High prevalence of sexually transmitted infections among women screened for a contraceptive intravaginal ring study,Kisumu,Kenya,2014

Abstract

We assessed prevalence and correlates of bacterial vaginosis (BV) and sexually transmitted infections (STIs) including herpes simplex virus type 2 (HSV-2), gonorrhoea (GC), syphilis (SYP), Chlamydia (CT) and HIV among Kenyan women aged 18–34 years who were screened for a contraceptive intravaginal ring study. Women provided demographic, behavioural and medical information, and underwent medical evaluation, including a pelvic exam. We computed crude and adjusted prevalence ratio (aPR) and 95% confidence interval (CI) using log-binomial regression. Of 463 women screened, 457 provided laboratory specimens and were included in the analysis. The median age was 25 years, interquartile range (21–28), and 68.5% had completed primary or lower education. Overall, 72.2% tested positive for any STI or BV. Point prevalence was 55.6, 38.5, 3.9, 2.0, 4.6, and 14.7% for HSV-2, BV, GC, SYP, CT, and HIV, respectively. Co-infection with HSV-2, BV, and HIV occurred in 28 (6.1%) participants. Having ≥1 STI/BV was associated with younger age at first sex (≤13 versus 17–19 years, aPR=1.27, 95% CI 1.07–1.51), history of exchange sex (aPR = 2.05, 95% CI 1.07–3.92), sexual intercourse in the past seven days (aPR = 1.17, 95% CI 1.01–1.36), and older age (30–34 versus 18–24 years, aPR = 1.26, 95% CI 1.06–1.48). STI/BV diagnosis was less likely for women reporting one lifetime sexual partner compared to women with ≥4 lifetime sexual partners (aPR = 0.70, 95% CI 0.54–0.92). Combination prevention approaches (biomedical, behavioural, social, and structural) tailored to women with diverse risk profiles may help mitigate STI/BV prevalence in this setting.

Keywords

Women human immunodeficiency virus herpes simplex virus

Introduction

A more robust commitment to sexually transmitted infections (STIs) prevention, diagnosis, and treatment is needed given that more than one million new STIs are acquired globally every day.¹ Worldwide, Chlamydia (CT) accounts for 131 million of those new STIs, gonorrhoea (GC) for 78 million, syphilis (SYP) for 5.6 million, and trichomoniasis for 143 million cases annually.¹ Left untreated, STIs can lead to severe acute and chronic sequelae, e.g. infertility, pelvic inflammatory disease, unfavourable pregnancy and perinatal outcomes.² Importantly, STIs may also facilitate the risk of sexual transmission and acquisition of HIV among women in sub-Saharan Africa (SSA).^3–5 Condoms are theoretically highly effective in preventing STIs and unintended pregnancy; however, inconsistent use makes these less effective in protecting against either.⁶ Women not using condoms with hormonal contraceptive methods (dual use) may be at increased risk of infection. Lack of STI prevention education, absence of routine STI screening, and limited access to STI services may lead to lower STI testing among contraceptive-using women.

STIs, especially HIV, overall are a leading cause of disease in Kenya.⁷ Emphasis on HIV, however, may minimize attention given to other STIs.⁷ STI control is predominately subsumed within HIV programme priorities. STI control relies on syndromic management and diagnostic testing is largely unavailable. To our knowledge, Kenya’s national prevalence and incidence data for STIs other than HIV are unavailable. Data collection typically includes self-report of genital ulcers and abnormal genital discharge as opposed to diagnosis of specific STIs, and health programmes rely on such syndromic surveillance and management rather than more specific testing.

The 2012 Kenya AIDS Indicator Survey showed that 0.9% of adolescents and adults aged 15–64 years of age self-reported having an STI (based on presence of genital ulcers and abnormal genital discharge) in the past 12 months, and that among those diagnosed with an STI, about 70% indicated that they had received treatment.⁷ A prospective cohort study conducted in Mombasa, Kenya, found an association between HIV and trichomoniasis among women.⁸ Some studies conducted in SSA suggested that prevalent genital herpes simplex virus type 2 (HSV-2) may increase acquisition of a new HIV infection. A longitudinal analysis of a cohort of high-risk Zimbabwean and Ugandan women showed that the population attributable risk of prevalent HSV-2 on HIV acquisition remained chronically high at approximately 50%.⁹ This study also demonstrated a causal link between HSV-2 infection and disruption of the vaginal microbiota leading to a higher prevalence of bacterial vaginosis (BV) among Kenyan women with HSV-2.⁹ BV is known to expedite lower genital tract HIV shedding and transmission.^10–12 It has been shown to diminish vaginal acidity and lactic acid levels, thereby increasing susceptibility to other STIs in addition to facilitating innate immune response associated with acquisition of HIV.^13–16 Laboratory studies have demonstrated that CT infection of endocervical endothelial cells may facilitate HIV crossing the mucosal barrier and targeting the underlying cells.¹³

A systematic review of epidemiological studies conducted from 1986 to 2006 in SSA countries showed an association between HIV infection and number of sex partners, history of paid sex (transactional or commercial sex), and HSV-2 infection or other STIs.¹⁷ A more recent review of the socio-demographic and behavioural risk factors of female sex workers in SSA demonstrated linkage of HIV risk to limited economic opportunities, multiple dependents, marital disruption, low education, gender-based violence, erratic condom use, higher number of clients, heavy episodic drinking, duration of sex work ≥3 years, STI co-infection, and engaging in anal sex.¹⁸

Global STI and HIV studies typically focus on high-risk individuals such as antenatal clinic attendees, sex workers, and men who have sex with men, while information on women from the general population is limited.¹⁹ Thus, our objectives were to (1) describe the baseline prevalence of SYP, GC, CT, HSV-2, HIV, and BV, among contraceptive-using women from the general female population screened for a contraceptive intravaginal ring study; and (2) identify behavioural and demographic factors associated with prevalent STI or BV infections, including HIV.

Material and methods

Ethical statement

The Scientific Ethical Review Unit of the Kenya Medical Research Institute; an Institutional Review Board for the US Centers for Disease Control and Prevention; and the Kenya Pharmacy and Poisons Board reviewed and approved the study protocol, consent forms, and data collection instruments. This trial is registered with ClinicalTrials.gov, number NCT02529683. Prior to administering a brief pre-screening assessment (described below), volunteers completed a verbal informed consent process in English, Kiswahili, or Dholuo, the three most common languages in our study’s geographical setting. Volunteers did not receive any incentives for completing the brief pre-screening questionnaire. Women proceeding to a more detailed behavioural and medical screening completed written informed consent, also available in each of the aforementioned languages, before initiation of data collection, medical procedures, and testing. Women taking part in the in-depth data and specimen collections received a bar of soap, 500 Kenya Shillings (approximately $5 USD) for transport, feminine sanitary pads, and a treated malaria bed net.

Setting and design

Between April 2014 and November 2014, we undertook recruitment, screening, and enrolment for an open-label, single group observational study of the contraceptive intravaginal ring, NuvaRing®. Study procedures have been described elsewhere.²⁰ Contraceptive-using women 18–34 years of age were drawn from the general population as opposed to specific key populations at increased risk of HIV or other STIs.

Our catchment area included Kisumu and surrounding villages within a 150-km radius. In brief, with the assistance of ten community health workers, we used convenience sampling to conduct venue-based recruitment in village gathering places and family planning clinics. In addition, participant referral without incentive occurred. Within our recruitment venues, the study staff delivered a study overview and obtained verbal consent privately from the interested volunteers in their preferred language (English, Swahili, or Dholuo) before administering a brief pre-screening computer-assisted personal interview (CAPI). Women who met the pre-screening criteria listed in Table 1 presented for a clinic-based screening visit, which involved an in-depth behavioural and medical eligibility assessment.

Table 1.

Eligibility criteria for the Kisumu Contraceptive Intravaginal Ring Study, Kisumu, Kenya, 2014.

Pre-screening (CAPIa assessment)
Fluent in English, Swahili, or Dholuo 18–34 years of age Able to provide standard national documentation of age (e.g. identity card, birth notification/certificate) for verification Resident of the Kisumu catchment area Has no plans to relocate outside of the catchment area within the next 12 months Vaginal intercourse within the past three months on more than one occasion Self-reported never receiving an HIV-positive test result	Injectable depot medroxy-progesterone acetate (DMPA) or oral contraceptive pill (OCP) use in the past three months Able to provide family planning or medical clinic documentation of DMPA or OCP use Not breastfeeding or within three months of parturition at screening Willing to switch from DMPA or OCP to NuvaRing® for six monthsb Willing to undergo periodic pelvic examination, monthly pregnancy testing, quarterly HIV testing, and testing for STIsc at baseline screening and study exit
Screening (ACASId and medical assessmente)
Met all pre-screening criteria Medically healthy with no contraindications for NuvaRing® use (e.g. thrombophlebitis or thromboembolic disorders, cerebral vascular or coronary artery disease, valvular heart disease with thrombogenic complications, severe hypertension, diabetes with vascular involvement, headaches with focal neurological symptoms) Tested negative for pregnancy and HIV Agreed to take part in study follow-up

^aComputer-assisted personal interview (CAPI) was administered by recruitment and community outreach staff.

^bSix-month NuvaRing® use also includes medical evaluation, such as collection of medical history, physical and pelvic examinations.

^cAssessment of sexually transmitted infections (STIs) included bacterial vaginosis (BV) testing. While BV is not classified as a sexually transmitted infection (STI), it increases a woman’s risk for acquiring HIV and other STIs.

^dAudio computer-assisted self-interview (ACASI) took place in a clinic’s computer room dedicated to participant use. All computers were equipped with headphones and privacy screens. A staff person was stationed in the room to assist participants.

^eNuvaRing® does not prevent against HIV or other STIs, so condom use was highly encouraged.

Before initiating in-depth screening procedures, all women provided written informed consent on the second more comprehensive form describing study follow-up and contraceptive ring use. Collection of demographic and behavioural information took place using audio computer-assisted self-interview (ACASI). To facilitate computer use, all women completed a self-directed, hands-on tutorial before beginning the ACASI questionnaire. A study clinician administered a medical evaluation CAPI, which included questions on three symptoms potentially indicative of an STI (currently having genital ulcers anywhere on the vagina and/or vulva, abnormal or smelly vaginal discharge, or pain during sexual intercourse), and performed a general physical examination as well as a pelvic examination. We used the collected venous blood samples for rapid and confirmatory testing of HIV using Determine HIV-1/2 Ag/Ab Combo test and Biorad 3^rd Gen enzyme-linked immunosorbent assay (ELISA), testing of HSV-2 using Kalon IgG HSV-2 ELISA, a screening Plasma Reagin and confirmatory SD Bioline SYP testing, and performed real-time polymerase chain reaction testing of GC and CT using COBAS AMPICLOR/COBAS Taqman assay on self-collected vaginal swab samples. We also performed BV assessment using Nugent Scoring (Gram stain of vaginal swab) and tested the collected urine samples for pregnancy using SAS Ultra human chorionic gonadotropin test. Rapid HIV testing and delivery of results as well as pre- and post-test counselling followed Kenyan Ministry of Health guidelines.²¹

Women who tested positive for SYP, GC, or CT received free treatment, which was consistent with national and World Health Organization guidelines, and were encouraged to invite their sexual partners to the study clinic for free STI testing and treatment. Women testing positive for HSV-2 did not receive treatment unless they had active skin infection with vesicles. Women who tested HIV-positive received additional counselling, CD4 and viral load testing, and referred to a patient support centre for appropriate HIV care services. Women who tested positive for pregnancy at screening received referrals to local antenatal care clinics and services.

Statistical analysis

We descriptively characterized women who completed the in-depth screening by frequencies and percentages for demographic, sexual history, vaginal health, and recent behavioural variables.

The dependent variable for our analysis combined laboratory screening test result for any STI (SYP, GC, CT, HSV-2, HIV) or BV and is henceforward referred to as STI/BV. Employing generalized linear modelling framework and log-binomial regression, we modelled occurrence of STI/BV and compared it among categories of explanatory variables using crude and multivariable-adjusted prevalence ratio (aPR) and 95% confidence interval (CI). Variables significant at the 0.2 level in univariable analysis underwent further examination using a multivariable regression model. Potential confounding effect of each covariate and two-way interactions was addressed and we obtained final variable selection by applying backward elimination and retaining predictors significant at the 0.05 level. The analyses were completed using STATA version 14.1 (STATA Corporation, College Station, Texas, USA).

Results

Characteristics of the study population

Of 692 pre-screened women, 463 completed the in-depth screening. Our analysis was restricted to 457 women who provided laboratory specimens. Among the 457 women, 47.5% were 18–24 years of age, 68.5% had completed primary or less education, including no schooling. Approximately one-third (31.2%) reported having been inherited (a traditional cultural practice - see Table 2). An estimated 63.8% reported being unemployed (Table 2). Among the current symptoms potentially indicative of an STI/BV, which were provided by 456 out of the 457 screeners, genital ulcers were self-reported by 2.4%, abnormal or smelly discharge by 3.1%, and pain during sexual intercourse by 6.1% (data not shown).

Table 2.

Demographic and behavioural characteristics of women at screening (n = 457), by sexually transmitted infection or bacterial vaginosis (STI/BVa) status, for the Kisumu Contraceptive Intravaginal Ring Study, Kisumu, Kenya, 2014.

Variable	Total(N = 457) n (%)	STI/BV-positive (n = 330) n (%)	STI/BV-negative (n = 127) n (%)	STI/BV prevalence	Prevalence ratio (95% CI)	p-value
Age at screening (years)b						<0.001
18–24	217 (47.5)	139 (42.1)	78 (61.4)	64.1	Ref
25–29	166 (36.3)	126 (38.2)	40 (31.5)	75.9	1.18 (1.04, 1.35)
30–34	74 (16.2)	65 (19.7)	9 (7.1)	87.8	1.37 (1.20, 1.56)
Marital statusb						0.007
Single	81 (18.5)	51 (16.2)	30 (24.4)	63.0	Ref
Married/cohabiting	303 (69.3)	218 (69.4)	85 (69.1)	71.9	1.14 (0.95, 1.37)
Separated/widowed/divorced	53 (12.1)	45 (14.3)	8 (6.5)	84.9	1.35 (1.10, 1.65)
Ever been inheritedc						0.799
No	253 (68.8)	188 (69.1)	65 (67.7)	74.3	Ref
Yes	115 (31.2)	84 (30.9)	31(32.3)	73.0	0.98 (0.86, 1.12)
Highest education completedb						0.013
Primary or less	311 (68.5)	236 (72.2)	75 (59.1)	75.9	1.19 (1.04, 1.37)
Secondary or more	143 (31.5)	91 (27.8)	52 (40.9)	63.6	Ref
Employment status						0.666
Unemployed	287 (63.8)	208 (64.4)	79 (62.2)	72.5	1.03 (0.91, 1.16)
Employed	163 (36.2)	115 (35.6)	48 (37.8)	70.6	Ref
Age at first sex (years)b						0.068
13 or less	79 (21.3)	63 (24.3)	16 (14.3)	79.7	1.24 (1.05, 1.48)
14–16	126 (34.0)	86 (33.2)	40 (35.7)	68.3	1.06 (0.89, 1.27)
17–19	128 (34.5)	82 (31.7)	46 (41.1)	64.1	Ref
20+	38 (10.2)	28 (10.8)	10 (8.9)	73.7	1.15 (0.91, 1.45)
History of unwanted or forced sexb						0.049
No	227 (65.4)	152 (62.3)	75 (72.8)	67.0	Ref
Yes	120 (34.6)	92 (37.7)	28 (27.2)	76.7	1.14 (1.00, 1.31)
History of exchange sexb						0.073
No	18 (4.7)	8 (3.0)	10 (8.8)	44.4	Ref
Yes	365 (95.3)	261 (97.0)	104 (91.2)	71.5	1.61 (0.91, 2.71)
History of sex during menses						0.437
No	354 (77.8)	253 (76.9)	101 (80.2)	71.5	Ref
Yes	101 (22.2)	76 (23.1)	25 (19.8)	75.2	1.05 (0.92, 1.19)
Abnormal vaginal bleeding in the past 12 months						0.690
No	354 (78.1)	254 (77.7)	100 (79.4)	71.8	Ref
Yes	99 (21.9)	73 (22.3)	26 (20.6)	73.7	1.03 (0.89, 1.17)
No. of lifetime sexual partnersc						0.005
1	60 (16.0)	35 (13.3)	25 (22.5)	58.3	0.73 (0.58, 0.92)
2–3	193 (51.6)	131 (49.8)	62 (55.9)	67.9	0.85 (0.74, 0.97)
≥4	121 (32.4)	97 (36.9)	24 (21.6)	80.2	Ref
No. of partners in the past three months						0.213
1	269 (82.8)	186 (81.2)	83 (86.5)	69.1	Ref
2+	56 (17.2)	43 (18.8)	13 (13.5)	76.8	1.11 (0.94, 1.31)
Unprotected vaginal or anal sex in the past three months						0.263
No	27 (8.2)	16 (6.9)	11 (11.2)	59.3	Ref
Yes	302 (91.8)	215 (93.1)	87 (88.8)	71.2	1.20 (0.87, 1.66 )
Any HIV-positive partners in the past three months						0.226
No	214 (72.1)	148 (70.1)	66 (76.7)	69.2	Ref
Yes	83 (27.9)	63 (29.9)	20 (23.3)	75.9	1.10 (0.94, 1.28)
Any partners of unknown HIV status in the past three months						0.428
No	147 (49.0)	107 (50.5)	40 (45.5)	72.8	Ref
Yes	153 (51.0)	105 (49.5)	48 (54.5)	68.6	0.94 (0.81, 1.09)
Cleaned inside the vagina (i.e. douching) in the past three months						0.831
No	150 (33.6)	110 (33.8)	40 (32.8)	73.3	Ref
Yes	297 (66.4)	215 (66.2)	82 (67.2)	72.4	0.99 (0.88, 1.11)
Sexual activity within the past seven daysb						0.015
No	133 (39.5)	83 (35.0)	50 (50.0)	62.4	Ref
Yes	204 (60.5)	154 (65.0)	50 (50.0)	75.5	1.21 (1.04, 1.41)
Alcohol use in the past 30 days						0.646
No	346 (75.7)	248 (75.2)	98 (77.2)	71.7	Ref
Yes	111 (24.3)	82 (24.8)	29 (22.8)	73.9	1.03 (0.91, 1.17)
Self-reported STIs in the past						0.963
No	262 (70.8)	185 (70.9)	77 (70.6)	70.6	Ref
Yes	108 (29.2)	76 (29.1)	32 (29.4)	70.4	1.00 (0.86, 1.15)
Pregnancy test result						0.851
Negative/other	449 (98.2)	324 (98.2)	125 (98.4)	72.2	Ref
Positive	8 (1.8)	6 (1.8)	2 (1.6)	75.0	1.04 (0.69, 1.56)
Drug use in the past 30 daysd
No	23 (74.2)	15 (65.2)	8 (100.0)	65.2
Yes	8 (25.8)	8 (34.8)	0 (0.0)	100

Sample sizes fluctuate slightly for some variables due to missing data.

CI: confidence interval.

^aAssessment of STIs included testing for syphilis (SYP), gonorrhoea (GC), Chlamydia (CT), herpes simplex virus type 2 (HSV-2), and HIV. While bacterial vaginosis (BV) is not classified as an STI, it increases a woman’s risk for acquiring HIV and other STIs.

^bCandidate explanatory variables selected at 0.2 level for multivariable analysis.

^cA traditional Luo cultural cleansing practice whereby a widow is required to marry a male relative of her late husband (often his brother). Cleansing through sexual intercourse is believed to expel evil spirits. The HIV concerns and stigma have led to the emergence of professional inheritors.²²

^dLow self-report of ever having used drugs; hence, low number of cases included for drug use in the past 30 days.

Overall, 72.2% (330/457) tested positive for STI/BV. The prevalence was 55.6% for HSV-2, 38.5% for BV, 14.7% for HIV, 4.6% for CT, 3.9% for GC, and 2.0% for SYP. Any three simultaneous infections occurred in 33 (7.2%) cases. Co-infection with HSV-2, BV, and HIV occurred in 28 (6.1%) participants. Among 67 (14.7%) women testing HIV-positive, 81.8% tested positive for HSV-2, 48.5% for BV, 10.6% for GC, and 1.5% for SYP (data not shown).

Univariable analysis

Univariable analysis showed that testing positive for our combined STI/BV outcome variable was more likely for women who were 25–29 years of age (PR = 1.18, 95% CI 1.04–1.35) or 30–34 years (PR = 1.37, 95% CI 1.20–1.56) compared to 18- to 24-year-olds, were separated/widowed/divorced (PR = 1.35, 95% CI 1.10–1.65) compared to single, had primary or less education (PR = 1.19, 95% CI 1.04–1.37) compared to those with secondary or more education, had history of unwanted or forced sex (PR = 1.14, 95% CI 1.00–1.31), or were sexually active within the past seven days (PR = 1.21, 95% CI 1.04–1.41) (Table 2).

Testing positive for STI/BV was less likely for women reporting having one (PR = 0.73, 95% CI 0.58–0.92) or 2–3 (PR = 0.85, 95% CI 0.74–0.97) lifetime sexual partners compared to those with ≥4 lifetime sexual partners (Table 2).

Table 3 shows the association between age at screening and BV, HSV-2, and HIV status, separately. Compared to women who were 18–24 years of age, those 25–29 years of age and those 30–34 years of age were more likely to be infected with HSV-2 (PR = 1.40, 95% CI 1.15–1.70 and PR = 1.87, 95% CI 1.55–2.26, respectively) or HIV (PR = 1.84, 95% CI 1.11–3.06 and PR = 1.87, 95% CI 1.01–3.45, respectively).

Table 3.

Association of age with bacterial vaginosis (BV), herpes simplex virus type 2 (HSV-2), and HIV at screening (n = 457) for the Kisumu Contraceptive Intravaginal Ring Study, Kisumu, Kenya, 2014.

Age at screening (years)	Total (N = 457) n (%)	Positive (N = 67) n (%)	Negative (N = 390) n (%)	Prevalence	Prevalenceratio (95% CI)	p-value
By BV status						0.389
18–24	217 (47.6)	78 (44.3)	139 (49.6)	35.9	Ref.
25–29	165 (36.2)	65 (36.9)	100 (35.7)	39.4	1.10 (0.85, 1.42)
30–34	74 (16.2)	33 (18.8)	41 (14.6)	44.6	1.24 (0.91, 1.69)
By HSV-2 status						<0.001
18–24	217 (47.6)	94 (37.0)	123 (60.9)	43.3	Ref.
25–29	165 (36.2)	100 (39.4)	65 (32.2)	60.6	1.40 (1.15, 1.70)
30–34	74 (16.2)	60 (23.6)	14 (6.9)	81.1	1.87 (1.55, 2.26)
By HIV status						0.040
18–24	217 (47.5)	22 (32.8)	195 (50.0)	10.1	Ref.
25–29	166 (36.3)	31 (46.3)	135 (34.6)	18.7	1.84 (1.11, 3.06)
30–34	74 (16.2)	14 (20.9)	60 (15.4)	18.9	1.87 (1.01, 3.45)

CI: confidence interval.

Sample sizes fluctuate slightly for some variables due to missing data.

Table 4.

Adjusted prevalence ratios for sexually transmitted infection or bacterial vaginosis status (STI/BVa) among women screened (n = 323),b Kisumu Contraceptive Intravaginal Ring Study, Kisumu, Kenya, 2014.

Variable	Adjusted prevalence ratio (95% CI)	p-value
Age at screening (years)		0.023
18–24	Ref
25–29	1.15 (0.98, 1.35)
30–34	1.26 (1.06, 1.48)
Age at first sex (years)		0.049
13 or less	1.27 (1.07, 1.51)
14–16	1.08 (0.90, 1.29)
17–19	Ref
20+	1.11 (0.87, 1.42)
History of exchange sex		0.030
No	Ref
Yes	2.05 (1.07, 3.92)
No. of lifetime sexual partners		0.025
1	0.70 (0.54, 0.92)
2–3	0.88 (0.76, 1.02)
4+	Ref
Sexual activity within the past seven days		0.035
No	Ref
Yes	1.17 (1.01, 1.36)

CI: confidence interval.

^aAssessment of STIs included testing for syphilis (SYP), gonorrhoea (GC), chlamydia (CT), herpes simplex virus type 2 (HSV-2), and HIV. While bacterial vaginosis (BV) is not classified as an STI, it increases a woman’s risk for acquiring HIV and other STIs.

^bAnalysis sample reduced from 457 to 323 due to missing responses on one or more explanatory variables.

Multivariable analysis

Testing positive for STI/BV increased with age and was highest among those aged 30–34 years (aPR=1.26, 95% CI 1.06–1.48) compared to those aged 18–24 years; it also showed positive association with early age at first sex (≤13 years) compared to those who initiated sexual activity at 17–19 years (aPR = 1.27, 95% CI 1.07–1.51), history of exchange sex (aPR = 2.05, 95% CI 1.07–3.92), and reporting sexual activity within the past seven days (aPR = 1.17, 95% CI 1.01–1.36) (Table 4). Testing positive for one or more STI/BV was less likely among women reporting one lifetime sexual partner compared to women reporting four or more lifetime sexual partners (aPR = 0.70, 95% CI 0.54–0.92) (Table 4).

Discussion

Among sexually-active, contraceptive-using women screened for a contraceptive intravaginal ring study in Kisumu, Kenya, 72.2% tested positive for STI/BV. This prevalence is consistent with estimates obtained from high-risk women 18–35 years of age surveyed in Beira, Mozambique²³ and other SSA countries.^24,25 Co-infection with BV, HSV-2, and HIV in our sample further supports potential relationships between imbalances in the vaginal microflora that increased risk for either viral or bacterial infections. While prevalence of BV was high among our sample of women, it is somewhat lower than what has been reported for studies targeting high-risk women.^26,27 This may be due to our recruitment approaches and eligibility criteria which focused on current contraceptive use rather than specific risk behaviour characteristics.

We found that HSV-2 was the most prevalent STI in our sample. We observed HSV-2 infection among slightly more than half of the women who completed the in-depth behavioural and medical screening. HSV-2 infection has been independently associated with increased risk of HIV-1 acquisition. Compared to other studies, we observed a higher HSV-2 prevalence that may be explained by age and other differences in study populations. A Kenyan population-based household survey found 42.0% prevalence of HSV-2 among women aged 15–64 years.²⁸ Kisumu Incidence HIV Cohort study, likewise, found HSV-2 and HIV prevalence of 44.8 and 21.2%, respectively, among women.²⁹ In one meta-analysis, HSV-2 was associated with a three-fold risk of HIV-1 among women in the general population.³⁰

Our findings also showed the association between several demographic characteristics and testing positive for STI/BV. The higher likelihood of testing positive for STI/BV among women 30–34 years, as compared to those 18–24 years, may have multiple explanations. Older women of reproductive age may be more likely to have long-standing vaginal infections, including those transmitted via sexual activity due to lasting exposure and limited access to diagnostic and treatment services. These women may be less educated and have less awareness of STI symptoms; therefore, have greater fear of stigmatization and higher rate of underreporting. Later life marital status change (divorce, separation, or widowhood) may lead some women to new sexual networks with high STI prevalence, or situations whereby sex is exchanged for protection, economic, social standing, or other reasons.^31–33

In our sample, the low number of participants reporting symptoms potentially indicative of an STI could mean that women were not willing to report these symptoms or that they may have been asymptomatic. While a comprehensive syndromic assessment was not undertaken, our findings suggest that without aetiologic testing, a syndromic management approach could increase the likelihood of missed STIs for some women.

We observed an increased risk of acquiring STI/BV for those with age of ≤13 years at first sex. Other studies have likewise shown that women who experience first sex at an early age are more likely to have STIs and engage in risky sexual behaviour (e.g. having multiple partners, low use of condoms, and inconsistent or incorrect contraceptive use).³⁴ Early age at first sex is associated with a variety of biological, sociocultural, behavioural, and structural factors that act separately and together to increase poor sexual and reproductive health outcomes for adolescent girls, including unintended pregnancy as well as HIV or other STIs.³⁵ An immature genital tract has been shown to have larger areas of cervical ectopy and trauma during sexual intercourse thereby facilitating infections.³⁶ Moreover, contextual factors (e.g. poverty, gender norms, power relations, menstrual care issues, sexual scripts, relationships with boyfriends) may undervalue the education of females and drive adolescent girls and young women to drop out of school, which then has implications for sexual activity as well as early marriage.³⁵

Lastly, our study suggests that sexual partners were important factors for having STI/BV. Among women in our study, self-reported sexual activity with one lifetime partner presented a 30% less likelihood of testing positive for any STI compared with women with four or more lifetime partners. Other studies have also correlated STI prevalence with sexual practices such as having many lifetime sexual partners.^37–39 A systematic review found that BV was significantly associated with an increased number of male sex partners or having a recent change of male partner.⁴⁰ Moreover, this systematic review indicated that observational data suggest that epidemiologic profile of BV was similar with other STIs.⁴⁰

Prior SSA studies proposed that exchange sex, which may be characterized by transactional sex, plays a key role in women’s risk of acquiring HIV and other STIs.⁴¹ History of intimate partner violence, alcohol use, multiple and concurrent partnerships, and non-use of condoms are plausible documented mechanisms linking transactional sex as well as sex work with HIV and STIs.^42–45 While a recent definition of transactional sex as ‘non-commercial, non-marital sexual relationships motivated by the implicit assumption that sex will be exchanged for material support or other benefits’⁴⁶ is helpful from a research perspective, the motivational, behavioural, and sociocultural complexities associated with it require greater attention. Additional information is needed to understand better the contribution of cultural practices that endorse resource redistribution and reciprocity within the context of courtship to exchange dynamics within a sexual relationship.⁴⁷

Strengths and limitations

Our analysis enabled us to examine demographic, behavioural, and biological correlates of the prevalent STIs. There were several limitations associated with our study. First, our sample size and recruitment approach did not permit generalization of the findings. The limited sample, particularly, restricted the power for assessing factors’ association with STI/BV prevalence among subgroups. Because we targeted women in the general community by behaviour (i.e. use of injectable and oral contraception), rather than by risk category, findings may also not be generalizable to particular risk groups. Nonetheless, our findings suggest that high prevalence of STI/BV is not restricted to key populations and possibly should be of broader public health concern in this setting. Second, while ACASI may have helped reduce the possibility of social desirability and other response bias shown with self-reported sexual risk behaviours, under-reporting may still have occurred. Third, our analysis was cross-sectional, so the direction of associations cannot be determined, and STI incidence information for our sample is absent. Fourth, the HIV, SYP, and HSV-2 serological tests did not distinguish between recent and past infections. Fifth, lack of specificity in our screening questions regarding diagnosis and treatment of BV or any STIs in the past does not permit us to examine whether treatment of primary infections reduces immunity to subsequent secondary infections. Last, correlates of STI/BV provide no evidence in terms of interventions that are likely to be effective in preventing these infections.

Conclusion

STIs are under-addressed diseases in settings with high HIV prevalence, especially among women in the general population. In general, most STIs among women may be asymptomatic; therefore, there is an increased likelihood that they will go untreated. Combination prevention approaches (biomedical, behavioural, social, and structural) tailored to women with diverse risk profiles may help mitigate STI prevalence in this setting. Syndromic management of STIs (prevailing in resource-poor settings) addresses symptomatic manifestations; yet, to alleviate burden of highly prevalent STIs, especially those associated with increased risk of HIV infection, a routine screening with high-quality diagnostics is warranted. Development of reliable, user-friendly, affordable STI point-of-care tests for use in resource-limited countries is needed.

Footnotes

Authors’ contribution

VOO, MAD, EML, RG, BN, VA, GO, and MM contributed substantially to the conceptualization and development of the research study and its implementation.VOO, EML, GO, RG, DAG, and MAD were involved significantly in the analysis and interpretation of data.MM and BN were involved substantially in the acquisition of data and clinical management of the study.All authors have substantially contributed to drafting and revising this work for important intellectual content, approved the final version, and bear responsibility for its accuracy and integrity.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

References

World Health Organization. Sexually transmitted infections (STIs) (Fact sheet), http://who.int/mediacentre/factsheets/fs110/en/ (2016, accessed 18 May 2017).

Maina

Kimani

Anzala

Prevalence and risk factors of three curable sexually transmitted infections among women in Nairobi, Kenya. BMC Res Notes 2016; 9: 193.

Wand

Ramjee

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.

McClelland

Richardson

Hassan

, et al. Improvement of vaginal health for Kenyan women at risk for acquisition of human immunodeficiency virus type 1: results of a randomized trial. J Infect Dis 2008; 197: 1361–1368.

Ward

Rönn

The contribution of STIs to the sexual transmission of HIV. Curr Opin HIV AIDS 2010; 5: 305.

ESHRE Capri Workshop Group. Simultaneous prevention of unintended pregnancy and STIs: a challenging compromise. Hum Reprod Update 2014; 20: 952–963.

National AIDS and STI Control Programme (NASCOP). Kenya AIDS indicator survey 2012: final report. Nairobi: NASCOP, http://nacc.or.ke/wp-content/uploads/2015/10/KAIS-2012.pdf (2014, accessed 5 March 2017).

McClelland

Sangare

Hassan

, et al. Infection with Trichomonas vaginalis increases the risk of HIV-1 acquisition. J Infect Dis 2007; 195: 698–702.

Masese

Baeten

Richardson

, et al. Incident herpes simplex virus type 2 infection increases the risk of subsequent episodes of bacterial vaginosis. J Infect Dis 2014; 209: 1023–1027.

10.

Cohen

Lingappa

Baeten

, et al. Bacterial vaginosis associated with increased risk of female-to-male HIV-1 transmission: a prospective cohort analysis among African couples. PLoS Med 2012; 9: e1001251.

11.

Mitchell

Balkus

Fredricks

, et al. Interaction between lactobacilli, bacterial vaginosis-associated bacteria, and HIV type 1 RNA and DNA genital shedding in U.S. and Kenyan women. AIDS Res Hum Retroviruses 2013; 29: 13–19.

12.

Noguchi

Richardson

Baeten

, et al. Risk of HIV-1 acquisition among women who use different types of injectable progestin contraception in South Africa: a prospective cohort study. Lancet HIV 2015; 2: e279–e287.

13.

Buckner

Amedee

Albritton

, et al. Chlamydia trachomatis infection of endocervical epithelial cells enhances early HIV transmission events. PLoS One 2016; 11: e0146663.

14.

Cherpes

Meyn

Krohn

, et al. Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis. Clin Infect Dis 2003; 37: 319–325.

15.

Hilber

Francis

Chersich

, et al. Intravaginal practices, vaginal infections and HIV acquisition: systematic review and meta-analysis. PLoS One 2010; 5: e9119.

16.

Mitchell

Marrazzo

Bacterial vaginosis and the cervicovaginal immune response. Am J Reprod Immunol 2014; 71: 555–563.

17.

Chen

Jha

Stirling

, et al. Sexual risk factors for HIV infection in early and advanced HIV epidemics in sub-Saharan Africa: systematic overview of 68 epidemiological studies. PLoS One 2007; 2: e1001.

18.

Scorgie

Chersich

Ntaganira

, et al. Socio-demographic characteristics and behavioral risk factors of female sex workers in sub-Saharan Africa: a systematic review. AIDS Behav 2012; 16: 920–933.

19.

Newman

Rowley

Vander Hoorn

, et al. Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS One 2015; 10: e0143304.

20.

McLellan-Lemal

Gust

Gvetadze

, et al. Characteristics of women screened for a contraceptive intravaginal ring study in Kisumu, Kenya, 2014. Res J Womens Health 2016; 3: 1. http://dx.doi.org/10.7243/2054-9865-3-1.

21.

National AIDS and STI Control Programme (NASCOP). Guidelines on use of antiretroviral drugs for treating and preventing HIV infection: a rapid advice. Nairobi: Ministry of Health, Kenya, http://healthservices.uonbi.ac.ke/sites/default/files/centraladmin/healthservices/Rapid%20Advice%20Booklet%202014%2024%20June%2012%20noon_0.pdf (2014, accessed 17 October 2017).

22.

Agot

Vander Stoep

Tracy

, et al. Widow inheritance and HIV prevalence in Bondo District, Kenya: baseline results from a prospective cohort study. PLoS One 2010; 5: e14028.

23.

Meque

Dube

Feldblum

, et al. Prevalence, incidence and determinants of herpes simplex virus type 2 infection among HIV-seronegative women at high risk of HIV infection: a prospective study in Beira, Mozambique. PLoS One 2014; 9: e89705.

24.

Vandepitte

Bukenya

Weiss

, et al. HIV and other sexually transmitted infections in a cohort of women involved in high-risk sexual behavior in Kampala, Uganda. Sex Transm Dis 2011; 38: 316–323.

25.

Kapiga

Sam

Shao

, et al. Herpes simplex virus type 2 infection among bar and hotel workers in northern Tanzania: prevalence and risk factors. Sex Transm Dis 2003; 30: 187–192.

26.

Francis

Looker

Vandepitte

, et al. Bacterial vaginosis among women at high risk for HIV in Uganda: high rate of recurrent diagnosis despite treatment. Sex Transm Infect 2016; 92: 142–148.

27.

Mukamuyango

Ingabire

Karita

, et al. Prevalence of HIV, sexual transmitted infections and high risk sexual behaviors among female sex workers in Kigali, Rwanda. AIDS Res Hum Retroviruses 2011; 30: A279–A279.

28.

Mugo

Dadabhai

Bunnell

, et al. Prevalence of herpes simplex virus type 2 infection, human immunodeficiency virus/herpes simplex virus type 2 coinfection, and associated risk factors in a national, population-based survey in Kenya. Sex Transm Dis 2011; 38: 1059–1066.

29.

Otieno

Ndivo

Oswago

, et al. Correlates of prevalent sexually transmitted infections among participants screened for an HIV incidence cohort study in Kisumu, Kenya. Int J STD AIDS 2015; 26: 225–237.

30.

Freeman

Weiss

Glynn

, et al. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 2006; 20: 73–83.

31.

Sherman

Harvey

Noell

Are they still having sex?” STIs and unintended pregnancy among mid-life women. J Women Aging 2008; 17: 41–55.

32.

Bodley-Tickell

Olowokure

Bhaduri

, et al. Trends in sexually transmitted infections (other than HIV) in older people: analysis of data from an enhanced surveillance system. Sex Transm Infect 2008; 84: 312–317.

33.

Voeten

Egesah

Varkevisser

, et al. Female sex workers and unsafe sex in urban and rural Nyanza, Kenya: regular partners may contribute more to HIV transmission than clients. Trop Med Int Health 2007; 12: 174–182.

34.

Ramjee

Daniels

Women and HIV in sub-Saharan Africa. AIDS Res Ther 2013; 10: 30.

35.

Oruko

Nyothach

Zielinski-Gutierrez

, et al. ‘ He is the one who is providing you with everything so whatever he says is what you do’: a qualitative study on factors affecting secondary schoolgirls’ dropout in rural Western Kenya. PloS One 2015; 10: e0144321.

36.

Moscicki

A-B

Holland

, et al. Cervical ectopy in adolescent girls with and without human immunodeficiency virus infection. J Infect Dis 2001; 183: 865–870.

37.

Gabster

Mohammed

Arteaga

, et al. Correlates of sexually transmitted infections among adolescents attending public high schools, Panama, 2015. PloS One 2016; 11: e0163391.

38.

de Lima

YAR

Turchi

Fonseca

, et al. Sexually transmitted bacterial infections among young women in Central Western Brazil. Int J Infect Dis 2014; 25: 16–21.

39.

Nankinga

Misinde

Kwagala

Gender relations, sexual behaviour, and risk of contracting sexually transmitted infections among women in union in Uganda. BMC Public Health 2016; 16: 440.

40.

Fethers

Fairley

Hocking

, et al. Sexual risk factors and bacterial vaginosis: a systematic review and meta-analysis. Clin Infect Dis 2008; 47: 1426–1435.

41.

Wamoyi

Stobeanau

Bobrova

, et al. Transactional sex and risk for HIV infection in sub-Saharan Africa: a systematic review and meta-analysis. J Int AIDS Soc 2016; 19: 20992.

42.

Dunkle

Jewkes

Brown

, et al. Gender-based violence, relationship power, and risk of HIV infection in women attending antenatal clinics in South Africa. Lancet 2004; 363: 1415–1421.

43.

Dunkle

Jewkes

Brown

, et al. Transactional sex among women in Soweto, South Africa: prevalence, risk factors and association with HIV infection. Soc Sci Med 2004; 59: 1581–1592.

44.

Jewkes

Dunkle

Nduna

, et al. Factors associated with HIV sero-status in young rural South African women: connections between intimate partner violence and HIV. Int J Epidemiol 2006; 35: 1461–1468.

45.

Onoya

Reddy

Sifunda

, et al. Transactional sexual relationships, sexually transmitted infection risk, and condom use among young Black women in Peri-urban areas of the Western Cape Province of South Africa. J Women’s Health Issues 2012; 22: e277–e282.

46.

Stoebenau

Heise

Wamoyi

, et al. Revisiting the understanding of “transactional sex” in sub-Saharan Africa: a review and synthesis of the literature. Soc Sci Med 2016; 168: 186–197.

47.

Moore

Biddlecom

Zulu

EM.

Prevalence and meanings of exchange of money or gifts for sex in unmarried adolescent sexual relationships in sub-Saharan Africa. Afr J Reprod Health 2007; 11: 44.