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Determinants of Persistent and Recurrent Chlamydia trachomatis Infection in Young Women: Results of a Multicenter Cohort Study

WHITTINGTON, WILLIAM L. H. PhD(C)*†; KENT, CHARLOTTE MPH‡; KISSINGER, PATRICIA PhD§; OH, M. KIM MD⌆; FORTENBERRY, J. DENNIS MD, MS¶; HILLIS, SUSAN E. PhD#; LITCHFIELD, BILLY MPA#; BOLAN, GAIL A. MD, MPH‡; ST. LOUIS, MICHAEL E. MD#; FARLEY, THOMAS A. MD, MPH** AND; HANDSFIELD, H. HUNTER MD*†

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Author Information

From the Department of *Medicine, University of Washington, and †Public Health—Seattle & King County, Seattle, Washington; the ‡Department of Public Health, San Francisco, California; §Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana; ⌆University of Alabama at Birmingham, Birmingham, Alabama; ¶Indiana University, Indianapolis, Indiana; #Centers for Disease Control and Prevention, Atlanta, Georgia; and **Louisiana Office of Public Health, New Orleans, Louisiana

The authors gratefully acknowledge the contributions of numerous other investigators, clinicians, study coordinators, and data managers at the study sites and the referral clinics in all five cities. Supported by cooperative agreements between each of the study centers and the Centers for Disease Control and Prevention (Atlanta, GA).

Correspondence: H. Hunter Handsfield, MD, Harborview Medical Center Box 359777, 325 Ninth Avenue, Seattle, WA 98104-2499. E-mail: hhh@u.washington.edu. Reprints are not available.

Received for publication March 9, 2000,

revised June 7, 2000, and accepted June 12, 2000.

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Abstract

Background: Sequelae of genital Chlamydia trachomatis infection in women are more strongly linked to repeat infections than to initial ones, and persistent or subsequent infections foster continued transmission.

Objective: To identify factors associated with persistent and recurrent chlamydial infection in young women that might influence prevention strategies.

Methods: Teenage and young adult women with uncomplicated C trachomatis infection attending reproductive health, sexually transmitted disease, and adolescent medicine clinics in five US cities were recruited to a cohort study. Persistent or recurrent chlamydial infection was detected by ligase chain reaction (LCR) testing of urine 1 month and 4 months after treatment.

Results: Among 1,194 women treated for chlamydial infection, 792 (66.4%) returned for the first follow-up visit , 50 (6.3%) of whom had positive LCR results. At that visit, women who resumed sex since treatment were more likely to have chlamydial infection (relative risk [RR], 2.0; 95% CI, 1.03–3.9), as were those who did not complete treatment (RR, 3.4; 95% CI, 1.6–7.3). Among women who tested negative for C trachomatis at the first follow-up visit, 36 (7.1%) of 505 had positive results by LCR at the second follow-up visit. Reinfection at this visit was not clearly associated with having a new sex partner or other sexual behavior risks; new infection was likely due to resumption of sex with untreated partners. Overall, 13.4% of women had persistent infection or became reinfected after a median of 4.3 months, a rate of 33 infections per 1,000 person months.

Conclusions: Persistent or recurrent infection is very common in young women with chlamydial infection. Improved strategies are needed to assure treatment of women’s male sex partners. Rescreening, or retesting of women for chlamydial infection a few months after treatment, also is recommended as a routine chlamydia prevention strategy.

IN THE UNITED STATES, an estimated three million persons acquire genital Chlamydia trachomatis infection annually. 1 In women, lower genital tract infection with C trachomatis frequently ascends to cause pelvic inflammatory disease and is a precursor to tubal infertility, ectopic pregnancy, and chronic pelvic pain. 2–4 Animal models and epidemiologic studies suggest that sequelae of genital chlamydial infection are more closely linked to second or subsequent infections than to initial infection. 5–7 Studies have described rates of persistent or recurrent infection of 5% to 38% in adolescents and young women treated for chlamydial infection. 8–13 However, data for these studies often were gathered retrospectively, follow-up periods were variable, incomplete behavioral data were available, and persistent infection due to therapeutic failure usually could not be distinguished from reinfection. The current study was designed to prospectively determine the frequency of persistence and reinfection with C trachomatis to identify preventable risk factors that might aid in the design of public health prevention strategies.

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Methods

Patients

The study was undertaken at reproductive health, sexually transmitted disease (STD), and adolescent medicine clinics in Birmingham, Alabama; Indianapolis, Indiana; New Orleans, Louisiana; San Francisco, California; and Seattle, Washington. At each site, females 14 to 34 years were invited to participate if they had uncomplicated, laboratory-documented infection with C trachomatis. The method used to diagnose the initial chlamydial infection varied among cities and clinics; in most cases, infection was documented by culture, nucleic acid probe test (Pace II, GenProbe Corp., San Diego, CA), ligase chain reaction (LCR) (LCx, Abbott Laboratories, Chicago, IL) or polymerase chain reaction (Amplicor, Roche Laboratories, Nutley, NJ). Each subject provided informed consent, and the study was approved by the institutional review boards for human subjects research of each research center and that of the Centers for Disease Control and Prevention.

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Study Design

A prospectively recruited cohort design was used. Limited demographic, clinical, and behavioral data were collected from clinical and laboratory forms completed when the initial diagnosis of chlamydial infection was made, before patients were enrolled in the study. The study was introduced and patients enrolled when they were informed of their test results, usually 5 to 10 days after the screening visit, at which time treatment was given if presumptive treatment had not been administered at the screening visit. Patients were treated with standard regimens (usually, doxycycline 100 mg twice daily by mouth for 7 days or single-dose azithromycin 1.0 g orally) and were asked to return for the first study visit at 1 month after treatment and for a second study visit 4 months after the completion of treatment. Scheduled intervals for the two follow-up visits were 21 to 42 days and 2.5 to 5.5 months, respectively. Standardized demographic, clinical, and behavioral data were collected by interview at each study visit, including history of compliance with treatment, vaginal intercourse since treatment or since the preceding visit, condom use, new and continuing sexual partnerships, selected partnership characteristics, and patients’ beliefs about whether their partners had been treated for chlamydial infection. All centers used the same data collection forms and the interviewers were trained in its use. At all centers except San Francisco, women who returned were financially compensated (USD $10.00–$20.00 per visit) for their time and inconvenience. Women who failed to return for follow-up visits were contacted by mail, telephone, or in person to reschedule return visits. At each return visit, the first 30 ml of voided urine was collected for a C trachomatis LCR test, which was performed according to the manufacturer’s instructions. 14,15 Women with positive LCR test results at the first follow-up visit were considered to have completed the study and were not followed up further.

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Data Management and Statistical Analysis

All data were entered into a single computer database (Epi Info version 6.04, Centers for Disease Control and Prevention and World Health Organization, Atlanta, GA). Dichotomous variables were compared by chi-square or Fisher’s exact test. Parametric or nonparametric tests were used as appropriate for the analysis of continuous variables. Multivariate techniques, including logistic regression, were used to investigate the relationship of factors while controlling for the effects of covariates. Mantel-Haenszel stratified techniques were used to estimate risk ratios and 95% CI. Attributable risk fractions were calculated using standard methods. 16

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Results

Study Population Characteristics

A total of 1,194 young women with documented C trachomatis infection agreed to participate in the study (Table 1). Recruitment by city ranged from 114 subjects in Indianapolis to 453 subjects in New Orleans. Those enrolled were most frequently seen at reproductive health clinics, most were black, and approximately half were age 19 years or younger.

Table 1
Table 1
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First Study Visit

Among the 1,194 women enrolled, 622 (52.1%) returned for the first follow-up visit as scheduled (21–42 days after treatment). An additional 170 women (14.2%) returned after 42 days. Thus, 792 women (66.3%) completed the first return visit (mean follow-up interval, 38 days; range, 21–210 days). The first-visit return rates at the five study centers ranged from 40% (Birmingham) to 78% (New Orleans) (P < 0.001). Follow-up rates were lower for women initially seen at STD clinics (189 of 366 patients [51.6%]) than those seen at other facilities (610 of 828 patients [73.7%], P < 0.001). Additionally, women who acknowledged having two or more sex partners in the 60 days before enrollment were somewhat less likely to return (90 of 154 women [58.4%]) than those with one partner or no partner (696 of 1,027 women [67.8%], P = 0.03).

Chlamydial infection was documented by urine LCR in 50 of the 792 women (6.3%) who returned for the first follow-up visit. Table 2 shows the associations of selected demographic and behavioral variables with persistent or recurrent infection at that visit. Infection was identified in 7.8% of those who resumed sexual activity since the initial visit, compared with 3.7% of those who reported no sexual activity in the interim (unadjusted relative risk [RR], 2.1; 95% CI, 1.1–4.2). Infection at the first return visit also was significantly associated in univariate analysis with acknowledgment by the woman that she failed to complete therapy as instructed (RR, 3.2; 95% CI, 1.5–6.9), an association that remained after controlling for treatment regimen. Women age 19 years or younger were slightly more likely to be have a chlamydial infection than women 20 years or older (RR, 1.3; 95% CI, 0.8–2.3), as were women who returned after the intended appointment window (RR, 1.7; 95% CI, 0.9–3.0). A self-report of having talked to male sex partners about the partners’ need for treatment, being told by partners that they were treated, and condom use during the most recent vaginal intercourse were not significantly associated with infection, nor was the age differential between the women and their partners (Table 2).

Table 2
Table 2
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In multivariate analysis that included age, completion of treatment, resumption of sexual activity, and return outside the intended appointment window, independent predictors of chlamydial infection at the first return visit were failure to complete treatment (RR, 3.4; 95% CI, 1.6–7.3), resuming sexual activity since completing treatment (RR, 2.0; 95% CI, 1.03–4.4), and return beyond the intended appointment window (RR, 1.8; 95% CI, 1.01–3.2). Those 19 years and younger were at somewhat greater risk of infection (RR, 1.4; 95% CI, 0.8–2.4) than women 20 years and older. Other behavioral factors, the type of clinical facility where the diagnosis was made, and research center did not significantly affect estimates of risk. Among the women who resumed sexual activity, 7.8 per 100 women were infected, compared with 3.7 per 100 women who did not report that they resumed sexual activity. Thus, the risk difference was 4.1 (95% CI, 0.9–7.4) and the univariate population attributable fraction due to the resumption of sex was 42% (2.7 infections per 100 women). The remaining infections likely were due to treatment failure.

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Second Study Visit

Of 742 women with negative test results for chlamydial infection at the first return visit, 419 (56.5%) were seen again within the intended interval of 2.5 to 5.5 months after treatment. An additional 86 women were seen before or after the intended interval. Thus, 505 women (68.1%) had a second visit 4 weeks or longer after the first return visit (median follow-up interval, 130 days [4.3 months] after initial infection; range, 70–408 days). An additional 21 women who returned but gave histories of repeat treatment for chlamydial infection after the first return visit; all tested negative for chlamydial infection at the second return visit and were excluded from analysis. The proportion of patients who returned for the second follow-up visit ranged from 42.8% to 72.5% among the five research centers. The 505 evaluable women who returned for the second return visit did not differ significantly in any demographic or behavioral variables from all enrolled subjects (data not shown).

Chlamydial infection was diagnosed by urine LCR at the second visit in 36 (7.1%) of 505 women (Table 3). Mean follow-up intervals since the first return visit were 92 days and 94 days for women with and without infection, respectively. Risk factors for recurrent infection that approached statistical significance by univariate analysis were an age of 19 years or younger (RR, 1.7; 95% CI, 0.9–3.3) and a history of being sexually active with at least one partner between the two visits (RR, 2.2; 95% CI, 0.7–7.1). Younger women were slightly less likely to resume sexual activity; among 224 women 19 years and younger, 175 (78.1%) acknowledged having sex since the first follow-up visit, compared with 241 (87.3%) of 276 women 20 years or older (P < 0.01). Among women who were sexually active after the first return visit, 19 (10.9%) of 175 women 19 years or younger were reinfected, compared with 14 (5.8%) of 241 women 20 years and older (P = 0.07). Age of sex partners, number of episodes of vaginal intercourse reported, and frequency of condom use were similar between infected and uninfected women (data not shown).

Table 3
Table 3
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In multivariate analysis that included age, resumption of sexual activity, and sex with new partners, being 19 years or younger was modestly associated with infection (RR, 1.8; 95% CI, 0.97–3.5;P = 0.08). Resumption of sexual activity was not significantly associated with infection (RR, 2.4; 95% CI, 0.8–7.7;P > 0.1). Having a new sex partner since the first return visit was not significantly associated with infection at the second visit (RR, 1.3; 95% CI, 0.7–2.6), and the univariate population attributable fraction due to a new sex partner was only 5.5%, suggesting that few infections could be attributed to this risk variable. Further, infection was not independently associated with having sex with partners that the woman classified as casual (nonsteady) or the use of a condom during the most recent episode of intercourse. At the first return visit, 426 of 493 women (86.4%) reported talking to all of their sex partners about the partners’ need for treatment, and 322 women (65.3%) reported that one or more of their partners said they had been treated. Neither the patients’ first return-visit report that they spoke with their partners about the partners’ need for treatment nor the patients’ belief that their partners were treated was associated in multivariate analysis with protection against reinfection at the second return visit.

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Discussion

This study documents a high rate of persistent or recurrent infection with C trachomatis in a cohort of young women followed up prospectively in five geographically diverse areas of the United States. Overall, 13.4% of women had persistent infection or reinfection within a median of 4.3 months of treatment for uncomplicated chlamydial infection. At the first posttreatment evaluation, which occurred at a median of 38 days after treatment, 6.3% of evaluated women were infected, a rate similar to that observed in a recent randomized clinical trial that measured outcome 1 month after treatment. 13 Infection at that visit was independently associated with incomplete medication compliance and with resumption of sexual activity, usually in a continuing sexual partnership, and teens were at somewhat higher risk than older women. These findings suggest that infection in the first few weeks after treatment resulted from reinfection both from untreated sex partners and from treatment failure. The frequency of persistent or recurrent infection was similar in patients treated with azithromycin, doxycycline, or other regimens. Different frequencies of chlamydial infection in women who had or had not resumed sexual activity permitted estimation of the fraction of infections due to therapeutic failure. The estimate of 3.7% is consistent with observations from contemporary therapy trials. 17,18 Therefore, some persistent infections probably are caused by failure to eradicate C trachomatis, despite compliance with treatment.

We considered all positive LCR test results for C trachomatis infection at the second return visit (median, 4.3 months after treatment and 3.0 months after a documented negative test at the first return visit) to be the result of reinfection, rather than persistent infection. These infections were not significantly associated with any of several partnership-linked variables. However, the frequencies of certain risk factors were lower in our study than in some other recent reports. 19,20 For example, only 8.6% of participants in this study reported multiple sex partners, and only 28.2% reported intercourse with a new partner during the interval between a negative LCR test result and the second study visit. Therefore even after several months, most C trachomatis reinfections in women in this study were acquired from the same male sex partner(s) they had when their infection was first diagnosed, an observation reported by other investigators. 8,21 This study was not designed to determine whether the partners had persistent (untreated) infections or had acquired new infections from other partners.

These observations suggest that the women’s sexual behaviors were not the primary determinants of reinfection, which implies that their partners’ sexual or healthcare behaviors were the more important determinants. Eighty-six percent of women reported speaking to their male partners about his need for treatment, and 65% reported that their partners said that they had been treated. However, we did not contact the partners, and this study was not designed to measure the actual sexual or healthcare-seeking behaviors of their male partners.

The interactions of women and men concerning STD treatment are complex; for example, fear of violence or fear of loss of the support of a relationship can inhibit a woman’s willingness to be assertive in asking her partner to seek treatment. Men and women respond differently to the risk message implicit in an STD diagnosis. 22 The availability of STD-linked healthcare services for men is limited in many settings. For example, lengthy waits at public STD clinics can be disincentives to receiving necessary care, and men may feel unwelcome or otherwise uncomfortable seeking care from their partners’ reproductive health providers. Further, urethral chlamydial infection in men often is asymptomatic, and the absence of symptoms may be a further disincentive to seeking care. Thus, further understanding of the steps needed to reduce the risk of reinfection in women will need to address the behaviors of both women’s sex partners and the women themselves. In any case, our results highlight the importance of assuring treatment of women’s male sex partners. Retrospective studies suggest that providing infected women with antibiotics to deliver to their male partner can reduce rates of reinfection in women, 23,24 and a prospective multicenter randomized trial of this strategy is underway.

The results of this study confirm that persistent and recurrent infection with C trachomatis is common among women who are treated for uncomplicated chlamydial infection. Approximately one in seven women remained infected or became reinfected at a rate equivalent to 33 infections per 1,000 person months of observation. Despite major differences in study design, this rate approximates the incidence estimate of 28 new infections per 1,000 person months that was recently reported by Burstein et al 11 in a longitudinal study of inner-city adolescents. We recruited and prospectively followed a cohort of young women through two follow-up visits, whereas Burstein et al retested a convenience sample of patients when they returned for any healthcare visit at selected facilities, without active follow-up efforts.

This study has several limitations, and further studies will be needed to confirm and refine our results. The low frequency of certain risk behaviors may have contributed to insufficient power to detect some potentially important determinants of chlamydial persistence or reinfection. Second, although follow-up rates at both the first and second return visits were good in view of the characteristics of populations at risk for STD, only about two thirds of eligible women returned for each follow-up visit. However, women returning for the second follow-up visit did not differ from enrolled women in a number of demographic and behavioral characteristics. Third, the variability of the actual intervals at which patients returned for study visits created an analytic challenge, although controlling for return before or after the nominal intervals did not significantly affect the results. Fourth, several kinds of tests were used to detect the patients’ original chlamydial infections. Because the specificities of all these tests are high, almost all patients were infected. However, some of the tests used are insensitive, and some infections undoubtedly were missed. Therefore, the results of this study may not apply to all infected women, perhaps especially those with low concentrations of C trachomatis in cervical secretions, who may be more likely to have chronic or subclinical infections. Finally, at most study centers the participants received financial incentives, and all patients received services that may not be available to other women with chlamydial infection, including counseling that emphasized the importance of preventing future infections. These factors might have influenced risk-taking behaviors and reduced the reinfection rate below that experienced by other women. 25 Thus, in some settings the actual rates of persistent or recurrent chlamydial infection may be higher than we observed.

Rescreening, or routine retesting of women several weeks or months after treatment, may be an important strategy in the control of chlamydial infections and their complications. Rescreening is distinct from test-of-cure, wherein patients are tested after a short interval to detect treatment failure; except in pregnant women, test-of-cure is not recommended for chlamydial infection treated with standard regimens. 26 Rescreening of women has been recommended as a gonorrhea control strategy, but has rarely been implemented on a wide scale because of poor compliance by persons at risk, 27 which in turn may be due in part to the need for a clinic visit and a vaginal speculum examination. However, nucleic acid amplification tests for C trachomatis on urine or on self-collected vaginal swabs or tampons 28–30 permit testing without a speculum examination, and even without a clinic visit if specimen transport can be arranged. Rescreening necessitates only a modest increment in the total number of C trachomatis tests performed, equivalent to the prevalence in the population tested less the proportion of patients who do not comply with rescreening. The performance and cost effectiveness of rescreening need careful analysis, but this and most other reported studies 8–13 have documented rates of persistent or recurrent chlamydial infection well above the minimum prevalences that make primary screening programs cost effective. 31–33

Because we were unable to identify definitive determinants of recurrent infection, we recommend that rescreening be offered to all women treated for chlamydial infection, with emphasis on those who are likely to resume sexual activity after treatment. The best interval for a single rescreening test cannot be precisely defined by the available studies, but our results suggest that a test 2.5 to 5.5 months after treatment may be appropriate. Based partly on the results of this study, routine rescreening with urine or vaginal-swab LCR testing 3 to 4 months after treatment recently was implemented for all women with chlamydial infection at public health clinics in King County, Washington and San Francisco, California and is used at some of the current investigators’ own clinics. Although assuring compliance will be challenging and rescreening must not supplant continued primary screening of young women at risk, this approach should be adopted as a routine strategy for chlamydia prevention.

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Chorba, T; Scholes, D; BlueSpruce, J; Operskalski, BH; Irwin, K
American Journal of Medical Quality, 19(4): 145-156.

Microbiological Research
Chlamydia trachomatis persistence: An update
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Perspectives on Sexual and Reproductive Health
Integrating Chlamydia trachomatis control services for males in female reproductive health programs
McConnell, KJ; Packel, L; Biggs, MA; Chow, JM; Brindis, C
Perspectives on Sexual and Reproductive Health, 35(5): 226-228.

Clinical Infectious Diseases
Concurrent sexually transmitted infections (STIs) in sex partners of patients with selected STIs: Implications for patient-delivered partner therapy
Stekler, J; Bachmann, L; Brotman, RM; Erbelding, EJ; Lloyd, LV; Rietmeijer, CA; Handsfield, HH; Holmes, KK; Golden, MR
Clinical Infectious Diseases, 40(6): 787-793.

International Journal of Std & AIDS
Chlamydia trachomatis infection: the efficacy and safety of a fast-track referral and treatment system
Sethupathi, M; Blackwell, A
International Journal of Std & AIDS, 20(3): 184-187.
10.1258/ijsa.2008.008321
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Journal of Infectious Diseases
The unexpected impact of a Chlamydia trachomatis infection control program on susceptibility to reinfection
Brunham, RC; Pourbohloul, B; Mak, S; White, R; Rekart, ML
Journal of Infectious Diseases, 192(): 1836-1844.

Obstetrics and Gynecology Clinics of North America
Developments in the screening for Chlamydia trachomatis: a review
Kohl, KS; Markowitz, LE; Koumans, EH
Obstetrics and Gynecology Clinics of North America, 30(4): 637-+.
10.1016/S0889-8545(03)00076-7
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International Journal of Std & AIDS
A retrospective study of recurrent chlamydia infection in men and women: is there a role for targeted screening for those at risk?
Evans, C; Das, C; Kinghorn, G
International Journal of Std & AIDS, 20(3): 188-192.
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Journal of Adolescent Health
Expedited Partner Therapy for Adolescents Diagnosed with Chlamydia or Gonorrhea: A Position Paper of the Society for Adolescent Medicine
Burstein, GR; Eliscu, A; Ford, K; Hogben, M; Chaffee, T; Straub, D; Shafii, T; Huppert, J
Journal of Adolescent Health, 45(3): 303-309.
10.1016/j.jadohealth.2009.05.010
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Perspectives on Sexual and Reproductive Health
Infrequency of sexually transmitted disease screening among sexually experienced US female adolescents
Fiscus, LC; Ford, CA; Miller, WC
Perspectives on Sexual and Reproductive Health, 36(6): 233-238.

Journal of Infectious Diseases
Evaluation of antimicrobial resistance and treatment failures for Chlamydia trachomatis: A meeting report
Wang, SA; Papp, JR; Stamm, WE; Peeling, RW; Martin, DH; Holmes, KK
Journal of Infectious Diseases, 191(6): 917-923.

Clinical Infectious Diseases
Patient-delivered partner treatment for male urethritis: A randomized, controlled trial
Kissinger, P; Mohammed, H; Richardson-Alston, G; Leichliter, JS; Taylor, SN; Martin, DH; Farley, TA
Clinical Infectious Diseases, 41(5): 623-629.

Antimicrobial Agents and Chemotherapy
Rifalazil pretreatment of mammalian cell cultures prevents subsequent Chlamydia infection
Suchland, RJ; Brown, K; Rothstein, DM; Stamm, WE
Antimicrobial Agents and Chemotherapy, 50(2): 439-444.

Sexually Transmitted Infections
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
LaMontagne, DS; Baster, K; Emmett, L; Nichols, T; Randall, S; McLean, L; Meredith, P; Harindra, V; Tobin, JM; Underhill, GS; Hewitt, WG; Hopwood, J; Gleave, T; Ghosh, AK; Mallinson, H; Davies, AR; Hughes, G; Fenton, KA
Sexually Transmitted Infections, 83(4): -.
ARTN 292
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Bmc Public Health
Repeat infection with Chlamydia trachomatis: a prospective cohort study from an STI-clinic in Stockholm
Edgardh, K; Kuhlmann-Berenzon, S; Grunewald, M; Rotzen-Ostlund, M; Qvarnstrom, I; Everljung, J
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Best Practice & Research in Clinical Obstetrics & Gynaecology
The role of serology, antibiotic susceptibility testing and serovar determination in genital chlamydial infections
Persson, K
Best Practice & Research in Clinical Obstetrics & Gynaecology, 16(6): 801-814.
10.1053/beog.2002.0321
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Antimicrobial Agents and Chemotherapy
Frequency of spontaneous mutations that confer antibiotic resistance in Chlamydia spp
Binet, R; Maurelli, AT
Antimicrobial Agents and Chemotherapy, 49(7): 2865-2873.
10.1128/AAC.49.7.2865-2873.2005
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Best Practice & Research in Clinical Obstetrics & Gynaecology
How, and how efficiently, can we treat Chlamydia trachomatis infections in women?
Guaschino, S; Ricci, G
Best Practice & Research in Clinical Obstetrics & Gynaecology, 16(6): 875-888.
10.1053/beog.2002.0336
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Archives of Pediatrics & Adolescent Medicine
Examination of the treatment and follow-up care for adolescents who test positive for Chlamydia trachomatis infection
Hwang, LY; Tebb, KP; Shafer, MAB; Pantell, RH
Archives of Pediatrics & Adolescent Medicine, 159(): 1162-1166.

International Journal of Std & AIDS
Patient-delivered partner medication in the UK: an unlawful but popular choice
Coyne, KM; Cohen, CE; Smith, NA; Mandalia, S; Barton, S
International Journal of Std & AIDS, 18(): 829-831.

Human Reproduction
Chlamydia trachomatis in infertile women undergoing uterine instrumentation: Screen or treat
Ng, EHY; Ngai, CSW; Ho, PC
Human Reproduction, 17(8): 2215-2216.

Contraception
Failure of family-planning referral and high interest in advanced provision emergency contraception among women contacted for STD partner notification
Golden, MR; Whittington, WLH; Handsfield, HH; Clark, A; Malinski, C; Helmers, JR; Hogben, M; Holmes, KK
Contraception, 69(3): 241-246.
10.1016/j.contraception.2003.10.018
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Sexually Transmitted Infections
Repeat chlamydia screening by mail, San Francisco
Bloomfield, PJ; Steiner, KC; Kent, CK; Klausner, JD
Sexually Transmitted Infections, 79(1): 28-30.

Sexually Transmitted Infections
Knowledge of sex partner treatment for past bacterial STI and risk of current STI
Niccolai, LM; Ickovics, JR; Zeller, K; Kershaw, TS; Milan, S; Lewis, JB; Ethier, KA
Sexually Transmitted Infections, 81(3): 271-275.
10.1136/sti.2004.012872
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Journal of Adolescent Health
Partner age not associated with recurrent Chlamydia trachomatis infection, condom use, or partner treatment and referral among adolescent women
Magnus, M; Schillinger, JA; Fortenberry, JD; Berman, SM; Kissinger, P
Journal of Adolescent Health, 39(3): 396-403.
10.1016/j.jadohealth.2006.01.005
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Bjog-An International Journal of Obstetrics and Gynaecology
Universal prophylaxis compared with screen-and-treat for Chlamydia trachomatis prior to termination of pregnancy
Cameron, ST; Sutherland, S
Bjog-An International Journal of Obstetrics and Gynaecology, 109(6): 606-609.
PII S1470-0328(02)01709-3
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Journal of Adolescent Health
Gonorrhea and chlamydia screening among young women: Stage of change, decisional balance, and self-efficacy
Banikarim, C; Chacko, MR; Wiemann, CM; Smith, PB
Journal of Adolescent Health, 32(4): 288-295.
10.1016/S1054-139X(02)00706-1
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Annals of Internal Medicine
High incidence of new sexually transmitted infections in the year following a sexually transmitted infection: A case for rescreening
Peterman, TA; Tian, LH; Metcalf, CA; Satterwhite, CL; Malotte, CK; DeAugustine, N; Paul, SM; Cross, H; Rietmeijer, CA; Douglas, JM
Annals of Internal Medicine, 145(8): 564-572.

Clinical Infectious Diseases
Centers for disease control and prevention sexually transmitted diseases treatment guidelines - Introduction
Workowski, KA; Berman, SM
Clinical Infectious Diseases, 44(): S73-S76.
10.1086/511430
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Clinical Infectious Diseases
Management of women with cervicitis
Marrazzo, JM; Martin, DH
Clinical Infectious Diseases, 44(): S102-S110.
10.1086/511423
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Sexually Transmitted Infections
Chlamydial and gonococcal reinfection among men: a systematic review of data to evaluate the nee for retesting
Fung, M; Scott, KC; Kent, CK; Klausner, JD
Sexually Transmitted Infections, 83(4): -.
ARTN 304
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Public Health Nursing
Providers' Experiences with Young People's Cognitive Representations and Emotions Related to the Prevention and Treatment of Sexually Transmitted Infections
Royer, HR; Zahner, SJ
Public Health Nursing, 26(2): 161-172.
10.1111/j.1525-1446.2009.00767.x
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International Reviews of Immunology
Cellular immunity and Chlamydia genital infection: Induction, recruitment, and effector mechanisms
Kelly, KA
International Reviews of Immunology, 22(1): 3-41.
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Infectious Disease Clinics of North America
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Golden, MR; Manhart, LE
Infectious Disease Clinics of North America, 19(2): 513-+.
10.1016/j.idc.2005.03.004
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Australian & New Zealand Journal of Obstetrics & Gynaecology
The importance of chlamydial infections in obstetrics and gynaecology: An update
Currie, MJ; Bowden, FJ
Australian & New Zealand Journal of Obstetrics & Gynaecology, 47(1): 2-8.
10.1111/j.1479-828X.2006.00670.x
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Best Practice & Research in Clinical Obstetrics & Gynaecology
Epidemiology of female genital Chlamydia trachomatis infections
Norman, J
Best Practice & Research in Clinical Obstetrics & Gynaecology, 16(6): 775-787.
10.1053/beog.2002.0325
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Annals of Internal Medicine
Screening for Chlamydia trachomatis in women 15 to 29 years of age: A cost-effectiveness analysis
Hu, D; Hook, EW; Goldie, SJ
Annals of Internal Medicine, 141(7): 501-513.

Health Education Journal
Reasons given by high school students for refusing sexually transmitted disease screening
Sanders, LS; Nsuami, M; Cropley, LD; Taylor, SN
Health Education Journal, 66(1): 44-57.
10.1177/0017896907073784
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Clinical and Experimental Medicine
Serovar-specific immune responses to peptides of variable regions of Chlamydia trachomatis major outer membrane protein in serovar D-infected women
Srivastava, P; Gupta, R; Jha, HC; Jha, R; Bhengraj, AR; Salhan, S; Mittal, A
Clinical and Experimental Medicine, 8(4): 207-215.
10.1007/s10238-008-0004-2
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Sexually Transmitted Infections
Correlation between culture testing of swabs and ligase chain reaction of first void urine from patients recently treated for Chlamydia trachomatis
Jang, D; Sellors, J; Howard, M; Mahony, J; Frost, E; Patrick, D; Bouchard, C; Dubois, J; Scholar, L; Chernesky, M
Sexually Transmitted Infections, 79(3): 237-239.

Journal of Bacteriology
Lateral gene transfer in vitro in the intracellular pathogen Chlamydia trachomatis
DeMars, R; Weinfurter, J; Guex, E; Lin, J; Potucek, Y
Journal of Bacteriology, 189(3): 991-1003.
10.1128/JB.00845-06
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Journal of Infectious Diseases
Repeated Chlamydia trachomatis Genital Infections in Adolescent Women
Batteiger, BE; Tu, W; Ofner, S; Van Der Pol, B; Stothard, DR; Orr, DP; Katz, BP; Fortenberry, JD
Journal of Infectious Diseases, 201(1): 42-51.
10.1086/648734
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Sexually Transmitted Diseases
Chlamydia trachomatis - The persistent pathogen - Thomas Parran award lecture
Stamm, WE
Sexually Transmitted Diseases, 28(): 684-689.

International Journal of Antimicrobial Agents
Effects of sustained antibiotic bactericidal treatment on Chlamydia trachomatis-infected epithelial-like cells (HeLa) and monocyte-like cells (THP-1 and U-937)
Mpiga, P; Ravaoarinoro, M
International Journal of Antimicrobial Agents, 27(4): 316-324.
10.1016/j.ijantimicag.2005.11.010
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Canadian Medical Association Journal
Canadian guidelines on sexually transmitted infections, 2006
MacDonald, N; Wong, T
Canadian Medical Association Journal, 176(2): 175-176.
10.1503/cmaj.061616
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Sexually Transmitted Infections
Provider willingness to screen all sexually active adolescents for chlamydia
Boekeloo, BO; Snyder, MH; Bobbin, M; Burstein, GR; Conley, D; Quinn, TC; Zenilman, JM
Sexually Transmitted Infections, 78(5): 369-373.

American Journal of Preventive Medicine
American college of preventive medicine practice policy statement - Screening for Chlamydia trachomatis
Hollblad-Fadiman, K; Goldman, SM
American Journal of Preventive Medicine, 24(3): 287-292.
10.1016/S0749-3797(02)00636-0
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New England Journal of Medicine
Effect of expedited treatment of sex partners on recurrent or persistent gonorrhea or chlamydial infection
Golden, MR; Whittington, WLH; Handsfield, HH; Hughes, JP; Stamm, WE; Hogben, M; Clark, A; Malinski, C; Helmers, JRL; Thomas, KK; Holmes, KK
New England Journal of Medicine, 352(7): 676-685.

Academic Emergency Medicine
Evaluation of risk score algorithms for detection of chlamydial and gonococcal infections in an emergency department setting
Al-Tayyib, AA; Miller, WC; Rogers, SM; Leone, PA; Law, DCG; Ford, CA; Rothman, RE
Academic Emergency Medicine, 15(2): 126-135.
10.1111/j.1553-2712.2008.00027.x
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International Journal of Std & AIDS
The demographical and clinical features of patients reattending a genitourinary medicine clinic and the role of counselling on subsequent incidence of sexually transmitted infections
Manavi, K; Bolton, N
International Journal of Std & AIDS, 19(3): 168-171.
10.1258/ijsa.2007.007189
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International Journal of Std & AIDS
Is there a need for rescreening of patients treated for genital chlamydial infections?
Mardh, PA; Persson, K
International Journal of Std & AIDS, 13(6): 363-367.

Journal of Infectious Diseases
Human leukocyte antigen and cytokine gene variants as predictors of recurrent Chlamydia trachomatis infection in high-risk adolescents
Wang, CB; Tang, JM; Geisler, WM; Crowley-Nowick, PA; Wilson, CM; Kaslow, RA
Journal of Infectious Diseases, 191(7): 1084-1092.

Infectious Disease Clinics of North America
Mucopurulent cervicitis: No longer ignored, but still misunderstood
Marrazzo, JM
Infectious Disease Clinics of North America, 19(2): 333-+.
10.1016/j.idc.2005.03.009
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Sexually Transmitted Diseases
Reinfections, persistent infections, and new infections after general population screening for Chlamydia trachomatis infection in the Netherlands
Veldhuijzen, IK; Van Bergen, JEAM; Gotz, HM; Hoebe, CJPA; Morre, SA; Richardus, JH
Sexually Transmitted Diseases, 32(): 599-604.

Clinical Infectious Diseases
Suboptimal Adherence to Repeat Testing Recommendations for Men and Women With Positive Chlamydia Tests in the United States, 2008-2010
Hoover, KW; Tao, GY; Nye, MB; Body, BA
Clinical Infectious Diseases, 56(1): 51-57.
10.1093/cid/cis771
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Sexually Transmitted Infections
Increasing chlamydia test of re-infection rates using SMS reminders and incentives
Downing, SG; Cashman, C; McNamee, H; Penney, D; Russell, DB; Hellard, ME
Sexually Transmitted Infections, 89(1): 16-19.
10.1136/sextrans-2011-050454
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Sexually Transmitted Infections
Chlamydia trachomatis re-infections in a population-based cohort of women
Liu, B; Guy, R; Donovan, B; Kaldor, JM
Sexually Transmitted Infections, 89(1): 45-50.
10.1136/sextrans-2011-050252
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Journal of Adolescent Health
Intrauterine Devices and Pelvic Inflammatory Disease Among Adolescents
Carr, S; Espey, E
Journal of Adolescent Health, 52(4): S22-S28.
10.1016/j.jadohealth.2013.01.017
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Medicine & Science in Sports & Exercise
Sports Preparticipation Examination to Screen College Athletes for Chlamydia trachomatis
HENNRIKUS, E; OBERTO, D; LINDER, JM; REMPEL, JM; HENNRIKUS, N
Medicine & Science in Sports & Exercise, 42(4): 683-688.
10.1249/MSS.0b013e3181bf53c1
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Current Opinion in Infectious Diseases
Urine nucleic acid amplification tests for the diagnosis of sexually transmitted infections in clinical practice
Gaydos, CA; Quinn, TC
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Current Opinion in Pediatrics
Sexually transmitted diseases treatment guidelines
Burstein, GR; Workowski, KA
Current Opinion in Pediatrics, 15(4): 391-397.

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Sexually Transmitted Diseases
Patient-Delivered Partner Treatment With Azithromycin to Prevent Repeated Chlamydia trachomatis Infection Among Women: A Randomized, Controlled Trial
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Sexually Transmitted Diseases, 30(1): 49-56.

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Sexually Transmitted Diseases
Sex Partner Selection, Social Networks, and Repeat Sexually Transmitted Infections in Young Men: A Preliminary Report
Ellen, JM; Gaydos, C; Chung, S; Willard, N; Lloyd, LV; Rietmeijer, CA
Sexually Transmitted Diseases, 33(1): 18-21.

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Sexually Transmitted Diseases
Condom Use and Risk of Gonorrhea and Chlamydia: A Systematic Review of Design and Measurement Factors Assessed in Epidemiologic Studies
Warner, L; Stone, KM; Macaluso, M; Buehler, JW; Austin, HD
Sexually Transmitted Diseases, 33(1): 36-51.

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Determining Risk Markers for Gonorrhea and Chlamydial Infection and Reinfection Among Adolescents in Public High Schools
Anschuetz, GL; Beck, JN; Asbel, L; Goldberg, M; Salmon, ME; Spain, CV
Sexually Transmitted Diseases, 36(1): 4-8.
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Incidence and Repeat Infection Rates of Chlamydia trachomatis Among Male and Female Patients in an STD Clinic: Implications for Screening and Rescreening
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Sexually Transmitted Diseases, 29(2): 65-72.

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Rescreening for Gonorrhea and Chlamydial Infection Through the Mail: A Randomized Trial
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Sexually Transmitted Diseases
Chlamydial Infections Among Female Adolescents Screened in Juvenile Detention Centers in Washington State, 1998–2002
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Sexually Transmitted Diseases, 33(2): 63-67.
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Patient-Delivered Partner Treatment and Other Partner Management Strategies for Sexually Transmitted Diseases Used by New York City Healthcare Providers
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Sexually Transmitted Diseases, 34(2): 88-92.
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Older Partners Not Associated With Recurrence Among Female Teenagers Infected With Chlamydia trachomatis
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Acceptability of Urine-Based Screening for Chlamydia trachomatis to Asymptomatic Young Men and Their Providers
Marrazzo, JM; Ellen, JM; Kent, C; Gaydos, C; Chapin, J; Dunne, EF; Rietmeijer, CA
Sexually Transmitted Diseases, 34(3): 147-153.
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Chlamydia trachomatis Reinfection Rates Among Female Adolescents Seeking Rescreening in School-Based Health Centers
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Sexually Transmitted Diseases, 35(3): 233-237.
10.1097/OLQ.0b013e31815c11fe
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Acquisition of Chlamydia trachomatis by Young Women During Their First Year of Military Service
SHAFER, MB; BOYER, CB; POLLACK, LM; MONCADA, J; CHANG, YJ; SCHACHTER, J
Sexually Transmitted Diseases, 35(3): 255-259.
10.1097/OLQ.0b013e31815c1bd0
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Chlamydia in the United States Military: Can We Win This War?
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Sexually Transmitted Diseases, 35(3): 260-262.
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California Guidelines for Expedited Partner Therapy for Chlamydia trachomatis and Neisseria gonorrhoeae
Bauer, HM; Wohlfeiler, D; Klausner, JD; Guerry, S; Gunn, RA; Bolan, G; the California STD Controllers Association,
Sexually Transmitted Diseases, 35(3): 314-319.
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The Prevalence of Chlamydia, Gonorrhea, and Trichomonas in Sexual Partnerships: Implications for Partner Notification and Treatment
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Sexually Transmitted Diseases, 32(4): 260-264.

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Factors Associated With Recurrent Chlamydial Infection and Failure to Return for Retesting in Young Women Entering National Job Training Program, 1998–2005
Joesoef, MR; Weinstock, HS; Johnson, RE
Sexually Transmitted Diseases, 35(4): 368-371.
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Incidence and Risk Factors for Genital Chlamydia trachomatis Infection: A 4-Year Prospective Cohort Study
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Sexually Transmitted Diseases, 36(5): 273-279.
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The Elephant Never Forgets; Piloting a Chlamydia and Gonorrhea Retesting Reminder Postcard in an STD Clinic Setting
Paneth-Pollak, R; Klingler, E; Blank, S; Schillinger, J
Sexually Transmitted Diseases, 37(6): 365-368.
10.1097/OLQ.0b013e3181cab281
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The Impact of Natural History Parameters on the Cost-Effectiveness of Chlamydia trachomatis Screening Strategies
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Sexually Transmitted Diseases, 33(7): 428-436.
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Internet-Based Screening for Chlamydia trachomatis to Reach Nonclinic Populations With Mailed Self-Administered Vaginal Swabs
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Sexually Transmitted Diseases, 33(7): 451-457.
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Patient-Delivered Partner Therapy for Chlamydial Infections: Attitudes and Practices of California Physicians and Nurse Practitioners
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Sexually Transmitted Diseases, 33(7): 458-463.
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Repeat Infection With Chlamydia and Gonorrhea Among Females: A Systematic Review of the Literature
Hosenfeld, CB; Workowski, KA; Berman, S; Zaidi, A; Dyson, J; Mosure, D; Bolan, G; Bauer, HM
Sexually Transmitted Diseases, 36(8): 478-489.
10.1097/OLQ.0b013e3181a2a933
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Acceptability of Urine-Based Screening for Chlamydia trachomatis in Asymptomatic Young Men: A Systematic Review
Marrazzo, JM; Scholes, D
Sexually Transmitted Diseases, 35(11): S28-S33.
10.1097/OLQ.0b013e31816938ca
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Sexually Transmitted Diseases
Rate and Predictors of Repeat Chlamydia trachomatis Infection Among Men
Markowitz, LE; Lloyd, L; Thomas, S; Birkjukow, N; Chung, S; Klausner, J; Schillinger, JA; Dunne, EF; Chapin, JB; Rietmeijer, CA; Kent, CK; Ellen, JM; Gaydos, CA; Willard, NJ; Kohn, R
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