Between 2009 and 2012, additional system-level strategies implemented included:
- Standardization of outreach by gastroenterology department schedulers whereby all FIT-positive participants with a referral received a minimum of 3 repeat telephone attempts at varying times of day and 1 or more personalized secure electronic messages over 10–21 days.
- A dedicated staff member in each service area, typically a nurse practitioner (NP) or equivalent, was assigned responsibility for ensuring that standard processes were being followed.
- Established a goal that ≥80% of FIT-positive participants, accessible by telephone and not requiring medical evaluation, would complete their diagnostic colonoscopy within 30 days of testing positive.
- A proportion of each medical center's overall budget was withheld at the beginning of each year and only dispensed if targets for overall colonoscopy access and timely follow-up were met. Physician salaries were not subject to change based on these targets, but the policy encouraged departments to maintain adequate colonoscopy capacity and scheduling flexibility to allow scheduling within about 2 weeks of telephone contact after a positive FIT.
Between 2013 and 2016, several gastroenterology departments began directly contacting participants by accessing daily lists of FIT-positive participants. FIT results from the central laboratory continued to be sent electronically to the patient's primary care provider. Primary care providers had the option to contact their patients directly to inform them of their FIT result and to place an electronic referral with their local gastroenterology department. However, an increasing proportion of participants were first contacted by a medical assistant or NP from the gastroenterology department, who explained the FIT result and directly booked the colonoscopy. Participants with concerns about the appropriateness of colonoscopy (e.g., severe comorbidities or participant refusal) were flagged for review by a gastroenterologist.
Overall cohort characteristics
Among 160,051 screening participants who had a positive FIT between 2006 and 2016, the mean age of participants was 62 years, 75,594 (47%) were women, and 90,545 (57%) were non-Hispanic white, 26,547 (17%) Asian, 20,388 (13%) Hispanic, 11,101 (7%) African American, and 11,470 (7%) other. There were no substantive differences in participant characteristics across the 3 study time intervals (Table 2).
Changes in time to colonoscopy follow-up after a positive FIT (all service areas)
Time to colonoscopy after a positive FIT significantly improved over the 10-year study period (Figure 2), concordant with the serial implementation of the described strategies (Table 1). After adjusting for participant characteristics, the proportion of participants who completed colonoscopy within 30 days after a positive FIT more than doubled between 2006–2008 and 2009–2012, from 9% (95% CI 9%–10%) to 23% (95% CI 23%–24%), and further to 34% in 2013–2016 (95% CI 34%–35%, P < 0.001). The proportion who completed colonoscopy within 180 days increased significantly from 67% in 2006–2008 (95% CI 66%–68%) to 79% in 2009–2012 (95% CI 78%–80%) and 83% in 2013–2016 (95% CI 83%–84%, P < 0.001). In sensitivity analyses, we used the time intervals 2006–2009, 2010–2013, and 2014–2016 and repeated the analyses accounting for possible clustering by service areas, but in both cases obtained very similar results (not shown).
Strategies which varied across service areas in 2016
Although the model described in Figure 1 had been implemented in most service areas by the end of the study period, variability remained (Table 3). For example, there was variation in the job title of those contacting participants (i.e., medical assistant or medical assistant team, NP, and physician assistant). In 8 of 14 responding service areas, a licensed provider (i.e., nurse or physician) attempted to contact participants before removing their name from the active list and notifying their primary care provider that no colonoscopy could be scheduled. In addition, only 3 service areas reported regular reviews of FIT-positive follow-up performance metrics, and only 4 reported consistent colonoscopy availability within 2 weeks of contacting participants. To examine whether service areas with higher colonoscopy completion rates at 30 and 180 days could be differentiated by the specific strategies implemented, we ranked service areas by their colonoscopy follow-up performance (Table 3). This analysis involved 21,291 participants who had a positive FIT in 2016. After adjusting for differences in participant characteristics across the 15 service areas, follow-up colonoscopy within 30 days varied between 10% (95% CI 9%–12%) to 59% (95% CI 56%–61%) (Table 3), and follow-up within 180 days varied between 72% (95% CI 70%–75%) and 88% (95% CI 86%–91%), with all but 1 service area having >80% completion within 180 days. However, we did not find any obvious patterns suggesting that higher performing service areas had implemented specific strategies or a greater number of strategies. For instance, two high-performing service areas (ranked first and fifth in Table 3) did not designate a person for tracking FIT-positive participants, neither routinely evaluated follow-up metrics, and only 1 directly accessed FIT-positive results.
Over 10 years, KPNC implemented several system-level strategies to improve FIT-positive follow-up rates, including establishing a 30-day goal for colonoscopy follow-up of positive FIT results, increasing colonoscopy capacity, developing a registry add-on to the electronic health record, and initiating early telephone contact with all test-positive participants. The system-wide implementation of these strategies coincided with substantial and significant improvements in timely colonoscopy follow-up between 2006 and 2016, with 84% of test-positive participants receiving a colonoscopy within 180 days of their FIT-positive result in 2016. However, for 2016, we did not find any obvious patterns suggesting that higher performing service areas had implemented specific strategies or a greater number of strategies.
Follow-up colonoscopy rates after positive stool tests vary widely by setting, but little is known about what differentiates programs with higher vs lower follow-up rates. Several US publications have reported 50%–60% follow-up rates after 6 months or 1 year, with gaps in care at multiple levels, including fecal testing of participants for whom colonoscopy is not appropriate because of age and comorbidities; primary care providers repeating fecal testing or failing to refer to gastroenterology departments; participants failing to present for colonoscopy; and system failures to track participants and adequately document reasons for not coordinating follow-up (10,12,22,28). A recent study reported marked differences in time to colonoscopy after a positive FIT between 4 health systems, including KPNC (11). The authors speculated that better rates of follow-up at KPNC vs 2 other integrated health systems (81% colonoscopy completion at 6 months vs 74% and 63%, respectively) might have been due to system-level factors, such as goal setting, regular performance monitoring, and control over colonoscopy capacity. KPNC chose a 30-day follow-up goal to minimize participant anxiety (consistent with European guidelines (6)) and to promote efficient processes of care. Recent research suggests that follow-up within 180 days after a positive FIT is not associated with adverse CRC outcomes (8), although no consensus exists on the appropriate follow-up interval. The fourth health system, a county-wide safety-net system, had only 50% follow-up at 6 months; the study authors speculated that the absence of a patient registry, inadequate colonoscopy capacity, and patient-level differences may have been contributing factors. Rates of colonoscopy follow-up within 6 months of >80% have been reported by several international organized screening programs, including a regional program in Italy with follow-up rates over 90% (29). These programs typically inform both participants and providers of FIT results by letter and/or telephone and manage colonoscopy appointments centrally, allowing for direct booking of colonoscopies when reporting test results (17,29,30). Early contact with all FIT-positive participants, as was done at KPNC, may partly explain the higher follow-up rates (31). Follow-up rates may also be lower in health systems with high rates of opportunistic screening colonoscopy, like many US programs; FIT in these settings may be more likely to be completed by participants reluctant to undergo colonoscopy.
Several of the strategies implemented within KPNC between 2006 and 2016 have been reported to be effective in other settings. A systematic review found moderate evidence supporting patient navigators, usually nurses, and reminders to primary care providers to complete colonoscopy referrals for FIT-positive participants (18). In the present study, most telephone contacts with FIT-positive participants were made by medical assistants or schedulers, typically using standardized scripts to educate and motivate patients, similar to randomized trials with nurse navigators (32,33) In 2 service areas, primary care departments tracked FIT-positive participants and reminded physicians to contact their patients and complete referrals; in the other service areas, staff in gastroenterology departments directly contacted participants to convey results and make electronic referrals, eliminating the need for primary care provider reminders. Two previous studies reported that automatic electronic referral to gastroenterology increased follow-up (34,35). Research from the Veterans Affairs health system found that direct referral to gastroenterology and adequate colonoscopy capacity were associated with shorter times to colonoscopy (20,36). Finally, another US health system achieved follow-up rates of over 80% with a registry and manual nurse audit (37).
Strengths of our study include a systematic qualitative and quantitative evaluation of practice variation within a large, multicenter, diverse community-based setting; evaluation of both system-wide and local strategies to improve follow-up; comprehensive follow-up of many FIT-positive participants; linkage of practice variation with patient outcomes; and the ability to track the same outcome while adjusting for participant characteristics over the study interval.
Limitations include the retrospective observational design, which decreased precision regarding the timing of each strategy's implementation, and the overlap of strategy implementation across service areas, which prevented a rigorous evaluation of the individual influences of the multiple strategies implemented. These factors, and the potential that unmeasured temporal changes could have influenced the results, preclude definitive assessments of causality. For example, we did not ask about the practice of maintaining open colonoscopy slots for semiurgent colonoscopy indications like positive FIT; this approach could decrease colonoscopy wait times (38). In attempting to capture the strategies implemented over time across service areas, we relied on information obtained from gastroenterology department leaders rather than measurable activities of the staff involved (e.g., medical assistant/registered nurses). As such, the findings could be subject to recall bias, and although if nondifferential, the resulting misclassification would be expected to bias results toward the null. Our analyses focused on the role of gastroenterology departments in facilitating follow-up because this was a KPNC-wide emphasis; however, primary care departments may have played a greater role in follow-up, which could have confounded our results. The misclassification of service areas would be expected to be nondifferential, leading to a potential bias toward the null. Our observations are from a single, large health system with an organized screening program, which may limit generalizability to smaller programs or individual practices. However, the impressive improvements in colonoscopy follow-up over time, combined with high plausibility regarding potential effects of the implemented strategies described, suggest that these strategies may be useful for consideration by other FIT programs. Finally, we did not measure the proportion of FIT-positive participants for whom follow-up colonoscopy was inappropriate, either because of a recent normal colonoscopy, informed refusal, or severe comorbidities, and thus may have underestimated the proportion of participants receiving appropriate timely follow-up.
Timely follow-up of positive tests is a critical component of effectiveness for FIT-based CRC screening programs. This large, multicenter qualitative and quantitative study of pragmatic strategies coinciding with improvements in FIT follow-up complements results from small randomized trials and supports goal setting for colonoscopy completion, electronic tracking of participants with positive FITs, organized (including dedicated personnel) primary care provider–directed evaluation/referral or direct referral to gastroenterology for colonoscopy, and scaling of colonoscopy capacity as potential fruitful strategies for improving timely follow-up of FIT-positive participants. Future intervention studies in multiple settings are needed to measure the potential beneficial effects of implementing individual strategies.
CONFLICTS OF INTEREST
Guarantor of the article: Kevin Selby, MD, MAS, accepts full responsibility for the conduct of the study, had access to the data, and had control of the decision to publish.
Specific author contributions: Planning and/or conducting the study: K.S., J.K.L., J.E.S., T.R.L, and D.A.C. Collecting and/or interpreting data: K.S., C.D.J., W.K.Z., and A.S. Statistical analysis: K.S., C.D.J., and P.B. Drafting the manuscript: K.S., C.D.J., J.K.L., J.E.S., T.R.L., and D.A.C. All authors approved the final draft submitted.
Financial support: This study was conducted as part of the National Cancer Institute–supported PROSPR network (U54 CA163262 [D.A.C.]). K.S. received funding from the Swiss Cancer Research Foundation (BIL KFS-3720-08-2015). J.K.L. received funding from the National Cancer Institute (K07 CA212057). The funding sources had no role in the design and conduct of the study, preparation of the manuscript, or decision to publish.
Potential competing interests: None.
WHAT IS KNOWN
- ✓ Rates of timely colonoscopy follow-up after a positive FIT for screening are as low as 50% in some settings
- ✓ The risk of CRC increases with colonoscopy delays of more than 180 days after a positive FIT
WHAT IS NEW HERE
- ✓ The implementation of several system-level strategies coincided with improved timely follow-up including setting a 30-day goal for follow-up, tracking FIT-positive participants, early telephone contact to schedule colonoscopies, and increasing colonoscopy capacity.
- ✓ Over a 10-year period, rates of colonoscopy follow-up within 180 days after a positive FIT improved from 67% to over 80%; intervention studies are needed to identify the most effective strategies for promoting timely follow-up.
✓ Multiple system-level interventions likely improve timely colonoscopy completion after positive FIT.
We thank the gastroenterology department chiefs and staff in Kaiser Permanente Northern California for sharing their time and insights.
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