PLOS ONE RESEARCH ARTICLE Sexually transmitted infections and factors associated with risky sexual practices among female sex workers: A cross sectional study in a large Andean city Luz Marina Llangarı́-Arizo ID1,2,3*, S. Tariq Sadiq4,5☯, Cynthia Márquez1☯, Philip Cooper1,5☯, Martina Furegato4☯, Liqing Zhou4,5‡, Luisa Aranha6‡, Miguel Martı́n Mateo1,2,3‡, Natalia Romero-Sandoval1,3‡ a1111111111 1 School of Medicine, Universidad Internacional de Ecuador, Quito, Ecuador, 2 Unitat de Bioestadı́stica, a1111111111 Facultat de Medicina, Universitat Autónoma de Barcelona, Barcelona, Spain, 3 Red Internacional Grups de a1111111111 Recerca d’Amèrica i Àfrica Llatines – GRAAL, Barcelona, Spain, 4 Applied Diagnostic Research and a1111111111 Evaluation Unit, St George’s University of London, London, United Kingdom, 5 Institute for Infection & a1111111111 Immunity, St George’s University of London, London, United Kingdom, 6 Ministerio de Salud Pública de Ecuador, Quito, Ecuador ☯ These authors contributed equally to this work. ‡ These authors also contributed equally to this work. * lullangari@uide.edu.ec OPEN ACCESS Citation: Llangarı́-Arizo LM, Sadiq ST, Márquez C, Cooper P, Furegato M, Zhou L, et al. (2021) Sexually transmitted infections and factors Abstract associated with risky sexual practices among female sex workers: A cross sectional study in a large Andean city. PLoS ONE 16(5): e0250117. Background https://doi.org/10.1371/journal.pone.0250117 There are limited published data on factors related to risky sexual practices (RSP) affecting Editor: Andrew R. Dalby, University of sexually transmitted infections (STIs) among female sex workers (FSWs) in Ecuador. Westminster, UNITED KINGDOM Received: October 13, 2020 Methods Accepted: March 30, 2021 Cross-sectional study of FSWs presenting for a consultation in a primary health care centre Published: May 6, 2021 during 2017. A questionnaire was administered to collect information on RSP and potential risk factors including age, membership of an FSW association, self-report of previous STI Peer Review History: PLOS recognizes the benefits of transparency in the peer review diagnosis, previous treatment for suspected STI and temporary migration for sex work. process; therefore, we enable the publication of Associations between RSP and potential risk factors were estimated by logistic regression. all of the content of peer review and author The proportion of STI was estimated from vaginal swabs by real-time PCR for four sexually responses alongside final, published articles. The transmitted pathogens (Neisseria gonorrhoeae, Trichomonas vaginalis, Chlamydia tracho- editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0250117 matis, and Mycoplasma genitalium). Copyright: © 2021 Llangarı́-Arizo et al. This is an open access article distributed under the terms of Results the Creative Commons Attribution License, which Of 249 FSWs recruited, 22.5% had reported RSPs at least once during sex work. Among permits unrestricted use, distribution, and FSWs reporting unprotected vaginal sex in the previous three months, 25.5% had at least reproduction in any medium, provided the original author and source are credited. one other RSP type. 17.6% (95%CI 13.3–22.8) had at least one active STI. Prevalence of co-infections was 2.4% (95%CI 1.1–5.2). In multivariable analysis, RSP was associated Data Availability Statement: All relevant data are within the paper and its Supporting information with age (adjusted OR 1.06; 95%CI 1.02–1.10), membership of an FSWs association (aOR files. 3.51; 95%CI 1.60–7.72) and self-reported previous STI (aOR 3.43; 95%CI 1.28–9.17). PLOS ONE | https://doi.org/10.1371/journal.pone.0250117 May 6, 2021 1/9 PLOS ONE STI and factors associated with risky sexual practices among female sex workers Funding: This study was supported by a grant Conclusions from the University Internacional del Ecuador [Grant Number UIDE-EDM04-2016-2017] https:// Among a population of female sex workers with high proportion of STIs, increasing age and www.uide.edu.ec/, Wellcome Trust Institutional belonging to an FSWs association was associated with a higher likelihood of engaging in Strategic Support Fund https://wellcome.org/what- RSP with clients. Engaging with FSWs organisations may reduce the burden of STI among we-do/our-work/institutional-strategic-support- fund and St George’s, University of London https:// sex workers. www.sgul.ac.uk/. The funders had no role in the study design, data collection, and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Introduction An estimated 376 million new infections worldwide occur annually with one of four sexually transmitted infections (STIs): chlamydia, gonorrhoea, syphilis and trichomoniasis [1]. In addi- tion, for gonorrhoea, there has been a significant increase in global prevalence of antimicrobial resistance (AMR), particularly to fluoroquinolones and azithromycin as well as worrying emergence of AMR to extended spectrum cephalosporins [2]. Importantly, less is currently known about AMR in South America. Risky sexual practices (RSP) are defined as any sexual activity that increases the risk of con- tracting STIs [3]. This may involve sexual activity with multiple partners, inconsistent condom use, having sex under the influence of drugs, or initiating sexual activity before the age of 18 years [4]. Female sex workers (FSWs), due to the dynamic of sex work and other individual and social circumstances, face several factors that make them vulnerable to RSP and therefore to STIs. Previous studies show that age, migration for sex work, place of soliciting clients or place where FSW engage in sex and community organization are associated with RSP [5–8]. On the other hand, some studies mention that a prior history of STI could be an indicator of RSP [9, 10]. In Ecuador, previously published data on RSP and STIs risk have focused largely on HIV infection [11, 12], men who have sex with men [13, 14] or transgender persons [15] while information for female sex workers (FSWs) is outdated and limited [16, 17]. In develop- ing countries there are few health programs in sex work environments coupled with limited STI surveillance and weak or non-existent structural approaches to RSP [18, 19]. Sex work is legal in Ecuador where it operates either outdoors or within closed establish- ments (known as “casas de tolerancia” [20, 21] or brothels. All brothels must be licensed, and FSWs, to work within such brothels, must obtain an “Integral Health Carnet” (IHC), an occu- pational license provided by the Ministry of Health that registers medical care, screening tests and vaccines, as well as educational and prevention activities, that is valid for 1 month. To obtain and maintain a validated IHC, FSWs must be over 18 years and regularly test negative for syphilis and HIV [22]. FSWs’ occupational associations aim to support occupational rights and to protect against violence and police harassment mainly when the work is on the street [21]. Sex work is present throughout the country but is concentrated in large cities where it is a major social and health issue related to poverty [20]. Exploring factors related to RSP is important because this information can be biased or lim- ited due to the stigma and discrimination that exists around sex work: better knowledge of RSP among FSWs helps to improve the effectiveness of prevention programs. In the present study, we analysed potential factors associated with RSP among FSWs in the Andean city of Quito. The specific objectives of this study were to identify factors related to unprotected oral, vaginal, or anal intercourse and to estimate the proportion of common STIs (gonorrhoea, trichomonas, chlamydia, and Mycoplasma genitalium) in a population of FSWs. PLOS ONE | https://doi.org/10.1371/journal.pone.0250117 May 6, 2021 2/9 PLOS ONE STI and factors associated with risky sexual practices among female sex workers These pathogens were considered together because of shared symptomatology and to provide a broader view of the potential public health consequences of RSP. Materials and methods Study design and sample collection A descriptive cross-sectional study was conducted among FSWs over 18 years of age in a pri- mary health centre in Quito, a large Andean City, during the last quarter of 2017. The women were enrolled using a convenience sample. Women attending for a health check-up at a public clinic required for validation of their IHC to allow them to continue to engage in sex work. In addition, women members of an asso- ciation of FSWs were contacted through visits to their workplaces (streets and “casas de toler- ancia”) and asked to attend the same clinic for evaluation. FSWs where excluded if they attended the medical consultation more than once, if pregnant or if unwilling to provide ques- tionnaire data. All participants provided written informed consent and none of them received any compensation for their participation. On each sample collection day all FSWs attending the clinic and willing to participate were enrolled consecutively prior to their medical consulta- tion. A single study identifier was used to link questionnaire with the biological samples. The number of female sex workers who agreed to participate, 249, makes it possible to esti- mate an expected prevalence of, 20% + -5%. Participants were interviewed by a local study investigator (LMLLA) using a questionnaire designed for the study, provided as a S2 File. Variables Included variables were age, membership of an FSW association, whether participants had temporarily left the city for sex work, self-report of being previously diagnosed with an STI (gonorrhoea, trichomonas, chlamydia, syphilis) and previous treatment (oral antibiotics, ‘pain pills’, vaginal ovules and creams) for suspected STI or genital infection at some point during sex work prescribed by a physician, having previously chronic pelvic pain at least once during their sex work, and number of medical and health-related consultations in the previous year. The variable of interest in this study is RSP that was defined as having oral (UPOS), vaginal (UPVS), or anal (UPAS) intercourse without a condom at some point during sex work and during last three months. Clinical samples collection and DNA preparation A vulvo-vaginal sample was collected using Xpert1 CT/NG patient-collected Vaginal Swab Specimen Collection kit (Cepheid), in addition to that required for routine clinical evaluation. DNA was extracted using the PureLink Genomic DNA Mini Kit (Thermo Fisher Scientific) according to manufacturer´s instructions. The quantity and quality of the DNA were mea- sured by spectrophotometry, using the Nanodrop ND-1000 (Thermo Scientific). PCR screening for STI Real-time polymerase chain reaction (RT-PCR) was done for N. gonorrhoeae, T. vaginalis, C. trachomatis and M. genitalium. Gene targets and primers for PCR detection are shown in S1 Table. RT-PCR was done using Applied Biosystems 7500 Fast Real Time PCR System in a vol- ume of 10 μl/reaction containing 5μl of Taqman™ Fast Universal PCR Master Mix, 1μl of 10x Exogenous Internal Positive Control (IPC) Mix, 0.2 ul 50x IPC DNA, 250 nM each of the PLOS ONE | https://doi.org/10.1371/journal.pone.0250117 May 6, 2021 3/9 PLOS ONE STI and factors associated with risky sexual practices among female sex workers primers, 100 Nm each of the probes and 50 ng of templates DNA. The cycling parameters were 95˚C for 10 min, followed by 40 cycles of 95˚C for 15 s. 60˚C for 1 min. Currently diagnosed with an STI was defined as having at least one positive reaction for any of the 4 pathogens and co-infection was defined as detection of two or more pathogens. Four samples were insufficient for PCR and these individuals were excluded from the estimation of the proportion. Statistical analysis Data entry and analysis were done using IBM1 SPSS1 version 24 computer software. Com- parisons of age by FSW membership of an association and RSP was done using t-tests. A p- value < 0.05 was considered statistically significant. Univariate and multivariable logistic regression models were used to explore associations between RSP and potential factors. Ethical considerations The study was conducted according to the Declaration of Helsinki and approved by the Ethical Committee of Universidad Internacional del Ecuador (02-02-17). Results Demographic and social characteristics Of 251 FSWs invited, 249 consented to participate. Median age of participants was 35 years (range 18–61 years). Among participants, mean age was higher in those that belonged to a FSW association (78/249; 31.3%) compared to those not belonging (40.1 years vs. 32.9, p<0.001) but was similar among those reporting that they temporarily migrate for sex work (79/249; 31.7%) compared to those who did not (34.1 years vs 35.6; p> 0.05). 24 (9.6%) self- reported a previous STI diagnosis at least once during their sex work (Table 1); previous gonorrhoea was reported by 13(5.3%), trichomoniasis by 6 (2.4%), chlamydia by 5 (2.0%) and syphilis by 6 (2.4%) participants. About twenty five percent of respondents had previous chronic pelvic pain. 185 (74.3%) declared treatment for an STI at least once during their sex work. 34 (13.7%) had only one medical visit in the last year including this study visit while approximately 50% reported between nine and eleven consultations which they received at least one of the following health-related services: information about STIs; examination or treatment for STIs symptoms; HIV test and prevention information, and receipt of free con- doms and instructions on their use. Risky sexual practices (RSP) Fifty-six (22.5%; 95% CI 17.8–28.6) FSWs reported engaging in RSP at least once during sex work. Among the 196 women who declared protected vaginal sex, three had some RSP: 1/196 Table 1. Background characteristics of female sex workers, Quito, 2017. Background Characteristics % or Mean Number Age (in years) 35.2 Membership of an FSWs association 31.3 78 Self-report of a previous STI diagnosis 9.6 24 Currently diagnosed with an STI 17.3 43 Previous treatment for suspected STI 74.3 185 Temporary migration for sex work 31.7 79 Risk sexual practices (RSP) 22.5 56 https://doi.org/10.1371/journal.pone.0250117.t001 PLOS ONE | https://doi.org/10.1371/journal.pone.0250117 May 6, 2021 4/9 PLOS ONE STI and factors associated with risky sexual practices among female sex workers (0.5%) UPAS and 3 (1.5%) UPOS. The mean age for those in the RSP group was greater than those in the non-RSP group (40.8 vs. 33.5 years, p<0.001). In the last three months, 47/53 (88.7%) women who reported having vaginal sex had UPVS, 7/8 (87.5%) women who reported anal sex had UPAS and 12/12 (100%) women who reported oral sex had UPOS. Of the FSWs that reported UPVS in the last three months, 12/47 (25.5%) had at least one other RSP: 7/47 (14.9%) UPAS and 9/47 (19.1%) UPOS. Vulvo-vaginal proportion of STI Of the 245 vulvo-vaginal samples, positivity rates were: N. gonorrhoeae (NG) 1.2% (95%CI 0.4–3.5), T. vaginalis (TV) 9.8% (95%CI 6.7–14.2), C. trachomatis (CT) 4.9% (95%CI 2.8–8.4), and M. genitalium (MG) 4.9% (95%CI 2.8–8.4). Overall, 17.6% (95%CI 13.3–22.8) of FSWs had at least one STI. Co-infection was detected in 2.4% (95%CI 1.1–5.2) and they were: 2 CT/ TV, CT/NG, NG/TV, CT/NG/TV, and CT/TV/MG. Of all women currently infected, four (9.3%) reported having had any STI in the past. Factors associated with RSP Univariate analyses factors showed significant association between RSP with age, membership of an FSWs association, self-report of a previous STI diagnosis and currently diagnosed with an STI. Previous treatment for suspected STI and temporary migration for sex work were not significant. In multivariable analysis showed that age (adjusted OR 1.06, 95%CI 1.02–1.10), membership of an FSW association (aOR 3.51; 95% CI 1.60–7.72) and self-report of a previous STI diagnosis (aOR 3.43 95% CI 1.28–9.17) remained significant Table 2. Discussion In the present study, we set out to improve our understanding of risky sexual practices (RSP), understood to mean genital or extragenital sexual intercourse without a condom, among a group of FSWs working in poor areas in central Quito, a large Andean city. Almost one in four FSWs participating in this study reported RSP, and among the FSWs that reported unpro- tected vaginal sex in the last three months, 25.5% had at least one other RSP type. This study reported that RSP was independently and positively associated with age, mem- bership of an FSW association and previous STI diagnosis. Risk by age increased 1.06 odds for each year and is consistent with previous studies reporting older FSWs to be more likely to engage in RSP to attract clients [5, 23]. Previous studies have reported that FSWs belonging to an association, support networks or peer groups are better at negotiating use of condoms with clients [24]; however, the results of our study showed that belonging to an FSWs’ association increased the likelihood of engaging in RSP independently of age. This could be explained by the fact that FSWs belonging to the association are more likely to be engaged in informal sex work on the street and consequently Table 2. Univariate and multivariable analysis of factors associated with RSP among FSWs of this study. Variables n (%) Crude OR 95% CI p- value Adjusted OR 95% CI p- value Age Mean, 35.2 years 1.09 1.05–1.13 <0.01 1.06 1.02–1.10 0.002 Membership of an FSWs association 78 31.3 4.26 2.28–7.94 <0.01 3.51 1.60–7.72 0.002 Self-report of a previous STI diagnosis 24 9,6 5.00 2.10–11.92 <0.01 3.43 1.28–9.17 0.01 Currently diagnosed with an STI 43 17.3 2.16 1.06–4.40 0.03 1.29 0.57–2.94 0.54 Previous treatment for suspected STI 185 74.3 0.83 0.42–1.61 0.577 1.25 0.56–2.78 0.59 Temporary migration for sex work 79 31.7 1.09 0.57–2.06 0.802 1.80 0.83–3.93 0.14 https://doi.org/10.1371/journal.pone.0250117.t002 PLOS ONE | https://doi.org/10.1371/journal.pone.0250117 May 6, 2021 5/9 PLOS ONE STI and factors associated with risky sexual practices among female sex workers have a reduced capacity to negotiate condom use [21, 25] to attract clients. Enforcing condom use is probably easier in the more ‘regulated’ and protected environment of brothels [8]. In this study, the main role of the FSWs’ association was to protect unregulated working spaces in cities [20, 21] and no to ensure implementation of effective preventive health education messages. Therefore, it is important to focus on these particularities of sex worker groups to improve STI prevention programs. In this study, temporary migrations between cities, that serve to obtain more clients and income, were not affected by age, and did not affect RSP. Other studies show that some mobile FSWs groups are unable to turn away clients for unprotected sex [5, 6]. This study observed that a self-report of a previous STI diagnosis was associated with RSP but a previous STI treatment was not. The discrepancies may be due to recall bias or social desirability bias related to self-reporting of STIs. Nevertheless, information about STI diagno- sis could be an indirect indicator of unprotected sexual behaviour [9]. The inconsistent condom uses in FSWs increase the risk of contracting STI through multi- ple factors including a large number of sexual partners, unsafe working conditions, and barri- ers to negotiation a consistent condom use [26]. Moreover, their vulnerability is exacerbated by the social and health inequalities which they face [27, 28]. In this study, the proportion of N. gonorroheae (1.2%) and C. trachomatis (4.9%) was lower than the reported in previous studies in Mexico (2.9% and 15.3%) [29] and Perú (1.6% and 16.4%) [30]. Regarding, the proportion of T. vaginalis (9.8%), it was higher than the rates reported in Peru (7.9%) [30], China (2.1%) [31] and Iran (6.1%) [32]. We observed a propor- tion of M. genitalium of 4.9%, somewhat lower than a 15.9% estimated among FSWs world- wide from a meta-analysis of studies between 1991 and 2016 [33]. To our knowledge, this is the first estimate of STI proportion in a group of FSWs in Ecuador using a highly sensitive molecular method (RT-PCR). Because of the sampling method, our study findings are not nec- essarily representative of the entire population of FSWs. The low relatively proportion of STIs observed here could indicate the importance of regulating and legalizing sex work and allow- ing FSWs access to health services. However, more data are needed to understand better the different elements of sex work at both city and country levels. The study had several potential limitations. Because all participants were FSWs attending a state health clinic for validation of their IHC, there may have been reduced heterogeneity with respect to potential risk factors. We did not study various risk factors that might have underes- timated RSP such as sexual behaviour with stable or occasional non-paying partners, educa- tional level, and alcohol or drug use [23]. The study recruited FSWs attending health clinics for IHC validation potentially leading in bias resulting from pressure to provide ‘correct’ responses [34]. There was also potential selection bias as a significant number of FSWs, not represented in this sample, are thought to engage informally in RSP without IHCs. Finally, the findings of this study may not be generalizable to FSWs working outside Quito in smaller cities and towns, where FSWs tend to be less organized and more vulnerable and consequently may have higher rates of RSPs. Conclusions In Quito, older FSWs, previously diagnosed with an STI and belonging to an FSW association, are more likely to engage in RSP with their clients. This study provides new information about the current proportion of STIs in FSW. Our data provide surprising and important elements that will inform and strengthen the capacity of public health interventions to reduce RSP and impact of STI among FSWs, key factors to improve their sexual health. PLOS ONE | https://doi.org/10.1371/journal.pone.0250117 May 6, 2021 6/9 PLOS ONE STI and factors associated with risky sexual practices among female sex workers Supporting information S1 Table. Gene targets and primers used for current diagnosed of STIs in this study. (DOCX) S1 Data. (XLSX) S1 File. Regression model. (PDF) S2 File. Questionnaire English and Spanish version. (PDF) Acknowledgments The authors would like to thank the FSWs associations for supporting the development of this study. Author Contributions Conceptualization: S. Tariq Sadiq, Cynthia Márquez, Philip Cooper, Natalia Romero- Sandoval. Data curation: Luz Marina Llangarı́-Arizo. Formal analysis: Luz Marina Llangarı́-Arizo, Martina Furegato, Miguel Martı́n Mateo. Funding acquisition: S. Tariq Sadiq. Investigation: Luz Marina Llangarı́-Arizo, Cynthia Márquez, Martina Furegato, Liqing Zhou, Luisa Aranha, Miguel Martı́n Mateo. Methodology: S. Tariq Sadiq, Liqing Zhou, Luisa Aranha. Project administration: Cynthia Márquez. Resources: Philip Cooper, Luisa Aranha. Software: Martina Furegato. Supervision: S. Tariq Sadiq, Cynthia Márquez, Philip Cooper, Miguel Martı́n Mateo, Natalia Romero-Sandoval. Validation: Philip Cooper, Liqing Zhou, Miguel Martı́n Mateo. Writing – original draft: Luz Marina Llangarı́-Arizo. Writing – review & editing: S. Tariq Sadiq, Cynthia Márquez, Philip Cooper, Martina Fure- gato, Liqing Zhou, Luisa Aranha, Miguel Martı́n Mateo, Natalia Romero-Sandoval. References 1. WHO. Report on global sexually transmitted infection surveillance 2018. 2018;978-92-4-156569-11. WHO | Report on global sexually transmitted infection surveillance 2018. In: WHO [Internet]. World Health Organization; [cited 23 Apr 2020]. http://www.who.int/reproductivehealth/publications/stis- surveillance-2018/en/ 2. Wi T, Lahra MM, Ndowa F, Bala M, Dillon J-AR, Ramon-Pardo P, et al. 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