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HIV Epidemiology Among Female Sex Workers and Their Clients in The Middle East and North Africa: Systematic Review, Meta-Analyses, and Meta-Regressions

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Chemaitelly et al.

BMC Medicine (2019) 17:119


https://doi.org/10.1186/s12916-019-1349-y

RESEARCH ARTICLE Open Access

HIV epidemiology among female sex


workers and their clients in the Middle East
and North Africa: systematic review, meta-
analyses, and meta-regressions
Hiam Chemaitelly1,3*, Helen A. Weiss2,3, Clara Calvert3, Manale Harfouche1 and Laith J. Abu-Raddad1,4,5*

Abstract
Background: HIV epidemiology among female sex workers (FSWs) and their clients in the Middle East and North
Africa (MENA) region is poorly understood. We addressed this gap through a comprehensive epidemiological assessment.
Methods: A systematic review of population size estimation and HIV prevalence studies was conducted and reported
following PRISMA guidelines. Risk of bias (ROB) assessments were conducted for all included studies using various quality
domains, as informed by Cochrane Collaboration guidelines. The pooled mean HIV prevalence was estimated using
random-effects meta-analyses. Sources of heterogeneity and temporal trends were identified through meta-regressions.
Results: We identified 270 size estimation studies in FSWs and 42 in clients, and 485 HIV prevalence studies in 287,719
FSWs and 69 in 29,531 clients/proxy populations. Most studies had low ROB in multiple quality domains. The median
proportion of reproductive-age women reporting current/recent sex work was 0.6% (range = 0.2–2.4%) and of men
reporting currently/recently buying sex was 5.7% (range = 0.3–13.8%). HIV prevalence ranged from 0 to 70% in FSWs
(median = 0.1%) and 0–34.6% in clients (median = 0.4%). The regional pooled mean HIV prevalence was 1.4% (95% CI =
1.1–1.8%) in FSWs and 0.4% (95% CI = 0.1–0.7%) in clients. Country-specific pooled prevalence was < 1% in most
countries, 1–5% in North Africa and Somalia, 17.3% in South Sudan, and 17.9% in Djibouti. Meta-regressions identified
strong subregional variations in prevalence. Compared to Eastern MENA, the adjusted odds ratios (AORs) ranged from 0.2
(95% CI = 0.1–0.4) in the Fertile Crescent to 45.4 (95% CI = 24.7–83.7) in the Horn of Africa. There was strong evidence for
increasing prevalence post-2003; the odds increased by 15% per year (AOR = 1.15, 95% CI = 1.09–1.21). There was also a
large variability in sexual and injecting risk behaviors among FSWs within and across countries. Levels of HIV testing
among FSWs were generally low. The median fraction of FSWs that tested for HIV in the past 12 months was 12.1%
(range = 0.9–38.0%).
Conclusions: HIV epidemics among FSWs are emerging in MENA, and some have reached stable endemic levels,
although still some countries have limited epidemic dynamics. The epidemic has been growing for over a decade, with
strong regionalization and heterogeneity. HIV testing levels were far below the service coverage target of “UNAIDS 2016–
2021 Strategy.”
Keywords: HIV, Sexually transmitted infections, Sex workers, Sex work, Prevalence, Incidence, Population size, Risk group
size, Middle East and North Africa

* Correspondence: hsc2001@qatar-med.cornell.edu; lja2002@qatar-


med.cornell.edu
1
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar,
Cornell University, Qatar Foundation–Education City, P.O. Box 24144, Doha,
Qatar
Full list of author information is available at the end of the article

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 2 of 30

Background countries extending from Pakistan to Morocco (Add-


The Middle East and North Africa (MENA) is one of only itional file 1: Figure S1), based on the convention in HIV
two regions where HIV incidence and AIDS-related mor- research [6, 7, 10, 11] and on World Health Organization
tality are rising [1]. Between 2000 and 2015, the increase (WHO), UNAIDS, and World Bank definitions [6]. MENA
in the number of new infections was estimated at over a was also classified by subregion comprising Eastern MENA
third, while that of AIDS-related deaths, at over threefold (Afghanistan, Iran, Pakistan), the Fertile Crescent (Egypt,
[1–3]. MENA has been described as “a real hole in terms Iraq, Jordan, Lebanon, Palestine, Syria), the Gulf (Bahrain,
of HIV/AIDS epidemiological data” [4], with unknown Kuwait, Oman, Qatar, Saudi Arabia, United Arab Emirates,
status and scale of epidemics in multiple countries [5–7]. Yemen), the Horn of Africa (Djibouti, Somalia, recently
Despite recent progress in HIV research and surveillance independent South Sudan), and North Africa (Algeria,
in MENA [8], including the conduct of integrated bio- Libya, Morocco, Sudan, Tunisia).
behavioral surveillance surveys (IBBSS) [5, 9], many of these Systematic searches were performed, up to July 29,
data are, at best, published in country-level reports, or never 2018, on ten international-, regional-, and country-level
analyzed. Since 2007, the “MENA HIV/AIDS Epidemiology databases; abstract archives of International AIDS Society
Synthesis Project” has maintained an active regional HIV conferences [14]; and Synthesis Project database which in-
database [6]. The first systematic syntheses of HIV data doc- cludes country-level and international organizations’
umented concentrated and emerging epidemics among reports and routine data reporting [6, 7] (Additional file 1:
men who have sex with men (MSM) [10] and people who Box S1). No language or year restrictions were used.
inject drugs (PWID) [11]. The majority of these epidemics Titles and abstracts of unique citations were screened for
emerged within the last two decades [10, 11]. relevance, and full texts of relevant/potentially relevant
Although the size of commercial heterosexual sex net- citations were retrieved for further screening. Any docu-
works is expected to be much larger than the risk networks ment/report including outcomes of interest based on pri-
of MSM and PWID [6, 7], estimates for the population mary data was eligible for inclusion. Case reports, case
proportion of female sex workers (FSWs), volume of clients series, editorials, commentaries, and studies in populations
they serve, and geographic and temporal trends in infection (such as “vulnerable women”) where overlap with FSWs is
remain to be established. This evidence gap was implied but engagement in sex work is not explicitly indi-
highlighted in the latest gap report by the Joint United Na- cated were excluded. Reference lists of reviews and all rele-
tions Programme on HIV/AIDS (UNAIDS) [3], indicating vant documents were hand searched for eligible reports.
“a lack of data on the burden of HIV among sex workers in In this article, the term study refers to a specific out-
the region” and stressing that “the epidemic among them is come measure (population size estimate, incidence, or
poorly understood” though “HIV in every country is prevalence) in a specific population. Therefore, one report
expected to disproportionately affect sex workers” [3]. could contribute multiple studies, and one study could be
This study characterizes HIV epidemiology among published in different reports. Duplicate study results were
FSWs and their clients in MENA by (1) systematically included only once using the more detailed report.
reviewing and synthesizing all available published and un-
published records documenting population size estimates, Data extraction and synthesis
population proportions, HIV incidence, and HIV preva- Data extraction was performed by HC and double extrac-
lence (including in proxy populations of clients such as tion by MH, with discrepancies settled by consensus or by
male sexually transmitted infection (STI) clinic attendees); contacting authors. Data were extracted from full texts by
(2) estimating, for each population, the pooled mean HIV native speakers (extraction list in Additional file 1: Box S2).
prevalence per country and regionally; (3) identifying the Population size estimates and population proportions
regional-level associations with prevalence, sources of het- were grouped based on being of national coverage or for
erogeneity, and temporal trends; and (4) synthesizing the specific subnational settings, and distinguishing between
key measures of sexual and injecting risk behaviors. current FSWs/clients and history of sex work/ex-client.
For FSWs, population proportion is defined as the pro-
Methods portion of all reproductive-age women that are engaged
Search strategy and selection criteria in sex work, that is the exchange of sex for money (sex
Evidence for population size estimate, population propor- work as a profession) [15, 16], and for clients, as the
tion, HIV incidence, and HIV prevalence in FSWs and proportion of men buying sex from FSWs using money.
clients was systematically reviewed as per Cochrane’s Col- Studies with mixed or non-representative samples (sam-
laboration guidelines [12]. Findings were reported following ples biased towards oversampling FSWs with no esti-
the Preferred Reporting Items for Systematic Reviews and mate adjustment) were excluded.
Meta-analyses (PRISMA) guidelines [13] (checklist in Add- Due to the paucity of studies directly looking at HIV
itional file 1: Table S1). MENA definition here includes 23 prevalence in clients of FSW, HIV prevalence studies in
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 3 of 30

male STI clinic attendees, or mixed-sex samples of pre- to allow for sampling variation and true heterogeneity [25,
dominantly men (> 60%), were used as a proxy for HIV 26]. Overall prevalence measures were replaced by their
prevalence in clients of FSWs [17, 18]. stratified measures where applicable.
Based on meta-analysis results for the pooled HIV preva- Heterogeneity was assessed using Cochran’s Q statistic to
lence in FSWs, epidemics were classified as concentrated confirm the existence of heterogeneity, I2 to estimate the
(prevalence > 5%), intermediate-intensity (prevalence magnitude of between-study variation, and prediction inter-
between 1 and 5%), and low-level (prevalence < 1%), as vals to estimate the 95% interval of distribution of true ef-
informed by epidemiological relevance and existing conven- fect sizes [26, 27].
tions [19–21]. Meta-analyses were implemented in R version 3.4.2 [28].
HIV incidence studies were identified and reported. Add-
itional contextual information was extracted from FSW Meta-regression analyses
studies included in the review. These include age, age at Random-effects meta-regression analyses were con-
sexual debut, age at sex work initiation, sex work duration, ducted to identify the regional-level associations with
marital status, and HIV/AIDS knowledge and perception of HIV prevalence in FSWs, sources of between-study het-
risk, as well as behavioral measures of condom use, inject- erogeneity, and temporal trend. Independent variables
ing drug use, sexual partnerships, and HIV testing. considered a priori were country/subregion, FSW popu-
Data were summarized using medians and ranges. lation type, sample size, median year of data collection,
sampling methodology, response rate, validity of sex
Quality assessment work definition, and HIV ascertainment (details in Add-
Risk of bias (ROB) assessments for population size esti- itional file 1: Table S3). The same factors (as applicable)
mates/population proportions and for HIV prevalence were considered for clients’ meta-regression analyses.
were conducted as informed by Cochrane Collaboration To avoid the exclusion of studies with zero prevalence,
guidelines [12] (criteria in Additional file 1: Table S2). an increment of 0.1 was added to the number of events
Briefly, size estimation studies were classified as having in all studies to calculate the log-transformed odds, that
“low” versus “high” ROB on each of the three domains is prevalence/(1 − prevalence), and corresponding vari-
assessing the (1) validity of sex work definition/engagement ance [29]. Factors showing strong evidence for an associ-
in paid sex (clear/valid definition; otherwise), (2) rigor of ation with the odds (p value ≤ 0.10) in univariable
estimation methodology (likely-to-yield representative esti- analysis were included in the multivariable analysis.
mate; otherwise), and (3) response rate (≥ 60%; < 60%). Meta-regressions were implemented in Stata/SE v.15.1 [30].
Prevalence studies were similarly classified on each of the
four domains assessing the (1) validity of sex work defin- Results
ition/engagement in paid sex (clear/valid definition; other- Search results and scope of evidence
wise), (2) rigor of sampling methodology (probability-based; Figure 1 shows the study selection process. A total of 16,
non-probability-based), (3) response rate (≥ 60% or ≥ 60% 131 citations were identified through databases. After ex-
of target sample size reached for studies using respondent- cluding duplicates and title and abstract screening, full texts
driven or time-location sampling; < 60%), and (4) type of of 336 unique citations were screened, and 87 reports were
HIV ascertainment (biological assays; self-report). eligible for inclusion. Hand-searching of reference lists of
Studies with missing information for a specific domain relevant reports yielded eight additional eligible reports.
were classified as having “unclear” ROB for that domain. Searching US Census Bureau and UNAIDS databases
Measures only extracted from routine databases were con- yielded 173 additional measures. Sixty-three detailed
sidered of unknown quality, as original reports were not country-level reports, 11 of which replaced eligible articles,
available for assessing ROB, and were not included in the and 134 additional measures were further identified
quality assessment. The impact of quality domains on through Synthesis Project database. In sum, data from 147
observed prevalence was examined in meta-regression eligible reports and 307 additional measures were included.
(described below). These yielded in total 312 size estimation, 6 HIV incidence,
and 554 HIV prevalence measures in FSWs and clients.
Meta-analyses Evidence for population size and/or population propor-
Pooled mean HIV prevalence in FSWs and client popula- tion of FSWs was available for 12 out of 23 MENA coun-
tions were estimated using random-effects meta-analyses, tries (270 studies). Population size/population proportion
by country and for the whole region. Variances were stabi- of clients was available in 42 studies from 10 countries. All
lized using Freeman-Tukey-type arcsine square-root 6 HIV incidence studies were among FSWs. A total of 485
transformation [22, 23]. Weighting was performed using HIV prevalence studies were identified in 287,719 FSWs
the inverse-variance method [23, 24]. Pooling was per- from 17 countries and 69 HIV prevalence studies in 29,531
formed using Dersimonian-Laird random-effects models clients (or proxy populations) from 10 countries. Prevalence
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 4 of 30

Fig. 1 Flow chart of the study selection process in the systematic review following PRISMA guidelines [13]

measures in FSWs and clients contributed respectively 674 reproductive-age women aged 15–49 years) was 0.6%
and 147 stratified measures for the meta-analyses (overall (range across studies = 0.2% in Egypt to 2.4% in Iran). The
prevalence measures were replaced by their strata in meta- median population proportion of current/recent clients
analyses). For all types of measures, there was a high het- (buying sex from FSWs in the past year) based on diverse
erogeneity in data availability across countries. samples of general population men was 5.7% (range across
studies = 0.3% in Sudan to 13.8% in Lebanon).
Population size estimates and population proportions of With high heterogeneity in estimation methodology, time
FSWs and clients frame, and scope between and within countries, it was
Table 1 and Additional file 1: Table S4 show the popula- deemed not meaningful to generate country-specific or re-
tion size estimate and population proportion studies for gional-pooled estimates for the size/population proportions.
FSWs and clients at the national and subnational levels,
respectively. At the national level, the median number of HIV incidence overview
current/recent FSWs (engaged in sex work in the past There were six incidence studies among FSWs (three
year) was 58,934 (range = 2218 in Djibouti to 167,501 in from each of Somalia and Djibouti; data not shown).
Pakistan), and the median population proportion (out of Three studies reported zero seroconversions [51, 52].
Table 1 Estimates of some national representation for the number and population proportion of FSWs, and the number and population proportion of clients of FSWs, in the
Middle East and North Africa (MENA) reported by identified studies
Country Author, year Year(s) of Estimation Sample type Reported size estimate
[citation] data collection methodology
Time frame N Range %* Range*
FSWs Egypt Bahaa, 2010 [31] 2004–2008 Convenience sample Women seeking VCT NR NR NR 0.4 NR
(self-report) testing
Jacobsen, 2014 [32] 2014 Enumeration (time-location FSWs in urban locations Current 22,986 6460–26,792 0.24 NR
geographical mapping)
Djibouti WHO, 2011 [33] 2009 NR FSWs NR 1000 NR NR NR
Chemaitelly et al. BMC Medicine

WHO, 2011 [33] 2011 Capture-recapture FSWs Current 2218 NR NR NR


Iran WHO, 2011 [33] 2010 Network scale-up General pop Current 80,000 NR NR NR
Sharifi, 2017 [34] 2015 Multiplier unique object FSWs Current 19,800 10,900–38,100 0.31 0.17–
0.58
(2019) 17:119

Sharifi, 2017 [34] 2015 Network scale-up General pop Current 98,500 87,000–109,400 1.54 1.36–
1.71
Sharifi, 2017 [34] 2015 Wisdom of the crowds FSWs Current 152,200 93,400–21,4300 2.38 1.46–
3.35
Lebanon Kahhaleh, 2009 [35] 1996 Pop-based survey (self-report) General pop (15–49 years) Past 12 M NR NR 0.54 NR
Kahhaleh, 2009 [35] 2004 Pop-based survey (self-report) General pop (15–49 years) Past 12 M NR NR 0.53 NR
Morocco WHO, 2011 [33] 2010 NR FSWs Current 67,000 NR NR NR
Bennani, 2013 [36] 2011 Multiplier unique object FSWs Past 6 M 85,000 NR NR NR
MOH, 2013 [37] 2013 Pop-based survey (self-report) Young women (15–24 years) Lifetime NR NR 6.9 NR
MOH, 2013 [37] 2013 Pop-based survey (self-report) Young women (15–24 years) Current NR NR 2.4 NR
Pakistan NACP, 2005 [38] 2005 Enumeration (time-location Brothel, kothikhana, home, Current 35,050 30,300–39,800 0.78 NR
(round I) geographical mapping) and street-based FSWs
Emmanuel, 2010 [39] 2006 Enumeration (time-location Brothel, kothikhana, home, Current 167,501 NR 0.44 NR
(round II) geographical mapping) and street-based FSWs
Emmanuel, 2013 2011–2012 Enumeration (time-location Brothel, kothikhana, home, Current 89,178 78,778–99,592 0.72 NR
[40, 41] (round IV) geographical mapping) and street-based FSWs
NACP, 2017 [42] 2016–2017 Enumeration (time-location Brothel, kothikhana, home, Current 64,829 57,734–70,428 NR NR
(round V) geographical mapping) and street-based FSWs
Sudan AFROCENTER Group, 2005 Self-report (convenience Young women NR NR NR 0.4 NR
2005 [43] sample)
Syria WHO, 2011 [33] 2011 NR FSWs Current 50,000 NR NR NR
Tunisia WHO, 2011 [33] 2005 NR FSWs Current NR 1000–5000 NR NR
WHO, 2011 [33] 2009 NR FSWs Current 10,000 NR NR NR
WHO, 2011 [33] 2011 NR FSWs Current 25,500 NR NR NR
Yemen MOH, 2010 [44] NR Enumeration (time-location FSWs Current 58,934 NR NR 1.16–2.10
geographical mapping)
Page 5 of 30
Table 1 Estimates of some national representation for the number and population proportion of FSWs, and the number and population proportion of clients of FSWs, in the
Middle East and North Africa (MENA) reported by identified studies (Continued)
Country Author, year Year(s) of Estimation Sample type Reported size estimate
[citation] data collection methodology
Time frame N Range %* Range*
Clients Afghanistan Todd, 2007 [45] 2005–2006 Pop-based survey (self-report) TB patients receiving Lifetime NR NR 3.57 NR
of FSWs treatment
Todd, 2012 [46] 2010–2011 Pop-based survey (self-report) Army recruits Lifetime NR NR 12.5 NR
Egypt Bahaa, 2010 [31] 2004–2008 Convenience sample (self-report) Men seeking VCT testing NR NR NR 0.9 NR
Chemaitelly et al. BMC Medicine

Lebanon Kahhaleh, 2009 [35] 1996 Pop-based survey (self-report) General pop (15–49 years) Past 12 M NR NR 9.7 NR
Adib, 2002 [47] 1999 Pop-based survey (self-report) Military conscripts Past 12 M NR NR 13.84 NR
Kahhaleh, 2009 [35] 2004 Pop-based survey (self-report) General pop (15–49 years) Past 12 M NR NR 5.65 NR
Morocco MOH, 2007 [48] 2007 Pop-based survey (self-report) Young men (15–24 years) Lifetime NR NR 35.3 NR
MOH, 2007 [48] 2007 Pop-based survey (self-report) Young men (15–24 years) Current NR NR 2 NR
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MOH, 2013 [37] 2013 Pop-based survey (self-report) Young men (15–24 years) Lifetime NR NR 10.5 NR
MOH, 2013 [37] 2013 Pop-based survey (self-report) Young men (15–24 years) Current NR NR 0.3 NR
Pakistan Mir, 2013 [49] 2007 Pop-based survey (self-report) Urban men (16–45 years) Lifetime NR NR 11.9 NR
Mir, 2013 [49] 2007 Pop-based survey (self-report) Urban men (16–45 years) Past 12 M NR NR 5.8 NR
Sudan NACP, 2004 [50] 2004 Convenience sample (self-report) Military personnel NR NR NR 0.3 NR
AFROCENTER Group, 2005 Convenience sample (self-report) Young men NR NR NR 0.5 NR
2005 [43]
The table is sorted by year(s) of data collection
Abbreviations: FSWs female sex workers, M months, MOH Ministry of Health, NACP National AIDS Control Programme, NR not reported, Pop population, TB tuberculosis, VCT voluntary counseling and testing, WHO World
Health Organization
*The decimal places of the population proportion figures are as reported in the original reports
Page 6 of 30
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 7 of 30

One study from Somalia reported a cumulative inci- FSWs), while 0.7% and 6.1% had high ROB on ≥ 2 do-
dence of 2.6% after 6 months of follow-up [51]. The mains, respectively.
other two from Djibouti—among predominantly Ethiop-
ian FSWs (91%)—reported a cumulative incidence of Pooled mean HIV prevalence
3.4% [51] and 11.6% [51] after 3 and 9 months of follow- The pooled mean HIV prevalence for the MENA region
up, respectively. All incidence studies were conducted was 1.4% (95% confidence interval (CI) = 1.1–1.8%) in
before the year 2000 and were limited in scale and FSWs and 0.4% (95% CI = 0.1–0.7%) in clients (Table 5).
scope. A difference was observed between the median preva-
lence and the pooled mean prevalence due to the high
clustering of prevalence measures close to zero.
HIV prevalence overview
In FSWs, the national-level pooled mean prevalence
HIV prevalence in FSWs ranged from 0 to 70%, with a
was 0 or < 1% in most countries (low-level epidemics);
median of 0.1% (Tables 2 and 3 and Additional file 1:
between 1 and 5% (intermediate-intensity epidemics) in
Table S5). There was a high heterogeneity, with almost
Algeria, Libya, Morocco, Somalia, and Sudan; and > 5%
half of the studies (46.8%) reporting zero prevalence.
(concentrated epidemics) in Djibouti (17.9%, 95% CI =
The median prevalence was 0% (range = 0–14%), 2.0%
13.6–22.6%) and South Sudan (17.3%, 95% CI = 8.7–
(range = 0–47.1%), and 18.8% (range = 0–70%) in coun-
28.1%).
tries with low-level (prevalence < 1%), intermediate-
In clients/male STI clinic attendees, the national-level
intensity (prevalence 1–5%), and concentrated epidemics
pooled mean prevalence was mostly 0 or < 1%. However,
(prevalence > 5%), respectively (epidemic classification
high prevalence was estimated in Djibouti (5.4%, 95% CI
based on the results of meta-analyses; see below and
= 1.5–10.8%) and South Sudan (13.5%, 95% CI = 4.5–
Table 5). Ranges indicated pockets of higher HIV preva-
28.8%).
lence, even in countries with low-level and intermediate-
There was evidence for the heterogeneity in effect size
intensity epidemics.
(prevalence) in meta-analyses. p value for Cochran’s Q
In clients/male STI clinic attendees, HIV prevalence
statistic was mostly < 0.0001, prediction intervals were
ranged from 0 to 34.6%, with a median of 0.4% (Table 4)
wide, and I2 was often > 50% indicating that most
. Studies also showed high heterogeneity with 37.7%
between-study variability is due to the true differences in
reporting zero prevalence. The median prevalence was
prevalence across studies rather than chance.
0% (range = 0–1.1%), 0.6% (range = 0–9.6%), and 7.4%
(range = 0.8–34.6%) in countries with low-level,
Associations with prevalence, sources of between-study
intermediate-intensity, and concentrated epidemics, re-
heterogeneity, and temporal trend
spectively. Ranges indicated pockets of higher HIV
Univariable meta-regressions for FSWs demonstrated
prevalence in countries with intermediate-intensity
strong evidence for an association with odds for sub-
epidemics.
region, population type, sample size, year of data collec-
tion, and response rate (Table 6). Meanwhile, there was
Quality assessment poor evidence for an association with sampling method-
Additional file 1: Tables S6-S9 show the summarized ology, validity of sex work definition, and HIV ascertain-
and study-specific quality assessments for the size esti- ment, which were hence dismissed from inclusion in the
mation and HIV prevalence studies in FSWs and clients. multivariable model. Most variability in odds was ex-
Almost all size estimation studies used clear/valid sex plained by subregion (adjusted R2 = 39.8%).
work definitions, and > 70% used rigorous size estima- Multivariable analysis indicated strong subregional dif-
tion methodologies. Similarly, > 70% of prevalence stud- ferences and explained 49.2% of the variation (Table 6).
ies in FSWs used clear/valid sex work definitions and Compared to Eastern MENA, the adjusted odds ratio
probability-based sampling for participants’ recruitment. (AOR) ranged from 0.2 (95% CI = 0.1–0.4) for the Fer-
Meanwhile, > 85% of prevalence studies in clients used tile Crescent to 45.4 (95% CI = 24.7–83.7) for the Horn
convenience sampling. of Africa. Studies with a larger sample size (≥ 100)
Overall, studies were of reasonable quality. The major- showed lower odds (AOR = 0.4, 95% CI = 0.2–0.6).
ity of size estimation studies in FSWs and clients had Compared with studies with data collection pre-1993,
low ROB on ≥ 2 quality domains (94.4% and 82.1%, re- studies conducted after 2003 showed strong evidence for
spectively), and none had high ROB on ≥ 2 domains. higher odds (AOR = 2.0, 95% CI = 1.2–3.3). Notably, the
Similarly, 85.0% of prevalence studies in FSWs and trend of increasing odds was evident only after control-
39.4% of studies in clients had low ROB on ≥ 2 domains ling for the strong confounding effect of the subregion.
(studies among STI clinic attendees mostly used con- The trend for each subregion was also overall increasing,
venience sampling, and few reported on contact with though the strength of evidence varied across subregions
Table 2 HIV prevalence in FSWs in the Middle East and North Africa (MENA), as reported in studies using probability-based sampling
Country Author, year [citation] Year(s) of City/province Study site Sampling Population Sample HIV prevalence*
data collection size
% 95% CI
Afghanistan SAR AIDS HDS, 2008 [53] 2006–2007 Jalalabad Community TLS FSWs 45 0 NR
SAR AIDS HDS, 2008 [53] 2006–2007 Mazar-i-Sharif Community TLS FSWs 87 0 NR
NACP, 2010 [54] (round I) 2009 Kabul Community RDS FSWs 368 0 NR
NACP, 2012 [55] (round II) 2012 Herat Community RDS FSWs 344 0.9 NR
Chemaitelly et al. BMC Medicine

NACP, 2012 [55] (round II) 2012 Kabul Community RDS FSWs 333 0 NR
NACP, 2012 [55] (round II) 2012 Mazar-i-Sharif Community RDS FSWs 355 0 NR
Egypt MOH, 2006 [56] (round I) 2006 Cairo Community Conv** FSWs 118 0.8 NR
MOH, 2010 [57] (round II) 2010 Cairo Community Conv** FSWs 200 0 NR
Iran Navadeh, 2012 [58] 2010 Kerman Community RDS FSWs 139 0 NR
(2019) 17:119

Sajadi, 2013 [59] (round I) 2010 National Facilities serving MCS FSWs 817 4.5 NR
vulnerable women
Kazerooni, 2014 [60] 2010–2011 Shiraz Community RDS FSWs 278 4.7 NR
Moaeyedi-Nia, 2016 [61] 2012–2013 Tehran Community RDS FSWs 161 5 NR
Mirzazadeh, 2016 [62] (round II) 2015 National Facilities serving MCS FSWs 1337 2.1 0.9–4.6
vulnerable women
Karami, 2017 [63] 2016 Tehran Community TLS FSWs 369 4.6 NR
Jordan WHO, 2011 [33] (round I) 2009 National Community RDS FSWs 225 0 NR
MOH, 2014 [64] (round II) 2013 Amman Community RDS FSWs 358 0.6 NR
MOH, 2014 [64] (round II) 2013 Irbid Community RDS FSWs 102 0 NR
MOH, 2014 [64] (round II) 2013 Zarqa Community RDS FSWs 212 0.5 NR
Lebanon Mahfoud, 2010 [65] 2007–2008 Greater Beirut Community RDS FSWs 95 0 NR
Libya Valadez, 2013 [66] (round I) 2010–2011 Tripoli Community RDS FSWs 69 15.7 3.2–32.6
Morocco MOH, 2012 [67] 2011–2012 Agadir Community RDS FSWs 364 5.1 2.1–8.6
MOH, 2012 [67] 2011–2012 Fes Community RDS FSWs 359 1.8 0–2.1
MOH, 2012 [67] 2011–2012 Rabat Community RDS FSWs 392 0 NR
MOH, 2012 [67] 2011–12 Tanger Community RDS FSWs 319 1.4 0.4–3.3
Pakistan Bokhari, 2007 [68] 2004 Lahore Red-light district SyCS FSWs 378 0.5 NR
NACP, 2005 [38] (round I) 2005 Faisalabad Community RDS and TLS Kothikhana, home, and 400 0 NR
street-based FSWs
NACP, 2005 [38] (round I) 2005 Hyderabad Community SyRS, RDS, and TLS Brothel, kothikhana, home, 400 0 NR
and street-based FSWs
Page 8 of 30
Table 2 HIV prevalence in FSWs in the Middle East and North Africa (MENA), as reported in studies using probability-based sampling (Continued)
Country Author, year [citation] Year(s) of City/province Study site Sampling Population Sample HIV prevalence*
data collection size
% 95% CI
NACP, 2005 [38] (round I) 2005 Karachi Community SyRS, RDS, and TLS Brothel, kothikhana, home, 400 0.8 NR
and street-based FSWs
NACP, 2005 [38] (round I) 2005 Lahore Community SyRS, RDS, and TLS Brothel, kothikhana, home, 400 0 NR
and street-based FSWs
NACP, 2005 [38] (round I) 2005 Multan Community Conv (take all), RDS, and TLS Brothel, kothikhana, home, 400 0 NR
and street-based FSWs
Chemaitelly et al. BMC Medicine

NACP, 2005 [38] (round I) 2005 Peshawar Community MCS Kothikhana, home, and 359 0 NR
street-based FSWs
NACP, 2005 [38] (round I) 2005 Quetta Community RDS and MCS Kothikhana, home, and 411 0.7 NR
street-based FSWs
NACP, 2005 [38] (round I) 2005 Sukkur Community RDS and TLS Kothikhana, home, and 368 0 NR
(2019) 17:119

street-based FSWs
NACP, 2007 [69] (round II) 2006 Bannu Community SyRS and MCS Kothikhana, home, and 194 0 NR
street-based FSWs
NACP, 2007 [69] (round II) 2006 Faisalabad Community SyRS and MCS Kothikhana, home, and 400 0 NR
street-based FSWs
NACP, 2007 [69] (round II) 2006 Gujranwala Community SyRS and MCS Kothikhana, home, and 400 0 NR
street-based FSWs
NACP, 2007 [69] (round II) 2006 Hyderabad Community SyRS and MCS Brothel, kothikhana, home, 398 0.3 NR
and street-based FSWs
NACP, 2007 [69] (round II) 2006 Karachi Community SyRS and MCS Brothel, kothikhana, home, 403 0 NR
and street-based FSWs
NACP, 2007 [69] (round II) 2006 Lahore Community SyRS and MCS Brothel, kothikhana, home, 425 0.02 NR
and street-based FSWs
NACP, 2007 [69] (round II) 2006 Larkana Community SyRS and MCS Brothel, kothikhana, home, 400 0 NR
and street-based FSWs
NACP, 2007 [69] (round II) 2006 Multan Community SyRS and MCS Brothel, kothikhana, home, 400 0 NR
and street-based FSWs
NACP, 2007 [69] (round II) 2006 Peshawar Community SyRS and MCS Kothikhana, home, street-based, 423 0 NR
and other FSWs
NACP, 2007 [69] (round II) 2006 Quetta Community SyRS and MCS Kothikhana, home, street-based, 398 0 NR
and other FSWs
NACP, 2007 [69] (round II) 2006 Sargodha Community SyRS and MCS Kothikhana, home, street-based, 400 0 NR
and other FSWs
NACP, 2007 [69] (round II) 2006 Sukkur Community SyRS and MCS Kothikhana, home, street-based, 400 0 NR
and other FSWs
Hawkes, 2009 [70] 2007 Abbottabad Community RDS FSWs 107 0 NR
Hawkes, 2009 [70] 2007 Rawalpindi Community RDS FSWs 426 0 NR
Page 9 of 30
Table 2 HIV prevalence in FSWs in the Middle East and North Africa (MENA), as reported in studies using probability-based sampling (Continued)
Country Author, year [citation] Year(s) of City/province Study site Sampling Population Sample HIV prevalence*
data collection size
% 95% CI
Khan, 2011 [71] 2007 Lahore Community RDS FSWs 730 0.7 NR
NACP, 2010 [72] (special 2009 Punjab and Sindh Community SyRS and MCS FSWs 2197 1.0 NR
IBBSS among FSWs)
NACP, 2012 [40] (round IV) 2012 DG Khan Community SyRS and MCS Kothikhana, home, street-based, 375 0.5 0.1–1.9
and other FSWs
Chemaitelly et al. BMC Medicine

NACP, 2012 [40] (round IV) 2012 Faisalabad Community SyRS and MCS Kothikhana, home, street-based, 376 0 NR
and other FSWs
NACP, 2012 [40] (round IV) 2012 Haripur Community SyRS and MCS Kothikhana, home, street-based, 211 0.9 0.3–3.4
and other FSWs
NACP, 2012 [40] (round IV) 2012 Karachi Community SyRS and MCS Brothel, kothikhana, home, 377 1.9 0.9–3.8
street-based, and other FSWs
(2019) 17:119

NACP, 2012 [40] (round IV) 2012 Lahore Community SyRS and MCS Brothel, kothikhana, home, 375 0.5 0.1–1.9
street-based, and other FSWs
NACP, 2012 [40] (round IV) 2012 Larkana Community SyRS and MCS Brothel, kothikhana, home, 375 1.9 0.9–3.8
street-based, and other FSWs
NACP, 2012 [40] (round IV) 2012 Multan Community SyRS and MCS Brothel, kothikhana, home, 375 0.3 0.05–1.5
street-based, and other FSWs
NACP, 2012 [40] (round IV) 2012 Peshawar Community SyRS and MCS Kothikhana, home, street-based, 367 0 NR
and other FSWs
NACP, 2012 [40] (round IV) 2012 Quetta Community SyRS and MCS Kothikhana, home, street-based, 345 0 NR
and other FSWs
NACP, 2012 [40] (round IV) 2012 Rawalpindi Community SyRS and MCS Kothikhana, home, street-based, 375 0 NR
and other FSWs
NACP, 2012 [40] (round IV) 2012 Sargodha Community SyRS and MCS Brothel, kothikhana, home, 345 0.3 0.05–1.6
street-based, and other FSWs
NACP, 2012 [40] (round IV) 2012 Sukkur Community SyRS and MCS Kothikhana, home, street-based, 375 0.8 0.3–2.3
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Bahawalpur Community SyRS and MCS Kothikhana, home, street-based, 351 0 NR
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Bannu Community SyRS and MCS Kothikhana, home, street-based, 196 1.5 1–4.4
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 DG Khan Community SyRS and MCS Kothikhana, home, street-based, 364 0.8 0.3–2.4
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Gujranwala Community SyRS and MCS Kothikhana, home, street-based, 304 0.7 0.2–2.4
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Gujrat Community SyRS and MCS Kothikhana, home, street-based, 250 0.4 0.1–2.2
and other FSWs
Page 10 of 30
Table 2 HIV prevalence in FSWs in the Middle East and North Africa (MENA), as reported in studies using probability-based sampling (Continued)
Country Author, year [citation] Year(s) of City/province Study site Sampling Population Sample HIV prevalence*
data collection size
% 95% CI
NACP, 2017 [42] (round V) 2016–2017 Hyderabad Community SyRS and MCS Kothikhana, home, street-based, 364 2.2 1.1–4.3
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Karachi Community SyRS and MCS Brothel, kothikhana, home, 387 2.6 1.4–4.7
street-based, and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Kasur Community SyRS and MCS Kothikhana, home, street-based, 364 0 NR
and other FSWs
Chemaitelly et al. BMC Medicine

NACP, 2017 [42] (round V) 2016–2017 Larkana Community SyRS and MCS Brothel, kothikhana, home, 364 4.1 2.5–6.7
street-based, and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Mirpurkhas Community SyRS and MCS Kothikhana, home, street-based, 364 4.1 2.5–6.7
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Nawabshah Community SyRS and MCS Kothikhana, home, street-based, 364 3.8 2.3–6.4
(2019) 17:119

and other FSWs


NACP, 2017 [42] (round V) 2016–2017 Peshawar Community SyRS and MCS Kothikhana, home, street-based, 265 3 1.5–5.8
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Quetta Community SyRS and MCS Kothikhana, home, street-based, 364 0 NR
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Rawalpindi Community SyRS and MCS Kothikhana, home, street-based, 364 0.3 0.1–1.5
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Sheikhupura Community SyRS and MCS Kothikhana, home, street-based, 363 1.7 1.1–4.9
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Sialkot Community SyRS and MCS Kothikhana, home, street-based, 193 0 NR
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Sukkur Community SyRS and MCS Kothikhana, home, street-based, 364 8.8 6.3–12.2
and other FSWs
NACP, 2017 [42] (round V) 2016–2017 Turbat Community SyRS and MCS Kothikhana, home, street-based, 72 0 NR
and other FSWs
Somalia Testa, 2008 [73] (round I) 2008 Hargeisa Community RDS FSWs 237 5.2 2.5–8.5
IOM, 2017 [74] (round II) 2014 Hargeisa Community RDS FSWs 96 4.8 0.2–9.3
Sudan Elkarim, 2002 [75] 2002 National Community MSysRS FSWs 367 4.4 NR
Abdelrahim, 2010 [76] 2008 Khartoum Community RDS FSWs 321 0.9 0.1–2.2
NACP, 2010 [77] 2008–09 Gezira Community RDS FSWs 267 0.1 NR
NACP, 2012 [78] 2011 Alshamalia Community RDS FSWs 305 0.3 0–1
NACP, 2012 [78] 2011 Blue Nile Community RDS FSWs 279 1.5 0–3
NACP, 2012 [78] 2011 Gadarif Community RDS FSWs 282 0.6 0–1
NACP, 2012 [78] 2011 Gezira Community RDS FSWs 296 0.7 0–1
NACP, 2012 [78] 2011 Kassala Community RDS FSWs 288 5.0 2–8
Page 11 of 30

NACP, 2012 [78] 2011 Khartoum Community RDS FSWs 287 0 NR


Table 2 HIV prevalence in FSWs in the Middle East and North Africa (MENA), as reported in studies using probability-based sampling (Continued)
Country Author, year [citation] Year(s) of City/province Study site Sampling Population Sample HIV prevalence*
data collection size
% 95% CI
NACP, 2012 [78] 2011 North Darfur Community RDS FSWs 303 0.7 0–3
NACP, 2012 [78] 2011 North Kordofan Community RDS FSWs 296 1 0–3
NACP, 2012 [78] 2011 Red Sea Community RDS FSWs 293 7.7 4–12
NACP, 2012 [78] 2011 River Nile Community RDS FSWs 291 0.7 0–2
NACP, 2012 [78] 2011 Sinnar Community RDS FSWs 303 0.7 0–2
Chemaitelly et al. BMC Medicine

NACP, 2012 [78] 2011 South Darfur Community RDS FSWs 299 0.2 0–1
NACP, 2012 [78] 2011 West Darfur Community RDS FSWs 284 1 0–3
NACP, 2012 [78] 2011 White Nile Community RDS FSWs 288 1.3 0–3
MOH, 2016 [79] 2015–2016 Juba, South Sudan Community RDS FSWs 835 37.9 33.6–42.2
(2019) 17:119

Tunisia Hsairi, 2012 [80] 2009 Tunis, Sfax, Community RDS Street-based FSWs 703 0.4 NR
and Sousse
Hsairi, 2012 [80] 2011 Tunis Community TLS Street-based FSWs 357 0.6 0–1.3
Hsairi, 2012 [80] 2011 Sfax Community TLS Street-based FSWs 284 0 NR
Hsairi, 2012 [80] 2011 Sousse Community TLS Street-based FSWs 347 1.2 0.02–2.3
Yemen Stulhofer, 2008 [81] (round I) 2008 Aden Community RDS FSWs 244 1.3 0–2.9
MOH, 2014 [82] (round I) 2010–2011 Hodeida Community RDS FSWs 301 0 NR
The table is sorted by year(s) of data collection
Abbreviations: CI confidence interval, Conv convenience, FSWs female sex workers, IBBSS integrated bio-behavioral surveillance survey, IOM International Organization for Migration, MCS multistage cluster sampling,
MOH Ministry of Health, MSyRS multistage systematic random sampling, NACP National AIDS Control Programme, NR not reported, RDS respondent-driven sampling, SAR AIDS HDS South Asia Region AIDS Human
Development Sector, SyCS systematic cluster sampling, SyRS systematic random sampling, TLS time-location sampling, WHO World Health Organization
*The decimal places of the prevalence figures are as reported in the original reports, but prevalence figures with more than one decimal places were rounded to one decimal place, with the exception of those below
0.1%. Most studies did not report the 95% CIs associated with prevalence
**Integrated bio-behavioral surveillance survey with sampling initially planned as respondent-driven but ended up being a convenience for logistical reasons
Page 12 of 30
Table 3 HIV prevalence in FSWs in the Middle East and North Africa (MENA), as reported in studies using non-probability sampling
Country Author, year Year(s) of City/province Study site Sampling Population Sample HIV prevalence*
[citation] data collection size
% 95% CI
Afghanistan Todd, 2010 [83] 2006–2008 Jalalabad, Kabul, and Community and NGO Conv FSWs 520 0.2 0.01–1.1
Mazar-i-Sharif
Djibouti Rodier, 1993 [84] 1987 Djibouti STI clinic Conv Street-based FSWs 66 4.6 NR
Rodier, 1993 [84] 1987 Djibouti STI clinic Conv Bar hostesses 221 1.4 NR
Constantine, 1992 1988 Djibouti NR Conv FSWs 33 18.2 NR
Chemaitelly et al. BMC Medicine

[52]
Rodier, 1993 [84] 1988 Djibouti STI clinic Conv Street-based FSWs 78 9.0 NR
Rodier, 1993 [84] 1988 Djibouti STI clinic Conv Bar hostesses 255 2.7 NR
Rodier, 1993 [84] 1990 Djibouti STI clinic Conv Street-based FSWs 116 41.7 NR
Rodier, 1993 [84] 1990 Djibouti STI clinic Conv Bar hostesses 180 5.0 NR
(2019) 17:119

Couzineau, 1991 1991 Djibouti STI clinic Conv Street-based FSWs 300 43 NR
[85]
Couzineau, 1991 [85] 1991 Djibouti STI clinic Conv Bar girls 397 13.1 NR
Rodier, 1993 [84] 1991 Djibouti STI clinic and residences Conv Street-based FSWs 292 36.0 NR
Rodier, 1993 [84] 1991 Djibouti STI clinic and residences Conv Bar hostesses 360 15.3 NR
Philippon, 1997 [86] 1995 Djibouti STI clinic Conv Street-based FSWs 176 49 NR
Marcelin, 2002 [87] 1998–1999 Djibouti STI clinics Conv Street-based FSWs 43 70 NR
Marcelin, 2002 [87] 1998–1999 Djibouti STI clinics Conv FSWs working in 123 7 NR
luxury bars
Egypt Sheba, 1988 [88] 1986–1987 Multiple cities NR Conv FSWs 87 0 NR
Watts, 1993 [89] 1986–1990 Urban areas Medical facilities Conv FSWs 349 0 NR
Kabbash, 2012 [90] 2009–2010 Greater Cairo Community Conv FSWs 431 0 NR
Iran Jahani, 2005 [91] 2002 NR Detainment center/prison Conv FSWs detained by 149 0 NR
the police
Kassaian, 2012 [92] 2009–2010 Isfahan Prison, drop-in centers, and Conv FSWs 91 0 NR
community
Taghizadeh, 2015 2014 Sari, Mazandaran Drop-in center Conv FSWs at a drop-in center 184 4 NR
[93]
Asadi-Ali, 2018 [94] 2015 Northern Iran Counseling center, drop-in Conv FSWs 133 1.5 NR
center, and community
Lebanon Naman, 1989 [95] 1985–1987 NR NR Conv FSWs 291 0.3 NR
Morocco MOH, 2008 [96] 2007 Agadir, Rabat/Sale, NGO clinic Conv FSWs presenting for 141 1.4 0.1–2.5
Tanger consultation
Pakistan Iqbal, 1996 [97] 1987–1994 Lahore Hospital Conv FSWs 21 0 NR
Baqi, 1998 [98] 1993–1994 Karachi VCT Conv FSWs in red-light district 77 0 NR
Page 13 of 30
Table 3 HIV prevalence in FSWs in the Middle East and North Africa (MENA), as reported in studies using non-probability sampling (Continued)
Country Author, year Year(s) of City/province Study site Sampling Population Sample HIV prevalence*
[citation] data collection size
% 95% CI
Anwar, 1998 [99] NR Lahore NR NR FSWs 103 1.9 NR
Bokhari, 2007 [68] 2004 Karachi Community Snowball FSWs in red-light district 421 0 NR
Shah, 2004 [100] 2004 Hyderabad Community Conv FSWs 157 0 NR
Shah, 2004 [101] 2004 Sindh Sentinel surveillance Conv FSWs 163 1.2 NR
Akhtar, 2008 [102] 2007 Faisalabad Community NR FSWs 246 0 NR
Chemaitelly et al. BMC Medicine

Raza, 2015 [103] 2014 Rawalpindi Clinics Conv FSWs NR 0 NR


Somalia Jama, 1987 [104] 1985–1986 Mogadishu Camp Conv FSWs attending health 85 0 NR
education program
Burans, 1990 [105] NR Mogadishu NR Conv FSWs 89 0 NR
(2019) 17:119

Scott, 1991 [106] 1989 Merka, Kismayu NR Conv FSWs 57 0 NR


Corwin, 1991 [107] 1990 Chismayu, Merca, NR Conv FSWs 302 3 NR
Mogadishu
Jama Ahmed, 1991 [51] 1991 Mogadishu PHC Conv FSWs 155 0.6 NR
Sudan Burans, 1990 [108] 1987 Port Sudan NR Conv FSWs 203 0 NR
McCarthy, 1995 [109] NR Juba, South Sudan NR Conv FSWs 50 16 NR
Tunisia Bchir, 1988 [110] 1987 Sousse NR Conv FSWs 42 0 NR
Hassen, 2003 [111] NR Sousse PHC Conv Legal FSWs 51 0 NR
Znazen, 2010 [112] 2007 Tunis, Sousse, and Gabes Medical facilities Conv Legal FSWs undergoing 183 0 NR
routine testing
The table is sorted by year(s) of data collection or year of publication if the year of data collection was not reported
Abbreviations: CI confidence interval, Conv convenience, FSWs female sex workers, MOH Ministry of Health, NGO non-governmental organization, NR not reported, PHC primary healthcare centers, STI sexually
transmitted infection, VCT voluntary counseling and testing
*The decimal places of the prevalence figures are as reported in the original reports, but prevalence figures with more than one decimal places were rounded to one decimal place, with the exception of those below
0.1%. Most studies did not report the 95% CIs associated with prevalence
Page 14 of 30
Table 4 HIV prevalence in clients of FSWs (or proxy populations of clients of FSWs such as male STI clinic attendees) in the Middle East and North Africa (MENA)
Country Author, year [citation] Year(s) of data collection City/province Study site Sampling Population Sample size HIV prev* Sexual contacts
% 95%
CI
Algeria MOH, 2009 [113] 2004 Oran Sent. surv. Conv STI clinic attendees 41 4.9 NR NR
MOH, 2009 [113] 2004 Tamanrasset Sent. surv. Conv STI clinic attendees 105 0 0 NR
MOH, 2009 [113] 2004 Tizi-Ouzou Sent. surv. Conv STI clinic attendees 11 9.1 NR NR
MOH, 2009 [113] 2007 National Sent. surv. Conv STI clinic attendees 571 3.3 NR NR
Chemaitelly et al. BMC Medicine

Djibouti Rodier, 1993 [84] 1987 Djibouti STI clinic Conv STI clinic attendees 252 0.8 NR NR
Rodier, 1993 [84] 1988 Djibouti STI clinic Conv STI clinic attendees 249 0.8 NR NR
Fox, 1989 [114] NR NR NR Conv Clients of FSWs 105 1.0 NR Clients of FSWs
Rodier, 1993 [84] 1990 Djibouti STI clinic Conv STI clinic attendees 106 1.9 NR NR
(2019) 17:119

OMS, 2001 [115] 1990 NR STI clinic Conv STI clinic attendees NR 2.2 NR NR
Rodier, 1993 [84] 1991 Djibouti STI clinic Conv STI clinic attendees 193 10.4 NR NR
OMS, 2001 [115] 1991 NR STI clinic Conv STI clinic attendees NR 9.2 NR NR
MOH, 1993 [116] 1992 NR Sent. surv. Conv STI clinic attendees NR 11.6 NR NR
MOH, 1993 [116] 1993 NR Sent. surv. Conv STI clinic attendees 411 14.4 NR NR
MOH, 2002 [117] 2001–2002 Djibouti STI clinic Conv STI clinic attendees 237 34.6 NR NR
Bortolotti, 2007 [6, 118] 2006 Djibouti STI clinic Conv STI clinic attendees 72 5.6 1.5– NR
13.6
Egypt Sheba, 1988 [88] 1986–1987 Multiple cities STI clinic Conv STI clinic attendees 302 0 NR NR
Sadek, 1991 [119] 1987–1988 Cairo STI clinic Conv STI clinic attendees 140 0.7 NR NR
Sadek, 1991 [119] 1989–1990 Cairo STI clinic Conv STI clinic attendees 125 0.8 NR NR
Fox, 1994 [120] 1993 Alexandria STI clinic Conv STI clinic attendees 200 0 NR NR
Fox, 1994 [120] 1993 Cairo STI clinic Conv STI clinic attendees 300 0.3 NR NR
Saleh, 2000 [121] 1998–2000 Alexandria STI clinic Conv STI clinic attendees 295 0 NR NR
Kuwait NAP, 1999 [122] 1984–1998 Sabah, Kuwait STI clinic Conv STI clinic attendees 3097 0.02 NR NR
Murzi, 1989 [123] 1988 Kuwait STI clinic Conv STI clinic attendees 305 0 NR NR
Al-Owaish, 2000 [124] 1996–1997 Kuwait STI clinic SyRS STI clinic attendees 617 0 NR 23% reported contact with FSWs,
(Kuwaiti) 1% with MSWs, 35% with girlfriend,
12% with a mix of the above
Al-Owaish, 2000 [124] 1996–1997 Kuwait STI clinic SyRS STI clinic attendees 1367 0 NR 61% reported contact with FSWs,
(non-Kuwaiti) 0.5% with MSWs, 28.5% with
girlfriend, 3% with a mix of the
above
Page 15 of 30
Table 4 HIV prevalence in clients of FSWs (or proxy populations of clients of FSWs such as male STI clinic attendees) in the Middle East and North Africa (MENA) (Continued)
Country Author, year [citation] Year(s) of data collection City/province Study site Sampling Population Sample size HIV prev* Sexual contacts
% 95%
CI
Al-Owaish, 2002 [125] 2002 Kuwait STI clinic Conv STI clinic attendees 599 0 NR NR
(non-Kuwaiti)
Al-Mutairi, 2007 [126] 2003–2004 Kuwait STI clinic Conv STI clinic attendees 520 0 NR 79% reported contact with FSWs
(predom. men)
Morocco Heikel, 1999 [127] 1992–1996 Casablanca STI clinic Conv STI clinic attendees 1131 0.9 NR NR
Chemaitelly et al. BMC Medicine

Manhart, 1996 [128] 1996 Agadir, Tanger, and STI clinic Conv STI clinic attendees 223 1.4 NR NR
Marrakech
Alami, 2002 [129] 2001 Rabat, Sale, Beni Sent. surv. Conv STI clinic attendees 422 0 NR 70.7% reported new sexual
Mellal, and Marrakech partner, 47% multiple sexual
partners in the past 3 months
(2019) 17:119

MOH, 2001 [130] 2001 Marrakech, Beni Mellal, Sent. surv. Conv STI clinic attendees 422 0 NR NR
and Rabat, Sale
Khattabi, 2005 [131] 2004 National Sent. surv. Conv STI clinic attendees NR 0.4 NR NR
MOH, 2013 [132] 2006 National Sent. surv. Conv STI clinic attendees 1180 0.2 NR NR
MOH, 2013 [132] 2007 National Sent. surv. Conv STI clinic attendees 986 0.4 NR NR
MOH, 2013 [132] 2008 National Sent. surv. Conv STI clinic attendees 1237 0.5 NR NR
MOH, 2013 [132] 2009 National Sent. surv. Conv STI clinic attendees 1103 0.3 NR NR
MOH, 2013 [132] 2010 National Sent. surv. Conv STI clinic attendees 1181 0.7 NR NR
MOH, 2013 [133] 2011 Fes, Meknes, and VCT Conv STI clinic attendees 88 2.3 NR NR
Laayoune Boujdour
MOH, 2013 [132] 2012 National Sent. surv. Conv STI clinic attendees 1070 0.3 NR NR
MOH, 2013 [133] 2012 National VCT and STI Conv STI clinic attendees 1297 0.4 NR NR
clinic
Pakistan Mujeeb, 1993 [134] NR Karachi STI clinic Conv STI clinic attendees 32 0 NR NR
Memon, 1997 [135] 1994–1995 Hyderabad STI clinic Conv STI clinic attendees 50 0 NR NR
(predom. men)
NAP, 1996 [136] 1995 Karachi STI clinic Conv STI clinic attendees 402 0 NR NR
(predom. men)
NAP, 1996 [136] 1995 Lahore STI clinic Conv STI clinic attendees 295 0 NR NR
(predom. men)
Rehan, 2003 [137] 1999 Karachi STI clinic Conv STI clinic attendees 138 0 NR 43% reported contact with FSWs,
12% with casual heterosexual
contact, 11.6% with MSM, 18.4%
reported bisexuality
Rehan, 2003 [137] 1999 Lahore STI clinic Conv STI clinic attendees 148 0 NR NR
(-
Page 16 of 30
Table 4 HIV prevalence in clients of FSWs (or proxy populations of clients of FSWs such as male STI clinic attendees) in the Middle East and North Africa (MENA) (Continued)
Country Author, year [citation] Year(s) of data collection City/province Study site Sampling Population Sample size HIV prev* Sexual contacts
% 95%
CI
Rehan, 2003 [137] 1999 Peshawar STI clinic Conv STI clinic attendees 93 1.1 NR NR
Rehan, 2003 [137] 1999 Quetta STI clinic Conv STI clinic attendees 86 0 NR NR
Bhutto, 2011 [138] 2000–2009 Larkana STI clinic Conv STI clinic attendees 4288 0.06 NR 83% reported a history of contact
with FSWs
Chemaitelly et al. BMC Medicine

Bokhari, 2007 [68] 2004 Karachi Trucking SRS Truck driver clients 120 0 NR Subsample including only clients
agencies of FSWs of FSWs
Razvi, 2014 [139] 2010–2014 Abbottabad STI clinic Conv STI clinic attendees 465 1.1 NR 8% refused to answer, 70% of
the rest reported contact with
FSWs, 21% with MSM, 7.5%
with married women
(2019) 17:119

NAP, 2012 [140] 2011 Balochistan Mines SRS Mine workers clients 381 0 NR Subsample including only men
of FSWs reporting contact with FSWs
at last sex
Somalia Ismail, 1990 [141] 1986 Mogadishu STI clinic Conv STI clinic attendees 101 0 NR 54% reported contact with FSWs
Scott, 1991 [106] 1989 Mogadishu STI clinic Conv STI clinic attendees 50 0 NR NR
Burans, 1990 [105] NR Mogadishu NR Conv STI clinic attendees 45 0 NR 40% reported contact with FSWs
(80% soldiers)
Corwin, 1991 [107] 1990 Chismayu, Merca, NR Conv Partners of FSWs 26 0 NR Partners of FSWs
and Mogadishu
Duffy, 1999 [142] 1999 Hargeisa Sent. surv. Conv STI clinic attendees 106 0.9 NR NR
WHO, 2005 [143] 2004 Bossasso Sent. surv. Conv STI clinic attendees 78 1.3 NR NR
WHO, 2005 [143] 2004 Hargeisa Sent. surv. Conv STI clinic attendees 52 9.6 NR NR
WHO, 2005 [143] 2004 Mogadishu Sent. surv. Conv STI clinic attendees 46 4.4 NR NR
UNHCR, 2007 [144] 2006–2007 Dadaab refugee camp STI clinic Conv STI clinic attendees 199 0.5 NR NR
Ismail, 2007 [145] 2007 Hargeisa STI clinic Conv STI clinic attendees 108 7.4 NR NR
NAP, 2010 [146] 2007 Puntland Sent. surv. Conv STI clinic attendees NR 1.5 NR NR
Sudan McCarthy, 1989 [147] 1987 Port Sudan and Suakin NR Conv Clients of FSWs 157 0 NR Subsample including only clients
of FSWs
McCarthy, 1989 [148] 1987–1988 Gederef, Port Sudan, Outpatient Conv Soldiers clients of 398 2.5 NR Subsample including only soldiers
Kassala, Omdurman, and military clinics FSWs reporting a history of contact with
Juba FSWs
Page 17 of 30
Table 4 HIV prevalence in clients of FSWs (or proxy populations of clients of FSWs such as male STI clinic attendees) in the Middle East and North Africa (MENA) (Continued)
Country Author, year [citation] Year(s) of data collection City/province Study site Sampling Population Sample size HIV prev* Sexual contacts
% 95%
CI
McCarthy, 1995 [109] NR Juba, South Sudan STI clinics Conv STI clinic attendees 37 13.5 NR Subsample including only men
clients of FSWs reporting contact with FSWs in
the past 10 years
US Cens. Bureau, 2004 Khartoum Sent. surv. Conv STI clinic attendees 72 1.4 NR NR
2017 [149]
Chemaitelly et al. BMC Medicine

US Cens. Bureau, 2004 Red Sea Sent. surv. Conv STI clinic attendees 164 1.8 NR NR
2017 [149]
Yemen Abdol-Quauder, 1992 Sanaa STI clinic Conv STI clinic attendees 30 0 NR NR
1993 [150]
The table is sorted by year(s) of data collection or year of publication if the year of data collection was not reported
Abbreviations: Cens Census, CI confidence interval, Conv convenience, FSWs female sex workers, MENA HIV ESP MENA HIV/AIDS Epidemiology Synthesis Project, MOH Ministry of Health, NAP National AIDS Program, NR
(2019) 17:119

not reported, OMS Organisation Mondiale de la Sante, Predom. predominantly, Prev prevalence, Sent. surv. sentinel surveillance, SRS simple random sampling, STI sexually transmitted infection, SyRS systematic random
sampling, UNHCR United Nations Higher Commission for Refugees, VCT voluntary counseling and testing, WHO World Health Organization
*The decimal places of the prevalence figures are as reported in the original reports, but prevalence figures with more than one decimal places were rounded to one decimal place, with the exception of those below
0.1%. Most studies did not report the 95% CIs associated with prevalence
Page 18 of 30
Table 5 Results of meta-analyses on studies reporting HIV prevalence in FSWs and their clients (or proxy populations of clients such as male STI clinic attendees) in the Middle
East and North Africa (MENA) by epidemic type
Country Studies (N) Samples HIV prevalence Pooled mean Heterogeneity measures
HIV prevalence**
Tested HIV positive Median* (%) Range* (%) % 95% CI Q (p value)† I2‡ (%; 95% CI) Prediction
interval£ (95%)
FSWs Low-level Afghanistan 9 3578 7 0 0–0.90 0.03 0.00–0.18 7.59 (p = 0.4744) 0.0 (0.0–62.9) 0.00–0.22
Bahrain 1 724 6 0.83 – 0.83¥ 0.30–1.80 – – –
Chemaitelly et al. BMC Medicine

Egypt 33 7222 16 0 0–1.49 0.03 0.00–0.14 36.26 (p = 0.2765) 12.8 (0.0–43.4) 0.00–0.34
Iran 32 17,277 211 0.02 0–14.00 0.99 0.34–1.88 569.63 (p < 0.0001) 94.6 (93.2–95.6) 0.00–8.84
Iraq 29 15,852 1 0 0–0.07 0.00 0.00–0.00 6.24 (p = 1.0000) 0.0 (0.0–0.0) 0.00–0.00
Jordan 7 1024 4 0 0–1.33 0.00 0.00–0.31 3.43 (p = 0.7537) 0.0 (0.0–48.9) 0.00–0.48
Lebanon 11 11,589 12 0.07 0–2.40 0.00 0.00–0.07 18.82 (p = 0.0426) 46.9 (0.0–73.6) 0.00–0.33
(2019) 17:119

Pakistan 81 26,678 217 0 0–8.80 0.35 0.18–0.57 368.57 (p < 0.0001) 78.3 (73.3–82.3) 0.00–3.06
Syria 56 97,071 12 0 0–0.20 0.00 0.00–0.00 32.37 (p = 0.9936) 0.0 (0.0–0.0) 0.00–0.00
Tunisia 53 22,224 59 0 0–2.30 0.02 0.00–0.11 124.81 (p < 0.0001) 58.3 (43.6–69.2) 0.00–0.89
Yemen 10 1767 34 0.25 0–7.00 0.82 0.00–2.91 63.01 (p < 0.0001) 85.7 (75.6–91.7) 0.00–11.67
Intermediate-intensity Algeria 33 4241 179 2.00 0–20.00 2.39 1.02–4.15 215.22 (p < 0.0001) 85.1 (80.1–88.9) 0.00–15.05
Libya 4 1249 28 8.43 1.08–18.18 4.86 0.81–11.37 34.41 (p < 0.0001) 91.3 (80.8–96.0) 0.00–47.09
Morocco 200 40,507 804 1.07 0–52.90 1.11 0.83–1.41 851.66 (p < 0.0001) 76.6 (73.3–79.6) 0.00–5.98
Somalia 17 2015 57 0.35 0–47.06 1.64 0.42–3.39 61.50 (p < 0.0001) 74.0 (57.7–83.8) 0.00–10.24
Sudan€ 22 7207 128 0.95 0–7.70 1.30 0.76–1.96 98.06 (p < 0.0001) 78.6 (68.1–85.6) 0.00–5.26
Concentrated Djibouti 68 22,028 4618 18.75 0–70.00 17.89 13.62–22.60 5127.36 (p < 0.0001) 98.7 (98.6–98.8) 0.00–63.91
South Sudan 8 5466 1108 18.50 2.82–37.90 17.32 8.66–28.14 554.81 (p < 0.0001) 98.7 (98.3–99.1) 0.00–61.99
All countries 674 287,719 7501 0.26 0–70.00 1.44 1.14–1.76 24,605.29 (p < 0.0001) 97.3 (97.2–97.4) 0.00–16.49
Clients of FSWs Low-level Egypt 6 1362 3 0.17 0–0.80 0.09 0.00–0.42 4.82 (p = 0.4386) 0.0 (0.0–73.7) 0.00–0.60
Kuwait 6 6505 1 0 0–0.02 0.00 0.00–0.04 0.36 (p = 0.9963) 0.0 (0.0–0.0) 0.00–0.07
Pakistan 12 6498 9 0 0–1.10 0.00 0.00–0.10 14.93 (p = 0.1857) 26.3 (0.0–62.6) 0.00–0.42
¥
Yemen 1 30 0 0 – 0.00 0.00–11.57 – – –
Page 19 of 30
Table 5 Results of meta-analyses on studies reporting HIV prevalence in FSWs and their clients (or proxy populations of clients such as male STI clinic attendees) in the Middle
East and North Africa (MENA) by epidemic type (Continued)
Country Studies (N) Samples HIV prevalence Pooled mean Heterogeneity measures
HIV prevalence**
Tested HIV positive Median* (%) Range* (%) % 95% CI Q (p value)† I2‡ (%; 95% CI) Prediction
interval£ (95%)
Intermediate-intensity Algeria 7 728 22 7.29 0–25.80 3.51 0.32–8.90 39.79 (p < 0.0001) 84.9 (70.8–92.2) 0.00–27.63
Morocco 84 10,348 47 0 0–8.00 0.00 0.00–0.05 76.30 (p = 0.6854) 0.0 (0.0–19.9) 0.00–0.05
Somalia 11 1010 21 0.94 0–9.62 1.38 0.25–3.11 25.74 (p = 0.0041) 61.1 (25.0–79.9) 0.00–8.46
Chemaitelly et al. BMC Medicine

Sudan€ 4 791 14 1.61 0–2.51 1.22 0.16–2.97 7.02 (p = 0.0711) 57.3 (0.0–85.8) 0.00–11.65
Concentrated Djibouti 15 2222 217 2.20 0–34.60 5.36 1.53–10.81 244.98 (p < 0.0001) 94.3 (92.0–95.9) 0.00–35.23
South Sudan 1 37 5 13.5 – 13.5¥ 4.54–28.77 – – –
All countries 147 29,531 339 0 0–34.60 0.38 0.14–0.71 977.96 (p < 0.0001) 85.1 (82.9–87.0) 0.00–6.60
(2019) 17:119

Abbreviations: CI confidence interval, FSWs female sex workers


*These medians and ranges are calculated on the stratified HIV prevalence measures
**Missing sample sizes for measures (or their strata) were imputed using median sample size calculated from studies with available information. Analyses excluding these studies had no impact on study findings

Q—the Cochran’s Q statistic is a measure assessing the existence of heterogeneity in effect size (here, HIV prevalence) across studies
‡2
I —a measure assessing the magnitude of between-study variation that is due to the differences in effect size (here, HIV prevalence) across studies rather than chance
£
Prediction interval—a measure estimating the 95% interval of the distribution of true effect sizes (here, HIV prevalence)
Based on results of meta-analyses for FSWs, countries were classified as having low-level HIV epidemic (prevalence < 1%), intermediate-intensity HIV epidemic (prevalence 1–5%), and concentrated HIV epidemic
(prevalence > 5%)
¥
Point estimate as only one study was available

Before 2011, South Sudan was part of Sudan, and thus, earlier measures from Sudan were based on studies that may have included participants from both Sudan and South Sudan
Page 20 of 30
Table 6 Results of meta-regression analyses to identify associations with HIV prevalence, sources of between-study heterogeneity, and trend in HIV prevalence in FSWs in the
Middle East and North Africa (MENA)
Variables Studies Samples Univariable analyses Multivariable analysis
Total N Total N OR (95% CI) LR test p value€ Variance explained R2£ (%) AOR (95% CI) p value LR test
p value¥
Country/subregion*
Eastern MENA Afghanistan, Iran, Pakistan 122 47,533 1.00 < 0.001 39.80 1.00 < 0.001
Fertile Crescent Egypt, Iraq, Jordan, Lebanon, Syria 136 132,758 0.17 (0.10–0.27) 0.21 (0.12–0.36) < 0.001
Chemaitelly et al. BMC Medicine

Bahrain and Yemen Bahrain and Yemen 11 2491 2.60 (0.78–8.67) 1.77 (0.52–6.01) 0.357
Horn of Africa Djibouti, Somalia, South Sudan 93 29,509 33.45 (19.77–56.58) 45.43 (24.66–83.68) < 0.001
North Africa Algeria, Libya, Morocco, Sudan, Tunisia 312 75,428 3.14 (2.09–4.72) 2.90 (1.80–4.68) < 0.001
Population type Street-based, venue-based, and 619 220,363 1.00 0.002 1.29 1.00 0.163
other FSWs†
Bar girls 55 67,356 0.33 (0.17–0.67) 0.66 (0.37–1.18) 0.163
(2019) 17:119

Total sample size of tested < 100 participants 75 4008 1.00 0.001 1.54 1.00 < 0.001
FSWs
≥ 100 participants 599 283,711 0.36 (0.20–0.65) 0.35 (0.21–0.56) < 0.001
Median year of data collection** < 1993 104 36,038 1.00 0.001 1.96 1.00 0.005
1993–2002 169 98,221 0.31 (0.17–0.56) 1.18 (0.71–1.95) 0.522
≥ 2003 401 153,460 0.57 (0.33–0.97) 2.03 (1.24–3.33) 0.005
Sampling methodology Non-probability sampling 570 254,072 1.00 0.217 0.08 – – –
Probability-based sampling 104 33,647 0.72 (0.42–1.21) – – –
Response rate ≥ 60% 96 31,161 1.00 0.043 0.64 1.00 0.544
< 60%/unclear 62 14,102 2.76 (1.24–6.13) 1.17 (0.60–2.27) 0.645

Not applicable 516 242,456 1.37 (0.80–2.37) 1.33 (0.79–2.23) 0.279
Validity of sex work definition Clear and valid definition 117 36,431 1.00 0.161 0.25 – – –
Poorly defined/unclear 41 8832 2.35 (0.96–5.73) – – –
Not applicable‡ 516 242,456 1.15 (0.70–1.90) – – –
HIV ascertainment Biological assays 157 44,894 1.00 0.786 0 – – –
Self-report, unclear, and not 517 242,825 0.94 (0.60–1.47) – – –
applicable‡
Abbreviations: AOR adjusted odds ratio, CI confidence interval, FSWs female sex workers, LR likelihood ratio, OR odds ratio
*Countries were grouped based on geography and similarity in HIV prevalence levels. Given the large fraction of studies with zero HIV prevalence, particularly in the Fertile Crescent, an increment of 0.1 was
added to a number of events in all studies when generating log odds, and Eastern MENA was thus used also as a statistically better reference. While this choice of increment was arbitrary, other increments
yielded the same findings, though some of the effect sizes changed in scale
**Year grouping was driven by independent evidence identifying the emergence of HIV epidemics among both men who have sex with men [10] and people who inject drugs [11] in multiple MENA
countries around 2003. Missing values for year of data collection (only six stratified measures) were imputed using data for year of publication adjusted by the median difference between year of
publication and median year of data collection (for studies with complete information)

A large fraction of studies did not separate the different forms of female sex workers, and thus it was not possible to analyze these as separate categories

Measures extracted only from routine databases with no reports describing the study methodology were not included in the ROB assessment

Predictors with p value ≤ 0.1 were considered as showing strong evidence for an association with (prevalence) odds and were hence included in the multivariable analysis
£
Adjusted R2 in the final multivariable model = 49.21%
¥
Page 21 of 30

Predictors with p value ≤ 0.1 in the multivariable model were considered as showing strong evidence for an association with (prevalence) odds
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 22 of 30

not shown). Including the year of data collection as a frames. Others reported different distributions for the
linear term, instead of a categorical variable, using only number of clients (and by client type), also over various
post-2003 data indicated strong evidence for increasing time frames. Summarizing the evidence was therefore
HIV odds (AOR = 1.15, 95% CI = 1.09–1.21, p < 0.0001; challenging, given the large type of measure variability.
not shown). No association was found with the popula- This being said, the mean number of clients in the past
tion type or response rate. month ranged from 4.4 to 114.0, with a median of 34.0 cli-
Meta-regression analyses for clients demonstrated ents. Median fraction of FSWs reporting (during the past
similar results to those of FSWs, but with wider CIs con- month) < 5 clients, 5–9 clients, and 10+ clients was
sidering the smaller number of prevalence studies (Add- 28.5%, 28.1%, and 19.1%, respectively. FSWs were equally
itional file 1: Table S10). There was evidence that likely to report regular and one-time clients during the
subregion was associated with HIV odds in clients, but past month (medians = 80.0% and 81.0%, ranges = 54.3–
no evidence that sample size or year of data collection 92.4% and 59.2–97.5%, respectively).
explained the between-study heterogeneity. FSWs reported a distribution of sex acts in the past
week, with a median of 41.2% reporting 1–2 acts, 32.0%
Sex work context and sexual and injecting risk behaviors reporting 3–4 acts, and 12.9% reporting 5+ acts. Anal
For the detailed sex work context and behavioral mea- sex with clients in the past month was reported by a me-
sures, we provide here (for brevity) only a high-level dian of 8.0% (range = 2.3–100%).
summary of key measures. Median fraction of FSWs that are married/cohabiting
was 45.3% (range = 0–99.6%), while that of FSWs report-
Sex work context ing non-paying partners was 48.5% (range = 6.8–86.2%).
Across studies, the mean age of FSWs ranged from 19.5 to The mean number of non-paying partners in the past
37.4, with a median of 27.8 years. Mean age at sexual debut month ranged between 1 and 3, with about two thirds
ranged from 14.0 to 22.5 years (median = 17.5), and mean reporting only one partner.
age at sex work initiation ranged from 17.5 to 27.5 years Only few studies investigated group sex: 7.7% [90] of
(median = 22.7). Mean duration of sex work ranged from FSWs reported ever engaging in group sex, 6.2% [68] and
0.7 to 14.3 years (median = 5.5). A median of 28.0% (range 12.9% [68] reported group sex in the past month, and
= 0.9–76.6%) of FSWs were single, 30.1% (range = 0– 10.0% [58] in the past week.
65.5%) were divorced, and 7.0% (range = 0–27.2%) were
widowed.
Injecting risk behavior, sex with PWID, and substance use
Reported condom use There was a large variability in injecting risk behavior
There was high heterogeneity in reported condom use and substance use among FSWs, but the highest levels
among FSWs by sexual partnership type and across and of injecting drug use were reported in Iran and Pakistan
within countries (Additional file 1: Table S11). Condom (Additional file 1: Table S12). Median of current/recent
use at last sex with clients ranged from 1.2 to 94.8% injecting drug use was 2.1% (range = 0–26.6%), but the
(median = 44.0%). Consistent condom use with clients majority of studies were from Pakistan. Studies in Iran
ranged from 0 to 95.2% (median = 26.3%) among all reported a history of injecting drug use in the range of
FSWs and from 38.2 to 45.3% (median = 42.3%) among 6.1–18.0% (median of 13.6%) among all FSWs and range
FSWs reporting condom use with clients. of 16.4–25.5% (median of 22.3%) among only ever/active
Median condom use at last sex with regular clients was drug users. A history of injecting drug use was reported
55.9% (range = 25.5–92.0%) and that with one-time clients by < 1% (median) of all FSWs (range = 0%–11.8%) in the
was 58.3% (range = 28.5–96.0%). Less condom use at last rest of MENA countries.
sex was found with non-paying partners (median = 22.0%, Fraction of FSWs reporting current/recent sex with
range = 4.9–78.3%). There was also variability in condom PWID ranged from 0.5 to 13.6% within Afghanistan and
use at last anal sex (range = 0–86.5%), though low levels 0–54.9% within Pakistan, with medians of 5.2% and
were generally reported (median = 18.5%). 5.6%, respectively. Sex with PWID was reported at 23.6%
The median fraction of FSWs who reported having a [93] among FSWs in Iran.
condom at the time of study interview was 12.5% (range = Close to a third of FSWs reported ever using drugs
0–66.1%). (median = 27.0%, range = 1.7–90.7%). A median of
8.9% reported current/recent drug use (range = 0.6–
Clients and partners 59.0%). Any substance use before/during sex was re-
Studies varied immensely in types of measures reporting ported by 37.8% (median, range = 1.0–88.1%). Alcohol
data on clients and partners. Some reported a mean num- use before/during sex was reported by 44.1% (median,
ber of regular/non-regular clients, but over various time range = 3.0–70.7%).
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 23 of 30

Knowledge of HIV/AIDS and perception of risk documented in half of the cities in the latest round in
Knowledge of HIV/AIDS was generally high among FSWs 2016–2017 [42]. These emerging epidemics among FSWs
across MENA (Additional file 1: Table S13). Vast majority were preceded by large and growing epidemics first
of FSWs ever heard of HIV (median = 81.9%, range = among PWID [11] and then among MSM [10, 11].
25.4–100%) and were aware of sexual (median = 72.0%, Some of the FSW epidemics, particularly those in
range = 50.8–94.9%) and injecting (median = 88.7%, range Djibouti and South Sudan, emerged much earlier, most
= 11.5–99.6%) modes of transmission, but to a lesser extent likely by late 1980s [6], mainly affected by geographic
of condoms as a prevention method (median = 51.6%, proximity and stronger population links to sub-Saharan
range = 14.1–89.8%)—condoms were more perceived as a Africa (SSA) [6]. Djibouti is a port country and the
contraception method. Levels of knowledge, however, major trade route for Ethiopia and a station for large
varied often substantially within the same country. international military bases [6, 151]. The majority of
Overall, FSWs did not perceive themselves at high risk FSWs operating in Djibouti are Ethiopians catering to
of HIV acquisition (Additional file 1: Table S14). Percep- the Ethiopian truck drivers transporting shipments from
tion of HIV risk was reported as at-risk (median = 34.6%, the Djibouti port [84–86]. South Sudan is socio-
range = 22.8–48.5), low-risk (median = 18.3%, range = culturally part of SSA, with a major fraction of FSWs
7.1–46.9), medium-risk (median = 16.4%, range = 5.3– coming from Uganda, Congo, and Kenya [79]. In these
36.1), and high-risk (median = 14.4%, range = 5.9–32.0). MENA countries, HIV in commercial heterosexual sex
networks (CHSNs) is well-established and epidemics are
HIV testing concentrated—though at levels lower than the hyper-
HIV testing among FSWs varied across countries, but endemic epidemics observed in SSA [152].
was generally low, with a median fraction of 17.6% Unlike the epidemics among PWID and MSM [10, 11],
(range = 4.0–99.4%) ever tested for HIV (Additional file 1: the FSW epidemics have been overall growing rather
Table S15). Only a median of 12.1% (range = 0.9–38.0%) slowly, with the prevalence being mostly < 5%. Strikingly,
of all FSWs tested for HIV in the past 12 months, and a considerable fraction of countries still do not appear to
nearly two thirds of those who ever tested did so in the have much HIV transmission in CHSNs, with consistently
past 12 months (median = 59.2%, range = 33.3–82.0%). very low prevalence, quite often even at zero level—46.8%
Majority of FSWs who ever tested were aware of their of studies in FSWs reported zero prevalence, and 7 out of
status (median = 91.9%, range = 60.0–99.0%). 18 countries had a pooled mean prevalence of zero or
nearly zero. One explanation for the observed low HIV
Discussion prevalence could be that HIV has not yet been effectively
Through an extensive, systematic, and comprehensive as- introduced into CHSNs—it took decades for HIV to be ef-
sessment of HIV epidemiology among FSWs and clients, fectively introduced into PWID [11] and MSM [10]
including data presented in the scientific literature for the networks. Another possible factor pertains to the structure
first time, we found that HIV epidemics among FSWs of CHSNs, characterized apparently by low connectivity
have already emerged in MENA, and some appear to have [6, 153, 154], which reduces the risk of HIV being intro-
reached their peak. Based on a synthesis and triangulation duced, or efficiently/sustainably transmitted. Unlike PWID
of evidence from studies on a total of 300,000 FSWs and and MSM, FSWs are also exposed to HIV mainly through
30,000 clients, a strong regionalization of epidemics has their clients, who have a lower risk of exposure to HIV
been identified. In Djibouti and South Sudan, the HIV than themselves, thus possibly contributing to slower
epidemic is concentrated with a prevalence of ~ 20% in epidemic growth [6].
FSWs. In Algeria, Libya, Morocco, Somalia, and Sudan, Other factors may also contribute to explaining the
the epidemic is of intermediate-intensity (prevalence 1– observed low HIV prevalence. The synthesized evidence
5%). Strikingly, in the remaining countries with available suggests a lower risk environment for FSWs in MENA,
data, the prevalence is < 1%, and most often zero. compared to other regions. The reported number of
A key finding is that HIV prevalence in FSWs has been clients is rather low at a median of 34 per month, at the
(overall) growing steadily since 2003. This is the same lower end of global range [155–158]. Close to half of
time in which independent evidence has identified the commercial sex acts are protected through condom use,
emergence of major epidemics among both PWID [11] with no difference between regular and one-time clients,
and MSM [10] in MENA. It is probable that the epidemics despite noted variability across and within countries.
among these key populations have been bridged to FSWs. HIV/AIDS knowledge also varies, but is generally sub-
An example is Pakistan, where the prevalence among stantial, with the majority of FSWs being aware of sexual
FSWs was < 1% in almost all cities in three consecutive and injecting modes of transmission, and over half are
IBBSS rounds between 2005 and 2012 [38, 40, 69]. How- aware of condoms as a prevention method. Injecting
ever, prevalence ranging from 1.5 to 8.8% was drug use and sex with PWID is low in most countries,
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 24 of 30

except for countries in Eastern MENA, notably rapid rise in prevalence among clients (as proxied by
Afghanistan, Iran, and Pakistan. Serological markers for male STI clinic attendees; Table 4), leading eventually to
hepatitis C virus (a marker of injecting risk) [159–161] are a prevalence > 1% in pregnant women [6].
also low in FSWs, assessed at a median of 1.1% (range = 0– HIV response to the epidemic in CHSNs in MENA con-
9.9%, not shown), with the highest measures reported in tinues to be weak and limited in scope and scale [185].
Iran [61, 162]. These relatively lower levels of risk behavior Criminality [151, 185] and stigma [186–188] associated
than other regions [163–165] stand in contrast to what has with sex work persist as barriers to surveillance and tar-
been observed in PWID and MSM in MENA [10, 11]. geted programming [189–191], leading even to the resist-
Importantly, with the efficacy of 60% in randomized ance to acknowledge the existence of sex work [192].
clinical trials [166–169], male circumcision, which is es- These challenges are compounded by the diverse typolo-
sentially at universal coverage across MENA [170], may gies and increased mobility of FSWs [41, 70, 151]. Across
have also slowed, or even substantially reduced HIV MENA, only 18% of FSWs reported ever testing for HIV,
transmission in CHSNs leading to the observed low HIV and fewer (12%) reported testing in the past 12 months,
prevalence [171]. Incidentally, the two most affected far below the 90% service coverage target of “UNAIDS
countries—South Sudan and Djibouti—are nearly the 2016–2021 Strategy” [193]. Programs, including health-
only two major settings where male circumcision is at care provision, where they exist, are nearly always imple-
low coverage in MENA, either nationally, as is the case mented by non-governmental organizations (NGOs), who
for South Sudan [170], or among clients of FSWs, as is often lack the resources or legal coverage to deliver com-
the case for Ethiopian truckers and international military prehensive prevention interventions [6, 185].
personnel stationed in Djibouti [151, 170]. Though HIV There are, however, notable exceptions. Morocco has
prevalence will probably continue to increase among established an evidence-informed national strategy and
FSWs and clients, the high levels of male circumcision rapidly scaled up provision of comprehensive services for
coupled with lower levels of risk behavior may prevent at-risk populations, including outreach peer education
significant epidemics, as seen elsewhere [172–174], from programs as well as testing and case management services
materializing in CHSNs in multiple MENA countries. [183, 185]. Voluntary counseling and testing centers were
HIV prevalence in FSWs in few countries, particularly in established nationwide, with FSWs estimated to constitute
Eastern MENA, may not necessarily reflect heterosexual as about a quarter of attendees in 2007 [183, 194]. Findings
much as iatrogenic exposures through injecting drug use. of the 2011–2012 IBBSS indicated that over a third of
Specifically, in Iran and Pakistan, countries with large HIV FSWs ever tested for HIV, the vast majority of whom were
epidemics among PWID [11], a considerable fraction of aware of their status [67]. Condom use at last sex also in-
FSWs report current/recent/history (14% in Iran and 2% in creased from 37% in 2003 to a median of 50% in 2011
Pakistan) of injecting drug use. High prevalence of sex work (Additional file 1: Table S11). Morocco’s success has been
is also reported in women engaging in injecting drug use grounded on a strong multisectorial response where
[93, 175, 176]. Current/recent/history of sex with PWID is NGOs, in partnership with the government, play a leading
also common (24% in Iran and 6% in Pakistan). The overlap role in implementing interventions [185]. In Iran, the large
between these key populations suggests a potential for HIV expansion of harm reduction services, including the first
to be bridged from PWID networks to CHSNs, as seem to women-operated services in MENA [11], is a promising
have occurred in Pakistan recently [42, 177, 178]. step for targeting FSWs most at risk.
Population proportion of current/recent FSWs ranged This study is limited by gaps in evidence. Epidemic status
from 0.2 to 2.4% across studies with a median of 0.6%, among FSWs remains unknown in six countries, as no data
while that of current/recent clients ranged from 0.3 to were identified. Others (Bahrain and Libya) also had lim-
13.8% with a median of 5.7%, both on the lower end of ited data to warrant a meaningful characterization of the
global range [179, 180]. Though these population pro- epidemic. The high heterogeneity of epidemics within
portions may seem small, the size of CHSNs is much lar- countries suggests that caution is needed when interpreting
ger than that of PWID and MSM [10, 11, 181]. This data without a representative national coverage. For in-
suggests that CHSNs could be a main driver of HIV inci- stance, while concentrated epidemics among FSWs are
dence in many countries despite the low HIV prevalence documented in southern Morocco [67, 195] and southern
in FSWs. An example is Morocco where the mode of Algeria [113, 196–198], these do not appear to be represen-
transmission analyses estimated that over half of HIV in- tative of FSWs at the national level [42, 67, 74, 78, 81, 82,
cidence is driven by CHSNs, despite an HIV prevalence 113, 195–199]. Hidden epidemics or outbreaks may also
of only ~ 2% in FSWs [182–184]. The role of CHSNs is exist in specific geographies within the country, but not ne-
even more significant in countries with concentrated ep- cessarily elsewhere. Data varied over time with high quality
idemics. In Djibouti, for example, the large HIV epi- and volume of evidence available mostly post-2000, thanks
demic among FSWs was mirrored shortly after by a to the expansion and funding of IBBSS studies. While the
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 25 of 30

pooled prevalence estimates were meant to provide a through NGOs leading the provision of comprehen-
summary of the relative standing of MENA countries in sive interventions, with governmental support, even if
the HIV epidemic, the large between-study heterogeneity discrete. Extending harm reduction services to women
suggests that caution is warranted when interpreting these PWID is also critical to curb HIV burden in FSWs
estimates. Studies in clients of FSWs/proxy populations re- most at risk, specifically in Eastern MENA. The win-
main limited with wide variability in evidence availability dow of opportunity for detecting epidemics at their
across MENA. nascence, and for controlling incidence in CHSNs,
A considerable fraction of studies used convenience should not be missed.
sampling, although meta-regression indicated no differ-
ence in the prevalence by sampling methodology. This Additional file
may be explained by FSWs being more “visible” [151,
200] compared to PWID [11] and MSM [10]. A sizable Additional file 1: Supplementary information including further details
fraction of studies was from routine data reporting with and additional results for the systematic review and meta-analytics of HIV
infection in female sex and their clients workers in the Middle East and
no sufficient documentation of study methodology. North Africa. Tables S1-S15. Figure S1. Box S1-S2. (DOCX 1819 kb)
However, most of these country-level program data were
presumably based on rigorous case definitions following
Abbreviations
WHO guidelines [6]. There is also a possibility that a AOR: Adjusted odds ratio; CHSNs: Commercial heterosexual sex networks;
fraction of studies may have enrolled women without a CI: Confidence interval; FSWs: Female sex workers; IBBSS: Integrated bio-
strict and valid definition for sex work, yet meta- behavioral surveillance surveys; MENA: Middle East and North Africa;
MSM: Men who have sex with men; NGOs: Non-governmental organizations;
regression findings showed no effect for the validity of PRISMA: Preferred Reporting Items for Systematic Reviews and Meta-analyses;
sex work definition on HIV prevalence. There was also PWID: People who inject drugs; ROB: Risk of bias; SI: Supplementary
no evidence that other study-specific quality domains, Information; SSA: Sub-Saharan Africa; STI: Sexually transmitted infection;
UNAIDS: Joint United Nations Programme on HIV/AIDS; WHO: World Health
including HIV ascertainment method and response rate, Organization
had an effect on prevalence. A considerable fraction of
studies reported zero prevalence, thus an increment of Acknowledgements
0.1 was added to a number of events to be able to con- The authors would like to thank Dr. Sara L. Thomas for her guidance in devising
the search strategy. The authors would also like to thank Ms. Adona Canlas for
duct the meta-regressions. While this choice of incre- her assistance in locating full texts of articles and Ms. Sarwat Mahmud for her
ment was arbitrary, other increments yielded the same help in generating the Middle East and North Africa regional map. The
findings, though some of the effect sizes changed in publication of this article was funded by the Qatar National Library.

scale. There was evidence for a small-study effect in


Authors’ contributions
meta-regression suggesting potential publication bias to- HC designed the study, conducted the systematic review of the literature,
wards studies reporting higher prevalence. performed the data analyses, and wrote the first draft of the article. MH
double extracted the data. CC contributed to the study design. HAW
contributed to the study design, data analyses, and drafting of the article.
Conclusions LJA conceived the study and contributed to the study design, data analyses,
HIV epidemics among FSWs are emerging in MENA, with and drafting of the article. All authors contributed to the discussion and
interpretation of the results and to the writing of the manuscript. All authors
some already established. The epidemic has been growing
have read and approved the final manuscript.
steadily in recent years, with strong regionalization and
heterogeneity. A contributing factor to epidemic growth Funding
appears to be the epidemics that emerged among PWID This publication was made possible by NPRP grant number 9-040-3-008 from
the Qatar National Research Fund (a member of Qatar Foundation). Infra-
[11] and MSM [10] nearly two decades ago. Strikingly, a structure support was provided by the Biostatistics, Epidemiology, and Bio-
large fraction of countries still do not appear to have any mathematics Research Core at the Weill Cornell Medicine-Qatar. Salary for
significant epidemic dynamics in CHSNs. These findings HAW was from the UK Medical Research Council (MRC) and the UK Depart-
ment for International Development (DFID) under the MRC/DFID Concordat
demonstrate the need for expanding surveillance systems, agreement (K012126/1). The statements made herein are solely the responsi-
including the conduct of repeated IBBSS studies with na- bility of the authors.
tional coverage to monitor HIV prevalence trends and to
detect the emergence of epidemics. There is also a pressing Availability of data and materials
All data are within the paper and its supplementary information.
need for mapping and size estimation studies to delin-
eate the diverse typologies of sex work and to ensure Ethics approval and consent to participate
evidence-informed response with adequate coverage of Not applicable
interventions.
Achieving “UNAIDS 2016–2021 Strategy” [193] ser- Consent for publication
Not applicable
vice coverage targets entails reaching out to the increas-
ingly dispersed FSW population [41, 70, 151]. Building Competing interests
on Morocco’s success, this would be best achieved The authors declare that they have no competing interests.
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 26 of 30

Author details Available from: http://files.unaids.org/en/media/unaids/contentassets/


1
Infectious Disease Epidemiology Group, Weill Cornell Medicine-Qatar, documents/epidemiology/2011/20110518_Surveillance_among_most_at_
Cornell University, Qatar Foundation–Education City, P.O. Box 24144, Doha, risk.pdf. Accessed Feb 2014: WHO Press; 2011.
Qatar. 2MRC Tropical Epidemiology Group, London School of Hygiene and 20. Wilson D, Halperin DT. “Know your epidemic, know your response”: a useful
Tropical Medicine, London, UK. 3Department of Infectious Disease approach, if we get it right. Lancet. 2008;372(9637):423–6.
Epidemiology, Faculty of Epidemiology and Population Health, London 21. UNAIDS/WHO working group on global HIV/AIDS and STI surveillance.
School of Hygiene and Tropical Medicine, London, UK. 4Department of Guidelines for second generation HIV surveillance: an update: know your
Healthcare Policy & Research, Weill Cornell Medicine, Cornell University, New epidemic. Geneva. WHO Press; 2011. Available from: https://apps.who.int/
York, NY, USA. 5College of Health and Life Sciences, Hamad bin Khalifa iris/bitstream/handle/10665/85511/9789241505826_eng.pdf;jsessionid=
University, Doha, Qatar. FDD5FD06D64A5A5BE5A6213B15E3A058?sequence=1. Accessed Feb 2014.
22. Freeman MF, Tukey JW. Transformations related to the angular and the
Received: 17 February 2019 Accepted: 22 May 2019 square root; 1950. p. 607–11.
23. Miller JJ. The inverse of the Freeman–Tukey double arcsine transformation.
Am Stat. 1978;32(4):138.
24. Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of
References
prevalence. J Epidemiol Community Health. 2013;67(11):974–8.
1. The Joint United Nations Programme on HIV/AIDS (UNAIDS). Global AIDS
25. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials.
update 2018. UNAIDS. Geneva; 2018.
1986;7(3):177–88.
2. The Jointed United Nations Programme on HIV/AIDS (UNAIDS). Global AIDS
26. Borenstein M. Introduction to meta-analysis. Chichester: Wiley; 2009.
update 2016. UNAIDS. Geneva; 2016.
27. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis.
3. The Joint United Nations Programme on HIV/AIDS (UNAIDS): The gap
Stat Med. 2002;21(11):1539–58.
report. UNAIDS. Geneva: 2014.
4. Bohannon J. Science in Libya. From pariah to science powerhouse? Science. 28. R core team. R: a language and environment for statistical computing.
2005;308(5719):182–4. Vienna: R Foundation for Statistical Computing; 2017.
5. Mumtaz GR, Riedner G, Abu-Raddad LJ. The emerging face of the HIV 29. Say L, Donner A, Gulmezoglu AM, Taljaard M, Piaggio G. The prevalence of
epidemic in the Middle East and North Africa. Curr Opin HIV AIDS. 2014;9(2): stillbirths: a systematic review. Reprod Health. 2006;3:1.
183–91. 30. StataCorp. Stata statistical software: release 15.1. College Station: StataCorp
6. Abu-Raddad L, Akala FA, Semini I, Riedner G, Wilson D, Tawil O. LP; 2017.
Characterizing the HIV/AIDS epidemic in the Middle East and North Africa: 31. Bahaa T, Elkamhawi S, Abdel RI, Moustafa M, Shawky S, Kabore I, Soliman C.
time for strategic action. Washington DC: The World Bank Press; 2010. Gender influence on VCT seeking in Egypt. In: International AIDS society,
7. Abu-Raddad LJ, Hilmi N, Mumtaz G, Benkirane M, Akala FA, Riedner G, Tawil WEPE0255: 2010; 2010.
O, Wilson D. Epidemiology of HIV infection in the Middle East and North 32. Jacobsen J.O. STJ, Loo V. Estimating the size of key affected populations at
Africa. Aids. 2010;24(SUPPL. 2):S5–S23. elevated risk for HIV in Egypt. National AIDS Program, Ministry of Health and
8. Saba HF, Kouyoumjian SP, Mumtaz GR, Abu-Raddad LJ. Characterising the Population-Egypt. Cairo 2014.
progress in HIV/AIDS research in the Middle East and North Africa. Sex 33. World Health Organization: HIV surveillance systems: regional update 2011.
Transm Infect. 2013;89(Suppl 3):iii5–9. 2011.
9. Bozicevic I, Riedner G, Calleja JM. HIV surveillance in MENA: recent 34. Sharifi H, Karamouzian M, Baneshi MR, Shokoohi M, Haghdoost A,
developments and results. Sex Transm Infect. 2013;89(Suppl 3):iii11–6. McFarland W, Mirzazadeh A. Population size estimation of female sex
10. Mumtaz G, Hilmi N, McFarland W, Kaplan RL, Akala FA, Semini I, Riedner G, workers in Iran: synthesis of methods and results. PLoS One. 2017;12(8):
Tawil O, Wilson D, Abu-Raddad LJ. Are HIV epidemics among men who e0182755.
have sex with men emerging in the Middle East and North Africa?: a 35. Kahhaleh JG, El Nakib M, Jurjus AR. Knowledge, attitudes, beliefs and
systematic review and data synthesis. PLoS Med. 2011;8(8):e1000444. practices in Lebanon concerning HIV/AIDS, 1996–2004. East Mediterr Health
11. Mumtaz GR, Weiss HA, Thomas SL, Riome S, Setayesh H, Riedner G, Semini I, J. 2009;15(4):920–33.
Tawil O, Akala FA, Wilson D, et al. HIV among people who inject drugs in 36. Bennani A, El Rhilani H, El Kettani A, Latifi A, El Omari B, Alami K,
the Middle East and North Africa: systematic review and data synthesis. Johnston LG. Estimates of the size of key populations at risk for HIV
PLoS Med. 2014;11(6):e1001663. infection: female sex workers and men who have sex with men,
12. Higgins JPT, Green S, Cochrane collaboration. Cochrane handbook for injecting drug users in Morocco in 2013. In: International AIDS
systematic reviews of interventions. Chichester, Hoboken, Wiley-Blackwell; Conference, WEPE180: 2014; 2014.
2008. 37. Royaume du Maroc-Ministere de la Sante: Enquete connaissances, attitudes
13. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting et pratiques des jeunes en matiere d’IST et VIH/SIDA. 2013.
items for systematic reviews and meta-analyses: the PRISMA statement. 38. National AIDS Control Program: HIV second generation surveillance in
PLoS Med. 2009;6(7):e1000097. Pakistan: national report round I. Pakistan: Canada-Pakistan HIV/AIDS
14. International AIDS Society: Abstract archives of International AIDS Society Surveillance Project; 2005.
conferences. Found at: http://www.abstract-archive.org/. Accessed 28 July 39. Emmanuel F, Blanchard J, Zaheer HA, Reza T, Holte-McKenzie M. The HIV/
2018. AIDS Surveillance Project mapping approach: an innovative approach for
15. McMillan K, Worth H, Rawstorne P. Usage of the terms prostitution, sex mapping and size estimation for groups at a higher risk of HIV in Pakistan.
work, transactional sex, and survival sex: their utility in HIV prevention Aids. 2010;24(Suppl 2):S77–84.
research. Arch Sex Behav. 2018;47(5):1517–27. 40. National AIDS Control Program. HIV second generation surveillance in
16. The Joint United Nations Programme on HIV/AIDS (UNAIDS). Transactional Pakistan. National Report Round IV 2011. National AIDS Control Program-
sex and HIV risk: from analysis to action. Available from: http://www. Pakistan. Islamabad; 2012.
unaidsorg/sites/default/files/media_asset/transactional-sex-and-hiv-risk_en. 41. Emmanuel F, Thompson LH, Athar U, Salim M, Sonia A, Akhtar N, Blanchard
pdf. 2018. JF. The organisation, operational dynamics and structure of female sex work
17. Gouws E, Cuchi P, International Collaboration on Estimating HIV Incidence in Pakistan. Sex Transm Infect. 2013;89(SUPPL. 2):ii29–33.
by Modes of Trasnmission. Focusing the HIV response through estimating 42. National AIDS Control Program. Integrated biological & behavioral
the major modes of HIV transmission: a multi-country analysis. Sex Transm surveillance in Pakistan 2016–17: 2nd generation HIV surveillance in Pakistan
Infect. 2012;88(Suppl 2):i76–85. round 5. National AIDS Control Program-Pakistan. Islamabad; 2017. p. 159.
18. Case KK, Ghys PD, Gouws E, Eaton JW, Borquez A, Stover J, Cuchi P, Abu- 43. Projects and Research Department (AFROCENTER GROUP). Baseline study on
Raddad LJ, Garnett GP, Hallett TB, et al. Understanding the modes of knowledge, attitudes, and practices on sexual behaviors and HIV/AIDS
transmission model of new HIV infection and its use in prevention planning. prevention amongst young people in selected states in Sudan. Sudan
Bull World Health Organ. 2012;90(11):831–838A. National AIDS Control Program, The United Nations Children's Fund
19. UNAIDS/WHO working group on global HIV/AIDS and STI surveillance. (UNICEF), and The Joint United Nations Programme on HIV/AIDS (UNAIDS).
Guidelines on surveillance among populations most at risk for HIV. Geneva. Sudan; 2005.
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 27 of 30

44. Ministry of Health-Republic of Yemen. Population size estimates among Conference, Durban, South Africa, 7/18-22, ePoster, Abstract TUPEC175:
most at risk populations in five major cities in Yemen. Ministry of Public 2016; 2016.
Health-Yemen. Sanaa; 2010. 63. Karami M, Khazaei S, Poorolajal J, Soltanian A, Sajadipoor M. Estimating the
45. Todd CS, Barbera-Lainez Y, Doocy SC, Ahmadzai A, Delawar FM, Burnham population size of female sex worker population in Tehran, Iran: application
GM. Prevalence of human immunodeficiency virus infection, risk behavior, of direct capture-recapture method. AIDS Behav. 2017;21:2394–400.
and HIV knowledge among tuberculosis patients in Afghanistan. Sex 64. Ministry of Health-Hashemite Kingdom of Jordan: Report to the Secretary
Transm Dis. 2007;34(11):878–82. General of the United Nations on the United Nations General Assembly
46. Todd CS, Nasir A, Mansoor GF, Sahibzada SM, Jagodzinski LL, Salimi F, Special Session on HIV/AIDS.2014.
Khateri MN, Hale BR, Barthel RV, Scott PT. Cross-sectional assessment 65. Mahfoud Z, Afifi R, Ramia S, Khoury DE, Kassak K, Barbir FE, Ghanem M, El-
of prevalence and correlates of blood-borne and sexually-transmitted Nakib M, Dejong J. HIV/AIDS among female sex workers, injecting drug
infections among Afghan National Army recruits. BMC Infect Dis. users and men who have sex with men in Lebanon: results of the first
2012;12:196. biobehavioral surveys. Aids. 2010;24(SUPPL. 2):S45–54.
47. Adib SM, Akoum S, El-Assaad S, Jurjus A. Heterosexual awareness and 66. Valadez JJ, Berendes S, Jeffery C, Thomson J, Ben Othman H, Danon
practices among Lebanese male conscripts. East Mediterr Health J. 2002; L, Turki AA, Saffialden R, Mirzoyan L. Filling the knowledge gap:
8(6):765–75. measuring HIV prevalence and risk factors among men who have
48. Royaume du Maroc-Ministere de la Sante, Cooperation Technique sex with men and female sex workers in Tripoli, Libya. PLoS One.
Allemande/GTZ: Enquete connaissances, attitudes et pratiques des jeunes 2013;8(6):e66701.
concernant les IST et le SIDA; 2007. 67. Ministry of Health-Morocco, The Joint United Nations Programme on HIV/
49. Mir AM, Wajid A, Pearson S, Khan M, Masood I. Exploring urban male non- AIDS (UNAIDS), The Global Fund. HIV integrated behavioral and biological
marital sexual behaviours in Pakistan. Reprod Health. 2013;10(1):22. surveillance surveys-Morocco 2011: female sex workers in Agadir, Fes, Rabat
50. Sudan National AIDS Control Programme-Federal Ministry of Health. HIV/ and Tanger. Ministry of Health-Morocco. Rabat; 2012.
AIDS/STIs knowledge attitude behavioural and practice among university 68. Bokhari A, Nizamani NM, Jackson DJ, Rehan NE, Rahman M, Muzaffar R,
students and military personnel, Sudan 2004. Sudan National AIDS Control Mansoor S, Raza H, Qayum K, Girault P, et al. HIV risk in Karachi and Lahore,
Programme. Khartoum; 2004. Pakistan: an emerging epidemic in injecting and commercial sex networks.
51. Jama Ahmed H, Omar K, Adan SY, Guled AM, Grillner L, Bygdeman S. Int J STD AIDS. 2007;18(7):486–92.
Syphilis and human immunodeficiency virus seroconversion during a 6- 69. National AIDS Control Program-Ministry of Health. HIV second generation
month follow-up of female prostitutes in Mogadishu, Somalia. Int J STD surveillance in Pakistan: national report round II. National AIDS Control
AIDS. 1991;2(2):119–23. Program-Pakistan. Islamabad; 2007.
52. Constantine NT, Fox E, Rodier G, Abbatte EA. Monitoring for HIV-1, HIV-2, 70. Hawkes S, Collumbien M, Platt L, Lalji N, Rizvi N, Andreasen A, Chow J,
HTLV-I sero-progression and sero-conversion in a population at risk in East Muzaffar R, Ur-Rehman H, Siddiqui N, et al. HIV and other sexually
Africa. J Egyptian Public Health Assoc. 1992;67(5–6):535–47. transmitted infections among men, transgenders and women selling sex in
53. SAR AIDS Human Development Sector-The World Bank. Mapping and two cities in Pakistan: a cross-sectional prevalence survey. Sex Transm Infect.
situation assessment of key populations at high risk of HIV in three cities of 2009;85(SUPPL. 2):ii8–ii16.
Afghanistan, vol. 23; 2008. 71. Khan MS, Unemo M, Zaman S, Lundborg CS. HIV, STI prevalence and risk
54. National AIDS Control Program, Johns Hopkins University Bloomberg School behaviours among women selling sex in Lahore, Pakistan. BMC Infect Dis.
of Public Health HIV Surveillance Project. Integrated behavioral & biological 2011;11:119.
surveillance (IBBS) in Afghanistan: year 1 report. National AIDS Control 72. National AIDS Control Program-Pakistan Ministry of Health. Progress report
Program-Afghanistan. Kabul; 2010. on the Declaration of Commitment on HIV/AIDS for the United Nations
55. National AIDS Control Program, Johns Hopkins University Bloomberg School General Assembly Special Session on HIV/AIDS. National AIDS Control
of Public Health HIV Surveillance Project. Integrated biological & behavioral Program-Pakistan. Islamabad; 2010.
surveillance (IBBS) in selected cities of Afghanistan: findings of 2012 IBBS 73. Testa A, Kriitmaa K. HIV & syphilis bio-behavioural surveillance survey (BSS)
survey and comparison to 2009 IBBS survey. National AIDS Control among female transactional sex workers in Hargeisa, Somaliland.
program-Afghanistan. Kabul; 2012. International Organization for Migration (Somaliland) and World Health
56. Ministry of Health, National AIDS Program, Family Health International. HIV/ Organization (Somalia). Hargeisa; 2008.
AIDS biological & behavioral surveillance survey round I: summary report. 74. International Organization for Migration (IOM). Integrated biological and
Ministry of Health-Egypt and Family Health International. Cairo; 2006. behavioural surveillance survey among vulnerable women in Hargeisa,
57. Ministry of Health, National AIDS Program, Family Health International, Somaliland. International Organization for Migration. Geneva; 2017.
Center for Development Services. HIV/AIDS biological & behavioral 75. Elkarim MAA, AHA, Ahmed S.M., et al: Situation analysis: behavioral &
surveillance survey round II: summary report. National AIDS Program-Egypt. epidemiological surveys & response analysis - HIV/AIDS strategic planning
Cairo; 2010. process 2002.
58. Navadeh S, Mirzazadeh A, Mousavi L, Haghdoost A, Fahimfar N, Sedaghat A. 76. Abdelrahim MS. HIV prevalence and risk behaviors of female sex workers in
HIV, HSV2 and syphilis prevalence in female sex workers in Kerman, south- Khartoum, North Sudan. Aids. 2010;24(SUPPL. 2):S55–60.
east Iran; using respondent-driven sampling. Iran J Public Health. 2012; 77. Sudan National AIDS Control Programme: UNGASS report 2008–2009, North
41(12):60–5. Sudan.2010.
59. Sajadi L, Mirzazadeh A, Navadeh S, Osooli M, Khajehkazemi R, Gouya 78. Sudan National AIDS Control Program: Integrated bio-behavioral HIV
MM, Fahimfar N, Zamani O, Haghdoost AA. HIV prevalence and surveillance (IBBS) among female sex workers and men who have sex with
related risk behaviours among female sex workers in Iran: results of men in 15 states of Sudan, 2011–2012. 2012.
the national biobehavioural survey, 2010. Sex Transm Infect. 2013; 79. Government of the Republic of South Sudan-Ministry of Health. A bio-behavioral
89(Suppl 3):iii37–40. HIV survey of female sex workers in South Sudan. South Sudan HIV/AIDS
60. Kazerooni PA, Motazedian N, Motamedifar M, Sayadi M, Sabet M, Lari MA, Commission. Juba; 2016.
Kamali K. The prevalence of human immunodeficiency virus and sexually 80. Hsairi M, Ben AS. Enquête sérocomportementale du VIH auprès des
transmitted infections among female sex workers in Shiraz, south of Iran: by travailleuses du sexe clandestines en Tunisie. Ministere de la Sante-Tunisie.
respondent-driven sampling. Int J STD AIDS. 2014;25(2):155–61. Tunis; 2012.
61. Moayedi-Nia S, Bayat Jozani Z, Esmaeeli Djavid G, Entekhabi F, Bayanolhagh 81. Stulhofer A, Bozicevic I. HIV bio-behavioural survey among FSWs in Aden,
S, Saatian M, Sedaghat A, Nikzad R, Jahanjoo Aminabad F, Mohraz M. HIV, Yemen; 2008.
HCV, HBV, HSV, and syphilis prevalence among female sex workers in 82. Ministry of Health-Republic of Yemen. UNGASS Country Progress Report
Tehran, Iran, by using respondent-driven sampling. AIDS Care. 2016;28(4): 2013. Ministry of Health-Yemen. Sanaa; 2014.
487–90. 83. Todd CS, Nasir A, Stanekzai MR, Bautista CT, Botros BA, Scott PT, Strathdee
62. Mirzazadeh A, Shokoohi M, Khajehkazemi R, et al. HIV and sexually SA, Tjaden J. HIV, hepatitis B, and hepatitis C prevalence and associated risk
transmitted infections among female sex workers in Iran: findings from the behaviors among female sex workers in three Afghan cities. Aids. 2010;
2010 and 2015 national surveillance surveys. In: 21st International AIDS 24(Suppl 2):S69–75.
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 28 of 30

84. Rodier GR, Couzineau B, Gray GC, Omar CS, Fox E, Bouloumie J, Watts D. 106. Scott DA, Corwin AL, Constantine NT, Omar MA, Guled A, Yusef M, Roberts
Trends of human immunodeficiency virus type-1 infection in female CR, Watts DM. Low prevalence of human immunodeficiency virus-1 (HIV-1),
prostitutes and males diagnosed with a sexually transmitted disease in HIV-2, and human T cell lymphotropic virus-1 infection in Somalia. Am J
Djibouti, East Africa. Am J Trop Med Hyg. 1993;48(5):682–6. Trop Med Hyg. 1991;45(6):653–9.
85. Couzineau B, Bouloumie J, Hovette P, Laroche R. Prevalence of AIDS 107. Corwin AL, Olson JG, Omar MA, Razaki A, Watts DM. HIV-1 in Somalia:
infection in target people of the Republic of Djibouti. [French]. Med Trop. prevalence and knowledge among prostitutes. Aids. 1991;5(7):902–4.
1991;51(4):485–6. 108. Burans JP, McCarthy M, el Tayeb SM, el Tigani A, George J, Abu-Elyazeed R,
86. Philippon M, Saada M, Kamil MA, Houmed HM. Attendance at a health Woody JN. Serosurvey of prevalence of human immunodeficiency virus
center of clandestine prostitutes in Djibouti. [French]. Cahiers Sante. 1997; amongst high risk groups in Port Sudan, Sudan. East Afr Med J. 1990;67(9):
7(1):5–10. 650–5.
87. Marcelin AG, Grandadam M, Flandre P, Nicand E, Milliancourt C, Koeck JL, 109. McCarthy MC, Khalid IO, El Tigani A. HIV-1 infection in Juba, southern
Philippon M, Teyssou R, Agut H, Dupin N, et al. Kaposi’s sarcoma herpesvirus Sudan. J Med Virol. 1995;46(1):18–20.
and HIV-1 seroprevalences in prostitutes in Djibouti. J Med Virol. 2002;68(2): 110. Bchir A, Jemni L, Saadi M, Milovanovic A, Brahim H, Catalan F. Markers of
164–7. sexually transmitted diseases in prostitutes in Central Tunisia. Genitourin
88. Sheba MF, Woody JN, Zaki AM, Morrill JC, Burans J, Farag I, Kashaba S, Med. 1988;64(6):396–7.
Madkour S, Mansour M. The prevalence of HIV infection in Egypt. Trans R 111. Hassen E, Chaieb A, Letaief M, Khairi H, Zakhama A, Remadi S, Chouchane L.
Soc Trop Med Hyg. 1988;82(4):634. Cervical human papillomavirus infection in Tunisian women. Infection. 2003;
89. Watts DM, Constantine NT, Sheba MF, Kamal M, Callahan JD, Kilpatrick ME. 31(3):143–8.
Prevalence of HIV infection and AIDS in Egypt over four years of 112. Znazen A, Frikha-Gargouri O, Berrajah L, Bellalouna S, Hakim H, Gueddana N,
surveillance (1986–1990). J Trop Med Hygiene. 1993;96(2):113–7. Hammami A. Sexually transmitted infections among female sex workers in
90. Kabbash IA, Abdul-Rahman I, Shehata YA, Omar AA. HIV infection and Tunisia: high prevalence of Chlamydia trachomatis. Sex Transm Infect. 2010;
related risk behaviours among female sex workers in greater Cairo, Egypt. 86(7):500–5.
Eastern Mediterr Health J. 2012;18(9):920–7. 113. Ministere de la Sante et de la Population et de la Reforme Hospitaliere,
91. Jahani MR, Alavian SM, Shirzad H, Kabir A, Hajarizadeh B. Distribution and Direction de la Prevention Comite National de Lutte contre les IST/VIH/
risk factors of hepatitis B, hepatitis C, and HIV infection in a female SIDA. Plan national strategique de lutte contre les IST/VIH/Sida 2008–2012.
population with “illegal social behaviour”. Sex Transm Infect. 2005;81(2):185. Programme Commun des Nations Unies sur le VIH/SIDA (ONUSIDA).
92. Kassaian N, Ataei B, Yaran M, Babak A, Shoaei P, Ataie M. HIV and other Geneva; 2009.
sexually transmitted infections in women with illegal social behavior in 114. Fox E, Haberberger RL Jr, Abbatte EA, Said S, Polycarpe D, Constantine NT.
Isfahan, Iran. Adv Biomed Res. 2012;1:5. Observations on sexually transmitted diseases in promiscuous males in
93. Taghizadeh H, Taghizadeh F, Fathi M, Reihani P, Shirdel N, Rezaee SM. Drug Djibouti. J Egyptian Public Health Assoc. 1989;64(5–6):561–9.
use and high-risk sexual behaviors of women at a drop-in center in 115. Organisation Mondiale pour la Sante-Djibouti. Etudes epidemiologiques sur
Mazandaran Province, Iran, 2014. Iran J Psychiatry Behav Sci. 2015;9(2):49–55. le VIH/SIDA et les IST a Djibouti de 1986 a 2001, Bulletin Epidémiologique
94. Asadi-Ali Abadi M, Abolghasemi J, Rimaz S, Majdzadeh R, Shokoohi M, Hebdomadaire de l’OMS; 2001. p. 49.
Rostami-Maskopaee F, Merghati-Khoei E. High-risk behaviors among regular 116. Ministry of Health-Djibouti: Rapport de la Surveillance de l’Infection a
and casual female sex workers in Iran: a report from Western Asia. Iran J VIH par Pasles Sentinelles en Republique de Djibouti, juillet - octobre
Psychiatry Behav Sci. 2018; In Press(In Press):e9744. 1993.1993.
95. Naman RE, Mokhbat JE, Farah AE, Zahar KL, Ghorra FS. Seroepidemiology of 117. Association Internationale de Developpement (IDA), Ministere de la Sante-
the human immunodeficiency virus in Lebanon. Preliminary evaluation. L Djibouti. Epidemie a VIH/SIDA/IST en Republique de Djibouti Tome I:
Med J. 1989;38(1):5–8. Analyse de la situation et analyse de la reponse nationale. CREDES. Paris;
96. Programme National de lutte contre les IST/SIDA, Ministere de la Sante- 2002.
Royaume du Maroc, Programme National de lutte contre les IST/SIDA. 118. Bortolotti V. Surveillance Sentinelle de L’Infection par le VIH 2006.
Etude de prevalence des IST chez les femmes qui consultent pour pertes Organisation Mondiale de la Sante. Djibouti; 2007.
vaginales et/ou douleurs du bas ventre. Ministere de la Sante-Maroc. Rabat; 119. Sadek A, Bassily S, Bishai M, et al. Human immunodeficiency virus and other
2008. sexually transmitted pathogens among STD patients in Cairo, Egypt. In: VII
97. Iqbal J, Rehan N. Sero-prevalence of HIV: six years’ experience at Shaikh International Conference on AIDS, Florence, Italy, 6/16–21, Poster MC3033:
Zayed Hospital, Lahore. J Pakistan Med Assoc. 1996;46(11):255–8. 1991; 1991.
98. Baqi S, Nabi N, Hasan SN, Khan AJ, Pasha O, Kayani N, Haque RA, Haq IU, 120. Fox E. HIV surveillance in Egypt. The Joint United Nations Programme on
Khurshid M, Fisher-Hoch S, et al. HIV antibody seroprevalence and HIV/AIDS (UNAIDS). Cairo; 1994.
associated risk factors in sex workers, drug users, and prisoners in Sindh, 121. Saleh EE, McFarland W, Rutherford G, et al. Sentinel surveillance for HIV and
Pakistan. J Acquir Immune Defic Syndr Hum Retrovirol. 1998;18(1):73–9. markers for high risk behaviors. In: XIII International AIDS Conference,
99. Anwar M, Jaffery G, Rasheed S. Serological screening of female prostitutes Durban, South Africa, 7/9–14, Poster MoPeC2398: 2000; 2000.
for anti-HIV and hepatitis B surface antigen. Pak J Health. 1998;35(3–4):69– 122. Kuwait National AIDS Program: Update UNAIDS epidemiological fact sheet
73. 1999.
100. Shah AS, Memon MA, Soomro S, Kazi N, Kristensen S. Seroprevalence of HIV, 123. Murzi M. Plan to combat AIDS, testing described. Joint Publication Res Serv.
syphilis, hepatitis B and hepatitis C among female commercial sex workers 1989;16:17–8.
in Hyderabad, Pakistan. Int AIDS Conf. 2004;2004:C12368. 124. Al-Owaish RA, Anwar S, Sharma P, Shah SF. HIV/AIDS prevalence among
101. Shah AS, Ghauri AK, Memon MA, Shaikh SA, Abbas SQ, Kristensen S. HIV male patients in Kuwait. Saudi Med J. 2000;21(9):852–9.
infection trends in the Sindh Province of Pakistan. In: International AIDS 125. Alowaish R, Anwar S. Sexually transmitted diseases among bachelor
Conference, C12336: 2004; 2004. community in Kuwait. Int AIDS Conf. 2002;2002:C11000.
102. Akhtar A, Aslam M, Arif M, Rehman K. Safer sex knowledge and attitude of 126. Al-Mutairi N, Joshi A, Nour-Eldin O, Sharma AK, El-Adawy I, Rijhwani M.
female sex workers in Pakistan. In: International AIDS Conference, Clinical patterns of sexually transmitted diseases, associated
THPE0334: 2008; 2008. sociodemographic characteristics, and sexual practices in the Farwaniya
103. Raza M, Ikram N, Saeed N, Waheed U, Kamran M, Iqbal R, Bakar M. HIV/AIDS region of Kuwait. Int J Dermatol. 2007;46(6):594–9.
and syphilis screening among high risk groups. J Rawal Med Coll. 2015; 127. Heikel J, Sekkat S, Bouqdir F, Rich H, Takourt B, Radouani F, Hda N, Ibrahimy
19(1):11–4. S, Benslimane A. The prevalence of sexually transmitted pathogens in
104. Jama H, Grillner L, Biberfeld G, Osman S, Isse A, Abdirahman M, Bygdeman patients presenting to a Casablanca STD clinic. Eur J Epidemiol. 1999;15(8):
S. Sexually transmitted viral infections in various population groups in 711–5.
Mogadishu, Somalia. Genitourin Med. 1987;63(5):329–32. 128. Manhart LE, Zidouh A, Holmes K, et al. Sexually transmitted disease (STD) in
105. Burans JP, Fox E, Omar MA, Farah AH, Abbass S, Yusef S, Guled A, Mansour three types of health clinics in Morocco: prevalence, risk factors, and
M, Abu-Elyazeed R, Woody JN. HIV infection surveillance in Mogadishu, syndromic management. In: XI International Conference on AIDS,
Somalia. East Afr Med J. 1990;67(7):466–72. Vancouver, 7/7–14, Poster MoC1627: 1996; 1996.
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 29 of 30

129. Alami K, Mbarek Ait N, Akrim M, Bellaji B, Hansali A, Khattabi H, Sekkat A, El commercial sex workers and intravenous drug users. Mid-term report. In:
Aouad R, Mahjour J. Urethral discharge in Morroco: prevalence of American University of Beirut and World Bank; 2008.
microorganisms and susceptibility of gonococcos. East Mediterr Health J. 155. Morison L, Weiss HA, Buve A, Carael M, Abega SC, Kaona F, Kanhonou L,
2002;8(6):794–804. Chege J, Hayes RJ, Study Group on Heterogeneity of HIV Epidemics in
130. Ministere de la Sante-Maroc: Etude sur les ecoulements urethraux, prevalence African Cities. Commercial sex and the spread of HIV in four cities in sub-
des germes et sensibilite du gonococque aux antibiotiques. 2001. Saharan Africa. AIDS. 2001;15(Suppl 4):S61–9.
131. Khattabi H, Alami K. Surveillance sentinelle du VIH: Resultats 2004 et 156. Lau JT, Tsui HY, Siah PC, Zhang KL. A study on female sex workers in
tendances de la seroprevalence du VIH. Ministere de la Sante-Maroc. Rabat; southern China (Shenzhen): HIV-related knowledge, condom use and STD
2005. history. AIDS Care. 2002;14(2):219–33.
132. Ministere de la Sante-Royaume du Maroc: Rapport sur les estimations de 157. Strathdee SA, Lozada R, Semple SJ, Orozovich P, Pu M, Staines-Orozco H,
l’epidemie du VIH/sida au Maroc. 2013. Fraga-Vallejo M, Amaro H, Delatorre A, Magis-Rodriguez C, et al.
133. Abu-Raddad L, Akala FA, Semini I, Riedner G, Wilson D, Tawil O. Characteristics of female sex workers with US clients in two Mexico-US
Characterizing the HIV/AIDS epidemic in the Middle East and North Africa: border cities. Sex Transm Dis. 2008;35(3):263–8.
time for strategic action. Washington DC: The World Bank Press; 2010 158. Elmore-Meegan M, Conroy RM, Agala CB. Sex workers in Kenya, numbers of
134. Mujeeb SA, Hafeez A. Prevalence and pattern of HIV infection in Karachi. J clients and associated risks: an exploratory survey. Reprod Health Matters.
Pakistan Med Assoc. 1993;43(1):2–4. 2004;12(23):50–7.
135. Memon GM. Serosurveillance of HIV infection in people at risk in Hyderabad 159. Mumtaz GR, Weiss HA, Vickerman P, Larke N, Abu-Raddad LJ. Using hepatitis
Sindh. J Pak Med Assoc. 1997;47(12):302–4. C prevalence to estimate HIV epidemic potential among people who inject
136. National AIDS Programme. HIV seroprevalence surveys in Pakistan. AIDS. drugs in the Middle East and North Africa. AIDS. 2015;29(13):1701–10.
1996;10(8):926–7. 160. Akbarzadeh V, Mumtaz GR, Awad SF, Weiss HA, Abu-Raddad LJ. HCV
137. Rehan N. Profile of men suffering from sexually transmitted infections in prevalence can predict HIV epidemic potential among people who
Pakistan. J Ayub Med Coll Abbottabad. 2003;15(2):15–9. inject drugs: mathematical modeling analysis. BMC Public Health. 2016;
138. Bhutto AM, Shah AH, Ahuja DK, Solangi AH, Shah SA. Pattern of sexually 16(1):1216.
transmitted infections in males in interior Sindh: a 10-year-study. J Ayub 161. Mumtaz GR, Weiss HA, Abu-Raddad LJ. Hepatitis C virus and HIV infections
Med Coll Abbottabad. 2011;23(3):110–4. among people who inject drugs in the Middle East and North Africa: a
139. Razvi SK, Najeeb S, Nazar HS. Pattern of sexually transmitted diseases in neglected public health burden? J Int AIDS Soc. 2015;18:20582.
patients presenting at Ayub teaching hospital, Abbottabad. J Ayub Med 162. Kassaian N, Ataei B, Yaran M, Babak A, Shoaei P. Hepatitis B and C among
Coll Abbottabad. 2014;26(4):582–3. women with illegal social behavior in Isfahan, Iran: seroprevalence and
140. National AIDS Control Program, Balochistan AIDS Control Program, Canada associated factors. Hepat Mon. 2011;11(5):368–71.
Pakistan HIV/AIDS Surveillance Project. Bio behavioral survey among mine 163. Decker MR, Wirtz AL, Baral SD, Peryshkina A, Mogilnyi V, Weber RA,
workers in Balochistan, Pakistan. National AIDS Control Program-Pakistan. Stachowiak J, Go V, Beyrer C. Injection drug use, sexual risk, violence and
Islamabad; 2012. STI/HIV among Moscow female sex workers. Sex Transm Infect. 2012;88(4):
141. Ismail SO, Ahmed HJ, Grillner L, Hederstedt Issa BA, Bygdeman S. Sexually 278–83.
transmitted diseases in men in Mogadishu, Somalia. Int J STD AIDS. 1990; 164. Ouedraogo HG, Ky-Zerbo O, Baguiya A, Grosso A, Goodman S,
1(2):102–6. Samadoulougou BC, Lougue M, Sawadogo N, Traore Y, Barro N, et al. HIV
142. Duffy G. Report on STD/HIV prevalence study in Somaliland: part 2; 1999. among female sex workers in five cities in Burkina Faso: a cross-sectional
143. World Health Organization: The 2004 First National Second Generation HIV/ baseline survey to inform HIV/AIDS programs. AIDS Res Treat. 2017;2017:
AIDS/STI Sentinel Surveillance Survey Among Pregnant Women Attending 9580548.
Antenatal Clinics, Tuberculosis and STD Patients. 2005. 165. Isac S, Ramesh BM, Rajaram S, Washington R, Bradley JE, Reza-Paul S, Beattie
144. The United Nations Refugee Agency (UNHCR). HIV sentinel surveillance among TS, Alary M, Blanchard JF, Moses S. Changes in HIV and syphilis prevalence
antenatal clients and STI patients in Dadaab refugee camps, Kenya. The United among female sex workers from three serial cross-sectional surveys in
Nations Refugee Agency. Nairobi; 2007. Karnataka state, South India. BMJ Open. 2015;5(3):e007106.
145. Ismail A, Ekanem E, Deq S, Arube P, Gboun M. Somaliland 2007 HIV/syphilis 166. Auvert B, Taljaard D, Lagarde E, Sobngwi-Tambekou J, Sitta R, Puren A.
sero-prevalence survey: a technical report; 2007. Randomized, controlled intervention trial of male circumcision for reduction
146. The Somaliland Puntland and South Central AIDS commissions (NACs): of HIV infection risk: the ANRS 1265 Trial. PLoS Med. 2005;2(11):e298.
Somalia United Nations General Assembly Special Session on HIV/AIDS 167. Bailey RC, Moses S, Parker CB, Agot K, Maclean I, Krieger JN, Williams CFM,
country progress report 2010. 2010. Campbell RT, Ndinya-Achola JO. Male circumcision for HIV prevention in
147. McCarthy MC, Burans JP, Constantine NT, El-Tigani El-Hag AA, El-Saddig El- young men in Kisumu, Kenya: a randomised controlled trial. Lancet. 2007;
Tayeb M, El-Dabi MA, Fahkry JG, Woody JN, Hyams KC. Hepatitis B and HIV 369(9562):643–56.
in Sudan: a serosurvey for hepatitis B and human immunodeficiency virus 168. Gray RH, Kigozi G, Serwadda D, Makumbi F, Watya S, Nalugoda F, Kiwanuka
antibodies among sexually active heterosexuals. Am J Trop Med Hyg. 1989; N, Moulton LH, Chaudhary MA, Chen MZ, et al. Male circumcision for HIV
41(6):726–31. prevention in men in Rakai, Uganda: a randomised trial. Lancet. 2007;
148. McCarthy MC, Hyams KC, El-Tigani El-Hag A, El-Dabi MA, El-Sadig El-Tayeb 369(9562):657–66.
M, Khalid IO, George JF, Constantine NT, Woody JN. HIV-1 and hepatitis B 169. Weiss HA, Quigley MA, Hayes RJ. Male circumcision and risk of HIV infection
transmission in Sudan. Aids. 1989;3(11):725–9. in sub-Saharan Africa: a systematic review and meta-analysis. AIDS. 2000;
149. United States Census Bureau. HIV/AIDS surveillance database. United States 14(15):2361–70.
Census Bureau. Washington, DC; 2017. 170. Morris BJ, Wamai RG, Henebeng EB, Tobian AA, Klausner JD, Banerjee J,
150. Abdol-Quauder AM. Acute Gonorrhoea in Yemen Republic Epidemiological Hankins CA. Estimation of country-specific and global prevalence of male
View. In: VIII International Conference on AIDS in Africa, Marrakech, circumcision. Popul Health Metrics. 2016;14:4.
Morocco, 12/12–16, Abstract TPC080: 1993; 1993. 171. Alsallaq RA, Cash B, Weiss HA, Longini IM Jr, Omer SB, Wawer MJ, Gray RH,
151. Jenkins C, Robalino DA. HIV/AIDS in the Middle East and North Africa: the Abu-Raddad LJ. Quantitative assessment of the role of male circumcision in
costs of inaction. Washigton, D.C.: The World Bank; 2003. HIV epidemiology at the population level. Epidemics. 2009;1(3):139–52.
152. Awad SF, Abu-Raddad LJ. Could there have been substantial declines in 172. Manopaiboon C, Prybylski D, Subhachaturas W, Tanpradech S,
sexual risk behavior across sub-Saharan Africa in the mid-1990s? Epidemics. Suksripanich O, Siangphoe U, Johnston LG, Akarasewi P, Anand A, Fox
2014;8:9–17. KK, et al. Unexpectedly high HIV prevalence among female sex workers
153. Family Health International, Implementing AIDS Prevention and Care Project in Bangkok, Thailand in a respondent-driven sampling survey. Int J STD
(IMPACT). Egypt’s final report April 1999–September 2007 for USAID’s AIDS. 2013;24(1):34–8.
Implementing AIDS Prevention and Care (IMPACT) Project. Family Health 173. Baral S, Beyrer C, Muessig K, Poteat T, Wirtz AL, Decker MR, Sherman SG,
International. Arlington; 2007. Kerrigan D. Burden of HIV among female sex workers in low-income and
154. Mishwar. An integrated bio-behavioral surveillance study among four middle-income countries: a systematic review and meta-analysis. Lancet
vulnerable groups in Lebanon: men who have sex with men; prisoners, Infect Dis. 2012;12(7):538–49.
Chemaitelly et al. BMC Medicine (2019) 17:119 Page 30 of 30

174. Papworth E, Ceesay N, An L, Thiam-Niangoin M, Ky-Zerbo O, Holland C, Programme Commun Des Nationa Unies sure le VIH/SIDA (ONUSIDA) and
Drame FM, Grosso A, Diouf D, Baral SD. Epidemiology of HIV among female The United Nations Children's Fund (UNICEF). Geneva; 2016.
sex workers, their clients, men who have sex with men and people who 197. Ministere de la Sante et de la Population et de la Reforme Hospitaliere.
inject drugs in West and Central Africa. J Int AIDS Soc. 2013;16(Suppl 3): Rapport d’activite sur la riposte nationale au VIH/SIDA, Algerie 2014.
18751. Programme Commun Des Nationa Unies sure le VIH/SIDA (ONUSIDA).
175. Farmanfarmaee S, Habibi M, Darharaj M, Khoshnood K, Zadeh Mohammadi Algerie; 2014.
A, Kazemitabar M. Predictors of HIV-related high-risk sexual behaviors 198. Ministere de la Sante et de la Population et de la Reforme Hospitaliere.
among female substance users. J Subst Abus. 2018;23(2):175–80. Rapport narratif de la riposte au VIH/SIDA. Algerie; 2017.
176. Mirahmadizadeh AR, Majdzadeh R, Mohammad K, Forouzanfar MH. 199. Elhadi M, Elbadawi A, Abdelrahman S, Mohammed I, Bozicevic I, Hassan EA,
Prevalence of HIV and hepatitis C virus infections and related behavioral Elmukhtar M, Ahmed S, Abdelraheem MS, Mubarak N, et al. Integrated bio-
determinants among injecting drug users of drop-in centers in Iran. Iran behavioural HIV surveillance surveys among female sex workers in Sudan,
Red Crescent Med J. 2009;11(3):325–9. 2011–2012. Sex Transm Infect. 2013;89(Suppl 3):iii17–22.
177. Melesse DY, Shafer LA, Emmanuel F, Reza T, Achakzai BK, Furqan S, 200. Busulwa R. HIV/AIDS situation analysis study, conducted in Hodeidah, Taiz
Blanchard JF. Heterogeneity in geographical trends of HIV epidemics and Hadhramut, Republic of Yemen. United Nations Development
among key populations in Pakistan: a mathematical modeling study of Programme, World Health Organization, and National AIDS Program-
survey data. J Glob Health. 2018;8(1):010412. Ministry of Health and Population. Sanaa; 2003.
178. Melesse DY, Shafer LA, Shaw SY, Thompson LH, Achakzai BK, Furqan S, Reza T,
Emmanuel F, Blanchard JF. Heterogeneity among sex workers in overlapping
HIV risk interactions with people who inject drugs: a cross-sectional study from
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in
8 major cities in Pakistan. Medicine (Baltimore). 2016;95(12):e3085.
published maps and institutional affiliations.
179. Vandepitte J, Lyerla R, Dallabetta G, Crabbe F, Alary M, Buve A. Estimates of
the number of female sex workers in different regions of the world. Sex
Transm Infect. 2006;82(Suppl 3):iii18–25.
180. Carael M, Slaymaker E, Lyerla R, Sarkar S. Clients of sex workers in different
regions of the world: hard to count. Sex Transm Infect. 2006;82(Suppl 3):
iii26–33.
181. Blanchard JF, Khan A, Bokhari A. Variations in the population size,
distribution and client volume among female sex workers in seven cities of
Pakistan. Sex Transm Infect. 2008;84(SUPPL. 2):ii24–7.
182. Mumtaz GR, Kouyoumjian SP, Hilmi N, Zidouh A, El Rhilani H, Alami K,
Bennani A, Gouws E, Ghys PD, Abu-Raddad LJ. The distribution of new HIV
infections by mode of exposure in Morocco. Sex Transm Infect. 2013;
89(Suppl 3):iii49–56.
183. Kouyoumjian SP, Mumtaz GR, Hilmi N, Zidouh A, El Rhilani H, Alami K,
Bennani A, Gouws E, Ghys PD, Abu-Raddad LJ. The epidemiology of HIV
infection in Morocco: systematic review and data synthesis. Int J STD AIDS.
2013;24(7):507–16.
184. Kouyoumjian SP, El Rhilani H, Latifi A, El Kettani A, Chemaitelly H, Alami K,
Bennani A, Abu-Raddad LJ. Mapping of new HIV infections in Morocco and
impact of select interventions. Int J Infect Dis. 2018;68:4–12.
185. Abu-Raddad LJ, Akala FA, Semini I, Riedner G, Wislon D, Tawil O. Policy
notes. Characterizing the HIV/AIDS epidemic in the Middle East and North
Africa: time for strategic action. Middle Wast and North Africa HIV/AIDS
Epidemiology Synthesis Project. World Bank/UNAIDS/WHO publication.
Washington (D.C.): The World Bank Press; 2010.
186. Mohebbi MR. Female sex workers and fear of stigmatisation. Sex Transm
Infect. 2005;81(2):180–1.
187. Dejong J, Mortagy I. The struggle for recognition by people living with HIV/
AIDS in Sudan. Qual Health Res. 2013;23(6):782–94.
188. DeJong J, Mahfoud Z, Khoury D, Barbir F, Afifi RA. Ethical considerations in
HIV/AIDS biobehavioral surveys that use respondent-driven sampling:
illustrations from Lebanon. Am J Public Health. 2009;99(9):1562–7.
189. Ministry of Health-Kingdom of Bahrain. UNGASS country progress report -
Kingdom of Bahrain: January 2012–December 2013. Ministry of Health-
Bahrain. Manama; 2014.
190. Ministry of Health-United Arab Emirates. United Arab Emirates – Global
AIDS response progress report 2014. Ministry of Health-United Arab
Emirates. Dubai; 2014.
191. Sultanate of Oman: Global AIDS response progress report 2014: January
2012–December 2013. 2014.
192. Ministry of Health-Kingdom of Saudi Arabia: Global AIDS response progress
report 2015. 2015.
193. The Joint United Nations Programme on HIV/AIDS (UNAIDS). UNAIDS 2016–
2021 strategy: on the fast-track to end AIDS. UNAIDS. Geneva; 2015.
194. El-Rhilani H. National voluntary counseling and testing database. The Joint
United Nations Programme on HIV/AIDS-Morocco. Rabat; 2010.
195. Ministry of Health-Kingdom of Morocco: Historique de la Surveillance
Sentinelle du VIH au Maroc par Site Depuis 1999. 2008.
196. Ministere de la Sante et de la Population et de la Reforme Hospitaliere,
Direction de la Prevention Comite National de Lutte contre les IST/VIH/
SIDA. Plan national strategique de lutte contre les IST/VIH/SIDA 2013–2015.

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