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. Author manuscript; available in PMC: 2016 Jan 12.
Published in final edited form as: Int J STD AIDS. 2014 May 8;26(4):225–237. doi: 10.1177/0956462414532447

Correlates of prevalent sexually transmitted infections among participants screened for an HIV incidence cohort study in Kisumu, Kenya

Fredrick Odhiambo Otieno 1, Richard Ndivo 1, Simon Oswago 1, Sherri Pals 2, Robert Chen 2, Timothy Thomas 2, Ernesta Kunneke 3, Lisa A Mills 2, Eleanor McLellan-Lemal 2
PMCID: PMC4709839  NIHMSID: NIHMS748359  PMID: 24810218

Abstract

Background

We determined the prevalence of four sexually transmitted infections and the demographic and behavioural correlates associated with having one or more sexually transmitted infections among participants in an HIV incidence cohort study in Kisumu, western Kenya.

Methods

Participants were enrolled from a convenience sample and underwent aetiologic sexually transmitted infection investigation. Demographic and behavioural information were collected and basic clinical evaluation performed. Multiple regression analysis was done to determine variables associated with having one or more sexually transmitted infections.

Results

We screened 846, 18- to 34-year-olds. One-third had at least one sexually transmitted infection with specific prevalence being, syphilis; 1.6%, gonorrhoea; 2.4%, herpes simplex virus type-2; 29.1%, chlamydia; 2.8%, and HIV; 14.8%. Odds of having any sexually transmitted infection were higher among participants who were women, were aged 20–24 or 30–34 years compared to 18–19 years, had secondary or lower education compared to tertiary education, were divorced, widowed or separated compared to singles, reported having unprotected sex compared to those who did not, reported previous sexually transmitted infection treatment, and tested HIV-positive.

Conclusion

Multiple strategies are needed to address the overall high prevalence of sexually transmitted infections as well as the gender disparity found in this Kenyan population. Structural interventions may be beneficial in addressing educational and socio-economic barriers, and increasing the uptake of health-promoting practices.

Keywords: Kenya, sexually transmitted infection, prevalence, correlates, Kisumu

Introduction

Sexually transmitted infections (STIs) are an important cause of morbidity, especially among African women, whose access to timely diagnosis and treatment is often deficient.14 Adverse sequelae include poor birth outcomes, neonatal and infant infections, ectopic pregnancy, anogenital cancer, infertility, pelvic inflammatory disease, and death.58 In addition, many STIs, in particular herpes simplex virus type 2 (HSV-2), facilitate transmission of human immunodeficiency virus (HIV).915

There are multiple correlates for the acquisition of different STIs, including demographic, behavioural, and biological considerations. With the exception of HSV-2, lower age has been shown to be a risk factor for the acquisition of STIs; younger people are at higher risk of acquiring STIs than are adults.1618 Gender and education have been found to be significant factors in STI acquisition. Kenyan women have a higher prevalence of HSV-2 than do men,19 and a study in Tanzania found that educated women are less likely to be infected with syphilis compared to their uneducated counterparts.20 Number of sexual partners has also been found to be a risk factor, with sexual concurrency21 and sexual networks22 analyses showing that an increasing number of sexual partners is associated with an increased risk of STI acquisition. HIV infection increases the chances of acquiring various STIs and vice versa. A study in Ethiopia found that HIV co-infection predisposes women to getting more ulcerative STIs, especially HSV-2, as well as to failing STI treatment.27

In January 2007, Kenya Medical Research Centre (KEMRI)/Centers for Disease Control and prevention (CDC) initiated an HIV incidence cohort study to prepare for future community-based HIV vaccine or other prevention trials among young adults in Kisumu. The purpose of this analysis was to use data from the screening visit for this cohort to determine: (1) overall prevalence of four STIs: syphilis, gonorrhoea, HSV-2, and chlamydia and (2) demographic and behavioural correlates of prevalent STIs.

Methods

Study population

Between January 2007 and March 2009, 1277 participants underwent pre-screening for the Kisumu Incidence Cohort Study (KICoS), an observational prospective cohort study to estimate the incidence of HIV seroconversion and to identify determinants of successful recruitment and retention.28 Healthy adults who were 18–34 years of age, residents of Kisumu, sexually active at least once in the past three months, HIV-negative, and not pregnant were eligible to be screened for study participation. Among the 867 who met eligibility for study consideration, 846 completed study screening. Reasons for not being eligible for study consideration or having not completed screening have been presented in the literature.28

Information regarding study recruitment has been published elsewhere.28 In brief, community engagement, which included setting up a Community Advisory Board and fostering collaboration with community leaders and stakeholders (e.g. chiefs, religious leaders, teachers, persons living with HIV, representatives of community-based organisations and special interest groups), occurred prior to initiating study recruitment in the Kisumu city and bordering districts within 150 kilometres of Kisumu city. Using convenience sampling, two methods were used to recruit study participants: venue-based recruitment and advertisement through study brochures. Recruitment venues included market centres, truck stops, beaches, churches, special interest groups, educational institutions, and HIV voluntary counselling and testing centres. Demographic and behavioural information from screened participants was collected using both staff-administered computer-assisted personal interview (CAPI) and participant self-administered audio computer-assisted self-interview (ACASI). In addition, participants underwent a medical examination which included genital examination for STIs and laboratory testing for gonorrhoea, chlamydia, syphilis, and HSV-2 regardless of symptoms or signs. In addition, rapid HIV test with pre- and post-test counselling was conducted. An appointment was scheduled two weeks thereafter to deliver laboratory results and make available final determination of study eligibility and, if eligible, complete enrolment.

Ethical approval

This study was approved by the KEMRI Scientific Steering Committee and Ethical Review Committee and the CDC Institutional Review Board. All persons interested in study participation provided written informed consent in one of the three languages of their preference (English, Dholuo, or Swahili) to screen for eligibility study enrolment. All persons who took part in the eligibility screening received a standard transport reimbursement of KES 300 (USD 3.50). In addition, they received counselling and treatment for STIs and other common ailments as well as provision of condoms (men and women).

Data analysis

Only participants who completed all screening procedures (n=846) were included in this analysis. Exact binomial confidence intervals were calculated for the prevalence of specific STIs. Initially, a log-binomial model was fit for correlates of STIs but did not converge. Therefore, three logistic regression models were fit for the outcome: acute STIs (chlamydia and gonorrhoea) model, chronic STIs (syphilis and HSV-2) model, and a combined model for both acute and chronic STIs. Unadjusted odds ratios were computed using bivariate analysis while adjusted odds ratios were computed using multiple regression analysis. The multiple regression model included all variables with p<.25 or those suspected to be important in the bivariate model. Data analysis was done using SAS for Windows version 9.2 (SAS, Cary, North Carolina, USA).

Measures

The dependent variable was defined as testing positive for syphilis, gonorrhoea, chlamydia, and/or HSV-2 during the screening visit of the study. Independent variables included gender, circumcision status (for men), age, highest level of education, employment status, marital status, ever inherited (referring to the Luo cultural practice of a widow being inherited by the men next of kin of the deceased husband or another man),29 alcohol use in the past 3 months, age at sexual debut, lifetime number of sex partners, anal sex in the past 3 months, time since last sex, unprotected sex at last sex with main partner, ever treated for an STI, and HIV-seropositive.

Laboratory analysis

Serum syphilis testing was performed using BD MicroVue RPR (Rapid Plasma Reagin) Card test (BD & Company, Baltimore, USA) and all reactive tests confirmed by Serodia® TP-PA Syphilis Test (Fujirebio Inc., Tokyo, Japan). Serum HSV-2 serology was tested using KALON® HSV-2 IgG enzyme-linked immunoassay (ELISA) (Kalon Biologicals Ltd., Surrey, UK) and infection with Chlamydia trachomatis or Neisseriae gonorrhoeae (self-administered vaginal swabs for women and urine for men) was evaluated by qualitative polymerase chain reaction, using COBAS® AMPLICOR CT/NG (Roche Diagnostics, Mannheim, Germany). Real-time parallel rapid HIV testing on whole blood was conducted using UniGold HIV-1/2 (Trinity Biotech, Wicklow, Ireland) and Determine HIV-1/2 (Abbott Labs, Tokyo, Japan) with Bioline (Meridian Life Science Company, Cincinnati, Ohio) used as a tie-breaker.

Results

Demographic characteristics

Among the 846 persons who completed all screening procedures, women and circumcised men accounted for 424 (50.4%) and 167 (19.8%) of the participants, respectively. The median age of participants was 22.0 years (range 18–34 years) with 62.6% being 20–24 years of age. The majority (81.4%) were Christian, and more than half (61.2%) of the participants had never been married. Of the 93.5% who had attended school, 69.8% had more than primary education. Those who were students at the time of screening accounted for 19.1% of the participants (Table 1).

Table 1.

Demographic characteristics of participants completing KICoS screening in Kisumu, Kenya (2007–2008).

Characteristic (n = 846) n/N Percentage
Gender/male circumcision statusa
 Women 424/842 50.4
 Uncircumcised men 251/842 29.8
 Circumcised men 167/842 19.8
Age, years
 18–19 105/846 12.4
 20–24 530/846 62.6
 25–29 149/846 17.6
 30–34 62/846 7.3
Religion
 Roman catholic 318/845 37.6
 Protestant or other Christian 370/845 43.8
 Muslim 27/845 3.2
 Nomiyab 45/845 5.3
 Other 60/845 7.1
 No religion 25/845 3.0
Marital status
 Never married 515/842 61.2
 Married or living as married 286/842 34.0
 Divorced/separated/widowedc 41/842 4.9
Level of education
 Primary or belowc 254/842 30.2
 Secondary 311/842 36.9
 Technical 63/842 7.5
 College or university 214/842 25.4
Currently employed
 No 440/844 52.0
 Yes 404/844 47.8
Occupation
 Farmer 28/841 3.3
 Salaried worker 22/841 2.6
 Casual worker 117/841 13.9
 Self-employed 146/841 17.4
 Homemaker 62/841 7.4
 Students not otherwise employed 161/841 19.1
 Not employed 279/841 33.2
 Other 26/841 3.1

Note: Sample sizes fluctuate slightly for some variables due to missing data. Some percentages do not sum to 100 due to rounding.

a

Four men refused to respond to question about circumcision status.

b

Religion of the Luo, the predominant ethnic group in the area.

c

Responses solicited separately then combined for analysis.

STI prevalence

Overall, 272 (32.2%) (95% CI 29.0, 35.4) participants had at least one STI, with women accounting for 75.7% of those infected. Specifically, the prevalence was 1.6% (95% CI 0.8, 2.8) for syphilis (men 0.7% and women 2.6%), 2.4% (95% CI 1.4, 3.6) for gonorrhoea (men 0% and women 4.7%), 29.1% (95% CI 26.0, 32.3) for HSV-2 (men 13.3% and women 44.8%), and 2.8% (95% CI 1.8, 4.2) for chlamydia (men 2.8% and women 2.8%). Prevalence of co-infection with more than one STI was 3.7% (95% CI 2.5, 5.2; men 1.2% and women 6.1%), 3.5% for those with two STIs (men 1.2% and women 5.9%) and 0.1% for those with three STIs (men 0.1% and women 0.2%). HSV-2 was present in all co-infections. Overall HIV prevalence was 14.8% (95% CI 12.2, 17.1) (men 7.8% and women 21.2%) with 10.0% (95% CI 8.1, 12.3) (men 3.1% and women 16.9%) of those screened having both HIV and another STI (Table 2).

Table 2.

Prevalence of specific sexually transmitted infections (STIs) among participants completing KICoS screening in Kisumu, Kenya, by age and gender (2007–2008).

Age (Years) Men
Women
Overall prevalence [95% exact CI]
18–19 (n = 49) 20–24 (n = 254) 25–29 (n = 76) 30–34 (n = 33) Total (n = 422) 18–19 (n = 56) 20–24 (n = 266) 25–29 (n = 73) 30–34 (n = 29) Total (n = 424)
Chlamydia 4.1% 3.4% 0.0% 3.0% 2.8% 1.8% 3.4% 2.7% 0.0% 2.8% 2.8% [1.8%–4.2%]
Gonorrhoea 0.0% 0.0% 0.0% 0.0% 0.0% 5.4% 4.1% 5.5% 6.9% 4.7% 2.4% [1.4%–3.6%]
Syphilis 0.0% 0.4% 1.3% 3.0% 0.7% 3.6% 1.9% 2.7% 6.9% 2.6% 1.6% [0.8%–2.8%]
HSV-2a 6.1% 10.6% 14.5% 42.4% 13.3% 25.0% 42.9% 56.2% 72.4% 44.8% 29.1% [26.0%–32.3%]
HSV-2b 6.3% 11.2% 17.7% 48.3% 14.4% 27.5% 46.5% 60.3% 77.8% 48.4% 31.5% [28.2%–34.9%]
HIV 7.8% 21.2% 14.8% [12.2%–17.1%]
HIV/STI coinfectionc 3.1% 16.9% 10.0% [8.1%–12.3%]
a

Indeterminates counted as negatives.

b

Indeterminates dropped from analysis.

c

Infection with HIV in addition to any other STI.

Multiple logistic regression analysis

The odds of having acute chlamydia or gonorrhoea were higher among women participants compared to circumcised men (Table 3). The odds of having chronic syphilis or HSV-2 (Table 4) were higher among participants who were women compared to circumcised men; were 20–24 or 30–34 years of age compared to 18–19 years; had secondary or lower education compared to college or university education: were divorced, widowed, or separated or were married or living as married compared to being single; reported having unprotected sex at last sex with main partner compared to those who did not; reported previous treatment for STIs compared to those who did not: reported previous STI treatment compared to those who did not; and tested HIV-positive compared to those negative. Conversely, the odds of having a chronic syphilis or HSV-2 were lower among participants who reported recreational drug use compared to those who did not and those who reported engaging in anal sex compared to those who did not.

Table 3.

Correlates of acute Chlamydia Trachomatis (CT) and Neisseriae gonorrhoeae (NG) among participants completing KICoS screening in Kisumu, Kenya (2007–2008).

Variable Have CT/NG
Bivariate
Multiple Regression
n/N (%) OR [95% CI] p Value AOR [95% CI] p Value
Gender/men circumcision status 0.0243 0.0442
 Circumcised men 4/167 (2.4) ref. ref.
 Uncircumcised men 8/251 (3.2) 1.34 [0.40–4.53] 0.6361 1.73 [0.44–6.85] 0.4341
 Women 30/424 (7.1) 3.10 [1.08–8.95] 0.0362 3.78 [1.07–13.36] 0.0392
Age, years 0.9358
 18–19 6/105 (5.7) ref.
 20–24 27/530 (5.1) 0.89 [0.36–2.20] 0.7938
 25–29 6/149 (4.0) 0.69 [0.22–2.21] 0.5346
 30–34 3/62 (4.8) 0.84 [0.20–3.48] 0.8089
Highest level of education 0.0418 0.2058
 College/University 6/214 (2.8) ref. ref.
 Technical 3/63 (4.8) 1.73 [0.42–7.14] 0.4463 2.45 [0.55–10.94] 0.2393
 Secondary 12/311 (3.9) 1.39 [0.51–3.77] 0.5158 1.60 [0.53–4.84] 0.4035
 Primary and below 21/254 (8.3) 3.12 [1.24–7.89] 0.0159 3.00 [0.99–9.12] 0.0532
Currently employed
 No 25/440 (5.7) ref.
 Yes 17/404 (4.2) 0.73 (0.39–1.37)
Marital status 0.0241 0.0919
 Never married 23/515 (4.5) ref. ref.
 Married/Living as married 13/286 (4.6) 1.02 [0.51–2.04] 0.9585 0.51 [0.23–1.15] 0.1038
 Divorced/Widowed/Separated 6/41 (14.6) 3.67 [1.40–9.59] 0.0081 1.55 [0.53–4.55] 0.4254
Ever inherited or been inherited
 No 40/797 (5.0) ref.
 Yes 1/34 (2.9) 0.57 [0.08–4.30] 0.5886
Alcohol use in the past 3 monthsb
 No 21/482 (4.4) ref.
 Yes 21/363 (5.8) 1.35 [0.73–2.51] 0.3458
Recreational drug use in the past 3 monthsb
 No 36/706 (5.1) ref.
 Yes 6/137 (4.4) 0.85 [0.35–2.06] 0.7235
Age of sexual debut, years 0.0724 0.3070
 22–34 4/26 (15.4) ref.
 16–21 18/458 (3.9) 0.23 [0.07–0.72] 0.0121 0.32 [0.08–1.28] 0.1079
 8–15 20/314 (3.4) 0.37 [0.12–1.19] 0.0960 0.53 [0.13–2.13] 0.3687
 <7 0/17 (0.0) undefined 0.9842 undefined 0.9826
Number of lifetime sex partners 0.6866
 0–1 3/111 (2.7) ref.
 2–5 23/429 (5.4) 2.04 [0.60–6.92] 0.2529
 6–10 9/156 (5.8) 2.20 [0.58–8.33] 0.2442
 >10 6/112 (5.4) 2.04 [0.50–8.36] 0.3230
Engaged in anal sex in the past 3 months
 No 31/684 (4.5) ref.
 Yes 10/152 (6.6) 1.48 [0.71–3.10] 0.2933
Time since last sex 0.0072 0.1477
 Never 2/15 (13.3) ref. ref.
 Within three months 27/676 (4.0) 0.27 [0.06–1.26] 0.0955 0.42 [0.08–2.19] 0.3039
 Four to six months 4/58 (6.9) 0.48 [0.08–2.92] 0.4267 0.63 [0.10–4.10] 0.6250
 More than six months 8/57 (14.0) 1.06 [0.20–5.61] 0.9443 1.18 [0.21–6.82] 0.8510
Unprotected sex at last sex with main partner in the past 3 monthsc
 No 9/265 (3.4) ref. ref.
 Yes 32/564 (5.7) 1.71 [0.81–3.64] 0.1629 1.59 [0.72–3.55] 0.2533
Ever treated for STI
 No 34/706 (4.8) ref.
 Yes 8/131 (6.1) 1.29 [0.58–2.84] 0.5348
HIV-positive
 No 35/723 (4.8) ref.
 Yes 7/123 (5.7) 1.19 [0.52–2.73] 0.6885

OR: odds ratio; AOR: adjusted odds ratio; CI: confidence interval; ref: reference group

a

Multiple regression model includes all variables with p <.25 in bivariate model.

b

Any use reported; not necessarily abuse or misuse.

c

Also includes participants who reported unprotected sex with a non-main or primary partner.

Note: Sample sizes fluctuate slightly for some variables due to missing data. Some percentages do not sum to 100 due to rounding.

Table 4.

Correlates of prevalent chronic syphilis and HSV-2 infections among participants completing KICoS screening in Kisumu, Kenya (2007–2008).

Variable HSV-2/Syphilis
Bivariate
Multiple regressiona
n/N (%) OR [95% CI] p Value AOR [95% CI] p Value
Gender/men circumcision status <0.0001 <0.0001
 Women 192/424 (45.3) 5.75 [3.50–9.44] <0.0001 4.99 [2.51–9.91] <0.0001
 Uncircumcised men 36/251 (14.3) 1.16 [0.65–2.07] 0.6065 0.75 [0.36–1.56] 0.4437
 Circumcised men 21/167 (12.6) ref. ref.
Age, years <0.0001 0.0528
 18–19 19/105 (18.1) ref. ref.
 20–24 143/530 (27.0) 1.67 [0.98–2.85] 0.0584 2.19 [1.09–4.42] 0.0282
 25–29 52/149 (34.9) 2.43 [1.33–4.42] 0.0038 2.00 [0.89–4.52] 0.0941
 30–34 35/62 (56.5) 5.87 [2.90–11.89] <0.0001 3.79 [1.42–10.15] 0.0080
Highest level of education <0.0001 0.0028
 Primary and below 118/254 (46.5) 5.12 [3.25–8.06] <0.0001 2.71 [1.43–5.14] 0.0022
 Secondary 92/311 (29.6) 2.48 [1.58–3.90] <0.0001 2.19 [1.24–3.87] 0.0070
 Technical 7/63 (11.1) 0.74 [0.31–1.77] 0.4956 0.70 [0.24–2.10] 0.5273
 College or university 31/214 (14.5) ref. ref.
Currently employed
 No 113/404 (25.7) ref. 0.0139 ref. 0.2524
 Yes 135/440 (33.4) 1.45 [1.08–1.96] 1.28 [0.84–1.96]
Marital status <0.0001 0.0090
 Never married 87/515 (16.9) ref. ref.
 Married or living as married 131/286 (45.8) 4.16 [3.00–5.77] <0.0001 1.87 [1.12–3.11] 0.0163
 Divorced/separated/widowed 28/41 (68.3) 10.60 [5.28–21.27] <0.0001 3.57 [1.30–9.84] 0.0137
Ever inherited or been inherited
 No 221/797 (27.7) ref. ref.
 Yes 22/34 (64.7) 4.78 [2.33–9.82] <0.0001 1.77 [0.64–4.88] 0.2707
Alcohol use in the past 3 monthsb
 No 175/482 (36.3) ref. ref.
 Yes 73/363 (20.1) 0.44 [0.32–0.61] <0.0001 0.76 [0.47–1.21] 0.2477
Recreational drug use in the past 3 monthsb
 No 232/706 (32.9) ref. ref.
 Yes 16/137 (11.7) 0.27 [0.16–0.47] <0.0001 0.36 [0.16–0.84] 0.0177
Age of sexual debut, years 0.2031 0.8661
 22–34 6/26 (23.1) ref. ref. 22–34
 16–21 148/458 (32.3) 1.59 [0.63–4.05] 0.3292 1.68 [0.49–5.80] 0.4082
 8–15 81/314 (25.8) 1.16 [0.45–2.99] 0.7605 1.63 [0.46–5.82] 0.4495
 < 7 4/17 (23.5) 1.03 [0.24–4.35] 0.9726 1.89 [0.30–11.84] 0.4954
Number of lifetime sex partners 0.0236 0.3161
 0–1 35/111 (31.5) ref. ref.
 2–5 144/429 (33.6) 1.10 [0.70–1.72] 0.6848 1.50 [0.83–2.74] 0.1835
 6–10 34/156 (21.8) 0.61 [0.35–1.05] 0.0748 1.95 [0.89–4.25] 0.0946
 > 10 27/112 (24.1) 0.69 [0.38–1.24] 0.2171 2.07 [0.87–4.93] 0.0996
Engaged in anal sex in the past 3 months
 No 216/684 (31.6) ref.
 Yes 30/152 (19.7) 0.53 [0.35–0.82] 0.0042 0.33 [0.18–0.61] 0.0003
Time since last sex 0.0038 0.8725
 Never 5/15 (33.3) ref. ref.
 Within three months 182/676 (26.9) 0.74 [0.25–2.19] 0.5818 1.72 [0.46–6.36] 0.4202
 Four to six months 23/58 (39.7) 1.31 [0.40–4.35] 0.6540 1.52 [0.34–6.78] 0.5854
 More than six months 27/57 (47.4) 1.80 [0.55–5.93] 0.3341 1.69 [0.40–7.15] 0.4790
Unprotected sex at last sex with main partner in the past 3 monthsc
 No 47/265 (17.7) ref. ref.
 Yes 195/564 (34.6) 2.45 [1.71–3.51] < 0.0001 1.77 [1.10–2.85] 0.0191
Ever treated for STI
 No 191/706 (27.1) ref. ref.
 Yes 53/131 (40.5) 1.83 [1.25–2.70] 0.0021 2.31 [1.31–4.06] 0.0037
HIV-positive
 No 165/723 (22.8) ref. ref.
 Yes 84/123 (68.3) 7.28 [4.80–11.06] < 0.0001 4.43 [2.56–7.68] < 0.0001

OR: odds ratio; AOR: adjusted odds ratio; CI: confidence interval; ref: reference group.

a

Multiple regression model includes all variables with p<.25 in bivariate model.

b

Any use reported; not necessarily abuse or misuse.

c

Also includes participants who reported unprotected sex with a non-main or primary partner.

Note: Sample sizes fluctuate slightly for some variables due to missing data. Some percentages do not sum to 100 due to rounding.

When all the STIs were combined together (Table 5), the odds of having one or more STI were higher among participants who: were women compared to circumcised men; were 20–24 or 30–34 years of age compared to 18–19 years; had secondary or lower education compared to college or university education; were divorced, widowed, or separated compared to being single; reported having unprotected sex at last sex with main partner compared to those who did not; reported previous treatment for STIs compared to those who did; and tested HIV-positive compared to those negative. On the other hand, the odds of having STIs were lower among participants who reported engaging in anal sex compared to those who did not.

Table 5.

Correlates of acute and chronic sexually transmitted infections (STIs) among participants completing KICoS screening in Kisumu, Kenya (2007–2008).

Variable Have STIsa
Bivariate
Multiple regressionb
n/N (%) OR [95% CI] p Value AOR [95% CI] p Value
Gender/men circumcision status <0.0001 <0.0001
 Women 206/424 (48.6) 5.92 [3.66–9.56] <0.0001 6.12 [3.20–11.72] <0.0001
 Uncircumcised men 43/251 (17.1) 1.29 [0.75–2.24] 0.3573 1.20 [0.61–2.33] 0.6000
 Circumcised men 23/167 (13.8) ref.
Age, years <0.0001 0.0431
 18–19 23/105 (21.9) ref.
 20–24 160/530 (30.2) 1.54 [0.94–2.54] 0.0886 2.13 [1.12–4.04] 0.0214
 25–29 53/149 (35.6) 1.97 [1.11–3.49] 0.0202 1.73 [0.82–3.64] 0.1508
 30–34 36/62 (58.1) 4.94 [2.49–9.79] <0.0001 3.41 [1.34–8.67] 0.0100
Highest level of education <0.0001 0.0006
 College or university 37/214 (17.3) ref.
 Technical 9/63 (14.3) 0.80 [0.36–1.76] 0.5741 1.09 [0.44–2.72] 0.8570
 Secondary 96/12 (30.9) 2.14 [1.39–3.28] 0.0005 2.02 [1.19–3.43] 0.0092
 Primary and below 129/254 (50.8) 4.94 [3.21–7.60] <0.0001 3.24 [1.80–5.83] <0.0001
Currently employed 0.0503 0.4533
 No 128/440 (29.1) ref. ref.
 Yes 143/404 (35.4) 1.34 (1.00–1.78
Marital status <0.0001 0.0133
 Never married 103/515 (20.0) ref.
 Married or living as married 136/286 (47.6) 3.63 [2.64–4.98] <0.0001 1.58 [0.98–2.57] 0.0635
 Divorced/separated/widowed 30/41 (73.2) 10.91 [5.29–22.50] <0.0001 4.04 [1.43–11.38] 0.0082
Ever inherited or been inherited <0.0001 0.5410
 No 243/797 (30.5) ref.
 Yes 22/34 (64.7) 4.18 [2.04–8.58] 1.34 [0.52–3.47]
Alcohol use in the past 3 monthsc <0.0001 0.5477
 No 185/482 (38.4) ref.
 Yes 86/363 (23.7) 0.50 [0.37–0.68] 0.87 [0.56–1.36]
Recreational drug use in the past 3 monthsc <0.0001 0.0616
 No 250/706 (35.4) ref.
 Yes 21/137 (15.3) 0.33 [0.20–0.54] 0.51 [0.25–1.03]
Age of sexual debut, years 0.5835
 22–34 9/26 (34.6) ref.
 16–21 155/458 (33.8) 0.97 [0.42–2.22] 0.9355
 8–15 94/314 (29.9) 0.81 [0.35–1.88] 0.6184
 <7 4/17 (23.5) 0.58 [0.15–2.31] 0.4416
Number lifetime sex partners 0.0133 0.3047
 0–1 37/111 (33.3) ref.
 2–5 158/429 (36.8) 1.17 [0.75–1.81] 0.4945 1.71 [0.96–3.02] 0.0674
 6–10 37/156 (23.7) 0.62 [0.36–1.07] 0.0850 1.69 [0.81–3.53] 0.1653
 >10 30/112 (26.8) 0.73 [0.41–1.30] 0.2870 1.88 [0.84–4.22] 0.1278
Engaged in anal sex in the past 3 months 0.0089 0.0005
 No 233/684 (34.1) ref.
 Yes 35/152 (23.0) 0.58 [0.39–0.87] 0.38 [0.22–0.65]
Time since last sex 0.0007 0.6119
 Never 5/15 (33.3) ref.
 Within three months 198/676 (29.3) 0.83 [0.28–2.46] 0.7342 2.11 [0.57–7.89] 0.2653
 Four to six months 264/58 (44.8) 1.63 [0.49–5.35] 0.4245 2.54 [0.58–11.16] 0.2183
 More than six months 30/57 (52.6) 2.22 [0.67–7.32] 0.1897 2.54 [0.60–10.71] 0.2058
Unprotected sex at last sex with main partner in the past three monthsd <0.0001 0.0054
 No 52/265 (19.6) ref.
 Yes 212/564 (37.6) 2.47 [1.74–3.49] 1.88 [1.21–2.94]
Ever treated for STI 0.0021 0.0037
 No 210/706 (29.8) ref.
 Yes 57/131 (43.5) 1.82 [1.24–2.66] 2.23 [1.30–3.82]
HIV-positive <0.0001 <0.0001
 No 187/723 (25.9) ref.
 Yes 85/123 (69.1) 6.41 [4.23–9.73] 3.24 [1.91–5.51]

OR: odds ratio; AOR: adjusted odds ratio; CI: confidence interval; ref: reference group.

a

The 4 STIs were syphilis, gonorrhoea, HSV-2 and Chlamydia.

b

Multiple regression model includes all variables with p<.25 in bivariate model

c

Any use reported; not necessarily abuse or misuse

d

Also includes participants who reported unprotected sex with a non-main or primary partner Note: Sample sizes fluctuate slightly for some variables due to missing data. Some percentages do not sum to 100 due to rounding.

Discussion

Our data show that more than a third of screened participants for an HIV incidence cohort study in periurban Kisumu, western Kenya, had at least one STI (syphilis, gonorrhoea, HSV-2, and/or chlamydia). These results are consistent with what was seen in two studies previously done in the study area.19,30 Several factors were associated with having an STI, including female gender, low education level, unprotected sex with a main partner, being divorced/widowed/separated or married, and being HIV-infected.

Women accounted for most (75.7%) STI infections, which is consistent with findings from other studies conducted in the same general geographical location, including the four cities study,30 the Asembo baseline cross-sectional HIV survey,31 and the Kenya Demographic and Health and Kenya AIDS Indicator Surveys.19,32 The 10-fold prevalence of HSV-2 infection compared to other STIs is consistent with the known epidemiology in many regions of the world.

Overall, the odds of having one or more STI were six times as great for women as circumcised men. The odds were 1.2 times as great for uncircumcised men as for circumcised men even though this was not significant; suggesting, as has been reported in other studies,20,33 that circumcision is protective for STIs in men. Even when the STIs were segregated by acuteness, the odds were still greater in women with women having four times and five times greater odds than their circumcised male counterparts. Not unexpectedly, unprotected sex with a main partner was also associated with having an STI.25,26,34 This, however, was not true with having an acute STI. Other studies have shown that women in this and other societies are often in a subordinate position and may lack the power to make decisions about condom use,3540 and that despite the provision of condoms and risk-reduction counselling, unprotected sex out of marriages continues.41,42

Our analysis also documents that having low education and being divorced, widowed, or separated are important correlates for having a chronic STI. Studies have shown that having increased education is associated with more knowledge, safer sexual behaviours, and lower HIV infection rates to the extent that education has been called the “social vaccine.”41 Our data suggests that marital status was associated with higher odds of having an STI for divorced/widowed or separated individuals, most of whom were women. This may be related to previous reports that divorce for women is a risk factor for being involved in commercial sex work and the starting of other relationships.4244 Divorced, widowed, or separated women may have pressing financial obligations, including dependent children, and few skills to earn money, thus they resort to some type of transactional sex, including sex work.

We found that HIV-positive individuals had more than four times the odds of having a chronic STI. Several other studies have also shown that a relationship exists between HIV infection and STIs.23,27,34,45 A study in Ethiopia found that HIV co-infection predisposes women to developing more frequent ulcerative STIs, especially HSV-2, as well as to failing STI treatment. 27 These findings were also seen in another study in Tanzania that enrolled high-risk women which are consistent with what was seen in this study.34 Behavioural interventions to prevent HIV have been shown to also work to prevent most STIs.13,4649 Biomedical interventions to prevent HIV such as tenofovir vaginal gel microbicide have been shown to have the potential to also prevent HSV-2 infection and, thus, may be especially helpful in impacting the HIV epidemic in sub Saharan Africa.5052

Even though several studies have shown anal sex to be a risk factor for prevalent and incident STIs,5358 we found the odds of having chronic STIs lower among participants who reported anal sex compared to those who did not. This may be due to the fact that we did not screen for any rectal STIs. We also found the odds of having STIs to be lower in those using recreational drugs contrary to what most studies have reported.5961 Reported recreational drug use was rare in our study population, which might reflect the lower availability of recreational drugs in inland western Kenya than at the coast and urban slums in Nairobi,6264 and we therefore feel that this finding in our analysis might reflect a spurious association due to low numbers.

Several limitations should be considered in the interpretation of our findings. First, our participants may not be representative of the Kisumu population as they were volunteers for a research study and were recruited through convenience sampling. However, the screening HIV prevalence we found is nearly identical to local population estimates from national surveillance data,19 suggesting that perhaps the study participants may be representative of the local community regardless of the convenience sampling and potential bias of desiring to participate in a research study. Second, there may be response bias as with any self-reported behavioural/risk data collection, although we believe use of ACASI facilitated more truthful responding65,66 than face-to-face interviews would have. Thirdly, our diagnosis of chlamydia/gonorrhoea was an assay for active disease, but for HSV-2 and syphilis was serology, which may have missed recent acquisition and which also classifies people as positive even if their infection was remote and is inactive. We also did not test for any rectal STIs and so could not correlate this to anal sex. Lastly, because this was a cross-sectional study evaluating prevalence of STI and HIV within a prospective study, we cannot determine timing or causality. The strength of our analysis, however, is that we were able to collect and correlate both behavioural and biological correlates of prevalent STI.

In conclusion, similar to HIV infection in Kenya, STI prevalence is high in this part of Kenya, with women more likely to be infected than men in our research setting. Multiple strategies are needed to address the overall high prevalence of STIs as well as the gender disparity. In addition to increasing screening and access to health care,67 and developing women-controlled biomedical interventions like vaginal microbides, 68 non-medical methods should be employed to reduce the gender disparity in HIV and STIs. Because HIV can be considered an STI (although it was considered separately in this analysis), the structural methods which may have an impact are virtually the same as for HIV, and would include focusing on education, about which the WHO has stated that, “…a good basic education ranks among the most effective-and cost-effective-means of HIV prevention.”69 In conjunction with education, reducing early marriage is another important strategy, as the husbands of married adolescents and young adult women are more likely to be HIV-positive compared to the male partners of single woman.31,70 Finally, empowerment of adolescent girls and women through structural and economic interventions has been effectively used to improve their health.3,71 By using multiple strategies (biomedical, socio-economic, and cultural), STI and HIV prevalence in Kenya could be reduced.

Acknowledgments

Funding

The study was funded through a cooperative agreement by the U.S. Centers for Disease Control and Prevention.

We are grateful to the study participants as well as Kayla Laserson, Katrina Kretsinger, Peter McElroy, Charles Vitek, Alan Greenberg, Laurence Slutsker, Kevin DeCock and John Vulule for their contribution to study design and protocol development, Clement Zeh for his expertise in laboratory analyses, and Deborah A. Gust for input on an earlier version of this manuscript. This paper is published with the approval of the Director of the Kenya Medical Research Institute.

Footnotes

Disclaimer

The findings and conclusions in this report are those of the author and do not necessarily represent the views of the Centers for Disease Control and Prevention. Use of trade names is for identification purposes only and does not constitute endorsement by the U.S. Centers for Disease Control and Prevention or the Department of Health and Human Services.

Conflict of interest

The authors declare no conflict of interest.

References

  • 1.Hook EW., III Gender differences in risk for sexually transmitted diseases. Am J Med Sci. 2012;343:10–11. doi: 10.1097/MAJ.0b013e31823ea276. [DOI] [PubMed] [Google Scholar]
  • 2.Kaushic C, Roth KL, Anipindi V, et al. Increased prevalence of sexually transmitted viral infections in women: the role of female sex hormones in regulating susceptibility and immune responses. J Reprod Immunol. 2010;88:204–209. doi: 10.1016/j.jri.2010.12.004. [DOI] [PubMed] [Google Scholar]
  • 3.Lee H, Pollock G, Lubek I, et al. Creating new career pathways to reduce poverty, illiteracy and health risks, while transforming and empowering Cambodian women’s lives. J Health Psychol. 2010;15:982–992. doi: 10.1177/1359105310371703. [DOI] [PubMed] [Google Scholar]
  • 4.WHO. Global prevalence and incidence of selected curable sexually transmitted infections. Geneva: World Health Organisation; 2001. [Google Scholar]
  • 5.Buve A, Laga M, Piot P. Sexually transmitted diseases: where are we now? Health Policy Plan. 1993;8:277–281. [Google Scholar]
  • 6.WHO. Guidelines for the management of sexually transmitted infections. Geneva: World Health Organisation; 2003. [Google Scholar]
  • 7.WHO. Sexually transmitted and other reproductive tract infections: a guide to essential practice. Geneva: World Health Organisation; 2005. [Google Scholar]
  • 8.WHO; WHO, editor. Global strategy for the prevention and control of sexually transmitted infections: 2006–2015: breaking the chain of transmission. Switzerland: World Health Organisation; 2007. [Google Scholar]
  • 9.Laga M, Manoka A, Kivuvu M, et al. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS. 1993;7:95–102. doi: 10.1097/00002030-199301000-00015. [DOI] [PubMed] [Google Scholar]
  • 10.Cohen MS, Hoffman IF, Royce RA, et al. Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. Lancet. 1997;349:1867–1873. doi: 10.1016/s0140-6736(97)02190-9. [DOI] [PubMed] [Google Scholar]
  • 11.Gilson L, Mkanje R, Grosskurth H, et al. Cost-effectiveness of improved treatment services for sexually transmitted diseases in preventing HIV-1 infection in Mwanza Region, Tanzania. Lancet. 1997;350:1805–1809. doi: 10.1016/S0140-6736(97)08222-6. [DOI] [PubMed] [Google Scholar]
  • 12.Wawer MJ, Sewankambo NK, Serwadda D, et al. Control of sexually transmitted diseases for AIDS prevention in Uganda: a randomised community trial. Lancet. 1999;353:535. doi: 10.1016/s0140-6736(98)06439-3. [DOI] [PubMed] [Google Scholar]
  • 13.Kamali A, Quigley M, Nakiyingi J, et al. Syndromic management of sexually-transmitted infections and behaviour change interventions on transmission of HIV-1 in rural Uganda: a community randomised trial. Lancet. 2003;361:645–652. doi: 10.1016/s0140-6736(03)12598-6. [DOI] [PubMed] [Google Scholar]
  • 14.WHO, editor. Sexually transmitted infections prevalence study methodology: guidelines for the implementation of STI prevalence surveys. Switzerland: World Health Organisation; 1999. [Google Scholar]
  • 15.Mayaud P, Mosha F, Todd J, et al. Improved treatment services significantly reduce the prevalence of sexually transmitted diseases in rural Tanzania: results of a randomized controlled trial. AIDS. 1997;11:1873–1880. doi: 10.1097/00002030-199715000-00013. [DOI] [PubMed] [Google Scholar]
  • 16.Fenton KA, Mercer CH, Johnson AM, et al. Reported sexually transmitted disease clinic attendance and sexually transmitted infections in Britain: prevalence, risk factors, and proportionate population burden. J Infect Dis. 2005;191:S127–S138. doi: 10.1086/425286. [DOI] [PubMed] [Google Scholar]
  • 17.Johnson LF, Dorrington RE, Bradshaw D, et al. The effect of syndromic management interventions on the prevalence of sexually transmitted infections in South Africa. Sex Reprod Health. 2011;2:13–20. doi: 10.1016/j.srhc.2010.08.006. [DOI] [PubMed] [Google Scholar]
  • 18.Smith JS, Robinson NJ. Age-specific prevalence of infection with herpes simplex virus types 2 and 1: a global review. J Infect Dis. 2002;186:S3–S28. doi: 10.1086/343739. [DOI] [PubMed] [Google Scholar]
  • 19.National AIDS and STI Control Programme. Kenya AIDS Indicator Survey 2007: Final Report. Nairobi: Ministry of Health, Kenya; Sep, 2009. [Google Scholar]
  • 20.Newell J, Senkoro K, Mosha F, et al. A population-based study of syphilis and sexually transmitted disease syndromes in north-western Tanzania. 2. Risk factors and health seeking behaviour. Genitourinary medicine. 1993;69:421–426. doi: 10.1136/sti.69.6.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Drumright LN, Gorbach PM, Holmes KK. Do people really know their sex partners? Concurrency, knowledge of partner behavior, and sexually transmitted infections within partnerships. Sex Transm Dis. 2004;31:437–442. doi: 10.1097/01.olq.0000129949.30114.37. [DOI] [PubMed] [Google Scholar]
  • 22.Doherty IA, Padian NS, Marlow C, et al. Determinants and consequences of sexual networks as they affect the spread of sexually transmitted infections. J Infect Dis. 2005;191:S42–S54. doi: 10.1086/425277. [DOI] [PubMed] [Google Scholar]
  • 23.Colvin M, Karim SSA, Connolly C, et al. HIV infection and asymptomatic sexually transmitted infections in a rural South African community. Int J STD AIDS. 1998;9:548–550. doi: 10.1258/0956462981922683. [DOI] [PubMed] [Google Scholar]
  • 24.Weiss HA, Buve A, Robinson NJ, et al. The epidemiology of HSV-2 infection and its association with HIV infection in four urban African populations. AIDS. 2001;15:S97–S108. doi: 10.1097/00002030-200108004-00011. [DOI] [PubMed] [Google Scholar]
  • 25.Yahya-Malima K, Evjen-Olsen B, Matee M, et al. HIV-1, HSV-2 and syphilis among pregnant women in a rural area of Tanzania: prevalence and risk factors. BMC Infect Dis. 2008;8:75. doi: 10.1186/1471-2334-8-75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Charvat B, Ssempijja V, Kigozi G, et al. Factors associated with the prevalence and incidence of herpes simplex virus Type 2 infection among men in Rakai, Uganda. J Infect Dis. 2009;199:945–949. doi: 10.1086/597074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Wolday D, G-Mariam Z, Mohammed Z, et al. Risk factors associated with failure of syndromic treatment of sexually transmitted diseases among women seeking primary care in Addis Ababa. Sex Transm Infect. 2004;80:393–394. doi: 10.1136/sti.2003.005660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Chege W, Pals SL, McLellan-Lemal E, et al. Baseline findings of an HIV incidence cohort study to prepare for future HIV prevention clinical trials in Kisumu, Kenya. J Infect Dev Ctries. 2012;6:870–880. doi: 10.3855/jidc.2636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Agot KE, Vander Stoep A, Tracy M, et al. Widow inheritance and HIV prevalence in Bondo District, Kenya: baseline results from a prospective cohort study. PLoS ONE. 2010;5:e14028. doi: 10.1371/journal.pone.0014028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Buve A, Carael M, Hayes RJ, et al. The multicentre study on factors determining the differential spread of HIV in four African cities: summary and conclusions. AIDS. 2001;15:S127–S131. doi: 10.1097/00002030-200108004-00014. [DOI] [PubMed] [Google Scholar]
  • 31.Amornkul PN, Vandenhoudt H, Nasokho P, et al. HIV prevalence and associated risk factors among individuals aged 13–34 years in rural western Kenya. PLoS ONE. 2009;4:e6470. doi: 10.1371/journal.pone.0006470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Central Bureau of Statistics (CBS) [Kenya], Ministry of Health (MoH) [Kenya], ORC Macro. Kenya Demographic and Health Survey 2003. Calverton, Maryland: CBS, MOH, and ORC Macro; 2004. [Google Scholar]
  • 33.Jansen HAFM, Morison L, Mosha F, et al. Geographical variations in the prevalence of HIV and other sexually transmitted infections in rural Tanzania. Int J STD AIDS. 2003;14:274–280. doi: 10.1258/095646203321264908. [DOI] [PubMed] [Google Scholar]
  • 34.Watson-Jones D, Weiss HA, Rusizoka M, et al. Risk factors for herpes simplex virus type 2 and HIV among women at high risk in Northwestern Tanzania: preparing for an HSV-2 intervention trial. J Acquir Immune Defic Syndr. 2007;46:631–642. doi: 10.1097/QAI.0b013e31815b2d9c. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Wingood GM, DiClemente RJ. Application of the theory of gender and power to examine HIV-related exposures, risk factors, and effective interventions for women. Health Edu Behav. 2000;27:539–565. doi: 10.1177/109019810002700502. [DOI] [PubMed] [Google Scholar]
  • 36.Green G, Pool R, Harrison S, et al. Female control of sexuality: illusion or reality? Use of vaginal products in south west Uganda. Social Sci Med. 2001;52:585–598. doi: 10.1016/s0277-9536(00)00162-3. [DOI] [PubMed] [Google Scholar]
  • 37.Gutiérrez L, Oh H, Gillmore M. Toward an understanding of (Em)Power(Ment) for HIV/AIDS prevention with adolescent women. Sex Roles. 2000;42:581–611. [Google Scholar]
  • 38.Maxwell C, Boyle M. Risky heterosexual practices amongst women over 30: gender, power and long term relationships. AIDS Care. 1995;7:277–294. doi: 10.1080/09540129550126515. [DOI] [PubMed] [Google Scholar]
  • 39.Ackermann L, de Klerk GW. Social factors that make South African women vulnerable to HIV infection. Health Care Women Int. 2002;23:163–172. doi: 10.1080/073993302753429031. [DOI] [PubMed] [Google Scholar]
  • 40.Ndeda MJA, editor. Mijadala on Social Policy, Governance and Development in Kenya. Nairobi Safari Club, Kenya: Development Policy Management Forum; 2006. Social policy and the subordination of women in Kenya. [Google Scholar]
  • 41.Bakilana A, Bundy D, Brown J, et al. Accelerating the education sector response to HIV/AIDS in Africa: a review of world bank assistance. Washington, DC: The World Bank; 2005. [Google Scholar]
  • 42.Voeten HACM, Egesah OB, Varkevisser CM, 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. doi: 10.1111/j.1365-3156.2006.01776.x. [DOI] [PubMed] [Google Scholar]
  • 43.Ray S, van de Wijgert J, Mason P, et al. Constraints faced by sex workers in use of female and male condoms for safer sex in urban Zimbabwe. J Urban Health. 2001;78:581–592. doi: 10.1093/jurban/78.4.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Wilson D, Chiroro P, Lavelle S, et al. Sex worker, client sex behaviour and condom use in Harare, Zimbabwe. AIDS Care. 1989;1:269–280. doi: 10.1080/09540128908253032. [DOI] [PubMed] [Google Scholar]
  • 45.WHO. Survey Report. Geneva: World Health Organisation; Sep, 2001. Prevalence survey of sexually transmitted infections among female sex workers and women attending ante natal clinics in Malaysia 1999–2000. [Google Scholar]
  • 46.Carey MP, Senn TE, Vanable PA, et al. Brief and intensive behavioral interventions to promote sexual risk reduction among STD clinic patients: results from a randomized controlled trial. AIDS Behav. 2010;14:504–517. doi: 10.1007/s10461-009-9587-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Aral SO, Peterman TA. Defining behavioral methods to prevent sexually transmitted diseases through intervention research. Infect Dis Clin North Am. 1993;7:861–873. [PubMed] [Google Scholar]
  • 48.Shahmanesh M, Patel V, Mabey D, et al. Effectiveness of interventions for the prevention of HIV and other sexually transmitted infections in female sex workers in resource poor setting: a systematic review. Trop Med Int Health. 2008;13:659–679. doi: 10.1111/j.1365-3156.2008.02040.x. [DOI] [PubMed] [Google Scholar]
  • 49.Stephenson JM. Evaluation of behavioural interventions in HIV/STI prevention. Sex Transm Infect. 1999;75:69–71. doi: 10.1136/sti.75.1.69. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Abdool Karim Q, Abdool Karim SS, Frohlich JA, et al. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science. 2010;329:1168–1174. doi: 10.1126/science.1193748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Andrei G, Lisco A, Vanpouille C, et al. Topical tenofovir, a microbicide effective against HIV, inhibits herpes simplex virus-2 replication. Cell Host Microbe. 2011;10:379–389. doi: 10.1016/j.chom.2011.08.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Tan D. Potential role of tenofovir vaginal gel for reduction of risk of herpes simplex virus in females. Int J Womens Health. 2012;4:341–350. doi: 10.2147/IJWH.S27601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.van der Bij AK, Stolte IG, Coutinho RA, et al. Increase of sexually transmitted infections, but not HIV, among young homosexual men in Amsterdam: are STIs still reliable markers for HIV transmission? Sex Transm Infect. 2005;81:34–37. doi: 10.1136/sti.2003.007997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Nicoll A, Hughes G, Donnelly M, et al. Assessing the impact of national anti-HIV sexual health campaigns: trends in the transmission of HIV and other sexually transmitted infections in England. Sex Transm Infect. 2001;77:242–247. doi: 10.1136/sti.77.4.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Jin F, Prestage GP, Zablotska I, et al. High rates of sexually transmitted infections in HIV positive homosexual men: data from two community based cohorts. Sex Transm Infect. 2007;83:397–399. doi: 10.1136/sti.2007.025684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 56.Spenatto N, Viraben R. Substantial increase in gonorrhoea among homosexual men attending an STD centre in Toulouse, France. Sex Transm Infect. 2001;77:391–392. doi: 10.1136/sti.77.5.391-a. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Truong HHM, Kellogg T, Klausner JD, et al. Increases in sexually transmitted infections and sexual risk behaviour without a concurrent increase in HIV incidence among men who have sex with men in San Francisco: a suggestion of HIV serosorting? Sex Transm Infect. 2006;82:461–466. doi: 10.1136/sti.2006.019950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Hart GJ, Flowers P, Der GJ, et al. Homosexual men’s HIV related sexual risk behaviour in Scotland. Sex Transm Infect. 1999;75:242–246. doi: 10.1136/sti.75.4.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Ko N-Y, Lee H-C, Chang J-L, et al. Prevalence of human immunodeficiency virus and sexually transmitted infections and risky sexual behaviors among men visiting gay bathhouses in Taiwan. Sex Transm Dis. 2006;33:467–473. doi: 10.1097/01.olq.0000204512.15297.5f. [DOI] [PubMed] [Google Scholar]
  • 60.Darrow W, Biersteker S, Geiss T, et al. Risky sexual behaviors associated with recreational drug use among men who have sex with men in an international resort area: challenges and opportunities. J Urban Health. 2005;82:601–609. doi: 10.1093/jurban/jti122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Bellis MA, Hughes K, Calafat A, et al. Sexual uses of alcohol and drugs and the associated health risks: a cross sectional study of young people in nine European cities. BMC Public Health. 2008;8:155. doi: 10.1186/1471-2458-8-155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Beckerleg S. How cool is heroin injection at the Kenya coast. Drugs Edu Prevent Policy. 2004;11:67–77. [Google Scholar]
  • 63.Smart RG, Murray GF, Arif A. Drug abuse and prevention programs in 29 countries. Subst Use Misuse. 1988;23:1–17. doi: 10.3109/10826088809027487. [DOI] [PubMed] [Google Scholar]
  • 64.Mugisha F, Arinaitwe-Mugisha J, Hagembe BON. Alcohol, substance and drug use among urban slum adolescents in Nairobi, Kenya. Cities. 2003;20:231–240. [Google Scholar]
  • 65.Turner CF, Ku L, Rogers SM, et al. Adolescent sexual behavior, drug use, and violence: increased reporting with computer survey technology. Science. 1998;280:867–873. doi: 10.1126/science.280.5365.867. [DOI] [PubMed] [Google Scholar]
  • 66.Oloo I, Gust DA, Shinde S, et al. Effect of gender of the recorded voice on responses to sensitive sexual behavior questions use of audio computer-assisted self-interview (ACASI) in Kisumu, Kenya. Field Methods. 2012;24:367–381. [Google Scholar]
  • 67.Wilkinson D, Abdool-Karim SS, Harrison A, et al. Unrecognized sexually transmitted infections in rural South African women: a hidden epidemic. Bull World Health Org. 1999;77:22–28. [PMC free article] [PubMed] [Google Scholar]
  • 68.Abdool Karim Q, Abdool Karim SS, Frohlich JA, et al. Effectiveness and safety of tenofovir gel, an antiretroviral microbicide, for the prevention of HIV infection in women. Science. 2010;329:1168–1174. doi: 10.1126/science.1193748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 69.World Bank. Education and HIV/AIDS: a window of hope. Washington DC: The World Bank; 2002. Contract No.: Document Number|. [Google Scholar]
  • 70.Clark S. Early marriage and HIV risks in sub-Saharan Africa. Stud Fam Plann. 2004;35:149–160. doi: 10.1111/j.1728-4465.2004.00019.x. [DOI] [PubMed] [Google Scholar]
  • 71.Wallerstein N. What is the evidence on effectiveness of empowerment to improve health? Copenhagen, WHO Regional Office for Europe (Health Evidence Network report) Copenhagen: World Health Organisation, Health Evidence Network WHOROfE; 2006. [Google Scholar]

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