Attitudes toward cancer screening in regional Japan during the COVID-19 pandemic: An anonymous survey

Abstract

The coronavirus disease (COVID-19) pandemic has raised concerns about the impact of delayed health check-ups and cancer screenings on cancer diagnosis and treatment. This study aimed to investigate the awareness of cancer patients on future screening measures during the pandemic in rural Japan. An anonymized open-data survey was undertaken in Fukui Prefecture, a rural region of Japan, in 2021. Participants were asked about their cancer screening history, screening frequency during the pandemic, and reasons for not undergoing screening. Among the 1262 respondents, the proportion of patients who underwent cancer screening in 2020 during the pandemic was similar to the proportion who underwent regular (annual or biannual) screening in 2019 before the pandemic. Of those who underwent regular screening, 82% still underwent screening in 2020, while only 21% of those who had irregular screenings. The number of respondents who believed they were healthy and did not require screening increased over time, possibly due to restrictions on going out and refraining from activities during the pandemic. This study in rural Japan found that regular cancer screening prior to the pandemic was associated with a more positive attitude toward screening during the pandemic. Raising awareness about the importance of cancer screening and encouraging participation is crucial for promoting positive attitudes in the future. The findings highlight the need for continued efforts to ensure access to screening services during the pandemic and future public health emergencies.

INTRODUCTION

Coronavirus disease (COVID-19) continues to be a public health emergency in the 21st century, having caused over 6 million deaths and nearly 800 million cumulative cases worldwide since the pandemic was declared.¹ At a global level, nonurgent medical services such as cancer screening have been restricted to reduce the risk of COVID-19 infection and the burden on health services.^2–5 In this context, the American Cancer Society published a recommendation that individuals postpone routine cancer screening and not go to a health-care provider until a later date.⁴ At the same time, individuals have been hesitant to access health-care services and participate in screening programs, fearing COVID-19 infection.^2,3 A recent meta-analysis has reported a significant decrease in cancer screening for breast, colorectal, and cervical cancer during the COVID-19 pandemic based on six studies on breast cancer, five on colorectal cancer, and three on cervical cancer. Compared to the pre-COVID-19 baseline, mammography screening decreased by 63%, colonoscopy screening by 11%, and cervical cancer screening by 10%.⁶ Although mortality data on the reduction in screening during the pandemic are not yet available, the potential increase in mortality is likely to be a global public health issue.

In Japan, the cancer screening uptake rate declined after the government declared the first state of emergency on March 13, 2020, imposing behavioral restrictions. The Japan Cancer Society undertook a questionnaire survey on the number of people who received five cancer screenings (lung, stomach, colon, breast, and cervical) in 2021 and compiled the results. The results showed that the number of people examined in 2020 decreased by 27.4% compared to 2019.⁷ Based on this and other factors, the Ministry of Health, Labor, and Welfare issued a notice on April 26, 2021, titled “The response in cancer screening in light of the declaration of a state of emergency for COVID-19.” The content of the notice emphasized that cancer screening is effective in reducing cancer mortality, and it is desirable to uptake cancer screening at the conventional screening intervals in accordance with the guidelines. Cancer screening is not considered a “nonessential and nonurgent outing” requiring self-restraint in areas where a state of emergency has been declared.⁸

Health literacy has been defined as the cognitive and social skills that determine the motivation and ability of individuals to gain access to, understand, and use information in ways that promote and maintain good health.⁹ It has been reported that lack of health literacy tends to be associated with lower uptake of cancer screening behaviors.^10–13 In Japan, evidence-based cancer screening is recommended,^14–16 and conducted by municipalities and includes individual and group screening, as well as workplace screening. The age and interval of screenings are as follows: (1) biannually for stomach cancer at age 50 or older, (2) annually for lung cancer at age 40 or older, (3) annually for colorectal cancer at age 40 or older, (4) biannually for breast cancer at age 40 or older, and (5) biannually for cervical cancer at age 20 or older.

Several studies have examined cancer screening participation rates and activities and cancer screening status during epidemic processes.^3–5 It was reported that 26.3% of women aged 30–79 years postponed or stopped breast cancer screening in Japan due to the pandemic, and one in four women postponed screening during the pandemic.¹⁷ However, there are no studies in Japan that have clarified the reasons why local residents in rural areas do not receive screening during the risk of COVID-19 infections, nor their attitudes toward health literacy and screening.

In 2020, due to the postponement or avoidance of cancer screening during the COVID-19 pandemic, the number of individuals undergoing cancer screening in Fukui Prefecture decreased by 16.9% compared to previous years. Delaying health checkups and cancer screenings would delay disease detection and prevent patients from receiving appropriate treatment at the right time. Therefore, we undertook a survey on the status and awareness of cancer screening during the COVID-19 pandemic for future cancer screening measures.

MATERIALS AND METHODS Data

This study utilized anonymized data from a survey undertaken by the Fukui Prefecture Department of Health and Welfare in June 2021. The survey was carried out anonymously, and the results were compiled as statistical data. The survey was commissioned by Fukui Prefecture and carried out by the Fukui Information Technology Association. A random sample of 2500 subjects was selected from the basic resident ledger. In this study, we adopted a stratified sampling approach to ensure a more balanced representation of participants across different demographic variables. Specifically, our resident ledger was divided into distinct strata based on age groups, sex, and living municipalities of residence. Within each stratum, we then randomly selected participants to ensure a proportionate representation from each subgroup. This stratified random sampling technique resulted in a diverse and representative sample. The survey was carried out free of charge and did not require respondents to provide their names. The survey form and return envelope did not require any personal information. Respondents were asked to select the applicable numbers.

Survey questions

The survey questionnaires can be referenced in Data S1. In this questionnaire, regular screening visits were defined as adherence to the recommended screening intervals for each type of cancer screening (e.g., annual screening for lung and colorectal cancers and biannual screening for cervical, breast, and stomach cancers).

Statistical analysis

To examine the relationship between the frequency of cancer screenings up to 2019 and cancer screenings in 2020, as well as the relationship between the locations of cancer screenings up to 2019 and those in 2020, we used χ²-tests and Fisher's exact tests. We also undertook analyses to investigate the relationships between reasons for receiving cancer screenings in 2020 and reasons for planning to receive cancer screenings in 2021, as well as the reasons for not receiving cancer screenings in 2019, 2020, and 2021. In addition, we explored the relationship between the frequency of screenings up to 2019 and reasons for not receiving screenings in 2020. Furthermore, we carried out these analyses separately for men and women. The level of statistical significance was set at less than 5%. IBM SPSS Statistics 28 (IBM) was used for all statistical analyses.

RESULTS

A total of 1262 respondents (50.5%) completed the survey. The respondents’ backgrounds are shown in Table 1. Those who reported having undergone cancer screening in fiscal year 2020 (April 1–March 31), when COVID-19 spread, were similar in proportion to those who had undergone screening regularly by 2019, before the spread of the disease. The number of those who did not receive cancer screenings was approximately the same as the total of those who had received cancer screenings irregularly before the spread of the disease and those who did not receive cancer screenings. However, the number of those who planned to receive cancer screenings in 2021 increased (Table 2). Of those who were screened regularly, 82% continued to be screened even during the COVID-19 pandemic. However, among those who had undergone cancer screening irregularly, only 21% of those with COVID-19 did so, showing a significant difference in the uptake rate (p < 0.001) (Table 3). Regarding the location of cancer screening, there was a decrease in the number of people who received cancer screening at group screening sites when comparing 2019 and 2020 (p = 0.001) (Table 4). Comparing the reasons for receiving cancer screening in 2020 with the reasons for wanting to receive cancer screening in 2021, there was an increase in the number of people who did not receive screening in the previous year (Table 5). The reasons for not undergoing cancer screening were compared for the 3 years 2019, 2020, and 2021. Concern about the spread of new COVID-19 infections decreased from 2020 to 2021 (21.0% vs. 16.3%, p = 0.032). Additionally, the number of respondents who believed they were healthy and did not need to be screened increased over the years (19.9% vs. 26.2% vs. 32.7%, p < 0.001) (Table 6). The reasons for not undergoing cancer screening in 2020, early in the COVID-19 pandemic, were compared between the groups that received screening regularly and those who received it irregularly. The main reason for not undergoing screening was concern about COVID-19 infection in both groups. The reason “No need because I am healthy” was significantly more common in the irregular screening group (20.9% vs. 7.8%, p = 0.005). The irregular screening group was also more concerned about the high cost of screening than the regular screening group (14.0% vs. 4.4%, p = 0.013). In addition, inadequate infection control measures was cited more often as the reason for not undergoing cancer screening among the regular screening group compared to the irregular screening group (8.9% vs. 1.8%, p = 0.004) (Table 7). The most frequently cited reason for encouraging cancer screening participation among individuals who did not plan to undergo screening in 2021 was “personal health concerns.” The second most common reason was “demise of COVID-19” (Table 8).

TABLE 1 Background of the study cohort of residents of Fukui Prefecture, Japan, 2021

Number of respondents n (%)	Total	Male	Female	Unknown
	1262	561 (44.4)	681 (54.0)	20 (1.6)
Age (years)
20–29	35 (2.8)	16 (45.7)	19 (54.3)	0 (0.0)
30–39	123 (9.7)	50 (40.7)	73 (59.3)	0 (0.0)
40–49	247 (19.6)	104 (42.1)	143 (57.9)	0 (0.0)
50–59	282 (22.3)	120 (42.6)	159 (56.4)	3 (1.1)
60–69	283 (22.4)	128 (45.2)	150 (53.0)	5 (1.8)
>70	279 (22.1)	138 (49.5)	130 (46.6)	11 (3.9)
No response	13 (1.0)	5 (38.5)	7 (53.8)	1 (7.7)

TABLE 2 Cancer screening status of the study cohort before, in the early stage, and during the COVID-19 pandemic.

Status of cancer screening	Number of respondents, n (%)
	Total	Male	Female	Unknown
2019, prepandemic
Regularlya	531 (42.1)	210 (37.4)	315 (46.3)	6 (30.0)
Irregularly	357 (28.3)	108 (19.3)	244 (35.8)	5 (25.0)
Never	332 (26.3)	224 (39.9)	102 (15.0)	6 (30.0)
No response	42 (3.3)	19 (3.4)	20 (2.9)	3 (15.0)
2020, early pandemic
Underwent	531 (42.1)	223 (39.8)	303 (44.5)	5 (25.0)
Did not undergo	686 (54.4)	317 (56.5)	356 (52.3)	13 (65.0)
No response	45 (3.6)	21 (3.7)	22 (3.2)	2 (10.0)
2021, pandemic
Willing to undergo	611 (48.4)	238 (42.4)	365 (53.6)	8 (40.0)
Undecided	380 (30.1)	171 (30.5)	205 (30.1)	4 (20.0)
Do not intend to undergo	232 (18.4)	132 (23.5)	94 (13.8)	6 (30.0)
No response	39 (3.1)	20 (3.6)	17 (2.5)	2 (10.0)

^a“Regularly” is defined as following the recommended screening intervals (annual or biannual) for each cancer screening type.

TABLE 3 Cancer screening rates in 2020 by frequency of screening prior to the COVID-19 pandemic.

[Table omitted. See PDF]

^a“Regularly” is defined as following the recommended screening intervals (annual or biannual) for each cancer screening type.

TABLE 4 Changes in cancer screening locations from pre-COVID-19 pandemic (up to 2019) to early pandemic (2020).

[Table omitted. See PDF]

TABLE 5 Changes in reasons for undergoing cancer screening in 2020 (early pandemic) and 2021 (pandemic).

[Table omitted. See PDF]

^a“Regularly” is defined as following the recommended screening intervals (annual or biannual) for each cancer screening type.

TABLE 6 Changes in reasons for not receiving cancer screening in 2019 (pre-COVID-19 pandemic), 2020 (early pandemic), and 2021 (pandemic).

[Table omitted. See PDF]

Abbreviation: NA, not applicable.

TABLE 7 Reasons for missed cancer screening during early COVID-19 pandemic (2020) by prepandemic (2019) screening frequency.

[Table omitted. See PDF]

Abbreviation: NA, not applicable.

^a“Regularly” is defined as following the recommended screening intervals (annual or biannual) for each cancer screening type.

TABLE 8 Encouraging factors for cancer screening participation in the future.

Conditions for receiving cancer screening	Number of respondents, n = 612
	n (%)
Personal health concerns	268 (43.8)
Demise of COVID-19	120 (19.6)
Vaccination	87 (14.2)
Safe screening sites	61 (10.0)
Others	60 (9.8)

DISCUSSION

This study aimed to investigate the attitudes of cancer screening recipients during the COVID-19 pandemic and provide insights for future cancer screening uptake measures in rural Japan. It is noteworthy that in the early phase of the pandemic in 2020, 82% of individuals who had previously undergone regular cancer screenings up to 2019 continued to undergo screening, while only 21% of those who undertook screening irregularly up to 2019 underwent cancer screening. Fear of COVID-19 infection was cited as the reason for not being screened by 32% of those in the regular screening group and 27% of those in the irregular group.

There are many studies reporting that cancer screening was postponed or discontinued due to the concerns about the potential higher risk of COVID-19 during the screening process.^2–4,18 This suggests that it is important to minimize the perceived risks associated with cancer screening. This is reflected in the results of an awareness survey, which found that individual and workplace examinations are preferred over group examinations, which carry a relatively high risk of infection. Therefore, it is important to install personal protective equipment in examination rooms, arrange waiting rooms in such a way that physical distancing can be maintained, prevent crowding, introduce an appointment system, individually assess COVID-19 symptoms before the examination, conduct rapid tests for COVID-19 detection, and perform sterilization and disinfection treatments at regular intervals.¹⁹ It has been reported that making the screening environment safe for those who do not undergo screening or delay it due to fear of infection can increase their willingness to participate in the screening process.^13,18 Currently, a survey regarding people's plans to receive cancer screening in 2021 has shown a decrease in fear of COVID-19 infection and an increase in the number of people who want to receive it.

One of the most concerning findings of our study is the increasing trend of individuals choosing not to undergo cancer screening due to the belief that they are healthy (Table 6). On the other hand, it is interesting to note that even during the COVID-19 pandemic, more people are intending to undergo cancer screening next year because they were not screened last year (Table 5). Previous studies highlight the influence of individuals' health literacy and behaviors on their disease prevention practices.^13,20 It has been observed that individuals with higher health literacy and positive health behaviors have significantly lower risks of chronic diseases, mortality, and morbidity compared to those lacking such awareness.¹⁹ Additionally, several studies have reported that health literacy promotes a positive attitude toward screening.^10–12 These findings are consistent with the results of our study, suggesting that individuals who undergo regular cancer screening and have a high level of health literacy are more likely to continue to undergo screening even during the COVID-19 pandemic. However, the irregular screening group, who do not undergo cancer screening regularly but only occasionally, tend to forgo cancer screening due to their perception of good health and a lack of perceived need for screening. This trend has been increasing over the years. Therefore, it is crucial to enhance health literacy and cultivate screening behavior, especially among this group of individuals. Early detection of cancer through screening can contribute to early intervention and assist them in maintaining a healthy lifestyle. Previous studies have also shown a relationship between individuals' health literacy and their attitudes toward cancer screening in a pandemic. Women who have adequate health literacy and had uptake breast cancer screening prior to the pandemic were found to have a more positive attitude toward cancer screening during the pandemic.¹⁹ It is important to promote awareness-raising activities to foster positive attitudes toward cancer screening and encourage participation in screening. These activities can be disseminated through various media channels such as social media, print, video, and audio media. Furthermore, it is essential to develop policies and strategies to resume cancer screening during the pandemic period.

Finally, household income has been found to be an important factor in cancer screening. A study undertaken in the United States found that the decrease in income and job loss due to COVID-19 has been shown to be associated with a decrease in cancer screening rates.²¹ The present study also showed that the irregular screening group was more likely to report economic reasons for not undergoing screening. These findings suggest that the economic damage caused by the COVID-19 pandemic has exacerbated the existing socioeconomic disparities in cancer screening attendance, further highlighting the need for targeted interventions to ensure equitable access to cancer screening.

This study has strengths as the first attitudinal study to show the impact of the COVID-19 pandemic on screening attitudes among cancer screening subjects in Fukui Prefecture. However, there were some limitations. First, the lack of specific information regarding the types of cancer screenings undertaken by the respondents. This limitation prevented us from analyzing the characteristics and outcomes related to specific cancer screening types, resulting in a partial aspect of the data being unaccounted for. Second, this study's response rate was 50%, and the lack of a detailed analysis of the response population and population distribution limits the representativeness of the sample and could affect interpretation. Third, as this study did not directly ask about health literacy or household income, we could not rigorously analyze the association between cancer screening uptake and these factors. Additionally, the self-reporting format of the data collection process could not be controlled, and data collection through face-to-face interviews was not possible due to the COVID-19 pandemic.

In conclusion, individuals who already have adequate health literacy and had uptake of cancer screening prior to the COVID-19 pandemic were found to have a more positive attitude toward cancer screening during the pandemic. It is important to raise health literacy and cultivate screening behavior among those who have irregular screening behaviors, in order to encourage participation in cancer screening. The development of policies and strategies that allow for the safe resumption of cancer screening during the pandemic period is also crucial.

AUTHOR CONTRIBUTIONS

Conceptualization, D. I. and Y. Y.; data acquisition, H. M. and H. H.; data analysis, interpretation, and statistical analysis, D. I. and Y. Y.; writing (original draft preparation), and review and editing, D. I., M. O., H. M., H. H., N. T., H. T., A. S., T. K. All authors have read the final version of the manuscript and agree to its publication.

ACKNOWLEDGMENTS

The authors would like to thank all those who cooperated in the survey of Fukui Prefecture.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflict of interest.

ETHICS STATEMENT

Approval of the research protocol by an institutional review board: This study was approved by the ethics committee of the University of Fukui (approval number: 20230008).

Informed consent: N/A.

Registry and the registration no. of the study/trial: N/A.

Animal studies: N/A.