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Original research
Prevalence of sexually transmitted infections and associated risk factors among female sex workers in Guinea-Bissau
  1. Jacob Lindman1,
  2. Mamadu Aliu Djalo2,
  3. Ansu Biai3,
  4. Fredrik Månsson4,
  5. Daniel Golparian5,
  6. Joakim Esbjörnsson4,
  7. Marianne Jansson6,
  8. Patrik Medstrand6,
  9. Magnus Unemo5,7,
  10. Hans Norrgren1
  11. Sweden Guinea-Bissau Cohort Research (SWEGUB CORE) group
    1. 1The Department of Clinical Sciences Lund, Lund University, Lund, Sweden
    2. 2Environmental Action in the Third World (ENDA), Bissau, Guinea-Bissau
    3. 3The National Public Health Laboratory, Bissau, Guinea-Bissau
    4. 4The Department of Translational Medicine, Lund University, Malmö, Sweden
    5. 5WHO Collaborating Centre for Gonorrhea and Other STIs, Faculty of Medicine and Health, Örebro University Hospital, Örebro, Sweden
    6. 6The Department of Laboratory Medicine, Lund University, Lund, Sweden
    7. 7Institute for Global Health, University College London, London, UK
    1. Correspondence to Dr Jacob Lindman, Department of Clinical Sciences Lund, Lund University, Lund, 221 85, Sweden; jacob.lopatko_lindman{at}med.lu.se

    Abstract

    Objective To estimate the prevalence of the curable sexually transmitted infections (STIs) Chlamydia trachomatis, Neisseria gonorrhoeae, Mycoplasma genitalium, Trichomonas vaginalis and Treponema pallidum, to identify associated risk factors and to assess ciprofloxacin resistance in N. gonorrhoeae-positive specimens among female sex workers (FSWs) in Guinea-Bissau.

    Methods For this cross-sectional study, FSWs were recruited from October 2014 to May 2019. A questionnaire on STI risk factors was completed by the study participants, and the women were asked to provide a vaginal swab for nucleic acid amplification tests for C. trachomatis, N. gonorrhoeae, M. genitalium, T. vaginalis (Aptima, Hologica), as well as a blood sample for T. pallidum serological testing and discriminatory HIV-testing. The prevalence of STIs was determined, and multivariate logistic regression was used to identify STI risk factors.

    Results The study included 467 women. The prevalence of current infection with any curable STI was 46.7%, and the most common pathogen was T. vaginalis (26.3%), followed by M. genitalium (21.9%), C. trachomatis (11.8%), N. gonorrhoeae (10.1%) and T. pallidum (2.8%). The proportion of asymptomatic infections among the diagnosed STIs was 61.8%, 61.5%, 55.3%, 55.3% and 52.2% for C. trachomatis, T. pallidum, N. gonorrhoeae, T. vaginalis and M. genitalium, respectively. The prevalence of the gyrA S91F mutation conferring ciprofloxacin resistance in N. gonorrhoeae-positive specimens was 84.0%. Significant risk factors for having a curable STI were age and HIV-1 infection, while use of female condoms was a protective factor.

    Conclusion This study demonstrated that the prevalence of curable STIs was high among FSWs in Guinea-Bissau during the study period, indicating an unmet need for STI services. Moreover, the results indicated that symptomatic treatment might be insufficient, highlighting a need for periodic aetiological testing to facilitate detection of asymptomatic as well as symptomatic STIs to stop ongoing transmission.

    • NEISSERIA GONORRHOEAE
    • Chalmydia Trachomatis
    • Mycoplasma genitalium
    • Sex Work
    • AFRICA

    Data availability statement

    Data are available upon reasonable request. The data set used for the current study is available from the corresponding author on reasonable request.

    http://creativecommons.org/licenses/by-nc/4.0/

    This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

    https://doi.org/10.1136/sextrans-2023-056015

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      WHAT IS ALREADY KNOWN ON THIS TOPIC

      • WHO’s Global Health Sector Strategy on Sexually Transmitted Infections for 2016–2021 was launched in 2016, and one of their key actions is to understand the STI epidemic and to define the possible key populations in each country.

      • We have recently shown that the overall HIV prevalence among female sex workers (FSWs) in Guinea-Bissau is four times higher, compared with women in the general population.

      • At the same time, there is a lack of data on the prevalence of curable STIs and associated risk factors among FSWs.

      WHAT THIS STUDY ADDS

      • FSWs in Guinea-Bissau are exhibiting high prevalence of STIs and most FSWs with an STI do not report symptoms.

      • High levels of ciprofloxacin resistance in Neisseria gonorrhoeae-positive specimens were observed, showing that this drug is no longer suitable for treatment of gonorrhoea in Guinea-Bissau.

      HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY

      • Overall our study indicates the need for development of STI control programmes in Guinea-Bissau, including periodic aetiological screening for curable STIs among FSWs, and a need to strengthen surveillance of curable STIs particularly among FSWs.

      Introduction

      Annually an estimated 376 million new cases of curable sexually transmitted infections (STIs), including Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis and Treponema pallidum, occur among adults worldwide.1 Mycoplasma genitalium is also a significant pathogen,2 however the prevalence is not yet estimated by the WHO and N. gonorrhoeae has been included in the WHO’s global priority list of antibiotic-resistant bacteria, as it has developed resistance to all antimicrobials introduced for first-line treatment during the last 80–90 years.3 4 Symptomatic and asymptomatic STIs are a major cause of morbidity.5 In addition, the role of curable STIs in the dynamics of HIV acquisition and transmission has been well established.6

      WHO’s Global Health Sector Strategy on Sexually Transmitted Infections for 2016–2021 was launched in 2016, setting four global targets for 2030, including a 90% reduction in the incidence of T. pallidum and N. gonorrhoeae.7 One of their key actions is to understand the STI epidemic and to define the possible key populations in each country. Female sex workers (FSWs) are vulnerable to both curable STIs and HIV given their high-risk sexual practices, which is further heightened by structural barriers such as low access to healthcare services, stigma and discrimination.8 Previous systematic reviews of STIs among FSWs in Africa have estimated the prevalence of N. gonorrhoeae, C. trachomatis, T. vaginalis to 7.6%,9 5.5%9 and 23%,10 respectively. A global review including one study from Africa, estimated the prevalence of M. genitalium among FSWs to 15.9%.11 In West Africa, the prevalence of T. pallidum among FSWs was 2.2% in Togo and 1.4% in Burkina Faso.12 Guinea-Bissau is a small country in West Africa and one of the least developed countries in the world.13 The estimated size of the sex worker population in the country is 790014 and we have recently demonstrated that the overall HIV prevalence is four times higher among FSWs in Guinea-Bissau compared with women in the general population.15 In contrast data on the prevalence of curable STIs and associated risk factors among most-at-risk-populations such as FSWs are, to our knowledge, non-existent. This further highlights the need of studies to better understand STI transmission to inform future targeted interventions and control programmes to reduce the burden of STIs in this most-at-risk-population (MARP) and to reach WHO global targets by 2030.

      In the present study, we investigated the prevalence of C. trachomatis, N. gonorrhoeae, T. vaginalis, T. pallidum and M. genitalium, identified associated risk factors and assessed ciprofloxacin resistance in N. gonorrhoeae among FSWs in eight cities in Guinea-Bissau.

      Methods

      Ethics

      All participants provided written informed consent (signature or thumb print).

      Study design

      A cross-sectional study of FSWs was designed and implemented through a collaboration between Lund University in Sweden, the National Public Health Laboratory (LNSP) in Guinea-Bissau, and Environmental Action in the Third World (ENDA—a non-governmental organisation in Guinea-Bissau). The inclusion of participants took place between October 2014 and May 2019.

      A target sample size of 400 individuals was calculated to give sufficient power based on an estimated prevalence of 40% for any of C. trachomatis, N. gonorrhoeae, M. genitalium, T. pallidum and T. vaginalis among the FSWs, a 95% CI of 1.96 (α=5%) and degree of absolute precision of 5% (d=0.05).

      Participants in the capital city of Bissau were included through venue-based convenience sampling at nine different venues, where FSWs are known to solicit sex. Participants in seven cities outside Bissau were identified through peer-based chain referral at 1–4 different venues depending on the size of the city (14 different venues in total) and were required to come to the mobile clinic during daytime.15 Inclusion criteria were: being biologically female, ≥16 years old, self-reported engagement in selling sex in the last 12 months and capacity to consent.

      Data collection

      A team of one trained nurse, one social worker and one driver undertook the data collection in a mobile clinic. Interviewer-administered questionnaires were used to obtain information on demographics (nationality, education, religion, sources of income, marital status, number of live children, alcohol and drug use), sexual history (age at sexual debut, age at start of sex work, previous HIV test, number of clients, condom use, payment from last client) and symptoms (genital ulcer, vaginal discharge or lower abdominal pain). All study participants underwent venous blood sampling and provided a high vaginal swab taken under nurse guidance. Blood and vaginal samples were stored at room temperature until transportation back to LNSP in Bissau the same day, for freezer storage (−20°C) and then transported on dry ice to Lund University, Sweden for long-term storage (−80°C) until analysis. All HIV-infected study participants were referred to an HIV treatment clinic of their choice for follow-up examination and treatment as per national guidelines. Furthermore, participants reporting STI symptoms received syndromic treatment and asymptomatic participants with a curable STI received directed treatment according to national guidelines.

      Laboratory procedures

      Blood samples were screened on site with the Determine HIV-1/2 test (Abbott Diagnostic Division, Hoofdorp, Holland). Confirmation and HIV type discrimination was performed at LNSP with Immunocomb HIV-1/2 BiSpot (Orgenics, Yavne, Israel) until September 2016 and thereafter with Geenius HIV-1/2 confirmatory assay (Biorad, Marnes-al-Coquette, France) as the production of Immunocomb ceased. Immunocomb and Geenius have been evaluated in parallel towards the ability to discriminate between HIV types.16 Prior to March 2016 HIV-1 viral load was determined at the Section of Clinical Virology at Lund University, Sweden, using an inhouse TaqMan quantitative PCR with primers and probes as described.17 From March 2016, plasma HIV-1 viral load quantification was performed using GeneXpert HIV-1 Quant Assay (Cepheid Innovations, USA) at LNSP, Bissau. Plasma was screened for evidence of past or present T. pallidum infection at LNSP with T. pallidum particle agglutination assay (TPPA; Fujirebio, Tokyo, Japan) and if positive further analysed with the Venereal Disease Research Laboratory test (VDRL; Sypal, Diagast, Lille Cedex, France) for the detection of active cases.18 Vaginal swabs in Aptima vaginal swab specimen collection tubes were tested at the WHO Collaborating Centre for Gonorrhea and Other STIs, Örebro University Hospital, Sweden, using the Aptima Combo 2 (C. trachomatis and N. gonorrhoeae), Aptima Trichomonas vaginalis, and Aptima Mycoplasma genitalium (only samples collected from July 2015) assays on a Panther Instrument, in accordance with the manufacturer’s instructions (Hologic, San Diego, California, USA). The sensitivity and specificity of these assays have been previously assessed, with sensitivities and specificities >90%.19 The ResistancePlus GC assay (SpeeDx, Sydney, Australia) was used to detect GyrA S91F mutations predicting ciprofloxacin resistance in N. gonorrhoeae-positive specimens in samples collected before September 2017. This assay has demonstrated 100% sensitivity/specificity for the detection of GyrA S91F mutation.20

      Data analysis

      Descriptive statistics were used to summarise the data. Frequency distributions were used to describe categorical variables. For continuous variables, the median and IQR were reported. The χ2 test was used to evaluate associations between categorical variables. Univariable logistic regressions were performed for STI status and potential risk factors (adjusted for age). Risk factors with p<0.10 in the univariable analysis were included in the multivariable model. Risk factors with p<0.05 in the final model were considered independent risk factors for STI. Stata V.13.121 was used to calculate STI prevalence and to perform statistical tests including multivariate regressions to determine risk factors for STI.

      Results

      Study participants characteristics

      Between October 2014 and May 2019, 639 women provided consent. Among them 52 women did not engage in sex work according to our definition and were excluded from further analysis. Complete biological samples (blood sample and vaginal sample) were available for 467/587 (79.6%) women (figure 1), which was used in further analysis. The median age was 27 years (IQR 22–33) and the median number of years of education was 6 (IQR 0–9). Almost half of the study participants (43.4%) had an alternative income in the informal sector, mostly selling food items at the roadside. The majority of the women were single (56.8%), 17.5% were divorced or separated, 11.6% were widowed, and 14.0% were married. The median age at start of sex work was 16 years (IQR 15–18). The median number of sex partners in the last week was 1 (IQR 1–12), and the median number of clients in the last day of sex work was 1 (IQR 1–2). The median income from the last client was ~US$4.08 (IQR 2.45–8.16). Further characteristics of the study participants are described in table 1.

      View this table:
      Table 1

      Basic characteristics of the study participants

      Figure 1
      Figure 1

      Flow chart indicating the number of study participants included in the data analysis.

      Prevalence of curable STIs and HIV

      The prevalence of current infection with any curable STI was very high (46.7%) and a large proportion of the women reported current STI symptoms (46.5%). However, there was no difference in curable STIs among women reporting symptoms (47.0%) compared with those not reporting symptoms (46.5%) (OR 0.97, 95% CI 0.67 to 1.41, p=0.876). Overall, T. vaginalis was the most common pathogen (26.3%), followed by M. genitalium (21.9%), C. trachomatis (11.8%), N. gonorrhoeae (10.1%) and T. pallidum (2.8%) (table 2).

      View this table:
      Table 2

      STI prevalence and prevalence by current symptoms

      In 31 of the 42 N. gonorrhoeae-positive specimens collected before September 2017, a gyrA result was successfully generated. Most of the N. gonorrhoeae-positive specimens had a gyrA S91F mutation conferring ciprofloxacin resistance (83.9%, 26/31). Of the remaining 11 samples, 4 samples were indeterminate for gyrA, 1 sample was inhibited in the amplification and 6 samples were used up.

      The prevalence of a positive TPPA test was 9.5% (44/463, 95% CI 7.0% to 12.5%) and 27.2% of participants with a positive TPPA test had a positive VDRL test (13/44). All participants with a positive TPPA and VDRL test except one woman denied current genital ulcers or having had genital ulcers in the previous year. The prevalence of co-infections was 15.2% (71/467, 95% CI 12.1% to 18.8%), and the most common dual co-infections were C. trachomatis/T. vaginalis, C. trachomatis/N. gonorrhoeae, M. genitalium/T. vaginalis and N. gonorrhoeae/T. vaginalis, with 21, 23, 20 and 18 women in each group, respectively.

      The HIV-1 prevalence was 27.0% (including HIV-1/2 dual-infected women) and the HIV-2 prevalence was 6.2% (including HIV-1/2 dual-infected women). Overall 30.2% (141/467, 95% CI 26.1% to 34.6%) were infected with HIV-1 and/or HIV-2. The prevalence of any curable STI among HIV-1 infected participants was 56.3% (71/126), which was significantly higher than 43.1% (147/341) for HIV-1-negative participants adjusted for age (OR 1.91, 95% CI 1.25 to 2.91, p=0.003). In addition, the prevalence of any curable STI among viraemic HIV-1-infected women (HIV-1 viral load ≥1000 copies/mL) was 63.2% (48/76), which was significantly higher than 37.9% (11/29) for virally suppressed HIV-1-infected women (HIV-1 viral load <1000 copies/mL) adjusted for age (OR 2.89, 95% CI 1.19 to 7.10, p=0.020). The prevalence of any curable STI among HIV-2-infected participants was 48.3% (14/29) which was not different to 47.7% (204/428) among HIV-2-negative participants (OR 1.32, 95% CI 0.59 to 2.96, p=0.492).

      Investigating the prevalence of curable STIs by type among HIV-1-infected and HIV-1-negative participants, M. genitalium was significantly more common in HIV-1-infected participants compared with HIV-1-negative participants adjusted for age, 30.2% (26/86) vs 18.8% (43/229) (OR 2.05, 95% CI 1.14 to 3.70, p=0.016). A positive TPPA test was also significantly more common in HIV-1-infected participants compared with HIV-1-negative participants adjusted for age, 17.6% (22/125) vs 6.5% (22/338) (OR 2.56, 95% CI 1.34 to 4.90, p=0.004).

      Risk factors for curable STIs

      Univariate analysis showed that age, HIV-1 infection and having two or more clients on the last day of sex work were risk factors for STI, while residing in the capital Bissau also tended towards being a risk factor (table 3). Previous use of female condoms tended towards being a protective factor. In the multivariate analysis age 26–35 years and HIV-1 infection were significant risk factors for STI while previous use of female condoms was a protective factor against being infected with a curable STI.

      View this table:
      Table 3

      Independent risk factors for STI in univariate and multivariate analyses

      Discussion

      In this cross-sectional study of prevalence of curable STIs among FSWs, the first in Guinea-Bissau, we found a high prevalence of all investigated STIs indicating the need of an STI control programme in this MARP.

      Almost half of the study participants (46.7%) had one or multiple curable STIs, which is more than three times higher compared with women in the general population from the most recent community-based study in Guinea-Bissau conducted in 2016 (14.9%).22 In that study the prevalence of C. trachomatis, N. gonorrhoeae, M. genitalium, T. vaginalis and T. pallidum was 5.7%, 3.9%, 2.8%, 9.9% and 0.8%, respectively, compared with 11.8%, 10.1%, 21.9%, 26.3% and 2.8%, respectively, in our study. Overall the prevalence of the investigated curable STIs in our study was mostly higher or comparable to those reported among FSWs in previous systematic reviews and studies in Africa. The prevalence of C.trachomatis in our study (11.8%) was more than two times higher than the estimated prevalence among FSWs in Africa in a recent systematic review (5.5%).9 In the same study the estimated prevalence of N. gonorrhoeae was 7.6%, while the prevalence of N. gonorrhoeae in our study was 10.1%. In a recent systematic review, the estimated pooled prevalence of T. vaginalis in the African region among FSWs was 23%,10 while the prevalence of T. vaginalis in our present study was slightly higher (26.3%). In another systematic review the reported prevalence of M. genitalium among FSWs was 15.9%,11 which is substantially lower than in our study (21.9%). However only one study from Africa was included in that study. In contrast the prevalence of M. genitalium found in a study investigating the prevalence of STIs among FSWs in Ghana and Benin was slightly higher than in our study.23 The prevalence of M. genitalium in that study was 26.3%. The prevalence of T. pallidum in our study was 2.8%, which is higher than previously reported among FSWs in Togo (2.2%) and Burkina Faso (1.4%).12

      The prevalence of all the studied curable STIs in our study was comparable among symptomatic and asymptomatic women even after prompting for symptoms (47.0% vs 46.4%). Many cases would thus not have been detected by the syndromic management approach. This might result in delayed treatment or no treatment at all and hence a higher prevalence and large reservoir for transmission and ongoing infection, which could lead to serious complications.5 Conversely the majority of symptomatic women in our study did not have a curable STI (53.0%) and it is well documented that syndromic treatment also leads to overtreatment, which contributes to antimicrobial resistance.24 We found the gyrA S91F mutation conferring ciprofloxacin resistance in 84% of N. gonorrhoeae-positive specimens, which is more than eight times higher compared with a study investigating antibiotic resistance in N. gonorrhoeae isolates collected in 2006–2008 with a resistance to ciprofloxacin of 10%.25 In that study, antibiogram was used to determine ciprofloxacin resistance compared with the gyrA S91 genotyping used in our study. GyrA S91 genotyping is a sensitive and specific method to predict in vitro ciprofloxacin resistance in N. gonorrhoeae.20 The sharp increase in and high proportion of ciprofloxacin resistance makes this drug no longer suitable for the treatment of gonorrhoea in Guinea-Bissau. A similar increase in N. gonorrhoeae resistant to ciprofloxacin has been reported worldwide according to the WHO global surveillance.26 These findings highlight the need for cheap and practical screening methods to facilitate periodic aetiological screening for asymptomatic STIs in high-risk populations as suggested by WHO.27

      The risk of curable STIs was reduced in women reporting use of female condoms although the number of women that had used female condoms was low. This is in concordance with a recent review investigating the effectiveness of female condoms in preventing HIV and curable STIs, which found that use of female condoms plus male condoms were more effective than use of male condoms only in preventing STIs.28 On the other hand, and a bit surprisingly, use of male condom was not associated with lower risk of STI although that may be explained by recall bias or incorrect use.29

      This study had several limitations. First, it is possible that the study participants in our study are not representative of FSWs in Guinea-Bissau. Respondent-driven sampling could have addressed this and resulted in a more representative sample. That was unfortunately not possible due to budget and resource limitations. Second, even though the number of study participants was sufficient to estimate the prevalence of STIs and determine some risk factors associated with STIs, the study was probably underpowered to detect all relevant risk factors. Third, questionnaire data are subject to recall bias and social desirability; in addition some questions may not have been truthfully answered. Lastly, almost half of the study participants reported sexual debut under the age of 16 years but FSWs under the age of 16 years were not eligible to participate. Because of this, data are lacking in a potentially important age group.

      In conclusion this is the first study to demonstrate the prevalence of curable STIs among FSWs in this region. With an estimated prevalence of 46.7% we show that curable STIs are a considerable burden among this MARP in Guinea-Bissau. We found a reduced risk of curable STIs in FSWs reporting use of female condoms and wider distribution of female condoms in this population should be explored. We also found a high level of ciprofloxacin resistance in N. gonorrhoeae-positive specimens, showing that this drug is no longer suitable for treatment of gonorrhoea in Guinea-Bissau as in most other countries worldwide. Finally, we showed that many FSWs with a curable STI do not report symptoms meaning that their STI would not be detected and treated with syndromic management, stressing the need for periodic aetiological STI screening with diagnostic tests in this population. Our results suggest that Guinea-Bissau is far from reaching the WHO’s STI elimination targets and that there is a need to strengthen surveillance of curable STIs and improve knowledge of STI prevalence, aetiology and antimicrobial resistance. Overall our results show that an STI control programme targeting FSWs in Guinea-Bissau and access to point-of-care diagnostic tests is urgently needed.

      Data availability statement

      Data are available upon reasonable request. The data set used for the current study is available from the corresponding author on reasonable request.

      Ethics statements

      Patient consent for publication

      Ethics approval

      This study involves human participants and was approved by the National Health Ethics Committee in Guinea-Bissau (010/CNES/INASA/2014 and 039/CNES/INASA/2016), the Regional Ethical Review Board, Lund University, Sweden (Dnr 2014/424). Participants gave informed consent to participate in the study before taking part.

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      Footnotes

      • Handling editor Laith J Abu-Raddad

      • Collaborators The authors thank all participants in the study. The listed authors and the members of the Sweden Guinea-Bissau Cohort Research (SWEGUB CORE) group, including Babetida N’Buna, Antonio Biague, Ansu Biai, Cidia Camara, Zacarias Jose da Silva, Joakim Esbjörnsson, Marianne Jansson, Sara Karlson, Jacob Lindman, Patrik Medstrand, Fredrik Månsson, Hans Norrgren, Gülsen Özkaya Sahin and Sten Wilhelmson, also thank the staff of the National Public Health Laboratory and Environmental Action in the Third World (ENDA) in Bissau, Guinea-Bissau for their assistance. Antonio Biague deceased.

      • Contributors JL acted as guarantor. HN was responsible for funding. All authors and members of the SWEGUB CORE group were involved in concept of the study and design. JL, FM, MAD and AB conducted the survey. Laboratory work was done by members of the SWEGUB CORE group, MU and DG. JL performed data analysis and prepared the manuscript. All authors critically revised the article and approved submission.

      • Funding The study was supported by the Swedish Research council (2013-06541), Lund University (Dnr F: 2014/354) and Region Skåne Research and Development (REGSKANE-826071).

      • Competing interests None declared.

      • Provenance and peer review Not commissioned; externally peer reviewed.