CHLAMYDIA TRACHOMATIS (CT) and Neisseria gonorrhoeae (GC) genital infections are the most common curable sexually transmitted infections (STIs) for which surveillance data are available in the United States. 1–3 Traditional efforts to reduce infection rates have depended on testing for infection in clinic settings during symptom-oriented or routine health care. Effectiveness of this strategy is limited by 2 important factors. First, most people with infection do not experience symptoms and therefore have no physical cue to seek health care. 4,5 Second, many people at risk of infection either do not seek routine care or are not tested during routine care. 6–14
Nucleic acid amplification tests (NAATs) now make it possible to detect CT and GC genital infections in urine samples collected from both women and men, and vaginal swabs collected from women. 15–17 The noninvasive nature of these tests makes it possible to obtain specimens outside of conventional clinic settings and send specimens to laboratories where they can be processed. This provides an important opportunity to develop screening strategies targeting those who are at risk of infection and currently being missed by clinic-based control efforts. NAATs also offer the prospect of augmenting clinic-based treatment efforts and increasing our general understanding of STIs.
STI testing beyond clinic walls raises some new and unique challenges. In contrast to clinic-based care, testing initiatives outside of clinic settings could lack private personal interactions with healthcare professionals who can discuss and recommend testing, so alternative strategies must be used to encourage testing. Specimens are typically self-collected, and some individuals could be reluctant to provide urine or vaginal swab specimens in nontraditional settings. 18,19 Specimens might need to be transported to laboratories by mail, which can present logistic problems. Communicating test results while protecting privacy could be difficult. Furthermore, persons already disenfranchised by the healthcare system could choose to forgo treatment if they are required to attend a conventional clinic, and the alternative of in-field treatment could limit follow-up counseling, preclude testing for other STIs, and complicate partner notification.
Literature published over the past 7 years describes the early use of NAATs to test for CT and GC infection outside of clinic settings. Our goal is to summarize this literature because it represents the prelude to a possible revolution in our ability to understand and control STIs through use of these tests. We describe the use of NAATs outside of clinics, whether specimens were actually provided by the populations being targeted for testing, procedures related to notification of test results, success of notification efforts, treatment strategies, documentation of treatment, and management of partners. We also attempt to highlight particularly promising approaches, gaps in our current knowledge, and areas for further research.
We searched the MEDLINE, PsycINFO, HealthSTAR, and Cochrane Library databases from January 1995 to August 2002, restricting our search to English-language articles describing research conducted with humans in developed countries. Search terms included sexually transmitted diseases, chlamydia, gonorrhea, screening, testing, reproductive health, adolescent health, nonclinic testing, urine testing, school-based, community health services, and home sampling. We also examined the reference lists of relevant articles.
Our review focuses on reports of CT or GC testing that involve self-collection of urine or vaginal specimens outside of clinic settings. We chose to include testing initiatives carried out at school-based health centers (SBHCs) because we viewed testing in these settings as primarily school-rather than clinic-based. Reports were included if they described at least 2 of the following: testing strategy, participation/refusal rates, system used to notify test-positive individuals of their test results, proportion of test-positive individuals notified, mechanism used to link test-positive individuals to health care and treatment, proportion of test-positive individuals treated, approach used to notify and treat partners, and proportion of partners traced and treated.
We identified 29 articles that met inclusion criteria. Two authors reviewed all selected articles and created summary tables. Tables were reviewed by all authors to identify overarching or notable themes.
Most of the testing programs we identified were directed at adolescents or young adults, although a few programs addressed other specific populations such as gay men. Specimens for CT and GC testing have been collected in schools, communities, and homes. Collection of specimens at home has occurred primarily in conjunction with household surveys in the United States but has been linked to a wider range of purposes in Europe.
Testing in School Settings
Studies in Maryland (MD), Louisiana (LA), and Pennsylvania (PA) have shown that screening for curable STIs is feasible in at least some schools in the United States (Table 1). 4,20–23 Two of these testing programs were conducted in SBHCs. In MD and PA, students who presented to a SBHC for any reason were asked to provide urine, or to self-collect vaginal swab specimens, for CT and GC testing. 20,23 The testing program was schoolwide in LA, 4,21,22 where all students were brought to testing areas during selected class periods to receive one-on-one counseling regarding the opportunity for CT and GC screening. PA and LA students could be tested whether or not they were sexually experienced.
Participation in testing programs based in school settings is complicated by the issue of a minor’s ability to legally consent to STI testing. Most adolescents can provide consent and receive confidential services for STI testing and treatment in clinical settings because of state minor consent laws. 24 Nonetheless, conducting STI testing on school grounds raises complex issues regarding parental consent. For example, in the testing program in middle school health centers in MD, parental permission was required for SBHC enrollment. Between 55% and 77% of students were enrolled. Although students could self-enroll in these SBHCs specifically for STD services without a parent’s consent, it is important to note that the participation rates shown in Table 1 are based on those who were sexually active and attending the clinic, not all students enrolled in the school. 20 In PA, testing was conducted in high school health centers and although it is unclear whether parental consent was required for SBHC use, the study population probably does not represent the total enrolled student population. 23 In the school-wide LA testing program, parental consent was required to test students who had not received prior parental consent to use a SBHC. 4,21,22 Refusal rates among LA parents ranged from 1.6% to 13.5%, with higher refusal rates in the schools that did not have SBHCs.
Within this context, among eligible students, participation rates in school-based testing programs have been moderately to extremely high. Where STI screening has been linked to SBHCs, from 75% to 95% of middle and high school students seen at SBHCs have been tested. 20,23 Recruitment appears more challenging, but still relatively successful, when school testing does not occur in SBHCs. In the LA schoolwide program, two thirds (67.8%) of students with parental consent in the original 3 schools chose to be screened the first year 21 and half (52.4%) of students with consent participated in CT testing in 5 schools added the third year. 4 Over the entire 3-year period, almost 90% of continuing students participated in at least 1 of the 5 rounds of testing, suggesting that repeated opportunities for screening can be particularly effective.
Among those tested, all 3 school-based interventions detected high proportions of positive tests. Between 8% and 21% of female students, and up to 6% of male students, tested positive for CT. 4,20–23 These results could underestimate infection among sexually active students, because 2 of the studies included sexually inexperienced students in their testing programs.
School-based testing programs generally have relied on the SBHCs or school nurses to communicate positive test results to students and arrange treatment. The proportions of test-positive students notified of results and treated generally have not been reported. One study documented in-house treatment for 88% of infected students. 21 Among those not treated, most had either dropped out or could not be located despite continued school enrollment. Whereas notification of test results has been carried out by SBHC staff or school nurses, it has been left up to infected students to encourage their partners to seek evaluation and treatment either at a SBHC (MD) or at a public STI clinic (LA). In LA, partners could be treated by school nurses if enrolled at the same school as the index patient, but most infected students reported that their partners were not enrolled students. 22
Testing in Community Settings
CT and/or GC testing programs in community settings are summarized in Table 2. 25–32 It is not easy to calculate participation rates for community-based efforts, at least in part because of the inherent difficulty in determining the numbers of those eligible for testing. When researchers have estimated the proportion of those approached who were actually tested, approximate participation rates range from 14% (peer outreach workers approaching teens in nonfacility settings) 26 to 40% (volunteer “drag nurses” approaching patrons of gay nightclubs). 25 Some studies have reported time taken to recruit samples. Outreach workers at Canadian community-based organizations were able to test 626 clients in 6 months, 31 and it took 20 months to test 486 male youth in Denver, Colorado. 32 The highest documented participation rates were at a community HIV testing center and youth detention center. 27,30
Some researchers have compared the effectiveness of encouraging care-seeking versus testing outside of clinic settings. When peers approached teen males in community settings and distributed coupons for a complete STI examination at a local clinic, less than 1% (5 of 1563) of coupons were redeemed, but 14% agreed to be tested in the field. 26 In another study, peer outreach workers encouraged male and female teens to have STI examinations at any of 4 local clinic sites, offered to accompany the teen to a clinic and assist with the screening process, and gave vouchers redeemable for $10 at the end of the clinic examination. 32 Despite all of these efforts, only 89 teens identified with the project (45 women and 44 men) were seen in clinics; in contrast, 486 male teens agreed to participate in urine testing outside of clinic settings for a $5 incentive. These investigators conducted focus groups to understand the greater acceptance of urine CT screening outside of clinic settings when compared with free comprehensive screening at school-based, community health, and public STI clinics. Embarrassment, anxiety about screening procedures, and the belief that one need not see a doctor unless symptomatic were reported as factors influencing choices about clinic versus nonclinic testing. 32
In community screening programs, among those tested, the proportions testing positive for CT infection have ranged from 2.0% to 28.3% among women and from 1.1% to 8.8% among men. 25–32 The proportions testing positive for GC have ranged from 3.0% to 13.1% among women and from 0.5% to 2.8% among men. 25,28,30,31 Multisite testing programs have shown that the proportion of positive tests varies by site. 29,32 The lowest yield program was at a community HIV testing site that served primarily older white clients in Denver, Colorado, 27 and the highest was at a youth detention center in Birmingham, Alabama. 30
Most community programs have successfully notified test-positive individuals of their results, although this frequently has required intensive effort. Notification appears to be most successful when identifying and contact information is collected at the time of testing. In one study that initially relied on tested individuals calling for their results in 2 weeks, only 19% of all participants and 22% of infected participants called. 25 When programs obtain identifying and contact information, maintaining privacy is challenging, especially when adolescents live at home with their parents. One study used a multifaceted notification approach in which staff provided participants with a phone number to call for results, asked participants for written consent to fax positive results to their doctor or clinic, and asked younger persons (presumably minors) for contact information for a “trusted adult” to whom positive results could be communicated. 28
Most community-based screening programs have reported high treatment rates (88–100%) for infected participants. Three of the 8 community programs offered treatment in the field if a test-positive person was unable or unwilling to go to a clinic for further evaluation and treatment; and when this method of treatment was offered, it was selected by 43% to 100% of test-positive cases. 26,27,32 In the 3 instances in which the testing-to-treatment interval has been noted, shorter intervals were linked to in-field treatment, 32 permission to fax test results to a physician, 28 and length of stay in juvenile detention centers. 30 Although some community-based initiatives have made intensive efforts to locate and treat partners, few have managed to treat more than half of the contacts elicited. 26,32
Testing in Home Settings in the United States
Five studies in the United States indicate that it is possible to test older adolescents and young adults for CT and GC in home settings (Table 3). 5,33–36 With the exception of one study involving distribution of home testing kits at a pharmacy and gym, 33 home testing studies in the United States have been conducted as part of household surveys targeting young women in the San Francisco Bay area, 34 males participating in the National Survey of Adolescent Males (NSAM), 5,35 and male and female adults (aged 18–25) in Baltimore, MD. 36 Between 84% and 91% of those approached as part of a household survey agreed to be tested, and these acceptance rates occurred within the context of financial incentives (typically $10–20) specifically linked to providing a specimen. The acceptance of home testing in “real-life” situations could be much lower. Only 38% of free home testing kits that were picked up at a pharmacy or gym in San Francisco were returned. 33 Logistic problems such as shipping problems and inadequate urine volume have been noted in several home-testing studies. 5,33,36
Home surveys in the United States have reported estimates of prevalence using weighted data to take into account complex sampling designs. CT prevalence has ranged from 3.0% to 5.7%. 5,34–36 Just 1.3% (1 of 76) of the predominantly white gay male population screened as part of the home-testing community campaign in San Francisco tested positive for CT. 33 Prevalence of GC infection was estimated at 5.3% from Baltimore’s household survey 36 and 3.9% (3 of 76) in the home-testing program in San Francisco. 33
Although survey researchers in the United States generally have not reported the proportions of infected participants notified of their results, notification strategies have included asking participants to call and having staff attempt notification by telephone, registered mail, or regular mail. In one regional study, follow-up meetings were arranged with all participants to discuss test results, and all with positive results were notified. 34 The home-testing program initiated in a pharmacy and gym asked participants to call for results and also collected identifying information so that those who tested positive but did not call could be contacted. 33 In all of these studies, persons notified of a positive test were counseled to go to a doctor or clinic for treatment. In the pharmacy/gym study, treatment was offered by home delivery or pharmacy pick-up (all elected pharmacy pick-up). 33 The proportions of test-positive individuals treated were either 100%33,34 or not reported. 5,35,36 Information on partner follow up has not been reported.
Testing in Home Settings in Europe
CT testing programs in home settings in Europe have been initiated by media campaigns and through clinics, schools, and household surveys (Table 4). 37–47 Many have relied on recruitment strategies linked to, or based in, clinical settings. European studies have not included GC testing.
Acceptance of CT home testing by European study populations has ranged widely. In studies in which recruitment was clinic-based, testing has been accepted by one third to one half of the patients approached or deemed eligible for home testing. 40,46,47 Once successfully recruited by a healthcare professional, the proportions who returned home test kits have been quite high. 40,42 The success of home testing through recruitment of patients on clinic rosters by mail has been influenced by population mobility and accuracy of mailing information. 41,47 British investigators achieved an 83% specimen return rate after mailing home testing kits to a random sample of general practice (GP) patients, but only after 2 further mailings and additional follow up with nonresponders by phone or at home. 41 Single follow-up reminders by mail appear to be associated with lower return rates. 46,47 With no follow-up reminders, less than one third (29%) of male undergraduate students returned home urine CT test kits. 45 Acceptance of home testing initiated through schools was relatively successful in one Danish study. Although fewer than one half of high school students met eligibility requirements, 93% of female and 97% of male students who were eligible submitted home CT test kits. 43 Moreover, among female students who agreed to be contacted 1 year later, over half (51–59%) returned mailed home testing kits after receiving a single mailed reminder. 44
A few British studies have attempted to assess barriers to participation in home sampling initiatives. Refusers who were asked about their reasons for declining to participate in a postal study cited low perceived risk, emotional reasons, and annoyance at being asked to provide personal information by mail. 41 A few participants in another home sampling study commented on the difficulty of correctly collecting vulvar swab and first-catch urine samples or described the process as messy or “personal.”46 In a study assessing the feasibility of linking urine testing to a general population survey, a comparison of respondents who did and did not provide a specimen showed that the only factor significantly associated with a lower likelihood of participating in urine testing was the presence of “anyone else in the house at the time” (odds ratio, 0.42; P = 0.03). 39 During interviews with a subset (n = 36) of male and female survey respondents, some voiced suspicions that the samples would be used for other purposes or indicated that they had agreed to provide urine only out of a “sense of obligation,” and some described the use of sequential informed consent as “unexpected” and potentially misleading. Factors such as personal motivation (eg, recognizing an opportunity for a free test), altruism (eg, understanding the need for surveillance data), lack of embarrassment, and rapport with the interviewer emerged as motivations for testing. 39
The proportion of those who test positive for CT in European home-testing studies has varied widely, influenced by the purpose and design of the study. High rates of test positivity were found when home testing was used to test partners of known CT-positive women 37 or to monitor for reinfection. 40 The lowest proportions of positive tests have generally been found in studies involving patient roster-derived samples. 41,45–47
Most of the European home-testing studies have notified participants of test results by mail 38,43–46 or by sending test results to the individual’s healthcare provider. 47 In a feasibility study for a household survey, participants with positive or equivocal results received a letter notifying them of a “possible infection” and were instructed to contact the study physician. Up to 3 reminder letters were sent if needed, but most participants (88%) contacted the study physician after the first letter. 39 In addition to informing participants of their test results and treatment options, the study physician asked individuals for their permission to forward their results to a physician or local STI clinic and requested consent for follow-up contact at 2 weeks. With this approach, they documented 100% notification and treatment rates for all 16 test-positive individuals. Similar treatment success was achieved by the Danish study involving high school students. 43,44 Most other home-testing studies in Europe have not reported treatment rates.
Few studies have described strategies for contacting sexual partners of those who test positive for CT or effectiveness of contact efforts. One home-testing study specifically focused on testing partners of women with positive CT tests diagnosed in GP clinic settings. 37 Women in the intervention group were asked to provide their male partners with CT home-testing kits that included a prepaid envelope in which to mail the sample. Women in the control group were asked to give their partners a packet that contained a written request to visit their doctor and a urethral swab to be collected by the doctor and returned in a prepaid envelope. Significantly more partners in the intervention group were tested as compared with the control group (68% vs. 28%), and partners of women in the intervention group were tested sooner (mean delay, 12.6 vs. 17.7 days).
Many creative strategies have been developed to initiate CT and/or GC testing in schools, communities, and at home using NAAT technology. Our review shows that initiation of testing in all of these settings is feasible. This provides tremendous opportunities to reduce rates of CT and GC infection among groups at risk of infection that are currently being missed by clinic-based control efforts. Our review also highlights opportunities to use testing outside of clinic settings to augment clinic-based treatment efforts such as efforts to test partners 37 and to monitor for reinfection. 40 Finally, testing for CT and GC infection as part of household survey research provides important opportunities to increase our general understanding of STIs. 5,34–36,39
Identification of promising approaches is influenced by the goal of testing. When the goal is to identify and treat infection among asymptomatic populations not linked to clinic settings, school-based or school-linked initiatives hold promise for reaching students. Most of the school-based studies that we reviewed reported moderately or extremely high recruitment rates, 4,20–23,43 and in many locations this was possible even with a requirement for explicit parental consent. Moreover, screening in schools does not require the presence of a SBHC. 4,43 When it is not feasible to collect STI specimens on school grounds because of policy or political reasons, 48 one randomized, controlled trial in Europe has shown that school-initiated home testing can dramatically increase the numbers of adolescents tested. 43
Particularly promising approaches for reaching other asymptomatic populations not linked to clinic settings include testing at carefully selected community facilities that serve those at risk of STIs (eg, juvenile detention centers), 29,30 partnering with community organizations that explicitly serve adolescents and young adults, 28,31 and designing intensive, tailored community outreach testing programs. 25,26,28,31,32 These approaches could be especially important when targeting young men. Two studies reported that young men were much more likely to agree to on-the-spot urine STI screening in the field than to agree to go to a clinic, 26,32 which underscores the importance of continuing to experiment with alternative screening strategies directed at men. Two programs have used media campaigns to encourage home testing among at-risk populations, 33,38 an approach that warrants further investigation.
Nonclinic-based testing also holds promise for improving the quality of STI-related health care delivered to populations already connected to traditional clinic settings. Home testing has been used in Europe to screen asymptomatic populations listed on clinic rosters. 41,46,47 In addition, home testing has been successfully used to improve the care of patients diagnosed with infection in clinic settings by increasing the numbers of partners treated 37 and by monitoring for repeat infections. 40
Alongside opportunities, our findings highlight the challenges of STI testing outside of clinic settings and that there is much to be learned. First, a better definition of who should be targeted for nonclinic screening initiatives is needed. The prevalence of infection among the populations in our review varied widely. Previous research has focused on defining CT screening algorithms in clinic settings, 16 but different screening algorithms could be more appropriate when targeting populations outside of clinic settings. Development of new algorithms will become feasible as CT and GC prevalence data from nonclinic population-based surveys become increasingly available. 5,36,49 The effectiveness of non-clinic-based initiatives in reaching their intended population also must be measured.
Second, most studies have not meaningfully assessed the effectiveness of alternative testing strategies in reducing infection rates. Few have reported the proportion of test-positive participants notified of their test results, and even fewer have reported the proportion of those notified who received treatment. When reported, the proportions notified of positive test results and treated have ranged from 22% to 100%. One longitudinal study 4 designed to estimate whether school-based screening produced lower rates of infection over time found that incidence infection rates for CT decreased among male (6.2% vs. 3.2%) but not female (11.5% vs. 10.3%) students. This highlights the complexity and importance of determining the overall effectiveness of alternative testing strategies as well as of specific program components.
Third, initiation of testing outside of clinic settings poses numerous logistic challenges. Choice of testing technology and type of specimen collection (eg, urine sample, vaginal swab) will be influenced by individuals’ willingness and ability to self-collect specimens outside of clinic settings, whether screening targets men, women, or both, distance from the laboratory, mode of transportation, laboratory capabilities, and influence of temperature on test performance. 18,50–54 There are also considerations pertaining to postal and packaging requirements if specimens are mailed. 53 In one recent study in the United States, packages for mailing urine specimens from the field to a laboratory had to meet minimum Federal Express packaging requirements for urine diagnostic specimens and be in compliance with Occupational Safety and Health Administration standards for noninfectious, diagnostic specimens and biologic requirements. 49
Fourth, communication and counseling about test results, treatment, partner notification, and risk reduction are complex phenomena. 55–58 Many patients who test positive for CT or GC in clinic settings are not notified of their test results or treated despite considerable provider effort. 59 If successfully notified, clinic patients could not receive counseling about partner notification and risk reduction. 6 Testing outside of clinic settings, independent of an existing relationship with a healthcare facility or professional, adds further challenges. For example, those tested outside of clinics could prefer passive notification strategies (eg, “don’t call me, I’ll call you”), 60 which could yield low notification and treatment rates. 25,61 Active notification approaches (eg, tracing and contacting those who test positive) are labor-intensive and require considerable sensitivity to issues of privacy and confidentiality. 53,62 Even after being notified of a positive GC or CT test result, some individuals are reluctant to seek health care but will accept in-field treatment, 27,32,33 which precludes comprehensive testing for other STIs. Finally, partner notification and risk-reduction counseling could be procedurally, qualitatively, and quantitatively different within the context of nonclinic-based testing initiatives, which will likely influence effectiveness. To date, investigators largely have failed to describe and evaluate counseling linked to nonclinic-based testing. Future research will need to address these complex issues, and to define the potential role of in-field treatment of index cases and partner-delivered therapy when testing is initiated outside of clinic settings.
Our review has several limitations. Although we conducted an extensive search, it is possible that we missed articles that should have been included. Furthermore, some articles were excluded based on our conceptualization of clinic-versus nonclinic-based care. For example, we excluded reports of screening of military recruits who were present in “physical examination sections” of military facilities 63 because we viewed this as conceptually similar to clinic-based screening. This does not minimize the potential importance of systematic screening programs targeting high-prevalence populations such as military recruits, regardless of whether screening is conducted in traditional clinic, nontraditional clinic, or distinctly out-of-clinic settings. Finally, defining a beginning and ending date for our review was necessary but also somewhat arbitrary, and reports published outside of this time interval were excluded.
In conclusion, the use of NAATs to detect CT and GC infection outside of clinic settings will undoubtedly continue in all parts of the world. 64 We agree with others that the next phase of research should focus on how to use screening outside of clinic settings to effectively reduce rates of infection. 16 Particular attention should be focused on defining the populations at risk of infection who are most likely to benefit from screening initiated outside of clinic settings and determining how to best target these populations. Programs to screen and reduce rates of infection need to be carefully designed and evaluated. Evaluations should focus particular attention on identifying program components that have a direct impact on effectiveness in decreasing rates of infection and disease. The cost-effectiveness of alternative testing strategies also needs to be evaluated and placed within the context of existing public health funding resources. Successful testing strategies for CT and GC could provide a template for programs to reduce infection with other curable STIs when comparable nonclinic testing technologies become available.
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