.". 2004.
ORIGINAL ARTICLE
Associationsof Sexual RiskTaking Among Kenyan Female Sex
Workers After Enrollment in an HIV-l Prevention Trial
G. Yadav, * R. Saskin,f§ E. N. Ngugi, # J. Kimani, 11F. Keli, 11K. Fonck; 11** K. S. MacDonald, ti
J. J. Bwayo,II M. Temmerman, ** The Kibera HJV Study Group, S. Moses, II and R. Kault§lI
Background: Female sex workers (FSWs) often lack the ability to
negotiate safer sex and arc at high risk for mv-I infection and sexually
transmitted infections (STIs).
Methods: Seronegative FSWs were enrolled in an STlJHIV-! prevention
trial in Nairobi, Kenya. Demographies and sexual risk taking
were assessed every 3 months. Predictors of reduced risk taking were
defined using multivariate logistic regression.
Results: Foul' hundred sixty-six FSWs were enrolled and followed
for just over 2 years each. A spectrum of sex work was apparent:
FSWs working in night clubs were younger, charged more for sex,
and used condoms more frequently; FSWs working from home were
older, charged less, and used condoms the least; and those working in
bars were intermediate. Increases in reported condom use were most
significant and sustained for FSWs working from home and charging
less for sex and were poorly maintained for bar-based FSWs. Selfreported
lower condom use, higher client numbers, and alcohol use
were associated with higher STl rates.
Conclusions: Home-based FSWs and those charging less for sex
used condoms the least at baseline but showed the greatest and most
sustained improvements over time. Potential response heterogeneity
Received for publication December 8, 2003; accepted May 6, 2004.
From the *Faculty of Arts and Sciences, University of Toronto, Toronto,
Ontario, Canada; [Dcpartrnent of Medicine, University of Toronto,
Toronto, Ontario, Canada; ~Mount Sinai Hospital, Toronto. Ontario,
Canada; §University Health Network, Toronto, Ontario, Canada; BOepart.
men! of Community Health Sciences and Medicine, University of
Manitoba, Winnipeg, Manitoba, Canada; 1jDepartment of Medical Microbiology,
University of Nairobi, Nairobi, Kenya; #Department of'Communiry
Health, University of Nairobi, Nairobi, Kenya; and "International
Centre for Reproductive Health, Department of Obstetrics and Gynaecology.
University of Ghent. Ghent, Belgium.
Members of The Kibera HIV Study Group are listed under ACknowledgments.
Supported by The Rockefeller Foundation (2000 HE 025), the European Cornmission
(DG Vlllf8, contract no. 7-RPR-28), the Canadian Research Chair
Programme (to R.K.), the Ontario HIV Treatment Network (to K.M.;
Career Scientist), and the Canadian Institutes of Health Research (to S.M.;
Investigator Award).
Reprints: Rupert Kaul, Clinical Science Division, Medical Sciences Building
#6356, University of Toronto. Toronto, Ontario, Canada M5S IA8 (e-mail:
rupert. kaul@utoronto.ca).
Copyright i\:i 2004 by Lippincott Williams & Wilkins
I Acquir Immune Defie Syndr • Volume 00, Number 0, Month ° 2004
in FSW subgroups should be considered in the design of Hlv-I prevention
programs.
Key Words: female sex workers, male condom, prospective, Africa,
workplace
(J Acquir Immune Defic Syndr 2004;00:000-000)
Female sex workers (FSWs) play an important role in the
dynamics of the HIV -1 epidemic in Africa. Factors including
gender inequality, economic disempowerment, and lack of
resources and education combine to place these women at an
enormously increased risk of acquiring HlV-I infection. 1.2 Infected
FSWs may also act as "core groups" in the HIV-l epidemic,
with male clients serving as bridges into the general
population.v" For these reasons, many HIV -1 prevention programs
have focused specifically on FSWs5 and have often
been very successful in reducing high-risk sexual behavior
and/or rates of sexually transmitted infections (STls) and
HIV-l infection.v"? However, there is a broad spectrum of
commercial sex work, with varying levels of sexual risk taking
and prevalence ofHIV-J infection among different FSW subpopulations.
I I It is therefore possible that the uptake or durability
ofHIV-l risk reduction interventions will vary, depending
on the demographics of the subpopulation targeted. It is
important to carefully document and evaluate the efficacy of
prevention programs in different situations and populations, 12
because resources allocated to HIV-l prevention fall far short
of what is necessary. J3
In 1998, a trial of antibiotic prophylaxis for acquisition
of both STls and HIV -1 infection was initiated in a cohort of
HIV -l-seronegative sex workers from the Kibera district of
Nairobi.14•15 A risk reduction program was provided for all
enrolled FSWs, and this was very successful in reducing rates
of high-risk behavior and STIsY However, self-identified
FSWs in this cohort practiced sex work in a number of very
different environments, as has- been reported for sex worker
cohorts elsewhere in Africa. II Therefore, tile purpose of this
study was to determine whether baseline factors could be identified
that predicted a greater or more sustained response to the
risk reduction intervention (ie, increased condom use and/or
Yadav et of / Aequir Immune Oefie Syncfr • Volume 00, Number 0, Month °2004
reduced client numbers), with the aim of improving our understanding
of how prevention strategies can be targeted to better
address the needs of vulnerable FSWs.
METHODS
Recruitment into this HIV/STI prevention trial was mediated
through a previously established network of FSW peer
educators 10,16 from May 1998 to January 2002. The study design
and baseline findings have been reported previously.v'"
Sex workers were defined as women who reported receiving
money or gifts in exchange for sex during the month before
initial screening. FSWs attended the clinic every month and
were administered the study drug as directly observed therapy.
All study subjects were provided with HIV -I prevention services
that included peer and clinic risk reduction counseling,
the provision of free condoms, and prompt treatment of symptomatic
STls. Two standardized l-hour risk reduction counseling
sessions were provided to all women at enrollment, and
subsequent clinic-based counseling was provided based on the
clients' perceived needs and self-reported risk behavior. Peerbased
risk reduction counseling was also provided to all study
participants through a series on monthly cohort "barazas" and
smaller community meetings. This peer-based counseling followed
a previously described model.'? with the addition of
counseling regarding the need to negotiate consistent condom
use with regular clients and boyfriends in addition to their
more commercial clients. I I A behavioral questionnaire was
administered at baseline and at 3-month intervals to assess
risk-taking behavior. Ethics approvals for the study were obtained
from institutional review boards at Kenyatta National
Hospital, Nairobi, Kenya, and the University of Manitoba,
Winnipeg Manitoba, Canada.
Laboratory Methods
All women underwent complete physical examination
and STI testing and treatment at enrollment, every 6 months,
and whenever clinically indicated. Cervical swabs were obtained
for Neisseria gonorrhoeae and Chlamydia trachomatis
polymerase chain reaction assays (Amplicor PCR Diagnostics,
Roche Diagnostic Systems. Ontario, Canada) and for N. gonorrhoeae
culture. If a genital ulcer was present, a swab of the
@ ulcer base was taken for M-polymerase chain reaction detection
of Haemophilus ducreyi, herpes simplex virus, and Treponema
palliduin (Roche Molecular Systems, Ontario, Canada).
Trichomonas iaginalis culture was performed using In Pouch
TV (Biorned Diagnostics, San Jose, CA), and blood specimens
were obtained for mV-I and syphilis serology. Any infections
identified were treated according to the Kenya National STl
Treatment Guidelines. In addition, monthly urine specimens
were collected at the time of directly observed study drug administration,
stored at -20°C, and tested for N. gonorrhoeae
and C. trachoma/is by polymerase chain reaction assay after
study completion.
2
Statistical Analysis
All FSWs undergoing HIV-I counseling and testing
completed a baseline clinic questionnaire and had ongoing access
to medical care through the clinic, whether they agreed to
participate in the randomized trial. For enrolled FSWs, selfreported
condom use, weekly client numbers, and hormonal
contraceptive use were recorded at baseline and every 3
months. Condom use was reported on a scale of 0 to 5, where
o represented no condom use and 5 represented condom use
with all clients. All other demographic and behavioral data
were collected only at the time of enrollment. Women were
divided into 3 groups based on their place of work 14 as follows:
group 1, work only from their own or client's home; group 2,
work from a nightclub or disco; group 3, work in a local bar or
lodging.
Baseline (enrollment) associations of sexual risk taking,
prevalent STls, and HIV -1 infection were examined using a
table for either l-way analysis of variance (for continuous variables)
or l test (for dichotomous variables) in SPSS version
10.0 (SPSS, Chicago, IL). The impact of baseline demographic
and behavioral factors on subsequent changes in risk taking
and STI rates was then prospectively modeled using multivariate
Poisson regression and logistic regression models for
correlated data (generalized estimating equations; PROC
GENMOD, SAS for Windows version 8.1, SAS Institute,
Cary, NC). Variables included in the model were those previously
associated with increased risk taking in other FSW cohorts
and those associated with differences in risk taking in the
baseline analysis (P < 0.05). These were place of work, charge
per sex act (dichotomized into charge for sex more or less the
cohort average), daily alcohol consumption, ever smoking,
and age at enrollment. Rates of condom use were analyzed
only at visits where women reported at least 1 weekly client
(ie, they were still active in sex work).
RESULTS
Cohort Characteristics and Follow-up
Four hundred sixty-six HIV -l=-seronegative FSWs were
enrolled in the trial from May 1998 to January 2002. Participants
were encouraged to remain in the trial for at least 2 years,
after which time they were free to choose to continue in the
trial or to exit the trial and attend the clinic as needed for routine
medical care. The mean duration of follow-up was 760
days, for a total of 969.6 person years of follow-up, and the
mean number of visits was 23.9.
Risk-Taking Behavior at Study Enrollment
When grouped according to place of work, significant
differences were observed between FSW subgroups with respect
to several behavioral and biologic variables at baseline
(Table I). Women working out of their homes or their clients' ffl@~!
e]004 Lippincott Williams & I-Vilkins