Epidemiology and Health

Original Articles

Socioeconomic inequality in organized and opportunistic screening for colorectal cancer: results from the Korean National Cancer Screening Survey, 2009-2021: Xuan Quy Luu, Kyeongmin Lee, Jae Kwan Jun, Mina Suh, Kui Son Choi; Epidemiol Health. 2023;45:e2023086. Published online September 17, 2023; DOI: https://doi.org/10.4178/epih.e2023086

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Abstract

OBJECTIVES
This study aimed to investigate socioeconomic status (SES)-based inequality in colorectal cancer (CRC) screening in Korea. We assessed whether the rates of opportunistic and organized CRC screening differed according to income and education levels.

METHODS

We analyzed data from the Korean National Cancer Screening Survey of 27,654 cancer-free individuals, aged 50-74 years, from 2009 to 2021. The weighted cancer screening rates with trends were estimated with the average annual percentage change using joinpoint regression. Inequality was calculated in both relative and absolute terms, based on a Poisson regression model.

RESULTS

The organized screening rate increased significantly from 22.1% in 2009 to 53.1% in 2020 and 50.6% in 2021, with an average annual change of 8.6% (95% confidence interval [CI], 4.9 to 12.5). In contrast, no significant trend was observed for opportunistic screening. The SES inequality in opportunistic screening uptake was indicated by a slope index of inequality (SII) of 9.74% (95% CI, 6.36 to 13.12), relative index of inequality (RII) of 2.18 (95% CI, 1.75 to 2.70) in terms of education level; and an SII of 7.03% (95% CI, 4.09 to 9.98), RII of 1.81 (95% CI, 1.41 to 2.31) in terms of measured income. Although there was an increasing trend in income inequality, no significant SES inequalities were observed in the overall estimates for organized screening.

CONCLUSIONS

Organized CRC screening is effective in improving the participation rate, regardless of SES. However, significant inequalities were found in opportunistic screening, suggesting room for improvement in the overall equity of CRC screening.

Summary

Korean summary
이번 연구는 한국의 대장암 검진에서 사회경제적 수준에 따른 불평등이 있는지를 분석했다. 국가암검진사업 도입 이래로 2009-2021년 연구기간 동안 공공검진을 통한 대장암 수검률은 지속적으로 증가한 반면, 개인검진의 증가는 관찰되지 않았다. 특히 공공 검진의 경우 소득이나 교육수준에 따른 수검률에 차이는 없는 반면, 개인검진에서는 상당한불평등이 관찰되었다.

Key Message
"The study investigated socioeconomic status (SES)-based inequality in colorectal cancer (CRC) screening in Korea. We found that the introduction of the National Cancer Screening Program for CRC effectively increased the participation rate, regardless of the SES of the individuals throughout the study period. However, significant inequalities were observed in opportunistic screening related to education and income."

Citations

Citations to this article as recorded by

Disparities in Cancer Incidence across Income Levels in South Korea
Su-Min Jeong, Kyu-Won Jung, Juwon Park, Nayeon Kim, Dong Wook Shin, Mina Suh
Cancers.2023; 15(24): 5898. CrossRef

Parental intention to vaccinate daughters with the human papillomavirus vaccine in Korea: a nationwide cross-sectional survey: Yejin Ha, Kyeongmin Lee, Bomi Park, Mina Suh, Jae Kwan Jun, Kui Son Choi; Epidemiol Health. 2023;45:e2023076. Published online August 17, 2023; DOI: https://doi.org/10.4178/epih.e2023076

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Abstract Summary PDF: Abstract
OBJECTIVES
We aimed to identify and compare the characteristics and factors associated with parental intention to vaccinate daughters under 12 years old against human papillomavirus (HPV), examining data from 2016 and 2020.
METHODS
Data were obtained from the Korean National Cancer Screening Survey conducted in 2016 and 2020. The present study included 3,510 parents with daughters under 12 years old. Changes in parental intention-to-vaccinate rates were calculated. To identify factors associated with parental intention to vaccinate their daughters, the chi-square test and logistic regression analysis were used.
RESULTS
The percentage of respondents intending to vaccinate their daughters increased from 33.4% in 2016 to 58.9% in 2020, constituting a 25.5 percentage point (%p) increase. Since 2016, the proportion of men expressing positive intention towards HPV vaccination increased by 31.5%p, while that of women demonstrated a 20.9%p increase. Logistic regression analysis indicated that parents with a strong intention to vaccinate their daughters tended to be younger, more educated, and aware of the free vaccination program available, as well as to have a history of HPV vaccination and to have undergone cervical cancer screening within 2 years, compared to those who did not intend to vaccinate. Being a mother with a history of HPV vaccination was the strongest predictor of positive intention to vaccinate a daughter.
CONCLUSIONS
The intention among parents to vaccinate daughters remains relatively low, although it is rising. To increase the HPV vaccination rate, strong recommendations and education should be provided to parents and the younger generation.; Summary

Korean summary
한국정부는 2016년부터 HPV 백신을 국가예방접종사업으로 도입하여 만 12세 여아를 대상으로 무료접종을 실시하고 있다. 12세 여아가 접종대상인만큼 부모의 HPV 백신에 대한 인식과 태도가 실제 예방접종에 중요한 영향을 미친다. 이 연구를 통해 2016년과 2020년을 비교했을 때 딸의 백신접종에 대한 의향이 증가하였음을 알 수 있었고, 특히 HPV 백신접종 경험이 있는 경우 딸의 백신접종에 대한 의향이 유의하게 높음을 확인하였다.

Key Message
In Korea, HPV vaccination was included in the national immunization program in 2016 for 12-year-old girls. The decision to undergo the HPV vaccination is closely associated with their parents’ perceptions of and attitudes toward the HPV vaccine. This study identified that parental intention increased from 2016 to 2020, and maternal history of HPV vaccination was the strongest predictor of positive intention to vaccinate a daughter.

Effect of mammography screening on the long-term survival of breast cancer patients: results from the National Cancer Screening Program in Korea: Xuan Quy Luu, Kyeongmin Lee, Jae Kwan Jun, Mina Suh, Kyu-Won Jung, Kui Son Choi; Epidemiol Health. 2022;44:e2022094. Published online October 26, 2022; DOI: https://doi.org/10.4178/epih.e2022094

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Abstract PDF Supplementary Material: Abstract
OBJECTIVES
This study investigated the effect of mammography screening on the long-term survival of breast cancer (BC) patients aged 40 years or older according to their screening history and duration since screening.
METHODS
The study cohort was organized from 3 nationwide databases of the Korean National Cancer Screening Program, the Korean Central Cancer Registry, and death certificates. We included 24,387 women diagnosed with invasive BC or ductal carcinoma in situ in 2008 and 2009 and followed up until December 31, 2019. Cox proportional-hazards regression was used to investigate the effect of BC screening on the risk of death.
RESULTS
Overall, 20,916 of 24,387 patients (85.8%) were alive at the end of the follow-up period (median: 10.5 years). The long-term survival rate was significantly lower in the never-screened group (80.3%) than in the screened group (88.9%) (p<0.001). A 35% reduction in the risk of BC death (hazard ratio [HR], 0.65; 95% confidence interval [CI], 0.60 to 0.70) from screening was observed. A subgroup analysis according to the cancer stage showed 62%, 36%, and 24% lower risks of BC death for the localized stage, regional stage, and distant stage, respectively. Women aged 40-49 years received the least benefit from BC screening (HR, 0.71; 95% CI, 0.62 to 0.81).
CONCLUSIONS
Mammography screening was effective in reducing the risk of BC-specific death in Asian women across all cancer stages. However, this effect was relatively small among women in their 40s, suggesting that more detailed and specialized screening strategies are needed for that age group.; Summary

Effect of Pap smears on the long-term survival of cervical cancer patients: a nationwide population-based cohort study in Korea: Xuan Quy Luu, Kyeongmin Lee, Jae Kwan Jun, Mina Suh, kyu-won Jung, Myong Cheol Lim, Kui Son Choi; Epidemiol Health. 2022;44:e2022072. Published online September 7, 2022; DOI: https://doi.org/10.4178/epih.e2022072

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Abstract Summary PDF Supplementary Material: Abstract
OBJECTIVES
This study aimed to investigate the effect of cervical cancer screening by Papanicolaou (Pap) smears on the long-term survival of cervical cancer patients.
METHODS
We constructed a retrospective cohort of 14,903 women diagnosed with invasive cancer or carcinoma in situ in 2008 and 2009 and followed up until December 31, 2019, by using individual-level data from 3 national databases of the Korean National Cancer Screening Program, the Korean Central Cancer Registry, and death certificates. Cox proportional-hazards regression was used to investigate the effect of cervical cancer screening on mortality.
RESULTS
In total, 12,987 out of 14,867 patients (87.4%) were alive at the end of the follow-up period (median: 10.5 years). Screened patients had a 38% lower risk of cervical cancer death than never-screened patients (hazard ratio [HR], 0.62; 95% confidence interval [CI], 0.54 to 0.70). Screening was associated with 59% and 35% lower risks of death, respectively, in screened patients with localized and regional stages. Furthermore, lower HRs among women who received screening were observed in all age groups, especially women aged 50–59 years (HR, 0.54; 95% CI, 0.42 to 0.69). The lowest HR for cervical cancer death was reported among patients screened within the past 2 years (HR, 0.54; 95% CI, 0.47 to 0.63), and the HRs increased with increasing time intervals.
CONCLUSIONS
Pap smear screening significantly reduced the risk of cervical cancer-specific death in Korean women across all cancer stages.; Summary

Korean summary
한국은 자궁경부암 발생과 사망을 낮추기 위하여 국가암검진사업으로 자궁경부암 검진을 실시하고 있다. 이 연구는 2008-2009년 자궁경부암 진단을 받은 30세-79세 14,903명을 대상으로 과거 자궁경부세포검진 여부에 따른 장기생존율을 추적 조사하였다. 그 결과 자궁경부암 검진을 받은 환자에서 사망 위험비가 약 38% 낮았으며, 2년 이내에 검진을 받은 환자군에서 사망 위험이 가장 낮았다.

Key Message
The Korean National Cancer Screening Program (KNCSP) has provided cervical cancer screening by Pap smear test. However, the survival, particularly long-term survival of cervical cancer patients, has never been evaluated in the KNCSP. This study reports a significant improvement in the long-term survival of screened cervical cancer patients, which persist in subgroup analysis by cancer stage. Patients who were screened within two years before the diagnosis had the best survival.

The classification capability of the Asia Pacific Colorectal Screening score in Korea: an analysis of the Cancer Screenee Cohort: Xuan Quy Luu, Kyeongmin Lee, Jeongseon Kim, Dae Kyung Sohn, Aesun Shin, Kui Son Choi; Epidemiol Health. 2021;43:e2021069. Published online September 16, 2021; DOI: https://doi.org/10.4178/epih.e2021069

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Abstract Summary PDF Supplementary Material

Abstract

OBJECTIVES
This study aimed to validate a simple risk assessment tool for estimating the advanced colorectal neoplasia (ACN) risk at colonoscopy screenings and potential factors relevant for implementing this tool in the Korean population.

METHODS

Our study analyzed data from the Cancer Screenee Cohort Study conducted by the National Cancer Center in Korea. The risk level was assessed using the Asia Pacific Colorectal Screening (APCS) score developed by the Asia-Pacific Working Group on Colorectal Cancer. Logistic regression models were used to examine the associations between colorectal-related outcomes and the risk level by APCS score. The discriminatory performance of the APCS score for various colorectal-related outcomes was assessed using C-statistics.

RESULTS

In 12,520 individuals, 317 ACN cases and 4,528 adenoma cases were found. The APCS tool successfully classified the study population into different risk groups, and significant differences in the ACN rate and other outcomes were observed. The APCS score demonstrated acceptable discrimination capability with area under the curve values ranging from 0.62 to 0.65 for various outcomes. The results of the multivariate logistic regression model revealed that the high-risk group had a 3.1-fold higher risk of ACN (95% confidence interval, 2.08 to 4.67) than the average-risk group. Body mass index (BMI) was identified as a significant predictor of ACN in both multivariate and subgroup analyses.

CONCLUSIONS

Our study highlighted significant differences in colorectal-related screening outcomes by colorectal risk level measured using the APCS score, and BMI could be used to improve the discriminatory capability of the APCS score.

Summary

Korean summary
검진의 위해성을 줄이면서 동시에 이득을 최대화할 수 있는 최적의 검진 프로그램은 암 발생 위험도를 고려하는 것이다. 이 연구는 Asia-Pacific Working Group on Colorectal Cancer에서 제안한 “Asia Pacific Colorectal Screening Score (APCS)”가 한국인에서 대장암 발생 위험도를 선별적으로 잘 구분해 낼 수 있음을 보여주었다. 나아가 대장암의 위험도 점수를 산출하는데 체질량지수가 중요한 예측 변수라는 것을 확인하였고, 한국인에서 대장암 발생 위험도의 변별력을 향상시키기 위해 기존의 APCS에 체질량지수를 추가할 것을 제안하였다.

Key Message
This study highlighted that the Asia Pacific Colorectal Screening Score by the Asia-Pacific Working Group on Colorectal Cancer could successfully classify Korean screenees into different risk groups with acceptable discriminatory capability. Furthermore, our study results also suggest that BMI is a significant predictor of colorectal-related health outcomes, which could be potentially added to the original APCS score for improving its discriminatory power.

Citations

Citations to this article as recorded by

Performance of the Asia–Pacific Colorectal Screening score in stratifying the risk of advanced colorectal neoplasia: A meta‐analysis and systematic review
Mai Ngoc Luu, Nhi Ai Trinh, Truc Le Thanh Tran, Thinh Phuong Dang, Toru Hiyama, Duc Trong Quach
Journal of Gastroenterology and Hepatology.2024;[Epub] CrossRef
A Comparison of Single and Combined Schemes of Asia-Pacific Colorectal Screening, Faecal Immunochemical and Stool Deoxyribonucleic Acid Testing for Community Colorectal Cancer Screening
Yuan Ze, Huiming Tu, Lin Zhang, Yu Bai, Yilin Ren, Xin Chen, Yuzheng Xue, Renjuan Sun, Yuling Yang, Jie Yang, Xuan Zhou, Li Liu
Journal of Multidisciplinary Healthcare.2023; Volume 16: 571. CrossRef
Advances in Screening Methods for Colorectal Cancer
碗宜张
Advances in Clinical Medicine.2023; 13(03): 2995. CrossRef
From Algorithms to Clinical Utility: A Systematic Review of Individualized Risk Prediction Models for Colorectal Cancer
Deborah Jael Herrera, Wessel van de Veerdonk, Daiane Maria Seibert, Moges Muluneh Boke, Claudia Gutiérrez-Ortiz, Nigus Bililign Yimer, Karen Feyen, Allegra Ferrari, Guido Van Hal
Gastrointestinal Disorders.2023; 5(4): 549. CrossRef
Socioeconomic inequality in organized and opportunistic screening for colorectal cancer: results from the Korean National Cancer Screening Survey, 2009-2021
Xuan Quy Luu, Kyeongmin Lee, Jae Kwan Jun, Mina Suh, Kui Son Choi
Epidemiology and Health.2023; 45: e2023086. CrossRef
A scoping review of risk-stratified bowel screening: current evidence, future directions
J. M. Cairns, S. Greenley, O. Bamidele, D. Weller
Cancer Causes & Control.2022; 33(5): 653. CrossRef

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