Background Limited data document sexually transmitted infections (STIs) among pregnant adolescents in sub-Saharan Africa, where prenatal screening typically includes only HIV and syphilis. Given that HIV incidence in this population is among the world's highest, we sought to assess the prevalence and factors associated with STIs in a population of rural pregnant adolescents in Tanzania.
Methods We enrolled 403 pregnant adolescent girls from 10 antenatal clinics near Mwanza, Tanzania. Girls answered structured interviews about sexual health and risk factors and were tested for six common STIs.
Results 199 girls (49.4%) had at least one STI. Herpes Simplex Virus- Type 2 was most prevalent (139 girls, 34.5%), followed by trichomoniasis (54 girls, 13.4%), chlamydia (46 girls, 11.4%), gonorrhoea (27 girls, 6.7%), syphilis (21 girls, 5.2%) and HIV (30 girls, 4.7%). Of note, 53/199 (26.6%) of girls with laboratory-proven STIs were asymptomatic. On multivariable analysis, the presence of any STI was associated with being in a long-term (as opposed to short-term) relationship (OR=2.6 (1.4 to 4.9) p=0.004), younger age at first sexual debut (OR=0.9 per year (0.8 to 0.99), p=0.034), increasing age difference between the girl and her partner (OR=1.1 (1.0 to 1.1) per year, p=0.03) and history of prior pregnancy (OR=1.6 (1.0 to 2.6), p=0.04).
Conclusions STIs affected half of rural pregnant adolescents in Tanzania. Our work demonstrates the urgent need to incorporate routine STI testing into antenatal care in Tanzania to prevent morbidity and mortality in young girls and their babies. We also identify behavioural and demographic risk factors that can be used to target interventions to those at highest risk.
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Pregnancy and childbirth complications are the second leading cause of death among girls aged 15–19 years worldwide.1 ,2 Adolescents also experience 30% more obstructed labour and account for 80% of vesico-vaginal fistulae worldwide.3 ,4 Sexually transmitted infections (STIs) may also contribute to this morbidity and mortality. Adolescents are at higher risk for STIs due both to increased biological susceptibility to STIs as well as to behavioural and social factors that may lead adolescent girls to more risky sexual encounters.5–7 Various hospital-based and community-based studies in Tanzania suggest that both pregnant women and adolescent girls have high STI rates,8–10 though these studies did not focus on pregnant adolescents, in whom the confluence of two risk factors likely amplifies infection rates. Undiagnosed and untreated STIs in adolescents have the potential for inflicting greater disability over more life-years, as well as causing irreversible effects, including infertility, miscarriage, congenital abnormalities and stillbirths.11–13
Pregnant women in Tanzania are routinely screened only for HIV and syphilis.14 The standard of care for diagnosis and treatment of other STIs is symptom based. This leads to untreated infections in asymptomatic women. Adolescents, even if symptomatic, may be less likely to receive treatment due to barriers to seeking care or difficulties disclosing their symptoms to healthcare workers.8 ,15 ,16 We sought to bridge this gap by performing a large, multi-community survey of pregnant adolescent girls to determine the prevalence and the clinical, demographic, behavioural and knowledge factors associated with common STIs. We hypothesised that the burden of STIs would be elevated in this high-risk group, and that girls’ knowledge about STI prevention and treatment would be poor. Our goal was to identify patterns and risk factors that would allow optimisation of prevention efforts in addressing the reproductive health needs of this vulnerable population.
Patients and methods
Setting and study population
This was a cross-sectional study conducted over a 9-month period in Mwanza city and its surrounding rural districts in northwest Tanzania. The study enrolled girls aged 20 years and below who were pregnant and attending antenatal clinics in the Magu, Misungwi, Ngudu, Ilemela, Nyamagana, Geita and Ukerewe districts of the Mwanza region. The fertility rate in this age group in Tanzania is 139/1000 for rural girls and 75/1000 for girls living in urban areas.17 We invited all adolescents who were attending the antenatal clinic on study days to participate. In order to maximise our efficiency, we enrolled adolescents on Mondays and Tuesdays as these days had the highest antenatal clinic attendance. Adolescents were excluded if they refused counselling and testing for HIV, if they were currently receiving antimicrobial treatment for an STI or HIV or if they did not complete all study procedures.
After providing written informed consent, adolescent girls first underwent a private interview in which they were asked sociodemographic, medical, behavioural and knowledge questions. The interview tools were developed in English and then translated into Kiswahili. Prior to data collection, all tools were pretested in a group of girls at one of the study sites and additional adjustments were made as necessary. Interviews were conducted in Kiswahili by the female principal investigator or by a female nurse trained to provide HIV counselling and testing. Based on the WHO's ‘10 facts on STIs’,18 study participants were asked questions that assessed their knowledge of STIs.
Girls were asked to provide urine for Neisseria gonorrhoeae (NG)/Chlamydia trachomatis (CT) testing. A swab of vaginal secretions was collected from the vaginal introitus for wet preparation and microscopic examination for diagnosis of Candida (using a potassium hydroxide solution), Trichomonas vaginalis (using a normal saline wet mount) and bacterial vaginosis by Nugent's criteria.15 ,19 The results for candidiasis and trichomoniasis were given on the screening day, together with treatment for STIs as indicated according to Tanzanian national guidelines.20 Girls with genital ulcers were started on oral acyclovir and injection Benzathine penicillin.
HIV voluntary counselling and testing was offered to all participants by the nurse counsellor. For those who agreed, a total of 5 mL of whole blood was collected, and a drop of this blood was used for on-site HIV rapid testing by the Determine HIV-1/HIV-2 Test Kit (Abbott Laboratories, Abbott Park, Illinois, USA). Determine-positive tests were confirmed using the Uni-Gold Recombigen rapid HIV test (Trinity Biotech PLC, Wicklow, Ireland). Girls were classified as HIV infected if both Determine and Unigold tests were positive, and as HIV uninfected if the Determine was negative. Testing was performed in the field and patients received their results immediately. Those with confirmed positive tests were referred to HIV Care and Treatment Clinics for further care and prevention of Mother-to-Child Transmission of HIV services. In case of discordant results (positive Determine with negative Uni-Gold test), blood samples were retested using RNA PCR at the Bugando Medical Centre reference laboratory. Those found to be positive by RNA PCR were considered positive for HIV.
The rest of the blood sample was centrifuged to separate serum each afternoon upon return to Bugando Medical Centre. Serum was transported to the National Institute for Medical Research laboratory to be screened for syphilis using the rapid plasma reagin (RPR) test (Becton Dickinson, Maryland, USA). RPR-positive samples were confirmed with the Treponema pallidum Particle Agglutination Assay (TPPA, Serodia Fujirebio Inc, Japan), with a positive result for both TPPA and RPR regarded as indicative of active syphilis. Herpes Simplex Virus- Type 2 (HSV-2) antibody was detected by the type-specific HSV-2 ELISA test (Kalon Biologicals, Guildford, UK).
DNA was purified from urine and tested for CT/NG using Amplicor CT/NG specimen preparation, amplification, internal control and detection kits (Roche Molecular Systems, Branchburg, New Jersey, USA). Gonorrhoea results were confirmed by 16S rRNA PCR testing.
Permission to conduct this study was obtained from the Mwanza regional medical officer and district medical officers and clinical health professionals stationed at participating district hospitals and health centres.
The study was explained to girls in a large group and subsequently one on one by a trained study nurse fluent in Kiswahili and the local languages (Kisukuma, Kikerewe). In order to participate in the study, girls were asked to provide written informed consent. Pregnant adolescents younger than 18 years provided written assent and their parent or guardian provided written assent. Those unable to write were asked to place their thumb print on the consent form.
Study data were managed using REDCap electronic data capture tools hosted at WCMC and analysed using Stata V.12 (College Station, Texas, USA). Continuous variables were summarised by median and IQR and categorical variables were summarised by frequency and percentage. Factors significantly associated with STIs on univariable analysis were examined by multivariable logistic regression. We used backward elimination, deleting the least significant factor one by one, to reach the final model that included significant factors only. Associations between factors were summarised as ORs along with 95% CIs and associated p values.
From April to December 2012, a total of 1298 women attended antenatal clinics on enrolment days and out of these 442 (34%) were adolescents. Our team invited 426 out of 442 girls to participate in the study; the other 16 girls left the clinic prior to invitation. Twenty chose not to participate and were excluded, and three girls were unwilling to provide a vaginal swab sample. None of the girls reported prior history of HIV or any STI. Therefore, a total of 403/426 (95%) girls consented or assented with parent/guardian consent for study participation and completed all study procedures.
Characteristics of study participants are shown in table 1. Girls’ ages ranged from 14 to 20 years, with the majority of girls being age 17 and above. Approximately two-thirds (258 girls, 64%) had completed primary school (7 years) and had no further education, while 33 (8.2%) of the girls had never attended any formal school. The majority of girls reported cohabiting with their partner, with only 46 (11.4%) in formal marriages. Over one-fourth of girls (87) knew that their partner had other partner(s) outside of their relationship; this was not significantly different among girls of different religions. Forty-one per cent of girls (164) had previously been pregnant. Approximately three-fourths of girls (297) reported having had more than one sexual partner in their lives, and girls’ sexual partners were a median of 7 years (IQR, 4–9) older than they were. More than half of girls (230, 57.1%) presented with signs and symptoms suggesting genital tract infection.
Prevalence of STIs
A total of 199/403 (49.4%) girls were found to have at least one STI (table 2). HSV-2 was the most common STI found in 139 (34.7%) girls, and 19 girls (4.7%) had HIV. Prevalences of other STIs were as follows: gonorrhoea 27 (6.7%), chlamydia 46 (11.4%), syphilis 21(5.2%) and trichomoniasis 54 (13.4%). A total of 30 girls had HIV, syphilis or both of these and would have been diagnosed during routine prenatal care. The remaining 169/403 (42%) would not likely have received diagnosis or treatment. Apart from STIs, many girls also presented with other genital infections, including candidiasis (71, 17.6%) and bacterial vaginosis (102, 25.3%).
Patterns of STIs
Among 199 girls with STIs, 7 (3.5%) had an ulcerative STI, 108 (54.3%) presented with vaginal discharge and 69 (34.7%) presented with other symptoms, the next most common of which were vaginal itching and painful micturition (table 2). Having more than one STI simultaneously occurred in 77/199 girls (38.7%) and was particularly common among those with gonorrhoea, chlamydia and syphilis. Nearly all girls with candidiasis (61, 85.7%) reported discharge, itching, dysuria or other symptoms. Of note, 53 (26.6%) presented with no symptom at all and therefore would not have received any STI screening or treatment according to the Tanzanian national guidelines.
Knowledge of STIs
Most girls lacked basic information about STIs (table 3). Although 86% of girls (348) knew that STIs exist, only 43% (175) knew that gonorrhoea, HIV or syphilis are STIs, and 99% (400) had not heard of genital herpes. Although 42% (168) knew that condoms prevent STIs, and 30% (121) of the girls admitted thinking that they were at risk of STIs and HIV, only 6% (25) of the girls reported regularly using condoms. Only 97 girls (24.1%) knew that they could transmit STIs to their unborn children, and 162 (40.2%) knew that STIs could cause infertility. Fifty-four girls (11.4%) did not know how STIs are transmitted and 77 girls (19.1%) did not know that STIs can be prevented. The most common misperceptions about STI prevention related to condoms, with 106 girls (26%) stating that condoms were ‘useless’ to prevent STIs or pregnancy. Others asserted that condoms were not effective in permanent couples (110, 27.3%), and more than one-fourth believed that they did not need to use condoms while pregnant because they were not susceptible to STIs (105, 26%).
Factors associated with STIs
We examined associations between the characteristics presented in table 1 and the presence of any of the six STIs. All characteristics that were associated with STIs with p values <0.10 on univariable analysis are presented in table 4. When subjected to multivariable analysis, factors that remained significantly associated with STIs included larger age difference between a girl and her partner (OR=1.1 (1.0 to 1.1) per increasing year difference, p=0.03), characterising the relationship as long term as opposed to short term (OR=2.6 (1.4 to 4.9), p=0.004) and a history of prior pregnancy (OR=1.6 (1.0 to 2.6), p=0.04).
One-half (199) of pregnant adolescent girls in northwest Tanzania had at least one STI. In a setting in which screening only for HIV and syphilis is routinely offered at antenatal clinic visits, this would have meant that over 40% of the entire study population (164 girls) would have remained undiagnosed and untreated. These infections could have major, irreversible health ramifications for these young girls and their unborn babies. Our work suggests that screening this vulnerable population for STIs needs to be incorporated as a routine part of adolescent prenatal care.
The most commonly diagnosed STI in this study, HSV-2 (139, 34.5%), is also one of the most devastating for neonates. Our findings, with over 30% of girls being HSV-2 seropositive a median of 3 years after initiation of sexual activity, corroborate a prospective study from Mwanza in 2002 that demonstrated annual HSV-2 incidence among adolescent girls to be ∼10%.21 We found that seven girls had active genital ulcers potentially attributable to HSV-2. When present during vaginal delivery, viral shedding from HSV-2 genital ulcers transmits infection to ∼40% of neonates during primary maternal HSV-2 infection and ∼3% during recurrence.22 HSV in neonates, particularly when not diagnosed and treated early, typically has catastrophic effects, including permanent neurological damage and death.23 Because neonatal transmission can be lessened with oral acyclovir for mothers and caesarean sections when genital ulcers are present,24 aggressive identification and treatment for mothers with symptomatic HSV-2 infection should be a major public health priority.
Furthermore, our findings highlight the importance of adding routine screening for other STIs, such as gonorrhoea and chlamydia, to current antenatal clinic procedures in Tanzania. Over 15% of girls in this study had gonorrhoea and/or chlamydia, and ∼30% of these girls were asymptomatic, suggesting that, even if pregnant girls did routinely receive treatment for symptomatic STIs, at least 30% would have remained undiagnosed. Dangers to babies of pregnant women with untreated gonorrhoea and chlamydia include prematurity (both infections), conjunctivitis and pneumonia (chlamydia) and ophthalmia neonatorum and disseminated infection (gonorrhoea). With the development of rapid CT/NG test capability using the Gene Xpert format25 and the increasing dispersal of these machines in resource-limited settings, same-day testing and treatment for these infections is becoming an achievable goal to improve both maternal and child health. As an illustrative model, the implementation of routine point-of-care syphilis testing for pregnant women in sub-Saharan Africa has been recently estimated to reduce stillbirths, neonatal deaths and congenital syphilis cases by 64 000, 25 000 and 32 000 per year, respectively, and to reduce disability-adjusted life-years by 2.6 million.26 Our data suggest that similar efforts now have the potential to reduce disease burden from undiagnosed CT/NG infections in newborns and in their mothers in Africa.
Our work identifies several important social characteristics that were associated with higher odds of having STIs in our study population. The presence of STIs was associated with a larger age difference between the girl and the partner and, interestingly, with a girl characterising her relationship with her partner as ‘long term’. Evidence demonstrates that in both of these situations, girls may feel that they have less need (or less negotiating ability) to request condom use.27–29 Girls who had already been pregnant at least once were also more likely to have an STI—again, possibly reflecting their inadequate use of condoms. It may be possible to use these findings to target screening, if resources are limited, to higher-risk adolescent girls who have older partners, ‘long-term’ relationships and history of prior pregnancy.
Of large public health importance, we noted that many adolescent girls possess minimal or erroneous knowledge about STIs. This corresponds with other local work that has demonstrated that myths and incorrect beliefs regarding STIs and childbearing are widespread in this region.30 Notably, nearly 80% of girls have at least attended primary school, suggesting that intensifying efforts to provide health education to girls in late primary school may be a simple way to provide vital reproductive health information to the large majority of girls. Important teaching topics highlighted by our study findings include signs, symptoms and side effects of STIs and methods of both STI and pregnancy prevention. As others have suggested, for this to be successful, teachers will need to be empowered to discuss sensitive health topics.31 Increasing adolescents’ knowledge of STI symptoms and sequelae may lead those with symptoms (who, in our study, were the majority of infected girls) to be more bold in admitting their symptoms and seeking treatment.
In conclusion, we identified disturbingly high rates of STIs in adolescent pregnant girls and revealed numerous possibilities for action. We suggest, for a start, that antenatal clinics urgently need more support so that routine STI screening with genital examination becomes standard for adolescents. Girls should be asked directly about symptoms and treated aggressively, whether syndromically in the absence of testing capabilities or with pathogen-directed therapy when more advanced diagnosis is possible. Clinical protocols should include screening women for genital ulcers beginning by week 36 with referrals for caesarean section if present. Educational strategies could include teaching girls about STI symptoms and long-term risks, including to their babies, as well as the potential risks of dating men far older than themselves. Further studies are currently underway to gather more qualitative information from girls who participated in this study in order to learn how to make reproductive healthcare more accessible for adolescents in order to begin to stem the large tide of STIs in this vulnerable population.
Half of pregnant adolescents in Tanzania had at least one sexually transmitted infection (STI), and 169 girls (40%) would have remained undiagnosed under current care standards.
Antenatal clinics urgently need more support to provide routine STI screening for pregnant adolescents in order to prevent neonatal morbidity and mortality.
Girls at highest risk are those who may have little negotiating power, such as those in longer-term relationships and those whose partners are substantially older.
Handling editor Jackie A Cassell
Acknowledgements The authors wish to thank the patients at health centres for their willing participation in this study. Sincere thanks also to Mrs Theresia Matulile and Mrs Juliana Dogani for their extensive work during data collection, and to the BMC and NIMR laboratories for sample processing and testing.
Contributors AH: conceptualised and designed the study, carried out all data collection, performed analysis, drafted the manuscript and approved the final manuscript. AK: assisted with designing the study, data collection, performed the analysis, revised the manuscript and approved the final manuscript. PH: assisted with data collection, data entry, data analysis and approved the final manuscript. SEK: assisted with study design, data analysis and approved the final manuscript. JMC: designed the study, assisted with data analysis and revised and approved the final manuscript. DWF: conceptualised and designed the study, supervised the data analysis and manuscript drafting and revised and approved the final manuscript. JAD: conceptualised and designed the study, supervised data collection and data entry, supervised data analysis and manuscript drafting and approved the final manuscript.
Funding This work was supported in part by grants from the US National Institutes of Health (National Institute of Allergy and Infectious Diseases (K24 AI098627 and K23AI110238); National Center for Advancing Translational Sciences (UL1 TR000457-06); Fogarty International Center (TW00018)) and by a US Agency for International Development (USAID) leadership development programme.
Competing interests None.
Ethics approval Ethical approval was granted by the research ethics committee at Bugando Medical Centre (BREC/001/02/2012), by the medical research coordinating committee of the National Institute for Medical Research in Tanzania (NIMR/HQ/R.8a/Vol. IX/826) and by the institutional review board at Weill Cornell Medical College (WCMC Protocol #0811010105).
Provenance and peer review Not commissioned; externally peer reviewed.