Trends in Cancer-Screening Rates in Korea: Findings from the National Cancer Screening Survey, 2004-2023
Article information
Abstract
Purpose
This study aimed to report the overall national trends in the rates of cancer screening based on recommendations and provide insights into the changing trends of these rates across different demographics.
Materials and Methods
This study used data from the Korean National Cancer Screening Survey (KNCSS), which surveys nationwide cancer-screening rates and includes 4,500 individuals meeting the Korean National Cancer Screening Program (NCSP) protocol age criteria. Cancer-screening rates were assessed using structured questionnaires; yearly trends were analyzed for both lifetime cancer-screening rates and rates of screening based on recommendations, and subgroup analyses were performed based on age and sex.
Results
The rates of cancer screening based on recommendations showed significant increments: the stomach cancer-screening rate increased from 39.2% in 2004 to 77.5% in 2023 (3.50% per year), the liver cancer-screening rate increased from 20.0% to 48.8% (4.30% per year), and the colorectal cancer, increased from 19.9% to 70.7% (5.15% per year). The breast cancer-screening rate increased from 33.2% to 72.7% (2.88% per year), and the cervical cancer, increased from 58.3% to 70.2% (1.08% per year). Despite some differences, particularly in relation to sociodemographic factors, screening rates increased significantly for all cancer types.
Conclusion
Cancer-screening rates in Korea increased consistently from 2004 to 2023, demonstrating the effectiveness of the national cancer-screening program. However, the increments in breast, cervical and lung cancer-screening rates were relatively lower, indicating the need for additional efforts and strategies.
Introduction
Cancer is the leading cause of death and a major disease in Korea [1,2]. In 2020, 247,952 newly diagnosed cases of cancer and 82,204 cancer-related deaths were reported in Korea [3], where the age-standardized cancer incidence rate has increased by 22.1% over the past 20 years, from 395.6 cases per 100,000 people in 2000 to 482.9 cases per 100,000 people in 2020, and the number of individuals diagnosed with cancer in 2020 was 4,433.9 per 100,000 people [3]. Among women, the age-standardized prevalence rate in 2020 reached approximately 4,770 cases per 100,000 people, accounting for approximately 5% of the population. This increase in cancer cases can primarily be attributed to the aging of the Korean population [4,5]; considering the ongoing pace of population aging, the socioeconomic burden of cancer is projected to continue increasing in the coming years.
Since 1999, Korea has implemented a comprehensive cancer-screening program targeting its population for cancer prevention and management. The National Cancer Screening Program (NCSP) was initiated in 1999 to offer free screening for gastric, breast, and cervical cancers, and its scope has expanded over time. Liver cancer screening was introduced in 2003, followed by colorectal screening in 2004. In response to the increasing prevalence of cervical cancer among individuals in their 20s, the screening age for cervical cancer was expanded to 20 years starting in 2016. Additionally, a national screening program for lung cancer targeting high-risk groups (individuals aged 54-74 years with at least 30 pack-years of smoking) was introduced in 2019 [6]. These initiatives highlight the continuous efforts of the Korean government to expand and enhance the coverage of the national cancer-screening program, adapt to changing trends, and prioritize the early detection and prevention of various types of cancer.
Similar to the early cancer detection through national screening programs discussed previously, cancer prevention and early detection and treatment are important to reduce the health, social, and economic burdens associated with cancer [7]. Cancer screening is essential for effective cancer management since it proactively aims to prevent and detect cancer in its early stages [7]. Unlike diagnostic tests primarily conducted for symptomatic individuals, cancer screening specifically targets asymptomatic populations, facilitating the identification of cancer before the onset of symptoms and enabling more favorable treatment outcomes. Moreover, screening procedures can identify and facilitate the removal of precancerous lesions such as adenomatous polyps, thereby serving as a preventive measure against conditions such as colorectal and cervical cancers [8,9]. Therefore, a comprehensive evaluation of cancer-screening rates, particularly among diverse population groups, and the identification of factors influencing screening participation from a public health perspective are paramount in augmenting cancer management endeavors [10].
International organizations such as the International Agency for Research on Cancer (IARC) analyze global cancer statistics and trends to assist countries in developing effective cancer screening strategies [11]. This collaborative effort performs a crucial role in the establishment of cancer screening programs, particularly in low- and middle-income countries. In the United States, national cancer screening behavior is monitored, leading to the development of relevant policies [10]. Moreover, there is a focus on enhancing continuous education and promotional activities to increase the participation rates in national cancer screening. Special attention is given to highlighting the significance of cancer screening and raising awareness among the public about the potential risks associated with not undergoing screening. In Korea, regular monitoring of screening practices is conducted to enhance the cancer screening rate, accompanied by attempts to enhance public understanding of the necessity for cancer screening through diverse educational and promotional campaigns.
Along with the consistent increase in screening rates, Korea’s national cancer-screening program has been considered to be a major contributing factor to the steady decrease in the incidence of major cancers over the past 20 years. While the overall annual percentage change (APC) in cancer incidence has increased by an average of 1.2 %, stomach cancer showed an average annual change rate of –2.1%, whereas cervical cancer exhibited a significantly decreased rate of –4.0% [3]. Despite the proven benefits and the provision of the national cancer-screening program, screening rates for some population groups remain low, and previous studies have shown that the screening rates vary in relation to household income, age, and education level [12]. The aim of this study was to analyze the overall trend of cancer screening rates according to guidelines, with the purpose of establishing a basis for the development of strategies and policies to improve screening rates. Furthermore, the study aimed to provide insights into the changing patterns of screening rates across sociodemographic differences.
Materials and Methods
This study used data from the Korean National Cancer Screening Survey (KNCSS), which has been conducted annually from 2004 to 2023 to survey nationwide cancer-screening rates in Korea based on population data [13]. Our study population, which was derived from the Korean NCSP protocol, consisted of 4,000 individuals who were screened between 2004 and 2023, including men aged 40-74 years and women aged 30-74 years. Additionally, since the national cervical cancer-screening target age group expanded to include women in their 20s from 2015, we also surveyed cervical cancer screening specifically in 500 women aged 20-29 years [13]. Since women in their 20s were only considered for cervical cancer screening and not for other types of cancer, their data were used only for subgroup analyses by age and calculating screening rates related to cervical cancer.
The KNCSS is conducted annually through face-to-face interviews to assess the national cancer-screening rates. To ensure that the survey participants were representative of the nationwide population, the KNCSS utilizes a stratified multistage sampling design based on population data categorized by region, age, and sex provided by the National Statistical Office of Korea. The sampling methodology has been described previously [13]. To perform a stratified multistage random sampling, the allocation of enumeration districts was based on the population size, and the final study clusters were chosen through a random selection process. A total of 5-7 households were randomly selected in urban areas, while 10-12 households were chosen in rural areas. Subjects were recruited through door-to-door outreach, with a minimum of three contact attempts made for each household. One individual was chosen from each household; in cases where there were multiple eligible individuals in the household, the individual whose date of birth was closest to the study date was selected.
In 2004, the survey was conducted through telephone interviews; however, since 2005, it has been conducted through face-to-face interviews with trained interviewers from professional survey agencies. Survey participants are recruited through household contact, with at least three contact attempts made for each household. One person from each household participates in the survey. Adequate explanations are provided to all participants, and their informed consent is obtained before they participate in the survey.
The sociodemographic factors of survey participants collected in the study included age, sex, education level, household income, marital status, residential area, and type of health insurance. The 2004 question didn’t include monthly household income and residential area did not distinguish between urban and rural areas. A structured questionnaire was used to assess the screening rates for six types of cancers (stomach, liver, colorectal, breast, cervical, and, since 2021, lung cancer). The key questions regarding participants’ cancer-screening experience, as identified in previous studies, included “Have you ever had a (specific type of cancer) screening test?”, “What screening method have you experienced?” (with multiple-choice options provided), and “When was the most recent (specific type of cancer) screening test using this method?”.
In this study, two types of cancer-screening rates were measured: the lifetime-screening rate and the rate of screening based on recommendations. Lifetime screening was defined as having undergone a screening test during one’s lifetime. On the other hand, participants who underwent screening tests according to the NCSP recommendations were classified as having been screened on the basis of recommendations. The detailed procedures and intervals of the NCSP recommendations for screening are as follows [13]: those who underwent screening according to gastric cancer screening recommendations were defined as ‘men and women aged 40 years or older who underwent the most recent upper endoscopy or upper gastrointestinal series examination within the past 2 years.’ For liver cancer screening, those who underwent screening according to screening recommendations were defined as follows; men and women over 40 years of age with a high risk of developing liver cancer (i.e., those with hepatitis B virus surface antigen [+] and hepatitis C virus antibody [+] or liver cirrhosis) and have had an abdominal ultrasound and serum α-fetoprotein test within the past 6 months. In case of colorectal cancer, before 2009, individuals who had undergone colonoscopy or double-contrast barium enema within the past 5 years or a fecal occult blood test (FOBT) within the past year were considered to have undergone colorectal cancer screening, as recommended. After 2009, individuals who had undergone a colonoscopy within ten years, double-contrast barium enema within the past 5 years, or an FOBT within the past year were considered to have undergone screening, as recommended. Those who received breast cancer screening as recommended were defined as ‘women aged 40 years or older who had their most recent screening with mammography within the past 2 years’, and for cervical cancer, ‘women aged 30 years or older who had their most recent screening with traditional cytology (Papanicolaou smear) within the past 2 years (including those in their 20s from 2015).’
The annual trends of both lifetime screening and screening based on recommendations were analyzed. For cancer screening based on recommendations, subgroup analyses were performed based on age and sex. For liver and lung cancer, since only the high-risk group was targeted for screening, the number of participants was insufficient for subgroup analysis, potentially lowering the reliability of the results. Therefore, these participants were excluded from the subgroup analysis. We applied a survey sample weight to obtain an unbiased estimate. The trends in screening rates were estimated using Joinpoint regression, and the results were summarized as an APC using a linear model for the raw values of each screening rate [14]. To illustrate the most fitting model, a single Joinpoint option was adopted for all analyses. Statistical analyses were performed using SAS ver. 9.4 (SAS Institute Inc., Cary, NC) and Joinpoint ver. 5.0.2 (National Cancer Institute, Bethesda, MD) [14].
Results
The respondents’ sociodemographic characteristics by year are presented in Table 1. The respondents’ demographic factors were distributed according to a planned sample ratio based on the national population proportion of Korea, and 4,000 individuals were selected. However, since 2014, an additional 500 women in their 20s have been surveyed to assess the rate of cervical cancer screening, causing age-composition changes. With the rise in education levels across the Korean population, the proportion of respondents with a middle school education or less significantly decreased from 41.4% in 2004 to 7.4% in 2023. Similarly, the proportion of unmarried individuals also significantly increased from 1.6% in 2004 to 16.8% in 2023.
Table 2 shows the lifetime-screening rates and rates of screening based on recommendations from 2004 to 2023. In the data for lifetime-screening rates, the rates for stomach, colorectal, and breast cancers showed a significant increase over the entire period: the rate for stomach cancer increased from 52.0 % in 2004 to 92.6% in 2023, that for colorectal cancer increased from 25.3% in 2004 to 90.0% in 2023, and that for breast cancer increased from 55.9% in 2004 to 92.2% in 2023 (Table 2, S1 Table).
In the data for the rates of screening based on recommendations, all five types of cancer (stomach, liver, colorectal, breast, and cervical) showed significant increasing trends over the entire period (lung cancer was excluded from the APC analysis because it was introduced into the national cancer-screening program only in the second half of 2019, while the screening rate began to be surveyed from 2021). The screening rate for stomach cancer increased by 3.50% per year (from 39.2% in 2004 to 77.5% in 2023), whereas that for liver cancer increased from 20.0% to 48.8% (4.30% per year). However, when applying a single Joinpoint option, the rate for stomach cancer screening initially showed a significant increasing trend (9.00% annually from 2004 to 2012) but did not show a significant trend afterward. The rate for liver cancer screening showed a significant increasing trend from 2004 to 2009 (11.35% annually) and 3.15% annually from 2009 to 2023. The colorectal cancer-screening rate increased from 19.9% to 70.7% (5.15% per year), and the breast cancer-screening rate increased from 33.2% to 72.7% (2.88% per year). The cervical cancer-screening rate increased from 58.3% to 70.2% (1.08% per year). An initial increase in the screening rate that did not persist in the later stage was observed for breast cancer and cervical cancer (breast cancer: 9.23% annually from 2004 to 2011; cervical cancer: 2.59% annually from 2004 to 2010). Interestingly, including women in their 20s in the analysis of cervical cancer showed a significantly increasing trend in the later period (6.88% annually from 2019 to 2023).
Fig. 1 illustrates the annual changes in the rates of cancer screening based on recommendations for stomach and colorectal cancers according to sex. Women underwent more stomach cancer screenings than men in 2004, but the annual increase in screening rates was faster in men than in women (APC: 3.87% in men and 3.05% in women) (S2 Table). However, in 2023, the gastric cancer-screening rates in men were slightly lower than that in women. The screening rate for colorectal cancer showed a significant increase in both men and women (APC: 5.02% in men and 4.93% in women annually).
Fig. 2 shows the trends in the recommended screening rates according to cancer type and age. Stomach and colorectal cancer showed a significant increase from 2004 to 2023 across all age groups (APC for stomach cancer: 4.14% for 40-49 years, 3.11% for 50-59 years, 2.49% for 60-69 years, and 3.45% for 70-74 years; APC for colorectal cancer: 6.45% for 50-59 years, 5.60% for 60-69 years, and 6.47% for 70-74 years), and breast cancer showed a significant increase in all groups (S3 Table). In case of cervical cancer, only the 60s and 70-74 age groups showed a significant increase (1.95% for 60-69 years and 3.15% for 70-74 years).
The data for the sources of cancer-screening costs are presented in Fig. 3. In 2004, 17.7% of the respondents received examinations using the NCSP supported by the government, and 21.1% paid for the screening themselves. In 2004, more people paid their own expenses to undergo screening. However, this trend was reversed in 2005, and the number of patients receiving screening examinations using the NCSP has continued to increase subsequently. In 2023, 58.6% of the respondents reported that they underwent screening using the NCSP. This affected the overall cancer-screening rate, and in 2023, 66.4% of all subjects underwent screening.
Discussion
Our study demonstrates a consistent increase in cancer-screening rates in Korea from 2004 to 2023. Although the findings showed some variations, the screening rates for all cancer types increased significantly. Screening rates also showed an increasing trend after the introduction of new programs, such as cervical and lung cancer screening, and the expansion of eligible participants. Specifically, the cervical cancer-screening rate, which includes the data for women in their 20s since 2015, has significantly increased over the last 4 years. Furthermore, the successful implementation of the National Lung Cancer Screening Program, which was newly introduced in the second half of 2019, was indicated by an increase in the screening rate from 21.3% in 2021 to 58.6% in 2023.
While most countries do not recommend gastric cancer screening at the national level, Japan recommends endoscopy every 2 years for individuals aged over 50 years [15]. However, gastric cancer screening is performed by only 36.7% of local governments in Japan [15], which is lower than the rate of gastric cancer screening in Korea. With the high participation rate in screening, gastric cancer screening contributed to reducing mortality rates from gastric cancer [16]. In fact, patients who underwent upper endoscopy as part of the National Cancer Screening Program had a lower probability of dying from gastric cancer [17].
For colorectal cancer screening, the rate of screening with the FOBT showed a steady increase until 2012 but showed a decreasing trend thereafter. However, the rate of colorectal cancer screening through colonoscopy significantly increased throughout the study period, which appears to reflect low confidence in FOBT and high confidence in colonoscopy in the screened population [18]. Considering the major factors influencing cancer screening, such as screening compliance and accuracy and sensitivity of the test, a screening program that appropriately considers both colonoscopy and FOBT is essential [19].
The U.S. Preventive Services Task Force recommends breast cancer screening for women aged between 50 and 74 years in the United States [20]. The U.S. government evaluates cancer-screening rates annually through the National Health Interview Survey. In 2019, the breast cancer-screening rate was 76.4%, which is higher than the corresponding rate in Korea (58.1%) [20]. Notably, the U.S. Department of Health and Human Services has set and managed the “Healthy People 2030 Target,” which aims to achieve a 77.1% screening rate, indicating that the current breast cancer-screening rate is nearly on target. In the United Kingdom, the National Health Service (NHS) conducts mammographic breast screening every 3 years through its breast-screening program [21], and in 2021, the UK’s breast cancer-screening rate was 65.3%, which is also higher than that in Korea [22]. Although the breast cancer screening rate in Korea is lower or similar compared to other countries, the introduction of breast cancer screening had significantly contributed to reducing breast cancer mortality. For those who participated in the national breast cancer screening program, the mortality rate from breast cancer was less than half that of those who did not participate [23]. The group with the most significant reduction in breast cancer mortality was women aged 45-54. However, given the still high prevalence of breast cancer, national efforts to increase the screening rate appear to be necessary.
Cervical cancer showed the smallest annual increase in screening rates among all cancers, a pattern similar to that observed in other countries: in the United States, the cervical cancer-screening rate decreased from 86.5% in 2000 to 73.5% in 2019 [24], and in the United Kingdom, it consistently decreased from 72.2% in 2020 to 69.9% in 2022 [25,26]. Although the cervical cancer-screening rate in Korea did not decrease, the rate of increase is slow, and the screening rate among those in their 20s remains low. This could be attributed to various reasons, but previous studies have reported that the lower screening rates is more pronounced in young women (ages 21-29 years) [27]. Another previous study showed that a lack of knowledge was the most common reason for not being screened on time across all groups and that human papillomavirus vaccination in the past did not appear to be a primary reason for not undergoing the most recent screening [28].
Certainly, the expansion of cervical cancer screening to individuals in their twenties was only implemented in 2016, indicating that awareness of the screening may still be relatively low. Despite the delayed initiation of screenings in 2016, the detection rates of precancerous cervical lesions and cervical dysplasia in individuals in their twenties in Korea have increased since the implementation [29]. This result suggests that cervical cancer screening in one’s twenties could be highly effective; this evidence indicates the need to develop plans to increase the participation rate in cervical cancer screening among women in their 20s in Korea and highlights the importance of ongoing education about cervical cancer screening.
Despite the substantial evidence of the benefits and guideline recommendations supporting the screening of high-risk populations, the screening rate for lung cancer in Korea (38.0%) is lower than that for other types of cancer. Although national data on this topic are limited, previous studies in other countries have estimated that approximately 20% of eligible individuals undergo lung cancer screening [30]. However, as proposed in previous studies, screening and follow-up for eligible adults is exceedingly important to gain substantial mortality-reduction benefits from screening in real-world settings [30,31]. Therefore, ensuring that eligible recipients undergo lung cancer screening is also a major task of Korea’s national cancer-screening program.
The annual increase in cancer-screening rates did not differ substantially according to sex, or age. The screening rate increased in most groups without any differences according to a specific age group or sex, indicating that Korea’s NCSP was working sufficiently. In other words, the increase in the screening rate did not differ according to the sex or age, which may have indicated differences in accessibility to screening institutions, suggesting that the NCSP is currently sufficient to reduce inequality in cancer screening. Additionally, the proportion of people undergoing screening through the NCSP increased significantly, and the national cancer-screening rate nearly doubled. These findings indicate that the NCSP has been effective in improving the screening rate of the entire population.
The NHS in the United Kingdom and the Guide to Community Preventive Services in the US commonly recommend several strategies to increase cancer-screening rates. These include reducing personal cost burdens through national support programs, such as Korea’s NCSP, focusing on education and screening recommendations for target groups, and medical training to improve the accessibility and accuracy of screening [10,32]. In Korea, continuous medical training is conducted through educational programs provided by the National Cancer Center. However, more consistent education covering target groups for certain cancers with lower screening rates may be required. In particular, education is likely to significantly increase the screening rates of newly introduced or expanded target groups, such as cervical cancer screening for women in their 20s and lung cancer screening. The provision of targeted education and recommendations may increase the participation rate in screening, thereby potentially increasing early detection and improving the outcomes of these cancers [10].
This study has several limitations. First, the participant cohort may not have been completely representative of the entire Korean population. Although the study used a multistage random sampling method based on geographic location, age, and sex, the distribution of other factors was not considered. However, efforts were made to maximize the representativeness by applying weights in the analysis after random sampling. Second, the response rate was relatively low (23.2%); the resultant non-response bias is challenging to fully exclude. However, continuous efforts were made to reduce the possibility of non-response bias by checking the sampling rate to ensure that the respondents represented the national population and visiting each household up to three times. Finally, this study relied on self-reported data, which could have introduced a recall bias. However, many studies have reported a strong correlation between the rates derived from chart audits and patient surveys [33]. Despite these limitations, this study holds significant value since it consistently monitored cancer-screening rates in a representative population group using the same survey since 2004. Such long-term monitoring has yielded valuable insights for policy decisions and interventions to improve cancer-screening rates.
The results of this study demonstrate that the cancer-screening rates in Korea consistently increased from 2004 to 2023. Moreover, this increase in screening rates was observed across different age groups and sexes, indicating a reduction in age- and sex-related disparities. Korea’s national cancer-screening program has been continuously updated and strengthened on the basis of the latest evidence regarding target populations and cancer types. These efforts are expected to contribute to improved outcomes in cancer prevention, early detection, and treatment, ultimately leading to higher survival rates and lower cancer-related mortality rates. Nevertheless, our findings also indicate the need to implement policies aimed at increasing the overall nationwide cancer-screening rates to enhance the effectiveness of the national cancer-screening program. Furthermore, additional strategies that specifically target cancer types or population groups with persistently low screening rates are also essential. These strategies will help promote and encourage participation in cancer screening among underscreened populations and further improve the effectiveness of the national cancer-screening program.
Electronic Supplementary Material
Supplementary materials are available at Cancer Research and Treatment website (https://www.e-crt.org).
Notes
Ethical Statement
The study protocol was approved by the Institutional Review Board of the National Cancer Center of Korea (approval number: NCC2022-0356). The research participants consented to participate in the survey for public purposes, and the requirement for submitting a written consent form was waived.
Author Contributions
Conceived and designed the analysis: Kang E, Choi KS, Jun JK, Kim Y, Lee HJ, Choi CK, Suh M.
Collected the data: Kang E, Kim TH, Lee SH, Suh M.
Contributed data or analysis tools: Kang E, Choi KS, Jun JK, Kim Y, Lee HJ, Choi CK, Kim TH, Lee SH, Suh M.
Performed the analysis: Kang E, Kim TH, Lee SH, Suh M.
Wrote the paper: Kang E, Choi KS, Jun JK, Kim Y, Lee HJ, Choi CK, Suh M.
Conflicts of Interest
Conflict of interest relevant to this article was not reported.
Acknowledgements
This study was supported by a Grant-in-Aid for Cancer Research and Control from the National Cancer Center of Korea (#2210773-3).