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Sexually Transmitted Infection Prevalence Among Women at Risk for HIV Exposure Initiating Safer Conception Care in Rural, Southwestern Uganda

Chitneni, Pooja MD∗,†; Bwana, Mwebesa Bosco MBChB, MPH‡,§; Owembabazi, Moran MPH§; O'Neil, Kasey MPH§; Kalyebara, Paul Kato MBChB, MMed; Muyindike, Winnie MBChB, MMed; Musinguzi, Nicholas MSc§; Bangsberg, David R. MD, MPH; Marrazzo, Jeanne M. MD, MPH; Haberer, Jessica E. MD, MPH§,∗∗; Kaida, Angela PhD††; Matthews, Lynn T. MD, MPH∗,∥

Author Information
Sexually Transmitted Diseases: August 2020 - Volume 47 - Issue 8 - p e24-e28
doi: 10.1097/OLQ.0000000000001197
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Sub-Saharan Africa (SSA) carries a high burden of sexually transmitted infections (STIs). In 2016, there were 376 million new cases of the 4 major, curable STIs: Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, and Treponema pallidum, and SSA had the highest global incidence of gonorrhea and trichomoniasis among men and women.1 Sexually transmitted infections can cause adult morbidity, increase HIV transmission and acquisition risk,2 and cause neonatal morbidity and mortality if transmitted perinatally.3

For people in HIV serodifferent relationships, tenofovir-based preexposure prophylaxis (TDF/FTC PrEP) is recommended by the World Health Organization and many countries (including Uganda) to reduce HIV infection risk by up to 90%.4 In addition, the World Health Organization and others emphasize the potential value of PrEP for HIV-exposed women planning for pregnancy as an efficient strategy to prevent perinatal transmission and promote women's health.4,5 In Uganda, the total fertility rate is 5.1 children per woman, and adult HIV prevalence is approximately 7%.6,7 Thus, many women with personal and/or partner pregnancy plans may be exposed to HIV. In addition, women are at increased risk for HIV acquisition: in Eastern and Southern Africa, young women acquire HIV at twice the rate of their male peers.8 The 2016 Ugandan Ministry of Health first recommended TDF/FTC PrEP to prevent HIV acquisition, and the Mbarara Regional Referral Hospital began offering PrEP in late 2017.9

Sexually transmitted infection prevalence among many key populations at risk for HIV exposure and considering PrEP has been shown to be high.10,11 The majority of this work has focused on gay, bisexual, and men who have sex with men populations in North America and Europe.10,11 There are, however, scant data on PrEP and STIs among women at risk for HIV acquisition in SSA. In addition, we are not aware of data on STI prevalence in the context of safer conception programming.

To our knowledge, no studies have determined STI prevalence through laboratory-screening in rural Uganda among women planning for pregnancy and considering PrEP as a part of safer conception care. As PrEP is disseminated across Uganda and SSA, knowledge of STI prevalence and associated risk factors will help to inform PrEP programming. In this study, we assessed STI prevalence and associated risk factors for chlamydia, gonorrhea, trichomoniasis, and syphilis among a cohort of women at risk for HIV acquisition and seeking safer conception care.

MATERIALS AND METHODS

Study Design and Participants

The Healthy Families PrEP Study (NCT03832530) is a mixed-methods, prospective, cohort study that assessed PrEP uptake and adherence among women at risk for HIV exposure with personal or partner plans to have a child in rural, southwestern Uganda. Inclusion criteria consisted of being an HIV-uninfected woman, 18 to 40 years old, fluent in the local language (Runyankole) or English, in a partnership with a man living with HIV or unknown HIV serostatus, personal or partner desire to conceive a child in the coming year, and not currently pregnant. Participants attended study visits at enrollment, 3, 6, and 9 months. Participants exited the study if they completed 9 months of follow-up or tested positive for HIV. Those with incident pregnancy were followed up to the end of pregnancy.

Recruitment was conducted primarily through the Healthy Families Clinical Program, a safer conception counseling program for couples and individuals affected by HIV, housed within the HIV clinic at the Mbarara Regional Referral Hospital.12 Additional recruitment measures included approaching women accessing HIV counseling and testing at the Mbarara Municipal Council, Bwizibwera, Kinoni, Kakoba, and Mbarara Regional Referral Hospital outpatient clinics.

Study Procedures

Counseling and Questionnaires

All participants were offered quarterly safer conception counseling visits, completed a sexual behavior diary, and completed a face-to-face questionnaire administered at study enrollment and exit. A separate STI questionnaire with questions regarding STI symptoms, medical/STI history, and sexual/relationship history was administered to participants who completed enrollment STI testing.13 Questionnaires were administered by research assistants in Runyankole or English. Data were collected and managed using REDCap electronic data capture tools hosted at Partners Healthcare.14

Laboratory Testing

Sexually transmitted infection laboratory screening began in June 2018 as a substudy, and all new enrollees to the parent study were invited to participate. Participants provided blood to screen for T. pallidum via a rapid immunochromatographic test confirmed by rapid plasma reagin. They had the option of self-collected or nurse-collected vaginal swabs to screen for C. trachomatis, N. gonorrhoeae, and T. vaginalis via nucleic acid amplification testing with GeneXpert. All participants completed β-human chorionic gonadotropin urine pregnancy testing and rapid HIV testing.

STI Treatment

Participants with a positive STI test result were notified and treated the same day or within days (same-day testing was not always feasible given power instability and participant time constraints). Participants with STI symptoms alone were not treated. All STI treatment was in accordance with Ugandan Ministry of Health STI treatment guidelines.9 Participants with a positive syphilis immunochromatographic test result received treatment regardless of rapid plasma reagin owing to its variability in different conditions15 and were given partner notification (PN) cards outlining the need for presumptive partner treatment with benzathine penicillin. Participants with chlamydia, gonorrhea, and trichomoniasis diagnoses received patient-delivered partner medications (PDPM) to give to sexual partner(s) and PN cards, which outlined the partner exposure, need for medical evaluation, and the purpose of PDPM.

Measures

The primary measure of interest of this substudy was the laboratory diagnosis of at least one STI. Pertinent covariates included age, number of sexual partners in the past 3 months, condom use at last sexual encounter, number of stillbirths, and a history of STIs, which were obtained from the questionnaires.

Statistical Analysis

Descriptive statistics were calculated by proportion (percentage) or median (interquartile range [IQR]). We used the Fisher exact test to assess the association between categorical variables and STI. In constructing the multivariable logistic model, we initially included all variables with a univariable P value ≤0.20. We then removed the variable with the highest P value >0.05, reran the reduced model, and repeated this process until all remaining variables had a P value ≤0.05. We considered this approach with the goal of maximizing the parsimony of our model in the setting of low absolute numbers of STI from the limited sample size.16 Data were analyzed with STATA V15.

Ethics

All participants provided voluntary informed consent at enrollment. Ethical approval was provided by the research ethics boards of Massachusetts General Hospital, University of Alabama at Birmingham, and Mbarara University of Science and Technology. Consistent with national guidelines, approvals were obtained from the Uganda National Council for Science and Technology and the Research Secretariat in the Office of the President.

RESULTS

Participant Sociodemographic Characteristics

Out of the 131 women who met parent study inclusion criteria, all 94 participants who were offered STI substudy participant consented. Among the 94 study participants who completed enrollment STI screening, the median age was 30 (IQR, 26–34) years. Most participants (87 [93%]) were married or living as married with their primary pregnancy partner. Twenty-six women (28%) reported a prior sexual partner with STI. Among 92 women reporting sexual intercourse in the prior 3 months, 59 (64%) reported condom use at last sexual encounter with her primary partner. Almost all women in this sample (94%) chose to initiate PrEP. Most participants (91 [97%]) chose to self-collect vaginal swabs (Table 1).

T1
TABLE 1:
Demographics Among 94 Women at Risk for HIV Exposure, Considering PrEP, and Seeking Safer Conception Care—With STI Compared With Those Without STI

STI Participant Prevalence and Treatment

Among the 94 women screened for STI, 23 (24%) had at least 1 STI including 12 (13%) with chlamydia, 2 (2%) with gonorrhea, 6 (6%) with trichomoniasis, 6 (6%) with syphilis, and 3 (3%) with STI coinfection (Fig. 1). All participants with STI received treatment at the study site.

F1
Figure 1:
Sexually transmitted infection prevalence among 94 women at risk for HIV exposure, considering PrEP, and seeking safer conception care. *Two participants with chlamydia/syphilis coinfection and 1 participant with chlamydia/trichomoniasis coinfection.

STI Partner Notification and Treatment

Among the 23 participants with STI, 22 (96%) of 23 were provided with PN cards and 16 (84%) of 19 eligible participants were given PDPM.

Factors Associated With STI

In the adjusted model, younger age (adjusted odds ratio [AOR], 0.87 for each year; 95% confidence interval [CI], 0.77–0.99), prior stillbirth (AOR, 5.04; 95% CI, 1.12–22.54), and not feeling vulnerable to HIV (AOR, 16.33; 95% CI, 1.12–237.94) remained significantly associated with having a current STI (Table 2).

T2
TABLE 2:
Factors Associated With Enrollment STI Using Unadjusted and Adjusted Multivariable Linear Regression Among 94 Women at Risk for HIV Exposure, Considering PrEP, and Seeking Safer Conception Care

DISCUSSION

To our knowledge, this is one of the first studies in SSA to demonstrate STI prevalence among women desiring pregnancy, at risk for HIV exposure, and seeking safer conception care. We describe a high, 24% STI burden among a population of women at risk for HIV with plans for pregnancy. Given the implications of undiagnosed STI for maternal and child health, these data highlight the importance of implementing STI screening for women and partners as part of safer conception care.

Our data demonstrate a high STI prevalence in Uganda similar to that of other areas in Eastern and Southern Africa. The VOICE trial, assessing topical and oral PrEP among 4843 women, found a 20% prevalence of chlamydia, gonorrhea, trichomoniasis, and syphilis in South Africa, Uganda, and Zimbabwe.19 In addition, the ECHO trial, assessing HIV risk among women using contraception, found an 18% chlamydia and a 5% gonorrhea prevalence across South Africa, Zambia, and Kenya.20

We found several factors associated with STI prevalence. We observed an association between STI and prior stillbirth, despite women with STI being younger, with fewer pregnancies, fewer livebirths, and fewer miscarriages. Syphilis accounts for 11% of stillbirths in SSA,21 and although our cohort was small and not powered to determine the effect of any one STI, our findings support the correlation between stillbirth and syphilis as well as adverse pregnancy outcome and STI found across the world.22 Uganda has a high prevalence of both syphilis and stillbirth, and although Ugandan clinical guidelines include antenatal syphilis point-of-care (POC) screening and treatment, in 2018 only 57% of antenatal clinic attendees received first-visit, laboratory screening for syphilis.9,23 The profound impact of stillbirth, precipitated in part by curable STIs, strongly argues for the prioritization of antenatal and preconception STI screening.

A history of STI is a strong predictor of future STI,24,25 but in our cohort, prior self-reported STI was significantly associated with a lack of current STI. The Carraguard study, a prospective HIV prevention trial of nearly 15,000 South African women found that baseline STI was significantly associated with incident STI.25 Reasons for our differing results may include misdiagnosis with the STI syndromic approach, protective immunity secondary to chlamydia,26 and women with prior STI receiving effective counseling to prevent STI recurrence.

This analysis is limited by a small, cross-sectional dataset, although it is strengthened by high-quality laboratory assessment.

Our findings highlight a high STI burden not previously described among Ugandan women at risk for HIV exposure and planning for pregnancy. Rapid advancements in STI POC technology provide hope for appropriate STI diagnoses, but as demonstrated by syphilis, even when POC testing is available, implementation can lag. Thus, we need to prioritize both the development and dissemination of POC diagnostics. Laboratory-based STI diagnostics will allow a greater emphasis on PN and a better understanding of how to break the transmission cycle. Understanding STI epidemiology and risk factors is the first step toward designing interventions for STI screening and treatment, especially as safer conception and PrEP programs expand across SSA.

REFERENCES

1. Rowley J, Vander Hoorn S, Korenromp E, et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: Global prevalence and incidence estimates, 2016. Bull World Health Organ 2019; 97:548–562P.
2. Sexton J, Garnett G, Rottingen JA. Metaanalysis and metaregression in interpreting study variability in the impact of sexually transmitted diseases on susceptibility to HIV infection. Sex Transm Dis 2005; 32:351–357.
3. Gomez GB, Kamb ML, Newman LM, et al. Untreated maternal syphilis and adverse outcomes of pregnancy: A systematic review and meta-analysis. Bull World Health Organ 2013; 91:217–226.
4. Guideline on When to Start Antiretroviral Therapy and on Pre-exposure Prophylaxis for HIV. Switzerland: WHO/UNAIDS, 2015.
5. Matthews LT, Beyeza-Kashesya J, Cooke I, et al. Consensus statement: Supporting safer conception and pregnancy for men and women living with and affected by HIV. AIDS Behav 2018; 22:1713–1724.
6. Group TWB. Fertility rate, total (births per woman). 2018. Available at: https://data.worldbank.org/indicator/SP.DYN.TFRT.IN. Accessed August 3, 2018.
7. UNAIDS. Uganda Country Fact Sheet 2016. 2018. Available at: http://www.unaids.org/en/regionscountries/countries/uganda. Accessed January 30, 2018.
8. UNAIDS. When women lead change happens: women advancing the end of AIDS. 2017. Available at: https://www.unaids.org/en/resources/documents/2017/when-women-lead-change-happens. Accessed February 20, 2019.
9. Uganda Clinical Guidelines 2016: National Guidelines for Management of Common Conditions. Uganda: Ministry of Health Uganda, The Republic of Uganda, 2016.
10. Liu AY, Cohen SE, Vittinghoff E, et al. Preexposure prophylaxis for HIV infection integrated with municipal- and community-based sexual health services. JAMA Intern Med 2016; 176:75–84.
11. Molina JM, Capitant C, Spire B, et al. On-demand preexposure prophylaxis in men at high risk for HIV-1 infection. N Engl J Med 2015; 373:2237–2246.
12. Matthews LT, Tukwasibwe D, Najjuma A, et al. Who seeks safer conception care in Uganda? A call for client-centered care for men and women affected by HIV #TUPEC476. In: Paper presented at: International AIDS Society Scientific Meeting; July 2019. Mexico City, Mexico, 2019.
13. Kaida A, Dietrich JJ, Laher F, et al. A high burden of asymptomatic genital tract infections undermines the syndromic management approach among adolescents and young adults in South Africa: Implications for HIV prevention efforts. BMC Infect Dis 2018; 18:499.
14. Harris PA, Taylor R, Minor BL, et al. The REDCap consortium: Building an international community of software platform partners. J Biomed Inform 2019; 95:103208.
15. Hamill MM, Mbazira KJ, Kiragga AN, et al. Challenges of rapid plasma reagin interpretation in syphilis screening in Uganda: Variability in Nontreponemal results between different laboratories. Sex Transm Dis 2018; 45:829–833.
16. Heinze G, Wallisch C, Dunkler D. Variable selection—a review and recommendations for the practicing statistician. Biom J 2018; 60:431–449.
17. Bunting L, Boivin J. Development and preliminary validation of the fertility status awareness tool: FertiSTAT. Hum Reprod 2010; 25:1722–1733.
18. Pulerwitz J, Gortmaker SL, De Jong W. Measuring sexual relationship power in HIV/STD research. Sex Roles 2000; 42(7/8):637–620.
19. Chirenje ZM, Gundacker HM, Richardson B, et al. Risk factors for incidence of sexually transmitted infections among women in a human immunodeficiency virus chemoprevention trial: VOICE (MTN-003). Sex Transm Dis 2017; 44:135–140.
20. #IAS2019: High HIV & STI rates in ECHO analyses [press release]. Health E-News 2019.
21. Lawn JE, Blencowe H, Waiswa P, et al. Stillbirths: Rates, risk factors, and acceleration towards 2030. Lancet 2016; 387:587–603.
22. Goldenberg RL, McClure EM, Saleem S, et al. Infection-related stillbirths. Lancet 2010; 375:1482–1490.
23. WHO/UNAIDS. WHO, Global Health Observatory Data Repository. Antenatal care (ANC) attendees tested for syphilis at first ANC visit, Data by country. Available at: http://apps.who.int/gho/data/node.main.A1358STI. Accessed August 1, 2019.
24. Abbai NS, Wand H, Ramjee G. Sexually transmitted infections in women participating in a biomedical intervention trial in Durban: Prevalence, Coinfections, and risk factors. J Sex Transm Dis 2013; 2013:358402.
25. Wand H, Ramjee G. Biological impact of recurrent sexually transmitted infections on HIV seroconversion among women in South Africa: Results from frailty models. J Int AIDS Soc 2015; 18:19866.
26. Batteiger BE, Xu F, Johnson RE, et al. Protective immunity to chlamydia trachomatis genital infection: Evidence from human studies. J Infect Dis 2010; 201(Suppl 2):S178–S189.
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