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Behaviour
Original article
Acceptability and ease of use of mailed HPV self-collection among infrequently screened women in North Carolina
  1. Chelsea Anderson1,
  2. Lindsay Breithaupt1,
  3. Andrea Des Marais1,
  4. Charlotte Rastas2,
  5. Alice Richman3,
  6. Lynn Barclay4,
  7. Noel T Brewer1,5,
  8. Jennifer S Smith1,5
  1. 1 Gillings School of Global Public Health, University of North Carolina, Chapel Hill, North Carolina, USA
  2. 2 School of Medicine, University of North Carolina, Chapel Hill, North Carolina, USA
  3. 3 College of Health and Human Performance, East Carolina University, Greenville, North Carolina, USA
  4. 4 American Sexual Health Association, Chapel Hill, North Carolina, USA
  5. 5 University of North Carolina Lineberger Comprehensive Cancer Center, Chapel Hill, North Carolina, USA
  1. Correspondence to Dr Jennifer S Smith, Department of Epidemiology, 2103 McGavran-Greenberg, Department of Epidemiology, UNC Gillings School of Global Public Health, Campus Box 7435, Chapel Hill, NC 27599, USA; jennifers{at}unc.edu

Abstract

Objectives Self-collection of cervico-vaginal samples for human papillomavirus (HPV) testing has the potential to make cervical cancer screening more accessible to underscreened women. We evaluated the acceptability and ease of use of home-based HPV self-collection within a diverse population of low-income, infrequently screened women.

Methods Participants were low-income women from North Carolina who had not received Pap testing in 4 or more years. Eligible women received a self-collection kit containing instructions and a brush for home-based sample collection. A total of 227 women returned a self-collected sample by mail and completed a questionnaire to assess their experiences with HPV self-collection. We described acceptability measures and used logistic regression to identify predictors of overall positive thoughts about the self-collection experience.

Results Nearly all women were willing to perform HPV self-collection again (98%) and were comfortable receiving the self-collection kit in the mail (99%). Overall, 81% of participants reported positive thoughts about home-based self-collection. Women with at least some college education and those who were divorced, separated or widowed were more likely to report overall positive thoughts. Aspects of self-collection that participants most commonly reported liking included convenience (53%), ease of use (32%) and privacy (23%). The most frequently reported difficulties included uncertainty that the self-collection was done correctly (16%) and difficulty inserting the self-collection brush (16%).

Conclusions Home-based self-collection for HPV was a highly acceptable screening method among low-income, underscreened women and holds the promise to increase access to cervical cancer screening in this high-risk population.

  • cervical neoplasia
  • HPV
  • screening
  • Uterine cervical neoplasms
  • early detection of cancer
  • papillomavirus infections
  • United States
  • female
  • humans

https://doi.org/10.1136/sextrans-2017-053235

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    Introduction

    In the USA, cervical cancer incidence and mortality have decreased in recent decades, largely due to widespread screening with cytology (Pap testing).1 However, in 2017, an estimated 12 820 US women will be diagnosed with invasive cervical cancer,1 with over half of new cases among women who have been screened infrequently or not at all.2 The primary cause of invasive cervical cancer and precancerous cervical lesions is persistent infection with high-risk types of human papillomavirus (HPV). Current cervical cancer screening recommendations from the US Preventive Services Task Force (USPSTF) for women aged 30 and older include Pap testing alone every 3 years, or HPV testing with Pap testing (cotesting) every 5 years.3 Recently, the US Food and Drug Administration (FDA) approved HPV testing as a stand-alone method of primary screening for cervical cancer,4 although HPV self-collection is not yet FDA-approved for clinical use. Self-collection of cervicovaginal samples at home with return by mail for HPV testing is a promising approach that may alleviate barriers to clinic-based cervical cancer screening, such as transportation limitations or discomfort with pelvic examinations.5–7

    In European studies, mailed delivery of self-collection kits for HPV testing has increased cervical cancer screening of underscreened and never-screened women compared with mailed written reminders to attend in-clinic screening.8–14 Systematic reviews have found that HPV testing of self-collected samples has a sensitivity for detection of high-grade lesions (cervical intraepithelial neoplasia 2 or more severe (CIN2+)) comparable to HPV testing of physician-collected samples.15 The self-collection method may complement current screening protocols by reaching women who have difficulty accessing or are resistant to clinic-based screening, making it especially relevant for underscreened women (i.e., those who have not consistently completed screening at recommended intervals).3 If implemented as a primary screening method, HPV self-collection conducted by mail could reduce the screening burden by requiring that only self-collection HPV-positive women attend follow-up in-clinic screening.

    Self-collection has been found to be highly acceptable in a wide range of demographic groups and geographical locations worldwide.16 Several US-based studies have found high acceptability among low-income populations when self-collection kits and results are delivered face-to-face in community settings.17–29 However, acceptability of mail-based self-collection in US women who are both low-income and underscreened has not been well characterised. Due to their increased risk of developing invasive cervical cancer, this is a priority population for screening by self-collection.2 30 Mail-based HPV self-collection could be particularly helpful to low-income and rural women who face transportation barriers. To our knowledge, two prior US studies have investigated acceptability among women who received HPV self-collection kits by mail,18 31 although neither focused exclusively on underscreened or low-income women.

    To expand the evidence base regarding acceptability of HPV testing conducted by mailed self-collected specimens, we present here data on the acceptability of home-based self-collection among low-income, underscreened women from 10 counties in North Carolina.

    Methods

    Recruitment and selection of participants

    Between January 2010 and September 2011, we recruited women from Wake, Durham, Harnett, Guilford, Wayne, Cumberland, Robeson, Richmond, Hoke and Scotland counties. Detailed study methods have been presented elsewhere.32 Recruitment involved flyers and posters, referral of callers from the United Way 2-1-1 social assistance hotline and direct outreach in locations likely to be visited by low-income women. Potential participants called the study’s hotline and were screened for study eligibility. Women were eligible if they lived in North Carolina, were aged 30–65, were not pregnant, had not undergone a hysterectomy and were low-income. Low income was defined as having children who qualified for the federal school lunch programme, having Medicaid or Medicare Part B insurance, or being uninsured and living at ≤200% of the federal poverty level. Eligibility criteria also required that women had not had Pap testing in the previous 4 years, including women who had never had a Pap test (n=4). The eligibility criteria for age, income and insurance ensured that women were eligible for free clinic appointments, follow-up screening and treatment through the North Carolina Breast and Cervical Cancer Control Program, Medicaid or their own insurance. Among 429 women who were sent an HPV self-collection kit, 275 (64%) returned a self-collected sample. Of these, 227 women (83% of returners) also completed the acceptability questionnaire and are included in this present analysis. The acceptability questionnaire was completed by only three women who did not return a sample (2%), so it is not possible to reliably make comparisons of self-collection acceptability between kit returners and non-returners.

    Procedures

    Participants received a self-collection ‘kit’ containing a Viba brush (Rovers Medical Devices BV, Oss, The Netherlands) for cervicovaginal sample collection, illustrated instructions and a prepaid return mailer. The kit also contained study consent forms and contact information for clinics in their county that perform free or low-cost Pap testing. We developed and pilot-tested the illustrated instructions for comprehension by low-literacy women. To complete self-collection, women were asked to insert the brush as far as it could comfortably go, rotate it five times and remove it. Participants then removed the brush head from the handle and placed it into a small phial of Scope mouthwash, a validated liquid preservation media for HPV DNA testing.33 The Viba brush is about 8 inches long, with a handle 1/4 inch in diameter and brush head with long, flexible plastic bristles. Self-collected samples were returned by mail using the prepaid return mailer. Women who did not return a self-collected sample were sent a reminder letter at 2 weeks, followed by a phone call at 3 weeks, and a second letter at 1 month.

    Study call centre staff contacted women who returned their self-collected samples and provided them with their HPV results. Staff delivering HPV results were based in a call centre run by the American Sexual Health Association (ASHA), a national organisation that promotes sexual health of individuals, families and communities.34 ASHA staff are well-trained in providing support on the meaning of HPV results. On that call, ASHA staff administered an acceptability questionnaire. Given that in-clinic Pap testing or co-testing is the screening method currently included in the USPSTF guidelines,30 ASHA staff also provided participants with information on clinics in their county offering free or low-cost cervical cancer screening, and encouraged them to obtain in-clinic screening. This further allowed an assessment of in-clinic attendance stratified by home HPV self-collection results (positive, negative). For future programme implementation, women with HPV self-collection negative results would be considered screening complete until the next screening round. After the study staff received notification of Pap testing completion by return of a postcard by the participant, or after 2 months without notification, the staff called the participants to complete a follow-up questionnaire. The participants received $30 for returning the self-collected sample and completing the acceptability questionnaire, $10 for reporting completion of Pap testing and $5 for completing the follow-up questionnaire. Approximately 18 months after self-collection kits were originally mailed, additional attempts were made to contact women who had not returned a sample to obtain basic acceptability and demographic data.

    The University of North Carolina Institutional Review Board (IRB) reviewed and approved the study protocol (IRB No 08–2099). Complete protocol has been described in Smith et al.32

    Questionnaires

    The acceptability questionnaire obtained data on sociodemographic characteristics and medical and reproductive history. Participants’ attitudes towards using self-collection, difficulties with self-collection, and concerns about receiving or returning the self-collected sample by mail were also assessed. The follow-up questionnaire assessed women’s willingness to perform self-collection again. Questionnaire items included previously validated measures of variables such as perceived risk and attitudes, and items developed specifically for the study, which were pilot-tested for comprehension (online supplementary file 1). Study materials and questionnaires used the terms ‘self-test’ and ‘self-testing’ for the self-collection and testing process, as this phrasing was found to be better understood by women in the lay population.

    Supplementary file 1

    Measures

    To assess overall attitude about the self-collection experience, we asked, ‘Overall, are your thoughts about the self-test mostly positive, mostly negative, or neutral?’ We created a binary variable of ‘mostly positive’ versus ‘neutral/mostly negative’ to assess predictors of positive thoughts about home self-collection. We excluded from this analysis 29 women with a ‘refused’, ‘don’t know’ or missing response. The acceptability questionnaire contained open-ended items such as ‘What did you like about the self-test’, and closed-ended items such as ‘Were you comfortable receiving the kit in the mail?’ We categorised open-ended responses inductively based on similar thematic elements. To assess difficulties with the self-collection, we used responses to the open-ended question, ‘What would you say was the most difficult part about doing the self-test?’ For these analyses, we categorised responses of ‘don’t know’ and ‘refused’ with ‘nothing’.

    Statistical analysis

    We conducted descriptive analyses for measures of self-collection acceptability and ease of use. Logistic regression was used to estimate ORs and 95% CIs to identify characteristics associated with mostly positive thoughts. Both age-adjusted and multivariable analyses were conducted. Multivariable models were adjusted for age, as well as education and marital status, which were significantly associated with positive thoughts in the age-adjusted model.

    Analyses were performed using SAS V.9.4 software.

    Results

    The median age of the 227 participating women was 44 years (range 30–64). Most were black (55%), had a high school education or less (62%), were uninsured (68%), were current smokers (51%) and lived in rural areas (79%) (table 1).

    View this table:
    Table 1

    Participant characteristics and predictors of overall positive thoughts about the HPV self-collection among infrequently screened women in North Carolina (n=227)

    Overall, 81% of the participants reported ‘mostly positive’ thoughts about the home self-collection and 17% reported ‘neutral’ thoughts. Women with at least some college education were more likely to report positive thoughts than those with a high school diploma or less (88% vs 76%; OR=2.4; 95% CI 1.0 to 5.5). Those who were divorced, separated or widowed were more likely to report positive thoughts than those who were married or living with a partner (90% vs 71%; OR=3.3; 95% CI 1.1 to 9.6). Positive thoughts about self-collection also appeared more common among women who reported not needing contraception (90%) compared with those currently using permanent contraception (73%), non-permanent contraception (78%) and those with a sexual partner but not currently using contraception (80%), although OR estimates were relatively imprecise.

    The most frequently reported positive attributes of the home self-collection included convenience (53%), ease of use (32%) and privacy (23%) (table 2). Although most participants reported no dislikes (70%), 10% reported that the self-collection was uncomfortable and 14% reported experiencing some difficulty in performing the self-collection. Examples of difficulties included removing the brush head from the handle and spilling the liquid preservation media. When we framed the question to specifically elicit report of difficulties, ‘what would you say was the most difficult part about doing the self-test’, 120 participants named at least one difficulty. The most commonly reported difficulties were being sure they did the self-collection correctly (16%) and inserting the self-collection brush (16%) (figure 1).

    View this table:
    Table 2

    Reported acceptability of HPV self-testing among infrequently screened women in North Carolina, US (n=227)*

    Figure 1
    Figure 1

    Difficulties performing human papillomavirus self-collection reported by 201 North Carolina, US women.

    Most participants were willing to perform HPV self-collection again (98%) and pay for the self-collection kit (91%). Almost all reported that the self-collection instructions were not hard to understand (99%) and were confident that they performed the self-collection correctly (97%). Only three women (1%) reported calling the study hotline to request help with performing the self-collection.

    Nearly all women were comfortable receiving the kit in the mail (99%). As to their preferred method for receiving the self-collection kit, 51% preferred the mail to a clinic or pharmacy, and 45% reported no preference. Most expressed that it would be more convenient (69%) and more private (82%) to perform the self-collection at home, rather than at a medical clinic. A small proportion reported discomfort with sending the sample back in the mail (18%) or expressed some degree of concern that their sample would ‘get into the wrong hands' (be seen or received by the wrong person) (18%).

    Few women provided advice for improving the self-collection instructions, although having a video was the most common suggestion (4%). The most frequent suggestion for improving the self-collection brush included making it softer or using a swab instead of a brush (17%).

    Discussion

    This study is among the first to evaluate the acceptability and ease of use of mailed HPV self-collection specifically among low-income US women overdue for cervical cancer screening. It demonstrates that mailed HPV self-collection is highly acceptable in this high-priority group. Nearly all participants who completed self-collection were willing to perform the self-collection again (98%) and most said that self-collection was more private (82%) and convenient (69%) when used at home than in a medical clinic. Almost all were comfortable receiving the self-collection kit in the mail. However, some participants reported some difficulty, such as being sure the self-collection was done correctly or difficulty inserting the self-collection brush.

    Strengths of our study include the focus on low-income, underscreened women with eligibility criteria that allowed for diversity with respect to demographic characteristics and geographical location within North Carolina. Additionally, our approach involved the use of mail for the distribution and return of kits, which has a good potential for scalability. Participants completed self-collection according to illustrated instructions that almost all reported were easy to understand, which is key for a model in which women complete the self-collection at home.

    Our study also has limitations. We recruited a convenience sample of women such that participants who chose to enrol may have had preconceived positive attitudes towards screening and health-conscious behaviours. However, all women in this study were overdue for Pap testing, and therefore a primary target population for at-home HPV self-collection. Other limitations are the moderate return rate of the self-collected sample and relatively low completion of the acceptability questionnaire among those who did not return a self-collected sample.32 OR estimates for overall positive thoughts about the HPV self-collection should be interpreted with caution given relatively wide CIs due to relatively small sample sizes, although they can be used to begin to understand differences in groups. Overall, our findings regarding difficulties and dislikes among women who did return a self-collected sample may inform future efforts to improve rates of participation and sample return.

    Our findings of high acceptability are consistent with those described in a recent systematic review of the acceptability of HPV self-collection in 37 studies from 24 countries.16 They are also in accordance with other studies using HPV self-collection specifically among underscreened women in the USA, most of which have provided kits personally in a community setting and have targeted specific ethnic groups.17 21 In a study of Mexican immigrant women in Texas who had not received a Pap test in the preceding 3 years, nearly all participants (99%) reported willingness to perform HPV self-collection on a regular basis for cervical cancer screening.21 Moreover, the majority indicated that self-collection was more convenient and less stressful than in-clinic Pap testing. Another study among underscreened Haitian and Latina women in Miami reported that 97% found the self-test to be easy to use and would use it again.17 A unique characteristic of our study is that it focused on underscreened women without narrowing to a particular demographic group. In our sample, positive thoughts about self-collection were common overall and were largely similar across demographic and other characteristics. However, our results suggested somewhat higher acceptability among women with more education and those who were separated, widowed or divorced.

    While overall acceptability was high in our sample, some participants did report difficulty with the self-collection process when prompted. The most commonly reported difficulties on the open-ended questions were uncertainty that the self-collection was done correctly and problems inserting the self-collection brush. Other acceptability studies have similarly reported participant uncertainty about performing self-collection correctly.31 35 For example, a prior study using home-based HPV self-collection reported that 57% of participants were not sure that they performed the self-collection correctly.31 However, in our study, responses to closed-ended questions provided some reassurance about women’s confidence in performing the self-collection. Overall, 97% of women in our sample strongly or somewhat agreed with the statement, ‘I am confident that I used the self-test correctly’. Nevertheless, future self-collection screening programmes could benefit from exploring ways to assure women they had completed the self-collection correctly.

    It is notable that nearly all women in the current study were comfortable with receiving the self-collection kit in the mail (99%) and only 4% indicated a preference for receiving the kit in a health clinic or a pharmacy rather than in the mail. These findings suggest that mail may be an acceptable method of reaching infrequently screened women. To our knowledge, only two prior US studies have used mail delivery of self-collection kits, with similarly promising findings regarding overall acceptability of this approach. In a study of Minnesota women aged 21–30 who were recruited via the internet, most participants who returned a self-collected sample by mail found the self-collection process to be easy (87%) and private (86%).31 A study among American Indian women (aged 21-65 years), in which participants had the option to receive and return an HPV self-collection kit by mail, reported that 96% found the self-collection kit easy to use and 62% preferred self-collection to Pap testing performed by a doctor or nurse.18 However, neither of these studies specifically targeted low-income, underscreened women, and neither queried participants’ comfort with the use of mail for receipt and return of the self-collection kit. In our study, roughly 20% of participants expressed discomfort with returning their sample by mail, with a similar proportion expressing concern that their sample could be seen or received by the wrong person. It is possible that incorporating simple measures, such as using certified mail for sample return or allowing self-sample return directly to a clinic or pharmacy, could alleviate these fears, thereby improving screening rates in programmes that use mailed HPV self-collection kits.

    Conclusions

    Overall, our results support the conclusion that mailed self-collection for HPV testing may be acceptable among low-income, underscreened women in the USA. Most women in our study were comfortable receiving their self-collection kit and returning their sample by mail, supporting the use of mailed HPV self-collection to increase access to cervical cancer screening for this high-risk population. Future research could expand on our findings by conducting interviews with women who did not return a sample to identify strategies for increasing self-collection completion rates.

    Key messages

    • Home-based self-collection of cervico-vaginal samples for HPV testing is a promising approach that may alleviate common barriers to clinic-based cervical cancer screening.

    • Most low-income, underscreened women reported an overall positive experience with home-based HPV self-collection.

    • Nearly all participants were willing to perform self-collection again, and most reported that self-collection was more private and convenient at home than in a clinic.

    • HPV self-collection is a highly acceptable screening method among low-income, underscreened women, and may increase access to cervical cancer screening in this high-risk population.

    Acknowledgments

    The authors sincerely than Allen Rinas for his contributions to study design; Meredith Kamradt, Rachel Larsen, Kristen Ricchetti, Kelly Murphy, Stephanie Zentz, and Sara B. Smith for their work on study logistics, database, and recruitment; and Florence Paillard for her assistance editing the manuscript. We also thank Meindert Zwartz a tRovers Medical Devices for contributing the Viba self-collection brushes, and Belinda Yen-Lieberman andJerome Belison at The Cleveland Clinic for conducting the HPV testing. QIAGEN donated kits for Hybrid Capture2 HPV testing. This research was supported by Kate B. Reynolds Charitable Trust. Additional support for staff time came from the NCCU-LCCC Partnership in Cancer Research (5 U54 CA156733), and NIH NCIR01 CA183891.

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    Footnotes

    • Handling editor Jackie A Cassell

    • Competing interests JSS has received research supplies, grants and consultancies from Hologic, Becton Dickinson, Rovers Medical Devices, and Trovagene over the past 5 years.

    • Ethics approval University of North Carolina Institutional Review Board (IRB no. 08-2099).

    • Provenance and peer review Not commissioned; externally peer reviewed.