1 Introduction

Cancer screening plays a pivotal role in disease prevention and early detection, significantly contributing to reduced cancer mortality and the mitigation of overall life expectancy loss. The effectiveness of screenings for cancers such as colorectal, cervical, and breast cancer has been well established through numerous studies, prompting both nationwide and municipal implementation efforts [1-3]. Effective cancer screening necessitates a well-managed system, tests with high sensitivity and specificity, and seamless integration with follow-up treatment [4, 5]. Among these factors, the participation rate of the target population in screenings is a crucial indicator, prompting efforts to identify barriers and enhance participation rates [6]. However, such cancer screening initiatives are known to be vulnerable to large-scale disasters and significant social changes. For example, following the Great East Japan Earthquake, the participation rates for colorectal and breast cancer screenings significantly declined in the most affected areas over several years [7, 8]. Understanding these declines and implementing appropriate countermeasures is vital.

The COVID-19 pandemic, which emerged in early 2020, caused a global public health crisis. Besides the direct increase in infections and deaths due to the virus, the pandemic brought about significant public health challenges through social isolation measures and restricted access to healthcare facilities [9-11]. The impact on cancer care has been particularly concerning, with reports from the UK indicating a decrease in new diagnoses for most solid tumors in 2020. Specifically, the short-term prognosis for colorectal cancer (CRC) worsened, highlighting the need for enhanced screening and diagnostic measures [12]. The continued decline in CRC screening rates remains a significant issue, with reports indicating that, as of 2022, screening rates at federally qualified health centers in the United States had not returned to pre-pandemic levels [13]. Addressing this situation with effective measures is crucial.

In Japan, a nationwide state of emergency was declared from late April to early May 2020, restricting inter-prefectural movement [14]. However, the actual surge in COVID-19 cases occurred towards the end of 2020, with intermittent outbreaks continuing thereafter, leading the Japanese government to issue region-specific states of emergency four times by September 2021. During this period, many healthcare facilities prioritized COVID-19 responses, leading to interruptions or delays in cancer screenings in several municipalities. Residents were advised to avoid non-essential outings and were reluctant to visit hospitals for fear of contracting COVID-19, further suppressing healthcare-seeking behaviors [15]. Consequently, there are concerns about an increase in advanced-stage cancers detected through screenings since the pandemic began [16, 17]. In response to the prolonged pandemic, the government has urged residents to continue necessary medical visits and cancer screenings, despite the ongoing crisis. Given this context, it is presumed that public perception of cancer screenings has evolved throughout the pandemic, but detailed analyses of the changes in screening behaviors in Japan are limited.

The aim of this study was to identify factors related to non-participation in CRC during the pandemic, focusing on changes in CRC screening behaviors in 2020 and 2021.

2 Method

2.1 Setting and Participants

We utilized data from the Japan COVID-19 and Society Internet Survey (JACSIS) study. JACSIS is a large-scale annual internet survey conducted during the pandemic, capturing changes in health behaviors and identifying relevant factors, designed to estimate nationwide representative values [18, 19]. The survey is administered by an internet survey company (Rakuten insight marketing Inc., Tokyo, Japan) with approximately 2.2 million panelists and conducted online from September to October each year. In these surveys, potential participants were selected based on stratification by gender, age, and their prefecture of residence to ensure a sample that is as representative of the national population as possible. Participants are typically re-invited from year to year, ensuring consistency in the survey cohort. Respondents were compensated with a small incentive for completing each survey. In this study, we focused on respondents who participated in both the surveys conducted from September to October 2021 and from September to October 2022. Out of the 31,000 respondents in 2021 and 32,000 respondents in 2022, we excluded invalid responses and created a panel data set of 19,482 individuals who participated in both surveys (Figure 1). Of these, we analyzed 13,261 individuals aged 40 to 74, who were the target for colorectal cancer screening in 2021 (Figure 1).

3 Result

3.2 Participation Rates in 2021 and 2022

In 2021, 5367 participants (40.5%) reported undergoing colorectal cancer screening. Among the 7894 participants (59.5%) who did not undergo screening, 1899 (14.3%) reported inability to screen due to reasons unrelated to COVID-19, yet intended future participation, while 1216 (9.2%) cited COVID-19-related reasons but planned to undergo screening later, 2463 (18.6%) could not screen for reasons unrelated to COVID-19 and did not intend to screen in the future, and 2316 (17.5%) cited COVID-19-related reasons and did not intend to screen in the future. In 2022, 6456 participants (48.7%) reported undergoing colorectal cancer screening. Among the 6805 participants (51.3%) who did not screen, 1786 (13.5%) cited reasons unrelated to COVID-19 but intended to screen in the future, 791 (6.0%) cited COVID-19-related reasons but intended to screen in the future, 2559 cited reasons unrelated to COVID-19 and did not intend to screen in the future, and 1669 (12.6%) cited COVID-19-related reasons and did not intend to screen in the future. Figure 2 illustrates the matrix of these responses. Of those screened in 2021, 4335 participants (80.8%) also underwent screening in 2022 (refer to Figure 2, column A). Of the 3115 participants who did not screen in 2021 but intended to (columns B and C of Figure 2), 1098 (35.2%) screened in 2022. Conversely, of the 4779 participants who did not screen in 2021 and did not intend to screen thereafter (columns D and E of Figure 2), 1023 (21.4%) screened in 2022. Those who cited COVID-19-related reasons for not screening and not intending to screen thereafter were more likely to screen in 2022 compared to those citing non-COVID-19-related reasons (18.0% vs. 25.0%, p < 0.05). Table S1 shows the screening rates in 2022 by various attributes.

4 Discussion

This study conducted a detailed analysis of involvement in CRC screening during the COVID-19 pandemic through a large-scale, two-year survey. Utilizing panel data, we examined trends in CRC screening uptake and found that the overall participation rate increased from 2021 to 2022. Interestingly, the inability to undergo screening in 2021 due to COVID-19 appeared to motivate participation in 2022, suggesting a reduction in the pandemic's impact on CRC screening. However, the majority of individuals who did not undergo screening in 2021 also refrained from participating in 2022, indicating that screening behaviors tend to become entrenched. These findings highlight the impact of COVID-19 on CRC screening and emphasize the need for targeted interventions for populations that remain unscreened.

This study suggests that the impact of COVID-19 on CRC screening lessened from 2021 to 2022. In this survey, 38% of respondents reported participating in CRC screening regularly and 19.6% irregularly before COVID-19. However, in 2021, 40.5% and in 2022, 48.7% reported actually attending the screenings. Similarly, a nationally representative survey conducted by the Ministry of Health, Labour and Welfare shows that colorectal cancer screening uptake in Japan slightly increased from 47.8% to 49.1% among males and from 40.9% to 42.8% among females between 2019 and 2022 [22]. While this reflects a modest national recovery, the more pronounced increase observed in our study suggests that certain populations may have experienced a more substantial rebound in screening participation. It is noteworthy that a significant number of individuals reported being unable to undergo CRC screening in 2022 due to the pandemic. Many countries have reported a decrease in CRC screening participation rates during the peak of the COVID-19 pandemic, noting declines especially in early 2020, followed by subsequent recoveries. For example, an Italian study noted a 5.1% decrease in participation rates during the peak period from January to March 2020, but rates returned to 2019 levels once screening activities resumed [23]. Similarly, in the United States, the number of fecal occult blood tests performed returned to 2019 levels by September 2020 [24]. Conversely, long-term impacts on screening trends have also been reported. In Canada, CRC screening participation in 2022 was still down by 4% compared to pre-pandemic levels [25]. These differences in impact are likely due to variations in the COVID-19 pandemic's status and the corresponding healthcare policies in each country. Our study also shows that while CRC screening rates in Japan are on a recovery trend, the impact of the pandemic persisted into 2022, highlighting the need for ongoing interventions. Notably, 65% of individuals who intended to undergo CRC screening in 2021 but did not, also did not undergo screening in 2022. Identifying the barriers preventing these groups from participating in screening is crucial for improving screening rates.

This study's finding that social factors such as age and work environment are associated with adherence to fecal occult blood screening aligns with previous research. Generally, it is known that individuals with lower educational levels, poverty, poor employment conditions, and younger age are less likely to participate in CRC screening [26]. In Japan, CRC screenings are often provided at workplaces alongside public health screenings, making the influence of occupation and income particularly pronounced during the COVID-19 pandemic. In fact, when analyzed by age group in the current study, the negative association of unemployment with screening participation was more pronounced among those in their 40s–60s, the working age group. Furthermore, the finding that men were more likely to undergo CRC screening in this study contrasts with previous reports suggesting that women are more likely to participate in the screenings [27]. Reports in Japan have also indicated that men are less likely to participate in CRC screenings compared to women [7]. On the other hand, our findings are consistent with trends observed in the Ministry of Health, Labour and Welfare's national health survey, which reports higher screening rates among men for stomach, lung, and colorectal cancer [22], while the survey provides only descriptive data without statistical analysis. Further research is needed to investigate the factors influencing gender differences in participation across these screening programs. In addition, it remains unclear whether the impact of socioeconomic status on CRC screening has changed before and after the pandemic. Globally, studies have reported both an increase in disparities due to COVID-19 and a narrowing of pre-existing gaps [28]. This study did not consider the impact of job losses or changes in work patterns, including remote work, during the pandemic, representing a limitation that future research should address. Analyzing changes in the influence of social factors on CRC screening participation in Japan during the pandemic is crucial for developing strategies to improve screening rates.

This study reveals that prior participation in screenings and the intention to participate in future screenings are strongly associated with subsequent screening participation. It may also highlight the fixed nature of groups who either consistently undergo CRC screening or consistently do not, even during the COVID-19 pandemic. These findings align with previous research indicating that knowledge about CRC and screenings, as well as a lack of trust in healthcare providers, can significantly impact an individual's willingness to undergo screenings, potentially affecting lifetime adherence to CRC screening [29]. The Japanese government and the Ministry of Health, Labour and Welfare have set a target CRC screening rate of 80%. To achieve this goal, it is crucial to focus on engaging those who consistently do not participate in CRC screenings. Analyzing trends in CRC screening participation and the factors influencing it, and then implementing personalized messaging to encourage participation [30], may be an effective approach.

This study has several limitations. First, since the survey collected information on screening status for the year prior to the response, the impact of the COVID-19 pandemic during its peak from March to May 2020 may be underestimated. Second, as the study focused on trends in fecal occult blood testing, it may not have adequately adjusted for the influence of other screening methods, such as past colonoscopies. However, by collecting information on respondents' medical histories and healthcare visits, the analysis attempts to account for these effects. Third, the reasons for not undergoing CRC screening related to COVID-19 include subjective elements and, finally, the survey is online self-reported; there are potentials for response bias and inaccuracy, and results may not be representative of the broader population. Fourth, the sample may not fully represent the general population, as most respondents were educated beyond high school, earned over 3 million Yen, and were internet users due to the online survey format. These factors may influence health behaviors and limit the generalizability of the findings. Nonetheless, the aim of this study is to understand how participants perceive these reasons in relation to their screening behavior.

5 Conclusion

A two-year survey revealed an increasing trend in CRC screening rates from 2021 to 2022. However, even in 2022, many respondents cited the COVID-19 pandemic as a reason for not participating in CRC screening, indicating concerns about its long-term impact. This study highlights the persistent segmentation of groups regarding CRC screening participation. Identifying the factors contributing to this fixed pattern and devising appropriate interventions are crucial for selecting suitable target groups for intervention.

Author Contributions

Hiroaki Saito: conceptualization (equal), data curation (equal), formal analysis (equal), methodology (equal), writing – original draft (equal). Aminu Kende Abubakar: formal analysis (equal), writing – original draft (equal). Akihiko Ozaki: conceptualization (equal), writing – review and editing (equal). Daisuke Hori: validation (supporting), writing – original draft (supporting), writing – review and editing (supporting). Michio Murakami: methodology (equal), supervision (equal), writing – review and editing (equal). Yudai Kaneda: writing – review and editing (equal). Masaharu Tsubokura: writing – review and editing (equal). Takahiro Tabuchi: funding acquisition (equal), project administration (equal), resources (equal), supervision (equal), writing – review and editing (equal).

Ethics Statement

Ethical approval to conduct the present study was obtained from the ethics committee of the Osaka International Cancer Institute (approval number: 20084-6). All procedures were performed in accordance with the ethical standards of the institutional and/or national research committees and the Declaration of Helsinki and its later amendments, or comparable ethical standards.

Consent

All participants provided web-based informed consent at registration.

Conflicts of Interest

A.O. receives personal fees from MNES Inc. and Kyowa Kirin Inc. A.O. and H.S. received personal fees from Taiho Pharmaceutical Co. Ltd. outside the submitted work. The other authors declare no conflicts of interest.