Skip to main content
BMJ Open Access logoLink to BMJ Open Access
. 2016 Jan 27;92(4):251–256. doi: 10.1136/sextrans-2015-052371

Prevalence of reproductive tract infections and the predictive value of girls’ symptom-based reporting: findings from a cross-sectional survey in rural western Kenya

Emily Kerubo 1, Kayla F Laserson 2, Newton Otecko 1, Collins Odhiambo 1, Linda Mason 3, Elizabeth Nyothach 1, Kelvin O Oruko 1, Ashley Bauman 3, John Vulule 1, Clement Zeh 4, Penelope A Phillips-Howard 1,3
PMCID: PMC4893088  PMID: 26819339

Abstract

Objectives

Reproductive tract infections (RTIs), including sexually acquired, among adolescent girls is a public health concern, but few studies have measured prevalence in low-middle-income countries. The objective of this study was to examine prevalence in rural schoolgirls in Kenya against their reported symptoms.

Methods

In 2013, a survey was conducted in 542 adolescent schoolgirls aged 14–17 years who were enrolled in a menstrual feasibility study. Vaginal self-swabbing was conducted after girls were interviewed face-to-face by trained nurses on symptoms. The prevalence of girls with symptoms and laboratory-confirmed infections, and the sensitivity, specificity, positive and negative predictive values of symptoms compared with laboratory results, were calculated.

Results

Of 515 girls agreeing to self-swab, 510 answered symptom questions. A quarter (24%) reported one or more symptoms; most commonly vaginal discharge (11%), pain (9%) or itching (4%). Laboratory tests confirmed 28% of girls had one or more RTI. Prevalence rose with age; among girls aged 16–17 years, 33% had infections. Bacterial vaginosis was the most common (18%), followed by Candida albicans (9%), Chlamydia trachomatis (3%), Trichomonas vaginalis (3%) and Neisseria gonorrhoeae (1%). Reported symptoms had a low sensitivity and positive predictive value. Three-quarters of girls with bacterial vaginosis and C. albicans, and 50% with T. vaginalis were asymptomatic.

Conclusions

There is a high prevalence of adolescent schoolgirls with RTI in rural Kenya. Public efforts are required to identify and treat infections among girls to reduce longer-term sequelae but poor reliability of symptom reporting minimises utility of symptom-based diagnosis in this population.

Trial registration number

ISRCTN17486946.

Keywords: ADOLESCENT, AFRICA, DIAGNOSIS, REPRODUCTIVE HEALTH, SEXUAL HEALTH

Introduction

An estimated half a billion new cases of curable sexually transmitted infections occur each year globally,1 2 with women being more susceptible and bearing the greatest burden of these infections. Reproductive tract infections (RTIs), including those sexually acquired, have historically been labelled a ‘silent’ epidemic among females, contributing to gynaecological morbidity and maternal mortality globally, including low-middle-income countries (LMICs).1 Untreated infections can lead to pelvic inflammatory diseases, ectopic pregnancy, infertility, cervical cancer, foetal loss or infant health complications, with a threefold to fivefold increase in risk of HIV acquisition and transmission.1 w1 Bacterial vaginosis is associated with increased risk for acquisition of HIV,3 w2 promotes viral shedding among HIV-infected females4 and increases susceptibility for other infections such as gonorrhoea, trichomoniasis and herpes simplex virus type-2 (HSV-2).5–8 w3 Adolescent females are vulnerable to bacterial vaginosis infection,1 w4 with an association between human papillomavirus infection, bacterial vaginosis and cervicitis.9 This is compounded by adolescent girls’ heightened susceptibility to HIV, for biological as well as socio-cultural reasons,10 in western Kenya, for example, young females have a sixfold greater risk of contracting HIV compared with young males.11

Although research on the burden of RTI among adolescent females in LMIC is limited, WHO estimates 80–90% of the global burden lies in LMICs.1 In Kenya, one in every five youths 15–24 years report sexual debut before the age of 15 years.w5 While HIV prevalence has fallen nationally, it remains static in rural parts of the former Nyanza Provincew5 and rises among girls during adolescence.11 For the region, RTI prevalence is also high, with a third of urban adolescent girls aged 15–19 years diagnosed with Trichomonas vaginalis,12 and a smaller proportion with other infections (9% Chlamydia trachomatis; 2% Neisseria gonorrhoeae, 3% syphilis).13 However, data are sparse on the prevalence of RTI among post-pubescent girls in rural African settings.

Symptom assessment has commonly been used to prescribe treatment of RTI, and a simplified algorithm to guide health workers in the implementation of syndromic management of RTI has been developed.14 w6 This was intended to define cause among the symptomatic rather than as a screening tool in the general population. Experts advocate supplementary point-of-care testing because of the poor predictive value of symptoms alone.15 Symptom guidelines at the national level have also been questioned in western Kenya when compared with laboratory diagnosis.w7 While menstrual studies among adolescent girls describe a high prevalence of RTI, seemingly due to poor hygiene,w8 most relied on reported symptoms.16 However, a study among women found symptom-based reporting was higher than laboratory-confirmed RTIs illustrating again the limitation of symptom reporting.16 The objective of this study was to measure the prevalence of RTI among adolescent schoolgirls in a menstrual feasibility study in rural western Kenya and to calculate the predictive value of girls’ symptom-based reporting against laboratory-confirmed infections.

Methods

Study setting

The population under study are resident in the Kenyan Medical Research Institute (KEMRI) and Centers for Disease Control and Prevention's health and demographic surveillance system (HDSS),w9 in Gem subcounty, Siaya County, western Kenya. This rural population are almost exclusively comprised of the Luo ethnic group who are mainly farmers.w9

Study design

Cross-sectional, laboratory-supported, RTI survey nested within a menstrual feasibility study.

Menstrual feasibility study

The ‘parent’ study, conducted August 2012 to November 2013, was a randomised controlled pilot examining the feasibility of menstrual solutions for girls in rural primary schools in western Kenya. In total, 30 of 62 schools participating in a baseline water, sanitation and hygiene survey reached eligibility for participation.17 No schools withdrew. All girls in study schools were enrolled if resident in the study area, were aged 14–16 years at enrolment, in classes 5–8, had no debilitation precluding participation and had experienced three or more menses. We estimated 669 participants followed to outcome provided 76% power to detect a 50% reduction in outcome (dropout), with an intra-cluster correlation coefficient of 0.01 and design effect of 1.21. Of 1005 target girls screened, 766 were enrolled and 40 (4%) refused, with the remaining 199 ineligible. Of the 766, 542 were in school for the cross-sectional RTI survey conducted in November 2013. Attrition (224 girls; 29.2%) prior to the RTI survey was due to withdrawal (2.1%), migration (12.4%), dropout (7.9%) and participants in class 8 exiting after their exams in October (6.8%).

RTI cross-sectional survey methods

Study nurses, trained by a gynaecologist, privately questioned participants on a list of RTI-associated signs and symptoms before sample collection (see online supplementary form S1). All survey tools were pilot tested and nurses explained symptoms when interviewing. Symptoms covered urinary complaints, pain or bleed during sexual intercourse, vaginal discharge, malodorous or fishy smell, genital itching/irritation, lower abdominal or vaginal pain or both, and abnormal bleeding (heavy or between periods).14 w6 w10

Nurses trained participants to obtain their own vaginal swab.18 Samples were transported daily to the KEMRI laboratory, prepared and analysed for Candida albicans, bacterial vaginosis, T. vaginalis, C. trachomatis and N. gonorrhoeae using standard methods.w11 Bacterial vaginosis was defined as a Nugent Score of 7–10. Girls with a laboratory-confirmed diagnosis were treated by study nurses according to Kenyan national guidelines.

Statistical analysis

Laboratory-confirmed infections were the measured outcome, and signs and symptoms the predictor variables, with age, socio-economic status (SES), age at menarche and prior use of sanitary pads also assessed as potential confounders. Data on SES were missing for 78 participants and were excluded from specific SES-related analysis. The prevalence of girls with individual infections and the 95% CI were calculated, then aggregated into all RTI. The prevalence of girls reporting symptoms were calculated, then aggregated into any symptom reported. Girls’ ages were collapsed into younger (<16 years) and older (>16 years) age groups. SES of participants was available from routine household surveys in the HDSS,w9 dichotomising quintiles into the poorest (1–2) and least poor (3–5). Differences due to age, SES, age of menarche and any prior sanitary pad use were assessed using Pearson's χ2 test. The sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) of symptoms alone, and then pooled, were computed for predicting each laboratory-confirmed (gold standard) infection, along with their 95% CI. Data analysis was performed using SPSS v.21.0.

Results

Of 542 adolescent schoolgirls present in school and approached for this study, 515 (95%) participated in the vaginal swabbing; 25 declined saying they were menstruating (including at a second follow-up) and 2 refused. Age at survey ranged from 14 to 17 years, with a mean of 15.2 years (SD 0.6 year). Participants’ median SES index was 4 (range 1–5), with 17% falling into the poorest two quintiles. Girls’ mean age of menarche was 13.6 years (SD 0.9 year), with 83.5% reporting some prior use of sanitary pads. Less than 1% of girls reported they were currently sexually active (past month), while 46 (9%) answered the question on symptoms occurring during sex. Of 515 girls who self-swabbed for laboratory confirmation of RTI diagnoses, 510 (99%) answered questions on symptoms.

A quarter of participants reported one or more symptoms (table 1). Most common among these was vaginal discharge, followed by pain or itching. There was no difference in overall symptoms reported by age, SES, age at menarche or prior use of sanitary pads. However, younger (<16 years) girls were twofold less likely to report vaginal discharge than girls aged >16 years (p=0.002; table 1). Overlapping of symptoms was common, with two-thirds of girls reporting two or more symptoms in addition to itching or sore vagina, malodorous smell, burning urine or bleeding between menses (see online supplementary table S2).

Table 1.

Prevalence of girls with reported symptoms by age group at survey

Prevalence (95% CIs) of girls with reported symptoms Age comparison
14–15 years 16–17 years Total Ratios χ2, p value
370 140 510*
Any symptom 82/370 22.2 (18.0 to 26.4) 40/140 28.6 (21.1 to 36.1) 122/510 23.9 (20.2 to 27.6) 0.78 (0.56 to 1.07) 2.29; 0.13
Heavy menstruation 25/370 6.8 (4.3 to 9.4) 8/140 5.7 (1.9 to 9.5) 33/510 6.5 (4.4 to 8.6) 1.18 (0.55 to 2.56) 0.18; 0.67
Between menses bleeding 15/370 4.1 (2.1 to 6.1) 5/140 3.6 (0.5 to 6.7) 20/510 3.9 (2.2 to 5.6) 1.14 (0.42 to 3.07) 0.06; 0.80
Burning urine 9/370 2.4 (0.8 to 4.0) 2/140 1.4 (−0.6 to 3.4) 11/510 2.2 (0.9 to 3.5) 1.70 (0.37 to 7.78) 0.49; 0.49
Frequency of urine 11/370 3.0 (1.3 to 4.7) 2/140 1.4 (−0.6 to 3.4) 13/510 2.5 (1.2 to 3.9) 2.08 (0.47 to 9.27) 0.98; 0.32
Abdominal/vaginal pain 30/370 8.1 (5.3 to 10.9) 15/140 10.7 (5.6 to 15.8) 45/510 8.8 (6.3 to 11.3) 0.76 (0.42 to 1.36) 0.86; 0.35
Pain during intercourse† 1/35 2.9 (−2.7 to 8.5) 1/11 9.1 (−7.9 to 26.1) 2/46 4.3 (−1.6 to 10.2) 0.31 (0.02to 4.62) 0.78; 0.38
Itchy/sore vagina‡ 16/365 4.4 (2.3 to 6.5) 6/139 4.3 (0.9 to 7.7) 32/504 4.4 (2.6 to 6.2) 1.02 (0.41 to 2.54) 0.001; 0.94
Malodorous smell 5/364 1.4 (0.2 to 2.6) 4/139 2.9 (0.1 to 5.7) 9/503 1.8 (0.6 to 3.0) 0.48 (0.13 to 1.75) 1.3; 0.26
Vaginal discharge 29/367 7.9 (5.1 to 10.7) 34/139 17.3 (11.0 to 23.6) 53/506 10.5 (7.8 to 13.2) 0.46 (0.28 to 0.76) 9.4; 0.002

*Five participants reporting ‘don't know’ for all symptoms are excluded. †Sample limited to girls responding to symptoms of pain or bleeding during sexual intercourse (n=46). ‡4–6 girls did not answer questions on vaginal itching, smell and discharge.

Laboratory tests confirmed 28% of participants had at least one RTI, with bacterial vaginosis the most common diagnosis among 18% of girls (table 2). T. vaginalis was threefold higher in older compared with younger girls (p=0.03). A higher proportion of girls in the poorest SES quintiles were diagnosed with bacterial vaginosis or C. albicans (p=0.076).

Table 2.

Prevalence of girls with laboratory-confirmed infections by age group

  Prevalence (95% CIs) of girls with laboratory diagnoses* Age comparison
14–15 years 16–17 years Total Ratios χ2, p value
Bacterial vaginosis 61/374 16.3 (12.2 to 20.4) 33/141 1.12 (0.58 to 2.15) 94/515 18.3 (14.6 to 22.0) 0.70 (0.48 to 1.02) 3.45; 0.06
Candida albicans 33/373 8.8 (5.8 to 11.8) 11/139 0.75 (0.56 to 1.02) 44/512 8.6 (6.1 to 11.1) 1.12 (0.58 to 2.15) 0.11; 0.74
Chlamydia trachomatis 10/371 2.7 (1.1 to 4.4) 3/140 0.32 (0.11 to 0.93) 13/511 2.5 (1.2 to 3.9) 1.26 (0.35 to 4.50) 0.13; 0.73
Trichomonas vaginalis 6/373 1.6 (0.3 to 2.9) 7/139 0.76 (0.07 to 8.26) 13/512 2.5 (1.2 to 3.9) 0.32 (0.11 to 0.93) 4.81; 0.03
Neisseria gonorrhoeae 2/371 0.5 (−0.2 to 1.2) 1/140 0.55 (0.26 to 1.15) 3/511 0.6 (−0.1 to 1.3) 0.76 (0.07 to 8.26) 0.5; 0.82
All reproductive tract infections 98/374 26.2 (21.7 to 30.7) 47/141 0.70 (0.48 to 1.02) 145/515 28.2 (24.3 to 32.1) 0.79 (0.59 to 1.05) 2.57; 0.11

*2–4 tests spoiled.

Three-quarters of girls with bacterial vaginosis and C. albicans infections were asymptomatic, with slightly higher proportions of girls with T. vaginalis, C. trachomatis and N. gonorrhoeae reporting at least one symptom (table 3). In the analysis of sensitivity and PPV, between girls’ reporting symptoms and laboratory-confirmed bacterial vaginosis, malodorous smell achieved a PPV >50%, while vaginal itching was 32%. There was a low sensitivity and PPV for girls’ reporting symptoms associated with C. trachomatis. Pain or bleed during intercourse was predictive for T. vaginalis among the few infected girls acknowledging sexual intercourse. The low prevalence of girls with N. gonorrhoeae (<1%) limited analysis. Burning urine had a low PPV (table 3).

Table 3.

Disease prediction of symptoms against laboratory diagnosis (95% CI) of reproductive tract infections

  Sensitivity Specificity PPV NPV
n % (95% CI) n % (95% CI) N % (95% CI) n % (95% CI)
Bacterial vaginosis
 Heavy menstruation 7/93 7.5 (3.1 to 14.9) 391/417 93.8 (91.0 to 95.9) 7/33 21.2 (9.0 to 38.9) 391/477 82.0 (78.2 to 85.3)
 Between menses bleeding 4/93 4.3 (1.2 to 11.0) 401/417 96.2 (93.8 to 97.8) 4/20 20.0 (5.7 to 43.7) 401/490 81.8 (78.1 to 85.2)
 Burning urine 2/93 2.2 (0.3 to 7.6) 408/417 97.8 (95.9 to 99.0) 2/11 18.2 (2.3 to 51.8) 408/499 81.8 (78.1 to 85.1)
 Frequency of urine 4/93 4.2 (1.2 to 10.4) 408/417 97.8 (95.9 to 99.0) 4/13 30.8 (9.1 to 61.4) 408/497 82.1(78.2 to 85.3)
 Abdominal/vaginal pain 10/93 10.7 (5.3 to 18.9) 382/417 91.6 (88.5 to 94.1) 10/45 22.2 (11.2 to 37.1) 382/465 82.2 (78.4 to 85.5)
 Pain during intercourse* 1/6 16.7 (0.5 to 64.1) 39/40 97.5 (86.4 to 99.9) 1/2 50.0 (1.3 to 98.7) 39/44 88.6 (75.4 to 96.2)
 Itchy/sore vagina† 7/92 7.6 (3.1 to 15.1) 397/412 96.4 (94.1 to 98.0) 7/22 31.8 (13.9 to 54.9) 397/482 82.4 (78.7 to 85.7)
 Malodorous smell 5/91 5.5 (1.8 to 12.4) 408/412 99.0 (97.5 to 99.7) 5/9 55.6 (21.2 to 86.3) 408/494 82.6 (79.0 to 85.8)
 Vaginal discharge 11/93 11.8 (6.1 to 20.2) 371/413 89.8 (86.5 to 92.6) 11/53 20.8 (10.8 to 34.1) 371/453 81.9 (78.0 to 85.3)
 Any symptoms 26/93 28.0 (19.1 to 38.2) 321/417 77.0 (72.6 to 80.9) 26/122 21.3 (15.0 to 29.7) 321/388 82.7 (78.6 to 86.4)
Candida albicans
 Heavy menstruation 4/44 9.1 (2.5 to 21.7) 435/463 94.0 (91.4 to 95.9) 4/32 12.5 (3.5 to 29.0) 435/475 91.6 (88.7 to 93.9)
 Between menses bleeding 1/44 2.2 (0.1 to 12.0) 444/563 95.9 (93.7 to 97.5) 1/20 5.0 (0.1 to24.9) 444/487 91.2 (88.3 to 93.5)
 Burning urine 0/44 0.0 (0.0 to 8.4) 452/463 97.6 (95.8 to 98.8) 0/11 0.0 (0.0 to 28.5) 452/496 91.1 (88.3 to 93.5)
 Frequency of urine 0/44 0.0 (0.0 to 8.0) 451/463 97.4 (95.5 to 98.7) 0/12 0.0 (0.0 to 26.5) 451/495 91.1 (88.3 to 93.5)
 Abdominal/vaginal pain 6/44 13.6 (5.2 to 27.9) 424/463 91.6(88.7 to 93.9) 6/45 13.3 (5.5 to 26.8) 424/462 91.8 (88.9 to 94.1)
 Pain during intercourse 0/8 0.0 (0.0 to 36.9) 36/38 94.7 (82.3 to 99.4) 0/2 0.0 (0.0 to 84.2) 36/44 81.8 (67.3 to 91.8)
 Itchy/sore vagina 1/44 2.3 (0.1 to 12.0) 437/457 95.6 (93.3 to 97.3) 1/21 4.8 (0.1 to 23.8) 437/480 91.0 (88.1 to 93.4)
 Malodorous smell 0/42 0.0 (0.0 to 8.4) 450/458 98.3 (96.6 to 99.2) 0/8 0.0 (0.0 to 36.9) 450/492 91.5 (88.6 to 93.8)
 Vaginal discharge 3/43 7.0 (1.4 to 19.1) 410/460 89.1 (85.9 to 91.8) 3/53 5.7 (1.2 to 15.7) 410/450 91.1 (88.1 to 93.6)
 Any symptoms 11/44 25.0 (13.2 to 40.3) 354/463 76.5 (72.3 to 80.3) 11/120 9.2 (4.7 to 15.8) 354/387 91.1 (88.2 to 94.1)
Chlamydia trachomatis
 Heavy menstruation 0/13 0.0 (0.0 to 24.7) 461/494 93.3 (90.6 to 95.4) 0/33 0.0 (0.0 to 10.6) 461/474 97.3 (95.4 to 98.5)
 Between menses bleeding 0/13 0.0 (0.0 to 24.7) 475/494 96.2 (94.1 to 97.7) 0/19 0.0 (0.0 to 17.7) 475/488 97.3 (95.5 to 98.6)
 Burning urine 1/13 7.7 (0.2 to 36.0) 484/494 98.0 (96.3 to 99.0) 1/11 9.1 (0.2 to 41.3) 484/496 97.6 (95.8 to 98.8)
 Frequency of urine 0/13 0.0 (0.0 to 24.7) 481/494 97.4 (95.5 to 98.6) 0/13 0.0 (0.0 to 24.7) 481/494 97.4 (95.5 to 98.6)
 Abdominal/vaginal pain 2/13 15.4 (1.9 to 45.5) 451/494 91.3 (88.5 to 93.6) 2/45 4.4 (0.5 to 15.2) 451/462 97.6 (95.8 to 98.8)
 Pain during intercourse 0/1 0.0 (0.0 to 97.5) 43/45 95.6 (84.9 to 99.5) 0/2 0.0 (0.0 to 84.2) 43/44 97.7 (88.0 to 99.9)
 Itchy/sore vagina 1/13 7.7 (0.2 to 36.0) 467/488 95.7 (93.5 to 97.3) 1/22 4.6 (0.1 to 22.8) 467/479 97.5 (95.7 to 98.7)
 Malodorous smell 0/13 0.0 (0.0 to 24.7) 478/487 98.2 (96.5 to 99.2) 0/9 0.0 (0.0 to 33.6) 478/491 97.4 (95.5 to 98.6)
 Vaginal discharge 2/13 15.4 (1.9 to 45.5) 439/490 89.6 (86.5 to 92.2) 2/53 3.8 (0.5 to 13.0) 439/450 97.6 (95.7 to 98.8)
 Any symptoms 4/13 30.8 (9.1 to 61.4) 377/494 76.3 (72.3 to 80.0) 4/121 3.3 (0.9 to 8.3) 377/386 97.7 (95.6 to 98.9)
Trichomonas vaginalis
 Heavy menstruation 1/12 8.3 (0.2 to 38.5) 464/495 93.4 (90.8 to 95.4) 1/32 2.9 (0.1 to 15.3) 464/475 97.7 (95.9 to 98.8)
 Between menses bleeding 0/12 0.0 (0.0 to 26.5) 475/495 96.0 (93.8 to 97.5) 0/20 0.0 (0.0 to 16.8) 475/487 97.5 (95.7 to 98.7)
 Burning urine 1/12 8.3 (0.2 to 38.5) 485/495 98.0 (96.3 to 99.0) 1/11 9.1 (0.2 to 41.3) 485/496 97.8 (96.1 to 98.9)
 Frequency of urine 0/12 0.0 (0.0 to 26.5) 483/495 97.6 (95.8 to 98.7) 0/12 0.0 (0.0 to 26.5) 483/495 97.6 (95.8 to 98.7)
 Abdominal/vaginal pain 2/12 16.7 (2.1 to 48.4) 452/495 91.3 (88.5 to 93.6) 2/45 4.4 (0.5 to 15.2) 452/462 97.8 (96.1 to 99.0)
 Pain during intercourse 2/2 100 (15.8 to 100) 44/44 100 (92.0 to 100) 2/2 100 (15.8 to 100) 44/44 100 (92.0 to 100)
 Itchy/sore vagina 1/12 8.3 (0.2 to 38.5) 469/489 95.9 (93.8 to 97.5) 1/21 4.8 (0.1 to 23.8) 469/480 97.7 (95.9 to 98.9)
 Malodorous smell 2/12 16.7 (2.1 to 48.4) 482/488 98.8 (97.3 to 100) 2/8 25.0 (3.2 to 65.1) 482/492 98.0 (96.3 to 100)
 Vaginal discharge 2/12 16.7 (2.1 to 48.4) 440/491 89.6 (86.6 to 92.2) 2/53 3.8 (0.5 to 13.0) 440/450 97.8 (96.0 to 98.9)
 Any symptoms 6/12 50.0 (21.1 to 78.9) 381/495 77.0 (73.0 to 80.6) 6/120 5.0 (1.9 to 10.6) 381/387 98.5 (96.7 to 99.4)
Neisseria gonorrhoeae*
 Heavy menstruation 1/3 33.3 (0.8 to 90.6) 472/504 93.7 (91.2 to 95.6) 1/33 3.0 (0.1 to 15.8) 472/474 99.6 (98.5 to 100)
 Between menses bleeding 1/3 33.3 (0.8 to 90.6) 486/504 96.4 (94.4 to 97.9) 1/19 5.3 (0.1 to 26.0) 486/488 99.6 (98.5 to 100)
 Burning urine 1/3 33.3 (0.8 to 90.6) 494/504 98.2 (96.4 to 99.0) 1/11 9.1 (0.2 to 41.3) 494/496 99.6 (98.6 to 100)
 Frequency of urine 0/3 0.0 (0.0 to 70.6) 491/504 97.4 (95.6 to 98.6) 0/13 0.0 (0.0 to 24.7) 491/494 99.4 (98.6 to 99.9)
 Abdominal/vaginal pain 1/3 33.3 (0.8 to 90.6) 460/504 91.3 (88.5 to 93.6) 1/45 2.2 (0.1 to 11.8) 460/462 99.6 (98.5 to 100)
 Itchy/sore vagina 1/3 33.3 (0.8 to 90.6) 477/498 95.8 (93.6 to 97.4) 1/22 4.6 (0.1 to 22.8) 477/479 99.6 (98.5 to 100)
 Malodorous smell 0/3 0.0 (0.0 to 70.7) 488/497 98.2 (96.6 to 99.1) 0/9 0.0 (0.0 to 33.6) 488/491 99.4 (98.2 to 100)
 Vaginal discharge 1/3 33.3 (0.8 to 90.6) 448/500 89.6 (86.6 to 92.1) 1/53 1.9 (0.1 to 10.1) 448/450 99.6 (98.4 to 100)
 Any symptoms 2/3 66.7 (9.4 to 99.1) 385/504 76.4 (72.3 to 80.0) 2/121 1.9 (0.2 to 5.8) 385/386 99.7 (98.6 to 100)

*Pain or bleed during intercourse was limited to 46 girls responding to symptoms of pain or bleeding during sexual intercourse (no data for N. gonorrhoeae).

†4–6 girls did not answer questions on vaginal itching, smell, discharge.

NPV, negative predictive value; PPV, positive predictive value.

Discussion

This study demonstrates over a quarter of young adolescent schoolgirls in a rural African setting had a laboratory-diagnosed RTI. One-third of older aged (16–17 years) girls were infected. The largest contribution to the infection pool was from bacterial vaginosis. The predictive value of reported symptoms was generally very low. Despite this, there remains inadequate data on laboratory-confirmed cases of RTI among school-aged girls in Africa.

This study was nested in a cluster randomised controlled pilot study examining the feasibility of girls’ use of menstrual care products in schools. Sampling bias may have occurred as schools have been shown to be protective against sexual infections such as HIV,19 20 resulting in a lower prevalence of RTI than among non-attending adolescent girls. We acknowledge use of some menstrual items may have potentially reduced some girls’ exposure to RTI,16 21 with outcomes on the effect of different products currently under evaluation. While a high reliability of self-obtained swabs for RTI diagnosis has been demonstrated elsewhere,18 w12 we note girls in our endline focus groups reported a minority of their peers avoided swabbing by spitting on the swabs. Such swabs were processed in the denominator and would have also possibly lowered the prevalence of girls with detected infections. Less than 1% of girls said they had sexual intercourse in the past month, and 9% answered a question on symptoms occurring during sex at face-to-face interview. This is an underestimate, as in a private self-completed survey 28% reported sexual exposure (unpublished). Studies in Kenya and Tanzania estimated up to a threefold higher prevalence of sexual exposure (including coerced) when girls self-completed surveys, for example, by computer.22 w13 No clinical examination of individuals was conducted, thus, the presence of a lesion (ulcer) relied on girls’ reporting an itchy/sore vagina. We cannot rule out that girls when faced with intimate questions about vaginal discharge or pain may have been too embarrassed, or too scared, to disclose symptoms face-to-face in the nurses’ interview.23 They may also be less familiar with their bodily ‘norm’ so symptoms may have gone unnoticed. Moreover, due to financial constraints, examination of other RTI such as syphilis and HSV-2 was not possible and we recommend that studies include these also to ensure comprehensive mapping of infection, and healthcare needs of adolescent girls.

Synonymous with our findings, a study conducted in South Africa reported symptomatic vaginal discharge among high-risk girls and women was a poor predictor of RTI and genital tract inflammation (sensitivity of 12.3% and specificity of 93.8%), with 87.7% of laboratory-diagnosed infections having no accompanying clinical symptoms.24 Similarly, a study in Botswana reported three-quarters of pregnant women attending antenatal clinics were asymptomatic.25 Syndromic management failed to capture half of women with T. vaginalis or bacterial vaginosis infections during antenatal care, leading to significant challenges for diagnosis and treatment among this critically vulnerable group.25 Adding to the evidence from South Africa26 and Botswana,25 27 our data suggest that the syndromic approach is not a good enough indicator of RTI, and new approaches are needed.

A study among African females found a high prevalence of bacterial vaginosis was associated with recent unprotected sexual intercourse.26 Among adolescent girls from South Africa and Kenya, 16–17-year-old sexually active girls reported minimal symptoms (2/60; 3.3%) while the prevalence of laboratory-confirmed RTI was very high (in 60 girls, 23 were diagnosed with bacterial vaginosis, 12 with C. albicans, 4 with T. vaginalis and 4 with C. trachomatis).26 28 w14

The relationship between bacterial vaginosis, N. gonorrhoeae, C. trachomatis and genital ulcer disease, and the increase in the risk of HIV transmission,3 5–8 w2–3 makes early detection and diagnosis of RTI a major public health imperative.2 w15 Studies in western Kenya among the Luo show a rapid rise in HIV and HSV-2 prevalence during adolescence among girls,11 suggesting that many of our schoolgirls not already infected with HIV are at further risk of acquiring HIV due to their RTI-infected status. A reduction in prevalence is possible, for example, in Tanzania in areas where women had improved access to laboratory diagnosis and treatment of RTIs, incident HIV infections were reduced by 40%.29 T. vaginalis infection is a common curable sexually transmitted infection with high prevalences observed in the African subcontinent.2 However, this vaginal condition may cause substantial morbidity among women in developing countries if untreated. No comparison study was available among adolescents; however, among pregnant women in Botswana, T. vaginalis was found in 19% and bacterial vaginosis in 38% of the study participants.25 Unless drastic measures are put into place, the high prevalence of infections found in young adolescent girls is likely to remain undetected and untreated, leading to a rising pool of infection in the local population, increasing morbidity and reducing their fertility, as well as increasing their risk of other RTI and HIV.

From our data, we have identified three priority areas for public health intervention among this female adolescent population. First, girls need to learn self-awareness of their own bodies to be able to recognise any changes in order that symptoms are detected as being different from their normal state. Second, girls need to understand that it is possible to have an RTI despite having no symptoms. Third, methods to achieve prevention must be made readily available to adolescent girls. Our data, combined with other findings, point to the urgent need for sexual and reproductive health education, including a focus on personal hygiene, combined with the provision of friendly sexual and reproductive health services including treatment and counselling services. The latter must be easily accessible to girls who have little free time and no resources to travel. Without such interventions, it is difficult to envisage any real progress in reducing the prevalence of RTI, poor maternal health outcomes and HIV acquisition.3 w15 One solution, in part, may be school-based,30 through school nurses who, as well as treating and referring girls to specialist services, could educate and counsel girls as they reach menarche and become sexually active.

In summary, our study adds to a sparse body of literature, showing a high prevalence of RTI among school-aged girls in a rural African setting. The majority of infections were asymptomatic, demonstrating a very poor sensitivity of symptom-based reporting. The use of syndromic management to reduce RTI and HIV incidence in this adolescent population would leave most of these very vulnerable girls untreated (even if they would present to a health clinic). Technological advancements that can enable quick, easy and cost-effective diagnosis of RTIs may be a desirable step towards realising effective management of reproductive health in rural African settings.

Key messages.

  • Adolescent schoolgirls in rural Kenya have a high prevalence of reproductive tract infections.

  • Symptom-based reporting has a poor sensitivity missing three-quarters of laboratory-confirmed infections.

  • Greater public health efforts are required to diagnose and treat infections among vulnerable girls to minimise long-term sequelae.

Supplementary Material

Web supplement 1
Web supplement 2
Web supplement 3

Acknowledgments

The authors are grateful to the participants, their parents, the schools and community for their assistance with this study. The authors thank the study nurses, field staff and laboratory support staff for their contributions. The KEMRI/CDC HDSS is a member of the Indepth Network. The director, KEMRI, approved the manuscript for publication.

Footnotes

Handling editor: Jackie A Cassell

Contributors: EK, NO, CO, EN and KOO collected the data and were involved with writing the manuscript. KFL, LM, JV, CZ and PAP-H designed the study and obtained the funding. NO and PAP-H analysed the data. EK, CO, AB and PAP-H wrote the manuscript. All authors reviewed and approved the manuscript.

Funding: This study was funded by the UK Joint Global Health Trials award as part of the menstrual feasibility study (grant G1100677/1).

Disclaimer: The findings and conclusions of this report are those of the authors and do not necessarily represent the official position of the CDC.

Competing interests: None declared.

Patient consent: Written informed consent and assent from parents and girls, respectively, were required for participation.

Ethics approval: The study was approved by KEMRI's National Ethical Review Committee (ethics number: 2198) and the Liverpool School of Tropical Medicine's Ethics Committee (ethics number: 12.11). The Institutional Review Board of the US Centers for Disease Control and Prevention approved a non-engaged waiver.

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

Data sharing statement: All study data are presented in the paper.

References

  • 1.WHO. Report on global sexually transmitted infection surveillance. Geneva, Switzerland: World Health Organization, 2013. [Google Scholar]
  • 2.WHO. Global prevalence and incidence of selected curable sexually transmitted infections. Geneva, Switzerland: World Health Organization, 2001. [Google Scholar]
  • 3.Cohen CR, Lingappa JR, Baeten JM, 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 10.1371/journal.pmed.1001251 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Mitchell C, Balkus JE, Fredricks D, 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. 10.1089/AID.2012.0187 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Balkus JE, Richardson BA, Rabe LK, et al. . Bacterial vaginosis and the risk of trichomonas vaginalis acquisition among HIV-1-negative women. Sex Transm Dis 2014;41:123–8. 10.1097/OLQ.0000000000000075 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Cherpes TL, Meyn LA, Krohn MA, et al. . Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis. Clin Infect Dis 2003;37:319–25. 10.1086/375819 [DOI] [PubMed] [Google Scholar]
  • 7.Wiesenfeld HC, Hillier SL, Krohn MA, et al. . Bacterial vaginosis is a strong predictor of Neisseria gonorrhoeae and Chlamydia trachomatis infection. Clin Infect Dis 2003;36:663–8. 10.1086/367658 [DOI] [PubMed] [Google Scholar]
  • 8.Gillet E, Meys JF, Verstraelen H, et al. . Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: a meta-analysis. BMC Infect Dis 2011;11:10 10.1186/1471-2334-11-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Caixeta RC, Ribeiro AA, Segatti KD, et al. . Association between the human papillomavirus, bacterial vaginosis and cervicitis and the detection of abnormalities in cervical smears from teenage girls and young women. Diagn Cytopathol 2015;43:780–5. 10.1002/dc.23301 [DOI] [PubMed] [Google Scholar]
  • 10.Yi TJ, Shannon B, Prodger J, et al. . Genital immunology and HIV susceptibility in young women. Am J Reprod Immunol 2013;69(Suppl 1):74–9. 10.1111/aji.12035 [DOI] [PubMed] [Google Scholar]
  • 11.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 10.1371/journal.pone.0006470 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Buve A, Weiss HA, Laga M, et al. . The epidemiology of trichomoniasis in women in four African cities. AIDS 2001;15(Suppl 4):S89–96. 10.1097/00002030-200108004-00010 [DOI] [PubMed] [Google Scholar]
  • 13.Buve A, Weiss HA, Laga M, et al. . The epidemiology of gonorrhoea, chlamydial infection and syphilis in four African cities. AIDS 2001;15(Suppl 4):S79–88. 10.1097/00002030-200108004-00009 [DOI] [PubMed] [Google Scholar]
  • 14.WHO. Guidelines for the management of sexually transmitted infections. Geneva, Switzerland: World Health Organisation, 2003. [Google Scholar]
  • 15.Romoren M, Hussein F, Steen TW, et al. . Costs and health consequences of chlamydia management strategies among pregnant women in sub-Saharan Africa. Sex Transm Infect 2007;83:558–66. 10.1136/sti.2007.026930 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Das P, Baker KK, Dutta A, et al. . Menstrual Hygiene Practices, WASH Access and the Risk of Urogenital Infection in Women from Odisha, India. PLoS ONE 2015;10:e0130777 10.1371/journal.pone.0130777 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Alexander K, Oduor C, Nyothach E, et al. . Water, sanitation and hygiene conditions in Kenyan rural schools: are schools meeting the needs of menstruating girls? Water 2014;6:1453–66. 10.3390/w6051453 [DOI] [Google Scholar]
  • 18.Tanksale VS, Sahasrabhojanee M, Patel V, et al. . The reliability of a structured examination protocol and self administered vaginal swabs: a pilot study of gynaecological outpatients in Goa, India. Sex Transm Infect 2003;79:251–3. 10.1136/sti.79.3.251 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Hallfors D, Cho H, Rusakaniko S, et al. . Supporting adolescent orphan girls to stay in school as HIV risk prevention: evidence from a randomized controlled trial in Zimbabwe. Am J Public Health 2011;101:1082–8. 10.2105/AJPH.2010.300042 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Hargreaves J, Morison L, Kim J, et al. . The association between school attendance, HIV infection and sexual behaviour among young people in rural South Africa. J Epidemiol Community Health 2008;62:113–19. 10.1136/jech.2006.053827 [DOI] [PubMed] [Google Scholar]
  • 21.Phillips-Howard P, Olilo G, Burmen B, et al. . Menstrual needs and associations with sexual and reproductive risks in rural Kenyan females: a cross-sectional behavioural survey linked with HIV prevalence. J Womens Health 2015;24:1–11. 10.1089/jwh.2014.5031 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Hewett PC, Mensch BS, Erulkar AS. Consistency in the reporting of sexual behaviour by adolescent girls in Kenya: a comparison of interviewing methods. Sex Transm Infect 2004;80(Suppl 2):ii43–8. 10.1136/sti.2004.013250 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Plummer ML, Wight D, Ross DA, et al. . Asking semi-literate adolescents about sexual behaviour: the validity of assisted self-completion questionnaire (ASCQ) data in rural Tanzania. Trop Med Int Health 2004;9:737–54. 10.1111/j.1365-3156.2004.01254.x [DOI] [PubMed] [Google Scholar]
  • 24.Mlisana K, Naicker N, Werner L, et al. . Symptomatic vaginal discharge is a poor predictor of sexually transmitted infections and genital tract inflammation in high-risk women in South Africa. J Infect Dis 2012;206:6–14. 10.1093/infdis/jis298 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Romoren M, Velauthapillai M, Rahman M, et al. . Trichomoniasis and bacterial vaginosis in pregnancy: inadequately managed with the syndromic approach. Bull World Health Organ 2007;85:297–304. 10.2471/BLT.06.031922 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Jespers V, Crucitti T, Menten J, et al. . Prevalence and correlates of bacterial vaginosis in different sub-populations of women in sub-Saharan Africa: a cross-sectional study. PLoS ONE 2014;9:e109670 10.1371/journal.pone.0109670 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Romoren M, Sundby J, Velauthapillai M, et al. . Chlamydia and gonorrhoea in pregnant Batswana women: time to discard the syndromic approach?. BMC Infect Dis 2007;7:27 10.1186/1471-2334-7-27 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Jespers V, van de Wijgert J, Cools P, et al. . The significance of Lactobacillus crispatus and L. vaginalis for vaginal health and the negative effect of recent sex: a cross-sectional descriptive study across groups of African women. BMC Infect Dis 2015;15:115 10.1186/s12879-015-0825-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Grosskurth H, Mosha F, Todd J, et al. . Impact of improved treatment of sexually transmitted diseases on HIV infection in rural Tanzania: randomised controlled trial. Lancet 1995;346:530–6. 10.1016/S0140-6736(95)91380-7 [DOI] [PubMed] [Google Scholar]
  • 30.Plummer ML, Wight D, Wamoyi J, et al. . Are schools a good setting for adolescent sexual health promotion in rural Africa? A qualitative assessment from Tanzania. Health Educ Res 2007;22:483–99. 10.1093/her/cyl099 [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Web supplement 1
Web supplement 2
Web supplement 3

Articles from Sexually Transmitted Infections are provided here courtesy of BMJ Publishing Group

RESOURCES