in Kenyan female sex workers? A retrospective case–control study. BMJ Open 2012;2:e000565. doi:10.1136/bmjopen-2011-000565

    • Contributors EM, PT, WJ, JK, LG and RK designed the study. EM, LM, AK, NN and RK analysed the data. CW and JK managed the clinical cohorts. All authors contributed to the writing and editing of the manuscript.

    • Funding This research was supported by grants from the Canadian Institutes of Health Research (RK; HET-85518 and MOP-89983); patient care activities and the purchase of antiretroviral drugs were funded by the President's Emergency Plan for AIDS Relief (PEPFAR). Salary support was provided by the Canadian Institutes of Health Research and the International Infectious Diseases and Global Health Training Program (LM) and the Canada Research Chair Program (RK).

    • Competing interests None.

    • Patient consent Obtained.

    • Ethics approval Ethics approval was provided by the University of Manitoba, University of Toronto, Kenyatta National Hospital.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data sharing statement There are no additional data available.