Sexually Transmitted Diseases:
Incidence and Correlates of Chlamydia trachomatis Infection in a High-Risk Cohort of Kenyan Women
Masese, Linnet MBChB, MPH*; Baeten, Jared M. MD, PhD*†‡; Richardson, Barbra A. PhD‡§¶; Deya, Ruth MBChB∥; Kabare, Emmanuel BSc∥; Bukusi, Elizabeth MBChB, MMed, MPH, PhD‡**††; John-Stewart, Grace MD, PhD*†‡; Jaoko, Walter MBChB, PhD∥; McClelland, R. Scott MD, MPH*†‡∥
From the Departments of *Epidemiology, †Medicine, ‡Global Health, and §Biostatistics, University of Washington, Seattle, WA; ¶Fred Hutchinson Cancer Research Center, Seattle, WA; Departments of ∥Medical Microbiology and **Obstetrics and Gynecology, University of Nairobi, Nairobi, Kenya; ††Kenya Medical Research Institute, Nairobi, Kenya
The authors thank the women who took part in this study for their commitment to participate as part of the research cohort. They also thank their clinical, laboratory, outreach, and administrative staff for their time and effort. They are grateful to the Municipal Council of Mombasa for providing clinical space at Ganjoni Municipal Clinic and to Coast Provincial General Hospital for providing laboratory space.
Supported by the National Institutes of Health (NIH; Grant P01 HD 64915). Two of the authors received training support from the Fogarty International Center (NIH 5D43-TW000007 to L.M. and R.D.). Additional support for the Mombasa Field Site was received from the University of Washington and Fred Hutchinson Cancer Research Center’s Center for AIDS Research, an NIH-funded program (P30-AI-27757). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Potential conflicts of interest: None declared.
R.S.M., L.M., J.M.B., B.A.R., G.J-S, E.B., and W.J. conceived the question and designed the study. R.S.M. obtained funding for the study. L.M., R.S.M., J.M.B., B.A.R., E.K., and R.D. participated in the collection and interpretation of the data. L.M, J.M.B., and B.A.R. conducted the data analyses. All authors participated in the preparation of the manuscript and approved the final draft for submission.
Correspondence: Linnet Masese, MBChB, MPH, Department of Epidemiology, University of Washington, HMC Box 359909, 325 9th Ave, Seattle, WA 98104-2499. E-mail: firstname.lastname@example.org.
Received for publication April 25, 2012, and accepted September 5, 2012.
Background: In Africa, data on Chlamydia trachomatis infection are scarce because reliable diagnosis is costly and not widely available. Our objective was to evaluate the incidence and correlates of C. trachomatis infection among high-risk Kenyan women.
Methods: We conducted prospective cohort analyses using data from a cohort of women who reported transactional sex. C. trachomatis testing was performed using the Gen-Probe Aptima GC/CT Detection System. We used Andersen-Gill proportional hazards modeling to evaluate correlates of C. trachomatis.
Results: Between August 2006 and December 2010, 865 women contributed 2011 person-years of observation. Sixty-four women experienced 101 episodes of C. trachomatis infection (incidence rate, 5.0/100 person-years). There was a large difference in incidence by age group: those younger than 25 years had an incidence of 27.6 per 100 person-years (95% confidence interval [CI], 16.3–46.5), those 25 to 34 years old had an incidence of 8.4 per 100 person-years (95% CI, 6.4–11.0), and those 35 years and older had an incidence of 2.6 per 100 person-years (95% CI, 1.8–3.6). In multivariate analyses, younger age (<25 and 25–34 years vs. ≥35 years; hazard ratio [HR], 8.5 [95% CI, 4.1–17.7] and 2.9 [95% CI, 1.7–5.0], respectively), depot medroxyprogesterone acetate use (HR, 1.8; 95% CI, 1.1–3.0), and recent Neisseria gonorrhoeae infection (HR, 3.3; 95% CI, 1.5–7.4) were significantly associated with increased risk of acquiring C. trachomatis infection.
Conclusions: The high incidence of C. trachomatis among younger high-risk women suggests the need for screening as an important public health intervention for this population.
In 1999, the World Health Organization estimated the global incidence of Chlamydia trachomatis infection to be 92 million cases worldwide, with 16 million (17%) occurring in Africa.1 However, estimates from resource-constrained settings including most of Africa are imprecise due to lack of surveillance, limited laboratory infrastructure and diagnostic capacity, and the widespread use of syndromic management. The few community-based studies that have measured C. trachomatis in sub-Saharan Africa suggest a low prevalence in the general population (1.6%–3.2%).2,3 A cross-sectional study among female adolescents in Uganda estimated C. trachomatis prevalence at 4.5%.4 Prevalence is much higher among high-risk groups when compared with community data. For example, prevalence estimates among female sex workers range from 9% in Nairobi, Kenya,5 to 28.5% in Dakar, Senegal.6
Incidence studies are particularly valuable in understanding the risk of a disease. Studies of the incidence of C. trachomatis infection in Africa are few.5,7,8 Among women attending family planning clinics in Zimbabwe and Uganda, the incidences of C. trachomatis were 3.6 and 4.1 per 100 person-years, respectively.8 In the past decade, 2 studies of female sex workers in Kenya have reported incidence rates of 6.5 and 9.0 per 100 person-years, respectively.5,7
Less than 10% of women infected with C. trachomatis develop immediate signs and symptoms of infection.9 The absence of symptoms in most of those infected results in a substantial number of cases that are unrecognized, untreated, and persist as a reservoir for ongoing transmission. In addition, immunity to C. trachomatis infection is partial and short-lived,10 so reinfection is common. C. trachomatis is associated with a number of serious reproductive health problems such as pelvic inflammatory disease, tubal infertility, ectopic pregnancy, and chronic pelvic pain.11 In addition, C. trachomatis infection has been associated with increased risk of HIV-1 acquisition.8,12 These data highlight the importance of screening and treatment of C. trachomatis to prevent the spread of this infection and related complications.
To add to the limited data characterizing the epidemiology of C. trachomatis in sub-Saharan Africa, we sought to determine the incidence and correlates of C. trachomatis infection among HIV-1–seropositive and HIV-1–seronegative women enrolled in a prospective cohort study of women at high risk for sexually transmitted infections (STIs).
MATERIALS AND METHODS
We conducted a longitudinal follow-up in an open cohort of female sex workers in Mombasa, Kenya. The eligibility criteria to join the cohort are as follows: age 18 to 50 years, residing in the Mombasa area, self-identifying as exchanging sex for payment in cash or in kind, and able to provide informed consent. The present analysis used the data collected between August 2006 and December 2010. This study was approved by the ethical review committees at Kenyatta National Hospital and the University of Washington. All participants provided written informed consent.
At enrollment and monthly follow-up visits, a study nurse conducted a standardized interview covering demographic data, medical, gynecologic, and sexual history. A study physician performed a physical examination including a pelvic speculum examination. Swabs of cervical and vaginal secretions were collected for laboratory diagnosis of STIs. After April 2008, the visit schedule for HIV-1–seropositive women who were not on antiretroviral therapy changed from monthly to every 3 months, consistent with local clinical standards for this group.
Between August 2006 and April 2008, C. trachomatis testing was performed monthly. After April 2008, testing was performed every 3 months. All participants received free outpatient medical services including treatment of STIs. Diagnosed STIs were treated according to World Health Organization13 and Kenyan national guidelines. Women received doxycycline 100 mg twice daily for 7 days if they were diagnosed as having C. trachomatis infection. Syndromic management was offered during examination visits if indicated. When participants returned to receive their tests results, additional treatment was provided if infections were diagnosed by laboratory testing that had not been treated syndromically at the prior visit.
Endocervical samples were tested for the presence of Neisseria gonorrhoeae and C. trachomatis by transcription-mediated amplification using the Gen-Probe Aptima GC/CT Detection System (Gen-Probe, San Diego, CA). Culture for N. gonorrhoeae was performed on modified Thayer-Martin media. Cervical Gram-stained slides were examined microscopically for gram-negative intracellular diplococci consistent with a diagnosis of N. gonorrhoeae infection. Vaginal Gram-stained slides were evaluated using Nugent’s14 criteria, with bacterial vaginosis (BV) being defined as a score of 7 to 10. Nugent scoring was performed by laboratory technicians with more than 10 years of experience with this technique. Internal quality assurance was performed weekly, and external quality assurance was performed semiannually. Saline and potassium hydroxide wet mounts were examined at ×40 power for the presence of motile trichomonads, clue cells, Lactobacillus morphotypes, and yeast. HIV-1 serostatus was determined by enzyme-linked immunosorbent assay (Detect HIV1/2 [BioChem Immunosystems, Montreal, Canada] or PT-HIV 1,2-96 [Pishtaz Teb Diagnostics, Tehran, Iran]). Positive test results were confirmed using a second enzyme-linked immunosorbent assay (Recombigen [Cambridge Biotech, Worcester, MA] or Vironostika HIV-1 Uniform II AG/AB [bioMerieux, Marcy l’Etoile, France]). For the confirmatory tests, the cutoff values used were as suggested by the manufacturers. In addition to the manufacturers’ recommendations, we took into consideration a gray zone. This gray zone range was determined by identifying 10% of readings above and 10% of readings below the cutoff. We performed repeat testing for any results that fell within this range.
All women who had more than 1 visit at which C. trachomatis testing was performed were included in the analyses. The outcome was time to C. trachomatis infection. The exposures of interest were known or suspected risk factors for C. trachomatis infection including age, hormonal contraceptive use (oral contraceptive pills [OCPs] or depot medroxyprogesterone acetate [DMPA] vs. no hormonal contraception), vaginal microbiota (intermediate vaginal microbiota or BV vs. normal vaginal microbiota), place of work (bar vs. nightclub or home based/other), educational level, marital status, sexual risk behavior in the past week (unprotected intercourse, number of sex partners), vaginal washing, presence of other genital tract infections (Trichomonas vaginalis, Candida albicans, N. gonorrhoeae), HIV-1 serostatus, and cervical ectopy. These were assessed as predictors of infection using Andersen-Gill proportional hazards models and the Efron method for ties. Participants were included in the analyses beginning in August 2006 (when Gen-Probe C. trachomatis screening was initiated) or from the date of enrollment for those who enrolled after August 2006. Data were censored at a participant’s last follow-up visit or at the end of the analysis period in December 2010. We first conducted univariate analyses to determine whether individual risk factors were associated with C. trachomatis infection. Variables that were associated with C. trachomatis (α = 0.10) in the univariate analyses were then included in the multivariate model.
As in previous analyses, we estimated that the effect of oral or injectable hormonal contraception would persist for 70 days after discontinuation of use.15 We assumed that C. trachomatis was acquired at the midpoint between the preinfection visit and the visit at which the infection was detected. Because visits were, on average, every 30 days, we used an exposure interval of 85 (70 + 15) days for women who changed their method of hormonal contraception. We used a 45-day exposure interval for other STIs and abnormal vaginal microbiota or BV (assuming approximately 30 days for a persistent effect and 15-day incubation period). The lag period included the current visit. Analyses were performed using PASW 18.0 (PASW Inc, Chicago, IL) and STATA 11 (StataCorp, College Station, TX).
Between August 2006 and December 2010, 865 women had more than 1 visit where C. trachomatis testing was performed. The baseline characteristics of these participants are presented in Table 1. Their median age was 35 years (interquartile range [IQR], 30–40). One hundred eighty-one women (20.9%) were using DMPA. At baseline, the prevalence of C. trachomatis was low (1.9%). With the exception of HIV-1 (n = 457; 52.8%), the prevalence of other STIs at baseline was also low.
Participants in this study contributed a total of 2011 person-years of follow-up. The median duration of follow-up was 3.8 years (IQR, 2.7–4.1). Sixty-four women experienced 101 episodes of C. trachomatis infection, resulting in an incidence of 5.0 per 100 person-years. Twenty women had more than 1 episode of C. trachomatis infection (range, 2–5 episodes). There was a large difference in incidence by age group. Women younger than 25 years had an incidence rate of 27.6 per 100 person-years (95% confidence interval [CI], 16.3–46.5), those 25 to 34 years old had an incidence rate of 8.4 per 100 person-years (95% CI, 6.4–11.0), and women 35 years and older had an incidence rate of 2.6 per 100 person-years (95% CI, 1.8–3.6). Although C. trachomatis infection was associated with a higher likelihood of reporting symptoms (lower abdominal pain and/or vaginal discharge) (odds ratio, 1.7; 95% CI, 1.0–3.0; P = 0.05), only a minority C. trachomatis episodes were symptomatic (n = 16, 15.8%). Of 101 episodes of C. trachomatis, 6 (5.9%) included coinfection with N. gonorrhoeae.
Several exposures including younger age, use of DMPA, more recent enrollment in the research cohort, having 1 or more sex partners in the last week, having 1 or more sexual encounters in the last week, being HIV-1 seropositive, and having recent or concurrent N. gonorrhoeae infection were associated with an increased likelihood of acquiring C. trachomatis infection, in univariate analyses (Table 2). In multivariate analyses, younger age (<25 and 25–34 years vs. ≥35 years; hazard ratio [HR], 8.5 [95% CI, 4.1–17.7] and 2.9 [95% CI, 1.7–5.0], respectively), DMPA use (HR, 1.8; 95% CI, 1.1–3.0), and recent or concurrent N. gonorrhoeae infection (HR, 3.3; 95% CI, 1.5–7.4) remained significantly associated with increased risk of acquiring C. trachomatis infection.
Although age was associated with the number of sexual partners and hormonal contraceptive use, there were no statistically significant interactions between age and either of these additional covariates. Condom use was not different among hormonal contraceptive users compared with women not using hormonal contraception, and the interactions between condom use and hormonal contraception were also not statistically significant (data not shown). Thus, only a nonstratified model is presented.
The overall incidence of C. trachomatis infection among female sex workers in Mombasa was 5.0/100 person-years, which is similar to incidence estimates from studies conducted among female sex workers in Nairobi between 1998 and 2002 and in Mombasa between 1993 and 2003.5,7 The incidence of C. trachomatis was markedly higher among younger women (18–25 years), suggesting the need for expansion of screening to address this problem among young at-risk women. Other factors associated with C. trachomatis infection were use of DMPA and recent or concurrent infection with N. gonorrhoeae.
Studies of risk factors for C. trachomatis have mostly been conducted in developed countries and have identified similar risk factors including younger age, higher number of sexual partners, and use of hormonal contraception.16–20 Recent prospective studies have also highlighted the potential importance of BV as a risk factor for infection with C. trachomatis.21,22 In contrast, we did not find an association between abnormal vaginal microbiota or BV and C. trachomatis infection. Further research is needed to explore the association between vaginal microbiota and incident STIs.
Susceptibility to C. trachomatis infection may be influenced by a number of biological factors. First, cervical ectopy occurs when the squamocolumnar junction lies outside the endocervix, resulting in exposed columnar cells. This anatomical characteristic has been associated with increased risk for numerous pathogens including C. trachomatis.23 Cervical ectopy tends to be greatest during adolescence and decreases with age.23 This age-dependent phenomenon may help to explain the higher incidence of C. trachomatis infection in younger women. A second important biological factor is exposure to DMPA, which induces a systemic hypoestrogenic state associated with decreased vaginal colonization with hydrogen peroxide–producing Lactobacillus species.24 This decrease in protective vaginal bacteria may, in turn, increase the risk of C. trachomatis infection. In our study, DMPA was associated with a nearly 2-fold increase in risk of C. trachomatis infection, adding to data suggesting a possible link between hormonal contraception and acquisition of STIs including HIV-1.25 We did not find an association between OCP use and C. trachomatis infection, possibly because of the relatively small number of women (n = 41; 4.7%) using OCP in this cohort. Condom use among women on hormonal contraception was similar to condom use among women not using any hormonal contraception. Moreover, we have previously noted that not every STI risk is increased in contraceptive users. A study conducted within this same cohort demonstrated that women using DMPA had a significantly decreased risk of BV (HR, 0.7; 95% CI, 0.5–0.8) and trichomoniasis (HR, 0.6; 95% CI, 0.4–1.0).15 These findings argue against condom use as the mediating factor for C. trachomatis infection among hormonal contraceptive users.
Women with a recent or concurrent N. gonorrhoeae infection were 3 times more likely to acquire C. trachomatis infection. Prior STI has previously been described as a risk factor for infection by other sexually transmitted pathogens.26 Although there may be biological interactions, it is likely that this effect is also mediated through exposure to higher-risk sexual networks, where a variety of STIs are circulating.
The strengths of our study include the large sample size and longitudinal follow-up that enabled us to assess the correlates of C. trachomatis infection. In addition, we used the Gen-Probe Aptima GC/CT Detection System, which has excellent sensitivity (94.2%) and specificity (97.6%) for detection of C. trachomatis on endocervical swabs.27 This study also had limitations. Sexual risk behavior was self-reported, making these data subject to recall and social desirability bias. The questions on sexual risk behavior were limited to the past 1 week to mitigate recall bias. In addition, we have recently demonstrated that within this cohort, self-reported behaviors are associated with biological outcomes including STIs and sperm in genital secretions.28 Nonetheless, some misreporting of sexual risk behaviors should be anticipated. Second, 20 women experienced more than 1 episode of C. trachomatis infection. We did not perform molecular testing to distinguish between treatment failure and reinfection. Future studies should consider molecular characterization to improve our understanding of C. trachomatis reinfection or persistence.
Findings from this study add to a sparse body of literature on the incidence and risk factors for C. trachomatis in Africa. Data from this study suggest that the risk of C. trachomatis among high-risk women younger than 25 years could be substantial. Studies on the incidence of C. trachomatis among young women in sub-Saharan Africa should be prioritized in view of potentially severe sequelae including pelvic inflammatory disease, tubal infertility, and increased HIV-1 susceptibility. Tubal infertility is especially of concern in Africa, where prevalences of infertility as high as 27% have been reported29 and motherhood may be closely associated with a woman’s status in the community.30 Studies from West Africa have shown that C. trachomatis antibodies were more likely to be detected among infertile women compared with fertile women.31,32 Development of inexpensive point-of-care tests that can be used in resource-limited settings would enhance the diagnosis and early management of this largely silent epidemic.
We found a high incidence of C. trachomatis infection among high-risk women younger than 25 years, suggesting the need for screening as an important public health intervention for younger high-risk women. In addition, data from general population women are urgently needed to gain a greater understanding of the extent to which the epidemic crosses over into the general population.
2. Orroth KK, Korenromp EL, White RG, et al.. Comparison of STD prevalences in the Mwanza, Rakai, and Masaka trial populations: The role of selection bias and diagnostic errors. Sex Transm Infect 2003; 79 (2): 98–105.
3. Pepin J, Deslandes S, Khonde N, et al.. Low prevalence of cervical infections in women with vaginal discharge in west Africa: Implications for syndromic management. Sex Transm Infect 2004; 80 (3): 230–235.
4. Rassjo EB, Kambugu F, Tumwesigye MN, et al.. Prevalence of sexually transmitted infections among adolescents in Kampala, Uganda, and theoretical models for improving syndromic management. J Adolesc Health 2006; 38 (3): 213–221.
5. Kaul R, Kimani J, Nagelkerke NJ, et al.. Monthly antibiotic chemoprophylaxis and incidence of sexually transmitted infections and HIV-1 infection in Kenyan sex workers: A randomized controlled trial. Jama 2004; 291 (21): 2555–2562.
6. Sturm-Ramirez K, Brumblay H, Diop K, et al.. Molecular epidemiology of genital Chlamydia trachomatis
infection in high-risk women in Senegal, West Africa. J Clin Microbiol 2000; 38 (1): 138–145.
7. McClelland RS, Lavreys L, Katingima C, et al.. Contribution of HIV-1 infection to acquisition of sexually transmitted disease: A 10-year prospective study. J Infect Dis 2005; 191 (3): 333–338.
8. van de Wijgert JH, Morrison CS, Brown J, et al.. Disentangling contributions of reproductive tract infections to HIV acquisition in African Women. Sex Transm Dis 2009; 36 (6): 357–364.
9. Korenromp EL, Sudaryo MK, de Vlas SJ, et al.. What proportion of episodes of Gonorrhoea
becomes symptomatic? Int J STD AIDS 2002; 13 (2): 91–101.
10. Batteiger BE, Xu F, Johnson RE, et al.. Protective immunity to Chlamydia trachomatis
genital infection: Evidence from human studies. J Infect Dis 2010; 201 (suppl 2): S178–S189.
11. Kamenga MC, De Cock KM, St Louis ME, et al.. The impact of human immunodeficiency virus infection on pelvic inflammatory disease: A case-control study in Abidjan, Ivory Coast. Am J Obstet Gynecol 1995; 172 (3): 919–925.
12. 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 (1): 95–102.
14. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation. J Clin Microbiol 1991; 29 (2): 297–301.
15. Baeten JM, Nyange PM, Richardson BA, et al.. Hormonal contraception and risk of sexually transmitted disease acquisition: Results from a prospective study. Am J Obstet Gynecol 2001; 185 (2): 380–385.
16. Datta SD, Sternberg M, Johnson RE, et al.. Gonorrhea
in the United States among persons 14 to 39 years of age, 1999 to 2002. Ann Intern Med 2007; 147 (2): 89–96.
17. Morrison CS, Bright P, Wong EL, et al.. Hormonal contraceptive use, cervical ectopy, and the acquisition of cervical infections. Sex Transm Dis 2004; 31 (9): 561–567.
18. Weinstock H, Berman S, Cates W Jr. Sexually transmitted diseases among American youth: Incidence and prevalence estimates, 2000. Perspect Sex Reprod Health 2004; 36 (1): 6–10.
19. Scott Lamontagne D, Baster K, Emmett L, et al.. Incidence and reinfection rates of genital chlamydial infection among women aged 16–24 years attending general practice, family planning and genitourinary medicine clinics in England: A prospective cohort study by the Chlamydia Recall Study Advisory Group. Sex Transm Infect 2007; 83 (4): 292–303.
20. Walker J, Tabrizi SN, Fairley CK, et al.. Chlamydia trachomatis
incidence and re-infection among young women—behavioural and microbiological characteristics. PLoS One 2012; 7 (5): e37778.
21. Brotman RM, Klebanoff MA, Nansel TR, et al.. Bacterial vaginosis assessed by Gram stain and diminished colonization resistance to incident gonococcal, chlamydial, and trichomonal genital infection. J Infect Dis 2010; 202 (12): 1907–1915.
22. Kaul R, Nagelkerke NJ, Kimani J, et al.. Prevalent herpes simplex virus type 2 infection is associated with altered vaginal flora and an increased susceptibility to multiple sexually transmitted infections. J Infect Dis 2007; 196 (11): 1692–1697.
23. Critchlow CW, Wolner-Hanssen P, Eschenbach DA, et al.. Determinants of cervical ectopia and of cervicitis: Age, oral contraception, specific cervical infection, smoking, and douching. Am J Obstet Gynecol 1995; 173 (2): 534–543.
24. Miller L, Patton DL, Meier A, et al.. Depomedroxyprogesterone-induced hypoestrogenism and changes in vaginal flora and epithelium. Obstet Gynecol 2000; 96 (3): 431–439.
25. Heffron R, Donnell D, Rees H, et al.. Use of hormonal contraceptives and risk of HIV-1 transmission: A prospective cohort study. Lancet Infect Dis 2012; 12 (1): 19–26.
26. Peterman TA, Tian LH, Metcalf CA, et al.. High incidence of new sexually transmitted infections in the year following a sexually transmitted infection: A case for rescreening. Ann Intern Med 2006; 145 (8): 564–572.
27. Gaydos CA, Quinn TC, Willis D, et al.. Performance of the APTIMA Combo 2 assay for detection of Chlamydia trachomatis
and Neisseria gonorrhoeae
in female urine and endocervical swab specimens. J Clin Microbiol 2003; 41 (1): 304–309.
28. McClelland RS, Richardson BA, Wanje GH, et al.. Association between participant self-report and biological outcomes used to measure sexual risk behavior in human immunodeficiency virus-1–seropositive female sex workers in Mombasa, Kenya. Sex Transm Dis 2011; 38 (5): 429–433.
29. Larsen U. Primary and secondary infertility in sub-Saharan Africa. Int J Epidemiol 2000; 29 (2): 285–291.
30. Gerrits T. Social and cultural aspects of infertility in Mozambique. Patient Educ Couns 1997; 31 (1): 39–48.
31. Omo-Aghoja LO, Okonofua FE, Onemu SO, et al.. Association of Chlamydia trachomatis
serology with tubal infertility in Nigerian women. J Obstet Gynaecol Res 2007; 33 (5): 688–695.
32. Siemer J, Theile O, Larbi Y, et al.. Chlamydia trachomatis
infection as a risk factor for infertility among women in Ghana, West Africa. Am J Trop Med Hyg 2008; 78 (2): 323–327.
© Copyright 2013 American Sexually Transmitted Diseases Association
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Data is temporarily unavailable. Please try again soon.