Skip Navigation
Skip to contents

Intest Res : Intestinal Research

IMPACT FACTOR

Articles

Page Path
HOME > Intest Res > Volume 21(4); 2023 > Article
Original Article
Tumor
The elderly population are more vulnerable for the management of colorectal cancer during the COVID-19 pandemic: a nationwide, population-based study
Hong Sun Kangorcid, Seung Hoon Jeonorcid, Su Bee Parkorcid, Jin Young Younorcid, Min Seob Kwakorcid, Jae Myung Cha,orcid
Intestinal Research 2023;21(4):500-509.
DOI: https://doi.org/10.5217/ir.2023.00004
Published online: August 29, 2023

Department of Internal Medicine, Kyung Hee University Hospital at Gangdong, College of Medicine, Kyung Hee University, Seoul, Korea

Correspondence to Jae Myung Cha, Department of Internal Medicine, Kyung Hee University Hospital at Gangdong, College of Medicine, Kyung Hee University, 892 Dongnam-ro, Gangdong-gu, Seoul 05278, Korea. Tel: +82-2-440-6113, Fax: +82-2-440-6295, E-mail: drcha@khu.ac.kr
• Received: January 8, 2023   • Revised: April 16, 2023   • Accepted: June 22, 2023

© Copyright 2023. Korean Association for the Study of Intestinal Diseases.

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

prev next
  • 2,283 Views
  • 197 Download
  • 1 Web of Science
  • 1 Crossref
  • 1 Scopus
See letter "To overcome medical gap in screening and surveillance of colorectal cancer during the COVID-19 pandemic" in Volume 21 on page 418.
  • Background/Aims
    The impact of coronavirus disease 2019 (COVID-19) on the management of colorectal cancer (CRC) may worse in elderly population, as almost all COVID-19 deaths occurred in the elderly patients. This study aimed to evaluate the impact of COVID-19 on CRC management in the elderly population.
  • Methods
    The numbers of patients who underwent colonoscopy, who visited hospitals or operated for CRC in 2020 and 2021 (COVID-19 era) were compared with those in 2019, according to 3 age groups (≥70 years, 50–69 years, and ≤49 years), based on the nationwide, population-based database (2019–2021) in South Korea.
  • Results
    The annual volumes of colonoscopy and hospital visits for CRC in 2020 were more significantly declined in the old age group than in the young age group (both P<0.001). In addition, the annual volume of patients operated for CRC numerically more declined in old age group than in young age group. During the first surge of COVID-19 (March and April 2020), old age patients showed statistically significant declines for the monthly number of colonoscopies (–46.5% vs. –39.3%, P<0.001), hospital visits (–15.4% vs. –7.9%, P<0.001), CRC operations (–33.8% vs. –0.7%, P<0.05), and colonoscopic polypectomies (–41.8% vs. –38.0%, P<0.001) than young age patients, compared with those of same months in 2019.
  • Conclusions
    Elderly population are more vulnerable for the management of CRC during the COVID-19 pandemic. Therefore, the elderly population are more carefully cared for in the management of CRC during the next pandemic.
In South Korea, the first case of novel coronavirus disease 2019 (COVID-19) was reported on January 20, 2020 [1]. After the declaration of the COVID-19 pandemic by the World Health Organization on March 12, 2020, several outbreaks of the COVID-19 occurred in South Korea between 2020 and 2021. The American Gastroenterological Association recommended that all elective procedures, such as screening and surveillance colonoscopy, should be delayed in asymptomatic patients during the COVID-19 pandemic [2]. The Korean Cancer Association guidelines also recommended that colorectal cancer (CRC) screening should be determined according to the shortage of medical resources and the COVID-19 status of the region [3]. Therefore, the COVID-19 pandemic has declined the number of screening and management of CRC in the world [4,5].
The impact of COVID-19 on the screening and management of CRC may worse in elderly population than in younger population, as almost all COVID-19 deaths occurred in elderly patients [6,7]. In a systematic review and meta-analysis of 42 studies with 423,117 patients, elderly patients had increased mortality due to COVID-19 with a pooled odds ratio of 2.6, and a hazard ratio of 1.3 [6]. In other systematic review and meta-analysis of 59 studies, elderly patients ( ≥ 70 years) had a higher infection risk with a relative risk (RR) of 1.7, a higher risk for severe COVID-19 disease with a RR of 2.1, an increased need for intensive care with a RR of 2.7, and a higher mortality with a RR of 3.6, compared with patients younger than 70 years [7]. Currently, no population-based studies have quantified the negative effect of COVID-19 on the management of CRC in the elderly population. A better understanding of the impact of the COVID-19 pandemic on colonoscopy and CRC management in the elderly population may be the first step toward the successful rearrangement of medical resources for the elderly population.
This study aimed to evaluate the impact of the COVID-19 pandemic on colonoscopy and CRC management in the elderly population.
1. Data Source
This was a nationwide population-based study using the Health Insurance Review and Assessment (HIRA) database of South Korea. In South Korea, the National Health Insurance (NHI) program covers approximately 98% of the total population with universal health coverage [8,9]. All healthcare providers and all Koreans are required to be covered under the NHI program, which is based on fee-for-services [9]. HIRA data is generated in the process of reimbursing providers under the NHI and contains comprehensive information on the relevant healthcare services, including various procedures, operations, examinations, treatments, and prescriptions [9]. Procedure codes in physician claims databases had a very high level of agreement with data in medical charts. The index date for extracting the study data from the HIRA database was August 1, 2022.
2. Study Population
In this study, the COVID-19 era was defined as the period from January 1, 2020 to December 31, 2021, as the first case of COVID-19 was reported in January 2020 and several outbreaks had continued to December 2021. In South Korea, the first surge of COVID-19 was encountered at March and April 2020 with the implementation of social distancing. During the COVID-19 era, the Korean government offered guidance on changes in standard medical practices to minimize COVID-19 transmission. As a result, many Koreans postponed colonoscopy to avoid exposure to COVID-19 [2], and CRC patients also delayed their hospital visit and operations for the CRC during the COVID-19 era.
We compared the claims of colonoscopy, hospital visit for CRC, and operations for CRC during the COVID-19 era (2020–2021) and pre-COVID-19 era (2019) as a reference. In this study, 3 age groups were defined as follows: young age ( ≤ 49 years), middle age (50–69 years), and old age ( ≥ 70 years) population. The young and middle age cutoff was based on the official age (50 years) for CRC screening in guidelines [10]. The middle age and old age cutoff were based on a systematic review and meta-analysis, which reported that patients aged ≥ 70 years had a higher rate of COVID-19 infection, severe COVID-19 disease, an increased need for intensive care, and higher mortality compared with patients younger than 70 years [7]. As the information used in this study was related only to pseudonyms, the requirement for informed consent was waived. This study was approved by the Institutional Review Board of Kyung Hee University Hospital at Gangdong, Seoul, Republic of Korea (IRB number: KHNMC 2022-05-045).
3. Definition of Variables
Data in this study were extracted using the HIRA claim codes [11]. Colonoscopy was defined as colonoscopy without polypectomy (E7660). Colonoscopic polypectomies were defined as a single polypectomy (Q7701), 2 or more polypectomies (Q7702), endoscopic mucosal resection (Q7703), or endoscopic submucosal dissection (QX706). Colonoscopic procedures were analyzed per patient because some patients underwent multiple colonoscopic procedures. CRC was defined as C18 (malignant neoplasm of the colon), C19 (malignant neoplasm of the rectosigmoid junction), C20 (malignant neoplasm of the rectum), and carcinoma in situ of the colon and rectum (D010, D011, and D012) based on the major diagnostic codes of the International Classification of Diseases, ninth revision codes. CRC claim codes in South Korea are reliable, as they are strictly registered in the HIRA system because CRC patients pay only 5% of their medical costs for 5 years by co-payment policy. CRC operations were defined as colectomy (QA671, QA672, QA673, QA679, Q2671, Q2672, Q2673, Q2679, Q1261, or Q1262) and/ or surgical resection of the rectum/sigmoid colon (QA921, QA922, QA923, QA924, Q2921, Q2922, Q2923, Q2924, Q2927, Q9292, QA928, or Q2928) in patients with CRC (Supplementary Table 1).
4. Statistical Analysis
The data during the COVID-19 era (2020–2021) were compared with the results of the same periods in 2019 for monthly and annual comparisons. For the monthly comparison, monthly data of 2019 were compared with those in 2020 and 2021. Descriptive analysis was performed on the entire population during the study period. Annual or monthly comparative analysis between 2 groups were done using the chi-square tests. All statistical tests were two-sided, and a P-value of < 0.05 was considered statistically significant. All statistical analyses were conducted using the R software package (R Foundation for Statistical Computing, Vienna, Austria; http://www.R-project.org).
1. Claim Data of Colonoscopy
The annual volumes of colonoscopies decreased by 8.7%, 7.0%, and 2.6% in the young age, middle age, and old age groups, respectively, in 2020 compared with those in 2019 (Table 1). The annual volumes of colonoscopies in 2020 significantly declined in middle and old age groups than those in young age group (both P<0.001). However, the annual volumes of colonoscopies in 2021 increased in all age groups compared with those in 2019. During the first surge of COVID-19 (March–April 2020), the monthly number of colonoscopies decreased in all age groups compared with those in 2019, however, they declined more significantly in middle and old age groups than those in young age group (all P<0.05) (Fig. 1). After the first surge of COVID-19 in 2020, the monthly number of colonoscopies slowly recovered in all age groups compared with those in 2019 (Fig. 2).
2. Claim Data of Hospital Visit for CRC
The annual volume of hospital visit for CRC decreased by 1.8%, 2.5%, and 3.6% in the young age, middle age, and old age groups, respectively, in 2020 compared with those in 2019 (Table 2). The annual volumes of hospital visit for CRC significantly declined in 2020 in old age group than those in young age group (P<0.05). In 2021, the annual volume of hospital visit for CRC was significantly less recovered in old age group than young age group (2.4% vs. 11.6%, P<0.05), compared with those in 2019. During the first surge of COVID-19, the monthly number of hospital visit for CRC were more significantly declined in old age group than young age group (–15.4% vs. –7.9%, P<0.001 in March) (Fig. 1). After the first surge of COVID-19 in 2020, the monthly number of hospital visits slowly recovered in all age groups compared with those in 2019 (Fig. 3).
3. Claim Data of Operation for CRC
The annual volume of patients operated for CRC decreased by 0.8%, 3.5%, and 5.8% in the young age, middle age, and old age groups, respectively, in 2020 compared with those in 2019 (Table 3). The annual volume of patients operated for CRC numerically more declined in old age groups than those in young age group, however, did not reach statistical significance. The annual volumes of patients operated for CRC in 2021 increased in all age groups compared with those in 2019. During the first surge of COVID-19, the monthly number of patients operated for CRC in 2020 decreased in all age groups, compared with those in 2019. However, they declined more significantly in old age group than those in young age group (–33.8% vs. –0.7%, P<0.05 in April) (Fig. 1). After the first surge of COVID-19 in 2020, the monthly number of patients operated for CRC slowly recovered in all age groups compared with those in 2019 (Fig. 4).
4. Claim Data of Colonoscopic Polypectomy
The annual volumes of colonoscopic polypectomies increased in all age groups in 2020 and 2021 compared with those in 2019 (Table 4). During the first surge of COVID-19, the monthly number of colonoscopic polypectomies declined in all age groups compared with those in 2019, however, more significantly declined in middle and old age groups than young age group (both P<0.001). After the first surge of COVID-19 in 2020, the monthly number of colonoscopic polypectomies rapidly recovered in all age groups compared with those in 2019.
This population-based study quantify the impact of the COVID-19 pandemic on colonoscopy and CRC management in elderly population. The annual volumes of colonoscopy and hospital visits for CRC in 2020 were more significantly declined in old age group than in young age group. In addition, the annual volume of patients operated for CRC numerically more declined in old age group than in young age group. During the first surge of COVID-19 (March–April 2020), elderly subjects showed statistically significant declines for the monthly number of colonoscopies, hospital visits, CRC operations, and colonoscopic polypectomies than young age patients, compared with those in same month of 2019. Our study results were consistent with those of Western studies [12,13], in that the annual volume of colonoscopy and CRC management markedly decreased during the COVID-19. But, our notable finding was that elderly patients are more vulnerable for the management of CRC during the first surge of COVID-19 pandemic. In South Korea, the first surge of COVID-19 in March and April 2020 was followed by 2nd epidemic wave in July to October 2020, 3rd epidemic wave from November 2020 to February 2021 and 4th epidemic wave from July to September 2021 [14]. Despite several epidemic waves of COVID-19, colonoscopy and management of CRC were gradually unaffected by COVID-19 epidemic changes after the first surge of COVID-19 in South Korea.
In recent studies [7,15-17], old age was an independent risk factor for COVID-19 mortality. In a UK-based study, elderly patients aged ≥ 75 years showed a 13-fold higher COVID-19 mortality risk compared with those aged < 65 years [15]. In a systematic review and meta-analysis, individuals aged ≥ 75 years had a 3.4-fold higher risk for COVID-19 mortality [16]. Based on 178,568 COVID-19 deaths from approximately 2.4 billion U.S. population, elderly patients aged ≥ 65 years had significantly higher COVID-19 mortality rates compared with younger individuals [17]. In a recent meta-analysis including 59 studies comprising 36,470 patients, elderly patients aged ≥ 70 years had a higher rate of COVID-19 mortality, COVID-19 infection, severe COVID-19 disease, and need for intensive care compared with patients younger than 70 years [7]. Due to the higher risk of COVID-19 transmission and mortality among elderly patients, the screening and management of CRC may be more decreased in the elderly patients than in young age group during the COVID-19 pandemic.
Therefore, efforts are needed to close the gap of colonoscopy and CRC management in the elderly population during the first surge of COVID-19. The gap of CRC management may be reduced by converting contact treatment to non-contact treatment for the elderly population. In the United States, for example, hospital visits decreased by 68%, but, telemedicine visits increased by 41% during COVID-19 [18]. In addition, colonoscopy may be converted to fecal immunochemical test (FIT) to reduce the backlog of elderly subjects who need to be screened for CRC [19]. FIT is a relatively non-contact and safe procedure, therefore, FIT could be an alternative to colonoscopy to elderly subjects, who are hesitant of hospital visits during COVID-19 [20]. However, colonoscopy is still preferred over FIT due to higher diagnostic yield of CRC. So, stool DNA-based test with a high diagnostic yield for CRC may be promising option for elderly subjects during COVID-19. A recent study showed that stool DNA-based methylated syndecan-2 test has increased sensitivity (90.2%) and specificity (90.2%) for detection of CRC as compared to FIT [21]. This test could be done entirely from home with no special preparation during COVID-19.
Temporary interruption of CRC screening and management during the COVID-19 pandemic may lead to additional deaths from CRC. In Canada, 6-month interruptions in CRC screening due to COVID-19 will lead to increase of CRC incidence until 2200 with more CRC deaths over the lifetime [22]. In the United Kingdom, a 12-month delay of CRC diagnosis due to COVID-19 was estimated to decrease in 6.4% of 5-year survival rate of CRC [18]. In addition, they expected to take 3–6 months for the return to pre-pandemic levels even after lifting all restrictions on CRC screenings [23]. Therefore, a substantial increase in the number of avoidable CRC deaths may be expected as a result of diagnostic delays of CRC during COVID-19. In our study, the volume of colonoscopies declined during only the first surge of COVID-19 (March–May 2020), which may little impact on the oncological outcomes of CRC. However, oncological outcomes of CRC affected by COVID-19 pandemic should be further evaluated in South Korea, especially for the elderly population.
The use of the HIRA database enabled us to perform the first Asian study to date that assessed the worse impact on the elderly population for the colonoscopy and CRC management during COVID-19. Our findings are virtually free from referral bias and are readily generalizable owing to the population-based design. However, this study has some limitations. One of the limitations of our study is the secondary data with uncertainty regarding the accuracy of the diagnosis. However, previous studies using the HIRA database have shown that procedures and diagnoses are accurately coded. No specific details regarding the indications of colonoscopy and detailed clinical information of each patient were recorded in the HIRA. In addition, it is challenging to generalize our findings to other countries, as the COVID-19 status and healthcare systems differ in each country. Finally, our population-based data included only 3 years of data, so they are not timely enough, but most timely available. Furthermore, there is a growing body of evidence to suggest similar findings observed internationally.
In conclusion, elderly population are more vulnerable for the colonoscopy and CRC management during the first surge of COVID-19 pandemic. Therefore, elderly population are more carefully cared for the colonoscopy and CRC management during the next pandemic.

Funding Source

The work was supported by a grant (21153MFDS601) from Ministry of Food and Drug Safety in 2022.

Conflict of Interest

No potential conflict of interest relevant to this article was reported.

Data Availability Statement

Not applicable.

Author Contributions

Conceptualization: Cha JM. Data curation: Kang HS, Jeon SH, Park SB. Formal analysis: Kang HS, Yoon JY, Kwak MS. Funding acquisition: Cha JM. Methodology: Yoon JY, Kwak MS, Cha JM. Supervision: Cha JM. Writing - original draft: Kang HS, Cha JM. Writing - review & editing: Cha JM. Approval of final manuscript: all authors.

Supplementary materials are available at the Intestinal Research website (https://www.irjournal.org).

Supplementary Table 1.

Operation Codes for Colorectal Cancers
ir-2023-00004-Supplementary-Table-1.pdf
Fig. 1.
The monthly change (%) of colonoscopy, hospital visit for colorectal cancer (CRC) and operation for CRC during the first surge of coronavirus disease 2019 (March and April of 2020), compared with those in 2019, more significantly declined in middle and old age groups than young age group (reference). Their statistical significance was expressed with aP<0.05, bP<0.001.
ir-2023-00004f1.jpg
Fig. 2.
The percentage change of colonoscopy claim in 2020 and 2021, compared to those of 2019, were more significantly declined in middle and old age groups than those in young age group in the first epidemic wave, but slowly recovered in all age groups even in the 2nd-4th epidemic waves. Statistical significance was expressed with aP<0.05, bP<0.001.
ir-2023-00004f2.jpg
Fig. 3.
The percentage change of hospital visit in 2020 and 2021, compared to those of 2019, were significantly declined in old age group than those in young age group in the first epidemic wave, but slowly recovered in all age groups even in the 2nd-4th epidemic waves. Statistical significance was expressed with aP<0.05, bP<0.001.
ir-2023-00004f3.jpg
Fig. 4.
The percentage change of colorectal cancer (CRC) operation in 2020 and 2021, compared to those of 2019, were significantly declined in old age group than those in young age group in the first epidemic wave, but slowly recovered in all age groups even in the 2nd-4th epidemic waves. Statistical significance was expressed with aP<0.05, bP<0.001.
ir-2023-00004f4.jpg
ir-2023-00004f5.jpg
Table 1.
Number of Patients Who Underwent Colonoscopya
Group Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
Young age
2019 46,502 37,854 41,126 41,725 40,790 39,623 46,073 48,838 41,409 51,223 61,418 66,936 563,517
2020 43,474 36,606 24,972 28,983 35,736 41,383 44,894 45,751 45,371 45,104 59,437 62,914 514,625
Change (%)b –6.5 –3.3 –39.3 –30.5 –12.4 +4.4 –2.6 –6.3 +9.6 –11.9 –3.2 –6.0 –8.7
2021 45,815 39,894 45,818 47,349 44,327 55,123 53,006 51,858 42,190 47,982 62,119 70,987 606,468
Change (%)b –1.5 +5.4 +11.4 +13.5 +8.7 +39.1 +15.0 +6.2 +1.9 –6.3 +1.1 +6.1 +7.6
Middle age
2019 76,230 63,451 80,500 80,814 79,534 74,638 87,650 89,389 71,612 94,330 103,402 105,251 1,006,801
2020 68,986 61,109 44,025 53,374 70,139 81,469 90,216 88,460 80,006 87,673 106,584 104,237 936,278
Change (%)b –9.5d –3.7e –45.3d –34.0d –11.8e +9.2d +2.9d –1.0d +11.7c –7.1d +3.1d –1.0d –7.0d
2021 75,182 65,260 91,606 93,098 85,321 91,612 93,734 84,013 72,135 97,644 114,145 117,154 1,080,904
Change (%)b –1.4e +2.9c +13.8e +15.2e +7.3e +22.7d +6.9d –6.0d +0.7e +3.5d +10.4d +11.3d +7.4e
Old age
2019 18,712 15,713 23,306 24,160 22,904 20,338 22,196 18,593 17,319 22,693 21,205 20,082 247,221
2020 17,626 15,398 12,480 16,277 21,761 25,378 24,776 19,896 18,895 21,852 24,442 22,054 240,835
Change (%)b –5.8e –2,.0e –46.5d –32.6c –5.0d +24.8d +11.6d +7.0d +9.1e +3.7d +15.3d +9.8d –2.6d
2021 19,065 16,486 27,805 27,301 22,566 22,914 24,086 20,047 19,610 25,788 26,121 24,024 275,813
Change (%)b +1.9c +4.9e +19.3d +13.0e –1.5d +12.7d +8.5d +7.8e +13.2d +13.6d +23.2d +19.6d +11.6d

a Colonoscopy was defined as colonoscopy without any therapeutic interventions (E7660).

b Change (%) means the percentage of change in 2020 or 2021 compared to that of 2019.

c-e Statistical significance was expressed with cP<0.05, dP<0.001, eP≥0.05 (no significance).

Table 2.
Number of Patients Who Visited Hospital for Colorectal Cancersa
Group Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
Young age
2019 4,779 4,249 4,310 4,482 4,316 4,294 4,535 4,448 4,303 4,576 4,491 4,590 53,373
2020 4,663 4,212 3,969 4,149 4,191 4,388 4,476 4,271 4,301 4,410 4,609 4,759 52,398
Change (%)b –2.4 –0.9 –7.9 –7.4 –2.9 +2.2 –1.3 –4.0 0.0 –3.6 +2.6 –3.7 –1.8
2021 4,759 4,541 4,973 4,860 4,671 5,155 5,141 5,034 4,927 4,957 5,221 5,341 59,580
Change (%)b –0.4 +6.9 +15.4 +8.4 +8.2 +20.1 +13.4 +13.2 +14.5 +8.3 +16.3 +16.4 +11.6
Middle age
2019 25,931 23,214 24,638 24,965 24,592 24,011 25,455 24,158 23,841 25,323 24,951 25,553 296,632
2020 25,487 23,242 22,487 23,122 23,842 24,835 24,908 23,354 23,575 24,071 24,893 25,534 289,350
Change (%)b –1.7e +0.1e –8.7e –7.4e –3.0e +3.4e –2.1e –3.3e –1.1e –4.9e –0.2e –0.1e –2.5e
2021 25,634 24,117 26,846 25,367 24,813 26,250 26,338 25,573 25,118 26,103 26,673 27,322 310,154
Change (%)b –1.1e +3.9e +9.0c +1.6c +0.9c +9.3d +3.5d +5.9c +5.4d +3.1c +6.9d +6.9d +4.6d
Old age
2019 19,475 17,473 19,205 19,825 19,272 18,810 19,987 18,745 18,653 20,035 18,984 19,199 229,663
2020 19,220 17,027 16,244 17,757 18,906 19,760 19,577 18,120 17,890 18,891 19,044 18,986 221,422
Change (%)b –1.3e –2.6e –15.4d –10.4e –1.9e +5.1e –2.1e –3.3e –4.1e –5.7e +0.3e –1.1c –3.6c
2021 18,700 18,093 20,415 19,841 19,021 20,156 19,936 19,391 19,256 20,117 20,162 20,080 235,168
Change (%)b –4.0e +3.5e +6.3d +0.1d –1.3d +7.2d –0.3d +3.4d +3.2d +0.4d +6.2d +4.6d +2.4d

a Colorectal cancer was defined as colorectal cancers (C18, C19, C20) including carcinoma in situ of colon and rectum (D010, D011, D012).

b Change (%) means the percentage of change in 2020 or 2021 compared to that of 2019.

c-e Statistical significance was expressed with cP<0.05, dP<0.001, eP≥0.05 (no significance).

Table 3.
Number of Patients Who Underwent Operations for Colorectal Cancersa
Group Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
Young age
2019 192 161 157 147 167 162 152 175 159 146 160 154 1,932
2020 168 145 164 146 177 167 166 154 162 164 149 154 1,916
Change (%)b –12.5 –9.9 +4.5 –0.7 +6.0 +3.1 +9.2 –12.0 +1.9 +12.3 –6.9 0.0 –0.8
2021 197 118 197 156 160 157 180 168 153 160 164 148 1,958
Change (%)b 2.6 –26.7 +25.5 +6.1 –4.2 –3.1 +18.4 –4.0 –3.8 +9.6 +2.5 –3.9 +1.3
Middle age
2019 1,030 773 928 814 803 734 878 734 770 707 797 825 9,793
2020 956 949 893 660 708 760 759 690 700 745 821 809 9,450
Change (%)b –7.2e +22.8c –3.8e –18.9e –11.8e +3.5e –13.6e –6.0e –9.1e +5.4e +3.0e –1.9e –3.5e
2021 972 828 938 807 777 822 787 828 689 843 873 827 9,991
Change (%)b –5.6e +7.1c +1.1e –0.9e –3.2e +12.0e –10.4c +12.8e –10.5e +19.2e +9.5e +0.2e +2.0e
Old age
2019 789 608 766 773 757 666 765 661 585 621 641 628 8,260
2020 643 709 658 512 683 736 685 585 631 649 661 626 7,778
Change (%)b –18.5e +16.6c –14.1e –33.8c –9.8e +10.5e –10.5e –11.5e +7.9e +4.5e +3.1e –0.3e –5.8e
2021 755 607 809 726 707 722 702 771 628 711 682 664 8,484
Change (%)b –4.3e –0.2c +5.6e –6.1e –6.6d +8.4e –8.2c +16.6e +7.4e +14.5e +6.4e +5.7e +2.7e

a Operations for colorectal cancer was defined as colectomy (QA671, QA672, QA673, QA679, Q2671, Q2672, Q2673, Q2679, Q1261, Q1262) and/or surgical resection of rectum/sigmoid colon (QA921, QA922, QA923, QA924, Q2921, Q2922, Q2923, Q2924, Q2927, Q9292, QA928, Q2928) in patients with colorectal cancer.

b Change (%) means the percentage of change in 2020 or 2021 compared to that of 2019.

c-e Statistical significance was expressed with cP<0.05, dP<0.001, eP≥0.05 (no significance).

Table 4.
Number of Patients Who Underwent Colonoscopic Polypectomiesa
Group Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
Young age
2019 19,667 16,193 19,183 20,776 21,170 21,095 23,714 24,635 21,204 27,841 34,673 38,087 288,238
2020 20,669 18,578 13,000 15,836 19,726 24,052 26,861 27,022 28,507 29,829 40,072 43,074 307,226
Change (%)b +5.1 +14.7 –32.2 –23.8 –6.8 14.0 13.3 9.7 34.4 7.1 15.6 13.1 +6.6
2021 27,176 23,032 28,545 31,424 30,679 38,345 36,220 36,182 30,651 36,415 47,912 54,991 421,572
Change (%)b +38.2 +42.2 +48.8 +51.3 +44.9 +81.8 +52.7 +46.9 +44.6 +30.8 +38.2 +44.4 +46.3
Middle age
2019 58,085 42,727 54,794 55,730 54,953 51,426 61,076 62,322 50,040 66,360 75,486 79,342 712,341
2020 58,234 45,538 33,979 41,481 54,486 63,656 71,353 70,216 63,989 70,351 86,738 89,946 749,967
Change (%)b +0.3d +6.6d –38.0d –25.6e –0.8d +23.8d +16.8c +12.7c +27.9d +6.0e +14.9e +13.4e +5.3d
2021 71,854 53,705 77,830 80,429 75,125 80,172 83,025 73,438 66,140 88,403 103,484 110,378 963,983
Change (%)b +23.7d +25.7d +42.0d +44.3d +36.7d +55.9d +35.9d +17.8d +32.2d +33.2e +37.1e +39.1d +35.3d
Old age
2019 14,307 10,901 16,887 17,485 16,366 14,729 16,227 13,111 12,111 16,619 16,260 15,567 180,570
2020 14,649 11,804 9,836 12,992 17,295 19,807 19,740 15,618 15,525 17,476 20,182 19,053 193,977
Change (%)b +2.4e +8.3d –41.8d –25.7e +5.7d +34.5d +21.6d +19.1d +28.2c +5.2e +24.1d +22.4d +7.4e
2021 17,856 13,490 23,705 23,719 19,366 19,426 20,761 16,569 16,663 22,881 23,643 22,208 240,287
Change (%)b +24.8d +23.8d +40.4d +35.7d +18.3d +31.9d +27.9d +6.4d +37.6d +37.7d +45.4d +42.7e +33.1d

a Colonoscopic polypectomy was defined as single colonoscopic polypectomy (Q7701), multiple colonoscopic polypectomy (Q7702), endoscopic mucosal resection (Q7703) and endoscopic submucosal dissection (QX706).

b Change (%) means the percentage of change in 2020 or 2021 compared to that of 2019.

c-e Statistical significance was expressed with cP<0.05, dP<0.001, eP≥0.05 (no significance).

  • 1. Jee Y, Kim YJ, Oh J, Kim YJ, Ha EH, Jo I. A COVID-19 mortality prediction model for Korean patients using nationwide Korean disease control and prevention agency database. Sci Rep 2022;12:3311.ArticlePubMedPMCPDF
  • 2. Sultan S, Lim JK, Altayar O, et al. AGA rapid recommendations for gastrointestinal procedures during the COVID-19 pandemic. Gastroenterology 2020;159:739–758.ArticlePubMedPMC
  • 3. Lee JB, Jung M, Kim JH, et al. Guidelines for cancer care during the COVID-19 pandemic in South Korea. Cancer Res Treat 2021;53:323–329.ArticlePubMedPMCPDF
  • 4. Morris EJ, Goldacre R, Spata E, et al. Impact of the COVID-19 pandemic on the detection and management of colorectal cancer in England: a population-based study. Lancet Gastroenterol Hepatol 2021;6:199–208.ArticlePubMedPMC
  • 5. Lui TK, Leung K, Guo CG, Tsui VW, Wu JT, Leung WK. Impacts of the coronavirus 2019 pandemic on gastrointestinal endoscopy volume and diagnosis of gastric and colorectal cancers: a population-based study. Gastroenterology 2020;159:1164–1166.ArticlePubMedPMC
  • 6. Dessie ZG, Zewotir T. Mortality-related risk factors of COVID-19: a systematic review and meta-analysis of 42 studies and 423,117 patients. BMC Infect Dis 2021;21:855.ArticlePubMedPMCPDF
  • 7. Pijls BG, Jolani S, Atherley A, et al. Demographic risk factors for COVID-19 infection, severity, ICU admission and death: a meta-analysis of 59 studies. BMJ Open 2021;11:e044640.ArticlePubMedPMC
  • 8. Kim L, Kim JA, Kim S. A guide for the utilization of Health Insurance Review and Assessment Service National Patient Samples. Epidemiol Health 2014;36:e2014008.ArticlePubMedPMC
  • 9. Kim JA, Yoon S, Kim LY, Kim DS. Towards actualizing the value potential of Korea Health Insurance Review and Assessment (HIRA) data as a resource for health research: strengths, limitations, applications, and strategies for optimal use of HIRA data. J Korean Med Sci 2017;32:718–728.ArticlePubMedPMCPDF
  • 10. Sung JJ, Ng SC, Chan FK, et al. An updated Asia Pacific Consensus Recommendations on colorectal cancer screening. Gut 2015;64:121–132.ArticlePubMed
  • 11. Health Insurance Review and Assessmen. Standard guide to calculating disease behavior statistics [Internet]. c2021 [cited 2023 Jan 9]. http://opendata.hira.or.kr/co.apndFile.dir/download.do?fileNm=illnessBehavior.pdf.
  • 12. Khan A, Bilal M, Morrow V, Cooper G, Thakkar S, Singh S. Impact of the coronavirus disease 2019 pandemic on gastrointestinal procedures and cancers in the United States: a multicenter research network study. Gastroenterology 2021;160:2602–2604.ArticlePubMedPMC
  • 13. Lantinga MA, Theunissen F, Ter Borg PC, et al. Impact of the COVID-19 pandemic on gastrointestinal endoscopy in the Netherlands: analysis of a prospective endoscopy database. Endoscopy 2021;53:166–170.ArticlePubMedPMC
  • 14. Jeon J, Han C, Kim T, Lee S. Evolution of responses to COVID-19 and epidemiological characteristics in South Korea. Int J Environ Res Public Health 2022;19:4056.ArticlePubMedPMC
  • 15. Ho FK, Petermann-Rocha F, Gray SR, et al. Is older age associated with COVID-19 mortality in the absence of other risk factors? General population cohort study of 470,034 participants. PLoS One 2020;15:e0241824.ArticlePubMedPMC
  • 16. Damayanthi HD, Prabani KI, Weerasekara I. Factors associated for mortality of older people with COVID 19: a systematic review and meta-analysis. Gerontol Geriatr Med 2021;7:23337214211057392.ArticlePubMedPMCPDF
  • 17. Yanez ND, Weiss NS, Romand JA, Treggiari MM. COVID-19 mortality risk for older men and women. BMC Public Health 2020;20:1742.ArticlePubMedPMCPDF
  • 18. Whaley CM, Pera MF, Cantor J, et al. Changes in health services use among commercially insured US populations during the COVID-19 pandemic. JAMA Netw Open 2020;3:e2024984.ArticlePubMedPMC
  • 19. Shaukat A, Church T. Colorectal cancer screening in the USA in the wake of COVID-19. Lancet Gastroenterol Hepatol 2020;5:726–727.ArticlePubMedPMC
  • 20. Gupta S, Lieberman D. Screening and surveillance colonoscopy and COVID-19: avoiding more casualties. Gastroenterology 2020;159:1205–1208.ArticlePubMedPMC
  • 21. Han YD, Oh TJ, Chung TH, et al. Early detection of colorectal cancer based on presence of methylated syndecan-2 (SDC2) in stool DNA. Clin Epigenetics 2019;11:51.ArticlePubMedPMCPDF
  • 22. Yong JH, Mainprize JG, Yaffe MJ, et al. The impact of episodic screening interruption: COVID-19 and population-based cancer screening in Canada. J Med Screen 2021;28:100–107.ArticlePubMedPMCPDF
  • 23. Maringe C, Spicer J, Morris M, et al. The impact of the COVID-19 pandemic on cancer deaths due to delays in diagnosis in England, UK: a national, population-based, modelling study. Lancet Oncol 2020;21:1023–1034.ArticlePubMedPMC

Figure & Data

REFERENCES

    Citations

    Citations to this article as recorded by  
    • To overcome medical gap in screening and surveillance of colorectal cancer during the COVID-19 pandemic
      Yoo Min Han
      Intestinal Research.2023; 21(4): 418.     CrossRef

    • PubReader PubReader
    • ePub LinkePub Link
    • Cite
      CITE
      export Copy Download
      Close
      Download Citation
      Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

      Format:
      • RIS — For EndNote, ProCite, RefWorks, and most other reference management software
      • BibTeX — For JabRef, BibDesk, and other BibTeX-specific software
      Include:
      • Citation for the content below
      The elderly population are more vulnerable for the management of colorectal cancer during the COVID-19 pandemic: a nationwide, population-based study
      Intest Res. 2023;21(4):500-509.   Published online August 29, 2023
      Close
    • XML DownloadXML Download
    Figure
    • 0
    • 1
    • 2
    • 3
    • 4
    Related articles
    The elderly population are more vulnerable for the management of colorectal cancer during the COVID-19 pandemic: a nationwide, population-based study
    Image Image Image Image Image
    Fig. 1. The monthly change (%) of colonoscopy, hospital visit for colorectal cancer (CRC) and operation for CRC during the first surge of coronavirus disease 2019 (March and April of 2020), compared with those in 2019, more significantly declined in middle and old age groups than young age group (reference). Their statistical significance was expressed with aP<0.05, bP<0.001.
    Fig. 2. The percentage change of colonoscopy claim in 2020 and 2021, compared to those of 2019, were more significantly declined in middle and old age groups than those in young age group in the first epidemic wave, but slowly recovered in all age groups even in the 2nd-4th epidemic waves. Statistical significance was expressed with aP<0.05, bP<0.001.
    Fig. 3. The percentage change of hospital visit in 2020 and 2021, compared to those of 2019, were significantly declined in old age group than those in young age group in the first epidemic wave, but slowly recovered in all age groups even in the 2nd-4th epidemic waves. Statistical significance was expressed with aP<0.05, bP<0.001.
    Fig. 4. The percentage change of colorectal cancer (CRC) operation in 2020 and 2021, compared to those of 2019, were significantly declined in old age group than those in young age group in the first epidemic wave, but slowly recovered in all age groups even in the 2nd-4th epidemic waves. Statistical significance was expressed with aP<0.05, bP<0.001.
    Graphical abstract
    The elderly population are more vulnerable for the management of colorectal cancer during the COVID-19 pandemic: a nationwide, population-based study
    Group Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
    Young age
    2019 46,502 37,854 41,126 41,725 40,790 39,623 46,073 48,838 41,409 51,223 61,418 66,936 563,517
    2020 43,474 36,606 24,972 28,983 35,736 41,383 44,894 45,751 45,371 45,104 59,437 62,914 514,625
    Change (%)b –6.5 –3.3 –39.3 –30.5 –12.4 +4.4 –2.6 –6.3 +9.6 –11.9 –3.2 –6.0 –8.7
    2021 45,815 39,894 45,818 47,349 44,327 55,123 53,006 51,858 42,190 47,982 62,119 70,987 606,468
    Change (%)b –1.5 +5.4 +11.4 +13.5 +8.7 +39.1 +15.0 +6.2 +1.9 –6.3 +1.1 +6.1 +7.6
    Middle age
    2019 76,230 63,451 80,500 80,814 79,534 74,638 87,650 89,389 71,612 94,330 103,402 105,251 1,006,801
    2020 68,986 61,109 44,025 53,374 70,139 81,469 90,216 88,460 80,006 87,673 106,584 104,237 936,278
    Change (%)b –9.5d –3.7e –45.3d –34.0d –11.8e +9.2d +2.9d –1.0d +11.7c –7.1d +3.1d –1.0d –7.0d
    2021 75,182 65,260 91,606 93,098 85,321 91,612 93,734 84,013 72,135 97,644 114,145 117,154 1,080,904
    Change (%)b –1.4e +2.9c +13.8e +15.2e +7.3e +22.7d +6.9d –6.0d +0.7e +3.5d +10.4d +11.3d +7.4e
    Old age
    2019 18,712 15,713 23,306 24,160 22,904 20,338 22,196 18,593 17,319 22,693 21,205 20,082 247,221
    2020 17,626 15,398 12,480 16,277 21,761 25,378 24,776 19,896 18,895 21,852 24,442 22,054 240,835
    Change (%)b –5.8e –2,.0e –46.5d –32.6c –5.0d +24.8d +11.6d +7.0d +9.1e +3.7d +15.3d +9.8d –2.6d
    2021 19,065 16,486 27,805 27,301 22,566 22,914 24,086 20,047 19,610 25,788 26,121 24,024 275,813
    Change (%)b +1.9c +4.9e +19.3d +13.0e –1.5d +12.7d +8.5d +7.8e +13.2d +13.6d +23.2d +19.6d +11.6d
    Group Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
    Young age
    2019 4,779 4,249 4,310 4,482 4,316 4,294 4,535 4,448 4,303 4,576 4,491 4,590 53,373
    2020 4,663 4,212 3,969 4,149 4,191 4,388 4,476 4,271 4,301 4,410 4,609 4,759 52,398
    Change (%)b –2.4 –0.9 –7.9 –7.4 –2.9 +2.2 –1.3 –4.0 0.0 –3.6 +2.6 –3.7 –1.8
    2021 4,759 4,541 4,973 4,860 4,671 5,155 5,141 5,034 4,927 4,957 5,221 5,341 59,580
    Change (%)b –0.4 +6.9 +15.4 +8.4 +8.2 +20.1 +13.4 +13.2 +14.5 +8.3 +16.3 +16.4 +11.6
    Middle age
    2019 25,931 23,214 24,638 24,965 24,592 24,011 25,455 24,158 23,841 25,323 24,951 25,553 296,632
    2020 25,487 23,242 22,487 23,122 23,842 24,835 24,908 23,354 23,575 24,071 24,893 25,534 289,350
    Change (%)b –1.7e +0.1e –8.7e –7.4e –3.0e +3.4e –2.1e –3.3e –1.1e –4.9e –0.2e –0.1e –2.5e
    2021 25,634 24,117 26,846 25,367 24,813 26,250 26,338 25,573 25,118 26,103 26,673 27,322 310,154
    Change (%)b –1.1e +3.9e +9.0c +1.6c +0.9c +9.3d +3.5d +5.9c +5.4d +3.1c +6.9d +6.9d +4.6d
    Old age
    2019 19,475 17,473 19,205 19,825 19,272 18,810 19,987 18,745 18,653 20,035 18,984 19,199 229,663
    2020 19,220 17,027 16,244 17,757 18,906 19,760 19,577 18,120 17,890 18,891 19,044 18,986 221,422
    Change (%)b –1.3e –2.6e –15.4d –10.4e –1.9e +5.1e –2.1e –3.3e –4.1e –5.7e +0.3e –1.1c –3.6c
    2021 18,700 18,093 20,415 19,841 19,021 20,156 19,936 19,391 19,256 20,117 20,162 20,080 235,168
    Change (%)b –4.0e +3.5e +6.3d +0.1d –1.3d +7.2d –0.3d +3.4d +3.2d +0.4d +6.2d +4.6d +2.4d
    Group Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
    Young age
    2019 192 161 157 147 167 162 152 175 159 146 160 154 1,932
    2020 168 145 164 146 177 167 166 154 162 164 149 154 1,916
    Change (%)b –12.5 –9.9 +4.5 –0.7 +6.0 +3.1 +9.2 –12.0 +1.9 +12.3 –6.9 0.0 –0.8
    2021 197 118 197 156 160 157 180 168 153 160 164 148 1,958
    Change (%)b 2.6 –26.7 +25.5 +6.1 –4.2 –3.1 +18.4 –4.0 –3.8 +9.6 +2.5 –3.9 +1.3
    Middle age
    2019 1,030 773 928 814 803 734 878 734 770 707 797 825 9,793
    2020 956 949 893 660 708 760 759 690 700 745 821 809 9,450
    Change (%)b –7.2e +22.8c –3.8e –18.9e –11.8e +3.5e –13.6e –6.0e –9.1e +5.4e +3.0e –1.9e –3.5e
    2021 972 828 938 807 777 822 787 828 689 843 873 827 9,991
    Change (%)b –5.6e +7.1c +1.1e –0.9e –3.2e +12.0e –10.4c +12.8e –10.5e +19.2e +9.5e +0.2e +2.0e
    Old age
    2019 789 608 766 773 757 666 765 661 585 621 641 628 8,260
    2020 643 709 658 512 683 736 685 585 631 649 661 626 7,778
    Change (%)b –18.5e +16.6c –14.1e –33.8c –9.8e +10.5e –10.5e –11.5e +7.9e +4.5e +3.1e –0.3e –5.8e
    2021 755 607 809 726 707 722 702 771 628 711 682 664 8,484
    Change (%)b –4.3e –0.2c +5.6e –6.1e –6.6d +8.4e –8.2c +16.6e +7.4e +14.5e +6.4e +5.7e +2.7e
    Group Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Total
    Young age
    2019 19,667 16,193 19,183 20,776 21,170 21,095 23,714 24,635 21,204 27,841 34,673 38,087 288,238
    2020 20,669 18,578 13,000 15,836 19,726 24,052 26,861 27,022 28,507 29,829 40,072 43,074 307,226
    Change (%)b +5.1 +14.7 –32.2 –23.8 –6.8 14.0 13.3 9.7 34.4 7.1 15.6 13.1 +6.6
    2021 27,176 23,032 28,545 31,424 30,679 38,345 36,220 36,182 30,651 36,415 47,912 54,991 421,572
    Change (%)b +38.2 +42.2 +48.8 +51.3 +44.9 +81.8 +52.7 +46.9 +44.6 +30.8 +38.2 +44.4 +46.3
    Middle age
    2019 58,085 42,727 54,794 55,730 54,953 51,426 61,076 62,322 50,040 66,360 75,486 79,342 712,341
    2020 58,234 45,538 33,979 41,481 54,486 63,656 71,353 70,216 63,989 70,351 86,738 89,946 749,967
    Change (%)b +0.3d +6.6d –38.0d –25.6e –0.8d +23.8d +16.8c +12.7c +27.9d +6.0e +14.9e +13.4e +5.3d
    2021 71,854 53,705 77,830 80,429 75,125 80,172 83,025 73,438 66,140 88,403 103,484 110,378 963,983
    Change (%)b +23.7d +25.7d +42.0d +44.3d +36.7d +55.9d +35.9d +17.8d +32.2d +33.2e +37.1e +39.1d +35.3d
    Old age
    2019 14,307 10,901 16,887 17,485 16,366 14,729 16,227 13,111 12,111 16,619 16,260 15,567 180,570
    2020 14,649 11,804 9,836 12,992 17,295 19,807 19,740 15,618 15,525 17,476 20,182 19,053 193,977
    Change (%)b +2.4e +8.3d –41.8d –25.7e +5.7d +34.5d +21.6d +19.1d +28.2c +5.2e +24.1d +22.4d +7.4e
    2021 17,856 13,490 23,705 23,719 19,366 19,426 20,761 16,569 16,663 22,881 23,643 22,208 240,287
    Change (%)b +24.8d +23.8d +40.4d +35.7d +18.3d +31.9d +27.9d +6.4d +37.6d +37.7d +45.4d +42.7e +33.1d
    Table 1. Number of Patients Who Underwent Colonoscopya

    Colonoscopy was defined as colonoscopy without any therapeutic interventions (E7660).

    Change (%) means the percentage of change in 2020 or 2021 compared to that of 2019.

    Statistical significance was expressed with cP<0.05, dP<0.001, eP≥0.05 (no significance).

    Table 2. Number of Patients Who Visited Hospital for Colorectal Cancersa

    Colorectal cancer was defined as colorectal cancers (C18, C19, C20) including carcinoma in situ of colon and rectum (D010, D011, D012).

    Change (%) means the percentage of change in 2020 or 2021 compared to that of 2019.

    Statistical significance was expressed with cP<0.05, dP<0.001, eP≥0.05 (no significance).

    Table 3. Number of Patients Who Underwent Operations for Colorectal Cancersa

    Operations for colorectal cancer was defined as colectomy (QA671, QA672, QA673, QA679, Q2671, Q2672, Q2673, Q2679, Q1261, Q1262) and/or surgical resection of rectum/sigmoid colon (QA921, QA922, QA923, QA924, Q2921, Q2922, Q2923, Q2924, Q2927, Q9292, QA928, Q2928) in patients with colorectal cancer.

    Change (%) means the percentage of change in 2020 or 2021 compared to that of 2019.

    Statistical significance was expressed with cP<0.05, dP<0.001, eP≥0.05 (no significance).

    Table 4. Number of Patients Who Underwent Colonoscopic Polypectomiesa

    Colonoscopic polypectomy was defined as single colonoscopic polypectomy (Q7701), multiple colonoscopic polypectomy (Q7702), endoscopic mucosal resection (Q7703) and endoscopic submucosal dissection (QX706).

    Change (%) means the percentage of change in 2020 or 2021 compared to that of 2019.

    Statistical significance was expressed with cP<0.05, dP<0.001, eP≥0.05 (no significance).


    Intest Res : Intestinal Research
    Close layer
    TOP