Sexually Transmitted Diseases:
Acceptability of Urine-Based Screening for Chlamydia trachomatis to Asymptomatic Young Men and Their Providers
Marrazzo, Jeanne M. MD, MPH*; Ellen, Jonathan M. MD†; Kent, Charlotte PhD‡; Gaydos, Charlotte PhD§; Chapin, Johanna MPH∥; Dunne, Eileen F. MD, MPH∥; Rietmeijer, Cornelis A. MD, PhD¶
From the *Department of Medicine, University of Washington, Seattle, Washington; the Departments of †Pediatrics and §Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland; the ‡San Francisco Department of Public Health, San Francisco, California; the ∥Centers for Disease Control and Prevention, Atlanta, Georgia; and ¶Denver Public Health, Denver, Colorado
The authors thank Julie Schillinger, Lauri Markowitz, Stuart Berman, Alisa Katai, Susan Whang, Jim Braxton, Laura Lloyd, Beth Weaver, Stewart Thomas, and the providers and subjects who participated in this study.
Correspondence: Jeanne M. Marrazzo, MD, MPH, Harborview Medical Center, Division of Infectious Diseases, 325 9th Avenue, Mailbox #359931, Seattle, WA 98104. E-mail: firstname.lastname@example.org
Received for publication January 7, 2006, and accepted May 18, 2006.
Objective: The objective of this study was to describe acceptability of urine chlamydia testing among asymptomatic men and providers’ attitudes toward testing.
Study Design: Asymptomatic men (no urethral discharge/dysuria) were offered free testing and characteristics of men who accepted were compared with those who declined. Acceptability logs tallied the proportion who accepted, and a standardized survey was administered to providers at study’s end.
Results: Median acceptance was 64% (range, 8–100%). Men accepting were younger and more likely to be in adolescent primary care or detention, to report higher numbers of recent partners, no prior sexually transmitted disease, time to last healthcare visit >1 year, and to have received an incentive. Provider-reported barriers to testing included difficulty in conveying importance of testing to asymptomatic men (65%) and time constraints (24%).
Conclusions: Asymptomatic men are likely to accept testing depending on venue and approach. However, barriers exist for men and providers, even when testing is free.
THE AVAILABILITY OF NUCLEIC ACID amplification testing (NAAT) of urine for Chlamydia trachomatis infection has dramatically increased the capability to screen asymptomatic men. At least 60%, and probably closer to 90%, of all men with genital chlamydial infection do not report urethral discharge or dysuria.1–9 However, a systematic approach to screening asymptomatic men has not been defined, and knowledge of whether such testing is acceptable to asymptomatic men is very limited. Similarly, no assessment of healthcare providers’ attitudes or practices about screening asymptomatic men has been reported.
Addressing acceptability of screening asymptomatic men for chlamydial infection is important for 3 reasons. First, selective screening for chlamydial infection in women has been associated with a reduction in symptomatic pelvic inflammatory disease (PID) and with marked declines in C. trachomatis prevalence.10,11 These declines have not been sustained, especially among adolescents, with prevalence at stable or increasing levels in some areas.12–14 Increasing use of NAAT, which is more sensitive than previously used tests, only partly explains these trends15; failure to detect and treat chlamydial infections in asymptomatic men may be a significant contributor that screening programs might address.16 Second, empiric treatment of male sex partners of women infected with C. trachomatis is recommended and, at a population level, likely to have a major favorable impact on the population prevalence of C. trachomatis.17 However, it is performed surprisingly infrequently, probably with significant consequence.18 For example, in one large study, 13.4% of women had persistent chlamydial infection or became reinfected within a median of 4.3 months after treatment.19 In most of these cases, reinfection occurred from exposure to men who were sex partners at the time of initial chlamydial infection, not from new partners acquired in the interim. This suggests high rates of reacquisition from untested, untreated, asymptomatic men. Because women who experience recurrent chlamydial infection are at increased risk of PID and ectopic pregnancy,20 this is concerning. Finally, understanding the acceptability of screening to asymptomatic men is necessary to fully inform our attempts to define the epidemiology of this infection in men and to develop comprehensive C. trachomatis control strategies that meaningfully involve men and their healthcare providers.
We performed a large, multicenter demonstration project to assess the feasibility of routine screening for C. trachomatis among asymptomatic men using urine-based NAAT outside of traditional sexually transmitted disease (STD) clinic settings. Across all 4 cities, over 23,000 asymptomatic men (median age, 21 years) were tested for C. trachomatis at over 50 different venues using several different approved NAAT assays.21 Approximately half of all testing occurred in adult detention and 19% in juvenile detention. School clinics accounted for 7% of testing, street outreach, 8%; adolescent and adult primary care, 8%; and all others, 7%. As part of this project, we also assessed the acceptability of urine-based testing to asymptomatic men and to the healthcare providers who participated, the characteristics of men who declined testing, and reasons that men declined testing.
Materials and Methods
To study the acceptability of urine-based testing for C. trachomatis to asymptomatic men and healthcare providers, we used the framework of the Male Chlamydia Demonstration Project, which has been previously described.21 Briefly, from October 1999 to April 2003, men who did not report either urethral discharge or dysuria were offered testing for C. trachomatis in detention facilities, high school and university-based clinics, primary care clinics, and community venues in 4 cities. Testing methodology varied among centers, but in all cases consisted of an approved NAAT assay performed on the first 10 to 15 cc of first-voided urine. NAAT testing was provided free of charge to all sites. Screening sites were chosen on the basis of their access to young men who would qualify for screening and their ability to logistically administer the study’s procedures. The healthcare providers who offered testing to asymptomatic men were either employees of the facility (for established clinics or settings, including school-based clinics, adolescent clinics, and correctional facilities) or staff devoted to the demonstration project (for outreach efforts created specifically to offer testing in new settings, including street outreach or university fraternities).
Providers and staff were not instructed to use any particular scripted language in offering the test, but were asked to 1) offer testing to men who were sexually active and who were in the required age range, and 2) instruct men on correct specimen collection and STD reporting requirements. With the exception of the Baltimore adult detention site, men were approached face-to-face by study or clinic staff and invited to undergo testing. In the Baltimore adult detention site, the availability of screening was announced weekly over a public address system, and interested men voluntarily presented to the jail health clinic.
At all sites, men who agreed to testing were asked questions addressing demographics, sexual history, and reason for testing. Incentives were provided at 2 sites in Seattle: the University Clinic, where male college students received a small monetary incentive to undergo STD screening, and several University of Washington fraternities, where a competition among the fraternities to attain the highest rates of testing was instituted as part of the demonstration project. Testing at the fraternities was integrated into a weekly outreach health education program run primarily by peer health educators.
Acceptability of testing to asymptomatic men was assessed in 3 ways. First, test acceptance was prospectively measured at 2 centers (all Seattle venues and San Francisco adult detention settings) by tracking the numbers of men tested relative to those approached. Second, study staff at participating venues in all 4 cities maintained acceptability logs over discrete time periods (detailed in Table 1) while the demonstration project was underway. These logs provided a standardized means of recording site-specific variables, including the type of personnel assessing clients’ eligibility for and offering screening, the number of men seen over the course of a week, and the number of men who actually accepted testing. The logs were completed either by the venue staff who offered testing to asymptomatic men or by study staff who directly interviewed providers to obtain the necessary information, depending on the type of venue involved. Third, in Seattle, demographic and sexual history data were collected on all men approached to participate regardless of whether they accepted testing. Men who declined testing were also asked to provide a specific reason for declining the test. For the analysis of these men, characteristics of those who accepted testing (accepters), including demographics, sexual history, most recent healthcare visit, prior STD, and STD testing, were compared with those who declined it (decliners); the effect of using incentives for testing was also assessed.
The acceptability to healthcare providers of testing asymptomatic men was assessed by administering a survey to providers who had worked at the venues involved in the demonstration project. We chose this group of providers because we aimed to measure indices of acceptability apart from simple availability of the test, which is often a function of considerable cost or the dictates of individual program policy; accordingly, urine-based NAAT was available free of charge to the venues in which these providers practiced during the project. A standardized, self-administered survey that measured attitudes and practices about screening asymptomatic men for C. trachomatis was administered to providers who had participated in the demonstration project at various venues. Administration of the survey was coordinated by local study staff in all 4 cities, who ensured that every venue that had participated in the study submitted at least one completed survey.
Using SPSS statistical software, release 11.5 (SPSS, Inc., Chicago, IL), the association between acceptance of C. trachomatis testing and subjects’ characteristics for subjects enrolled in Seattle was measured by χ2 analysis, the Mann-Whitney U test (for nonparametric comparisons of continuous variables), and logistic regression (for multivariable analysis). Characteristics assessed included subjects’ demographics and history of STDs, sexual history, venue type, and recent access to any health care, as well as inclusion of incentives in the screening effort. All tests for statistical significance were 2-sided and a level of P <0.05 was considered significant. Interactions between terms entered into the multivariable analysis were assessed using a likelihood ratio test. Because a substantial proportion of subjects (36%, as further discussed in “Results”) did not respond to at least one of 3 questions about sexual history on the questionnaire (namely, number of recent sex partners and new sex partner in the prior 2 months and condom use at last sex), the multivariable analysis was performed not only on the entire study population, but also on the subset of men who responded to all 3 of these questions; results for the latter analysis are presented, as described in “Results.” For all centers, acceptability logs were reviewed and responses quantified and organized using a predefined categorization scheme. To describe a summary measure of test acceptance, the median percent was used to provide a more robust estimate given the observed wide range of testing uptake across different venues.
The numbers of asymptomatic men tested for C. trachomatis and the percentage positive at each of the 4 cities were as follows: Baltimore, 2,838 (10%); Denver, 3,323 (9%); Seattle 765 (1%), and San Francisco, 15,706 (5%).
Subjects’ Acceptability of Screening by City and Venue Type
In Seattle, 1,080 men were offered testing. Of these, 859 (79%) accepted testing. In San Francisco adult detention settings, a total of 10,515 men were approached for testing, and 9,419 (89.6%) accepted.
Review of the acceptability logs administered at all centers, summarized in Table 1, revealed that the majority of men in most settings were approached; however, testing uptake ranged widely depending on the type of venue and the approach used. Acceptance varied widely across cities even within the same venue type (for example, median acceptance in school-based clinics ranged from 17% to 66%) but was highest in juvenile detention (68%) and lowest in Baltimore adult detention settings (9.6%) and community-based outreach (24%). Median test acceptance as estimated by acceptability logs across all sites was 64%.
Predictors of Subjects’ Accepting Testing in Seattle
More detailed information on accepters and decliners was available for subjects enrolled in Seattle, where 1,080 men were offered testing. Of this total, 859 (79%) accepted testing, of whom 765 (88%) were asymptomatic. Full data on most variables on the questionnaire, defined as response to the sexual history components of the questionnaire (report of recent new sex partner, number of recent sex partners, and condom use at last sex), were available for a subset of 681 subjects (63% of all subjects, termed “responders”). The sex partner history variables were chosen for defining nonresponders because they were associated with the highest rate of nonresponse overall, and nonresponse to one was highly correlated with nonresponse to the others. Relative to men who were characterized as responders using this categorization, nonresponders were older (20 vs. 17 years; P <0.001), more likely to report being of white race (odds ratio [OR], 1.5; 95% confidence interval [CI], 1.2–2.0) and to have more sex partners in the prior 2 months (1.6 vs. 0.5; P = 0.03), to have attended a site that offered incentives for chlamydia testing (OR, 5.7; 95% CI, 4.6–7.2), and to accept testing (OR, 4.0; 95% CI, 2.7–5.9). There were no differences in responders versus nonresponders with regard to report of prior STD, previous chlamydia testing, condom use at last sex, and time to receipt of last healthcare visit. Despite these differences in the 2 groups, the main findings of multivariable analysis did not differ whether they were included in the model, as described subsequently.
Characteristics of responders who accepted testing are compared with those who declined testing in Table 2. In the multivariable analysis that controlled for subjects’ characteristics as well as whether an incentive was offered, accepters were significantly more likely to be younger than 20 years and to report a higher number of sex partners in the prior 2 months, not knowing whether they had previously had any STD, and less recent use of any health care (specifically, last health care was sought more than 1 year previously). Receipt of incentive was also independently associated with accepting testing; thus, acceptance rates for testing were highest in the 2 university-based venues: a weekly outreach program offered at different university fraternities run primarily by peer health educators and a university health clinic that offered the testing as part of a general STD research project. In multivariable analysis, men who accepted chlamydia testing did not differ from those who declined by race or in their report of condom use at last sex (with main or casual sex partner), new sex partner (2 months), or ever having been tested for C. trachomatis. Importantly, these findings did not change significantly when the multivariable analysis was performed on all 1,080 subjects in the study; however, because nonresponders generally did not respond to multiple questions, estimates for the categories of “no response” were highly unstable for several variables.
Of the 221 men who refused testing in Seattle, only 39 (18%) provided a specific reason for doing so using the self-administered questionnaires. The most commonly cited reasons were not feeling at risk for any STD (28%) and lack of symptoms (21%). Other reasons reported were lack of time (5%), not being sexually active (5%), and having tested recently for an STD (5%). Less common reasons (cited by one and 2 subjects, respectively) included having only one partner and reluctance to be tested as a result of the requirement of name reporting should the test be positive.
Acceptability of Screening to Providers
Surveys were administered to 59 healthcare providers at the demonstration project sites. All of the venues at which the demonstration project was conducted contributed at least one survey response, with 25 respondents from school-based clinics (42%), 19 from primary care clinics (community-based; 32%), 7 from street outreach projects (12%), and 8 from corrections settings (14%). The majority of respondents were nurse practitioners (66%), with the remainder identified as physicians (14%), nurses (8.5%), and physician assistants (6.8%). Of all respondents, 35 (59%) reported that they did not routinely screen asymptomatic, sexually active men for C. trachomatis. As shown in Table 3, none of these providers reported a lack of NAAT availability as the stated reason for not doing so, as would be expected because the tests were supplied as part of this study. A substantial minority (21%) of providers used an age cutoff for screening men; almost all had chosen 25 years. The most commonly cited reasons for not testing men related to providers’ perception that men themselves did not see themselves at risk for STD (49%) and not having adequate time (24%). When queried specifically regarding why they believed asymptomatic young men declined testing (Table 4), most providers reported that asymptomatic men believed they did not need testing because they did not see themselves at risk for STDs (61%) or because they did not have symptoms (65%). A substantial minority of providers cited other beliefs (Table 4), and most (88%) cited more than one. There were no differences in any measure by type of provider (nurse, physician, health outreach worker, health educator) or by venue type (data not shown).
In our large, national study of the feasibility of offering urine-based NAAT for C. trachomatis to young asymptomatic men outside of STD clinics, we found that testing was generally well accepted by men. However, even in settings where most men were invited to undergo testing, acceptance rates varied considerably by venue and city, although testing was made available at no cost to the sites or to the men who participated. Our data identify several reasons for incomplete uptake of testing. First, men who declined testing most commonly cited the absence of genitourinary symptoms and a belief that they were not at risk for STD. Providers indicated that most asymptomatic men did not perceive themselves to be at risk for STD and that the majority of men they saw with chlamydial infection were asymptomatic. Second, as illustrated by wide variation in testing uptake in our study’s participating adult detention settings, the manner in which testing is offered to asymptomatic men probably impacts the likelihood of their accepting a test. An encouraging finding was that in one city (Seattle) where data were collected on men who declined as well as those who accepted testing, men in key target groups were significantly more likely to accept testing than to decline it, including adolescents, those who had not sought any recent health care, and those with a higher number of recent sex partners. Small incentives also increased the likelihood that men would accept testing. These findings contribute to our limited understanding of why testing of asymptomatic men for chlamydial infection does not routinely occur, even in venues with relatively high C. trachomatis prevalence where this is likely to be cost-effective,22,23 and highlight areas that require attention before coordinated efforts to screen men at high risk of chlamydial infection are likely to be successful.
Simply making urine NAAT available and affordable outside of STD clinics may not ensure widespread uptake of testing of appropriate screening targets for several key reasons. First, although provision of testing in alternative venues may remove the potential stigma associated with seeking care and testing at STD clinics, significant concerns associated with STD testing are likely to remain.24–26 Eliciting these concerns, and related attitudes toward testing (particularly reasons for refusal and related beliefs), may require an approach other than the traditional self-administered questionnaire. For example, Blake and colleagues assessed young men’s beliefs and opinions about obstacles to and motivators for obtaining chlamydia screening in 4 focus groups.27 Participants expressed a wide variety of concerns about testing, including privacy and confidentiality, as well as considerable lack of knowledge about chlamydial infection itself and the meaning of a positive test. Some participants, for example, thought they could potentially die from a chlamydial infection or that a positive test might mean they were at risk of also having AIDS. The authors concluded that home-based chlamydia testing could potentially avoid many of the barriers to testing cited by participants and are currently exploring this further by offering testing with an Internet-based approach.
Second, both the male subjects and the providers who participated in our study reported that lack of symptoms was a compelling reason for men to decline testing, yet most men with chlamydial infection are asymptomatic.1–9 These findings indicate that young men at risk for chlamydial infection require education about the rationale for and value of chlamydia testing, including the implications that infection has for their sex partners. Finally, uptake of testing by asymptomatic men is likely to be strongly affected by the context in which the test is offered. For example, incarcerated youth asked to submit a urine sample for STD testing at registration may be more likely to comply, given the circumstances, than might youth approached in the context of a street-based outreach project. Individual providers or outreach staff might also impact men’s decision to be tested. In the one other study that has compared persons who accepted urine-based chlamydia testing with those who refused, overall acceptance among 1,231 people seeking care at an urban pediatric emergency department was 71%.28 Although those who accepted testing were older (16 vs. 15 years), black, and uninsured or insured by Medicaid, acceptance rates also differed significantly by which of the 3 study interviewers invited subjects to participate.
Our study has several limitations. Most important was that we used several methods to estimate the acceptability of testing. For example, full questionnaire-based data on men who did not accept testing were available for only the subset of men enrolled in Seattle; thus, findings from this part of the analysis might not be generalizable to other settings, particularly because the Seattle sites had a very low prevalence of C. trachomatis. However, acceptance rates were relatively similar across venues that used similar methods to approach men, and the diversity of these methods likely reflects what will occur in a real-world male screening program. Second, among the men specifically queried about reasons for declining testing, relatively few provided a reason for doing so. This observation supports the need for alternative formats to elicit men’s knowledge, beliefs, and attitudes about chlamydia screening,27 an implication also supported by the relatively high frequency with which men did not respond to several key variables on the questionnaire, even when they accepted testing. Third, the structured observation periods for defining acceptability were limited in some cases by the relatively short time periods covered and may not have accurately represented practices over the whole project. Finally, healthcare providers were surveyed toward the end of this project, during which free NAAT was provided. Although we succeeded in our attempt to gain representation of at least one provider from every venue that participated, we did not survey every individual provider who was involved in the project. For these reasons, the attitudes we report may not be representative of all providers in every venue or in settings where no efforts to screen men had occurred. However, addressing concerns of the group can provide insight for future research and policy efforts on screening asymptomatic men for chlamydial infection.
For asymptomatic men, the decision to be tested for chlamydial infection probably involves numerous complex factors. These include stimuli that might motivate men themselves to seek testing, including self-perceived risk for STD (possibly mediated by perception of sex partners’ risk behavior as well as their own), notification that a partner has an STD (identified through routine screening or detection at syndromic evaluation), and education about the purpose and value of screening (provided through peers, in media or educational venues, or at healthcare encounters not originally intended to provide STD care). Other factors might involve opportunistic encounters at which men are presented with screening options, including screening in schools, sports teams, detention settings, or in outreach projects. Our findings indicate that a successful approach to a cogent policy for screening asymptomatic men will need to emphasize a variety of these factors and should certainly include education of men and their providers about the largely asymptomatic nature of genital chlamydial infections, the value of screening in preventing adverse health outcomes (particularly in women), and continued availability of screening in critical venues—particularly detention settings and clinics for teens, especially in areas with high chlamydia prevalence—outside of STD clinic settings.
In summary, the major implication of our study is that although offering free chlamydia screening to men will not ensure universal acceptance of screening, most men are likely to accept testing depending on the venue and how they are approached. Future research should include more detailed qualitative assessments of asymptomatic men’s attitudes toward chlamydia screening, particularly as it relates to the potential value this approach might have for female partners’ health. As policy for screening asymptomatic men for chlamydial infection becomes clear, more systematic assessment of healthcare providers’ attitudes and practices regarding screening, and of system barriers to implementation, will be necessary.
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