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Original Study

Internet-Based Screening for Sexually Transmitted Infections to Reach Nonclinic Populations in the Community: Risk Factors for Infection in Men

Chai, Shua J. MD, MPH*; Aumakhan, Bulbulgul MD, PhD*; Barnes, Mathilda BS; Jett-Goheen, Mary BS; Quinn, Nicole BS; Agreda, Patricia MS, MBA; Whittle, Pamela BA; Hogan, Terry MPH; Jenkins, Wiley D. PhD§; Rietmeijer, Cornelis A. MD, PhD; Gaydos, Charlotte A. MS, MPH, DrPh*†

Author Information
doi: 10.1097/OLQ.0b013e3181e3d771
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Over 1.1 million cases of Chlamydia trachomatis and over 300,000 cases of Neisseria gonorrhoeae infection were reported nationwide in 2007, making chlamydia and gonorrhea the 2 most commonly reported infectious diseases in the United States.1 These infections are known to lead to severe consequences. Pelvic inflammatory disease occurs in up to 40% of untreated women,2 which can further result in infertility, ectopic pregnancy, and chronic pelvic pain.1 Chlamydial infection can also result in male infertility.3 Because chlamydial infections are usually asymptomatic, only less than half of the active infections are diagnosed.4 Both chlamydia and gonorrhea increase risk of human immunodeficiency virus (HIV) transmission.5

Trichomonas vaginalis is the most prevalent nonviral sexually transmitted infection (STI) nationwide; approximately 8 million cases occur per year.6 Trichomonas infection can cause pregnancy complications7 in women. It also increases the odds of HIV infection,8,9 and can cause pelvic inflammatory disease in HIV-infected women.6 Up to one-third of infected women and most of infected men are asymptomatic.6

Asymptomatic men increase the burden of STI sequelae in their female partners and screening specific high-risk men can be cost-effective.10 Since 1993, screening of sexually active women under the age of 26 has been recommended,11 but no guidelines exist for screening men. Some guidance documents support screening certain high-risk men.12

STI screening can reduce STI sequelae, including pelvic inflammatory disease, by 60%,13 but certain high-risk groups such as young adults aged 15 to 24 years face significant barriers to screening. Lack of transportation, cost, and confidentiality issues impede access to screening and treatment.14,15

A novel internet-based screening program targeting women began in 2004,16,17 which bypassed barriers to screening and accessed hard-to-reach high-risk women. Women found internet-based screening acceptable and self-collection of specimens preferable.14 Since September 2006, a new program began which targeted men. Because no prior published data exist on using internet-based screening in men for 3 prevalent STIs, we studied whether this method of screening was acceptable to men, whether internet-based screening reaches a high-risk population, and identified demographic and sexual behavior risk factors that place this population at risk for STIs.

MATERIALS AND METHODS

We provided free kits, testing, and treatment to men ≥14 years, who resided in Baltimore (MD), Maryland (outside Baltimore), the District of Columbia (DC), West Virginia, select counties of Illinois, and Denver (CO). We advertised the study through flyers in schools, hospitals, and the community, and also through local radio station announcements. The institutional review boards of Johns Hopkins University, Baltimore City Health Department, and the State of Maryland approved the study for all study sites. Written collection instructions and diagrams showing how to collect the sample were included in the kits and also displayed on the website.

Website Design and Development

The www.iwantthekit.org website for female screening was expanded to include a section for men (Fig. 1). Linked pages covered educational topics, written at an eigth-grade reading level, about STIs, testing, and treatment. A link initiated a confidential e-mail request for a kit, which was mailed by the study coordinator to a requestor's address.

F1-5
Figure 1.:
Homepage of www.iwantthekit.org.

Components of the Self-collected Urine and Urethral Swab Kit

Prenumbered kits included an instruction manual, a male flocked swab (Copan Diagnostics, Inc, Murrieta, CA),18 GenProbe (GenProbe, Inc, San Diego, CA) transport media in a Copan UriSwab urine collection kit, a contact form, a questionnaire, 2 consent forms, and a postage-paid return mailer. Participants were asked to complete the contact form, as sort of a reminder, just in case a participant forgets to call for his results; the form also collected basic demographic information without identifiers. Participants were instructed to carry out the following instructions: (1) self-collect the penile swab by following the included male anatomy diagram for self-sampling the penile urethra and place it in the GenProbe specimen transport tube, and (2) self-collect a urine sample on the Copan sponge-on-a-shaft and place it in another GenProbe transport tube. Participants were then asked to seal both transport tubes in plastic biohazard bags, and mail them to the laboratory in the provided envelope along with the dated consent form, contact form, and completed questionnaire with the kit number.

Laboratory Methods

Urine and penile Copan swabs were tested by transcription-mediated amplification (TMA) (Gen Probe APTIMA Combo 2 [AC2], San Diego, CA), a nucleic acid amplification test approved by the Food and Drug Administration for screening male urine and urethral samples for gonorrhea and chlamydia.19 Samples were also tested for trichomonas using an analyte specific reagent TMA (GenProbe), which has been verified against previously validated real-time polymerase chain reaction for trichomonas.20,21 For each STI, participants were considered positive if the urine sample was positive or if a positive penile sample was also positive on a confirmatory test using a different nucleic acid amplification test (NAAT) primers for the organism.

Results and Treatment

When a participant called the toll-free number for results, he was required to give his kit number and password. The project coordinator helped infected men select a treatment clinic; results were faxed to the clinic and an appointment was scheduled. The coordinator contacted the clinic later to verify treatment. Contact form data were used to provide information for those men who forgot to call.

Cohort

Participants were included in the study only if they submitted a sample for testing and a signed consent form. Questionnaire submission was considered optional; those without a returned questionnaire had their questionnaire responses treated as missing data.

Statistical Analysis

Outcome included STI positivity, which was coded as a binary variable. Participants with a positive test result by either urine or penile swab for any one of chlamydia, gonorrhea, or trichomonas infection were considered positive for an STI. Participants with negative test results by urine and swab for all 3 STIs were considered negative. For bivariate analyses, all variables were treated as categorical variables, and dummy variables were used as needed. STI positivity was regressed on demographic and risk factor variables using logistic regression to determine unadjusted odds ratios.

Multivariable logistic regression was conducted using the a priori plausible risk factors age, race, and geographic location, which were identified in the literature,22 and also risk factors associated with the outcome in bivariate analyses with P ≤ 0.20. For the multivariable model, age and age at first sexual experience were entered as continuous variables. STI positivity was regressed on these risk factors to determine adjusted odds ratios. Interactions between risk factors were examined, and a parsimonious model with all predictors having a P < 0.05 was selected by lowest Akaike's information criteria23 score. Goodness of model fit was tested using the Hosmer–Lemeshow method.24 Statistical analyses were performed using the software package Stata, version 10.1 (College Station, TX). P < 0.05 was considered significant.

RESULTS

Kits Received for Testing

Between September 2006 and May 2009, 1644 male kits were requested online and 512 (31%) were returned for testing. Of the kits returned, 6 did not include signed consent forms, 2 kits were received from outside states, and 3 participants who were tested reported no prior sexual activity. These were therefore excluded from analyses, leaving a total of 501 (98%) men for this study.

Demographic Characteristics

Of the 501 participants in this study, 476 (95%) returned questionnaires. All questions had ≤10% missing responses, except for presence of symptoms, prior use of internet-based screening, and prior testing for an STI (11%–13% missing). Of the participants, 45% were black, 47% white, 2% Asian, and 6% other (Table 1); 93% were non-Hispanic. The median reported age was 24.5 years (interquartile range, 21–30 years) and the majority of the participants were single (84%). More than 75% of participants were from the Maryland-DC metropolitan area (Baltimore, Maryland outside Baltimore, District of Columbia, and West Virginia), as Illinois and Denver were added later in the program.

T1-5
TABLE 1:
Basic Demographic Characteristics, Reported Symptoms, and Screening Results—Internet-Based Screening Cohort of Men (N = 501)

More than half of the participants earned between $10,000 and $49,999 (55%), and currently had health insurance coverage (53%). Approximately one-third had at least a high school education (31%) or had attended some college (31%), and one-quarter had at least a bachelor's degree (25%).

Results of Testing

Of the 501 men, 106 (21%) tested positive for at least one of the STIs caused by C. trachomatis, N. gonorrhoeae, or T. vaginalis (Table 1). Of the 106 men who tested positive, 64 (13%) tested positive for chlamydia, 4 (1%) for gonorrhea, and 49 (10%) for trichomonas; 9 men (8%) tested positive for chlamydia and trichomonas; and 1 man (1%) tested positive for all 3. Men who tested positive for any STI were significantly most likely to report one or more of the following symptoms (P = 0.003): penile discharge (P < 0.001), pain during urination (P = 0.049), and penile itching (P = 0.032). Chlamydia positivity varied by location; the highest prevalence was seen in Baltimore (18%), followed by Denver (17%), Maryland (13%), District of Columbia (8%), Illinois (7%), and West Virginia (2%). Penile swab sensitivity was higher than urine for both chlamydia (93% vs. 78%) and trichomonas (82% vs. 40%). All men testing positive for any STI were treated except for one (99% treated). Time taken from sample collection to testing did not exceed the manufacturer's package insert recommendation for any of the samples.

Risk Factors for Infection

In bivariate analyses, race, geographic location, lower income, and lack of condom use were significantly associated with STI positivity (Table 2). Alcohol use before sex was associated with STI negativity. Black and “other” races had 2.60 (95% confidence interval [CI] = 1.57–4.32) and 3.16 (95% CI = 1.25–7.97) times greater odds of STI positivity as compared with whites, respectively. Men from Maryland (odds ratio [OR] = 10.88, 95% CI = 1.46–81.1), Baltimore City (OR = 19.61, 95% CI = 2.57–149.8), Illinois (OR = 13.53, 95% CI = 1.65–110.8), and Denver (OR = 16.51, 95% CI = 2.08–131.3) had significantly higher odds of STI positivity as compared with West Virginia (Table 2). Less condom use and lower income were both associated with increasing the odds of STI positivity. More men with multiple or new partners, and men who had sex with men, used condoms “Most of the time,” and few used condoms “Never” as compared with men without these risk factors (P ≤ 0.01). Prior treatment for an STI was not associated with either STI positivity or condom use.

T2A-5
TABLE 2:
Bivariate Logistic Regression of Sexually Transmitted Infection Status on Risk Factors for Infection—Internet-Based Screening Cohort of Men (N = 501)
T2B-5
TABLE 2:
(Continued)

In multivariable analyses, age, race, and income were significantly associated with STI positivity after controlling for other factors in the model (Table 3). For every 5-year increase in age, odds of STI positivity decreased by 38% (95% CI = 9%–57%). As compared with white, black and “other” races had 2.87 (95% CI = 1.52–5.42) and 3.96 (95% CI = 1.36–11.59) times greater odds of STI positivity, respectively. Furthermore, as compared with participants from West Virginia, men from Baltimore (OR = 11.23, 95% CI = 1.36–93.0), Illinois (OR = 9.96, 95% CI = 1.15–86.1), and Denver (OR = 14.20, 95% CI = 1.61–125.2) had significantly higher odds of STI positivity. A trend of lower income was significantly associated with higher risk of STI positivity, except for participants earning >$100,000.

T3-5
TABLE 3:
Multivariable Logistic Regression of Sexually Transmitted Infection Status on Risk Factors for Infection—Internet-Based Screening Cohort of Men (N = 423)

Lack of condom use was also significantly associated with STI positivity. A trend in increased STI positivity was noted with decreased condom use, and men who reported never using condoms had 4.96 (95% CI = 1.76–13.95) times greater odds of STI positivity.

Acceptability of Internet-Based Screening

Most STI-negative (78%) and STI-positive (72%) participants preferred a self-administered specimen versus one conducted at a clinic (overall, P = 0.283) (Table 4). Both groups reported that penile swabs were safe (STI-negative = 87%, STI-positive = 84%, P = 0.806) and “very easy” or “easy” to use (STI-negative = 90%, STI-positive = 87%, P = 0.368). Although 12% to 14% of men had used internet-based screening previously, most had not (STI-negative = 88%, STI-positive = 86%, P = 0.739). The majority in both groups stated that they would use internet-screening again (STI-negative = 90%, STI-positive = 88%, P = 0.565).

T4-5
TABLE 4:
Acceptability of Internet-Based Screening by Sexually Transmitted Infection Status—Internet-Based Screening Cohort of Men (N = 501)

DISCUSSION

To our knowledge, we report here the first internet-based screening program for 3 prevalent STIs in men. A prior report demonstrated that internet-based screening was feasible in low-risk men (chlamydia prevalence 4%),25 but did not include gonorrhea or trichomonas, 2 highly prevalent STIs. As more individuals access the internet to obtain health information, conduct health transactions, and find sexual partners, integrating testing of prevalent STIs into this medium may become increasingly important.26

Similar to internet-based screening in women, internet-based screening in men also reached very high-risk men with a high prevalence of STIs (21%). Prevalence of chlamydia (13%) in our study was greater than that seen in high-risk men across the United States, including incarcerated young men (6.8%–7.9%)22,27 and male youth in inner-city schools (7.5%–10.1%).15,28 Men in certain urban areas in this study, including Baltimore and Denver, had chlamydia prevalence (18% and 17%, respectively) equal to or higher than high-risk men in STI clinics.29

Prevalence of trichomonas (10%) was only slightly higher in STI clinics (12%–13%).29,30 Although gonorrhea prevalence (0.8%) was much higher in STI clinics (12.8%),30 its prevalence in our study was similar in community-dwelling men in the highest risk age-group nationwide (0.45%; ages, 20–24). The lower prevalence of gonorrhea versus reported symptoms suggests that we reached mostly high-risk, asymptomatic men, because in men gonorrhea is most often symptomatic, which leads them to be tested. Prevalence of coinfection with chlamydia was similar among female patients in emergency departments (8%).31

In this study, men also had a high prevalence of prior STIs (34%). Although 29% of men reported having a partner with a prior STI, only 11% of those men reported always using a condom during sex, that is, 2 synergistically high-risk behaviors. More than half of the men reported having a new partner and more than one-third reported multiple partners in the past 3 months.

Certain demographic characteristics were associated with STI positivity. The STI surveillance data state that, males in their late teens to early 20s have the highest prevalence of chlamydia and gonorrhea,1 which are consistent with our finding that age was independently associated with STI positivity. After controlling for income, location, and age, and examining factors such as perceptions of testing confidentiality and insurance status, which can affect healthcare access,32 it was found that black race was associated with increased STI prevalence, which is consistent with prior studies.22,27 However, previously reported unmeasured factors, including perceptions of discrimination, lack of perception of risk, unavailability of services, and healthcare staff prejudices,32 might help to partially explain this association.

Although few men reported race as “other”, those men had very high odds of STI positivity. The public health effect of this finding is unclear. Although previous smaller studies have not shown an association between poverty and STI prevalence,33 results from larger nationwide studies34 agree with our finding that income is independently associated with STI positivity. The observed dose-response relationship of increased STI prevalence with decreased income provides greater evidence for this association. Not surprisingly, STI prevalence varied by geographic location, which has been previously reported.1

Certain risk behaviors were also associated with STI positivity. As expected,35 lack of consistent and correct condom use was associated with increased STI positivity in a dose-response relationship, and the magnitude of the association (OR = 4.96 for the “Never” use category) is convincing of the efficacy of condoms against STI transmission. However, several known behavioral risk factors were not associated with STI positivity in our study, including multiple or new sexual partners,36 male-to-male sex,1 and prior STIs.10 The lack of association between increased STI positivity and these risk factors might be largely explained by condom use. Men with multiple or new partners, and men who had sex with men, reported using condoms significantly more frequently than those who did not report these risk factors. No association between prior STIs and STI positivity was found in this study; the previously reported study examining internet-based testing found a similar lack of association.25

Men who submitted a sample found internet-based screening acceptable. Penile swabs were perceived as safe, and the majority of men rated swabs as “Very easy” or “Easy” to self-collect. Among the men who participated in this study, 77% preferred a self-administered STI specimen, suggesting that internet-based screening might capture a population that would otherwise not be tested. Importantly, the majority of men who submitted a sample stated that they would use internet-based screening again, suggesting its high overall acceptability. Although our study had a high return rate (31%) of samples for an internet-based service, the acceptability for men who did not submit a sample is unknown.

Internet-based screening, especially if provided free of charge, may overcome barriers to STI testing for multiple high-risk populations who might not otherwise be tested. Over 45% of the men accessing internet-based screening had no health insurance, a known barrier to STI testing.32 Also, youth may lack money and fear breach of privacy. Among the men who accessed internet-based screening, 11% comprised of youth and 70% of the participants felt that internet-based screening was private. Low-income blacks, an underserved population for STI screening,32 were reached in large proportions. Screening for STIs can be cost-effective in high-risk men,37 and the prevalence of chlamydia in this study (13%) was even higher than that seen in high-risk groups (2.3%–3.2%). Self-testing costs appear to be lower than clinic testing costs, even after accounting for partial kit return rates. Using estimated indirect costs for clinic testing of chlamydia and gonorrhea ($62/visit38), provider costs ($25/visit), direct costs for testing in our laboratory ($30/test), direct costs of our mailed kits ($10/kit), and the 31% kit return rate, we estimated total costs for clinic testing to be at $117/test, and for self-testing at $62/test. We estimated that self-testing yielded a net savings of $55/test.

Several limitations exist in our findings. Because internet-based screening was voluntary and is inherently targeted to individuals who use the internet, self-selection might have biased the results. Some data suggest that me who use the internet to find sexual partners39 are at higher risk of contracting an STI, which might have led to false associations. However, this effect was most likely minimal, because risk factors reported in this study are well-established. In fact, a recent report suggests no association between seeking sexual partners on the internet and STI prevalence,26 perhaps because internet use for all types of activities, including finding sexual partners, has become normalized across many populations. Because risk factors were self-reported, recall difficulties might have introduced reporting errors. Although some data were missing, their effect was most likely minimal because few (9%) individuals were excluded from the final multivariable model.

Lack of access to computers because of low income and low educational level could challenge the effectiveness of internet-based screening. However, recent evidence suggests most adults living in public housing have access to a computer, and disparities are narrowing.40 Although internet-based screening for STIs such as syphilis and HIV cannot be easily conducted, these STIs are far less prevalent nationwide as compared with chlamydia, gonorrhea, and trichomonas.

AC2 TMA testing was recently reported to have lesser sensitivity for chlamydia and gonorrhea in self-collected glans specimens.41 However, AC2 testing was more sensitive in male penile swabs in our study as compared with first-catch urine. We do not have an explanation for these differences. Additional characterization of AC2 performance in male penile and glans swabs is needed.

Internet-based screening can reach a high-risk population for STI testing and treatment. Risk factors for STIs in this population reflect known STI risk factors. Because people at a greater risk for STIs face barriers and have a high preference for self-testing, internet-based screening has the potential to reach populations which might not otherwise access STI testing. Although internet-based screening is most likely cost-saving, detailed, additional cost effectiveness studies will be needed and certain measures, such as implementation of secure web-based result notification, could serve to increase efficiency. With additional data in this nascent area, further clarification on the role of STI screening in men might be obtained to inform future guidelines. In an era of healthcare reform and transition, internet-based services could provide additional options to obtain low-cost, accessible healthcare.

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