Abstract
Purpose:
Colonoscopy can prevent morbidity and mortality from colorectal cancer (CRC), and is the most commonly used screening method in the US. Barriers to colonoscopy at multiple levels can contribute to disparities. Yet, in rural settings, little is known about who delivers colonoscopy and facilitators and barriers to colonoscopy access through screening completion.
Methods:
We conducted a qualitative study with providers in rural Oregon who worked in endoscopy centers or primary care clinics. Semi-structured interviews, conducted in July and August, 2021, focused on clinician experiences providing colonoscopy to rural Medicaid patients, including workflows, barriers, and access. We used thematic analysis, through immersion crystallization, to analyze interview transcripts and develop emergent themes.
Findings:
We interviewed 19 providers. We found two categories of colonoscopy providers: primary care providers (PCPs) doing colonoscopy on their own patients (n=9, 47%) and general surgeons providing colonoscopy to patients referred to their services (n=10, 53%). Providers described barriers to colonoscopy at the provider, community, and patient levels, and suggested patient supports could help overcome them. Providers found current colonoscopy capacity sufficient, but noted PCPs trained to perform colonoscopy would be key to continued accessibility. Finally, providers shared concerns about the shrinking number of PCP endoscopists, especially with anticipated increased screening demand related to the CRC screening guideline shift.
Conclusions:
These themes reflect opportunities to address multilevel barriers to improve access, colonoscopy capacity, and patient education approaches. Our results highlight that PCPs are an essential part of the workforce that provides colonoscopy in rural areas.
Keywords: Colorectal cancer screening, rural health, endoscopy, colonoscopy
INTRODUCTION
Screening for colorectal cancer (CRC) is an effective way to prevent morbidity and mortality,1–3 and colonoscopy is the most commonly used screening method in the US.4 Unfortunately, rates of CRC screening remain below national targets.5–7 Moreover, inequities in CRC screening have been observed for rural and low-income populations.7–11
Barriers to CRC screening for rural residents can be related to a wide array of patient and provider characteristics and challenges,12–14 and these multi-faceted barriers become even more pronounced for residents covered by Medicaid insurance.11,15,16 While expanded Medicaid coverage through the Affordable Care Act has been associated with increased rates of CRC screening, this improvement has limiting factors, such as continued lower rates of access to primary and specialist providers for Medicaid compared to other insurance types.17–20 Since insurance expansion alone is not sufficient to increase screening rates to meet national targets,21,22 examining multilevel barriers to screening, including access, in rural areas more broadly can help inform efforts to increase screening rates and decrease inequities.12,16,23–25
The provision of colonoscopy in rural areas is likely to differ from that in urban settings, because of variation in who provides colonoscopy, geographic proximity to medical facilities, and patterns of referral to screening and treatment.12,13,26,27 Notably, colonoscopy is effective as a primary screening method, but also is needed as a follow-up procedure after abnormal results from other types of screening, such as fecal immunochemical tests (FIT) or FIT-DNA tests.28–30 Studies have pointed to lower ratios of gastroenterologists (GIs), general surgeons, and specialty surgical centers to population numbers in rural areas than in urban areas.12,13,31 Few family physicians or primary care providers (PCPs) provide colonoscopy to their patients (about 3% across the US), but this number is higher in rural areas.32 General surgeons also fill this gap in providing colonoscopies in rural areas due to low numbers of GIs located in rural areas.33
A number of studies have indicated that PCPs and general surgeons, including rural physicians, perform colonoscopies that meet quality standards.34–38 More research is needed about this workforce given their importance in rural areas where colonoscopy services are more limited than urban areas.26,32 Some scholars anticipate that the recent shift in CRC screening guidelines from initiation at age 50 to 45 may strain endoscopic resources.39,40 In addition to understanding who is delivering colonoscopy, we know little about workflow processes after a patient is identified through to colonoscopy completion in rural settings. Understanding these operational details and how they might vary could prove crucial to improving CRC screening rates and ensuring colonoscopy resources are not shifted away from higher risk or higher need populations, which might contribute to worse access for vulnerable populations and even greater disparities.39–45
Therefore, we conducted this qualitative research study with rural providers in primary care and endoscopy centers to examine the breadth of providers performing colonoscopy and to explore their views on access and challenges related to colonoscopy in rural settings. Because successful completion of many cancer screenings (e.g., CRC, breast, lung) are delivered across various clinical environments and professional roles, our focus on colonoscopy may provide an important leverage point for future multicomponent and multilevel interventions to improve rural cancer screening rates.
METHODS
This qualitative study was conducted in alignment with a pragmatic trial, SMARTER CRC (Screening More Patients for CRC through Adapting and Refining Targeted Evidence-based Interventions in Rural Settings),46 and pilot funding from the BRIDGE-C2 Center (Building Research in Implementation and Dissemination to close Gaps and achieve Equity in Cancer Control). 47 SMARTER CRC is testing the implementation, effectiveness, and maintenance of a mailed FIT and patient navigation program to improve rates of CRC screening in Oregon clinics serving rural Medicaid enrollees.46 The BRIDGE-C2 Center is evaluating primary care clinic-based interventions to improve the provision of evidence-based cancer prevention, and is one of seven Implementation Science Centers in Cancer Control, funded by the National Cancer Institute.48 All study procedures were reviewed and approved by the Oregon Health & Science University Institutional Review Board (IRB#20681).
Sample selection and recruitment:
From July to August of 2021, we recruited colonoscopy providers who worked in endoscopy centers or primary care clinics in rural Oregon that also served patients insured by Medicaid. We had three sources for participant recruitment based on referrals: 1. Asking the Medicaid health plans participating in the SMARTER CRC study to identify rural colonoscopy providers; 2. Asking the primary care clinics in the SMARTER CRC study to identify providers; and 3. Contacting other primary care clinics that had participated in research studies with the Oregon Rural Practice-based Research Network (ORPRN). ORPRN is a network of primary care clinicians, community partners, and academics that studies the delivery of health care with the aim of reducing rural health disparities. Participants were eligible if they practiced in geographic regions that were designated as rural or frontier by the Oregon Office of Rural Health or with a Rural-Urban Commuting Area code of 4 or higher.49,50 We recruited different provider types (e.g., PCP, surgeon) and from practice types (e.g., hospital, independent clinics). Primary care clinics, endoscopy centers, and individual participants were approached directly via phone or email to recruit eligible providers. Once participants agreed to participate, they were scheduled for an interview and sent calendar invitations via the Microsoft Outlook scheduling system.
We use the term “colonoscopy” to refer to primary screening for CRC with colonoscopy, colonoscopies completed after an abnormal FIT (i.e., follow-up colonoscopy), and colonoscopies completed in response to symptoms (i.e., diagnostic colonoscopy). At the time of the study, the Oregon state legislature required Medicaid and commercial insurance to cover the cost of colonoscopy, whether it was a primary screening or follow-up after an abnormal FIT.51,52
Data collection and analysis:
The semi-structured interview guide included 17 questions, was developed by a qualitative analyst (NR), and refined using feedback from the project team (see Appendix A). Questions addressed provider experiences providing colonoscopy to patients in rural areas, as well as workflows, barriers, and access. The interview guide further explored whether providers saw different barriers for Medicaid patients than for patients having other types of insurance.
One team member (CB) conducted 50-minute interviews with participants between July and August, 2021, by Zoom or by telephone, depending on participant preference. Interviews were recorded and professionally transcribed by Rev.com. Transcripts were validated, de-identified and imported to ATLAS.ti for coding by two project team members (NR and CB).
Data analysis occurred between August and November 2021. We used an immersion crystallization approach for data analysis 53–55. Documents were reviewed and coded for key themes (e.g., workflow, barriers, access), then individual cases were analyzed to look for patterns by region or practice type. We noticed key differences based on provider type, where some participants were performing colonoscopy on patients from their own primary care practices, while others were general surgeons providing colonoscopy to patients referred from primary care. Finally, we looked for similarities and differences between PCPs versus general surgeons. Preliminary themes were reviewed and refined with full study team and the SMARTER CRC advisory board to finalize themes and enhance credibility and validity of the results.
RESULTS
Demographics:
We outreached to 52 total providers; 19 (37%) agreed to participate. Of the 19 participating providers, 9 (47%) were PCPs, with MD, DO, or Family Medicine roles. Ten (53%) of the participating providers were general surgeons. Practice locations were geographically distributed across rural areas of the state and included 17 (89%) rural and 2 (11%) frontier locations. Providers were employed by hospital systems (n= 9, 47%), Federally Qualified Health Centers (FQHCs) (n=2, 11%), and independent clinics (n=7, 37%), with one provider employed by both a hospital system and independent clinic (n= 1, 5%). A higher proportion of PCPs agreed to participate (n= 17, 53%) as compared to the general surgeons contacted (n= 36, 27%). The SMARTER CRC primary care practice list yielded the highest number of participants (n=14, 74%) compared to either the health plan list (n=2, 11%) or word of mouth based on other OPRRN studies (n=3, 16%). No colonoscopy providers on the Medicaid health plan lists were GI specialists, and two practices suggested GI specialists located in urban settings (and therefore not meeting inclusion criteria).
Our analysis identified four key themes: 1) colonoscopy processes and workflows were distinct based on colonoscopy provider type; 2) perceived barriers to colonoscopy included transportation and unknown patient costs, while a facilitator was providing patient supports to overcome fear and reluctance; 3) PCP endoscopists were important for rural colonoscopy capacity and access; and 4) response to the USPSTF guideline shift in screening initiation age was generally positive.
Two distinct workflows based on colonoscopy provider type
We found two distinct processes for patients needing a colonoscopy: 1) PCPs doing colonoscopy procedures for patients seen in their clinical practices, and 2) general surgeons providing colonoscopy to patients referred to their services from primary care. The associated workflows for these two provider types are summarized in Table 1, and the notable differences are presented below. Provider type had implications on a wide range of interview topics, including differences in the scheduling process, pre-procedure visits, and bowel preparation and patient education as described below.
Table 1.
Colonoscopy Workflow Differences for Rural Providers: Primary Care Providers vs. General Surgeons (with Referred Patients)
| Referral | Scheduling appointments | Pre-Procedure visit | Bowel Prep/Patient Education | Colonoscopy | Sharing of results | Referral to Cancer care | |
|---|---|---|---|---|---|---|---|
| Primary care providers (PCP) (Completing colonoscopy on own patients) | PCP’s clinic staff put in referral through their own EHR. The referral was also sent to the corresponding surgery center or hospital. | Scheduled a colonoscopy during primary care visits, either during in visit, or at Front desk with a scheduler | Completed in PCP clinic during the referring appointment. No separate pre-procedure visit was completed |
Patient education was completed during primary care visits, bowel prep is discussed during these visits and patients are given printed materials when they schedule | Once a week appointments at local surgery centers | Shared with patient via phone call or EHR. | Referred to oncology or colorectal surgeon. |
| General Surgeons | Referred through EHR or fax from primary care provider | Referral coordinators or office managers coordinated scheduling | Most providers required separate pre-procedure visits with patients | Some mailed information packets prior to colonoscopy. Most distributed information packets at pre-procedure visits | In surgery center or hospital depending on where provider has privileges | Sent the results to the PCP via EHR or fax. Surgery clinic staff or surgeon called patients with results | Managed surgical treatment themselves if it is a malignancy they can remove. If chemotherapy is needed, referred to hospital system. |
In relation to scheduling appointments, both provider types reported using a first come, first served approach unless the referred patient was showing symptoms, such as blood in stool, weight loss, or anemia. Patient education before the procedure differed in how and when patients were given pre-colonoscopy educational information. The PCPs who typically performed colonoscopies on patients in their own practice were able to schedule a colonoscopy and provide pre-procedure counseling during a single primary care visit with their patient. General surgeons, on the other hand, were often farther removed from the scheduling process, with referral coordinators located at the surgery center responsible for following up and getting patients on their schedule. They were also more likely to have a separate pre-procedure visit that happened after patients were referred to colonoscopy. This difference in process potentially reduced the number of times PCPs needed to follow-up with the patient pre-procedure, and increased clinician perceptions of patient comfort. For example, one provider (4, PCP) described, “I think the [colonoscopy education] discussion is usually I guess briefer because I know the patient and I’ve already made sure that I think they should have a colonoscopy.”
Most providers reported that their practices provided information packets either during pre-procedure visits or in the mail covering colonoscopy preparation, but the packets had limitations. One provider (6, PCP) commented that while the current process in their office for mailing pre-procedure information packets was “like a well-oiled machine,” it was “devoid of personality.” Another (Provider 5, PCP) commented that the onus was on the patients to follow up and often the pre-procedure information gets “lost in translation and people don’t understand [its] importance.”
Perceived barriers and facilitators to colonoscopy
While workflows differed in key respects as described above, providers reported similar barriers to receipt of colonoscopy. However, general surgeons commented on patient barriers less frequently than the PCP participants. The most common barriers identified were transportation challenges and the inability to take time off work. Some providers described community transportation services available for their patients, but these services did not generally offer a companion, which was needed to ensure the patient made it home safely after the procedure. One provider (11, GS) highlighted this challenge:
“Transportation would be one issue. Not necessarily getting here, but having someone pick you up and take you home. Because I do run into patients who don’t have any family members that live in the area [and] who, for some reason or other, don’t have friends that would come and pick them up.”
While cost was not perceived as preventing patients from getting their initial screening colonoscopy, providers described it as a barrier for follow-up colonoscopies, particularly if their patient had an abnormal FIT result. Providers perceived that screening colonoscopies were covered at 100%, but with a positive FIT test or a polyp “it’s no longer a screening colonoscopy, it’s diagnostic and so they get stuck with their 20% copay. For some of them that’s a really hefty bill.” (Provider 2, PCP)
PCPs in particular noted that education could support patients who were more reluctant to obtain a colonoscopy. Providers noted that “some people [are] looking for a way out” (Provider 10, PCP) and that “fear of discomfort and the unknown of colonoscopies” (Provider 8, PCP) often got in the way, even when their patient knew they needed a colonoscopy. To address this barrier, some providers described sharing patient education around the risks of CRC versus colonoscopy.
Additionally, both types of providers thought that the addition of a program to navigate patients to colonoscopy would be helpful, both to remove the burden from their practice and to help patients address barriers to scheduling and receiving colonoscopy. Two providers shared the following:
I totally see how the navigator at the Cancer Treatment Center helps. It would also take just that, the calls, the questions, the education, and just put it on to somebody else instead of my office, that’s how it would help. (Provider 3, GS)
[Navigation] probably would be good for follow-up after we send the order and it gets authorized by insurance or whatever. It probably would be nice to have somebody follow up with the patient on those things that need to happen to them to get there and to get it done. So, getting their prep done, making sure they have somebody to take care of whatever they need to do at home while they’re gone, that they have a ride home, that they’ve talked to the hospital and gotten scheduled. … or if they’ve decided they don’t want to do that, that I am aware and then we can talk about what are their other options. (Provider 4, PCP)
PCP endoscopists important for rural colonoscopy capacity and access
Overall, providers reported that their current capacity for colonoscopy was sufficient to meet the needs of their rural patients. Most providers reported a range of wait times for the next available colonoscopy appointment, from two weeks to two months, with an average reported wait time of one month. Providers indicated that they felt that colonoscopy was very accessible to their patients. One provider (77, PCP) commented “[Colonoscopies are] pretty accessible. We have five providers in our small county that do them, so I think if you want a colonoscopy, you can get one pretty easily, I think.” Providers also confirmed the lack of GI specialists located in rural areas (indicated by our recruitment referrals). One surgeon (Provider 7) stated that he and his two general surgeon partners did all the screening colonoscopies in the region as “there are not gastroenterologists in the [rural area].” This was seconded by another surgeon (Provider 11), who said that he did “the majority of [colonoscopies],” and noted other providers who did colonoscopies in the area were family practice providers. Another provider (10, PCP) noted that PCPs were essential to making colonoscopy accessible in rural areas, saying, “There aren’t enough GIs and surgeons to go around to all little rural areas in America to provide the service and there are many of my patients that wouldn’t otherwise go two/three hours to the city to have this done, if they can’t get it done in their hometown.”
However, PCP providers highlighted two concerns that could impact ongoing access to colonoscopy in rural communities: a trend for fewer PCPs to get trained in endoscopic procedures and turf issues. Providers pointed out a decline in amount of colonoscopy training hours for PCPs and the importance of including this area of care in rural training and residency programs. For example, one PCP provider (6) commented on how he “doesn’t train anybody to do colonoscopy, [because] they have no free time” anymore, citing changes to the residency hour shift length (from 30 hour to 16 hours). Another provider (10, PCP) stated that there are going to be “less and less opportunities for people that are going into primary care to get endoscopy training.” A third provider (12, PCP) highlighted the need to train more PCPs to perform colonoscopy, saying, “It’s not a difficult procedure. You just got to have time and build some confidence and have experience.” Compounding the lack of training opportunities, some PCPs highlighted the tension between GI specialists, general surgeons, and PCPs, describing the “touchy relationship” (Provider 10, PCP) between the three groups over a “fairly territorial procedure.” (Provider 8, PCP) The need for local colonoscopy provided by PCPs in rural areas was echoed by another provider who said: “[I] think there’s a real place for [PCPs performing colonoscopy]…. And I’m a strong believer that the best care is local care.” (Provider 5, PCP)
Guideline shift to screening initiation at age 45
Overall, the perception among providers of the shift to a lower starting age for routine screening was viewed positively, with a few providers indicating that they were increasingly finding CRC in younger people. Providers were generally unconcerned about the impact of the guideline shift on rural colonoscopy capacity, and did not anticipate a large influx of patients. One provider (56, General Surgeon) commented that “the vast majority of my patients and just generally people that I talk to assume that 50 is when they should start,” indicating that younger patients may not know that they were now eligible for CRC screening. Another provider (11, General Surgeon) suggested that “not too many 45-year-olds want to come in and have a colonoscopy. So I think it’s going to be a hard sell.” Other providers stated that the lowering of the age wouldn’t change the numbers significantly due to the size of their service area, with one provider (1, PCP) saying, “Five years in a rural area of 7,000 people [is] not going to affect the capacity of how we take care of our patients much. Even if that’s an extra one referral a day, that’s one referral a day.”
The biggest concern providers described in relation to the guideline shift was uncertainty about how insurance plans would cover the newly eligible population. One provider (4, PCP) stated that even though they were aware of the recommendation change, they hadn’t made a formal change to the clinic policy because “nobody sort of knows whether or not billing would pay for it.” Another provider (1, PCP) compared the CRC screening guideline shift to insurance coverage for human papillomavirus (HPV) vaccination, saying, “For example, when the HPV vaccine was available for 35 and plus, it took quite some time for insurance companies to catch up. But now it’s great.”
Discussion
We present several key findings from interviewed providers of colonoscopy serving rural Medicaid patients including the context of colonoscopy in rural settings as provided by either PCPs or general surgeons, barriers and facilitators to colonoscopy, and capacity overall as well as in light of the recent guideline shift to lower screening initiation. These themes reflect opportunities to address multilevel barriers with interventions, such as improving practice-level communications, ensuring continued PCP colonoscopy capacity, and facilitating patient education.
The different workflows (i.e., for general surgeons and PCPs) for colonoscopy referral and completion might inform interventions to better support rural colonoscopy provision. PCPs doing colonoscopy procedures on patients in their own practice thought their more streamlined referral and patient education processes might have reduced the burden on their patients who needed a colonoscopy. PCPs in our study were already doing a lot to educate patients about CRC screening methods, and the streamlined referral and education might improve patient experience. Interestingly, while the workflows of the two different colonoscopy provider types were different, this context did not seem to affect perceptions of barriers and facilitators, which were similar across all providers.
The barriers perceived by providers, such as transportation, cost, and reluctance to get the procedure, are consistent with prior research.56–59 One important finding is that providers noted cost concerns relating to patients being billed for colonoscopies performed as follow-up to stool-based testing. However, Oregon passed State legislation (House Bill 2560) in 2015 eliminating additional cost of most colonoscopies in response to an abnormal FIT result for commercially insured and Medicaid patients, and recently (January, 2023) Medicare changed to cover this gap as well. As several providers seemed unaware of this policy change, efforts are needed to ensure patients and providers have adequate information about the cost of health services. This barrier is especially important because research indicates delayed follow-up colonoscopy is linked to worse health outcomes,60,61 and colonoscopy completion rates following abnormal FIT tests have been as low as 31-35% in prior research.62,63
Providers suggested that patient education supports could help facilitate receipt of colonoscopy for their patients. In particular, patient navigation63–65 was perceived to be a potential effective strategy. The context differences noted above in our settings could inform the implementation of navigation. For example, it could be part of a more general panel management or population health approach in settings where the PCP provides colonoscopy services. On the other hand, for general surgeons conducting colonoscopy, a colonoscopy-specific navigator based in either the primary care clinic or surgical center might facilitate engagement and understanding given that the existing written communications were perceived as impersonal.64,65
Our study supports prior research that indicates non-GI specialists are crucial to the provision of colonoscopy in rural areas.30,32,37,38 Our recruitment through rural practices and health plans identified only two GIs, and these were both located in urban areas and thus not included in the final sample. In addition, several providers expressed the importance of PCPs to providing colonoscopy services in these rural areas given the lack of specialists in their geographic location. Our findings suggest that to ensure access and capacity in rural areas, training opportunities and practice level supports should be available for PCPs in colonoscopy.26 While general surgeons receive training in colonoscopy as part of their residency (typically at a recommended threshold of 50 colonoscopies), training programs generally recommend at least 100 to 200 procedures for competency, and a high number of completed procedures (275–500) are standard for colonoscopy specialists.66–68 Prior literature has highlighted this tension between high quality colonoscopy procedures and access to screening.26,38,69–72 While there is conflicting research about quality of colonoscopy services performed by non-GI specialists, research supports the idea that colonoscopy performed by general surgeons and PCPs are safe overall,34–38 and a recent study concluded screening colonoscopies performed by most physicians in rural and underserved areas met quality standards.72 To ensure continued colonoscopy access in rural communities, support for the training and mentoring of rural, non-GI endoscopists could be critical to have a sufficient number of providers.12,30,37,38,72 In particular, targeted education, quality tracking, and increased training exposure to colonoscopy have been recommended by others to ensure high-quality colonoscopies by physicians practicing in rural areas.70,72
The providers in our study were supportive of the recommended guideline change from age 50 to 45. However, some providers noted possible future capacity concerns relating to the perception that the number of PCPs providing colonoscopy will shrink. In rural areas, a transition in a single provider can have a profound impact on access to care if one individual providing colonoscopy services leaves in a rural practice. In addition, providers in this study felt colonoscopy was accessible to their patients and community, though CRC screening rates remain low in rural areas.9 This may indicate variation of accessibility in different rural areas; a difference between types of colonoscopy providers, with better access for those that provide colonoscopy services for their own patients; or issues beyond colonoscopy access, such as patient awareness, cost, fears about the procedure, etc.. Future research is needed to establish if the perception of sufficient capacity for colonoscopy in rural areas reflects actual trends in other sources of data, especially given some indications that colonoscopy services may have been negatively affected by the pandemic.30
Our study has several limitations. First, our sample of providers included only PCPs or general surgeons who performed colonoscopies; we did not interview any GI specialists, as these professionals practice in urban settings. Future work could explore if perceptions and workflows are similar or different for GIs in urban settings who see a high proportion of rural patients. Second, we only interviewed colonoscopy providers serving at least some Medicaid patients. However, we anticipate the number of providers who do not provide care to a Medicaid population would be very small. We also do not have information about years of provider experience, the number of procedures performed, or colonoscopy quality measures, such as rates of completed colonoscopies (cecum reached), or adenoma detection rates for the providers in our sample. Despite these limitations, our study provides valuable insight into an important and understudied group of providers serving a crucial role in rural access to preventive care.
Conclusion
By interviewing rural colonoscopy providers, we found that both PCP and general surgeons provided colonoscopy in rural areas and uncovered context details about colonoscopy referral and completion by rural patients. Providers described multiple barriers to colonoscopy in rural areas, such as transportation and cost, and emphasized patient education could be improved to overcome reluctance. Our results highlight that PCPs are an essential part of the workforce that provides colonoscopy services in rural areas and may be even more important if the new screening guidelines increase demand for these services. Our findings suggest multi-level opportunities to address the barriers to colonoscopy in rural settings, such as spreading patient navigation services, increasing PCP endoscopist training opportunities, and ensuring practice-level interventions for colonoscopy referral and follow-up are flexible enough for both types of workflows described in this research. Future research could explore data from observational visits or surveys to validate findings and inform the types of interventions needed for PCP endoscopists compared to GI specialists. Research is also needed to further assess colonoscopy capacity, quality, and provider characteristics in rural settings.
Acknowledgments
This study was conducted as part of the NCI-funded consortium The Accelerating Colorectal Cancer Screening and Follow-up through Implementation Science (ACCSIS) Program. The overall aim of ACCSIS is to conduct multi-site, coordinated, transdisciplinary research to evaluate and improve colorectal cancer screening processes using implementation science strategies. The research team would also like to acknowledge our clinical practice and coordinated care organization research partners who are part of the SMARTER CRC study. We would also like to thank Jaime Scott who assisted with some of the literature review and interview guide refinement.
Funding sources
Research reported in this publication was supported by the National Cancer Institute of the National Institutes of Health under Award Number UH3CA244298, Screening More patients for CRC through Adapting and Refining Targeted Evidence-based Interventions in Rural settings (SMARTER CRC) and Award Number P50CA244289, the BRIDGE-C2 Center (Building Research in Implementation and Dissemination to close Gaps and achieve Equity in Cancer Control). This program is supported by funding provided through The Accelerating Colorectal Cancer Screening and Follow-up through Implementation Science (ACCSIS) Program is a Beau Biden Cancer Moonshot℠ Initiative. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Conflicts of Interest:
Disclosures From 2020 – present, Dr. Coronado has served as a Scientific Advisor on contracts through the Center for Health Research for Exact Sciences and Guardant Health. She is also the PI on a contract through the Center for Health Research funded by Guardant Health that is assessing adherence to a commercially available blood test for colorectal cancer. All other authors declare no potential conflicts of interest.
Appendix 1: Interview Guide
The questions below are the general topic areas we will explore with interview participants. These questions will be modified in light of what is learned during the interview and to fit the experiences of the interviewee.
Introductory Script
Thank you for participating in this interview. My name is [insert name] and I am part of a research team at the Oregon Rural Practice-based Research Network (ORPRN) that is studying colorectal cancer screening in rural communities. I’m a [say 1-2 sentences about your role on the team, be BRIEF]. As part of this study, we are interested in understanding community resources and specialty care in your area. Our research is focused on gathering feedback from stakeholders to adapt materials and methods to promote CRC screening using mailed fecal test outreach for rural and frontier populations and pilot-testing outreach to support patients with an abnormal fecal test result to obtain a follow-up colonoscopy. We’re especially focused on patients with Medicaid because the research shows lower screening rates for this population. As part of this study, we are interested in understanding your clinic’s experiences providing colonoscopy services in rural Oregon. Your responses today –and those of primary care staff members and patients- will help us understand the health care experiences of rural residents and be used by our team identify areas of success as well as those needing improvement.
We would like to record interviews so we can accurately capture your experiences in your own words. This interview recording will be transcribed and all proper names and places will be coded to protect your identity and privacy. Do I have permission to audiotape our interview?
If “Yes”, please record the person’s consent to record on the audio recording. Please have the interviewer complete the following sentence on recording: “My name is [insert name], today is [insert date] and I consent to this audio recording”.
Opening/Warm up Questions
-
Thank you. Can you tell me about who you are, the organization you work for, and what you do?
Possible probes:- How long have you worked there?
- What is your training or background?
- Do you live in the community where the clinic is located?
Grand Tour Questions
-
1The goal of this interview is to better understand your experience providing endoscopy care to rural Oregonians. I’d like to start with learning more about your clinic--Can you describe a little bit about your clinic?
- Probe: How large is your service area?
- Probe: How many providers do you have?
- Probe: How do you prioritize patients (e.g., screening colonoscopy vs. positive FIT, insurance status)
- Probe: What do they look like as a setting (independent vs. tied to a hospital)
Workflow
I’d like to understand a bit about how patients get to your clinic and how they get scheduled.
-
2
Can you tell me about how it usually works when patients are referred to you?
Possible Probes:- How does your workflow function now with COVID?
- Are there differences in workflows based on insurance types?
- How do you get results back to the PCP? Does this depend on the outcome?
- Does your facility notify primary care when patients are unable to be reached for an appointment?
- What is the approximate percentage of patients who are referred to your facility successfully make an appointment? What would you estimate is the average wait time for appointments?
- If a patient needs additional treatment, what does that process look like? Who makes decisions about where they go?
-
3
What gets in the way of patients scheduling or completing appointments?
Possible Probes:- Is this similar or different for Medicaid patients?
-
4
What seems to work really well?
-
5How are patients told about how to do colonoscopy prep?
- Probe: what prep do you generally recommend for patients?
- Probe: Do you generally conduct pre-procedure visits? If so, among which patients?
-
6Describe the referral to care process for patients who are found to have cancer.
- Probes: Where are patients generally referred? Is primary care notified of referral?
- Probes: What, if any, barriers do patients face in obtaining timely referral or receiving treatment?
-
7
What resources or programs are available to help patients?
Possible Probe- If transportation is a factor, what resources are available to patients?
- If cost is a factor, what resources are available to patients?
- If language is a factor, what resources are available to patients?
-
8
Who do you commonly get endoscopy referrals from? What works or doesn’t work from those different clinics?
-
9
What navigation activities are you currently conducting in your office?
Possible probes:- Do you complete reminder calls or texts? When do these go out?
- Do you give out any informational sheets or do a pre-procedure visit?
-
10
What would you want to see out of a navigation program?
-
11What do you wish primary care clinics knew about your process?
- Probe: what are the characteristics of primary care practices that are interfacing/interacting with you successfully?
-
12What would you like patients to know before they are referred to you?
- Probe: main barriers, reasons for cancellations, scheduling hurdles
-
13
Overall, how available or accessible do you think colonoscopy is for rural patients in your area?
Guidelines & FIT screening
-
14As you may be aware, the USPSTF guidelines for colorectal cancer screening have recently changed with screening to begin at age 45. What was the overall reaction at the practice like to these changes?
- Probe: How does this impact your practice (e.g., capacity to do the colonoscopies)
- Probe: Perceptions/attitudes about FIT testing for first-line screening
- Probe: Perceptions/attitude about Cologuard for first-line screening
- Probe: Thoughts about expanding the workforce of clinicians who can perform colonoscopy
- Probe: Do you feel that the guideline shift will impact the accessibility of colonoscopy for rural patients?
-
15
Is there anything else we should know in order to understand the role of endoscopy providers in CRC screening?
Survey Questions:
On average, what does it cost patients to get an endoscopy at your clinic?
What is the average wait time that it takes to get a patient on the schedule for an endoscopy?
- What percent of your endoscopy procedures are:
- Medicaid
- Medicare
- Other insurance (commercial, Veteran, IHS)
- Other populations (Latino/Latina, AI/Native American, etc.)
What are your cancellation rates?
References
- 1.D’Andrea E, Ahnen DJ, Sussman DA, Najafzadeh M. Quantifying the impact of adherence to screening strategies on colorectal cancer incidence and mortality. Cancer Med. Jan 2020;9(2):824–836. doi: 10.1002/cam4.2735 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Davidson KW, Barry MJ, Mangione CM, et al. Screening for Colorectal Cancer: US Preventive Services Task Force Recommendation Statement. Jama. May 18 2021;325(19):1965–1977. doi: 10.1001/jama.2021.6238 [DOI] [PubMed] [Google Scholar]
- 3.Lin JS, Piper MA, Perdue LA, et al. U.S. Preventive Services Task Force Evidence Syntheses, formerly Systematic Evidence Reviews. Screening for Colorectal Cancer: A Systematic Review for the US Preventive Services Task Force. Agency for Healthcare Research and Quality (US); 2016. [PubMed] [Google Scholar]
- 4.CDC. Colorectal cancer statistics. Division of Cancer Prevention and Control, Centers for Disearch Control and Prevention. Accessed 1/5/2023, 2023. https://www.cdc.gov/cancer/colorectal/statistics/index.htm [Google Scholar]
- 5.Siegel RL, Miller KD, Goding Sauer A, et al. Colorectal cancer statistics, 2020. CA Cancer J Clin. May 2020;70(3):145–164. doi: 10.3322/caac.21601 [DOI] [PubMed] [Google Scholar]
- 6.Sharma KP, Grosse SD, Maciosek MV, et al. Preventing Breast, Cervical, and Colorectal Cancer Deaths: Assessing the Impact of Increased Screening. Prev Chronic Dis. Oct 8 2020;17:E123. doi: 10.5888/pcd17.200039 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Society AC. Colorectal Cancer Facts & Figures 2020-2022. American Cancer Society. Accessed 11/17/22, 2022. https://www.cancer.org/content/dam/cancer-org/research/cancer-facts-and-statistics/colorectal-cancer-facts-and-figures/colorectal-cancer-facts-and-figures-2020-2022.pdf [Google Scholar]
- 8.Cole AM, Jackson JE, Doescher M. Colorectal cancer screening disparities for rural minorities in the United States. J Prim Care Community Health. Apr 1 2013;4(2):106–11. doi: 10.1177/2150131912463244 [DOI] [PubMed] [Google Scholar]
- 9.Ojinnaka CO, Choi Y, Kum HC, Bolin JN. Predictors of Colorectal Cancer Screening: Does Rurality Play a Role? J Rural Health. Summer 2015;31(3):254–68. doi: 10.1111/jrh.12104 [DOI] [PubMed] [Google Scholar]
- 10.Carmichael H, Cowan M, McIntyre R, Velopulos C. Disparities in colorectal cancer mortality for rural populations in the United States: Does screening matter? Am J Surg. Jun 2020;219(6):988–992. doi: 10.1016/j.amjsurg.2019.09.027 [DOI] [PubMed] [Google Scholar]
- 11.Sanchez JI, Shankaran V, Unger JM, Madeleine MM, Selukar SR, Thompson B. Inequitable access to surveillance colonoscopy among Medicare beneficiaries with surgically resected colorectal cancer. Cancer. Feb 1 2021;127(3):412–421. doi: 10.1002/cncr.33262 [DOI] [PubMed] [Google Scholar]
- 12.Aboagye JK, Kaiser HE, Hayanga AJ. Rural-Urban Differences in Access to Specialist Providers of Colorectal Cancer Care in the United States: A Physician Workforce Issue. JAMA Surg. Jun 2014;149(6):537–43. doi: 10.1001/jamasurg.2013.5062 [DOI] [PubMed] [Google Scholar]
- 13.Rosenblatt RA, Hart LG. Physicians and rural America. West J Med. Nov 2000;173(5):348–51. doi: 10.1136/ewjm.173.5.348 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Walker GV, Grant SR, Guadagnolo BA, et al. Disparities in Stage at Diagnosis, Treatment, and Survival in Nonelderly Adult Patients With Cancer According to Insurance Status. Journal of Clinical Oncology. 2014;32(28):3118–3125. doi: 10.1200/jco.2014.55.6258 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Koh HK, Oppenheimer SC, Massin-Short SB, Emmons KM, Geller AC, Viswanath K. Translating Research Evidence Into Practice to Reduce Health Disparities: A Social Determinants Approach. American Journal of Public Health. 2010;100(S1):S72–S80. doi: 10.2105/ajph.2009.167353 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Purnell TS, Calhoun EA, Golden SH, et al. Achieving Health Equity: Closing The Gaps In Health Care Disparities, Interventions, And Research. Health Aff (Millwood). Aug 1 2016;35(8):1410–5. doi: 10.1377/hlthaff.2016.0158 [DOI] [PubMed] [Google Scholar]
- 17.Lyu W, Wehby GL. The Impacts of the ACA Medicaid Expansions on Cancer Screening Use by Primary Care Provider Supply. Med Care. Mar 2019;57(3):202–207. doi: 10.1097/mlr.0000000000001053 [DOI] [PubMed] [Google Scholar]
- 18.Rhodes KV, Kenney GM, Friedman AB, et al. Primary care access for new patients on the eve of health care reform. JAMA Intern Med. Jun 2014;174(6):861–9. doi: 10.1001/jamainternmed.2014.20 [DOI] [PubMed] [Google Scholar]
- 19.Richards MR, Saloner B, Kenney GM, Rhodes KV, Polsky D. Availability of New Medicaid Patient Appointments and the Role of Rural Health Clinics. Health Serv Res. Apr 2016;51(2):570–91. doi: 10.1111/1475-6773.12334 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.McConnell KJ, Charlesworth CJ, Zhu JM, et al. Access to Primary, Mental Health, and Specialty Care: a Comparison of Medicaid and Commercially Insured Populations in Oregon. J Gen Intern Med. Jan 2020;35(1):247–254. doi: 10.1007/s11606-019-05439-z [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Hicklin K, O’Leary MC, Nambiar S, et al. Assessing the impact of multicomponent interventions on colorectal cancer screening through simulation: What would it take to reach national screening targets in North Carolina? Prev Med. Sep 2022;162:107126. doi: 10.1016/j.ypmed.2022.107126 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Hassmiller Lich K, O’Leary MC, Nambiar S, et al. Estimating the impact of insurance expansion on colorectal cancer and related costs in North Carolina: A population-level simulation analysis. Prev Med. Dec 2019;129s:105847. doi: 10.1016/j.ypmed.2019.105847 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Kruse-Diehr AJ, Oliveri JM, Vanderpool RC, et al. Development of a multilevel intervention to increase colorectal cancer screening in Appalachia. Implement Sci Commun. May 19 2021;2(1):51. doi: 10.1186/s43058-021-00151-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Paskett ED, Young GS, Bernardo BM, et al. The CITIES Project: Understanding the Health of Underrepresented Populations in Ohio. Cancer Epidemiol Biomarkers Prev. Mar 2019;28(3):442–454. doi: 10.1158/1055-9965.Epi-18-0793 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Oshiro M, Kamizato M, Jahana S. Factors related to help-seeking for cancer medical care among people living in rural areas: a scoping review. BMC Health Serv Res. Jun 28 2022;22(1):836. doi: 10.1186/s12913-022-08205-w [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Evans DV, Cole AM, Norris TE. Colonoscopy in rural communities: a systematic review of the frequency and quality. Rural Remote Health. Apr-Jun 2015;15(2):3057. [PubMed] [Google Scholar]
- 27.Bronfenbrenner U Developmental research and public policy. Res Publ Assoc Res Nerv Ment Dis. 1973;51:352–80. [PubMed] [Google Scholar]
- 28.Baxter NN, Goldwasser MA, Paszat LF, Saskin R, Urbach DR, Rabeneck L. Association of colonoscopy and death from colorectal cancer. Annals of internal medicine. Jan 6 2009;150(1):1–8. doi: 10.7326/0003-4819-150-1-200901060-00306 [DOI] [PubMed] [Google Scholar]
- 29.Winawer SJ, Flehinger BJ, Schottenfeld D, Miller DG. Screening for colorectal cancer with fecal occult blood testing and sigmoidoscopy. J Natl Cancer Inst. Aug 18 1993;85(16):1311–8. doi: 10.1093/jnci/85.16.1311 [DOI] [PubMed] [Google Scholar]
- 30.Barsouk A, Saginala K, Aluru JS, Rawla P, Barsouk A. US Cancer Screening Recommendations: Developments and the Impact of COVID-19. Med Sci (Basel). Mar 1 2022;10(1)doi: 10.3390/medsci10010016 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Naylor KB, Tootoo J, Yakusheva O, Shipman SA, Bynum JPW, Davis MA. Geographic variation in spatial accessibility of U.S. healthcare providers. PLoS One. 2019;14(4):e0215016. doi: 10.1371/journal.pone.0215016 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Physicians AAoF. AAFP Colonoscopy Position Paper. American Academy of Family Physicians. Accessed 1/19/2023, 2023. https://www.aafp.org/about/policies/all/colonoscopy-position-paper.html [Google Scholar]
- 33.Doumouras AG, Anvari S, Cadeddu M, Anvari M, Hong D. Geographic variation in the provider of screening colonoscopy in Canada: a population-based cohort study. CMAJ Open. Mar 13 2018;6(1):E126–e131. doi: 10.9778/cmajo.20170131 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Holub JL, Morris C, Fagnan LJ, Logan JR, Michaels LC, Lieberman DA. Quality of Colonoscopy Performed in Rural Practice: Experience From the Clinical Outcomes Research Initiative and the Oregon Rural Practice-Based Research Network. J Rural Health. Feb 2018;34 Suppl 1(Suppl 1):s75–s83. doi: 10.1111/jrh.12231 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Kozbial K, Reinhart K, Heinze G, et al. High quality of screening colonoscopy in Austria is not dependent on endoscopist specialty or setting. Endoscopy. Mar 2015;47(3):207–16. doi: 10.1055/s-0034-1390910 [DOI] [PubMed] [Google Scholar]
- 36.Kolber MR, Wong CK, Fedorak RN, Rowe BH. Prospective Study of the Quality of Colonoscopies Performed by Primary Care Physicians: The Alberta Primary Care Endoscopy (APC-Endo) Study. PLoS One. 2013;8(6):e67017. doi: 10.1371/journal.pone.0067017 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Mehran A, Jaffe P, Efron J, Vernava A, Liberman MA. Colonoscopy: why are general surgeons being excluded? Surg Endosc. Dec 2003;17(12):1971–3. doi: 10.1007/s00464-003-8806-5 [DOI] [PubMed] [Google Scholar]
- 38.Wilkins T, LeClair B, Smolkin M, et al. Screening colonoscopies by primary care physicians: a meta-analysis. Annals of family medicine. Jan-Feb 2009;7(1):56–62. doi: 10.1370/afm.939 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Crockett SD, Ladabaum U. Potential Effects of Lowering Colorectal Cancer Screening Age to 45 Years on Colonoscopy Demand, Case Mix, and Adenoma Detection Rate. Gastroenterology. Mar 2022;162(3):984–986.e5. doi: 10.1053/j.gastro.2021.11.024 [DOI] [PubMed] [Google Scholar]
- 40.Liang PS, Allison J, Ladabaum U, et al. Potential Intended and Unintended Consequences of Recommending Initiation of Colorectal Cancer Screening at Age 45 Years. Gastroenterology. Oct 2018;155(4):950–954. doi: 10.1053/j.gastro.2018.08.019 [DOI] [PubMed] [Google Scholar]
- 41.Ramanadhan S, Davis MM, Armstrong R, et al. Participatory implementation science to increase the impact of evidence-based cancer prevention and control. Cancer Causes Control. Mar 2018;29(3):363–369. doi: 10.1007/s10552-018-1008-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Powell BJ, Beidas RS, Lewis CC, et al. Methods to Improve the Selection and Tailoring of Implementation Strategies. J Behav Health Serv Res. Apr 2017;44(2):177–194. doi: 10.1007/s11414-015-9475-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Megna B, Shaukat A. Is 45 the new 50? Controversies in lowering the screening age for colorectal cancer. Expert Rev Gastroenterol Hepatol. Oct 2019;13(10):915–917. doi: 10.1080/17474124.2019.1681973 [DOI] [PubMed] [Google Scholar]
- 44.Hyams T, Mueller N, Curbow B, King-Marshall E, Sultan S. Screening for colorectal cancer in people ages 45–49: research gaps, challenges and future directions for research and practice. Transl Behav Med. Feb 16 2022;12(2):198–202. doi: 10.1093/tbm/ibab079 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Mannucci A, Zuppardo RA, Rosati R, Leo MD, Perea J, Cavestro GM. Colorectal cancer screening from 45 years of age: Thesis, antithesis and synthesis. World J Gastroenterol. Jun 7 2019;25(21):2565–2580. doi: 10.3748/wjg.v25.i21.2565 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Coronado GD, Leo MC, Ramsey K, et al. Mailed fecal testing and patient navigation versus usual care to improve rates of colorectal cancer screening and follow-up colonoscopy in rural Medicaid enrollees: a cluster-randomized controlled trial. Implement Sci Commun. Apr 13 2022;3(1):42. doi: 10.1186/s43058-022-00285-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.BRIDGE C-2 Center. Center for Primary Care Research and Innovation. Accessed March 1st, 2023, https://bridgetoinnovation.org/our-initiatives/bridge-c2-center/
- 48.Oh AY, Emmons KM, Brownson RC, et al. Speeding implementation in cancer: The National Cancer Institute’s Implementation Science Centers in Cancer Control. J Natl Cancer Inst. Feb 8 2023;115(2):131–138. doi: 10.1093/jnci/djac198 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Health OOoR. Primary Care Service Areas: Rural and Frontier Definitions. 2020. https://www.ohsu.edu/oregon-office-of-rural-health/orh-primary-care-service-areas
- 50.USDA. Rural-Urban Commuting Area Codes. Accessed 17 Aug. 2020, 2020. https://www.ers.usda.gov/data-products/rural-urban-commuting-area-codes.aspx
- 51.Gray C Greenlick Wants Free Comprehensive Colon Screenings; Insurers Want Delay. The Lund Report. https://www.thelundreport.org/content/greenlick-wants-free-comprehensive-colon-screenings-insurers-want-delay [Google Scholar]
- 52.Oregon Laws 2015. In: Legislature O, editor. Chapter 206: Secretary of State; 2015. [Google Scholar]
- 53.Miller WLCB. The dance of interpretation. In: Crabtree BFMW, ed. Doing qualitative research. 2nd ed ed. Sage Publications, Inc; 1999:127–143. [Google Scholar]
- 54.Cohen DJ, Crabtree BF. Evaluative criteria for qualitative research in health care: controversies and recommendations. Annals of family medicine. Jul-Aug 2008;6(4):331–9. doi: 10.1370/afm.818 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Malterud K Qualitative research: standards, challenges, and guidelines. Lancet. Aug 11 2001;358(9280):483–8. doi: 10.1016/s0140-6736(01)05627-6 [DOI] [PubMed] [Google Scholar]
- 56.Hughes AG, Watanabe-Galloway S, Schnell P, Soliman AS. Rural-Urban Differences in Colorectal Cancer Screening Barriers in Nebraska. J Community Health. Dec 2015;40(6):1065–74. doi: 10.1007/s10900-015-0032-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Honein-AbouHaidar GN, Kastner M, Vuong V, et al. Systematic Review and Meta-study Synthesis of Qualitative Studies Evaluating Facilitators and Barriers to Participation in Colorectal Cancer Screening. Cancer Epidemiol Biomarkers Prev. Jun 2016;25(6):907–17. doi: 10.1158/1055-9965.Epi-15-0990 [DOI] [PubMed] [Google Scholar]
- 58.Davis TC, Morris J, Rademaker A, Ferguson LA, Arnold CL . Barriers and Facilitators to Colorectal Cancer Screening Among Rural Women in Community Clinics by Heath Literacy. J Womens Health Issues Care. 2017;6(6)doi: 10.4172/2325-9795.1000292 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Plumb AA, Ghanouni A, Rainbow S, et al. Patient factors associated with non-attendance at colonoscopy after a positive screening faecal occult blood test. J Med Screen. Mar 2017;24(1):12–19. doi: 10.1177/0969141316645629 [DOI] [PubMed] [Google Scholar]
- 60.Corley DA, Jensen CD, Quinn VP, et al. Association Between Time to Colonoscopy After a Positive Fecal Test Result and Risk of Colorectal Cancer and Cancer Stage at Diagnosis. Jama. Apr 25 2017;317(16):1631–1641. doi: 10.1001/jama.2017.3634 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Lee YC, Fann JC, Chiang TH, et al. Time to Colonoscopy and Risk of Colorectal Cancer in Patients With Positive Results From Fecal Immunochemical Tests. Clin Gastroenterol Hepatol. Jun 2019;17(7):1332–1340.e3. doi: 10.1016/j.cgh.2018.10.041 [DOI] [PubMed] [Google Scholar]
- 62.Green BB, Baldwin LM, West II, Schwartz M, Coronado GD. Low Rates of Colonoscopy Follow-up After a Positive Fecal Immunochemical Test in a Medicaid Health Plan Delivered Mailed Colorectal Cancer Screening Program. J Prim Care Community Health. Jan-Dec 2020;11:2150132720958525. doi: 10.1177/2150132720958525 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 63.Cusumano VT, Myint A, Corona E, et al. Patient Navigation After Positive Fecal Immunochemical Test Results Increases Diagnostic Colonoscopy and Highlights Multilevel Barriers to Follow-Up. Dig Dis Sci. Nov 2021;66(11):3760–3768. doi: 10.1007/s10620-021-06866-x [DOI] [PubMed] [Google Scholar]
- 64.Dougherty MK, Brenner AT, Crockett SD, et al. Evaluation of Interventions Intended to Increase Colorectal Cancer Screening Rates in the United States: A Systematic Review and Meta-analysis. JAMA Intern Med. Dec 1 2018;178(12):1645–1658. doi: 10.1001/jamainternmed.2018.4637 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65.Idos GE, Bonner JD, Haghighat S, et al. Bridging the Gap: Patient Navigation Increases Colonoscopy Follow-up After Abnormal FIT. Clin Transl Gastroenterol. Feb 22 2021;12(2):e00307. doi: 10.14309/ctg.0000000000000307 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Spier BJ, Durkin ET, Walker AJ, Foley E, Gaumnitz EA, Pfau PR. Surgical resident’s training in colonoscopy: numbers, competency, and perceptions. Surg Endosc. Oct 2010;24(10):2556–61. doi: 10.1007/s00464-010-1002-5 [DOI] [PubMed] [Google Scholar]
- 67.Lee SH, Chung IK, Kim SJ, et al. An adequate level of training for technical competence in screening and diagnostic colonoscopy: a prospective multicenter evaluation of the learning curve. Gastrointest Endosc. Apr 2008;67(4):683–9. doi: 10.1016/j.gie.2007.10.018 [DOI] [PubMed] [Google Scholar]
- 68.Di Paola LE, Mahler M, Sala Lozano A, Nardi MA, Ladenheim RI, García Diéguez M. Definition of minimum procedures required to certify competence in gastrointestinal endoscopy using the Delphi method. Rev Esp Enferm Dig. Apr 1 2022;doi: 10.17235/reed.2022.8553/2021 [DOI] [PubMed] [Google Scholar]
- 69.Rutter MD, Senore C, Bisschops R, et al. The European Society of Gastrointestinal Endoscopy Quality Improvement Initiative: developing performance measures. Endoscopy. Jan 2016;48(1):81–9. doi: 10.1055/s-0035-1569580 [DOI] [PubMed] [Google Scholar]
- 70.Edwards JK, Norris TE. Colonoscopy in rural communities: can family physicians perform the procedure with safe and efficacious results? J Am Board Fam Pract. Sep-Oct 2004;17(5):353–8. doi: 10.3122/jabfm.17.5.353 [DOI] [PubMed] [Google Scholar]
- 71.Azzopardi J, DeWitt DE. Quality and safety issues in procedural rural practice: a prospective evaluation of current quality and safety guidelines in 3000 colonoscopies. Rural Remote Health. 2012;12:1949. [PubMed] [Google Scholar]
- 72.Brajcich BC, Yang AD, Keswani RN, et al. The quality of screening colonoscopy in rural and underserved areas. Surg Endosc. Jul 2022;36(7):4845–4853. doi: 10.1007/s00464-021-08833-z [DOI] [PubMed] [Google Scholar]
