The HIV Care Continuum and HIV-1 Drug Resistance Among Female Sex Workers: A Key Population in Guinea-Bissau
The HIV Care Continuum and HIV-1 Drug Resistance Among Female Sex Workers: A Key Population in Guinea-Bissau
The HIV Care Continuum and HIV-1 Drug Resistance Among Female Sex Workers: A Key Population in Guinea-Bissau
Abstract
Introduction: Female sex workers (FSW) are considered a key group for HIV transmissions in sub-Saharan Africa.
The HIV Care Continuum and HIV drug resistance (HIVDR) among FSW has not been well studied in most countries
in West Africa. In the current study we describe the HIV Care continuum and prevalence of HIVDR among FSW in
Guinea-Bissau.
Methods: A venue-based recruitment and peer-referral of FSW was used in seven cities in Guinea-Bissau from Octo-
ber 2014 to September 2017. We administered a questionnaire, performed discriminatory HIV-testing and collected
blood specimens for CD4 count, viral load and HIVDR genotyping.
Results: The survey included 440 FSW. The overall HIV-prevalence among FSW was 26.8%. Of the HIV-1 (HIV-1 single-
or dually HIV-1/HIV-2) infected FSW (N = 104), 58.7% were previously diagnosed with HIV-1 at enrolment and 41.4%
reported taking antiretroviral therapy (ART) compared to 28.6% of the HIV-2 single-infected FSW (N = 14). Among
HIV-1 infected FSW on ART (N = 43), 55.8% were virally suppressed (< 1000 copies/ml) and of all HIV-1 infected FSW,
29.8% were virally suppressed. Among ART experienced FSW (N = 22), 50.0% had HIVDR. HIVDR was also found in
9.4% of treatment naïve FSW (N = 53).
Conclusion: The majority of FSW who knew their HIV status received ART, however a large proportion of FSW were
not aware of their HIV positive status. This translated into a great majority of the HIV-infected FSW not being virally
suppressed. Amongst treatment naïve FSW nearly a tenth had HIVDR, suggesting that sexual transmission of HIVDR is
occurring in this at-risk-population.
Keywords: Antiretroviral therapy, HIV care continuum, HIV seroprevalence, Sex workers, Africa, Drug resistance
mutations
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Lindman et al. AIDS Res Ther (2020) 17:33 Page 2 of 11
and until March 2016 all samples were transported on program (https://hivdb.stanford.edu/hivdb/by-mutat
dry ice for HIV-1 viral load (VL) measurement and drug ions/) [29].
resistance genotyping at the Section of Clinical Virol-
ogy at Lund University, Sweden (please see below for Statistics
details). From March 2016, plasma HIV-1 viral load The Chi square test was used for categorical variables
quantification was performed using GeneXpert at LNSP and the two-tailed Mann–Whitney test U test for con-
in Bissau [23]. The results of CD4 measurements and VL tinuous variables. Trends in change of seroprevalence of
measurements were provided to participants at the next HIV was analyzed by Cochran-Armitage test for linear
visit at the mobile clinic where the study nurse assisted trend adjusted for age. FSW were defined as virally sup-
with interpretation of the results. All HIV infected FSW pressed with an HIV-1 VL < 1000 copies/ml [30, 31]. The
were referred to an HIV treatment clinic of their choice continuum outcomes were characterized using two dif-
together with their results for follow-up examination and ferent approaches; using all HIV-1/dual-infected FSWs as
treatment per national guidelines. the denominator or by using HIV-1/dual-infected FSW
achieving the prior step in the continuum as the denomi-
nator. Logistic regression was used to assess predictors of
HIV‑1 plasma viral load determination and drug resistance outcomes in the HIV care cascade. Due to sample size,
genotyping we were only able to investigate diagnosed HIV infection
HIV-1 viral load was prior to March 2016 determined vs. undiagnosed HIV infection. Covariates were assessed
using an in-house TaqMan quantitative PCR (qPCR) with in univariate and multivariate analysis. Covariates con-
primers and probes as described [24]. qPCR was done sidered for inclusion in the multivariate model were age,
using the ABI StepOnePlus System (Applied Biosystems) region, education, condom use, number of clients last day
and the SuperScript III Platinum One-Step qRT-PCR Kit of sex work, alcohol consumption and number of chil-
(Invitrogen) according to the manufacturer’s instruc- dren. The final model was derived from an initial explan-
tions. Polymerase chain reaction (PCR) conditions were atory model with all variables included. Models were
as follows: 50 °C for 10 min and 95 °C for 2 min, followed compared using likelihood ratio tests and Aikaki´s infor-
by 40 cycles of 95 °C for 15 s, and 60 °C for 45 s. Stocks mation criterion. In the final model the most important
of HIV-1 strain IIIB which had been quantified by elec- variables—age, region, education, condom use—were
tron microscopy (Advanced Biotechnology Incorporated, included. Data were managed in EPI INFO version 7.14
Columbia MD), were used as standards. Known virus and analyzed by STATA 13 [32, 33].
copy numbers were spiked into HIV-negative human
plasma and extracted as previously described [24]. The Results
qPCR assay had a limit of quantification of five RNA cop- During the study period 847 women visited the mobile
ies/qPCR reaction with a linear range between 1 06 and 5 clinic. Among them, 490 women consented to partici-
RNA copies/reaction. pate in the study but 50 women did not engage in sex
HIV-1 drug resistance genotyping were determined as work according to our definition and were not included
follows: HIV-1 RNA was extracted from blood plasma, in the study. Thus a total of 440 women were included
and HIV-1 pol sequences were amplified by RT-PCR and between October 2014 and September 2017, 63.2% of
nested PCR as described [25]. The final length of all the the women were included in the capital Bissau. Figure 1
HIV-1 pol sequences following removal of regions corre- shows the flowchart of the included study participants.
sponding to the primers, editing and alignment was 1035 The median age was 28 (Interquartile range (IQR) 22-35).
bases, corresponding to nucleotide positions 2268–3302 The overall HIV-prevalence at inclusion was 26.8% (95%
of HXB2 (GenBank accession number K03455), cover- CI 22.7–31.2, n = 118). The total prevalence of HIV-1
ing positions 6-99 of the protease and positions 1-251 single-infection, HIV-2 single-infection and HIV-1/2
of the reverse transcriptase regions. The presence of dual infection was 20.5% (95% CI 16.8–24.5, n = 90),
drug resistance mutations (DRM) was assessed using the 3.2% (95% CI 1.8–5.3, n = 14) and 3.2% (95% CI 1.8–5.3,
Stanford Genotypic Resistance Interpretation Algorithm n = 14), respectively. The overall HIV-prevalence over
[26]. DRM in self-reported treatment naïve individuals the 3-year study period decreased over time from 32.6%
were examined according to the calibrated population (95% CI 25.6–40.1) between October 2014 and Septem-
resistance tool v6.0 beta (http://cpr.stanford.edu/cpr. ber 2015 (N = 172), 26.0% (95% CI 17.8––35.7) between
cgi), based on the WHO surveillance transmitted drug October 2015 and September 2016 (N = 100), to 21.4%
resistance mutation list of 2009 [27, 28]. DRM in FSW (95% CI 15.4-28.4) between October 2016 and Septem-
on current ART and DRM in FSW reporting treatment ber 2017 (N = 168) (p = 0.02 comparing the HIV preva-
discontinuation was assessed using The Stanford HIVdb lence over three time periods). After age-adjustments no
Lindman et al. AIDS Res Ther (2020) 17:33 Page 4 of 11
HIV-1
Seroconverters^ VL ≥1000 VL <1000 VL ≥1000 VL <1000
n=64 n=26 n=9 n=5
n=3
Genotyped for Genotyped for Genotyped for Genotyped for Genotyped for
HIVDR HIVDR HIVDR HIVDR HIVDR
n=3 n=63 n=9 n=9 n=0
Fig. 1 Flowchart of the study population. HIVDR, HIV drug resistance mutations; VL, Viral load. ^Three individuals seroconverting from
HIV-seronegative to HIV-1 seropositive status during the study period
statistically significant declining trend could be detected younger FSW (< 30 years) were more likely to be previ-
(p = 0.58 comparing the HIV prevalence over three ously undiagnosed (adjusted odds ratio (AOR) 2.7 (95%
time periods). Table 1 presents summary characteris- CI 1.2–6.5, p = 0.02), and there was some evidence that
tics of HIV-infected participants stratified by HIV type FSW residing outside Bissau were more likely to have
and HIV-negative participants. HIV-1 single-infected an undiagnosed HIV infection (AOR 2.7 (95% CI 1.0–
FSW were younger (median age 30 years IQR 25–37) 6.8, p = 0.05)). More importantly, an unknown HIV
compared to both HIV-2 single-infected (38 years IQR diagnosis was associated with inconsistent condom
28–44, p = 0.03) and HIV-1/2 dual-infected (46.5 years use with clients (AOR 3.0 (95% CI 1.04–8.9, p = 0.04)
IQR 35–49, p < 0.001) FSW but older than HIV-nega- (Table 2).
tive FSW (26 years IQR 22–32, p < 0.001). HIV-2 single- A history of HIV care was reported in 49.0% (95% CI
infected FSW had a higher median CD4 cell count (1039, 39.1–59.0, n = 51) of all HIV-1 infected FSW (Fig. 1),
IQR 727–1177) compared to both HIV-1 single-infected and in 83.6% (95% CI 71.9–91.8, n = 51) of the FSW
women (615 IQR 377–811 (p < 0.001)) and HIV-1/2 dual- previously diagnosed with an HIV-1 infection. Among
infected women (525 IQR 296–741 (p = 0.001)), while the HIV-2 single-infected FSW 28.6% (95% CI 8.4–58.1,
there was no significant difference between HIV-1 sin- n = 4) reported a history of HIV care, of whom all
gle-infected women and HIV-1/2 dual-infected women reported current ART use. Of all HIV-1 infected FSW,
(p = 0.38). 41.4% (95% CI 31.7–51.4, n = 43) reported taking ART
compared to 84.3% (95% CI 71.4–92.9, n = 43) of HIV-1
infected FSW with a history of HIV care and 70.5%
HIV and the care continuum
(95% CI 57.4–81.4, n = 43) of HIV-1 infected FSW with
The HIV Care continuum among all HIV-1 infected a previous diagnosis. Among the HIV-1 infected FSW
FSW including HIV-1/2 dual-infected women is pre- reporting current ART use, 55.8% (95% CI 39.9–70.9,
sented in Fig. 2 and in the following. Among the 104 n = 24) were virally suppressed, which was 23.1% (95%
HIV-1 infected FSW, 58.7% (95% CI 48.5–68.2, n = 61) CI 15.4–32.4, n = 24) of all women testing HIV-1 posi-
knew their HIV status. The median CD4 cell count and tive. An additional 6.7% (95% CI 2.7–13.4, n = 7) of
VL was 559 cells/mm3 (IQR 322.5–751) and 2707 cop- HIV-1 infected women were virally suppressed despite
ies/ml (IQR 20–15849), respectively. The correspond- not reporting ART use, which means that a total of
ing figures for HIV-1 infected FSW without a previous 29.8% of HIV-1 infected women (95% CI 21.2–39.6,
HIV diagnosis was 618 cells/mm3 (IQR 439–856) and n = 31) were virally suppressed. Self-reported adher-
8110 copies/ml (IQR 2677–57800), respectively. Among ence ≥ 90% measured by VAS, among 27 of the HIV-1
the 14 HIV-2 single-infected FSW 64.3% (95% CI 35.1– infected FSW reporting current ART use, was associ-
87.2, n = 9) knew their HIV status. Parameters associ- ated with viral suppression after age adjustments (odds
ated with undiagnosed HIV infection were determined ratio 20.0, 95% CI 2.5–161.7, p = 0.01).
by multivariable analysis. The analyses showed that
Lindman et al. AIDS Res Ther (2020) 17:33 Page 5 of 11
Table 1 Selected summary characteristics among HIV infected participants stratified by HIV type and HIV negative
participants
HIV-1 single-infected HIV-1/2 dual- HIV-2 single- HIV negative (n = 322) HIV-1
(n = 90) infected (n = 14) infected (n = 14) vs HIV
negative
p-value
HIV‑1 resistance mutations NNRTI only resistance mutations were detected in 18.2%
All resistance mutations identified in HIV-1 infected (95% CI 5.2–40.3, n = 4), NRTI only resistance mutations
FSW with a viral load ≥ 1000 copies/ml are summarized in 9.1% (95% CI 1.1–29.2, n = 2) and NNRTI + NRTI
in Table 3. Among HIV-1 infected FSW with a viral mutations were detected in 18.2% (95% CI 5.2–40.3,
load < 1000 copies/ml no HIVDR were detected in the n = 4). One individual had a protease inhibitor acces-
nine samples that were analyzed for HIVDR. At least one sory mutation. There was no difference in time on ART
HIVDR was detected in 9.4% (95% CI 3.1–20.7, n = 5) between FSW with or without HIVDR (3.6 IQR 1.7-4.4
of the 53 treatment naïve FSW, as compared with 50.0% and 3.2 years IQR 1.8–6.1, respectively, p = 0.59).
(95% CI 28.2–71.8, n = 11) of 22 ART experienced FSW. Table 4 shows all resistance mutations by subset in
Among the treatment naïve FSW, 6.0% (95% CI 1.2–15.7, the 16 FSW with a HIVDR. Overall, the most common
n = 3) had NNRTI mutations, and 4.0% (95% CI 0.5–13.0, NNRTI resistance mutation was K103N which was found
n = 2) had nucleoside reverse transcriptase inhibitor in 43.8% (95% CI 19.7–70.1, n = 7) of FSW with a HIVDR
(NRTI) mutations. Among the 22 ART experienced FSW, mutation. The most common NRTI mutation was
Lindman et al. AIDS Res Ther (2020) 17:33 Page 6 of 11
Fig. 2 HIV care continuum among all HIV-1 infected FSW (n = 104). The y-axis and the figures in the bars indicate the proportion of all women
testing HIV-1 positive. The proportion of women from each preceding step is described in the text
M184V which was found in 37.5% (95% CI 15.2–64.6, while the HIV-2 prevalence was nearly two times higher
n = 6) of FSW with a HIVDR mutation. By splitting the among the FSW observed in our study compared to
study period in two 18.5-month time strata; September adult women in the most recent community-based study
2014 to 15th March 2016 and 16th March 2016 to Sep- from Bissau, were the HIV-1 and HIV-2 prevalence was
tember 2017, we investigated if any temporal trends in 5.2% and 3.4% respectively [35]. The CD4+ T cell lev-
prevalence of PDR among treatment naïve FSW could els were generally high, also among FSW not previously
be seen. The prevalence of PDR were 4.2% (95% CI 0.1– diagnosed, probably due to a relatively short duration of
21.1, n = 1) among 24 treatment naïve FSW included in infection among most participants.
the first time-period and 13.8% (95% CI 3.9–31.6, n = 4) Our finding that more than one-third of all HIV-1
among 29 treatment naïve FSW included in the last time- infected FSW and HIV-2 infected FSW were not aware of
period (p = 0.26 comparing the prevalence in the two their HIV infection is considerably higher than reported
time periods). in studies from Malawi, South Africa and Zimbabwe [13,
14, 37]. This is a concern because individuals that are
Discussion unaware of their HIV status will not be linked to HIV
In this study, we investigated the HIV care continuum care. Another concern is the increased risk of onward
and HIV-1 drug resistance among 440 FSW across six HIV transmission since FSW unaware of their HIV infec-
sites in Guinea-Bissau. The overall HIV prevalence was tion were more likely to have inconsistent condom use
26.8%, with nearly four times higher total HIV-1 preva- with clients. Currently, WHO recommends HIV testing
lence (23.6%) than total HIV-2 prevalence (6.4%) when every 12 months for FSW [38]. It is therefore plausible
including HIV-1/2 dual-infected FSW in each group. The that frequent testing strategies for FSW would be benefi-
comparably low HIV-2 prevalence is in concordance with cial in Guinea-Bissau, particularly among younger FSW
the decreasing HIV-2 prevalence that has been observed and FSW residing outside the capital Bissau.
in an occupational cohort of police officers, among preg- A meta-analysis and systematic review among FSW in
nant women and the general population. [34–36] The low-and-middle-income-countries found an estimated
prevalence of HIV-1 was more than four times higher ART coverage of 39.3% (27.2–52.9%) [11]. The ART
Lindman et al. AIDS Res Ther (2020) 17:33 Page 7 of 11
Table 2 Association between sociodemographic factors and transmission risk factors with a previously undiagnosed HIV
infection
n Undiagnosed HIV OR 95% CI p AORa 95% CI p
infection
HIV-type
HIV-1 90 40 (44.4%) Ref
HIV-2 14 5 (35.7%) 0.7 0.2–2.2 0.54
HIV-1/2 dual infected 14 3(21.4%) 0.3 0.1–1.3 0.12
Age
≥ 30 73 23 31.5%) Ref Ref
< 30 45 25 (55.6%) 2.7 1.3–5.9 0.01 2.7 1.2–6.5 0.02
Nationality
Guinea-Bissau 109 44 (40.4%) Ref
Otherb 9 4 (44.4%) 1.2 0.3–4.7 0.81
Region
Bissau 59 18 (30.5%) Ref Ref
Outside Bissauc 59 30 (50.9%) 2.4 1.1–5.1 0.03 2.4 1.0-5.8 0.05
Marital status
Single 38 15 (39.5%) Ref
Married 22 8 (36.4%) 0.9 0.3–2.6 0.81
Divorced/widowed 54 22 (40.7%) 1.1 0.5–2.5 0.90
Data missing 4 3 (75.0%)
Children
≥ 1 child 98 36 (36.7%) Ref
None 16 10 (62.5%) 2.9 1.0–8.6 0.06
Data missing 4 2 (50.0%)
Education (years)
None 48 18 (37.5%) Ref Ref
1–5 24 9 (37.5%) 1 0.4–2.8 1.0 Ref
6–9 26 9 (34.6%) 0.9 0.3–2.4 0.81 Ref
10–12 10 7 (70.0%) 3.9 0.9–16.7 0.07 4.2 0.9–19.9 0.08
Data missing 10 5 (50.0%)
Another source of incomed
No 61 22 (36.1%) Ref
Yes 53 25 (47.2%) 1.6 0.7–3.4 0.23
Data missing 4 1 (25.0%)
Number of c lientse
≥2 40 14 35.0%) Ref
0–2 62 30 (48.4%) 1.7 0.8–3.9 0.18
Data missing 16 4 (25.0%)
Condom use with clientf
Consistent 85 31 (36.5%) Ref Ref
Inconsistent 23 37 (60.9%) 2.7 1.1–7.0 0.04 3.0 1.04–8.4 0.04
Data missing 10 3 (30.0%)
Alcohol comsumptiong
Never 74 35 (47.3%) Ref
Yes 40 12 (30.0%) 0.5 0.2–1.1 0.08
Data missing 4 1(25.0%)
AOR adjusted odds ratio, CI confidence interval, OR odds ratio, p p-value, Ref reference category
a
In the final multivariate model the following variables were included; age, region, education (0–9 years vs 10–12 years), and condom use
b
Including Gambia and Senegal
c
Including Canchungo, Bafata, Gabu, Bambadinca, Buba, Quebo
d
Besides sex work
Lindman et al. AIDS Res Ther (2020) 17:33 Page 8 of 11
Table 2 (continued)
e
Number of clients last day of sex work
f
Do you accept condomless sex with clients?; inconsistent including “Yes”, Consistent including “No”
g
Alcohol consumption last month; Yes including “Every day”, “Once a week”, “less than once a week”, No including “Never”
Table 3 Summary characteristics by treatment status among HIV-1 infected participants with viral load ≥ 1000 copies/ml
Treatment naivea (n = 53) ART expereriencedb (n = 22) Treatment
Naive vs ART
experienced
p-value
coverage among all HIV-1 infected FSW in our study non-adherence, but given our findings regarding PDR,
was 41.4%, which is comparable to this meta-analysis as it is possible that some of these mutations represents
well as other studies of FSW from Zimbabwe (43.4%) and transmitted drug resistance. In nearly half of the FSW
South Africa (43.9%), but lower than in Malawi (52.2%) on treatment with viremia, non-mutated virus was
[13, 14, 37]. The corresponding ART coverage for HIV-2 identified which suggest treatment interruptions as the
single-infected women in our study was 28.6%. We cause of their virological failure. Other explanations
recently showed that HIV-2 is more pathogenic than pre- could be problems with drug dosing or absorption, as
viously thought and that the majority of HIV-2 infected previously described by Lessells et al. [41].
individuals will progress to HIV-related disease and Total HIVDR in our study (as percentage of all HIV-1
death without treatment, further emphasizing the impor- infected participants) was in line with a recent study
tance of high ART coverage among HIV-2 infected indi- from South Africa (15.4% vs 16.7%) [37]. Similarly to
viduals [39]. our study, the report from South Africa included both
The status of the UNAIDS goals among the general FSW on treatment, FSW reporting treatment discon-
population of women of the same age in Guinea-Bissau tinuation, and treatment naïve FSW. The most com-
have not been detailed. However, the ART coverage mon resistance mutation in the ART naïve FSW was
among FSW in our study did not reach the 90-90-90 the K103N and K103S mutations, which is similar to
goals set by UNAIDS but among FSW on ART 55.8% a recent study of pregnant women in Guinea Bissau
were virally suppressed, indicating that the majority [25]. The prevalence of PDR was high, especially in the
of FSW are likely to be adherent to their ART regime second part of the study were the prevalence reached
[40]. Moreover, more than half of the FSW on treat- 13.8% although with a large uncertainty of the estimate.
ment that failed to suppress their virus had at least one This is worrisome and further studies are necessary
HIVDR mutation. It is likely that many of these muta- to investigate if PDR is increasing in Guinea-Bissau.
tions represent acquired resistance mutations due to Moreover, the most frequent mutations found in our
Lindman et al. AIDS Res Ther (2020) 17:33 Page 9 of 11
Table 4 HIVDR mutations by treatment status among 16 in other studies of FSW [13, 14]. The most likely expla-
FSW with detectable HIVDR in Guinea-Bissau nation is misclassification, but it could also be possi-
Drug class HIVDR Treatment ART Total (n = 16) ble that a small proportion of these women were elite
Mutation Naive experienceda controllers [21, 43]. Regarding HIVDR data, the sample
(n = 16) (n = 5) (n = 11) was small and therefore limited the generalizability.
NNRTI K103N/S 3 (60.0%) 4 (36.4%) 7 (43.8%)b Moreover, it cannot be excluded that women report-
A98G 0 (0.0%) 2 (18.2%) 2 (12.5%) ing not being on ART could have previously received
E1238A 0 (0.0%). 1 (9.1%) 1 (6.3%) PMTCT, even though fieldworkers probed for this.
K238N 0 (0.0%) 1 (9.1%) 1 (6.35)
K238T 0 (0.0%) 1 (9.1%) 1 (6.3%)
P225H 0 (0.0%) 1 (9.1%) 1 (6.3%) Conclusion
V106A 0 (0.0%) 1 (9.1%) 1 (6.3%) This is the first study to characterize the HIV care con-
V179E 0 (0.0%) 1 (9.1%) 1 (6.3%) tinuum among FSW in Guinea-Bissau. Our study sug-
Y188H 0 (0.0%) 1 (9.1%) 1 (6.3%) gests that FSW are highly burdened to HIV compared
Y188L 1 (20.0%) 0 (0.0%) 1 (6.3%) to adult women in Guinea-Bissau, and of all HIV-1
NRTI M184V 0 (0.0%) 6 (54.5%) 6 (37.5%)b infected women only a third were virally suppressed.
M41L 1 (20.0%) 1 (9.1%) 2 (12.5%)
We also found high levels of HIVDR mutations among
T215Y 0 (0.0%) 2 (18.2%) 2 (12.5%)
both treatment naïve FSW and FSW on ART. Future
D67N 1 (20.0%) 0 (0.0%) 1 (6.3%)
studies are needed to assess HIV prevalence and
E44D 0 (0.0%) 1 (10.0%) 1 (6.3%)
HIVDR mutations among FSW and other most-at-risk-
K219E 1 (20.0%) 0 (0.0%) 1 (6.3%)
populations (MARPs) in the region. Such studies would
T215FY 0 (0.0%) 1 (9.1%) 1 (6.3%)
be pivotal to inform future targeted interv against
T215I 1 (20.0%) 0 (0.0%) 1 (6.3%)
MARPs in resource-limited settings like Guinea-Bissau.
PI L89V 0 (0.0%) 1 (9.1%) 1 (6.3%)b
Data are n (%) Abbreviations
ART antiretroviral therapy, HIVDR HIV-1 drug resistance, NNRTI non-nucleoside
FSW: Female sex workers; HIVDR: HIV drug resistance; ART: Antiretroviral
reverse transcriptase inhibitors, NRTI nucleoside reverse transcriptase inhibitor, therapy; PDR: Pre-treatment drug resistance; NNRTI: Non-nucleoside reverse
PI protease inhibitors transcriptase inhibitors; LNSP: The National Public Health Laboratory; ENDA:
a Environmental action in the third world; VAS: Visual analog scale; VL: Viral load;
Including 10 study participants with current ART use and 1 study participant
qPCR: Quantitative PCR; PCR: Polymerase chain reaction; DRM: Drug resistance
with previous ART use
mutations; AOR: Adjusted odds ratio; NRTI: Nucleoside reverse transcriptase
b
The most common HIVDR in each drug class highlighted in italics inhibitor; MARPs: Most-at-risk-populations.
Acknowledgements
study has also been reported to be common among The authors would first and foremost like to thank all participants in the study.
The listed authors and the members of the Sweden Guinea-Bissau Cohort
patients failing first line ART in the country [42]. Research (SWEGUB CORE) group, including Babetida N’Buna, Antonio Biague,
Female sex workers are a highly mobile and vulner- Ansu Biai, Cidia Camara, Zacarias Jose da Silva, Joakim Esbjörnsson, Marianne
able population in Guinea-Bissau. We therefore used Jansson, Sara Karlson, Jacob Lindman, Patrik Medstrand, Fredrik Månsson,
Hans Norrgren, Gülsen Özkaya Sahin, and Sten Wilhelmson, also wish to thank
a mixed venue-based and chain-referral convenience the staff of the National Public Health Laboratory and ENDA in Bissau, Guinea-
sampling. Hence, it is possible that our study popula- Bissau for their assistance during data collection and sampling handling of
tion is not representative of all FSW in Guinea-Bis- this study.
sau. In addition, we could not adjust for clustering by Authors’ contributions
recruitment chain or venue, other than city, because JL, PM, JE and HN designed the study, oversaw implementation, conducted
data on which participants were recruited by whom statistical analyses, provided interpretation of study findings and drafted
the article. MAD and AB contributed to study design, provided guidance for
or from where were not recorded. It is possible that study conduction and undertook data collection. FM and MJ contributed to
Respondent Driven Sampling could have addressed study design, provided guidance for study conduction and contributed to
these difficulties, but due to budget and resource limita- interpretation of findings. All authors critically revised the article and approved
submission.
tions, we decided to use the more cost-effective mixed
venue-based and chain-referral convenience sampling. Funding
Information on HIV care continuum outcomes mainly Open access funding provided by Lund University. The study was supported
by the Swedish Research council (2013-06541), Lund University (Dnr F:
relied on self-report, and thus subject to social desira- 2014/354) and Region Skåne Research and Development (REGSKANE-826071).
bility and misclassification. Of the HIV positive women
reporting not being on ART, 6.7% had a VL < 1000 cop- Availability of data and materials
The dataset used for the current study is available from the corresponding
ies/ml. Discrepancies between viral suppression and author on reasonable request
self-reporting of not being on ART has been shown also
Lindman et al. AIDS Res Ther (2020) 17:33 Page 10 of 11
Ethics approval and consent to participate programme for prevention of HIV, an integrated response (SAPPH-IRe)
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Consent for publication 17. HIV drug resistance report 2017. Geneva: World Health Organization;
Not applicable. 2017. Licence: CC BY-NC-SA 3.0 IGO.
18. Wilhelmson S, Mansson F, Lopatko Lindman J, Biai A, Esbjornsson J, Nor-
Competing interests rgren H, et al. Prevalence of HIV-1 pretreatment drug resistance among
The authors declare that they have no competing interests. treatment naive pregnant women in Bissau, Guinea Bissau. PLoS One.
2018;13(10):e0206406.
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