Sage Journals: Discover world-class research

Abstract

Background:

Primary testing for high-risk human papillomavirus (HPV) via self-collection can increase cervical cancer screening rates. In the United States, federally qualified health center (FQHC) patients often have low incomes, lack health insurance, are medically underserved, and are screened less than the national average. Implementation of HPV self-collection can increase cervical cancer screenings among FQHCs.

Objectives:

To assess the potential impact of implementing HPV self-collection with FQHC patients by considering perspectives of frontline clinical and administrative staff and leadership to identify patient-focused implementation considerations.

Design:

This qualitative study utilized focus groups and key informant interviews, and transcripts were analyzed using a coding-based thematic analysis. Emergent themes regarding self-collection implementation perspectives were mapped onto Consolidated Framework for Implementation Research constructs to identify potential facilitators and barriers to implementation for FQHC patient populations.

Methods:

Participants from six FQHCs in North Carolina were identified. Forty-five clinical and administrative staff participated in focus groups. One chief executive officer, senior level administrator, chief medical officer, and clinical data manager from each FQHC (N = 24) were interviewed one-on-one. Coding-based thematic analysis was applied to focus group and interview transcripts to uncover emerging themes.

Results:

Interviewees indicated that HPV self-collection can be advantageous to patients who do not routinely visit the clinic due to socioeconomic and cultural barriers. Programs must consider these barriers and patient literacy to ensure proper self-collection utilization. For example, FQHC patients may benefit from illustrated instructions for proper self-collection procedures.

Conclusion:

Tailoring an HPV self-collection implementation to FQHC patient populations may be an important strategy for increasing screening.

Keywords

cervical cancer federally qualified health centers human papillomavirus self-collection

Introduction

Testing for oncogenic high-risk human papillomavirus (HPV) infection has become fully incorporated into national cervical cancer screening guidelines in the United States.¹ The U.S. Preventive Services Task Force currently recommends primary HPV testing alone or HPV/cytology co-testing every 5 years for women aged 30–65 years, as an alternative to Pap testing alone.¹ For women between 21 and 29 years of age, cytology alone is recommended every 3 years.¹ The American Cancer Society screening guidelines recommend HPV primary screening to begin as early as 25 years of age.²

Incidence and mortality of HPV-driven cervical cancer has decreased, in large part through the development of effective screening and timely treatment of cervical precancerous lesions. Despite the success of this approach, an estimated 60% of cervical cancer cases had not been screened within 3 years of their diagnosis.^3,4 This represents a major healthcare concern, as an estimated 23% of U.S. screen-eligible women are overdue for screening.⁵ Socioeconomic factors, including living below the federal poverty level, being a racial/ethnic minority, having low educational attainment, having no insurance or being underinsured, and residing in rural communities, have been shown to negatively influence screening rates.^6
–10 Thus, alternative screening strategies, such as self-collection of cervico-vaginal samples by patients themselves (HPV self-collection) are needed to increase screening awareness, access, and subsequent utilization.

Patients at high-risk for developing cervical cancer represent a population that should be targeted for alternative screening strategies. One opportunity is to implement innovative screening services in collaboration with federally qualified health centers (FQHCs) whose mandate is to improve the quality and delivery of care to medically underserved populations.¹¹ Although cervical cancer screening services are provided by FQHCs, and quality measures are metricized to determine and monitor the performance of prevention-care delivery, FQHC patients are screened for cervical cancer at a rate of 55% which is substantially lower than the national average of 80%.¹²

There are very few studies evaluating the logistics, economic hardship, or technical instruction required to achieve the benefits from a self-collection HPV diagnostic test introduced into widespread use in FQHCs. Our previous studies have assessed key logistical concerns with implementing HPV self-collection into FQHCs, as well as stressed the importance of self-collection approval by regulatory authorities, which is crucial to the quality and delivery of care at FQHCs. Herein, we present qualitative data that focused on the potential impact of HPV self-collection on patients. Data are presented from focus groups and key informant interviews with FQHC frontline clinical and administrative staff and leadership to understand how an HPV self-collection intervention could impact their FQHC patients. Data are anticipated to inform innovative approaches for the future implementation of an HPV self-collection approach into FQHCs and how to best serve this patient population.

Methods

Study setting and design

Clinic identification

In collaboration with the North Carolina Community Health Center Association, 6 out of 40 eligible FQHCs in North Carolina were purposefully selected and agreed to participate. The six FQHCs were purposefully selected based on size and geographic location to ensure representation of FQHCs of various sizes in both urban and rural catchment areas. Two small FQHCs (consisting of 1 or 2 clinical sites) served urban and rural areas; two medium FQHCs (consisting of 3 to 6 clinical sites) served urban and rural areas; and two large FQHCs (consisting of >6 clinical sites) served rural areas. Rural and urban classifications were designated by zip code. A representative of each FQHC helped recruit participants for focus groups and key informant interviews. FQHCs were excluded if they previously participated or already agreed to participate in future HPV self-collection study with the University of North Carolina (UNC).

Focus groups

Six focus groups were conducted with FQHC providers and staff, including physicians, physician assistants, medical assistants, nurses, nursing assistants, and administrative staff. About 6 to 10 participants from each FQHC participated in each focus group, for a total of 45 study participants. Small FQHCs had 19 participants across 2 focus groups, medium FQHCs had 13 participants across 2 focus groups, and large FQHCs had 13 participants across 2 focus groups. Focus groups used a facilitated process to brainstorm ideas, characterize organizational culture and norms, and uncover factors that influence opinions, behaviors, or motivations among FQHC clinical and administrative staff for the implementation of self-collection for HPV testing among women overdue for cervical cancer screening. Overarching issues that emerged from these discussions were used to develop interview guides to conduct follow-up key informant one-on-one interviews. Each clinic was compensated $500 for their staff’s participation.

Key informant interviews

Twenty-four interview participants were selected from the six FQHCs based on job title and professional role. Roles included: chief executive officer (CEO; n = 6), chief medical officer (CMO; n = 6), senior-level administrator (n = 6), and clinical data manager (n = 6). One participant in each role and from each of the six FQHCs were identified and agreed to participate. Interviews provided detailed information about key clinic personnel and administrative decision-making perceptions regarding implementing an intervention for self-collection for HPV testing within the clinic population served by the clinic, as well as opinions about the benefits of, or concerns about, the use of self-collection for HPV testing. Each participant received $100 via gift card for completing the interview.

Focus group and key informant interview guides

Constructs from the Consolidated Framework for Implementation Research (CFIR) were used to inform the development of focus group and key interview guides.⁴¹ To conceptualize emerging themes, CFIR considered five major domains:

Inner setting: What are potential facilitators and barriers that may affect willingness to implement self-collection for HPV testing?

Individual characteristics: What are the perceived benefits to/drawbacks to adopting self-collection for HPV testing?

Outer setting: What external factors or other considerations discourage efforts to improve cervical cancer screening coverage?

Intervention characteristics: What resources are needed for the implementation of an HPV self-collection intervention?

Implementation process: How would current organizational practices (staffing, scope of practice, workflows, quality assurance, and other protocols) need to be modified?

Data collection procedures

Focus group procedures

Focus groups were conducted from January 2020 to March 2021, until data saturation was reached. The first two focus groups were conducted in-person. Due to the COVID-19 pandemic, the remaining four focus groups were conducted virtually through a cloud-based video conferencing platform that enabled audio recording. Study background material on self-collection for HPV testing was provided (Supplemental Appendix A), and verbal consent to participate was obtained prior to discussions, which lasted approximately 60 minutes. Qualitative research team members facilitated the sessions using a structured focus group guide to elicit insights from FQHC staff regarding the benefits to and barriers of implementing HPV self-collection to the FQHC patient population, and the considerations needed for implementation (Supplemental Appendix B).

Key informant interview procedures

Interviews were conducted from May to September 2021. After verbal consent to participate was obtained, interviews, lasting approximately 30–45 minutes, were completed by telephone, by qualitative research team members, who followed semi-structured, participant-focused interview guides (Supplemental Appendix C). One guide was used for interviews with CEOs, CMOs, and other senior-level administrators. Interviews with leadership further explored perceived benefits and barriers to the patient population, introducing an HPV self-collection outreach, and subsequent diagnostic considerations. The interview guides were pilot tested among two clinical providers at UNC. The use of verbal consent to ensure participation in virtual interviews, including the script and documentation via audio recordings was approved by the Institutional Review Board (IRB) prior to data collection.

Data analysis

All focus group discussions and interviews were audio-recorded. Files were transcribed by a professional transcription service and transcripts were imported into Dedoose version 9.0.17 (Sociocultural Research Consultants, LLC, Los Angeles, United States), a qualitative research software management tool, to facilitate analysis. Codebooks were developed based on the research questions and notes taken during data collection by qualitative research team members. An initial codebook was pilot tested by independently coding a randomly selected focus group transcript. Two additional codebooks (one for CEO/CMO/senior level administrators and one for clinical data managers) were pilot tested by independently coding several interview transcripts. A consensus coding approach was utilized, where codebooks were developed, piloted, and reconciled, leading to refinements to an updated codebook until replication was achieved across coders.^13
–15 Final codebooks were then applied appropriately to the remaining focus group transcripts by two independent coders, and interview transcripts by two pairs of coders, for a total of six coders. Code reports were generated for each code, and narrative summaries were written with descriptions of the identified themes and sub-themes that emerged and included illustrative quotes highlighting each theme.

The UNC IRB reviewed and approved the study protocol (IRB Number: 19-1639). This study qualified as exempt from human studies research given that it included data about patient implications from professionals in their job settings (as opposed to personal health information), no sensitive information was obtained, and it involved only minimal risk to participants. Informed consent was obtained from all participants. The methods reported were validated by the Consolidated Criteria for Reporting Qualitative Research Guidelines.⁴²

Results

Clinical care considerations (Table 1)

Table 1.

HPV self-collection clinical care considerations for federally qualified health center implementation.

Theme	Subtheme	Representative quote
Perceptions of screening by FQHC populations	Require assurance that self-collection is equally effective and not substandard care	“. . . We serve this underserved population. I want to make sure that they would understand that the test we’re giving them is considered an effective screening and that they’re not getting substandard care.” (FG4)
Population is self-pay or on public insurance	Cost of kit	“So, clearly, from a patient perspective, cost. How is it paid for? How much does it cost? If it’s $150.00, it’s never going to happen. If it’s $45.00, might happen. If it’s $50.00 and somebody covers $25.00 and you just have to pay $25.00, it might happen.” (ID 004)
Self-collection methodology	Comfort level and accuracy of self-collection process	“. . . One of the main barriers would be comfort level for the patient, knowing if they’re doing sampling correctly, and whether they would even be willing to insert a cotton swab into the vagina to collect a sample.” (ID 014)
		“My only concern would be making sure that they’re getting a sufficient sample. Making sure that it’s done well enough for the reading to be performed. . .“ (FG4)
		“The Q-tip is fairly long; they can hold the end of it. It’s like they really don’t have to actually touch themselves. Maybe you could sell it that way, saying, ‘You’re really not gonna be touching yourself. You’re gonna be touching the Q-tip. The Q-tip is just gonna touch you up in the side,’ a lot of it plays into the education you give to the patient. . .” (FG3)
Self-collection instructions	Low education attainment	“. . . [the patients] need pictures so they understand. . . And then when you think fifth-grade reading level, you better do fifth-grade reading level and nothing above it.” (FG5)
		“In all of our patients, health literacy can be an issue. So, just making sure that folks knew how to do it correctly. There’ve been folks that have dumped out the liquid that goes to the fit [colorectal] kit and send in samples or sending away too much of a sample.” (ID 009)
	Multicultural/ethnic populations	“. . . We do service some lower-income populations to where the women aren’t educated or they don’t speak English. We do have those populations here in our area. So as long as it was something that was easy enough to explain for them to understand.” (ID 008)
Kit distribution	May be preferrable to provide kit within an in-clinic location	“. . . They would be more comfortable doing it because they’ll feel like they’re in a healthcare setting. So, if they feel like they do anything wrong or anything they can ask questions or just have that extra hand there to help.” (FG4)
		“. . . Any visit where they’re there, I can say, . . . ‘looks like you’re due. . .for your cervical cancer screening, why don’t I send this home with you, and this is what you do. You can mail it back, and we’ll let you know the results.’ . . . give them the opportunity do the Pap smear with us if they prefer that . . . they can have a choice.” (ID 001)
	May be preferrable to provide kit by mail for at home use	“. . . Probably the most effective way would be through the mail because you’re gonna have patients that just aren’t gonna come to the health center. So, I think mail would probably be the best way to do it. . .my recommendation would be [to mail them back] to a lab.” (ID 014)
	Use of an external company	“. . .If it’s an external company where they’re dropping the kits off [at the clinic] . . . it would probably work out better. You would get more tests delivered to the patients . . . and they mail it back to the company.” (FG1)
Kit return	Patient kit return rate may be an issue	“I think the distribution would be fine getting it to the patients. I think it would be the return. . .I’m not for sure the patients would return those. I think it’d be just like the FOBTs. . .I think the return rate would be low.” (ID 006)
	Drop-off or mail-in options needed	“You have some patients that are like I don’t want to put my stuff in the mail, I will just take it up there myself. . .but then some that with transportation issues is like okay, well, I’ll just throw it in the mail. . .I think there needs to be an option of either mailing it back in or actually dropping it off at the health center.” (ID 013)

FQHC: federally qualified health center; FG4: focus group 4; FG3: focus group 3; FG5: focus group 5; FG1: focus group 1; FOBT: fecal occult blood test; HPV: human papillomavirus.

Prior to implementing a self-collection approach within FQHCs, participants wanted to ensure that a self-collection method was effective and provided the same quality as provider-based collection. Participants repeatedly highlighted that costs to patients would pose as a barrier to the FQHC patient population who rely primarily on self-pay or on public insurance. With a self-collection method, there was a concern not only about whether patients would be willing to self-collect, but also if they would be afraid to collect once they saw the device. Furthermore, special collection instructions would need to be developed for their patients, who tend to be lower income, have low educational attainment, and do not speak English. Specifically, simple instructions with pictures, and a bilingual option were discussed. Participants reported that patients would need multiple options for receiving, collecting, and returning the sample. There was no consensus as to which delivery and transport options would be preferred, comparing: receiving the kit at-home to self-collect at-home, receiving the kit in-clinic to self-collect at-home, or self-collecting in-clinic. Participants suggested having an external company provide and process the kits could expand the reach of self-collection to patients. Mixed responses were also received about preferred options for kit return; therefore, both a mail-in to the lab and return to the clinic approach would be helpful to offer.

Benefits (Table 2)

Table 2.

Perceived benefits of HPV self-collection implementation to the patient population as reported by federally qualified health center frontline clinical staff and leadership.

Theme	Subtheme	Representative quote
Socioeconomics	Childcare	“. . . They [patients] literally are the sole provider of childcare to their children, and they’re not gonna come to the clinic because they can’t.” (FG2)
	Transportation	“Those who have an issue with transportation would benefit from this. . . patients oftentimes don’t seek the care they need because they have no way of getting to the healthcare provider.” (FG3)
		“Not having to come back for an appointment definitely is a big one. a lot of our patients have to drive 20 or 30 minutes to get here. And they’ll say they don’t have gas money. They don’t have a ride. They don’t have a car.” (FG1)
		“And think about in those migrant camps the females that can’t come to the doctor. . .” (FG2)
	Cost of healthcare	“With regular HPV testing, we have a lot of patients that that’s their main concern. They really don’t want to complete the testing because it’s so expensive. If this was a cheaper option, I think that could be a selling point.” (FG2)
Patient medical history	Women who feel uncomfortable with or don’t want a pelvic examination	“But for the women who just keep no-showing to these appointments because they are uncomfortable getting undressed doing it.” (FG6)
		“It reduces a barrier for people who don’t want to come in for this test now or those who don’t have the time to come into the clinic.” (ID 017)
		“. . . Patients who have not been sexually active for many years at a time, in terms of comfort level of doing that sensitive exam, that may help their self-collecting. Same thing for anyone who’s been involved in domestic violence, abuse or anything; having that self-collection may make them more at ease and more adherent as far as areas for where they may not be doing that exam.” (ID 022)
	Women who are not compliant with screening	“. . . A patient who’s very noncompliant who hardly ever keeps their appointments, and they just happen to be in there. Even though you don’t want to go outside of what they’re in for, yeah, catch them while you can. That kind of patient, I guess. . .because some women are just not going to get undressed and allow it.” (FG6)
Multicultural/racial populations	Generational perspectives	“Well, a lot of cultures too, they base their decisions off what the doctor says. If the doctor says, ‘This is what we do.’ So, if the doctor says, ‘We need a Pap smear.’ Then they’re gonna do a Pap smear. If the doctor says, ‘We can get a self-collection.’ Then a self-collection is what they would do.” (FG2)
Multicultural/racial populations	Influence of cultural values	“I think there probably is kind of a cultural mindset of women not wanted to be touched in their genital area. I think there’s a problem with comfort with having a provider doing an examination of that kind down there. . . . particularly people in their 40s and 50s, and older I think they’re more uncomfortable with it [genital exam by a provider]. . . . the younger generation in their 20s is probably more comfortable. They’re probably better educated about it, more accepting of it.” (ID 014)

FG2: focus group 2; FG3: focus group 3; FG1: focus group 1; HPV: human papillomavirus; FG6: focus group 6.

Participants envisioned that HPV self-collection would benefit their patients who have difficulties attending their in-clinic appointments. Providers mentioned some common reasons their patients do not attend their in-clinic appointments, such as their inability to find childcare (as they are often the sole childcare providers), not having their own transportation, and/or insufficient gas money. Self-collection may also benefit migrant patients since their transient lifestyle can prohibit regular visits to the clinic. Furthermore, participants believed that patients who are uncomfortable receiving a Pap smear due to discomfort, sexual history or abuse, and obesity, may also benefit from a self-collection approach.

Barriers (Table 3)

A consistent barrier to self-collection implementation according to FQHC clinic staff and leadership was related to the literacy of their patient population, as most patients have limited educational attainment or are non-native English speakers. It was believed that patients would require a significant amount of education to accept the test, collect the sample, and not confuse the HPV test with a Pap smear test. Participants questioned the feasibility of self-collection for their patients, as most have difficulty finding transportation, and would likely struggle to find time for self-collection and to return the self-collection kit on time. Additionally, concerns stemmed from patients not having consistent means of communication for follow-up. Framing the implementation to address cultural influences must be considered, as many patients face body discomfort with a self-collection approach and may feel uncomfortable discussing sexually transmitted infections and sending out their cervico-vaginal samples in the mail. Participants further raised the need to consider the reimbursements and cost of testing, as most FQHC patients do not have insurance or are inadequately insured.

Table 3.

Perceived patient barriers to HPV self-collection implementation as reported by federally qualified health center frontline clinical staff and leadership.

Themes	Subthemes	Representative quote
Health literacy	Low education attainment or non-English speakers	“. . . We do service some lower-income populations to where the women aren’t educated or they don’t speak English, So, as long as it was something that was easy enough to explain for them to understand.” (ID 008)
	Low education attainment or non-English speakers	“It would be like more, or less professional people, or the ones who have at least finished high school. But, we have so many who never got passed 9th, or 10th grade. I’ve had to do education type things that you would not believe. . . . we have a lot of patients who are very, very uneducated in this area.” (FG3)
	Sufficient education required for patient acceptance	“I don’t know whether our patient population, especially our women population, would be able to do that. I mean, even myself as a nurse I’m not for sure I would want to do self-collect for HPV or not. First of all, they’re going to have to get educated about how to do it, and I’m just not for sure they would even want to do it even if I could get the education. I just think that they would rather have a provider to do instead of them do themselves.” (ID 006)
	Sufficient education required for patient acceptance	“I would say probably one of the main barriers would be comfort level for the patient, knowing if they’re doing sampling correctly, and whether they would even be willing to insert a cotton swab or whatever into the vagina to collect a sample.” (ID 014)
	For accurate self-collection	“The initial thought that I had was – while this is good, how can you ensure that they’re gonna collect it appropriately? How are you gonna ensure that they hit the correct spot in other words for testing?. . . because you have to obtain that from a certain area in the female body.” (FG1)
	On Pap smear testing vs HPV stand-alone testing	“. . .A lot of our patients would just make the assumption that this is the equivalent of getting their pap done, and not really understand that it’s just for HPV virus, and not the pap.” (FG3)
Socioeconomic considerations	Turn-around time for collection	“. . . Worry about the collection time. Most of the patients have problems with transportation. How are they gonna know the turnaround time to send this stuff back for accuracy. They got to collect it, and they got to take it to a lab and then send it back to us.” (FG2)
	Contacting patients	“Getting ahold of patients because their phone numbers change like the wind here. . . . the big barrier is getting ahold of patients to get that documented back to see what’s going on. . . even addresses change. . .” (ID 006)
	Reimbursement for self-collection	“Just need to clarify like financial-wise how we were gonna roll with that. . .. The overwhelming majority of our patients are uninsured, so we’re about 70 percent-ish uninsured, which is statewide. most folks, pay our lowest level of sliding scale fees, that doesn’t often totally cover the cost of their labs.” (ID 009)
Multicultural/racial populations	Body discomfort with self-collection	“So, say someone comes in for discharge complaints. If there’s no other symptoms of PID, we can send them to the bathroom to record a swab of the discharge. And some people just are not quite comfortable. They would rather us do it just to make sure it’s done right or done correctly I should say. So, just that comfort, being able to do it yourself, and ensure an accurate test.” (FG5)
	Mistrust of healthcare system	“I don’t see success in mailing something foreign in that there may be some mistrust around where is this information going, and who’s going to house it, and you’ll have my DNA” (ID 019)
	Reluctance to discuss HPV	“We find that with some populations, it’s a cultural thing that you don’t talk about with HPV. And so, again that education is important. They don’t understand what it is and the importance of just screening to prevent it.” (ID 024)

FG3: focus group 3; HPV: human papillomavirus; FG1: focus group 1; FG2: focus group 2; PID: pelvic inflammatory disease; FG5: focus group 5; DNA: deoxyribonucleic acid.

Discussion

This study is among the first to consider what the impact of implementing self-collection for HPV testing on the FQHC patient population would be. As a first step, we explored the perspectives of frontline leadership and staff at FQHCs. Given that many patients of FQHCs have low health literacy or are non-English speakers, these frontline FQHC staff highlighted the importance of providing clear and easily understandable instructions (inclusive of illustrations) to ensure proper procedures for self-collection and the timely return of samples for laboratory processing. HPV self-collection was noted as likely being particularly beneficial to patients who do not routinely visit the clinic, due to transportation, childcare, and other cost-related barriers; discomfort with provider-based collection; and the influence of cultural norms. As such, clinical care considerations should be made during implementation planning to ensure that implementation strategies mitigate these barriers, while supporting proper self-collection, timely specimen return, and cost-related obstacles that might be faced by FQHC patients.

A lack of understanding of cervical cancer screening methods has long been a concern, especially among women screened at FQHCs. In 2013, a study at FQHCs found that 85% of women surveyed did not entirely understand the purpose of a Pap smear.¹⁶ Another recent study echoed the lack of understanding around Pap testing, and highlighted that racial disparities exist in basic knowledge about cervical cancer screening processes and guidelines.¹⁷ Additionally, HPV testing utilization was higher among younger women who had a greater understanding of the virus,^18,19 supporting frontline FQHC employees’ assumptions that the use of illustrated instructions may be essential to increase HPV testing and the acceptance and quality of self-collection.²⁰

Our findings support the growing evidence that HPV self-collection can increase access to cervical cancer screenings, especially among patients who are not routinely attending clinic visits. Offering a self-collection approach can reduce the need for a provider to collect patient samples in-clinic, by allowing patients to collect samples themselves either at -home or in-clinic.^21,22 Frontline FQHC staff reported that patients who do not routinely visit the clinic, often do so due to transportation barriers, lack of childcare, discomfort with provider-based collection, and the influence of cultural norms. These findings are consistent with the patient reported barriers identified in our My Body My Test-3 (MBMT-3) trial among under-screened women in North Carolina, which may impact a woman’s ability to complete in-clinic screening.²³ Participants expressed that these barriers also affect patients’ ability to follow-up with recommended after test results are received. A meta-analysis reported similar findings, indicating that follow-up care attendance is limited by the lack of time, transportation, childcare; financial difficulty; education level; and influence of culture.²⁴ A recent study has also found that self-collection can address some of these same patient-level barriers, as patients have cited an advantage to self-collection includes convenience, ease of use, privacy, absence of embarrassment (dignity), and comfort.²⁵ Despite these advantages, disadvantages were also noted including discomfort in the self-collection procedures, uncertainty about self-collecting an adequate sample, and body comfort.²⁵

In addition to these patient-level barriers, participants identified further clinical care considerations needed as implementation strategies were designed. For example, participants expressed concerns regarding the quality of testing with self-collection, questioning whether HPV testing using a self-collection method would have the same accuracy as with a provider-collected sample. Academic-based clinical studies have evaluated the performance of such collection methodology on the specificity and sensitivity of various HPV detection assays and found little discordance between provider- and patient-collected samples for the detection of high-grade cervical precancer/cancer, if highly sensitive assays were used.^26
–29 Study participants further noted that the cost of self-collection kits would be a concern among the FQHC patient population who tend to be self-paying or on public health insurance. Interestingly, a Canadian study among Muslim women found that if costs of HPV self-collection were not covered by a public health program or health insurance, they would not utilize a self-collection approach.³⁰ However, our previous MBMT-3 study found that among 227 low-income women recruited from FQHCs and health departments who returned their completed self-collection kits along with an acceptability questionnaire, 92% were willing to pay for the kits themselves, with 48% were willing to pay $25 or more.²³ Not only did our participants raise concerns about costs associated with the kits, but having multiple routes for self-collection kit distribution and return are needed, in order to mitigate additional barriers that impact patients’ ability to return tests for processing.

Strengths and limitations

Strengths of our study include its focus on urban and rural FQHCs, as well as the diverse patient population served by these organizations. Additionally, to ensure a rich perspective, our study first used focus groups with diverse frontline FQHC staff to garner a broad perspective. Results from these focus groups were then used to develop a more in-depth interview guide for use with CEOs, CMOs, and Senior Level Administrators at FQHCs. Despite such strengths, our study has a few limitations that should be considered when interpreting results. The selection of FQHCs in North Carolina may have affected the generalizability of our results to populations served by other FQHCs, including in various states across America. In addition, because the study was conducted during the COVID-19 pandemic, we used virtual meetings with FQHC staff instead of in-person meetings. Doing so may have resulted in less personal connections being made and therefore fewer or different topics being discussed during the focus group and interviews. However, recent studies have found similarities in thematic findings among online modalities and in-person data collection.³¹ Monetary compensation for the participants may also have an unidentified effect on their motivation and attitudes during the study. Our study is limited by the absence of a formal reflexivity process. Interviewer characteristics and potential biases were not systematically documented, which may have influenced the ways interviews were conducted, and how data were interpreted. Including structured reflexivity in future research would strengthen the credibility of findings. Although our study is unique in that perspectives from frontline clinical staff and leadership is provided regarding the future implementation of self-collection for HPV testing and the implications for patient populations, we did not directly interview women. This study compliments our previous research to identify barriers and acceptability of HPV self-collection among underscreened women, showing widespread acceptance among target populations for this novel screening technology.^20,32
–37 Although the concerns raised by providers may be familiar to healthcare professionals, there is limited formal documentation of these perspectives in the scientific literature. This study contributes to the evidence base needed for the development of implementation strategies, policy decisions, and clinical guidelines that are grounded in the real-world experiences of healthcare providers. By systematically capturing and analyzing these views, the study helps bridge the gap between known barriers and actionable, evidence-based approaches to scaling up self-collection for HPV testing.

Policy and research implications

Self-collection for HPV testing is being evaluated as a viable option to increase cervical cancer screening. Cervical cancer screening programs in countries outside the United States are utilizing self-collection to broaden screening access.³⁸ Regulatory authorities in the European Union have approved self-collection to be used for HPV testing.³⁸ On the other hand, HPV self-collection has yet to be approved in the United States by the Food and Drug Administration for clinical practice, although discussions are ongoing. Interest remains high in evaluating self-collection to increase screening rates, particularly among medically underserved and underscreened women in the United States. Recently developed self-collection modalities could enable and encourage insufficiently screened women to participate in cervical cancer screening.³⁹ It is important to note that other interventions thought to enhance access to care for marginalized people have instead presented with almost immediate disparities, perpetuating health inequities among those with low socioeconomic status (SES), while those of high SES reap the benefits.⁴⁰ Thus, it is critical to plan for ensuring equity in screening access prior to launching of new interventions for disease control.⁴⁰

Future studies should evaluate the effectiveness and equity of an HPV self-collection process on cervical cancer screening rates, as well as any unintended consequences associated with self-collection. They both should be assessed among women who have and have not been vigilant with their previous screening, with particular attention to women from marginalized communities. Importantly, we encourage that likely inequities from the introduction of self-collection for HPV testing be considered now, prior to widespread use so that testing could be used to reduce and not exacerbate disparities in cervical cancer screening.

Conclusion

As self-collection for HPV testing is widely considered for implementation, both nationally and globally, understanding the barriers that people from marginalized populations, such as those commonly served by FQHCs, face that hinder them from completing cervical cancer screening, is essential. Our findings provide critical considerations to ensure that HPV self-collection implementation can more directly accommodate the needs of diverse FQHC patient populations, and alleviate the barriers they face, so that this valuable resource can fully be utilized and ultimately, reduce deaths from this preventable cancer among vulnerable under-screened populations.

Supplemental Material

sj-doc-3-whe-10.1177_17455057251362581 – Supplemental material for Implementing self-collection for primary human papillomavirus testing: Perspectives on implications for federally qualified health center patient populations

Supplemental material, sj-doc-3-whe-10.1177_17455057251362581 for Implementing self-collection for primary human papillomavirus testing: Perspectives on implications for federally qualified health center patient populations by Amanda Le, Liisa S. Smith, Stephanie B. Wheeler, Kara Giannone, MaryShell Zaffino, Jennifer Elston Lafata and Jennifer S. Smith in Women's Health

Supplemental Material

sj-docx-1-whe-10.1177_17455057251362581 – Supplemental material for Implementing self-collection for primary human papillomavirus testing: Perspectives on implications for federally qualified health center patient populations

Supplemental material, sj-docx-1-whe-10.1177_17455057251362581 for Implementing self-collection for primary human papillomavirus testing: Perspectives on implications for federally qualified health center patient populations by Amanda Le, Liisa S. Smith, Stephanie B. Wheeler, Kara Giannone, MaryShell Zaffino, Jennifer Elston Lafata and Jennifer S. Smith in Women's Health

Supplemental Material

sj-docx-2-whe-10.1177_17455057251362581 – Supplemental material for Implementing self-collection for primary human papillomavirus testing: Perspectives on implications for federally qualified health center patient populations

Supplemental material, sj-docx-2-whe-10.1177_17455057251362581 for Implementing self-collection for primary human papillomavirus testing: Perspectives on implications for federally qualified health center patient populations by Amanda Le, Liisa S. Smith, Stephanie B. Wheeler, Kara Giannone, MaryShell Zaffino, Jennifer Elston Lafata and Jennifer S. Smith in Women's Health

Supplemental Material

sj-pdf-4-whe-10.1177_17455057251362581 – Supplemental material for Implementing self-collection for primary human papillomavirus testing: Perspectives on implications for federally qualified health center patient populations

Supplemental material, sj-pdf-4-whe-10.1177_17455057251362581 for Implementing self-collection for primary human papillomavirus testing: Perspectives on implications for federally qualified health center patient populations by Amanda Le, Liisa S. Smith, Stephanie B. Wheeler, Kara Giannone, MaryShell Zaffino, Jennifer Elston Lafata and Jennifer S. Smith in Women's Health

Footnotes

Acknowledgements

The authors sincerely thank the interviewers and clinics for their contributions to and participation in this study.

ORCID iDs

Amanda Le

Jennifer S. Smith

Ethical considerations

The University of North Carolina Institutional Review Board reviewed and approved the study protocol (IRB Number: 19-1639).

Consent to participate

This study qualified as exempt from human studies research given that it included data about patient implications from professionals in their job settings (as opposed to personal health information), no sensitive information was obtained, and it involved only minimal risk to participants. Informed consent was obtained from all participants.

Consent for publication

The consent for publication was obtained from all participants.

Author contributions

Amanda Le: Writing – original draft; Writing – review & editing; Formal analysis.

Liisa S. Smith: Writing – original draft; Writing – review & editing.

Stephanie B. Wheeler: Writing – review & editing.

Kara Giannone: Formal analysis; Data curation; Investigation; Writing – review & editing; Validation.

MaryShell Zaffino: Writing – review & editing; Data curation.

Jennifer Elston Lafata: Writing – review & editing.

Jennifer S. Smith: Conceptualization; Funding acquisition; Investigation; Methodology; Writing – review & editing; Project administration; Data curation; Supervision; Resources; Visualization.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was funded by the National Institute of Health (NIH) National Cancer Institute (NCI) UH2/3 grant (CA202663). This work was also supported in part by the University of North Carolina at Chapel Hill’s Connected Health Applications & Interventions Core (CHAI Core) through a grant from the NIH (DK056350) to the University of North Carolina Nutrition Obesity Research Center and/or from the NCI (P30-CA16086) to the Lineberger Comprehensive Cancer Center.

Declaration of conflicting interests

The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: Jennifer S. Smith has received research grants and consultancies from Hologic and Becton Dickenson over the past 5 years. Stephanie B. Wheeler receives unrelated grant funding from the Pfizer Foundation and AstraZeneca. Jennifer E. Lafata receives unrelated grant funding from Genentech. The remaining authors have no conflicts of interest to declare.

Data availability statement

The data used to support the findings of this work are available on request from the authors.

Supplemental material

Supplemental material for this article is available online.

References

U.S. Preventive Services Task Force, Curry

Krist

, et al. Screening for cervical cancer: US Preventive Services Task Force Recommendation Statement. JAMA 2018; 320(7): 674–686.

Fontham

ETH

Wolf

AMD

Church

, et al. Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society. CA Cancer J Clin 2020; 70(5): 321–346.

Benard

Jackson

Greek

, et al. A population study of screening history and diagnostic outcomes of women with invasive cervical cancer. Cancer Med 2021; 10(12): 4127–4137.

Landy

Mathews

Robertson

, et al. A state-wide population-based evaluation of cervical cancers arising during opportunistic screening in the United States. Gynecol Oncol 2020; 159(2): 344–353.

Suk

Hong

Rajan

, et al. Assessment of US Preventive Services Task Force Guideline–Concordant Cervical Cancer Screening Rates and reasons for underscreening by age, race and ethnicity, sexual orientation, rurality, and insurance, 2005 to 2019. JAMA Netw Open 2022; 5(1): e2143582.

Gamble

Mawokomatanda

, et al. Surveillance for certain health behaviors and conditions among states and selected local areas—Behavioral risk factor surveillance system, United States, 2013 and 2014. MMWR Surveill Summ 2017; 66(16): 1–144.

Katz

Zimmermann

Moore

, et al. Perspectives from health-care providers and women about completing human papillomavirus (HPV) self-testing at home. Women Health 2017; 57(10): 1161–1177.

McDaniel

Hallam

Cadwallader

, et al. Persistent racial disparities in cervical cancer screening with Pap test. Prev Med Rep 2021; 24: 101652.

Datta

Pana

Mayrand

, et al. Racial/ethnic inequalities in cervical cancer screening in the United States: an outcome reclassification to better inform interventions and benchmarks. Prev Med 2022; 159: 107055.

10.

Tsui

Llanos

Doose

, et al. Determinants of abnormal cervical cancer screening follow-up and invasive cervical cancer among uninsured and underinsured women in New Jersey. J Health Care Poor Underserved 2019; 30(2): 680–701.

11.

Huguet

Hodes

Holderness

, et al. Community health centers’ performance in cancer screening and prevention. Am J Prev Med 2022; 62(2): e97–e106.

12.

Jaqua

Nguyen

Morton

, et al. Improving cervical cancer screening rates at an urban federally qualified health center family medicine residency clinic. Perm J 2022; 26(2): 21–27.

13.

Creswell

. Qualitative inquiry and research design: choosing among five approaches. Sage Publications, 2007.

14.

Patton

MQ.

Qualitative research and evaluation methods. Sage Publications, 2002.

15.

Bradley

Curry

Devers

KJ.

Qualitative data analysis for health services research: developing taxonomy, themes, and theory. Health Serv Res 2007; 42(4): 1758–1772.

16.

Hawkins

Benard

Greek

, et al. Patient knowledge and beliefs as barriers to extending cervical cancer screening intervals in Federally Qualified Health Centers. Prev Med 2013; 57(5): 641–645.

17.

Kasting

Wilson

Zollinger

, et al. Differences in cervical cancer screening knowledge, practices, and beliefs: an examination of survey responses. Prev Med Rep 2016; 5: 169–174.

18.

Johnson

Head

Scott

, et al. Persistent disparities in cervical cancer screening uptake: knowledge and sociodemographic determinants of papanicolaou and human papillomavirus testing among women in the United States. Public Health Rep 2020; 135(4), 483–491.

19.

Sonawane

Suk

Chiao

, et al. Evaluation of cervical cancer screening uptake and adherence among women without human papillomavirus vaccination in the US. JAMA Netw Open 2021; 4(10): e2131129.

20.

Kilfoyle

Des Marais

Ngo

, et al. Preference for human papillomavirus self-collection and Papanicolaou: survey of underscreened women in North Carolina. J Low Genit Tract Dis 2018; 22(4): 302–310.

21.

Castanon

Rebolj

Burger

, et al. Cervical screening during the COVID-19 pandemic: optimising recovery strategies. Lancet Public Health 2021; 6(7): e522–e527.

22.

Lofters

Moineddin

Hwang

, et al. Predictors of low cervical cancer screening among immigrant women in Ontario, Canada. BMC Womens Health 2011; 11: 20.

23.

Smith

Des Marais

Deal

, et al. Mailed human papillomavirus self-collection with Papanicolaou test referral for infrequently screened women in the United States. Sex Transm Dis 2018; 45(1): 42–48.

24.

Limmer

LoBiondo-Wood

Dains

Predictors of cervical cancer screening adherence in the United States: a systematic review. J Adv Pract Oncol 2014; 5(1): 31–41.

25.

Daponte

Valasoulis

Michail

, et al. HPV-based self-sampling in cervical cancer screening: an updated review of the current evidence in the literature. Cancers (Basel) 2023; 15(6): 1669.

26.

Des Marais

Zhao

Hobbs

, et al. Home self-collection by mail to test for human papillomavirus and sexually transmitted infections. Obstet Gynecol 2018; 132(6): 1412–1420.

27.

Arbyn

Smith

Temin

, et al. Detecting cervical precancer and reaching underscreened women by using HPV testing on self samples: updated meta-analyses. BMJ 2018; 363: k4823.

28.

Zhao

Lewkowitz

Chen

, et al. Pooled analysis of a self-sampling HPV DNA Test as a cervical cancer primary screening method. J Natl Cancer Inst 2012; 104(3): 178–188.

29.

Islam

Mutua

Kabare

, et al. High-risk human papillomavirus messenger RNA testing in wet and dry self-collected specimens for high-grade cervical lesion detection in Mombasa, Kenya. Sex Transm Dis 2020; 47(7): 464–472.

30.

Camara

Zhang

Lafferty

, et al. Self-collection for HPV-based cervical screening: a qualitative evidence meta-synthesis. BMC Public Health 2021; 21(1): 1503.

31.

Guest

Namey

O’Regan

, et al. Comparing interview and focus group data collected in person and online. Patient-Centered Outcomes Research Institute (PCORI), 2020.

32.

Racey

Gesink

Burchell

, et al. Randomized intervention of self-collected sampling for human papillomavirus testing in under-screened rural women: uptake of screening and acceptability. J Womens Health (Larchmt) 2016; 25(5): 489–497.

33.

Anderson

Breithaupt

Des Marais

, et al. Acceptability and ease of use of mailed HPV self-collection among infrequently screened women in North Carolina. Sex Transm Infect 2018; 94(2): 131–137.

34.

Bansil

Wittet

Lim

, et al. Acceptability of self-collection sampling for HPV-DNA testing in low-resource settings: a mixed methods approach. BMC Public Health 2014; 14(1): 596.

35.

Serrano

Ibáñez

Robles

, et al. Worldwide use of HPV self-sampling for cervical cancer screening. Prev Med 2022; 154: 106900.

36.

Zeno

Brewer

Spees

, et al. Racial and ethnic differences in cervical cancer screening barriers and intentions: the My Body My Test-3 HPV self-collection trial among under-screened, low-income women. PLoS One 2022; 17(10): e0274974.

37.

Des Marais

Brewer

Knight

, et al. Patient perspectives on cervical cancer screening interventions among underscreened women. PLoS One 2022; 17(12): e0277791.

38.

Elfström

Gray

Dillner

Cervical cancer screening improvements with self-sampling during the COVID-19 pandemic. Elife 2023; 12: e80905.

39.

Arbyn

Verdoodt

Snijders

, et al. Accuracy of human papillomavirus testing on self-collected versus clinician-collected samples: a meta-analysis. Lancet Oncol 2014; 15(2): 172–183.

40.

Phelan

Link

BG.

Controlling disease and creating disparities: a fundamental cause perspective. J Gerontol B Psychol Sci Soc Sci 2005; 60 Spec No 2: 27–33.

41.

Damschroder

Aron

Keith

, et al. Fostering implementation of health services research findings into practice: a consolidated framework for advancing implementation science. Implementation Sci 2009; 4: 50.

42.

Tong

Sainsbury

Craig

Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups. Int J Qual Health Care 2007; 19(6): 349–357.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.05 MB

0.03 MB

0.36 MB