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Chlamydia trachomatis Testing in the Second British National Survey of Sexual Attitudes and Lifestyles: Respondent Uptake and Treatment Outcomes

McCadden, Angela*; Fenton, Kevin A. MD*†; McManus, Sally MSC; Mercer, Catherine H. PhD*; Erens, Bob PhD; Carder, Caroline MSc§; Ridgway, Geoff MD§; Macdowall, Wendy MSc; Nanchahal, Kiran PhD; Byron, Christos L.; Copas, Andrew PhD*; Wellings, Kaye MSC§; Johnson, Anne M. MD*

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Sexually Transmitted Diseases: June 2005 - Volume 32 - Issue 6 - p 387-394
doi: 10.1097/01.olq.0000162364.65643.08
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GENITAL CHLAMYDIAL INFECTION IS the most common bacterial sexually transmitted infection in the United Kingdom with over 80,000 new infections being diagnosed in genitourinary medicine (GUM) clinics annually.1 It is well-recognized that a large prevalent pool of undiagnosed infection exists, in part a consequence of the asymptomatic nature of the infection.2 In England, public health response to genital chlamydia prevention and control has been scaled up in the past 5 years, and implementation of a national opportunistic screening program is in progress.3 Early indications are that these programs are acceptable to both the public and professionals4,5; however, few studies have provided information on the experiences and outcomes of notifying asymptomatic individuals who test positive for chlamydia outside of traditional clinical settings.6–10

The need for such data is becoming increasingly important. The increasing availability of nucleic acid amplification testing (NAATs) have allowed innovative approaches to providing urinary tests in nontraditional settings,11–13 including population-based household and postal surveys, occupational, penal, and educational institutions.14–17 Interventions such as telephone results notification, text-messaging, partner-delivered therapy, and partner notification by phone or by centralized third-party providers have been implemented or are being proposed.18 These approaches will require a reconsideration of the ways in which patient testing, treatment, and partner notification are managed, documented, and evaluated.

We have previously demonstrated the acceptability and feasibility of chlamydia testing as part of a probability sample survey of sexual attitudes and lifestyles.19 In this article, we report on the treatment, partner notification preferences, and outcomes of respondents diagnosed with genital chlamydial infection as part of a large national probability sample study of sexual attitudes and lifestyles in Britain (Natsal, 2000). We also present an analysis of factors predictive of urine sample provision, which led to the weighting scheme used here and earlier2 in estimation of population chlamydia prevalence.

Methods

Natsal 2000 is a stratified probability sample survey of 11,161 men and women aged 16 to 44, residing in Britain, interviewed between May 1999 and February 2001.2,20,21 The response rate (after weighting to correct for unequal selection probabilities) was 65.5%. Details of the survey methodology and questionnaire are published elsewhere.2,20,21 Briefly, a stratified sample of 40,523 addresses was selected from the small-user postcode address file for Britain, using a multistage probability cluster design, with oversampling in Greater London.22 Interviewers visited all selected addresses and at each address, enumerated residents aged 16 to 44, and then randomly selected one to be invited to participate. Interviews took place in respondents’ homes. A questionnaire was developed for a combination of face-to-face computer-assisted personal interviews carried out by trained interviewers and computer-assisted self-interview (CASI).23 The majority of questions were identical to a previous survey conducted a decade earlier (Natsal 1990)24–26 with additional questions that focused on patterns of partnership formation, sexual mixing, and sexually transmitted infection (STI) acquisition.13,27

Chlamydia trachomatis Prevalence Study

A random half (by alternate sampling points) of sexually active respondents aged 18 to 44 years were invited to provide a urine specimen for ligase chain reaction (LCR) testing for C. trachomatis infection. Sixteen and 17 year olds were not invited to participate in the study. Trained interviewers verbally introduced the study at the end of the main interview and provided written information regarding genital chlamydia infection, the rationale for testing, and the nature of the urine test. Respondents were informed that they would be only be notified (by letter) in the event of a positive LCR result. Respondents gave signed informed consent before providing 10 mL of urine in a sterile plastic container containing boric acid. The sample was then labeled (study identification number and date) and immediately packaged for transfer by first class mail to a central laboratory for LCR testing. When any delay in transporting the samples was anticipated (eg, collection over long weekends and holidays), interviewers were advised to store samples at 2 to 8°C until ready for posting. On arrival, a 1-mL aliquot of each sample was centrifuged and processed according to manufacturers (Abbot LCx® C. trachomatis assay) instructions. Positive and equivocal LCR results were reported to the study research nurse who then notified respondents.

All patients diagnosed C. trachomatis-positive or equivocal by LCR were initially contacted by mail. The first letter informed respondents of the possibility of infection and invited them to contact the study research nurse to discuss their results. If necessary, reminder letters were sent after 7, 14, and 21 days. All contacts with chlamydia-positive respondents were managed by a single study research nurse (AM). On contacting the research nurse, the caller identity was confirmed by checking their name, date of birth, and address. The respondent was then reminded why a sample was collected and what the test was for before the positive diagnosis was given. General facts about chlamydial infection were discussed, including transmission and treatment, stressing that any sexual partners would also require antibiotic treatment. Options for receiving treatment at either the respondent’s general practitioner’s office or local GUM clinic were given and arrangements made for written consent from the respondent for release of their result to their preferred service. The research nurse encouraged patients to attend their local sexual health service for treatment and recommended screening for other STIs. Retesting at local sites was advocated for those receiving equivocal tests or when verification of the result was requested by the respondent. Respondents gave consent for results to be passed on to their general practitioner or local GUM clinic, and to be recontacted after 2 to 3 weeks.

The research nurse also handled all correspondence with the treating physician. Once written consent was obtained from the respondent, an information pack was sent to the physician containing details about the Natsal 2000 study, a hard copy of the patient’s results, a recommended treatment protocol, and management outcomes pro forma for return to the study team. The management outcomes pro forma was used to obtain information on the date the respondent was seen, what treatment was prescribed, partner notification activity, and outcomes.

Patient follow-up interviews were undertaken by the research nurse to confirm compliance with treatment, check if partners had been notified, and to inquire generally on the well-being of the respondent after their experience of receiving a positive diagnosis as a result of participating in the study. These were done approximately 2 weeks after the initial telephone discussion with respondents and verbatim notes were taken. This final telephone interview asked about treatment compliance, partner notification activity, and outcomes, and provided a final opportunity to clear up any unresolved issues for the respondent. Patients were also asked how they felt about having participated in the study, about being informed of a positive result, and what happened when they approached their chosen clinical service for treatment. The interview also provided an opportunity for respondents to make any comments or suggestions regarding the process and conduct of the study.

Data Analysis

In analysis, data were weighted for differential selection probabilities and through poststratification as described elsewhere.21

We constructed a logistic regression model for urine sample provision using independent demographic indicators (age, sex, region, social class, ethnicity, educational qualifications, marital status), behavior (number of sexual partners in past year, condom use [ever], heterosexual anal sex [ever], HIV testing, homosexual contact [ever], injected drug use [past 5 years], GUM clinic attendance, STD diagnosis, partners from abroad, new partners [in last year], concurrent partners [last year], and interview characteristics (presence of other people in the household during the interview, any children in the household).

To provide unbiased estimation of the population chlamydial prevalence here and earlier,2 we additionally weighted for the urine sample provision rates using the inverse of the predicted probabilities from the regression model outlined above.

All quantitative data analysis was performed in STATA 7 using the complex survey analysis functions, accounting for the clustering, weighting, and stratification.

Detailed notes were taken during both the patient notification and follow-up interviews by the research nurse(Fig. 1). These were then analyzed first to examine recurring major themes and within each theme to explore the nature, range, and contexts of the responses. This qualitative analysis allowed for use of the rich interview data, providing some insight into the process of patient notification and treatment outcomes.

F1-11
Fig. 1:
Summary topic guides for patient notification and debriefing interviews with a Natsal 2000 research nurse.

Ethics.

We obtained ethical approval from University College London Hospitals NHS Trust, North Thames Multicentre, and all local research ethics committees in Britain.

Results

Overall Response Rates

A total of 11,161 respondents were interviewed in Natsal 2000. A total of 5105 were invited to provide a urine sample for C. trachomatis testing using the inclusion criteria identified in the methods section. A total of 3628 respondents agreed to provide urine samples and 3608 samples were actually received and tested at the laboratory, a 70.6% response rate to urine testing. Twenty samples were not tested as a result of delays in transit times or spillage in the mail. The median transit time between urine sample collection and arrival in the laboratory was 4 days (mean, 3.63; mode, 2). Seventy-three samples tested positive (31 men and 42 women). The prevalence (after weighting for unequal selection probabilities and to match the corresponding age/sex population profile) was 2.2% (95% confidence interval [CI], 1.5–3.3%) among men and 1.5% (95% CI, 1.1–2.1%) among women. After the additional urine provision weighting as described in “Methods,” the prevalence estimate remained the same (previously published2). Twenty respondents had equivocal results, 12 of whom provided a second sample for retesting. All 12 retested LCR-negative.

Provision of a urine sample varied significantly by demographic indicators, including gender, area of residence, socioeconomic status and ethnicity, as well as behavioral variables as used in Table 1, such as homosexual partnership, heterosexual anal sex, STI diagnosis, and unprotected sex (Table 1). After controlling for significant variables in the model, the response rate in Wales was significantly lower compared with almost all other regions in Britain (with the exception of eastern England) (Fig. 2). People in the professional social class (social class I) were more likely to provide a urine sample compared with the other nonmanual and manual social classes. White respondents were more likely to participate to the study, whereas Asians were less likely.

T1-11
TABLE 1:
Odds Ratios for Probability of Participation in the Urine Study
F2-11
Fig. 2:
Model-predicted urine study participation rates.Notes for Figure 2: Instead of discussing the variation in the odds of responding comparing with the average response (Table 2), the above formula can be used to calculate the model-predicted probability of response (i.e., response rate) for each of the significant variables in the model after adjusting for the effects of all other independent variables (i.e., when the other variables are held constant). These model-predicted response rates (and confidence intervals) are plotted in Figure 2. For ease of presentation, the intercept of the response model was changed so that the average response rate matched the actual response rate of 71% (black bar in the middle of each graph).Key: *L: London, NE: North East, NW: North West, EM: East Midlands, WM: West Midlands, SW: South West, EA: Eastern, SE: South East, W: Wales, S: Scotland. # Social class category I: professional, II: managerial and technical, IIINM: skilled nonmanual, IIIM: skilled manual, IV: semiskilled manual, V: unskilled manual. @ UPI: unprotected intercourse.

Participation rates differed by gender, and there was a significant interaction between gender and unprotected intercourse, and gender and anal intercourse. Women who had one or more heterosexual vaginal and/or anal sexual partners without a condom in the past year were more likely to participate compared with men who had no unprotected intercourse (Table 1 and Fig. 2). There was also a higher participation rate for men and women combined who had unprotected intercourse in the past year. Finally, respondents who reported anal intercourse were more likely to take part in the urine study compared with those who have never had anal sex. Women who have had anal intercourse were more likely to participate compared with men who have had anal sex (Table 1 and Fig. 2).

Patient Notification

All 73 chlamydia-positive respondents were sent at least one letter of notification about their results. The average time from sample provision to receiving of the first notification letter was 21 days. In total, 65 of 73 (89.0%) respondents contacted the study research nurse. Of these, 54 (83.1%) responded to the first letter, 4 (6.2%) to the second reminder letter, and 4 (6.2%) to a third reminder; and 3 followed the final notification letter sent by the study physician (KF). Hence, approximately 1 in 10 (7 of 73) chlamydia-positive respondents failed to contact the research team after four attempts to notify them over a 4- to 6-week period (Fig. 3).

F3-11
Fig. 3:
Summary of chlamydia testing results, treatment, and partner notification outcomes in Natsal 2000.

Treatment and Partner Notification Outcomes

All 65 notified respondents provided consent to have their results forwarded onto either their general practitioner (50 respondents) or local GUM clinic (15 respondents). Management ProFormas were returned from 27 (54%) general practitioners and 8 (53%) GUM clinics. One general practitioner had referred the patient on to the sexual health service for treatment and partner notification. All of the remaining 26 respondents seen by a general practitioner received the recommended antibiotic therapy and partner notification was discussed in all 26 cases. Only 21 of 26 (81%) respondents reported having traceable sexual contacts (their current sexual partner only) and 17 (81%) of these partners were treated by the respondent’s general practitioner (usually by partner-delivered therapy). Partners of respondents who were not offered treatment were referred either to their own general practitioner for treatment or to local GUM services. In one case, a general practitioner did not recommend treatment for the husband of a chlamydia-positive respondent because they were “in a stable relationship.” In this instance, the research nurse contacted the respondent and reiterated the importance of treating her current sexual partner.

The eight respondents referred to GUM all received the correct treatment and partner notification. Seven had traceable sexual partners (their current sexual partner only), all of whom had been advised to attend the GUM clinic for treatment. The sexual partner of a male chlamydia-positive respondent was diagnosed with symptomatic pelvic inflammatory disease when subsequently seen at the local GUM clinic. She had not previously seen a doctor regarding her symptoms.

Follow-up Interviews

After treatment, the study nurse contacted 45 (69%) of the notified respondents for the debriefing interview. Of these 45, 15 were patients on whom no management pro forma had been received after their referral. Therefore, treatment and partner notification outcomes were confirmed for 49 (75%) respondents who were notified of their result.

The purpose of the debriefing interview was to gather qualitative feedback about the process and conduct of all aspects of the study. It was also usually an opportunity to confirm that the respondent and any sexual partners had completed treatment. In some cases making contact for telephone interview proved difficult despite numerous attempts and therefore among these cases in whom contact was achieved, discussion was sometimes limited by circumstance; for example, when a respondent was in a public place or when a respondent was resistant to discussion. Priority at these times was to establish whether treatment had been received, but not always from what source this treatment was received.

Regarding participation in the urine testing study, most respondents expressed little reservation about being approached to participate in the urine testing component of Natsal 2000, although a small minority expressed being somewhat surprised about being asked or somewhat embarrassed. A few respondents said they would have preferred to have been informed about the possibility of a request for a urine sample at the beginning of the interview.

All respondents expressed surprise and concern at testing positive for C. trachomatis. The most common responses were being “worried” and “shocked” at the diagnosis, although at the same time very “glad to know” about their diagnosis. Almost all respondents said they had discarded the leaflets about chlamydial infection or the study. The majority of respondents denied any prior knowledge about the infection and said they did not remember much of the verbal information given to them by the interviewer.

The initial patient notification interview with the research study nurse was universally helpful in providing information on the diagnosis and clarifying options for treatment. Respondents usually felt reassured by the end of the initial telephone interview. Although it is difficult to assess reaction by telephone, very few respondents expressed anger or obvious emotional distress. The most frequent questions asked by both men and women regarded the likely duration of infection and the consequences of the infection on fertility. Respondents felt that this interview also helped underscore the importance of partner notification and ways in which this could be done.

The majority of respondents seen by their general practitioner reported that this was “fine” and many explicitly stated that, because they got along well with their general practitioner, this was the appropriate place to be seen. Among those choosing to attend their local GUM clinic, many reported being initially nervous, but this was rapidly overcome by the reassurance and professionalism of clinic staff. When asked what they (respondents) would have changed about the process, few additional comments to those mentioned here were received.

Discussion

Our study illustrates some of the challenges facing management and follow up of patients who provide biological samples as part of larger population-based surveys. Although the overall participation rate was high, those who provide urine samples are more likely to report higher-risk sexual lifestyles than those who do not. Among those who do participate, loss to follow up may complicate efforts to notify respondents of their results and to ensure treatment and partner notification resolution. Our findings have implications for future studies of this nature as well as the implementation of genital chlamydia screening programs in which similar methodologies for patient notification and follow up may be used.

Our findings confirm earlier studies in this field. In 1994, the American Centers for Disease Control and Prevention (CDC) tested the feasibility of adding an STD testing component to a national survey of adolescent males.13 Like with our study, interviewers collected urine samples from respondents to a behavioral and demographic household interview survey and limited sample collection to those 18 years of age or over. Although this was a much smaller sample (124 persons were interviewed of which 82 were eligible for urine collection), findings from the study also suggested higher-risk sexual lifestyles among those willing to provide a sample. Response rate to the study was 85% and overall prevalence of genital chlamydial infection was found to be 6% as compared with 2.2% among male respondents in Natsal 2000.

The bias from complete nonparticipation in a behavioral survey is difficult to assess, because little or no information is obtained from those who refuse to participate.28 In contrast, the bias from nonprovision of biological samples as part of larger behavioral surveys can generally be assessed, because those who do not provide samples may answer many survey questions describing their sexual experience. Consequently, it is in general possible to minimize the potential bias from sample nonprovision through an additional weighting scheme as we have in this study and earlier.2 Similar challenges to calculating prevalence or positive rates may also be seen in genital chlamydial screening programs in which selection and participation biases may result in considerable variations in the chlamydia prevalence across and within clinical settings.4,5 In some cases, this may result in higher-than-anticipated prevalence estimates being obtained. Aside from estimation of population prevalence, in which the objective of a program is to identify and treat as many infections as possible, then our findings should be viewed as encouraging, suggesting that women who agree to provide a sample may be those at greater risk.

Our study also uncovers some of the pragmatic problems facing researchers and practitioners who undertake chlamydia testing in the field. Loss to follow-up can be a major deterrent to our ability to identify and contact patients after having provided biological samples. Although all patients were notified of their positive result within 3 weeks postinterview, we failed to make contact with 10% of chlamydia-positive respondents. Although some may have acted on the information and sought their own treatment, we have no means of verifying this. This contrasts to community screening programs in which local screening coordinators have considerably greater capacity to verify with the screening sites, patients’ general practitioners, and local sexual health services whether treatment has been received. Thus, in the English chlamydia screening pilot,4,5 over 90% of the female chlamydia-positive cases were known to have received treatment. Although the majority of respondents contacted us after the first letter, a further 17% were added by sending a further three letters (the last by recorded mail from the study physician). We have previously shown that the most common reason for delays in responding were people being away on vacation; however, other reasons for noncontact, eg, lack of time, may also be relevant.19 The vigor with which positive participants are pursued will vary with the testing or screening program and the resources available. The national chlamydia screening program in England recommends that at least three attempts be made to notify individuals who receive a positive chlamydia screening test.3 Such a strategy seems justified when viewed with our results.

In general, the notified respondents were motivated to seek and comply with treatment, and intervention by the research nurse was required in only a few cases. This usually involved direct liaison with the general practitioner to facilitate retreatment among poorly compliant individuals. Given the choice, most respondents opted for treatment at their general practitioner’s office. This was despite strong encouragement from the study nurse on the benefits of a full sexual health screen, which would be available at local GUM services. Convenience and familiarity were given as the reasons for preferring to see the general practitioner in most cases. In some areas, visiting the GUM clinic would have entailed a much longer journey. In contrast with Duncan et al,29 who reported anxiety about stigma in their qualitative sample, only one respondent expressed concern about stigma associated with attending the GUM clinic.

For each chlamydia-positive respondent, we determined the number of partners eligible for partner notification and treatment. Because the majority of respondents reported only one eligible partner, we were able to confirm notification and treatment for a very high proportion of at-risk partners. This was considerably higher than that obtained in the English chlamydia screening pilots in which between 41% and 52% of at-risk partners had their treatment verified.4,5 This improved uptake of treatment by partners may in part reflect differences of age, marital status, and reported partnerships in this general population sample compared with populations attending clinical settings in the pilot study. It may also reflect the willingness of general practitioners to prescribe treatment for partners and the occasional use of patient-delivered therapy—strategies that are not currently recommended in the national chlamydia screening program.

As chlamydia screening and testing using NAATs become more commonplace in STI prevention and control programs, so too will the need for innovative approaches to manage these conditions in as efficient and cost-effective ways as possible. We have demonstrated some of the pitfalls and benefits in the application of these novel-testing methods in terms of respondent participation, follow up, and resolution. Nevertheless, our overall success in notifying and following up chlamydia-positive respondents and the lessons learned from our experiences should help to develop ways for refining these approaches in the future.

Acknowledgments

Angela McCadden was the study nurse who organized patient contact and follow up and was the lead writer of this article. Kevin Fenton participated in the design and implementation of this study and supervised the C. trachomatis substudy. Sally McManus and Christos Byron undertook the statistical analysis with contributions from Cath Mercer and Andrew Copas. Caroline Carder and Geoff Ridgway helped design and coordinate the laboratory testing and reporting. Anne Johnson, Kaye Wellings, Bob Erens, and Julia Field were coinvestigators and participated in the design and management of the main study and preparation of the manuscript. Wendy Macdowall and Kiran Nanchahal all contributed to the study organization and manuscript preparation.

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