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. 2020 Dec 21;15(12):e0244357. doi: 10.1371/journal.pone.0244357

Risk factors of HIV infection among female entertainment workers in Cambodia: Findings of a national survey

Sovannary Tuot 1, Alvin Kuo Jing Teo 2, Pheak Chhoun 1, Phalkun Mun 3, Kiesha Prem 2,4, Siyan Yi 1,2,5,*
Editor: Petros Isaakidis6
PMCID: PMC7751854  PMID: 33347494

Abstract

Background

Cambodia has been well recognized for its success in the fight against the HIV epidemic. However, challenges remain in eliminating HIV infections in key populations, including women working in entertainment establishments, such as massage parlors, karaoke bars, or beer gardens. This study explored the prevalence of HIV and identified factors associated with HIV infection among female entertainment workers (FEWs) in Cambodia.

Methods

This national biological and behavioral survey was conducted in 2016 in Phnom Penh and 17 provinces. We used a two-stage cluster sampling method to recruit FEWs for HIV testing performed on-site and face-to-face interviews using a structured questionnaire. We investigated factors associated with HIV infection using multiple logistic regression.

Results

This study included 3149 FEWs with a mean age of 26.2 years (SD 5.7). The adjusted prevalence of HIV was 3.2% (95% CI 1.76–5.75). In the multiple logistic regression model, the odds of HIV infection were significantly higher among FEWs in the age group of 31 to 35 (AOR 2.72, 95% CI 1.36–8.25) and 36 or older (AOR 3.62, 95% CI 1.89–10.55); FEWs who were not married but living with a sexual partner (AOR 3.00, 95% CI 1.16–7.79); FEWs who had at least ten years of formal education (AOR 0.32, 95% CI 0.17–0.83); FEWs who reported having abnormal vaginal discharge (AOR 3.51, 95% CI 1.12–9.01), genital ulcers or sores (AOR 2.06, 95% CI 1.09–3.17), and genital warts (AOR 2.89, 95% CI 1.44–6.33) in the past three months; and FEWs who reported using illicit drugs (AOR 3.28, 95% CI 1.20–4.27) than their respective reference group. The odds of HIV infection were significantly lower among FEWs working in karaoke bars (AOR 0.26, 95% CI 0.14–0.50) and beer gardens (AOR 0.17, 95% CI 0.09–0.54) than among freelance FEWs.

Conclusions

The prevalence of HIV among FEWs in Cambodia remains much higher than that in the general population. These findings indicate that differentiated strategies to address HIV and other sexually transmitted infections should be geared towards FEWs working as freelancers or in veiled entertainment venues such as massage parlors and freelance sex workers. Prevention efforts among venue-based FEWs should be sustained.

Introduction

The national response to the human immunodeficiency virus (HIV) in Cambodia has been described as tri-phasic [1]. In the first phase (1991–2000), Cambodia faced one of the fastest-growing HIV epidemics in Asia; and in 1998, the HIV prevalence peaked at 1.7% among the general adult population aged 15 to 49 [2, 3]. The second phase (2001 to 2010) was characterized by combined efforts related to treatment, decentralization of services, and enhanced focus on key populations [4]. As a result of these strategies, the epidemic was significantly controlled. In recognition of the national success in controlling the HIV epidemic, Cambodia was feted with the United Nations' Millennium Development Goal award in 2010 [5, 6]. The current third phase (2011–2020) aims to achieve three-zero targets: (1) zero new HIV infection, (2) zero AIDS-related death, and (3) zero AIDS-related discrimination in communities [4]. Initial evidence suggests that the HIV epidemic is on a downward trajectory, and the HIV prevalence in the general adult population aged 15 to 49 declined to 0.6% in 2016 [7]. Due to the expanded access to antiretroviral therapy (ART), annual AIDS-related deaths have been reduced by two-thirds over the past ten years [1, 8].

Despite these tremendous successes, Cambodia has faced significant challenges in controlling the HIV epidemic in key populations, including female entertainment workers (FEWs). In Cambodia, FEWs refer to women working in entertainment establishments such as karaoke bars, massage parlors, or beer gardens. FEWs working in these establishments may or may not be involved in transactional sex. The FEW population also includes freelance sex workers who solicit clients in public places, such as streets or parks, or on calls. In 2008, the Cambodian government enacted a new Law to Suppress Human Trafficking and Sexual Exploitation [9], which has made health interventions in sites used for transactional sex more difficult. Due to the closure of many brothels, sex work has moved to entertainment-based venues or other informal and hidden settings like streets and parks. The distinction between direct and indirect sex work has become obscured, and an increase in indirect transactional relationships, such as sweethearts, have been documented [10]. In the Cambodian context, “sweethearts” refer to romantic non-commercial sexual relationships. For FEWs, a sweetheart is typically a boyfriend or regular client in the form of indirect transactional sex through living support, dinner dates, gifts, or shopping trips. Such relationships usually involve a lack of condom use as displays of trust and intimacy [11].

Among FEWs, the HIV prevalence is exceptionally high in sub-groups such as brothel-based (17.4%) and street-based (37.3%) sex workers than among women working in other entertainment establishments (9.8%) [7]. Couture et al. conducted a prospective study of young FEWs in the capital city of Phnom Penh and found that the HIV incidence among the FEWs was 3.6 per 100 person-years (95% confidence interval [CI], 1.2%–11.1%) [12]. The identified risk factors of the HIV infection in the study included being freelance sex workers and younger age of first sex (≤15 years). Our recent study found that almost half of the FEW participants had not tested for HIV in the past six months preceding the survey [11]. Sexually transmitted infections (STIs), substance use, mental health problems, and gender-based violence were also commonly reported among FEWs in Cambodia [12–20], while the rates of consistent condom use remain consistently low [11, 21]. These conditions and behaviors have been reported as risk factors of HIV infection and HIV risk behaviors among this key population [12–17].

Collectively, these empirical data suggest that FEWs in Cambodia remain at disproportionally high risk of HIV infection. Due to the significant changes in the sex and entertainment industry landscapes, the information on the burden of HIV infection and its related risk factors needs to be closely followed up. The strategic information with up-to-date data on the HIV epidemic and programmatic response is crucial to Cambodia, particularly in the wake of the shrinking international HIV funding. The reduced funding is due to the country’s status change from a low-income to a lower-middle-income country in 2016 [22]. More strategic decisions need to be made to adapt to the limited resources to achieve the ambitious global targets of ending the HIV epidemic by 2030. Therefore, we conducted this study to explore the HIV prevalence and identify risk factors associated with HIV infection among FEWs in Cambodia.

Materials and methods

Study sites and participants

This National Integrated Biological and Behavioral Survey among FEWs (FEW-IBBS) was conducted in 2016 in Phnom Penh and 17 other provinces purposively selected out of the 25 provinces in Cambodia. The FEW population size in the selected provinces represented more than 90% of the total FEWs in Cambodia in 2015 [7, 23]. The survey included women who were (1) working in the entertainment establishments or as freelance sex workers; (2) aged at least 18 years; (3) sexually active, defined as having had vaginal or anal sexual intercourse with at least one man in the past 12 months; (4) able to communicate in Khmer; (5) able and willing to provide written informed consent; and (6) willing to be physically present at the study site for an interview and HIV testing.

Sample size calculation

We used the Open Epi calculator version 3.02 [24] to calculate the sample size required to estimate the HIV prevalence. In 2016, the estimated total number of FEWs in Cambodia was 40215, working in 2571 entertainment establishments, including 896 freelance FEWs [3, 7]. Using the HIV prevalence of 3.1% in the most recent national survey [23], a design effect of 1.5, 10% refusal rate, and a 95% confidence level, the minimum sample size required for the survey was 3100 FEWs.

Sampling procedures

Venue-based FEWs were sampled using a multi-stage cluster sampling design. First, we listed all the entertainment establishments clusters (karaoke bars, massage parlors, beer gardens, and beer companies) in the selected areas and the estimated number of FEWs in each cluster. Next, we assigned a number to each cluster. We used a random number calculator to randomly select a cluster from the list. Subsequently, we invited all the FEWs in the selected clusters to partake in the study. We repeated the random cluster selection until the target sample size was attained.

We used a time-location sampling method to recruit freelance FEWs. We established a sampling frame comprised of all known hotspots where freelance FEWs were known to assemble using information obtained from non-governmental organizations (NGOs) working with this population in the different localities. Before data collection, the study team worked closely with the respective NGOs to conduct a feasibility assessment and updated the sampling frame accordingly. We randomly selected the locations, date, and time (in four-hour time periods) for participant recruitment. We anticipated that the number of hotspots in each province would be small. Therefore, we included all hotspots and invited all FEWs found at the hotspots to participate in the study.

Data collection training

In this national survey, we involved representatives of key stakeholders, including FEW communities, in every stage of the survey, from study design to questionnaire development and validation, data collection, and finding dissemination. Pre-data-collection workshops and training were conducted with data collection teams and representatives of HIV key stakeholders, NGOs working with FEWs, and FEW communities. Data collection teams were composed of team leaders from the Surveillance Unit of the National Center for HIV/AIDS, Dermatology and STD, staff members of the respective provincial health department, and representatives of NGOs, community outreach workers, and FEW communities. The training covered: (1) sampling methods, including mapping and eligibility criteria, (2) informed consent procedures, (3) participants’ privacy and confidentiality, (4) study protocol and interview techniques, (5) blood specimen collection, and (6) record-keeping and completion of the survey forms. We also pretested the questionnaire during the training.

Questionnaire development

We developed a structured questionnaire for face-to-face interviews, which took approximately 30 minutes to complete. Standardized and validated tools were adapted from previous studies among HIV key populations in Cambodia [18–20, 25, 26]. The structured questionnaire was initially developed in English and then translated into Khmer, Cambodia’s national language. It was then back-translated into English by another translator to ensure that the original items’ “content and spirit” were maintained. A consultative meeting was held with representatives of key stakeholders working on HIV and harm reduction programs, including NGOs and FEW communities, to review the study protocol and tools. A pilot study was conducted with 20 FEWs in Phnom Penh, later excluded from the main study.

Variables and measurements

Socio-demographic characteristics included age (continuous), urbanicity of study sites, marital status, years of formal education attained (continuous), and type of entertainment venue for which the woman was working. We also collected information on living duration in the current city (continuous) and working duration in the current entertainment venue (continuous).

For HIV risks, we collected information regarding the participant’s HIV status and sexual behaviors with commercial partners, defined as having sexual intercourse in exchange for money or gifts, and non-commercial partners. These included the number of sexual partners (continuous), condom use frequency (always, frequently, sometimes, never), STI diagnosis, and experiences of STI symptoms (yes or no) in the past three months. We also collected information on illicit drug use (heroin, marijuana, amphetamine-type stimulants, or other types of drugs) and alcoholic drinks at work (yes or no) in the past three months. For participants who reported living with HIV, we collected self-reported HIV care and treatment information, including ART.

All participants received HIV testing regardless of whether they already knew their HIV-status. A blood sample was obtained from each participant by a trained laboratory technician through finger-prick and tested for HIV antibodies using the HIV-1/2 Determine™ test, following the national protocol [27]. We confirmed the test results by the HIV 1/2 STAT-PAK™ test on-site. If a specimen was reactive by the HIV-1/2 Determine™ test but non-reactive by the HIV 1/2 STAT-PAK™ test, the participant was recommended to go for a confirmatory test at an ART clinic of their choice with support from a community outreach worker. HIV test result was provided to the participants verbally after the interview, together with post-test counseling. All participants attended a pre- and post-test counseling session provided by trained counselors from HIV confidential counseling and testing centers located in the study sites. Those tested positive for HIV were referred to an ART clinic of their choice by a local NGO working in the respective area for care and treatment services according to the national guidelines. All participants received a token of appreciation valued at approximately US$4 for their time and effort.

Statistical analyses

Sampling weights that corrected for non-response and sample design were applied. Standard errors were adjusted for clustering at the venue level [28]. We calculated the HIV prevalence by dividing the number of HIV-positive participants by the total number of participants tested. In bivariate analyses, we used the Chi-squared test (or Fisher’s exact test when a cell count was smaller than five) for categorical variables and Student’s t-test for continuous variables. A multiple logistic regression model was built to identify risk factors associated with HIV infection. We transformed the age and education level into categorical variables. We included age, education level, marital status, types of entertainment establishments, and other variables significantly associated with HIV infection in bivariate analyses (p<0.05) simultaneously in the model. We then removed variables not statistically significant from the model using a backward stepwise selection method. We reported adjusted odds ratios (AOR) with its associated 95% CI and p-values. Statistical analyses were conducted using STATA version 12.0 (Stata Corp, Texas, United States).

Ethical considerations

The National Ethics Committee for Health Research, Ministry of Health, Cambodia approved the study (Ref no: 297NECHR). The data collection team explained to the participants about the study and obtained their written consent. Participation in the study was voluntary, and participants could refuse to respond to any questions or discontinue their participation at any time. We also extended free HIV testing to eligible individuals who refused to participate in this study if they wanted. We maintained the confidentiality of the participants by using unique codes, and no personal identifiers were recorded.

Results

HIV prevalence and socio-demographic characteristics

Of 3353 FEWs invited, 148 (4.4%) refused to participate in the study, primarily due to their time constraints. Fifty-six participants (1.8%) with missing data of main variables or HIV testing results were further excluded from the analyses. In total, we included 3149 FEWs in the analyses. The mean age of the participants was 26.2 years (SD 5.7). The adjusted HIV prevalence among FEWs in this study was 3.2%. The prevalence was 11.1% among freelance FEWs (11.1%) and 4.3% among FEWs working in massage parlors. Of those who knew their HIV-positive status (n = 29), 86.2% were on ART. As shown in Table 1, most of the participants were aged 30 or younger, and 38.6% were divorced or widowed. The participants' education level was generally low, with 60.1% having attained six years or less of formal education. More than two-thirds (70.6%) worked in karaoke bars, and 43.9% reported having worked in the current venue for more than one year. HIV infection was significantly associated with age groups, marital status, formal education level, entertainment venue type, and working duration in the current entertainment venue.

Table 1. Socio-demographic characteristics of HIV-positive and HIV-negative FEWs (n = 3149).

Variables Total HIV-negative HIV-positive P-value*
Age groups <0.001
< 21 584 (18.5) 581 (18.9) 3 (4.2)
21–25 1004 (31.9) 994 (32.3) 10 (13.9)
26–30 905 (28.7) 894 (29.1) 11 (15.3)
31–35 455 (14.4) 423 (13.7) 32 (44.4)
≥ 36 201 (6.4) 185 (6.0) 16 (22.2)
Current marital status <0.001
Never married 1072 (34.0) 1061 (34.5) 11 (15.3)
Married, living together 548 (17.4) 540 (17.5) 8 (11.1)
Married, not living together 113 (3.6) 109 (3.5) 4 (5.6)
Divorced/widowed 1215 (38.6) 1180 (38.3) 35 (48.6)
Not married, living with a partner 201 (6.4) 187 (6.1) 14 (19.4)
Level of formal education attained <0.001
≤ 6 1894 (60.1) 1834 (59.6) 60 (83.3)
7–9 958 (30.4) 948 (30.8) 10 (13.9)
≥ 10 years 297 (9.4) 295 (9.6) 2 (2.8)
Type of entertainment venues <0.001
Massage parlors 93 (3.0) 89 (2.9) 4 (5.6)
Freelance sex workers 351 (11.1) 312 (10.1) 39 (54.2)
Beer companies 101 (3.2) 99 (3.2) 2 (2.8)
Karaoke bars 2223 (70.6) 2197 (71.4) 26 (36.1)
Beer gardens 381 (12.1) 380 (12.3) 1 (1.4)
Duration of working for the current entertainment venue ≥ 12 months 1380 (43.9) 1336 (43.4) 44 (61.1) 0.003
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Abbreviations: FEW, female entertainment workers; HIV, human immunodeficiency virus.

*Chi-square test (or Fisher's exact test when a cell count was smaller than 5) was used.

HIV risk behaviors

Table 2 shows that 24.9% of women reported always using condoms with non-commercial partners in the past three months. Of the 1396 (53.0%) women who reported having sexual intercourse in exchange for money or gifts in the past 12 months, 19.5% reported having two or more commercial partners on the last working day, and 80.5% reported always using condoms with this type of partners in the past three months. Regarding substance use, 7.7% reported using illicit drugs in the past three months, with amphetamine-type stimulants being the most commonly used drugs. About two-thirds (62.6%) reported drinking alcohol at work every day, and 80.8% reported having five or more alcoholic drinks on their last working day. About one in five (20.2%) reported having been diagnosed with an STI in the past three months. The most common facilities where the participants received the STI diagnosis were public health facilities (55.4%) and NGOs’ clinics (34.7%). The participants also reported different forms of STI symptoms experienced in the past three months, including abnormal vaginal discharge (33.9%), lower abdominal pain (25.8%), ulcers or sores in genital areas (2.5%), and genital warts (1.3%). HIV infection was significantly associated with consistent condom use levels with non-commercial partners, involvement in transactional sex, the number of commercial sex partners, and forced sex and gang-rape experience. HIV infection was also significantly associated with STI diagnosis and symptoms and substance use, including illicit drug use, alcohol use, and binge drinking.

Table 2. HIV risks among HIV-positive and HIV-negative FEWs in the study (n = 3149).

Sexual behaviors and STI symptoms Total HIV-negative HIV-positive P-value*
Condom use with non-commercial partners in the past 3 months (n = 1473) <0.001
Always 367 (24.9) 349 (24.2) 18 (56.3)
Frequently 67 (4.5) 66 (4.6) 1 (3.1)
Sometimes 245 (16.7) 241 (16.7) 4 (12.5)
Never 794 (53.9) 785 (54.5) 9 (28.1)
Had sex in exchange for money or gifts in the past 12 months 1396 (53.0) 1343 (52.3) 53 (77.9) <0.001
Had ≥2 commercial sex partners on last working day (n = 1396) 272 (19.5) 254 (18.9) 18 (34.0) 0.007
Condom use with commercial sexual partners in the last 3 month (n = 1292) 0.12
Always 1040 (80.5) 996 (80.3) 44 (86.3)
Frequently 95 (7.4) 93 (7.5) 2 (3.9)
Sometimes 113 (8.7) 109 (8.8) 4 (7.8)
Never 44 (3.4) 43 (3.5) 1 (2.0)
Forced sex in the past 3 months 42 (1.4) 36 (1.2) 6 (8.3) <0.001
Gang rape in the past 3 months 40 (1.3) 35 (1.1) 5 (6.9) <0.001
Illicit drug use in the past 3 months 242 (7.7) 216 (7.0) 26 (36.1) <0.001
ATS use 205 (86.1) 181 (85.4) 24 (92.3) 0.55
Injecting drug use 19 (8.1) 16 (7.7) 3 (11.5) 0.45
Drinking alcohol at work every day 1970 (62.6) 1941 (63.1) 29 (40.3) <0.001
Having ≥5 alcoholic drinks on the last working day 2545 (80.8) 2500 (81.2) 45 (62.5) <0.001
Having been diagnosed with an STI in the past 3 months 635 (20.2) 613 (19.9) 22 (30.6) 0.03
STI symptoms in the past 3 months
Abnormal vaginal discharge 1066 (33.9) 1033 (33.6) 33 (45.8) 0.03
Lower abdominal pain 814 (25.8) 785 (25.5) 29 (40.3) 0.005
Genital ulcers or sores 78 (2.5) 72 (2.3) 6 (8.3) 0.001
Genital warts 42 (1.3) 38 (1.2) 4 (5.6) 0.02
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Abbreviations: ATS, amphetamine-type stimulants; FEW, female entertainment workers; HIV, human immunodeficiency virus; IBBS, integrated biological and behavioral survey.

*Chi-square test (or Fisher's exact test when a cell count was smaller than 5) was used.

Risk factors of HIV infection

Table 3 shows the results of the multiple logistic regression analysis. After controlling for other covariates, the odds of HIV infection were significantly higher among FEWs in the age group of 31 to 35 (AOR 2.72, 95% CI 1.36–8.25) and 36 or older (AOR 3.62, 95% CI 1.89–10.55) than those in the age group of <21 years. The odds of HIV infection were significantly higher among FEWs who were not married but living with a partner than those who were never married and not living with a partner (AOR 3.00, 95% CI 1.16–7.79). The odds of HIV infection were significantly lower among FEWs who had attained at least ten years of formal education than those attaining ≤six years of formal education (AOR 0.32, 95% CI 0.17–0.83). Compared to freelance FEWs, the odds of HIV infection were significantly lower among FEWs working at karaoke bars (AOR 0.26, 95% CI 0.14–0.50) and beer gardens (AOR 0.17, 95% CI 0.09–0.54). The odds of HIV infection were significantly higher among FEWs who reported having abnormal vaginal discharge (AOR 3.51, 95% CI 1.12–9.01), genital ulcers or sores (AOR 2.06, 95% CI 1.09–3.17), and genital warts (AOR 2.89, 95% CI 1.44–6.33) in the past three months than those who did not. The odds of HIV infection were also significantly higher among FEWs who reported using illicit drugs (AOR 3.28, 95% CI 1.20–4.27) than those who did not.

Table 3. Factors associated with HIV infection among female entertainment workers (n = 3149).

Variables in the final model AOR (95% CI) P-value*
Age group
< 21 Reference
21–25 1.62 (0.43–5.20) 0.48
26–30 1.81 (0.47–4.05) 0.39
31–35 2.72 (1.36–8.25) 0.001
≥ 36 3.62 (1.89–10.55) 0.004
Current marital status
Never married, not living with a partner Reference
Not married, living with a partner 3.00 (1.16–7.79) 0.02
Married, living together 0.56 (0.20–1.53) 0.25
Married, not living together 2.17 (0.62–7.63) 0.23
Divorced/widowed 1.24 (0.56–2.74) 0.60
Level of formal education attained
≤ 6 Reference
7–9 0.74 (0.36–1.52) 0.41
≥10 years 0.32 (0.17–0.83) 0.02
Type of entertainment venues
Freelance sex workers Reference
Massage parlors 0.91 (0.28–2.92) 0.87
Beer companies 0.34 (0.07–1.60) 0.17
Karaoke bars 0.26 (0.14–0.50) <0.001
Beer gardens 0.17 (0.09–0.54) 0.01
Illicit drug use in the past 3 months
No Reference
Yes 3.28 (1.20–4.27) 0.002
Had abnormal vaginal discharge in the past 3 months
No Reference
Yes 3.51 (1.12–9.01) 0.01
Had genital ulcer or sores in the past 3 months
No Reference
Yes 2.06 (1.09–3.17) 0.02
Had genital warts in the past 3 months
No Reference
Yes 2.89 (1.44–6.33) 0.006
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Abbreviations: AOR, adjusted odds ratio; CI, confidence interval; FEW, female entertainment workers; HIV, human immunodeficiency virus.

*Age, marital status, education level, entertainment venue, and variables associated with HIV infection in the bivariate analyses at a level of p<0.05 were simultaneously included in the model.

Discussion

We found that the HIV prevalence among FEWs in this national survey was 3.2%, about six times higher than the estimated 0.6% prevalence among the Cambodian general population [4] and 0.3% among Cambodian pregnant women attending antenatal care in the same year [7]. This study also identified several risk factors associated with HIV infection among FEWs in this national survey. Our results showed that the risk of HIV infection increased significantly with age and was associated with the nature of entertainment venues where FEWs were working. The prevalence was also significantly higher among FEWs with histories of illicit drug use and STI diagnosis and symptoms such as genital warts, genital ulcers or sores, and abnormal vaginal discharge. The risk of HIV infection was inversely associated with years of formal education attained.

We found that the HIV prevalence was exceptionally high among specific subgroups of FEWs, such as freelance FEWs (11.1%) and FEWs working in massage parlors (4.3%). Past surveys have also indicated a high HIV prevalence among various groups of FEWs, such as brothel-based (17.4%) and street-based (37.3%) sex workers, as compared to the prevalence among women working in other entertainment establishments (9.8%) [12]. In the absence of a safer working environment such as brothels [12, 17, 29], our findings suggest that differentiated programming is needed to ensure that HIV prevention efforts are intensified, particularly for street-based and freelance FEWs.

The higher prevalence of HIV among FEWs in the older age groups found in this study is in line with findings from another study that reported a similar relationship between HIV infection and older FEWs in Cambodia [30]. The cumulative exposure to HIV risks could explain this association. Previous studies in Cambodia also suggested that street-based FEWs tend to be older than women working in brothels and entertainment venues [12, 14, 17]. In this study, most HIV positive cases detected in the older age groups (>30 years) were aware of their HIV status before the survey.

This study found that FEWs who were not married but living with their partners were at a higher risk of HIV. We also observed a similar trend among FEWs who were married but not living with their partners. This observation is consistent with findings from previous studies in Cambodia, which showed low rates of consistent condom use in non-commercial relationships among FEWs [11, 19, 20]. In our recent study, unprotected sex was reported by FEWs to be a way to express trust and faithfulness to their regular non-commercial partners (sweethearts) [11, 19]. Together, these findings may explain the higher risk of HIV among non-married FEWs living with partners. Given the consistency of this observation, new strategies to increase consistent condom use among FEWs are warranted.

Besides, our results indicated that the risk of HIV was higher among FEWs who reported illicit drug use. This finding could be attributed to the negative impact of illicit drug use on consistent condom use, numbers of sex partners, or unsafe injection practices [12, 31–33]. Furthermore, our study found that the presence of STI symptoms was associated with HIV infection, and it is consistent with other evidence regarding the relationship between STIs and HIV infection [12, 16]. The high prevalence of STI symptoms observed in our study is congruous with findings from other studies conducted among FEWs in Cambodia [11, 12, 14, 19]. These results suggested that tailored education efforts should be implemented, emphasizing regular condom use, condom negotiation skills, and the detrimental effects of alcohol and other substance use on HIV exposure. Risk-reduction education is crucial, given that the prevalence of HIV was higher among less educated FEWs.

Strengths and limitations

The strengths of this study include the implementation of multi-stage sampling procedures to engage a large sample of FEWs across sites with a high burden of HIV in Cambodia. We used standardized data collection procedures and validated tools to collect biological samples and survey data across all study sites. Furthermore, this survey involved pertinent stakeholders at different national health system levels, NGOs, and community members in developing the study protocol, tools, and strategies for disseminating study findings.

Despite these strengths, this study also has several limitations. First, this study did not include seven provinces with a lower burden of HIV and a smaller FEW population. Therefore, the study findings may not be generalized to a national level, although the data were appropriately weighted in the analyses. Second, we collected data on sensitive issues such as sexual behaviors using self-reported measures through face-to-face interviews that may result in potential social desirability bias. The risks are likely to be underestimated, given the cultural norms governing sexual behaviors and substance use in Cambodia. Third, albeit minimal, the monetary incentive given to the participants and their connection to the ongoing community-based HIV programs may have affected their genuine motivation to partake in the study and potentially influenced their response to the survey. Nevertheless, we believe that we took sufficient measures to minimize these potential effects throughout the data collection. Finally, we could not meet the sample size requirement for freelance FEWs due to difficulty reaching this population. Therefore, generalizability to the entire population of freelance FEWs could be limited.

Conclusions

This study documents the prevalence and risk factors of HIV infection among FEWs in Cambodia. The results showed that the HIV infection risk was associated with older age, the nature of the entertainment venues where FEWs were working, and history of illicit drug use and STI symptoms in the past three months. The risk of HIV infection was inversely associated with years of formal education attained. These findings indicate that differentiated strategies for HIV prevention among FEWs should be geared towards the FEWs working as freelancers or in veiled entertainment venues, such as massage parlors, and freelance FEWs. However, prevention efforts for venue-based FEWs should be maintained. Innovative interventions such as online services and mobile health technologies using text and voice messaging may be more useful than the current reliance on physical outreach activities to effectively reach freelance and other high-risk FEWs for early HIV detection and linking them to treatment and care services.

Supporting information

S1 Questionnaire. (English).

(PDF)

Click here for additional data file. (303.1KB, pdf)
S2 Questionnaire. (Khmer).

(PDF)

Click here for additional data file. (254KB, pdf)
S1 Data

(XLSX)

Click here for additional data file. (1.6MB, xlsx)

Acknowledgments

This study was conducted in a collaboration between the National Center for HIV/AIDS, Dermatology and STD and the consortium partners of the HIV/AIDS Flagship Project, including KHANA, FHI360, PSI/PSK. We thank all implementing partners and participants in the study who fully supported the study. Special thanks go to Janika Sullivan, a master’s student from the Public Health Program, Touro University California, USA and an international intern at KHANA Center for Population Health Research for her excellent inputs in the manuscript development.

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

This study was funded by the Global Fund to Fight AIDS, Tuberculosis, and Malaria through the National Center for HIV/AIDS, Dermatology, and STD. The funding was part of the GF-New Funding Model grant (GF-NFM 2015-2017). KHANA Center for Population Health Research provided technical support to the study design, data collection, data analyses, and report writing. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. No authors received a salary from the funder.

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Decision Letter 0

Petros Isaakidis

23 Oct 2020

PONE-D-20-22691

Risk factors of HIV infection among female entertainment workers in Cambodia

PLOS ONE

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Reviewer #1: I Don't Know

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Reviewer #1: Very clear study findings yet quite simple and predictable results for those who work with this topic and sector i.e street based SWs (or FEWs) are generally more vulnerable at risk to structural violence, which has direct link with higher HIV risks and prevalence. HIV prevalence is greater in the above 30 years of age etc

While the data supports conclusion, the low recruitment of freelance SWs studied would bring bias the results

Some bias may have also been introduced by the data collectors as they are not part of the Peer FEW community, and no mentioned of sensitization to this stigmatized population.

The acronym SW (sex worker) and using FEW (female entertainment worker) instead may confuse the identity of the studied population to the wider sector reader.

Would have expected to see violence (SGBV) as a risk factor for HIV in Sws , as may miss a significant opportunity to better guide interventions addressing the needs of FSWs, and in particular those whoa re 'freelance'

would have been good to understand where do most FSWs receive a 'diagnosis' of STIs? is this using SAM or lab tests at a health facility?

I would recommend to expand the referencing bibliography from similar contexts where SW occurs . Not sure if an article (No 26) on MSM is relevant

Abortion is mentioned as a contributing risk factor to HIV infection, not sure what can be infered form this, unless it is in discussion with inconsistent condom and contraceptive use . SRHR aspect could be further expanded.

Reviewer #2: The authors of the study report result of a HIV prevalence survey among female entertainment workers in Cambodia. The results show a higher prevalence of HIV-infection among this vulnerable population. The authors conclude by recommending that differentiated services should be available to these population groups based on their vulnerability assessment.

This study is very interesting, and I would like to congratulate the authors on providing evidence on the needs of this vulnerable population. However, there are aspects which need more clarity.

Major comments

1. In the study sites and participants section, the authors describe about the FEW-IBBS 2016 survey. While in the variables section, the authors mention that they developed a structured questionnaire. It is not clear from the methods section if the current findings come from the IBBS survey or from a separate survey. While most elements of the study design and questionnaire development are present throughout the manuscript, it will be easier for the readers if the authors can describe the design for the survey from which they are reporting their current findings in a dedicated study design section.

2. While the authors give a background on the study setting, especially about the work of FEWs, there are some aspects which are not clear, especially for readers who are unfamiliar with the Cambodian setting. From the definition of FEWs in the article, it seems that all of them are involved in transactional sex. However, in the results, the authors report that 53% had transactional sex in the past one year. This piece of information also goes against the inclusion criteria (line 116), which mentions that only those who had sex at least once in the past 12 months were included. If this definition included both transactional and non-transactional sex, then I am not clear how the risk due to the participants work as FEW is defined.

3. The authors use the term “sweetheart” in the manuscript. The way it is defined, I understand “sweetheart” as something akin to a “sugar daddy”. However, given the context of the study, it is not clear how “sweetheart” and FEWs are connected. This may be due to my inability to understand the terms being used in a Cambodian context. Hence, for clarity this needs more description. While “sweethearts” are mentioned in the introduction and discussion, they are not mentioned in the results. It is also not clear; how did the authors distinguish between “sweethearts” and FEWs engaged in commercial sex.

On a related note, in the discussion (lines 306-307), the authors mention, ‘unprotected sex was reported by the participants to be a way to express trust and faithfulness to their regular non-commercial partners (sweethearts)’. This finding is not found in the results section and appears for the first time in the discussion section. It is also not clear from the study methodology how did the authors arrive at this finding.

4. The authors mention that they conducted HIV testing for those who participated in the survey. However, it is not clear what happened with those who already knew their HIV status. Were they retested for this study? More information on this needs to reported in the methods and results section. The only clue regarding this comes from lines 301-303 in the discussion section, where the authors mention that most participants older than 30 years knew their HIV status. Information about ART status of those who knew their status will also be helpful.

5. The authors mention about desirability bias in the limitations section. They also mention that steps were taken to mitigate desirability bias. However, what steps were taken has not been mentioned. The only mention about this comes from line 340, which says “sufficient measure”. It is important to understand this, since, from the manuscript text, it seems that the surveyors, or at least the organisations that they worked for were known to the participants and the participants received some kind of services from them. This can affect participants’ response and hence it is important to explicitly mention what measures were taken to avoid this bias. It will also be helpful to mention who the surveyors were and how were they trained to avoid these biases. It would also be pertinent to mention how were the survey procedures were monitored.

6. The authors report a higher odds of HIV among those with STI. However, the model used does not contain condom use frequency. Could this result be due to the fact that those with STIs have infrequent condom use, which could also be the independent risk factor for HIV?

7. In sample size calculations, the authors seem to have calculated the overall sample size required for inclusion in the survey. However, in the limitations (line 342), the authors mention that they were unable to reach the sample size for freelance FEWs. Were different sample sizes for different subgroups calculated?

8. In the methods section (line 179), the authors mention that participants received a, ‘gift card not exceeding 4USD’. Did participants receive different amounts? If yes, what was the criteria for who received what amount?

9. In 348, the authors use the term “recent history of STI symptoms”. While the definition of ‘recent’ is not mentioned in the methods, from the results section we understand that it is three months. Please mention this definition, along with any other relevant operational definitions, in the methods section. Also, please rethink the use of the word ‘recent’ in the discussion.

10. In the conclusion, the authors recommend differentiated preventive services for FEWs in older age group since they had a higher odds of living with HIV than the lower age groups. I would request the authors to re-think about this. While it is true that the results show that FEWs had a higher proportion of those living with HIV. However, we do not know from the results how long ago did they test positive for HIV. In light of this, it is necessary that preventive measures should not be focussed only on the older age groups. It is necessary to ensure that preventive and testing services should be available from even the youngest age groups, since in this way, they might be able to effect behavioural change early, which might help prevent new HIV infections.

11. The authors mention that they found lower proportion of FEWs testing HIV-positive at the establishments. They also mention that, “street based FEWs tend to be older than those working in brothels and entertainment avenues”. Are these two facts related? Could it be that the entertainment avenues prefer to employ those who are younger? Or is it that if someone tests HIV-positive, then they might not be allowed to work at these entertainment avenues? Please revisit the related conclusion based on the answers to these questions.

12. The authors mention in the strengths that they had involved all stakeholders. It is very important during this kind of work to involve all the stakeholders from the beginning and I would like to congratulate the authors on this. It would be nice to understand a little more on what was done.

13. In line 91-93, the authors mention, ‘The identified risk factors of the HIV infection in the study included being freelance sex workers and younger age of first sex (≤15 years)’. However, this factor seems missing from this study. Was this variable collected and analysed?

Minor comments

1. Line 63 – The authors mention about a triphasic response. While, the second and third phases are clearly mentioned, the first phase is not clearly demarcated. It would be easier to read if the first phase is also clearly labelled so.

2. Line 113 – It would be good to also mention the total number of provinces for readers who are not aware about Cambodian setting.

3. Line 203 – It might be pertinent to report on how many participants refused to participate.

4. The tables as they stand are not very clear which makes them difficult to read. Please format them in a manner so that the subgroups and the totals are easily readable. Also, using row percent might make the tables easier to interpret, especially for tables 1 and 2.

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Reviewer #1: Yes: Lucia O'Connell

Reviewer #2: No

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PLoS One. 2020 Dec 21;15(12):e0244357. doi: 10.1371/journal.pone.0244357.r002

Author response to Decision Letter 0

4 Dec 2020

Journal Requirements

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at:

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

RESPONSE: We have formatted our manuscript and all supporting documents in accordance with PLOS ONE’s style requirements.

2. Please include a copy of the interview guide used in the study, in both the original language and English, as Supporting Information, or include a citation if it has been published previously."

RESPONSE: We have included a copy of the questionnaire (in Khmer and English) as supplementary information.

3. Please state whether you validated the questionnaire prior to testing on study participants. Please provide details regarding the validation group within the methods section.

RESPONSE: A structured questionnaire was developed based on similar previous national surveillance surveys among female entertainment workers and our recent studies. These studies are routinely conducted by the national HIV program to observe the trend of the HIV prevalence and risk behaviors among key populations in Cambodia using standardized methods and tools. We have added the following information in a new sub-section, ‘Questionnaire development,’ (Lines 165-174):

We developed a structured questionnaire for face-to-face interviews, which took approximately 30 minutes to complete. Standardized and validated tools were adapted from previous studies among HIV key populations in Cambodia [18-20,25,26]. The structured questionnaire was initially developed in English and then translated into Khmer, Cambodia’s national language. It was then back-translated into English by another translator to ensure that the original items’ “content and spirit” were maintained. A consultative meeting was held with representatives of key stakeholders working on HIV and harm reduction programs, including NGOs and FEW communities, to review the study protocol and tools. A pilot study was conducted with 20 FEWs in Phnom Penh, later excluded from the main study.

We note that you have indicated that data from this study are available upon request. PLOS only allows data to be available upon request if there are legal or ethical restrictions on sharing data publicly. For information on unacceptable data access restrictions, please see http://journals.plos.org/plosone/s/data-availability#loc-unacceptable-data-access-restrictions.

In your revised cover letter, please address the following prompts:

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b) If there are no restrictions, please upload the minimal anonymized data set necessary to replicate your study findings as either Supporting Information files or to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. Please see http://www.bmj.com/content/340/bmj.c181.long for guidelines on how to de-identify and prepare clinical data for publication. For a list of acceptable repositories, please see http://journals.plos.org/plosone/s/data-availability#loc-recommended-repositories.

We will update your Data Availability statement on your behalf to reflect the information you provide.

RESPONSE: We have received permission from the National Center for HIV/AIDS, Dermatology and STD and uploaded the anonymized data set as a Supplementary Material file.

5. Thank you for stating the following financial disclosure:

[The funders had no role in study design, data collection and analysis, decision to

publish, or preparation of the manuscript].

At this time, please address the following queries:

a. Please clarify the sources of funding (financial or material support) for your study. List the grants or organizations that supported your study, including funding received from your institution.

b. State what role the funders took in the study. If the funders had no role in your study, please state: “The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.”

c. If any authors received a salary from any of your funders, please state which authors and which funders.

d. If you did not receive any funding for this study, please state: “The authors received no specific funding for this work.”

Please include your amended statements within your cover letter; we will change the online submission form on your behalf.

RESPONSE: To address the queries, we have included the following amended statements in the cover letter:

a. This study was funded by the Global Fund to Fight AIDS, Tuberculosis, and Malaria through the National Center for HIV/AIDS, Dermatology, and STD. The funding was part of the GF-New Funding Model grant (GF-NFM 2015-2017). KHANA Center for Population Health Research provided technical support to the study design, data collection, data analyses, and report writing.

b. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

c. No authors received a salary from the funder.

d. The authors received no specific funding for this work.

6. We noticed you have some minor occurrence of overlapping text with the following previous publication(s), which needs to be addressed:

https://bmcpublichealth.biomedcentral.com/track/pdf/10.1186/s12889-016-2814-6?site=bmcpublichealth.biomedcentral.com

In your revision ensure you cite all your sources (including your own works), and quote or rephrase any duplicated text outside the methods section. Further consideration is dependent on these concerns being addressed.

RESPONSE: Thank you for the comment. We apologize for the oversight. We have rephrased the duplicated texts accordingly.

Reviewer 1

Very clear study findings yet quite simple and predictable results for those who work with this topic and sector i.e street based SWs (or FEWs) are generally more vulnerable at risk to structural violence, which has direct link with higher HIV risks and prevalence. HIV prevalence is greater in the above 30 years of age etc.

While the data supports conclusion, the low recruitment of freelance SWs studied would bring bias the results.

RESPONSE: We thank the reviewer for your time reviewing our manuscript and providing constructive comments for improving it. We acknowledge the limitation due to the low recruitment rate of freelance sex workers. We have addressed all the reviewer’s comments and revised the manuscript accordingly. Please find our point-by-point response to your comments below.

Some bias may have also been introduced by the data collectors as they are not part of the Peer FEW community, and no mentioned of sensitization to this stigmatized population.

RESPONSE: Thank you for raising these essential comments. In this national survey, we involved representatives of key stakeholders, including FEW communities, in every stage of the survey (study design, tool development and validation, data collection, findings dissemination). We have provided further information regarding the sensitization and preparation for the data collection in ‘Data collection training’ as follows (Lines 151-163):

In this national survey, we involved representatives of key stakeholders, including FEW communities, in every stage of the survey, from study design to questionnaire development and validation, data collection, and finding dissemination. Pre-data-collection workshops and training were conducted with data collection teams and representatives of HIV key stakeholders, NGOs working with FEWs, and FEW communities. Data collection teams were composed of team leaders from the Surveillance Unit of the National Center for HIV/AIDS, Dermatology and STD, staff members of the respective provincial health department, and representatives of NGOs, community outreach workers, and FEW communities. The training covered: (1) sampling methods, including mapping and eligibility criteria, (2) informed consent procedures, (3) participants’ privacy and confidentiality, (4) study protocol and interview techniques, (5) blood specimen collection, and (6) record-keeping and completion of the survey forms. We also pretested the questionnaire during the training.

The acronym SW (sex worker) and using FEW (female entertainment worker) instead may confuse the identity of the studied population to the wider sector reader.

RESPONSE: We thank you for pointing out this issue. We understand that using the acronyms (SW and FEWs) may confuse the identity of the study population. Female entertainment workers are unique to HIV programs in Cambodia. They are women working in entertainment establishments, and many (but not all) are involved in sex work. Our previous studies found that approximately half of the female entertainment workers reported transactional sex in the past three months preceding the surveys. Therefore, it is fair to call them female entertainment workers, rather than sex workers. To minimize the confusion, we have defined female entertainment workers and revised the descriptions of female sex workers (from the literature) and female entertainment workers in this study where applicable. Please see Lines 78-81:

In Cambodia, FEWs refer to women working in entertainment establishments such as karaoke bars, massage parlors, or beer gardens. FEWs working in these establishments may or may not be involved in transactional sex. The FEW population also includes freelance sex workers who solicit clients in public places, such as streets or parks, or on calls.

Would have expected to see violence (SGBV) as a risk factor for HIV in Sws, as may miss a significant opportunity to better guide interventions addressing the needs of FSWs, and in particular those who are 'freelance'

RESPONSE: We agreed that GBV is a critical issue and can be a risk factor for HIV infection among female sex and entertainment workers. In our recent studies, we have reported high exposure to GBV and its relationships with HIV risks, substance abuse, and mental health in this population. Unfortunately, we did not collect information on GBV in this national biological and behavioral survey to accommodate more competitive questions required for addressing the goal and objectives of the survey.

Would have been good to understand where do most FSWs receive a 'diagnosis' of STIs? is this using SAM or lab tests at a health facility?

RESPONSE: STI symptoms and diagnosis were self-reported. From our data, the most common facilities where the participants received STI diagnosis were public health facilities (55.4%) and NGOs’ clinics (34.7%). These facilities follow the national guidelines. We have included these figures in the Results section (Lines 255-257).

I would recommend to expand the referencing bibliography from similar contexts where SW occurs. Not sure if an article (No 26) on MSM is relevant

RESPONSE: We thank the reviewer for this comment and agree that the referencing bibliography should be expanded within the contexts of female sex and entertainment workers. We have included relevant references where suitable. Reference No 26 (on MSM) was our previous national biological and behavioral survey among men who have sex with men, from which relevant questions on HIV risks (sexual behaviors, substance use, access to HIV services) were adapted.

Abortion is mentioned as a contributing risk factor to HIV infection, not sure what can be infered form this, unless it is in discussion with inconsistent condom and contraceptive use . SRHR aspect could be further expanded.

RESPONSE: This is an excellent comment. To avoid confusion, we have removed the mention of abortion as a contributing risk factor to HIV infection. We have also expanded the discussion on sexual and reproductive health and rights as suggested where relevant.

Reviewer 2

General comments:

The authors of the study report result of a HIV prevalence survey among female entertainment workers in Cambodia. The results show a higher prevalence of HIV-infection among this vulnerable population. The authors conclude by recommending that differentiated services should be available to these population groups based on their vulnerability assessment.

This study is very interesting, and I would like to congratulate the authors on providing evidence on the needs of this vulnerable population. However, there are aspects which need more clarity.

RESPONSE: We thank the reviewer for the encouraging comments about the contribution of this study to the body of knowledge on the needs of this vulnerable population.

Major comments

1. In the study sites and participants section, the authors describe about the FEW-IBBS 2016 survey. While in the variables section, the authors mention that they developed a structured questionnaire. It is not clear from the methods section if the current findings come from the IBBS survey or from a separate survey. While most elements of the study design and questionnaire development are present throughout the manuscript, it will be easier for the readers if the authors can describe the design for the survey from which they are reporting their current findings in a dedicated study design section.

RESPONSE: We apologize for the confusion caused by our unclear description in the methods section. We also thank the reviewer for the opportunity to clarify. Data used for this study were collected in the national biological and behavioral survey among female entertainment workers (FEW-IBBS 2016). We developed a structured questionnaire for the FEW-IBBS 2016. The authors of this manuscript were the core team members of the survey. We have revised several parts in the Materials and Methods section and believe it is now clearer.

2. While the authors give a background on the study setting, especially about the work of FEWs, there are some aspects which are not clear, especially for readers who are unfamiliar with the Cambodian setting. From the definition of FEWs in the article, it seems that all of them are involved in transactional sex. However, in the results, the authors report that 53% had transactional sex in the past one year. This piece of information also goes against the inclusion criteria (line 116), which mentions that only those who had sex at least once in the past 12 months were included. If this definition included both transactional and non-transactional sex, then I am not clear how the risk due to the participants work as FEW is defined.

RESPONSE: We agree that the contexts of female entertainment workers can be confusing, especially for readers who are unfamiliar with HIV programs in the Cambodian setting. Differentiated from female sex workers, female entertainment workers are women working in different entertainment venues who may or may not sell sex. However, the umbrella population also covers female sex workers, mostly freelance or street-based sex workers, since brothel-based sex work has become illegal under a new law to suppress human trafficking and sexual exploitation. Our previous studies have consistently shown that approximately half of the female entertainment workers are involved in transactional sex. We have revised the definition of female entertainment workers as follows (Lines 78-81):

In Cambodia, FEWs refer to women working in entertainment establishments such as karaoke bars, massage parlors, or beer gardens. FEWs working in these establishments may or may not be involved in transactional sex. The FEW population also includes freelance sex workers who solicit clients in public places, such as streets or parks, or on calls.

We included the third inclusion criteria to exclude female entertainment workers who were not sexually active. It stated ‘sexually active, defined as having had vaginal or anal sexual intercourse with at least one man in the past 12 months,’ which referred to both transactional and non-transactional sex.

3. The authors use the term “sweetheart” in the manuscript. The way it is defined, I understand “sweetheart” as something akin to a “sugar daddy”. However, given the context of the study, it is not clear how “sweetheart” and FEWs are connected. This may be due to my inability to understand the terms being used in a Cambodian context. Hence, for clarity this needs more description. While “sweethearts” are mentioned in the introduction and discussion, they are not mentioned in the results. It is also not clear; how did the authors distinguish between “sweethearts” and FEWs engaged in commercial sex.

On a related note, in the discussion (lines 306-307), the authors mention, ‘unprotected sex was reported by the participants to be a way to express trust and faithfulness to their regular non-commercial partners (sweethearts)’. This finding is not found in the results section and appears for the first time in the discussion section. It is also not clear from the study methodology how did the authors arrive at this finding.

RESPONSE: We thank the reviewer for raising these valid concerns. We have included the following statement to explain sweetheart in the context of this study in the Introduction section (Lines 87-90):

In the Cambodian context, “sweethearts” refer to romantic non-commercial sexual relationships. For FEWs, a sweetheart is typically a boyfriend or regular client in the form of indirect transactional sex through living support, dinner dates, gifts, or shopping trips. Such relationships usually involve a lack of condom use as displays of trust and intimacy.

We also revised the wording and added references to support the statement on Lines 323-324 in the Discussion.

In our recent study, unprotected sex was reported by FEWs to be a way to express trust and faithfulness to their regular non-commercial partners (sweethearts) [11, 19].

4. The authors mention that they conducted HIV testing for those who participated in the survey. However, it is not clear what happened with those who already knew their HIV status. Were they retested for this study? More information on this needs to reported in the methods and results section. The only clue regarding this comes from lines 301-303 in the discussion section, where the authors mention that most participants older than 30 years knew their HIV status. Information about ART status of those who knew their status will also be helpful.

This national integrated biological and behavioral survey aimed to track the changes in the prevalence of HIV and risk behaviors among female entertainment workers, an HIV key population in Cambodia. Therefore, all participants received HIV testing, followed by the questionnaire interviews. In the questionnaire, we also asked participants about their HIV status. Those who already knew their HIV-positive status were further questioned about HIV treatment and care services they had received. We have revised the paragraph as follows (Lines 189-201):

All participants received HIV testing regardless of whether they already knew their HIV-status. A blood sample was obtained from each participant by a trained laboratory technician through finger-prick and tested for HIV antibodies using the HIV-1/2 Determine™ test, following the national protocol [27]. We confirmed the test results by the HIV 1/2 STAT-PAK™ test on-site. If a specimen was reactive by the HIV-1/2 Determine™ test but non-reactive by the HIV 1/2 STAT-PAK™ test, the participant was recommended to go for a confirmatory test at an ART clinic of their choice with support from a community outreach worker. HIV test result was provided to the participants verbally after the interview, together with post-test counseling. All participants attended a pre- and post-test counseling session provided by trained counselors from HIV confidential counseling and testing centers located in the study sites. Those tested positive for HIV were referred to an ART clinic of their choice by a local NGO working in the respective area for care and treatment services according to the national guidelines. All participants received a token of appreciation valued at approximately US$4 for their time and effort.

We have also added ART status of those who knew their status in the Results (Lines 233-234).

5. The authors mention about desirability bias in the limitations section. They also mention that steps were taken to mitigate desirability bias. However, what steps were taken has not been mentioned. The only mention about this comes from line 340, which says “sufficient measure”. It is important to understand this, since, from the manuscript text, it seems that the surveyors, or at least the organisations that they worked for were known to the participants and the participants received some kind of services from them. This can affect participants’ response and hence it is important to explicitly mention what measures were taken to avoid this bias. It will also be helpful to mention who the surveyors were and how were they trained to avoid these biases. It would also be pertinent to mention how were the survey procedures were monitored.

RESPONSE: We thank the reviewer for raising this critical issue that may lead to potential bias in the results and conclusions. The participant recruitment was done with support from NGOs and outreach workers working with female entertainment workers in the respective study sites. However, the questionnaire interviews were conducted by independent teams who did not work directly with female entertainment workers in HIV intervention programs.

We have provided further information regarding the sensitization and preparation for the data collection in ‘Data collection training’ as follows (Lines 151-163):

In this national survey, we involved representatives of key stakeholders, including FEW communities, in every stage of the survey, from study design to questionnaire development and validation, data collection, and finding dissemination. Pre-data-collection workshops and training were conducted with data collection teams and representatives of HIV key stakeholders, NGOs working with FEWs, and FEW communities. Data collection teams were composed of team leaders from the Surveillance Unit of the National Center for HIV/AIDS, Dermatology and STD, staff members of the respective provincial health department, and representatives of NGOs, community outreach workers, and FEW communities. The training covered: (1) sampling methods, including mapping and eligibility criteria, (2) informed consent procedures, (3) participants’ privacy and confidentiality, (4) study protocol and interview techniques, (5) blood specimen collection, and (6) record-keeping and completion of the survey forms. We also pretested the questionnaire during the training.

6. The authors report a higher odds of HIV among those with STI. However, the model used does not contain condom use frequency. Could this result be due to the fact that those with STIs have infrequent condom use, which could also be the independent risk factor for HIV?

RESPONSE: Thanks for the opportunity to clarify this confusing result. Given the exploratory nature of this study, the multiple regression model was built based on the results from bivariate analyses. As described in the ‘Statistical analyses,’ we included age, education level, marital status, types of entertainment establishments and other variables that achieved p<0.05 in the bivariate analyses in the model simultaneously. We then removed variables not statistically significant from the model using a backward stepwise selection method. Condom use frequency with non-commercial partners was significantly associated with HIV infection in bivariate comparison but did not retain its significant association with HIV infection after controlling for other covariates. Thus, it was removed from the model.

7. In sample size calculations, the authors seem to have calculated the overall sample size required for inclusion in the survey. However, in the limitations (line 342), the authors mention that they were unable to reach the sample size for freelance FEWs. Were different sample sizes for different subgroups calculated?

RESPONSE: Thank you for the comment. We did not calculate different sample sizes for different sub-groups. In this study, we regarded freelance sex workers as FEWs according to the definition employed in the national HIV program. Hence, the sample size was calculated for the entire study population. Despite meeting the overall target sample size, we acknowledged that the sub-group of freelance sex workers might be underrepresented, despite striving to reach this population. They are the most difficult to reach due to their hidden nature and illegality of sex work in the country.

8. In the methods section (line 179), the authors mention that participants received a, ‘gift card not exceeding 4USD’. Did participants receive different amounts? If yes, what was the criteria for who received what amount?

RESPONSE: We apologize for the unclear statement. We have amended it for clarification as follows (Lines 200-201):

All participants received a token of appreciation valued at approximately US$4 for their time and effort.

9. In 348, the authors use the term “recent history of STI symptoms”. While the definition of ‘recent’ is not mentioned in the methods, from the results section we understand that it is three months. Please mention this definition, along with any other relevant operational definitions, in the methods section. Also, please rethink the use of the word ‘recent’ in the discussion.

RESPONSE: We agree that the description of the variables was not very clear. We have included the operational definitions in ‘Variables and measurements’ as follows (Lines 181-188):

For HIV risks, we collected information regarding the participant’s HIV status and sexual behaviors with commercial partners, defined as having sexual intercourse in exchange for money or gifts, and non-commercial partners. These included the number of sexual partners (continuous), condom use frequency (always, frequently, sometimes, never), STI diagnosis, and experiences of STI symptoms (yes or no) in the past three months. We also collected information on illicit drug use (heroin, marijuana, amphetamine-type stimulants, or other types of drugs) and alcoholic drinks at work (yes or no) in the past three months. For participants who reported living with HIV, we collected self-reported HIV care and treatment information, including ART.

Throughout the text, we have refrained from using the word ‘recent’ but stated the exact time period for the individual variable for clarity.

10. In the conclusion, the authors recommend differentiated preventive services for FEWs in older age group since they had a higher odds of living with HIV than the lower age groups. I would request the authors to re-think about this. While it is true that the results show that FEWs had a higher proportion of those living with HIV. However, we do not know from the results how long ago did they test positive for HIV. In light of this, it is necessary that preventive measures should not be focussed only on the older age groups. It is necessary to ensure that preventive and testing services should be available from even the youngest age groups, since in this way, they might be able to effect behavioural change early, which might help prevent new HIV infections.

RESPONSE: Thank you for raising this critical comment. We agree that our results did not tell when the infections occurred as we measured HIV prevalence, not incidence. It is likely that the association between HIV infection and older age instead explains the accumulative exposure to HIV infection of FEWs in the older age group, or they may have lived with HIV for years. We have revised the conclusions as follows (Lines 362-372):

This study documents the prevalence and risk factors of HIV infection among FEWs in Cambodia. The results showed that the HIV infection risk was associated with older age, the nature of the entertainment venues where FEWs were working, and history of illicit drug use and STI symptoms in the past three months. The risk of HIV infection was inversely associated with years of formal education attained. These findings indicate that differentiated strategies for HIV prevention among FEWs should be geared towards the FEWs working as freelancers or in veiled entertainment venues, such as massage parlors, and freelance FEWs. However, prevention efforts for venue-based FEWs should be maintained. Innovative interventions such as online services and mobile health technologies using text and voice messaging may be more useful than the current reliance on physical outreach activities to effectively reach freelance and other high-risk FEWs for early HIV detection and linking them to treatment and care services.

11. The authors mention that they found lower proportion of FEWs testing HIV-positive at the establishments. They also mention that, “street based FEWs tend to be older than those working in brothels and entertainment avenues”. Are these two facts related? Could it be that the entertainment avenues prefer to employ those who are younger? Or is it that if someone tests HIV-positive, then they might not be allowed to work at these entertainment avenues? Please revisit the related conclusion based on the answers to these questions.

RESPONSE: Thanks for raising these excellent points, which are all true. We have revised the conclusions to reflect these facts and their relationship in the conclusions (Lines 362-372):

This study documents the prevalence and risk factors of HIV infection among FEWs in Cambodia. The results showed that the HIV infection risk was associated with older age, the nature of the entertainment venues where FEWs were working, and history of illicit drug use and STI symptoms in the past three months. The risk of HIV infection was inversely associated with years of formal education attained. These findings indicate that differentiated strategies for HIV prevention among FEWs should be geared towards the FEWs working as freelancers or in veiled entertainment venues, such as massage parlors, and freelance FEWs. However, prevention efforts for venue-based FEWs should be maintained. Innovative interventions such as online services and mobile health technologies using text and voice messaging may be more useful than the current reliance on physical outreach activities to effectively reach freelance and other high-risk FEWs for early HIV detection and linking them to treatment and care services.

12. The authors mention in the strengths that they had involved all stakeholders. It is very important during this kind of work to involve all the stakeholders from the beginning and I would like to congratulate the authors on this. It would be nice to understand a little more on what was done.

RESPONSE: We thank the reviewer for these encouraging comments. In this national survey, we involved representatives of key stakeholders, including FEW communities, in every stage of the survey, from study design to tool development and validation, data collection, and findings dissemination. We have included this information in Materials and Methods (Lines 151-163).

In this national survey, we involved representatives of key stakeholders, including FEW communities, in every stage of the survey, from study design to questionnaire development and validation, data collection, and finding dissemination. Pre-data-collection workshops and training were conducted with data collection teams and representatives of HIV key stakeholders, NGOs working with FEWs, and FEW communities. Data collection teams were composed of team leaders from the Surveillance Unit of the National Center for HIV/AIDS, Dermatology and STD, staff members of the respective provincial health department, and representatives of NGOs, community outreach workers, and FEW communities. The training covered: (1) sampling methods, including mapping and eligibility criteria, (2) informed consent procedures, (3) participants’ privacy and confidentiality, (4) study protocol and interview techniques, (5) blood specimen collection, and (6) record-keeping and completion of the survey forms. We also pretested the questionnaire during the training.

13. In line 91-93, the authors mention, ‘The identified risk factors of the HIV infection in the study included being freelance sex workers and younger age of first sex (≤15 years)’. However, this factor seems missing from this study. Was this variable collected and analysed?

RESPONSE: In this study, being freelance sex workers was significantly associated with HIV infection in both bivariate and multiple regression analyses. We have presented and discussed this finding in the Results, Discussion, and Conclusions. However, the national survey did not collect data on the age of first sex as it was not a significant factor in previous national surveys. We will include the question in our upcoming surveys of HIV key populations.

Minor comments

1. Line 63 – The authors mention about a triphasic response. While, the second and third phases are clearly mentioned, the first phase is not clearly demarcated. It would be easier to read if the first phase is also clearly labelled so.

RESPONSE: We apologize for this oversight. We have added ‘first phase’ to the second sentence in paragraph 1 of the introduction (Line 63).

2. Line 113 – It would be good to also mention the total number of provinces for readers who are not aware about Cambodian setting.

RESPONSE: We have added the total number of provinces in Cambodia as follows (Lines 116-118):

This National Integrated Biological and Behavioral Survey among FEWs (FEW-IBBS) was conducted in 2016 in Phnom Penh and 17 other provinces purposively selected out of the 25 provinces in Cambodia.

3. Line 203 – It might be pertinent to report on how many participants refused to participate.

RESPONSE: We have added the following information at the beginning of the Results section (Lines 228-231):

Of 3353 FEWs invited, 148 (4.4%) refused to participate in the study, primarily due to their time constraints. Fifty-six participants (1.8%) with missing data of main variables or HIV testing results were further excluded from the analyses. In total, we included 3149 FEWs in the analyses. The mean age of the participants was 26.2 years (SD 5.7).

4. The tables as they stand are not very clear which makes them difficult to read. Please format them in a manner so that the subgroups and the totals are easily readable. Also, using row percent might make the tables easier to interpret, especially for tables 1 and 2.

RESPONSE: We thank the reviewer for this comment. We understand that there are different ways to present the tables. However, we have received different opinions from reviewers and our research team members. Therefore, we would like to keep the table presentation and format in the way they are now. We believe these are also a common way employed in scientific papers. We hope the reviewer would agree with this.

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Decision Letter 1

Petros Isaakidis

9 Dec 2020

Risk factors of HIV infection among female entertainment workers in Cambodia: findings of a national survey

PONE-D-20-22691R1

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Acceptance letter

Petros Isaakidis

11 Dec 2020

PONE-D-20-22691R1

Risk factors of HIV infection among female entertainment workers in Cambodia: findings of a national survey

Dear Dr. Yi:

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