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Original Study

Comprehensive Assessment of Sociodemographic and Behavioral Risk Factors for Mycoplasma genitalium Infection in Women

Hancock, Emily B. MS*; Manhart, Lisa E. PhD*; Nelson, Sara J. MPH*; Kerani, Roxanne PhD*†; Wroblewski, Jennifer K. H. MPH; Totten, Patricia A. PhD

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doi: 10.1097/OLQ.0b013e3181e8087e
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Mycoplasma genitalium is an emerging sexually transmitted organism1,2 and, similar to Chlamydia trachomatis and Neisseria gonorrhoeae, has been associated with cervicitis,3–7 endometritis,8,9 pelvic inflammatory disease, 8,9 and tubal factor infertility.10,11 Given their common mode of transmission, bacterial sexually transmitted infections (STI) share many common risk factors, including young age, female gender, black race, urban residence, childhood sexual abuse, multiple or concurrent sexual relationships, and young age at sexual debut.12–14 Partnership discordance by ethnicity, level of commitment, and number of lifetime partners, as well as poor knowledge of partner behavior have also been associated with bacterial STI.15–18

In addition to shared risk factors, gonococcal and chlamydial infections are each characterized by distinct risk factors, and these characteristics have guided the approach to targeting control strategies. N. gonorrhoeae circulates in networks of more marginalized individuals19 and is more geographically concentrated than C. trachomatis,20,21 whereas the strongest risk factors for chlamydial infection include female gender and young age.22 As a result, chlamydial control strategies are dominated by screening programs targeting young women, whereas gonorrhea control strategies are driven by partner notification efforts to identify and treat infected partners.

As evidence continues to emerge that M. genitalium is associated with reproductive tract disease in women, targeted control strategies will need to be developed. However, unlike other bacterial STI, the risk factors for infection with M. genitalium that would guide such control strategies are not clearly established. A relatively small number of studies to identify risk factors in women have been conducted.1,3,23–25 Therefore, we sought to identify detailed sociodemographic, sexual behavior, and partnership characteristics associated with M. genitalium infection in women and determine if risk factors for M. genitalium differ from those for C. trachomatis and N. gonorrhoeae.

MATERIALS AND METHODS

Study Setting and Subjects

Women attending the Public Health-Seattle and King County STD (sexually transmitted disease) clinic at Harborview Medical Center in Seattle, WA, were enrolled in a cross-sectional study of behavioral risk for STI between 2000 and 2006. Potential participants were approached by a study interviewer in clinic waiting rooms. Women aged 14 to 45 were eligible to participate if they had STI symptoms, wished to have an STI test, or were contacts to STI, whereas non-English speakers and women <14 or >45 were ineligible.

After providing informed consent, participants completed an hour-long computer-assisted survey interview consisting of questions based on the Wave III questionnaire of the National Longitudinal Study of Adolescent Health,26 along with additional questions on sexual behavior. An interviewer collected data on demographics and health characteristics, whereas a self-administered portion asked sensitive questions related to sexual experiences, history of STI, delinquency, substance abuse, and characteristics of the individuals' 3 most recent sexual partnerships. After the interview, a clinician performed a routine clinical examination, unless patient flow patterns required that an examination occur before the interview.

During the clinical examination, after obtaining sexual history and symptom information, the clinician inspected the external genitalia and performed a speculum examination. Self-obtained vaginal specimens were tested for M. genitalium using a research-use only transcription mediated amplification assay (Gen-Probe, Incorporated, San Diego, CA).27 Cervical swab specimens were assessed for C. trachomatis by culture and N. gonorrhoeae by Gram staining and/or culture. Of the 1113 women who completed the study, 23 had examination data only and were excluded, resulting in a total sample size of 1090 women. The Institutional Review Board at the University of Washington approved all study procedures.

Statistical Analyses

We used Pearson's χ2 and Fisher's exact tests (when expected cell values were ≤5) to compare categorical sociodemographic and sexual behavior characteristics, as well as those of the most recent sexual partnership for women with and without each pathogen and the Wilcoxon rank sum test to compare continuous measures. Any factor associated with a given organism at P < 0.10 was further evaluated in multivariate models.

We used multivariate logistic regression to identify characteristics independently associated with each organism, developing a separate model for each pathogen and seeking the most parsimonious model. Characteristics that remained significantly associated with each pathogen at P < 0.05 were retained in the final model. All analyses were performed using Intercooled Stata version 9.2 (Stata Corp, College Station, TX).

RESULTS

Study Population

The median age of women enrolled was 24 (range: 16–45) and less than half were white (44.7%), with 34.9% black. The majority of women had never been married (79.3%) and 46.6% had only a high school education or less. Approximately half of the women had an income of less than $10,000 per year (54.8%). Most women (52.4%) attended for symptoms; 41.9% attended for screening, and only 4.6% were contacts to STI.

Prevalence

M. genitalium infection was detected in 84 women (7.7%). Sixty-three women (5.8%) had C. trachomatis and 26 (2.4%) had N. gonorrhoeae. Coinfection with M. genitalium and C. trachomatis occurred in 7 women, with M. genitalium and N. gonorrhoeae in 4 women, and with C. trachomatis and N. gonorrhoeae in 11 women. One woman was coinfected with all 3 organisms. Women with M. genitalium were somewhat less likely to report symptoms as their reason for visit (39.4% vs. 53.6%, P = 0.09) than women without M. genitalium.

Univariate Analyses

Prevalent M. genitalium infection was significantly associated with several individual sociodemographic factors (Table 1). Women infected with M. genitalium were more likely to be younger, of black race, never married, and report less than a high school education. They were more likely to report an annual income <$10,000, and smoking compared to noninfected women, but less likely to have ever been diagnosed with depression, or live alone. Few differences in sexual behavior characteristics were observed between women with and without M. genitalium. Only younger age at sexual debut, use of Depo-Provera, and ever receiving a previous diagnosis of STI were associated with M. genitalium infection; whereas ever having had a miscarriage, condom use, engaging in anal sex, douching, or the number of sex partners in the past year was not associated with M. genitalium infection.

T1-9
TABLE 1:
Demographic and Sexual Behavior Characteristics in Women With and Without M. genitalium Infection Attending the PHSKC STD Clinic From 2000 to 2006 (N = 1090)

A small number of the characteristics of the most recent partnership reported by each participant were associated with M. genitalium infection (Table 2). Women with M. genitalium infection were more likely to report having a nonwhite partner, a partner with less than a high school education, a low income partner (less than $10,000 annually), or a partner who had spent a night in jail. They were less likely to report having a partner who used intravenous drugs, and somewhat less likely to report having performed oral sex. Although age difference, income discordance, and having concurrent sex partners in the most recent partnership were marginally associated with M. genitalium, other partnership characteristics and specific sexual behaviors were not.

T2-9
TABLE 2:
Characteristics of the Most Recent Sexual Partnership in Women With and Without M. genitalium Infection Attending the PHSKC STD Clinic From 2000 to 2006

Multivariate Analyses

Independent Risk Factors for Prevalent M. genitalium Infection.

In multivariate analyses (Table 3), women under the age of 20 were nearly twice as likely to have M. genitalium infection (adjusted odds ratio [AOR]: 1.8; 95% confidence interval: 1.01–3.33) compared to older women. Risk for M. genitalium was nearly 3-fold higher (AOR: 2.8; 1.40–5.72) for nonwhite than white women. Smokers were also 70% more likely to have M. genitalium than nonsmokers (AOR: 1.7; 1.03–2.83) and never-married women were 2.6 times more likely to be infected with M. genitalium than currently married or previously married women (AOR: 2.6; 1.08–6.25). Finally, women who used Depo-Provera were twice as likely to have M. genitalium as women who did not use Depo-Provera (AOR: 2.3; 1.19–4.46). However, when any hormonal contraceptive use was assessed in place of Depo-Provera, there was no significant relationship with M. genitalium infection, suggesting the effect is related to the pharmacological formulation of Depo-Provera, rather than to contraceptive use in general. Having a nonwhite partner was the sole partnership characteristic associated with M. genitalium, with infection 3.4 times more likely among women whose most recent partner was nonwhite (AOR: 3.4; 1.83–6.29) than among women with a white partner, even after adjusting for the woman's own race. In contrast, there was no association with number of partners, STI history, income, education, condom use, or other sexual behaviors in the multivariate model.

T3-9
TABLE 3:
Characteristics Independently Associated With M. genitalium, C. trachomatis, and N. gonorrhoeae Infection

Risk Factors for M. genitalium Compared With Those for C. trachomatis and N. gonorrhoeae.

Very few risk factors were common in women with M. genitalium, C. trachomatis, and N. gonorrhoeae. Only age <20 and nonwhite race were associated with increased risk for all 3 bacterial STI (Table 3). Drug use, most strongly associated with N. gonorrhoeae (AOR: 6.2; 1.40–27.81) and slightly less so with C. trachomatis (AOR: 2.4; 1.20–4.66), was not associated with M. genitalium infection, nor was fewer years of education, which was only associated with N. gonorrhoeae. Despite the fact that douching and hormonal contraceptive use were not associated with either M. genitalium or C. trachomatis, risk for N. gonorrhoeae was elevated among women who reported douching, but lower for women using hormonal contraceptives in the past year. STI diagnosis in the past year, typically associated with most STI, was only associated with increased risk for C. trachomatis, and number of partners was not associated with any of the 3 bacterial infections.

No partnership characteristics were commonly associated with all 3 pathogens. Similarly, none of the specific sexual behaviors examined were independently associated with either M. genitalium or C. trachomatis infection, but meeting and having sexual intercourse with a new partner on the same day, and engaging in anal sex with the most recent partner were strongly associated with increased risk for N. gonorrhoeae.

DISCUSSION

M. genitalium infection was detected in 7.7% of women attending an urban STD clinic, and was more common than either C. trachomatis (5.8%) or N. gonorrhoeae (2.4%). Nevertheless, these prevalences are relatively low for a group of women seeking care or testing for STI and reflect the generally low STI prevalences in the Pacific Northwest Region. Risk factors for prevalent M. genitalium infection were primarily comprised of general sociodemographic characteristics and partner race rather than risky sexual behaviors. Our direct comparison of risk factors for M. genitalium infection to C. trachomatis and N. gonorrhoeae revealed that only young age and nonwhite race were common to all 3 bacterial STI and nonwhite race, both of the woman and of her partner, was the strongest risk factor for M. genitalium. The highest risk behaviors (drug use, having sex on the same day as meeting a partner, and anal sex) were only associated with gonococcal infection and not M. genitalium.

Women with M. genitalium in this study had a notable absence of many previously identified risk factors. Other studies have consistently reported an increased risk for M. genitalium infection with higher numbers of recent sexual partners1,3,23,24 so the absence of a significant relationship among these women was unexpected. However, the number of partners was also not associated with either gonococcal or chlamydial infection in multivariate models, and the higher risk nature of women attending STD clinics, in general,28 may partially explain this lack of association. Having a partner with symptoms and shorter duration of a steady relationship were risk factors for M. genitalium infection in Danish women,24 neither of which was associated with M. genitalium here. Among women of a similar age range attending this same STD clinic in the 1980s, younger age and smoking were similarly associated with M. genitalium infection, but frequent douching, proliferative phase of the menstrual cycle, and history of spontaneous abortion were also identified as risk factors,3 which was not the case here. Finally, in a general population sample of young US adults, having ever lived with a sex partner and having used a condom at last vaginal intercourse were identified as risk factors for M. genitalium, unlike these results.1 Differences in study populations likely account for many of these differences.

Young age, nonwhite race, and drug use have consistently been identified as risk factors for a broad spectrum of STI.12,29,30 Less consistent condom use in younger women, and/or higher prevalence of STI in adolescent males may drive the association between young age and STI.31 Biologic mechanisms in younger women such as greater cervical ectopy32 may also explain their increased risk for STI. Drug use likely heightens risk for STI acquisition by decreasing inhibition and therefore increasing high-risk sexual behavior. This hypothesis is supported by Ross and Radcliffe, who noted that the association between illicit drug use and acquiring N. gonorrhoeae was no longer statistically significant after adjustment for multiple new partners, suggesting that the relationship was mediated by increased risk behavior.33 Given the absence of an association between M. genitalium and high-risk sexual behavior, it is not surprising that drug use was also not associated with M. genitalium. The association with never having been married may be related to the young age of women with M. genitalium. Depo-Provera use alone was associated with an increased risk for M. genitalium, but other hormonal contraceptive use was not, which is inconsistent with data from Kenyan sex workers.34 In that study, hormonal contraception was more strongly associated with M. genitalium than Depo-Provera use (although both were related); thus the relationship between M. genitalium and contraceptive use merits further exploration. We did not observe a significant association in multivariate analyses between any of the 3 bacteria and having concurrent sex partners, which was expected since having concurrent partners does not necessarily put an individual at higher risk for STI beyond the risk associated with her number of partners.35 However, we also found no association between any STI and having a partner with concurrent partners, which is often a risk factor for STI. Other studies, however, have noted the difficulty in measuring partner's concurrency,17,36 and the lack of association we observed here may be due to inadequate knowledge of partner behavior among the women enrolled.

The importance of identifying risk factors for infection with M. genitalium and developing a control strategy assumes that infection with this organism results in adverse sequelae. Although previous studies have established a strong association between M. genitalium infection and urethritis in men,7,37,38 the evidence for an association between M. genitalium and cervicitis in women is less consistent. Some studies report a strong relationship with cervicitis3,7,25 as well as with acute endometritis,8 pelvic inflammatory disease,9 and infertility,10 whereas others report no association.23,39,40 Further research is needed to definitively determine the role of M. genitalium infection in female reproductive tract disease before control strategies are adopted; risk factors identified here and from other studies may help target populations for such future studies.

This comparison of risk factors for prevalent M. genitalium infection to those for N. gonorrhoeae and C. trachomatis is characterized by several strengths and limitations. The relatively higher prevalence of M. genitalium (7.7%) provided sufficient power to identify risk factors associated with infection with this emerging pathogen. The transcription mediated amplification assay used to detect M. genitalium provided high sensitivity relative to the culture methods used for C. trachomatis and N. gonorrhoeae, and this may explain some of the disparity in the prevalences of the 3 bacteria, although not entirely. Although the cross-sectional nature of this study limits conclusions about cause-and-effect relationships, our results suggest that some risk factors for infection with M. genitalium are clearly different from other bacterial pathogens. Nevertheless, we examined a large number of potential risk factors, and some of our findings may be due to chance or influenced by uncontrolled confounding. Since we did not have a single characteristic of interest that we were testing, but rather sought to identify multiple characteristics independently associated with M. genitalium, a slightly different modeling strategy may have resulted in variations on the characteristics we identified here. For example, in some cases we chose 1 of 2 or more closely related variables for inclusion in final multivariate models. However, in all of these cases, the choices were between variables measuring similar constructs (e.g., general sociodemographic vs. high risk sexual behavior characteristics), thus the general conclusions are robust. Although we had adequate power to assess characteristics associated with M. genitalium, the prevalence of N. gonorrhoeae was relatively low (2.4%), reducing power for those analyses. Generalizability of these results may be limited to other urban STD clinic settings, but the use of a computer-assisted survey interview questionnaire likely reduced social desirability bias, as it has in other settings.41

Risk factors for prevalent infection with M. genitalium, C. trachomatis, and N. gonorrhoeae, differed by sociodemographic, sexual behavior, and partnership characteristics, consistent with the circulation of these STI in different sexual networks. These results confirm previous reports of this phenomenon for C. trachomatis and N. gonorrhoeae,19 and suggest the same is true for M. genitalium. In contrast to N. gonorrhoeae, M. genitalium infection was characterized by general sociodemographic and partnership attributes rather than by high-risk behavior, similar to the pattern observed with C. trachomatis infections. Notably these characteristics represent risk factors for prevalent infection and are likely to differ from those for incident infection.

The relatively high prevalence of M. genitalium suggests that control programs may become necessary as data on disease associations in women continue to accumulate. The development of such programs is often guided by the reproductive number (R0), a measure of the sustainability of an infection in a population. R0 equals βcD, where β represents the transmission probability, c the contact rate, and D the duration of infection.42 Reducing one or more of these components so that R0 <1 makes endemic infection unsustainable. Although our cross-sectional data limit our ability to accurately estimate either β or c or D, our observed lack of association with numbers of partners (a proxy for contact rate), along with data indicating that M. genitalium infection may have a long duration of infection40 suggests that it may not require high rates of partner change to sustain transmission. Therefore, as we begin to develop control strategies for this emerging sexually transmitted pathogen, broad-based testing for and treatment of M. genitalium, similar to chlamydial control strategies, may be more effective than strategies designed to identify hard to reach high-risk populations such as those employed in the control of gonorrhea. Further longitudinal studies explicitly designed to identify characteristics and sexual network patterns related to incident M. genitalium infection will be essential to determine if risk factors for incident infection are similar to those for prevalent infection, and further inform the development of control strategies.

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