World Journal of AIDS, 2011, 1, 94-99
doi:10.4236/wja.2011.13014 Published Online September 2011 (http://www.SciRP.org/journal/wja)
Antiretroviral Therapy among HIV-1 Infected
Female Sex Workers in Benin: A Comparative
Study with Patients from the General Population
Souleymane Diabaté1,2, Djimon Marcel Zannou3, Nassirou Geraldo4, Annie Chamberland1,
Jocelyn Akakpo3, Carin Ahouada3, Marguerite Massinga Loembé5, Sévérin Anagonou3,
Annie Claude Labbé6, Michel Alary2, Cecile Tremb la y 1
1Centre de Recherche du Centre Hospitalier de l’Université de Montréal, Montréal, Canada; 2URESP, Centre de recherche FRSQ du
CHA universitaire de Québec, Québec, Canada; 3Centre National Hospitalier Universitaire de Cotonou, Cotonou, Bénin; 4Dispensaire
IST, Centre de Santé de Cotonou I, Cotonou, Bénin; 5Institut de Médecine Tropicale d’Anvers, Anvers, Belgique; 6Université de
Montréal, Hôpital Maisonneuve-Rosemont, Montréal, Canada.
Received June 7th, 2011; revised June 24th, 2011; accepted July 4th, 2011.
ABSTRACT
Objective: The aim of this study conducted in Benin was to compare HIV-1 infected female sex workers (FSW) and pa-
tients from the general population (GP) to see whether there was a difference in adherence level, mortality rate and
immuno-virologic response to antiretroviral therapy (ART). Methods: Fifty-tree FSW and 318 patients from the GP
were recruited and followed for at least one year. We compared both cohorts according to poor-adherence (taking
<95% of the p ills), CD4 count increa se, undetectable viral load (VL; ≤50 copies/mL) and crude mortality rate. We con-
structed a multivariate regression model to assess factors associated with undetectable VL. Results: During the first
year, the proportion of FSW with poor-adherence was significantly higher than that of the GP patients (19.3% versus
7.5%; p < 0.0001) and median gain in CD 4 count among FSW was slightly lower (103/mm3 versus 129/mm3; p = 0.085).
In the multivariate model (including CD4 at ART initiation and the sub-coho rt i.e. FSW vs GP patients), duration under
ART (p = 0.003) as well as CD4 count at enrolment in the study (p < 0.0001) and good-adherence (0.057) were inde-
pendently associated with undetectable VL. When adherence was withdrawn from this model, there was a borderline
significant asso ciation be tween detectable VL an d being a FSW (p = 0.074). The crude mortality rate was 1.11 per 100
persons-years among the GP patients and 4.65 per 100 persons-years among FSW. Conclusion: Response to ART was
lower among FSW compared to GP patients, as a result of poorer adherence. Specific behavioural interventions are
needed to improve adherence and response to ART among FSW.
Keywords: ART, FSW, Adherence
1. Introduction
In 2009, more than 22.5 million people (including ap-
proximately 1.8 million new infections) were living with
HIV in sub-Saharan Africa [1]. In this region, female sex
workers (FSW) and their clients have played an impor-
tant role in the extension of the epidemic to the general
population (GP) [2,3]. Consequently, both groups have
been targeted by various prevention interventions like
promotion of condom use and diagnosis and treatment of
sexually transmitted infections (STI). These interventions
aiming at reducing HIV acquisition as well as transmis-
sion have, indeed, contributed to an increase in condom
use and a decline in STI prevalence [4-6]. Nonetheless,
in sub-Saharan Africa, HIV prevalence among FSW is
still 3 to 4 times higher than among the general popula-
tion (19% versus 5.2%) [7]. It is therefore important to
consider improving access to antiretroviral therapy (ART)
for FSW and to scale-up other preventive interventions
shown to be effective [8]. According to recent findings
on the efficacy of ART for HIV prevention [9], providing
early ART to HIV-infected female sex workers has the
potential to have a considerable impact on HIV transmis-
sion to their clients and therefore contribute to HIV pre-
vention in the general population. Despite the increasing

Antiretroviral Therapy among HIV-1 Infected Female Sex Workers in Benin: A Comparative Study 95
with Patients from the General Population
number of treated patients in sub-Saharan Africa, little is
known about access to ART among FSW [1]. The objec-
tive of this prospective study conducted in Cotonou (Be-
nin) was to compare HIV-1 infected FSW and patients
from the GP to see whether there was a difference in ad-
herence level, mortality rate and immuno-virologic re-
sponse to ART.
2. Methods
From September 2008 to September 2010, we consecu-
tively enrolled and followed 371 HIV-1 infected adults
(aged ≥ 18 years) receiving a first-line ART composed of
two nucleoside reverse transcriptase inhibitors (NRTI)
plus a non-nucleoside reverse transcriptase inhibitor
(NNRTI) or a protease inhibitor (PI)): Fifty-three (53)
patients were FSW recruited at the Dispensaire IST
(medical center dedicated since 1989 to routine check-up
and STI treatment among FSW) and 318 patients were
from the GP. The GP patients were recruited at the Cen-
tre de traitement ambulatoire (CTA) du Centre national
hospitalier universitaire de Cotonou (reference center for
HIV treatment in Benin). After enrolment in the study,
FSW were seen every 3 months and patients from the GP
every 4 months (in accordance with existing follow-up
visits’ chronograms in each study center). World Health
Organisation (WHO) clinical stages III/IV or CD4 count
≤ 200 /mm3 were the main conditions for ART initiation
in Benin. The study was approved by the research ethics
committees of the Centre hospitalier de l’Université de
Montréal and the CHA universitaire de Québec in Can-
ada, and of the Ministry of Health in Benin. An informed
consent form was signed by all the participants.
Adherence counselling was routinely done in each
study center and the interviewers were all trained on the
study procedures. Adherence to ART was assessed
through self-report of missed doses: taking < 95% of the
pills prescribed during the four days preceding each visit
was defined as poor adherence [10]. Adherence to ART
and CD4 count (Flow cytometry) were measured at study
entry and at each follow-up visit. For patients who initi-
ated treatment before enrolment in the study, baseline
CD4 count, age and WHO clinical classification were
collected from the medical files. Viral load (VL, bDNA)
was performed for all patients only at study entry. De-
scriptive comparisons using chi-square or Fisher’s exact
tests (proportions) and Student’s t test (means) were per-
formed to compare both cohorts according to baseline
characteristics. A univariate model was performed for
each potential determinant of undetectable VL. All vari-
ables with a P value ≤ 0.10 were included in a multivari-
ate model to determine those independently associated
with undetectable VL (≤50 copies/mL). Data were ana-
lysed with SAS version 9.2 (SAS Institute, Cary, NC,
USA).
3. Results
At ART initiation, the median age (IQR) in both groups
was comparable: thirty nine (39; (33 - 43)) years for the
FSW and 37 (31 - 43) years for the patients from the GP
(p = 0.179). The majority of the GP patients were fe-
males (62.3%) and Beninese (91%). The FSW were from
Benin (30%) and neighbouring countries like Togo
(30%), Ghana (24%) and Nigeria (15%). The proportion
of non educated FSW was higher (35.9% versus 22.6%;
p = 0.034). At enrolment in the study, median duration
(IQR) under ART was 21 (4 - 38) months for the GP
patients and 4.3 (0 - 24.3) months for the FSW (p <
0.003). At ART initiation, most of the GP patients
(73.9%) were classified as WHO clinical stages III/IV as
compared with FSW (22.6%, p < 0.0001).
The NRTI mostly prescribed was stavudine (71.7% for
the GP patients and 77.4% for the FSW) whereas the
NNRTI mostly prescribed was efavirenz for patients
from the GP (72.4%) and nevirapine for FSW (73.6%;
Table 1). During follow-up, 19 ART modifications due
to side effects were observed among the GP patients
(none among the FSW). These treatment modifications
occurred after a median (IQR) duration under ART of 32
(7.8 - 53.8) months. In 18/19 cases (94.7%), stavudine
was replaced by zidovudine because of lipodystrophy
(lipoatrophy: 11/18, lipoatrophy plus lipohypertrophy:
3/18) and peripheral neuropathy (4/18). There were 13
(8.6%) switches to second-line ART in the GP patients.
The Median time (IQR) from initiation to switch to sec-
ond-line was 37.6 (27.9 - 49.0) months. Among the FSW,
we observed 4 (7.5%) switches. The 17 switches oc-
curred after availability of the VL measured at study en-
try and were mostly related to insufficient viro-immu-
nologic response (88.2%).
During the first year, poor adherence, as assessed at
follow-up visits, varied between 11.8% and 27.3% among
the FSW and between 5.9% and 10.6% among the GP
patients. Overall, the proportion of FSW with poor ad-
herence was significantly higher than that of the GP pa-
tients (19.3% versus 7.5%; p < 0.0001). There was no
difference in adherence levels according to gender in the
GP patients. The main reasons for missing doses reported
by the FSW were being out of home (58.6%) and running
out of pills (20.7%).
At ART initiation, median CD4 count/mm3 (IQR)
among the GP patients and the FSW was similar 115 (53
- 184) versus 134 (67 - 175, p=0.141), respectively. Dur-
ing the first year of treatment, we observed an increase in
CD4 count/mm3 among the FSW, but, median (IQR)

Antiretroviral Therapy among HIV-1 Infected Female Sex Workers in Benin: A Comparative Study
with Patients from the General Population
96
Table 1. Antiretroviral combinations in 53 HIV-1 infected female sex workers and 318 patients from the general population,
Cotonou, Benin.
Antiretroviral combinations General population (number, %) Female sex workers (number, %)
Stavudine + Lamivudine + Efavirenz 164 (51.6) 9 (17)
Zidovudine + Lamivudine + Efavirenz 65 (20.4) 5 (9.4)
Lamivudine + Didanosine + Efavirenz 2 (0.6) -
Stavudine + Lamivudine + Nevirapine 63 (19.8) 32 (60.4)
Zidovudine + Lamivudine + Nevirapine 23 (7.2) 7 (13.2)
Stavudine + Lamivudine + Indinavir 1 (0.3) -
Total 318 53
gain 103 (25 - 178) was to some extent lower as com-
pared with the GP patients 129 (75 - 232; p = 0.085;
Figure 1). At study entry, 57% of the GP patients and
34% of the FSW had undetectable VL.
After adjustment for CD4 count at ART initiation,
treatment duration, as well as CD4 count and good ad-
herence at enrolment in the study were independently
associated with undetectable VL (Table 2; model 1).
When we withdrew adherence from this model, being
recruited from the GP was found to be related to unde-
tectable VL (Tabl e 2, model 2). The crude mortality rate
was 1.11 per 100 person-years (3 deaths/270.33 per-
son-years) among the GP patients and 4.65 per 100 per-
son-years (2 deaths/43 person-years) among FSW.
In a sub-group analysis, we observed that from ART
initiation to year-3, CD4 count has increased progres-
sively among the GP patients (t test for trend = 18.92; p
< 0.0001; Figure 1). Median (IQR) gain in CD4 count
during the same period was 263 (196 - 345)/mm3. There
was no difference in CD4 progression according to the
NNRTI used (nevirapine or efavirenz, p = 0.585). In ad-
dition, the proportion of the GP patients recruited with
undetectable VL was similar irrespective of the NNRTI
prescribed (nevirapine, 60.5% and efavirenz, 55.7%; p =
0.366). Due to their small number, FSW were excluded
from these sub-group analyses concerning follow-up > 1
year and the relation between the NNRTI regimen (nevi-
rapine versus efavirenz) and immuno-virologic response.
4. Discussion
Irrespective of their HIV status, FSW from Cotonou and
its suburbs are requested to undergo each month a routine
medical visit. This preventive approach is an opportunity
for healthcare workers for early detection and treatment
of STI and other morbidities. It also allows testing for
HIV and prescription of cotrimoxazole prophylaxis if
better clinical conditions at ART initiation among FSW
needed. As a consequence, there was a trend towards as
compared with the GP patients: the proportion of sub-
jects with advanced WHO clinical stages (III/IV) was
lower among FSW. This observation, in agreement with
previous results showing a decrease in STI prevalence
among FSW in Benin, supports the importance of main-
taining and reinforcing preventive efforts towards
high-risk groups [5,11].
As previously described, stavudine (the most pre-
scribed NRTI in our study populations) was the main
cause for most of the first-line ART modifications due to
peripheral neuropathy and lipodystrophy [12,13]. This
known stavudine toxicity profile has led the WHO to
recommend less toxic agents such as tenofovir or zido-
vudine [14]. Lipodystrophy did not lead to regimen mo-
dification in FSW probably because of a lower median
duration under ART [13,15]. Most of the switches to
second-line ART were based on VL measured at enrol-
ment in the study. This is a paradox since all (except one)
patients with elevated viral load also had immunologic
failure and could have been switched to second-line
therapy earlier, based on this sole parameter. It appeared
that clinicians were less confident if they had to base
their decision of switching to second-line on CD4 counts
only [16]. This conservative attitude needs to be ad-
dressed by training activities aiming at strengthening
physicians’ prescription abilities but also by facilitating
access to VL, in particular for patients with insufficient
immune response [17].
In general, FSW have higher challenges for treatment
adherence because of their mobility motivated by many
reasons such as looking for new clients and avoiding
harassment from the police, from the brothel owners or
sometimes from their boyfriends. To prevent the negative
impact of this social instability on adherence level, care

Antiretroviral Therapy among HIV-1 Infected Female Sex Workers in Benin: A Comparative Study 97
with Patients from the General Population
Figure 1. Comparative CD4 counts increase in HIV-1 treated female sex workers and patients from the general population,
Cotonou, Benin. Note: Number s represent median CD4 counts/mm³; For patients who initiated antiretroviral therapy before
study entry, CD4 counts were obtained from their medical file; Due to limited data, FSW were excluded from analyses of
more than 12 months.
Table 2. Multivariate regression model asse ssing factors associated w ith undetectable viral load among HIV-1 tr eated female
sex workers and patients from the general population, Cotonou, Benin.
Undetectable viral load (≤50 copies/mL)
Model 1: with adherence Model 2: without adherence
Variables OR 95% CI P value OR 95% CI P value
CD4 count ≥ 350/mm3† 3.01 1.87 - 5.11 <0.0001 3.01 1.87 - 5.06 <0.0001
Duration under ART ≥ 6 months 2.3 1.31 - 3.92 0.003 2.5 1.46 - 4.20 0.008
Being recruited from the general population 1.2 0.54 - 2.84 0.612 1.9 0.94 - 3.97 0.074
Taking at least 95% of the pills prescribed† 2.3 0.97 - 5.27 0.057 - - -
†Measured at enrolment (as was viral load); OR, Odds ratio; CI, Confidence interval; Both models were adjusted for CD4 count at ART initiation.
givers at Dispensaire IST have decided to prescribe
whenever possible the most simplified ART regimen
available: a twice per day fixed-dose combination com-
posed of stavudine, lamuvidine and nevirapine (Triomune;
Cipla, Mumbai, India) [18-20]. This explains why FSW
were more exposed to Nevirapine. Nonetheless, the ma-
jority of our study patients who claimed poor adherence
were FSW and self-reported main reasons for not taking
pills were indeed related to instability: being out of home
and running out of pills. Strategies aiming at maximising
adherence to antiretroviral therapy among FSW should
tackle inherent factors like social instability.
During the first year of treatment, CD4 count recovery
among FSW and GP patients reached expected levels
[21]. However, this recovery was to some extent lower
among FSW. In addition, viral load suppression was
stronger in GP patients (Table 2; model 2), whereas the
crude mortality rate was higher in the FSW. Response to
ART appeared then to be less good among FSW. This
difference in response to ART was neither due to gender
nor to a difference of efficacy between nevirapine and
efavirenz: our subgroup analyses (GP patients), in ac-
cordance with previous results, showed that response to
ART did not vary significantly between subjects treated
by either of these drugs [22-24]. Moreover, we have re-
cently shown (based on the same study cohorts) that the

Antiretroviral Therapy among HIV-1 Infected Female Sex Workers in Benin: A Comparative Study 98
with Patients from the General Population
prevalence of primary resistance to ART was similar in
both the FSW and the GP patients [25]. Then, the re-
maining factor that could explain the difference in re-
sponse to ART between both groups is cumulative ad-
herence levels. Indeed, in our multivariate regression
model 2, being a GP patient was associated with unde-
tectable VL. In model 1, this association was dissipated
by good adherence i.e. taking at least 95% of the pills
prescribed by the doctors. Specific behavioural interven-
tions targeting FSW are therefore needed to improve
adherence and response to ART: as primary drug resis-
tance has been found to be elevated in this population,
poor adherence resulting in partial viral suppression can
rapidly jeopardize ART benefits [10,25-26]. Our study
has some limitations including the small number of
HIV-1-treated FSW and the short-term follow-up. How-
ever, our data provides important insights on the feasibil-
ity and also on the challenges of ART delivery in the
FSW population in sub-Saharan Africa.
In conclusion, response to ART was not as good among
female sex workers, compared with patients from the ge-
neral population, as a result of poorer adherence. Efforts
to improve response to ART among female sex workers
should target inherent factors impacting adherence such
as social instability. In addition, large size and long term
follow-up studies are needed to better analyse the deter-
minants and the extent to which response to ART among
female sex workers is different from response among the
general population patients.
5. Acknowledgements
We would like to thank the patients and the staff at the
Dispensaire IST and the Centre de traitement ambulatoire
du Centre national hospitalier universitaire de Cotonou.
We also thank the staff at the Centre de recherche du
Centre hospitalier universitaire de Montréal and the
Unité de recherche en santé des populations du Centre de
recherche FRSQ du CHA universitaire de Québec for
their administrative and technical assistance.
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