This analysis of the short-term effects of the lockdown during the first wave of the COVID-19 pandemic on a programmatic FIT-based CRC screening showed a temporary decrease in participation but a large decrease in adherence to diagnostic colonoscopy. The mean time to the performance of colonoscopy for individuals with FIT-positive disrupted by the pause of CRC screening rose threefold compared to the mean in the previous year. While no differences in distress levels were found in individuals with a positive FIT result pending colonoscopy compared to individuals with a negative FIT result during the lockdown, greater perceptions of emotional well-being affected by COVID-19 were associated with increased levels of psychological distress in CRC screening participants.
The global decreases of 5% in participation among invitees during the first quarter of 2020 compared to previous years are in line with a recent study conducted in Northern Taiwan, where a slight decrease of 3.5% in the FIT screening uptake rate was observed during the first wave of COVID-19 compared to that in previous years [3]. Participation rates since resuming seem to be recovered. However, the COVID-19 era could bring an opportunity to programs with low participation rates (< 45%) to implement innovations such as social media campaigns to boost cancer screening participation [13, 14]. In this sense, our findings show that participation among individuals who received SMS reminders after resumption of screening was twice as high as in individuals where SMS failed.
A major concern from our study is the decrease observed in colonoscopy adherence rates among individuals invited during the first quarter of 2020 when compared to the previous year. Individuals with a positive FIT result have a high risk of advanced neoplasm; therefore, a decrease in diagnostic colonoscopy adherence can result in worse health outcomes [15, 16]. Fear of contracting COVID-19 in health care settings has been widely reported; specifically, in the context of screening, previous studies have shown that 50% of colonoscopies after a positive FIT result were refused because of fear of contracting COVID-19 during the first wave [3]. We are unable to determine whether the decrease in colonoscopy adherence was due to the endoscopic units (fewer attempts to locate patients) and/or was due to the individuals' fear of being infected by the COVID. The work of ensuring that individuals understand the importance of the positive FIT result and the reassurance that the colonoscopy procedure will be performed safely is key in conducting a FIT-based CRC screening program.
As expected, the mean time to performance of the colonoscopy among FIT-positive individuals affected by the pause of the program was three times longer than usual. When resuming colonoscopies, we established a prioritization criterion stratified by fecal hemoglobin concentration levels, which is strongly associated with the likelihood of having advanced neoplasm at colonoscopy. To safeguard the capacity of the endoscopy units during the next outbreaks of COVID-19, the program increased the FIT cutoff point to 31 µg Hb/g feces, thus decreasing the number of screening colonoscopies by 25%. A negative consequence to be monitored is the expected loss of 6% of CRC diagnoses and 20% of high-risk adenomas.
Our findings show that in comparison to individuals with a negative FIT result, individuals with a positive FIT result did not report increased levels of psychological distress preceding colonoscopy. Although distress levels may be elevated if individuals do not fully understand the meaning of the screening test results, no differences in distress levels were found in our study. Among all interviewees, the levels of distress were higher in those individuals, whose emotional well-being was greatly interfered with by the COVID-19 pandemic, illustrating the associated fear and the competing health risks during the first wave. Previous studies have shown increased psychological distress levels after a positive FIT result and that levels of distress decreased after a confirmatory diagnostic procedure; therefore, it is imperative to guarantee that the time between procedures is as short as possible [5, 17].
The limitations of the study include potential selection bias. When evaluating psychological distress, we only considered individuals with a scheduled colonoscopy in June-September 2020. A total of 120 individuals did not undergo colonoscopy in our endoscopic units. Of those, approximately 34% underwent colonoscopy at a private center, 25% could not be reached by the endoscopy nurse, and 41% refused their colonoscopy. We cannot rule out that individuals who refused to undergo colonoscopy had a higher level of psychological distress than their counterparts who agreed to receive a colonoscopy. If any, the effect size would be small.
During the first wave of COVID-19, nearly a quarter of our target population was not invited due to the pause of CRC screening (approximately 111,000 individuals). From those, around 45,500 individuals would have completed the FIT at home, of which 5.1 % would have had a FIT-positive screening, and around 3.8% of those will have CRC. This equates to 88 undiagnosed CRC cases due to the screening pause. Additionally, more than 943 people will have advanced adenomas undetected, with a 2.6 to 4.2% [18] annually transition to CRC if not removed. To minimize the long-term impact of the COVID-19 pandemic on CRC screening, strategies should be implemented to reduce the screening backlog while considering endoscopic capacity constraints. A range of strategies are possible, from skipping one screening round for those affected by the pause to implementing catch-up. In the latter case, it would be important to shorten recovery time as much as possible, for instance, by increasing FIT positivity threshold [19–21]. To maximize diagnostic yield with limited endoscopic capacity, we could also consider prioritizing colonoscopies after a FIT positive result rather than post-polypectomy surveillance colonoscopies due to their greater benefits [22].
The efforts of the COVID-19 and Cancer Global Modelling Consortium (ccgmc.org) to simulate different scenarios of recovery strategies for cancer screening are noteworthy. However, real-world data could be useful to validate the calibrated models in different settings to facilitate decision-makers to choose the best recovery strategy for their screening programs.