HIV Testing and Counseling Among Female Sex Workers: A Systematic Literature Review

HIV testing uptake continues to be low among Female Sex Workers (FSWs). We synthesizes evidence on barriers and facilitators to HIV testing among FSW as well as frequencies of testing, willingness to test, and return rates to collect results. We systematically searched the MEDLINE/PubMed, EMBASE, SCOPUS databases for articles published in English between January 2000 and November 2017. Out of 5036 references screened, we retained 36 papers. The two barriers to HIV testing most commonly reported were financial and time costs—including low income, transportation costs, time constraints, and formal/informal payments—as well as the stigma and discrimination ascribed to HIV positive people and sex workers. Social support facilitated testing with consistently higher uptake amongst married FSWs and women who were encouraged to test by peers and managers. The consistent finding that social support facilitated HIV testing calls for its inclusion into current HIV testing strategies addressed at FSW.


Introduction
Worldwide, early HIV testing is a public health priority especially among key populations such as female sex workers (FSWs) [1][2][3]: out of the estimated 33 million people living with HIV in the world, 19 million do not know their status [1]. Early HIV diagnosis has gained significant attention within key global health institutions, including the Joint United Nations Program on HIV/AIDS (UNAIDS) and the recently established 90-90-90 targets [4]. It is proposed that by 2020, 90% of all people living with HIV should know their HIV status, 90% of all people with diagnosed HIV should receive sustained antiretroviral treatment, and 90% of all people receiving antiretroviral treatment should reach viral suppression [4]. Historically, HIV prevention efforts focused on key populations, including sex workers, as an effective approach to reduce HIV transmission, particularly in the early phase of the epidemic [5].
Several systematic reviews have examined HIV prevalence [6][7][8] and effectiveness of different HIV prevention interventions for SWs [9][10][11][12]. Shahmanesh et al. presented evidence for the efficacy of multi-component interventions, and⁄or structural interventions [9]. A Cochrane review of behavioral interventions concluded that, compared with standard care or no intervention, behavioral interventions are effective in reducing HIV and the incidence of STIs amongst FSWs [10]. A systematic review of community empowerment interventions in low-and middle-income countries demonstrated significant protective combined effect for HIV infection (prevalence), STIs such as gonorrhea and chlamydia, and increase of consistent condom use with all clients [12]. A systematic review of community empowerment interventions in generalized and concentrated epidemics has shown their positive impact on HIV prevalence, estimated number of averted infections among SWs and adult population, and expanded coverage of ART [11]. These previous studies did not systematically assess HIV testing approaches, but rather examined the combined effect of a variety of prevention activities. Thus, they failed to address unique determinants of different HIV testing approaches.
HIV testing activities among sex workers were assessed in only two papers including a meta-analysis of communitybased approaches [13], and a study of barriers to HIV testing in Europe [14]. According to these studies, communitybased HIV testing leads to higher HIV testing rates than facility-based testing, and the most common barriers to HIV testing are low-risk perception, fear and worries, poor accessibility to healthcare services, health providers' reluctance to offer the test, and scarcity of financial and human resources. Still, neither of those studies focused on FSWs nor systematically reviewed unique facilitators and barriers to HIV testing faced by this group. The present review compiles existing evidence on HIV testing among FSWs in order to better meet the needs of this group while implementing the first target of the 90-90-90 strategy. Our specific objectives are: (1) to summarize data on key barriers and facilitators to HIV testing among FSWs, and (2) to systematically review frequencies of testing, willingness to test, and return rates to collect HIV test results in this population.

Methods
We applied a free text strategy and MeSH terms to systematically scan the electronic databases MEDLINE/PubMed using the platform OVID, and EMBASE and SCOPUS. We employed a combination of terms that covered the concepts 'HIV', 'Sex work' and 'Test'. We conducted several scoping searches to identify the most efficient search strategy, which we provide in "Annex 1: Search strategy". Guidelines, reports and policy documents were searched using Google Scholar and employed to inform the discussion of findings. We exported all identified references (5036) into the bibliographic management software ENDNOTE X7.
The first author (AT) screened titles and abstracts against the following inclusion criteria: (1) published in a peer-reviewed journal between January 2000 and November 2017; (2) written in English; and (3) presenting data on HIV testing among FSWs. We excluded duplicates and studies for which no abstract or full text was available (N = 17). After reviewing the full text of 95 pre-selected articles against the above mentioned inclusion criteria, 36 papers were retained for a more detailed review. The first author extracted data systematically using a standardized form that included information on the period of study, location, study population, design, research questions, key findings, and conclusions ("Annex 2: Data extraction form"). Next the quality of qualitative papers was assessed using the guide for critically appraising qualitative research by Spencer et al. [15]. The modified Downs and Black checklist was applied to quantitative and mixed-methods papers [16]. We used a midpoint score of 9 for qualitative papers and 12.5 for quantitative ones as a cut off between low-and high-quality studies. Overall, two quantitative papers with score of 10 [18] and 9 [17] points failed to meet the criteria; three papers received 12 points [19,20]. The vast majority of quantitative papers lacked information needed for assessment. We were unable to appraise four abstracts: three, for the limited data presented, and one, being a mathematical modeling paper [21] that did not fit well with the quality appraisal tools employed. We decided to include all papers into the review in order to provide a comprehensive picture; at the same time, we considered it important to stress the results of the quality assessment ("Annex 3: Quality assessment"). The results of the search and screening process are described in Fig. 1.
Guided by the socio-ecological model (SEM) developed by Blanchard et al. [22] we classified data into three levels: macro-, meso-, and micro-level factors ( Table 1). The macro level consisted of economic and policy factors. The meso level included social networks, organizations, cultural norms, and values. The micro level included individual socio-demographic characteristics, knowledge, risk awareness, and behavioral factors. We also extracted data on previous experiences of HIV testing and ways to encourage uptake. The PRISMA check list is provided as "Annex 4: PRISMA 2009 Checklist".

Results
Out of the 36 studies retained for review, most were quantitative (N = 20) and conducted in Asia (N = 18). Nine papers reported work conducted in Africa, three in Europe, three in Russia, and one in Macedonia. Three studies were conducted in Latin America, two in Canada and one in Australia. Eighteen studies were cross-sectional, and twenty-five focused exclusively on FSWs.
We identified a high variability of outcome measures employed in the studies reviewed. For example, the frequency of HIV testing was measured using different time frames and included "last month" and "recent testing" with a time period corresponding to "recent" that varied from 1 year to 1 month.

Conceptual Framework: Barriers and Facilitators of HIV Testing Amongst FSWs
In this study we employed an adapted version of the socioecological framework developed by Blanchard et al. [22] to organize and analyze our findings systematically. As shown in Fig. 2 n/a n/a n/a n/a n/a n/a n/a n/a n/a 6. Burke et al. [54] n/a n/a n/a n/a n/a n/a n/a n/a n/a n/a n/a n/a Oral fluid test Home testing 36. Xu et al. [23] n/a n/a n/a n/a

Socio Demographic Characteristics
Sixteen articles focused on socio-demographic characteristics. We found no consistent associations [18,27,31,32,[44][45][46] of education and age [23,31,45] with HIV testing uptake. Highly educated women in the Philippines and Iran were more likely to test [39,45], but studies in China reported higher HIV testing uptake amongst women with both high [23] and low education level [31]. In two studies conducted in China and one in the Philippines, older age facilitated HIV testing [31,44,45], but in Russia, Ethiopia and Kenya older-aged FSWs [46,47] and those aged + 30 [27] were less likely to test compared to younger FSWs. In Uzbekistan and India, younger age decreased testing [18,32]. Higher income was associated with testing in India and the Philippines [18,45] and in Russia poverty impeded access to healthcare, including HIV testing [24]. Ten studies reported that having children and/or being pregnant and/or being in a permanent relationship facilitated HIV testing [19,23,27,28,30,34,45,[47][48][49]. Married women in China [19] and those with a regular sexual partner in the Philippines [45] and in China [23] were more likely to test. According to a study conducted in Vietnam, unmarried women were less likely to test [30]. In Kenya, Zambia, Benin, Ethiopia, Russia and India, having children or being pregnant facilitated HIV testing [27,28,34,[47][48][49]. In Iran, incarceration was associated with recent testing [39].
In Canada and Benin, migrant FSWs [25,29] had limited access to healthcare because of language barriers, which led to low HIV testing rates.

MACRO LEVEL
HIV testing policies: mandatory testing, forced testing, non-anonymous testing, lack of confidentiality, guarantee retention to treatment Health care funding: health care entitlements, free ART, formal and informal payments. Criminalization: criminalization of sex work/drug use.

MESO LEVEL
Sex work venue: level of income generated by sex work venues, indoors/outdoors. Social network: support and attitude of peers, sex work managers, family. Stigma and discrimination: fear of being identified as HIV+, fear of imprisonment if testing HIV+, fear to disclose history of sex work/drug use, discrimination from health care providers, discrimination from family members, self-stigmatization, negative perceptions about the quality of health care. Costs (transport and time): time constraints, density of HIV testing sites, travel costs to collect results.

MICRO LEVEL
Socio-demographic characteristics: education, age, income level, family status, migration status. Risk behaviors: type and number of sexual partners, condom use, age at sex work initiation and period of engagement in sex work, drug and alcohol use.

Risk Behaviors
Seven studies reported nearly inconsistent patterns on how regular condom use influenced HIV testing. Using condoms during every instance of each sexual intercourse both facilitated and impeded testing depending on the type of sexual partner [19,20,25,31,33,39,41]. Three articles reported that inconsistent condom use with a client -facilitated testing [25,31,33], but using condoms inconsistently with a husband or lover was negatively associated with testing [33].
In China, a quantitative study identified that condom use was associated with HIV testing [20], although in a previous qualitative study the same author found that FSWs who used condoms consistently felt to be sufficiently protected from HIV and not in need of testing [41]. In Iran, consistent condom use during each sexual intercourse was associated with recent testing [39]. Initiation of sex work at an older age [18,20,33,35,45] and engaging in sex work for a longer period of time [18,20,33,45] facilitated HIV testing. In Uzbekistan, FSWs who started sex work before the age of 18 were less likely to test [32], and in Canada older age of sex work initiation was positively associated with recent testing [25]. FSWs who engaged in sex work for a longer time had a higher uptake of testing [18,20,33,45] and willingness to test [19]. FSWs employed for shorter periods [27,32] were less likely to test.
Having a lower number of clients/sexual partners was associated with HIV testing in China [23], but was reported to decrease testing in Vietnam [30], Iran [39] and Uzbekistan [32].

Sex Work Venue
Of the six articles that addressed sex work venues [18,25,31,41,45,50], most reported that working indoors and at high-income venues generating higher income impelled HIV testing. Working in a high-income venue and out of the street predicted testing in China, Vietnam and India [18,31,50]. However, in Canada, FSWs working indoors were less likely to have recently tested for HIV than those working outdoors [25].

Social Support
About half of the articles reviewed assessed how FSWs' social interactions influenced their decision to test for HIV [18-20, 24, 26, 29, 34, 38, 40, 41, 43, 45, 47-51]. Positive attitudes and support from peers, family and partners facilitated HIV testing [19,20,24,26,29,34,40,41,45,[48][49][50][51]. In China, women were more likely to test if accompanied by peers [19,20]. In Russia, family support was an important condition for accessing healthcare, including HIV testing, as women could rely on their family financially and emotionally [24]. Participation in self-support groups in India [18] and Uganda [51] and receiving condoms from HIV prevention programs in China [38] facilitated testing. Positive views of FSWs' employers towards HIV testing [41,45] or requiring the test [43,50] increased the uptake. However, in China and Ethiopia, employers expressed concerns towards HIV testing and how it could impact the sex work business [41,47]. In Guinea, HIV testing was forbidden by some managers [26]. In Zambia and Russia, fear of negative reaction of their sexual partner if diagnosed HIV-positive, prevented women from engaging in HIV testing [34,49].
In Benin, healthcare workers reported that women did not like to be recognized as FSWs, and that this could prevent them from seeking healthcare [29]. In several African countries, health providers discriminated against sex workers and their family members [52]. In Russia, FSWs were concerned that they would be treated badly or denied healthcare if identified as sex workers or drug users [46]. In China, FSWs worried about meeting an acquaintance at the testing site and being recognized as HIV+ [41], while in Vietnam, they feared imprisonment if diagnosed with HIV [50]. Selfstigma resulting from widespread negative views of HIV+ people and sex work decreased testing across several African countries [52]. Thirteen articles reported that anticipated stigma and discrimination at health facilities hampered service utilization [19,20,24,26,29,37,41,46,[48][49][50][51][52]. In Russia, Vietnam, Uganda and several African countries, private hospitals were defined by FSWs as more friendly and of higher quality than public health facilities, and were reported to be preferable places to get healthcare services, including HIV testing [24,[50][51][52].
In China [41], Vietnam [50], India [48], Uganda [51], Zambia [49], Ethiopia [47] and Russia [46], lack of confidentiality was reported as a major barrier to HIV testing. Unwillingness to be included in official registers of HIV+ people decreased access to testing in China [41] and Russia [24]. In Russia, FSWs without a residence permit or passport are not entitled to accessing healthcare. Free-of-charge HIV testing is available only upon giving up anonymity, and if a woman utilizes state-sponsored HIV testing at a local clinic, the results are officially recorded into her personal medical records [24]. In India and Ethiopia, to access HIV and AIDS treatment, women are required to show an identity card [47,48]. In Uganda, all women diagnosed HIV positive were given two papers indicating test result and further referrals while all diagnosed HIV negative were given one paper with test result only [51].
FSWs were forced to test against their will or were tested surreptitiously without consent in Kampala (Uganda), Hillbrow and Limpopo (South Africa) [52] and during police detainment in Uzbekistan [32] and Macedonia [53]. In Vietnam, among the FSWs who tested for HIV, only 54% did it voluntarily [33]. FSWs who had spent time in rehabilitation or detention centers [24,30,50] or had ever been pregnant [24,50] were more likely to have undergone HIV testing. In Victoria, Australia, screening of sex workers is mandatory despite its lack of cost-effectiveness [21].
These studies suggest that HIV testing might increase if FSWs can easily access testing sites and receive support from peers, friends and healthcare workers along with educational activities [19,20,45,[50][51][52].

Discussion
This systematic review of barriers and facilitators to HIV testing amongst FSWs found that the two barriers to HIV testing most commonly reported are (1) costs, including transportation, formal/informal payments, and time, and (2) stigma, including fear of involuntary disclosure of HIV status/history of sex work, negative attitudes of healthcare workers, and discriminatory policies. Social support facilitated HIV testing, with consistently higher uptake amongst married FSWs, and those encouraged to test by peers, healthcare workers or employers.
The majority of the studies reviewed were conducted in low and middle-income countries with only three studies identified in high-income settings. Only one study evaluated the cost-effectiveness of HIV testing amongst FSWs. Most studies addressed micro, or micro and meso levels of the SEM with predominance of micro-level factors. Thirteen studies analyzed concurrently the macro, meso and micro levels. Our findings support previous calls to develop HIV testing strategies that fully account for structural factors [55,56] and highlight the need for a more nuanced investigation of how micro-, meso-and macro-level factors intersect to influence HIV testing uptake.
Few studies assessed frequencies of collecting test results or compared them with testing frequencies. The outcome most frequently assessed was "ever in life" testing although this outcome measure fails to capture the frequency of HIV testing. Furthermore, the highest percentage of recently tested FSWs was reported by a Canadian study and constituted 76.1%, an outcome too low to meet either WHO recommendations [3,57] or the "90-90-90" target [1], which highlights necessity to increase efforts to promote HIV testing amongst FSWs. Taken together, our results suggest addressing simultaneously several outcome measures when assessing HIV testing programs among female sex workers, including accessibility of testing, willingness to be tested, regularity and collecting test results.
In line with previous studies of HIV testing behavior of different populations [14,58,59], we found that scarcity of financial resources, low perceived risk and poor HIV knowledge were barriers to HIV testing for FSWs. Similar to the results reported for female migrants [58], we observed an association between having children and HIV testing uptake. This might be manifestation of women's and particularly pregnant women's greater exposure to HIV testing, as an offer of HIV testing became generally the norm in reproductive and antenatal care settings [3,60]. On the other hand, several papers reviewed suggested that women in permanent relationships and with children might have higher motivation to stay healthy and thus, might seek out testing themselves. For example, in Vietnam, FSWs in permanent relationships were more likely to be tested in the year 2000 before HIV testing became widely implemented as a part of national antenatal health care program across the country [61]. Overall, social support from family, peers, sex work managers and healthcare workers are instrumental for promoting HIV testing uptake among FSWs, yet the same sources might contribute to further stigma and discrimination.
We did not find any consistent associations between age of participants [58] or their educational level [58,59] and HIV testing, but working in the sex industry for a longer period and starting sex work at older ages were associated with higher HIV testing uptake. These findings suggest that the willingness to test for HIV might increase with time and relate closely with HIV risk awareness.
The inconsistency of results on how condom use and number of clients influenced testing might be explained by FSWs' engagement in different types of concurrent sexual partnerships. While using condoms with commercial clients might be perceived as prevailing acceptable behavior [62], the decision to use a condom in cohabiting relationships or with a husband might be influenced by interpersonal factors related to partnership intimacy (e.g., trust, emotional closeness, power or reproductive desires) [63]. Moreover, there is a need to account not only for the type of partnerships, but also for their duration. Consistency of condom use might decrease with longer duration of relationships with non-paying partners [63], but may increase with commercial permanent partners [64]. The relationship intimacy may be at play in the HIV testing decision-making process among FSWs and for consistent condom use. Testing behavior might be influenced by increased trust, emotional closeness and familiarity. A more nuanced understanding of how HIV testing behavior is influenced by risky sexual behaviors in different types of partnerships and how it changes over time is needed. In turn, relationship power might be an important modifiable factor, which might be considered when developing HIV testing interventions for FSWs.
The inconsistencies between results in relation to sexual/ drug use behavior and HIV testing might be due to differences in targets of HIV testing approaches across countries. For example, in Canada efforts were concentrated on reaching street-based sex workers and those injecting drugs, leaving out those working indoors, in more high-income venues. Nevertheless, at that time sex work was fully decriminalized in Canada [65]. In contrast, in Uzbekistan and Russia HIV testing might be less accessible for sex workers and drug users because of punitive laws. In these countries, HIV testing is provided solely through government-affiliated settings, including so-called "friendly cabinets" and thus, sex workers and drug users might avoid state clinics or at least avoid disclosing who they are, as they might be stigmatized by healthcare providers or even arrested. Our results demonstrate how laws might diminish promising health-promoting interventions in some countries while in others, supporting policies and concentrated efforts might lead to the successful enrolment of most vulnerable populations.
Furthermore, factors, such as violations of human rights when forcing FSWs to test, lack of confidentiality and anonymity, discriminatory attitudes of healthcare workers, fear of testing HIV+ and being identified as a sex worker and/or a drug user, are manifestations of prevailing stigma. Unfortunately, there are still cases where the violation of basic human rights is "justified" and sex workers are perceived as victims and objects of pity, who should be helped when applying mandatory or forced testing. Our findings highlight the importance to tackle overlapping stigma and discrimination across all three levels of SEM in order to promote HIV testing among sex workers [66]. This is in line with the WHO's call to enforce the 5 Cs principles and to institutionalize policies preventing discrimination and promoting tolerance towards sex workers and people living with HIV [61,67]. As reported before, introduction of discriminative laws and policies criminalizing sex work and/or HIV transmission may fuel stigma [65,[68][69][70].
This review has several limitations. It is restricted to studies published in English, but only three pre-selected studies were excluded for this reason, so the impact upon the findings is likely to be minimal. We included studies published during the last 17 years to account for recent HIV testing approaches. It is unlikely that the content of previously published articles would have substantially altered our findings, as rapid HIV testing started in the early 2000s. We excluded eight citations with neither abstract, nor title available. We acknowledge that our findings are based on the topics presented by the selected studies, and thus, are restricted by the reported information. Despite the limitations mentioned above, this study provides a broad overview of the different aspects of HIV testing across the global SEM, provides important insights on how HIV testing uptake could be promoted among FSWs, and suggests avenues for further research.

Conclusion
The consistent finding that social support facilitated HIV testing calls for the inclusion of meso-level factors into current HIV testing strategies directed at FSW. Studies on the role of macro-level factors and their intersections with the meso and micro levels are needed to inform interventions that facilitate HIV testing uptake amongst FSWs.

Annex 3: Quality Assessment
The quality of the qualitative papers (Table 1) was assessed using the guide for critically appraising qualitative research [15].The checklist consisted of 18 items assessing findings, design, sample, data collection, analysis, reporting, reflexivity and neutrality, ethics and auditability. As in previous research [66] we used a midpoint score of 9 as a cut off between low-and high-quality studies.
We assessed the quality of the quantitative and mixedmethods papers using the modified Downs and Black checklist [16]. The 26 questions of the checklist represented items of reporting, external and internal validity, and power. As the majority of studies did not report power calculations of the sample size and none was single or double blinded, we excluded the power (#27) and the blinding (#13, 14) questions. Thus, the modified checklist consisted of 24 questions with a maximum score of 25 points). A midpoint score of 12.5 was considered to distinguish the high-quality studies ( Table 2). Case report n/a Specify study characteristics (e.g., PICOS, length of follow-up) and report characteristics (e.g., years considered, language, publication status) used as criteria for eligibility, giving rationale.

Yes
Information sources 7 Describe all information sources (e.g., databases with dates of coverage, contact with study authors to identify additional studies) in the search and date last searched.

Yes
Search 8 Present full electronic search strategy for at least one database, including any limits used, such that it could be repeated.
Yes ("Annex 1: Search strategy") Study selection 9 State the process for selecting studies (i.e., screening, eligibility, included in systematic review, and, if applicable, included in the meta-analysis).
Yes (Fig. 1) Data collection process 10 Describe method of data extraction from reports (e.g., piloted forms, independently, in duplicate) and any processes for obtaining and confirming data from investigators.

Data items 11
List and define all variables for which data were sought (e.g., PICOS, funding sources) and any assumptions and simplifications made.

12
Describe methods used for assessing risk of bias of individual studies (including specification of whether this was done at the study or outcome level), and how this information is to be used in any data synthesis.

Not available
Summary measures 13 State the principal summary measures (e.g., risk ratio, difference in means). Yes Synthesis of results 14 Describe the methods of handling data and combining results of studies, if done, including measures of consistency (e.g., I 2 ) for each meta-analysis.

Not applicable
Risk of bias across studies 15 Specify any assessment of risk of bias that may affect the cumulative evidence (e.g., publication bias, selective reporting within studies).

Yes
Additional analyses 16 Describe methods of additional analyses (e.g., sensitivity or subgroup analyses, meta-regression), if done, indicating which were pre-specified.

Study selection 17
Give numbers of studies screened, assessed for eligibility, and included in the review, with reasons for exclusions at each stage, ideally with a flow diagram.
Yes (Fig. 1) Study characteristics 18 For each study, present characteristics for which data were extracted (e.g., study size, PICOS, follow-up period) and provide the citations.
Yes (Table 1) Risk of bias within studies 19 Present data on risk of bias of each study and, if available, any outcome level assessment (see item 12).

Not available
Results of individual studies 20 For all outcomes considered (benefits or harms), present, for each study: (a) simple summary data for each intervention group (b) effect estimates and confidence intervals, ideally with a forest plot.

Not applicable
Synthesis of results 21 Present results of each meta-analysis done, including confidence intervals and measures of consistency.

Not applicable
Not available Discussion Summary of evidence 24 Summarize the main findings including the strength of evidence for each main outcome; consider their relevance to key groups (e.g., healthcare providers, users, and policy makers).
Yes (Table 1) Limitations 25 Discuss limitations at study and outcome level (e.g., risk of bias), and at review-level (e.g., incomplete retrieval of identified research, reporting bias).

Conclusions 26
Provide a general interpretation of the results in the context of other evidence, and implications for future research.

Yes
Funding Funding 27 Describe sources of funding for the systematic review and other support (e.g., supply of data); role of funders for the systematic review.

Not available
Moher et al. [71]. For more information, visit: www.prism a-state ment.org.