Sexually Transmitted Diseases:
Home-Based Self-Sampling and Self-Testing for Sexually Transmitted Infections: Acceptable and Feasible Alternatives to Provider-Based Screening in Low-Income Women in São Paulo, Brazil
Lippman, Sheri A. MPH*†; Jones, Heidi E. MPH‡; Luppi, Carla G. PhD§; Pinho, Adriana A. MPH§; Veras, Maria Amelia M. S. PhD§; van de Wijgert, Janneke H. H. M. PhD∥
From the *Division of Epidemiology, University of California, Berkeley, California; the †Population Council, Campinas, Brazil; the ‡Population Council, New York, NY; §Centro de Estudos, São Paulo, Brazil, and the Department of Social Medicine, Santa Casa Medical School, São Paulo, Brazil; and the ∥IATEC Foundation and Center for Poverty-Related Communicable Diseases, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
The authors thank Juan Diaz, Paul Hewett, Barbara Mensch, Rute Sampaio de Oliveira, Cristhiane Herold de Jesus, and Manoel Ribeiro for their collaboration in study design and implementation and the clinic staff for their time and patience. The authors also thank Dr. Helio Hehl Caiaffa and his team at the Microbiology Laboratory at the Santa Casa Hospital, and Jeanne Moncada at the San Francisco General Hospital Chlamydia Laboratory for assistance with laboratory procedures. The authors thank Victor Zubeldia and Lídia Rodrigues de Oliveira Silva for graphic design of the collection brochure.
This study was funded by the Office of Population and Reproductive Health, Bureau for Global Health, U.S. Agency for International Development, under the terms of Award No. HRN-A-00-99-00010.
The opinions expressed herein are those of the authors and do not necessarily reflect the views of the U.S. Agency for International Development.
Correspondence: Sheri A. Lippman, MPH, Division of Epidemiology, University of California, Berkeley 140 Warren Hall, Berkeley, CA 94720-7360. E-mail: firstname.lastname@example.org.
Received for publication June 20, 2006, and accepted August 27, 2006.
Objective: The objective of this study was to determine whether home-based screening for sexually transmitted infections (STIs) is acceptable, feasible, and increases the proportion of women screened among low-income women in São Paulo, Brazil.
Study Design: Eight hundred eighteen women were randomized to receive a clinic appointment or a kit for home-based STI self-collection and testing. All participants collected 2 vaginal swabs, one for polymerase chain reaction detection of chlamydia, gonorrhea, and trichomoniasis and another for a self-conducted rapid test for trichomoniasis.
Results: Slightly more women responded to the initiative within 2 weeks in the home group (80%) than in the clinic group (76%) with younger women showing improved response to home-based screening. Ninety-four percent of home group participants successfully completed self-collection and self-testing on their first attempt.
Conclusions: Home-based self-collection and self-testing was acceptable, feasible, and resulted in a slightly higher response rate. Home sampling and testing provide promising alternatives to clinic-based STI screening across diverse contexts.
INCREASINGLY, PROVIDERS, POLICYMAKERS, AND RESEARCHERS have recognized that an effective response to the global sexually transmitted infection (STI) epidemic necessitates alternative and multiple strategies for STI screening and treatment.1 Provider-dependent, clinic-based screening programs capture only a small proportion of infections in women, principally because screening requires an often inconvenient clinic visit and uncomfortable pelvic examination, which may discourage clinic attendance, particularly among younger women.2 Additionally, most clinic-based screening for STI in the developing world rely on syndromic diagnosis, which captures only symptomatic STI, less than 50% of most bacterial STI in women.3 Recent advances in STI diagnostics make screening outside of the clinic environment with noninvasive collection feasible,4–8 in turn leading to an increase in the number of women screened by virtue of convenience, privacy, and avoiding the stigma of clinic attendance.
In the last 10 years, researchers have assembled an impressive collection of evidence that screening for Chlamydia trachomatis (Ct), Neisseria gonorrhoeae (Ng), and Trichomonas vaginalis (Tv) can be conducted effectively outside of the clinic environment. Studies have demonstrated that women, including young women, are capable of collecting their own vaginal samples,7,9–12 that several nucleic acid amplification tests, including polymerase chain reaction (PCR), perform well on self-collected vaginal specimens12–15 and that PCR testing of vaginal swabs transported dry are an accurate diagnostic method for detecting chlamydia and gonorrhea16 as well as trichomonas infection.17 Additionally, women often prefer the self-collection process, which may involve introduction of a cotton-tipped swab or tampon into the vagina or urine collection, over provider collection.7,9–11 Hard-to-reach populations, or those least likely to access health services, report a strong preference for self-sampling.18,19 Recent efforts to provide STI screening in community settings have successfully improved the proportion of women screened in resource-rich countries. For example, Ostergaard et al. found that home-based self-sampling and mailing specimens to a central laboratory increased the number of women tested for chlamydia 11-fold in Denmark when compared with uptake of provider-collected sampling for STI testing in clinics.20 Similarly, studies in the United Kingdom,21,22 Sweden,23 and the United States5,7 have shown that mailing samples for chlamydia and gonorrhea testing is feasible, acceptable, and may reach people unlikely to seek screening.
Little research has been conducted to date regarding the acceptability and feasibility of nonclinic-based strategies for STI screening in developing countries. One study conducted in South Africa found that self-sampling was feasible and acceptable in the clinic, suggesting that home-based strategies could be tested in this setting.24 Moreover, no research in either resource-poor or wealthy nations has been undertaken documenting the use of self-testing and diagnosis for STI outside of the clinic setting. Self-testing for STI would involve not only self-collection of a sample such as a vaginal swab, but also execution of the test and diagnosis by the individual without the assistance of a provider. With growing advances in the development of rapid point-of-care tests, self-tests for STIs, similar to home pregnancy tests, could become available in the near future.25,26 We tested the acceptability and feasibility of introducing self-sampling and self-testing in both the home and clinic environment in a low-income population in São Paulo, Brazil. We hypothesized that offering home-based screening kits, including rapid STI self-diagnosis for trichomoniasis, would increase the proportion of women screened and treated for STI, especially among younger women. To our knowledge, this study was the first in the Latin American region to explore the use of home-based self-sampling and testing for STI.
Materials and Methods
From April to November 2004, 818 women 18 to 40 years old were randomized at enrollment to receive either a home-based STI self-collection and testing kit (experimental group) or an appointment for clinic-based STI self-collection and testing (control group) at the study clinic: the Centro de Saúde Escola Dr. Alexandre Vranjac, Barra Funda (CSEBF). Study participants were recruited from the clinic population, including women seeking family planning services, cervical cancer screening, pediatric care or care for other health concerns, and from the clinic catchment area in a working class neighborhood in central west São Paulo, Brazil. Nonclinic-based recruitment included outreach by community health agents, staff invitation at local businesses, and newspaper advertisements. Eligible participants self-identified as able to read well enough to follow collection and testing instructions. The study protocol was approved by the ethical committees of the Irmandade Santa Casa de Misericórdia de São Paulo, the Brazilian National Ethics Committee (Comissão Nacional de Ética em Pesquisa), and the Population Council.
Daily recruitment meetings at the clinic included a discussion of study procedures, instruction for collection of vaginal swabs and self-testing, and STI prevention education. After the recruitment meeting, eligible women who chose to participate in the study and provided informed consent were assigned the next available study identification number in numeric sequence, underwent either an interviewer-administered or computer-administered questionnaire, STI/HIV risk reduction counseling, and finally, opened an envelope with their study number indicating whether they were randomized to the home or clinic group. Identification numbers were randomized before study commencement in blocks of 16 to ensure that the numbers in each group would remain steady throughout the study. Study staff and investigators in Brazil, including the study coordinator who assigned study ID numbers, were masked to the randomization sequence; home and clinic group numbers were assigned and randomization envelopes were compiled by the investigative team in New York. Blinding of randomization group was not possible once the randomization envelope for each participant was opened, because procedures for home and clinic groups differed.
Women randomized to the home group were given a kit with their prelabeled study ID number to take home. Home kits included a cotton-tipped swab for performance of Xenotope's XenoStrip Tv test (Xenotope Diagnostics, San Antonio, TX), the trichomonas test materials, and a brochure with instructions and captioned pictures describing how to collect a vaginal sample and conduct and interpret the test. Figure 1 displays a condensed version of the instruction brochure, which also included a response section to indicate the sampling date, time, and test results. Home kits also contained a Dacron swab used for self-collection to be returned to the clinic and sent to the laboratory for PCR testing of chlamydia, gonorrhea, and trichomonas. Participants were instructed to collect the sample and perform the testing within 14 days of enrollment and to bring the used XenoStrip Tv test and the Dacron swab to the clinic in provided packets as soon as possible, always within 7 days of sample collection.
Women randomized to clinic-based screening received an indistinguishable kit, also prelabeled with their study identification number, which included condoms, information regarding STIs, local resources for reproductive health services, and an appointment card for STI screening at the study clinic. Clinic appointments were scheduled within 2 weeks of enrollment. Clinic group participants received the same instructions and performed the same collection and testing procedures as the home group participants; however, clinic group participants performed the trichomonas test in front of a nurse to allow for observation of any difficulties and assistance if necessary. They also underwent speculum examination and collection of 2 clinician-obtained endocervical specimens: one for storage and possible future testing, and one for performing a clinic-based rapid test for gonorrhea and chlamydia (data not shown).
Participants responded to a questionnaire on acceptability of home-based self-collection and testing at sample dropoff (home group) or at the end of the clinic-based STI screening appointments (clinic group). Women who did not come to the clinic for their appointment or did not return the home-sampling kits to the clinic within 2 weeks were given one reminder to come in for sample collection or dropoff. During a 6-week follow-up visit, for which participants received up to 3 reminders, all participants were given an additional opportunity to screen for STI if they had not done so previously.
Self-testing for trichomonas was performed using the Xenotope Diagnostics' Inc. XenoStrip Tv Trichomonas Test, an immunochromatographic test that detects antigens directly from self-obtained vaginal swabs and provides results within 10 minutes. Dry self-obtained vaginal swab specimens were delivered to the Microbiology Laboratory at the Santa Casa Hospital, São Paulo, where they were tested for the presence of chlamydia and gonorrhea using COBAS AMPLICOR CT/NG PCR (Roche Molecular Diagnostics, Pleasanton, CA). Trichomonas was diagnosed using an inhouse PCR test adapted from a previously validated assay27; PCR protocols were reviewed by the San Francisco General Hospital Chlamydia Laboratory.
Data were double-entered in Epi Info v6.04d days (Centers for Disease Control and Prevention, Atlanta, GA) and analyzed with STATA version 8.2.28 The hypothesis that a higher proportion of women in the home group would respond to the screening initiative as compared with the clinic group was evaluated with z-statistics for difference in proportions, using one-tailed tests, given the unidirectional hypothesis. Bivariate analysis of differences in sociodemographic, health-seeking, behavioral characteristics, and acceptability and feasibility variables between randomization groups were evaluated using t tests for differences in means for continuous variables and z-tests for differences in proportions for dichotomous variables.
Predictors of response to the screening protocol within 2 weeks of enrollment and of preferences for self-collection, home-based collection, and self-testing were assessed by logistic regression. Potential predictors included: 1) sociodemographic variables, including age, income, education, housing characteristics, marital status, and race; 2) health service utilization and variables predictive of acceptability of self-testing, including prior enrollment at the study clinic, history of Pap smear, home pregnancy test use, and tampon use; 3) sexual behavioral variables, including lifetime partners, current partners, recent concurrent partners, and condom use; and 4) current STI symptoms, past infections, and risk perception. Predictor variables were entered into logistic models and tested one at a time with likelihood ratio testing. Potential confounders and effect modifiers of the relationship between randomization group and compliance were identified in bivariate analysis; effect modifiers were identified by adding interaction terms into the models one at a time.
Of 1,038 women screened for study eligibility, 128 (12%) were not eligible mostly because of young age. Of 910 eligible women, 92 (9%) chose not to participate principally as a result of time constraints and prior commitments. Only one woman declined to participate because she was uncomfortable with self-collection and testing. Overall, 410 women were randomized to the home group and 408 to the clinic group; approximately 60% of both groups were registered at the study clinic before participating in the study. Participants' mean age and years of schooling were 28 and 9 years, respectively, with a mean and median income of approximately U.S. $375 and U.S. $272 a month, respectively (Table 1). Six percent of the sample lived in favelas (slums) or in shacks. Overall, 13% of participants who were screened had any of 3 STIs (Ct, Ng, Tv) based on PCR diagnosis with no difference between the home and clinic groups. Home and clinic group participants differed only by average lifetime number of partners and marital status.
The results of response to the screening initiative are portrayed in Figure 2. A modestly greater proportion of women in the home group returned samples to the study clinic within 2 weeks of enrollment (80%) as compared with women presenting for screening in the clinic group (76%) (one-sided P = 0.06). After receipt of a reminder phone call or letter (per participant consent) for nonresponders at 2 weeks, a slightly higher proportion of home group participants responded before the 6-week follow-up visit (n = 381 of 410 [93%]) as compared with clinic group response (n = 359 of 403 [89%]) (one-sided P = 0.03). By the end of the study, participation in screening reached 96% of those enrolled and all but one woman received complete treatment for PCR-diagnosed infections. The considerable response rate reflects the study staff's repeat invitations and reminders (up to 3) to present at the clinic for the follow-up visit 6 weeks after enrollment.
Among women screened (n = 787), 96% were comfortable collecting their own vaginal sample and found self-collection easy (Table 2). Ninety-two percent of participants thought the rapid trichomonas test was easy to perform, and, although approximately 10% found the results moderate or challenging to read, participants' and providers' interpretation agreed in 98% of home group tests when the test was valid. Overall, home-based testing was feasible: 94% of home group participants were able to complete collection and self-testing at home on their first attempt. Difficulties for test performance mainly reflected poor understanding of instructions or small mishaps: 5 women (4 in the home group and one in the clinic group) poured a preservative packet included in the testing kit into the solution, 2 people spilled the liquid, and one person diluted the solution with water. Women followed recommendations closely for timing their sample collection and dropoff; women in the home group collected their samples and brought them to the clinic a median of 6 days (interquartile range: 3–12) after receiving the testing kits (data not shown). The home group had a slightly higher proportion of inhibited and contaminated samples for PCR testing as compared with the clinic group; however, the difference was not statistically significant. Over 60% of the women in the home group reported preferring home-based self-collection and self-testing in the future, whereas only half of the clinic group preferred self-collection over provider collection and fewer preferred self-testing (42%). Only one fourth of clinic group participants would opt for home collection, the only study procedure they did not experience.
Multivariate analyses for predictors of response to the initiative within 2 weeks demonstrate an interaction between age and randomization group (Table 3). The negative coefficient (0.94 odds ratio) for the interaction term implies that although response to the screening initiative was higher overall in the home group, this improved response in the home group decreased with increasing age. Conversely, as the women in the clinic group got progressively older, their compliance improved. Specifically, odds ratios for response to the screening initiative in the home group as compared with the clinic group went from 2.4 among 18 year olds to 1.6, 1.2, 0.9, and 0.6 among 25, 30, 35, and 40 year olds, respectively (age-specific data not shown). Response to screening was negatively related to difficulty getting to the study venue, having no bathrooms in the home, and family income, and positively related to prior enrollment at the study clinic. Other covariables were not associated with response to the initiative; education was no longer associated when income was included in the model.
Randomization group was the strongest predictor for preference of self-collection and testing procedures in the future (Table 4). The experimental group had 1.7, 4.4, and 1.9 times the odds of preferring self-collection, home-based collection, and self-testing, respectively, compared with the clinic group. Every additional bathroom in one's home increased the odds of preferring self collection (odds ratio = 1.5) and home-based collection (odds ratio = 1.3) compared with provider and clinic-based collection. Family income was positively associated with preference for self-collection and self-testing, whereas having had a Pap smear, having a gynecologic complaint, positive rapid trichomonas test, or a concurrent partnership were negatively associated with a preference for self-collection, home-based collection, and/or self-testing (Table 4).
Introduction of home-based self-collection and testing for STIs resulted in a small increase in response to screening as compared with clinic-based self-screening in a low-income population of Brazilian women, demonstrating the feasibility of a home-based testing approach in this population as well as the potential to improve screening rates. A slightly higher proportion of women in the experimental, home-based screening arm responded to the screening initiative within 2 weeks and within 6 weeks than in the control arm. However, the response rate was high in both arms with over 75% responding within 2 weeks. P values for small differences in response rates between the 2 groups were quite low as a result of the ample sample size to detect minor differences; we can conclude that offering home-based screening garnered at least as good of a response, if not slightly better, than clinic-based screening. Additionally, the number of total infections treated in the experimental arm was equivalent with that in the control arm by the end of the study. A number of factors likely contributed to the exceptional return in both groups: 1) study staff aimed to screen and treat all enrolled participants, sending multiple reminders; 2) the high-quality care at the study clinic and personal relationships with study staff; and 3) the novelty of self-testing and receipt of instantaneous results with new diagnostics. Additionally, because women in the home group were required to drop off their specimens at the study clinic rather than mail in the specimens, some added benefits of home-based testing were likely lost, making the groups more similar. Returning specimens by mail was not an option for return of home-based screening kits in Brazil both because it is illegal to mail biologic materials and because mailing requires declaration of contents at central post offices; there are no mailboxes for bulky post.
Our findings are consistent with research documenting that home-based screening improves uptake, can increase infections diagnosed and treated, and may result in fewer adverse sequelae. A trial in Denmark6,20 found that female students randomized to home sampling had higher uptake of screening,20 and fewer infections and fewer cases of pelvic inflammatory disease at 1 year of follow up6 compared with students offered clinic-based testing. The same investigative team randomized young residents in one Danish county to receive home sampling kits by mail, a reply card for kit request by mail, or an opportunity for usual care. Response in the former 2 groups was more than quadruple and triple that of women in the usual care, clinic-based screening group.4
As hypothesized, age was an important predictor for uptake of home screening with younger women responding more readily to home-based screening. Given that young women may not feel comfortable in the clinic environment, particularly with pelvic examinations, self-collection and home-based STI testing may increase the number of young women getting screened for STIs. One study offering home-based testing in Sweden found uptake to be the highest in the 20- to 24-year-old age group.23 A study in the United States demonstrated that half of the girls (13–19 years old) diagnosed with an STI would not have pursued screening were self-collection not an option.9 In Brazil, like in most contexts, young women have high prevalences of STI29,30 and are less likely than older women to seek gynecologic care.31 A recent study in Brazil found that less than half of sexually active women aged 15 to 19 reported having ever seen a gynecologist before the study, and yet 12% of them tested positive for chlamydia and 2% for gonorrhea.32 Offering alternatives to pelvic examinations may, thus, significantly improve screening rates in the youngest and often most vulnerable women. Not surprisingly, response to this STI screening initiative was also related to prior enrollment at the clinic and logistic factors such as having an available bathroom for collection and ease reaching the study clinic. Logistic barriers are not insurmountable; 2 homeless women in the study returned with their testing kits and asked to collect their samples in the clinic bathroom.
Home-based self-testing is acceptable and feasible in this study population, 80% of which has a per-capita income less than or equivalent to one minimum salary in Brazil (compared with 30% of the population in São Paulo). Most women followed illustrated instructions and completed the procedures successfully. The fact that slightly more women in the clinic group than the home group completed self-collection and testing successfully on their first attempt (98% vs. 94%) is likely the result of assistance from the clinic nurses who, although instructed not to interfere in clinic-based self-collection and testing on the first try, may have provided some guidance to clinic group participants. Additionally, timing of kit dropoff was successful; dry swabs can sit for up to 7 days at ambient temperature (Barbara Van Der Pol, personal communication, December 9, 2003) and women in the home group returned their samples a mean of 1.5 days after collection. Although mishandling of specimens may be more likely to occur in nonclinic settings, inhibited and contaminated specimens were not significantly more common in the home group than the clinic group. Interestingly, 9 women in the home group reported that a partner assisted them during the collection and testing process; such unexpected findings are a welcome indication that that women may seek assistance with self-tests if necessary.
Preference for self-collection (67%), home collection (61%), and self-testing (59%) was highly associated with randomization group. The experience of being in the home group and successfully completing the collection alone is the strongest predictor for preferring this method. Participants in the clinic group responded hypothetically to preferences for home collection and, without the firsthand experience, may have felt less confident that they would be able to successfully complete the process. Our finding that self- and home-based collection was preferred generally to provider-based practices is comparable to findings in other studies, although some have documented even stronger preferences for self collection.7,9–11 Because the quality of care at our study clinic, a training site run by the Santa Casa Faculty of Medical Sciences in São Paulo, was exceptionally high, clinic-based services likely had a better reception in our study than they would in less optimal circumstances.
The current system of care in Brazil relies on syndromic management to diagnose and treat STIs.33 Although syndromic management is advantageous in that screening and treatment is provided in a single visit, the syndromic management algorithm for women performs poorly, resulting in gross overtreatment, as is currently the case in Brazil where the national flow chart yielded 49% and 19% specificity for gonorrhea and/or chlamydia and trichomoniasis and/or bacterial vaginosis diagnosis in women, respectively.34 Generally, no system exists to capture and treat asymptomatic STI in Brazil; for women who seek care, indications for STI screening and pelvic examination include report of symptoms indicative of an STI and abnormalities identified during a Pap collection or wet mount. In our study population, of the 101 women who tested positive for an STI by PCR, only 30 of them (30%) potentially would have been screened for STI at the clinic given these indications. Making home-based collection kits available at pharmacies or available free of charge in public services could potentially reach the 70% of women with infections who would be missed through current clinical screening programs. In fact, half of the study participants stated that they would purchase a self-collection and self-testing STI kit at the pharmacy for up to U.S. $4; 35% would pay more.
Home-based STI screening is not meant to supplant clinic screening programs, but instead, offering this alternative strategy may encourage testing and treatment among those least likely to seek medical care and may reduce costs of repeat speculum examinations by using noninvasive collection. Clinic-based programs offer the essential benefit of counseling and partner notification as well as Pap smear screening; however, Pap screening can be limited to every 3 years for most women. With growing advances in the development of rapid point-of-care tests, self-tests for STIs may be a reality in the near future. Test developers aim to make inexpensive and easy-to-use rapid STI diagnostics for use on self-collected samples. Based on our findings, self-collection and rapid tests are a feasible and acceptable option for home-based STI screening in low-income populations in developing country settings and should be introduced in resource-rich and poor countries alike.
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International Journal of Std & AIDSPilot study of the utility and acceptability of tampon sampling for the diagnosis of Neisseria gonorrhoeae and Chlamydia trachomatis infections by duplex realtime polymerase chain reaction in United Kingdom sex workersInternational Journal of Std & AIDS
American Journal of EpidemiologyUsing sexually transmitted infection biomarkers to validate reporting of sexual behavior within a randomized, experimental evaluation of interviewing methodsAmerican Journal of Epidemiology
Future MicrobiologyDiagnostic challenges of sexually transmitted infections in resource-limited settingsFuture Microbiology
Bmc Public HealthBaseline assessment of prevalence and geographical distribution of HPV types in Chile using self-collected vaginal samplesBmc Public Health
Current Opinion in Infectious DiseasesChlamydia trachomatis and ectopic pregnancy: recent epidemiological findingsCurrent Opinion in Infectious Diseases
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