The impact of the COVID-19 pandemic on clinical practices related to colorectal cancer and colonoscopy in South Korea: a nationwide population-based study

Article information

Intest Res. 2024;.ir.2024.00066

Publication date (electronic) : 2024 November 29

doi : https://doi.org/10.5217/ir.2024.00066

Jin Young Yoon, Moon Hyung Lee, Min Seob Kwak, Jae Myung Cha

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

Correspondence to Jae Myung Cha, Department of Gastroenterology, 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 2024 May 10; Revised 2024 July 26; Accepted 2024 September 21.

Abstract

INTRODUCTION

Since the first occurrence of coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in early December 2019 in Wuhan, China, it has rapidly spread worldwide [1]. The World Health Organization (WHO) declared COVID-19 a public health emergency on January 30, 2020 and subsequently a pandemic on March 11, 2020. In Korea, the first case of COVID-19 was reported on January 20, 2020, and thereafter spread nationwide with regional outbreaks [2]. The rising severity and mortality from COVID-19 infection has caused increasing fear in individuals, leading governments to implement lockdowns and concentrate limited medical resources on places to fight against COVID-19. Therefore, most healthcare delivery systems worldwide were put on hold and were forced to face significant challenges. As there was evidence for the presence of SARS-CoV-2 RNA in stool specimens and the potential risk of viral transmission through fecal and oral routes, the current major guidelines, including the American Gastroenterological Association, the British Society of Gastroenterology, and the U.S. Surgeon General and the American College of Surgeons, recommended that all elective endoscopic procedures, such as screening, therapeutic colonoscopy, and gastrointestinal surgery, should be delayed in asymptomatic patients during the COVID-19 pandemic [3-5]. As a result, several studies reported a decline in colorectal cancer (CRC) screenings, new CRC diagnosis, and CRC-related surgical procedures in the early stages of the COVID-19 pandemic [6-8].

We are still in the midst of the endemic of COVID-19 despite of worldwide COVID-19 vaccination, because the complete eradication of COVID-19 has not been declared. In addition, many experts are warning that the next pandemic will be coming. Therefore, we should have information on the changes of clinical practices related to CRC during COVID-19 pandemic to develop an optimal strategy on CRC screening and management during pandemic. However, there has been little data on this issue in Korea.

In this study, we aimed to assess the changes of clinical practices related to CRC screening and management during the COVID-19 pandemic, based on nationwide population-based data in Korea.

METHODS

RESULTS

1. Volume of Diagnostic Colonoscopy

The total annual number of patients undergoing diagnostic colonoscopies decreased by 6.9% in 2020 but increased by 8.1% in 2021 compared to that in the pre-COVID-19 era (2019) (Table 1). Considering the monthly number of patients undergoing diagnostic colonoscopies, those in March 2020, the first surge of COVID-19, marked the largest drop by 43.8% compared with those in the same month in 2019, followed by 32.8% in April, and by 10.9% in May (Fig. 1). Since June 2020, the total number of patients undergoing diagnostic colonoscopies has started to catch up and even exceeded in most of the months compared to the same month in 2019, except for an 8.1% decrease in October 2020, during which there was a second surge of COVID-19 infection. It had gone up by 26.0% in June 2021 compared to that in June 2019.

Table 1.

A Year-Wise Comparison of the Number of Patients per Month Who Underwent Diagnostic Colonoscopies^a in South Korea

Fig. 1.

A year-wise comparison of monthly number of patients who underwent diagnostic colonoscopies in South Korea.

Compared to those in March 2019, the number of diagnostic colonoscopies in men decreased by 41.4% in March 2020, increased by 8.9% in March 2021, while those in women, decreased by 46.2% and increased by 19.2% (Supplementary Fig. 1). The number of outpatient-based diagnostic colonoscopies decreased by 45.9% in March 2020 and increased by 15.3% in March 2021, while that of inpatient-based decreased by 22.9% and increased by 1.6% (Supplementary Table 2). The number of diagnostic colonoscopies in primary, secondary, and tertiary care centers decreased by 46.3%, 45.2%, and 25.1%, respectively, in March 2020, and increased by 20.5%, 5.5%, and 19.3%, respectively in March 2021.

2. Volume of Therapeutic Colonoscopy

The total annual number of patients undergoing therapeutic colonoscopies increased by 6.0% in 2020 and notably by 37.7% in 2021 compared with those in 2019 (Table 2). Compared to that in the same month during the pre-COVID-19 era, the number of patients undergoing therapeutic colonoscopies reduced by 37.5%, 25.2%, and 1.1%, respectively in only March, April, and May 2020. Since June 2020, it started to increase compared to the same month in 2019, and the increase has been maintained in all subsequent periods. Those in March, April, and May 2020 with decrease in monthly comparison rather markedly increased in 2021 and increased by 43.2%, 44.3%, and 35.3% respectively compared with those in 2019 (Fig. 2).

Table 2.

A Year-Wise Comparison of the Monthly Numbers of Patients Who Underwent Therapeutic Colonoscopies^a in South Korea

Fig. 2.

A year-wise comparison of the monthly number of patients who underwent therapeutic colonoscopies in South Korea.

Compared to that in March 2019, the number of therapeutic colonoscopies in men decreased by 36.5% in March 2020, increased by 35.6% in March 2021, and in women decreased by 39.0% and increased by 54.6%, respectively (Supplementary Fig. 2). The number of outpatient-based therapeutic colonoscopies decreased by 36.6% in March 2020 and increased by 51.3% in March 2021, and that of inpatient-based decreased by 22.7% and increased by 19.6%, respectively (Supplementary Table 3). The number of therapeutic colonoscopies at primary, secondary, and tertiary care centers decreased by 36.5%, 42.0%, and 18.7%, respectively, in March 2020, and increased by 55.6%, 25.3%, and 42.3%, respectively in March 2021.

3. Operations for CRC

Table 3 shows the monthly numbers of patients who underwent CRC surgery in Korea with a year-wise comparison. The annual number of patients operated for CRC decreased by 4.2% in 2020 and increased by 2.3% in 2021 compared with that in 2019 (Fig. 3). A monthly comparison of the number of patients operated for CRC began to decrease by 7.4% in March 2020, marking the biggest drop of 24.1% in April 2020, followed by a 9.2% decrease in May 2020. Unlike a considerable increase in the volume of colonoscopies in 2021, the number of patients operated for CRC did not have a notable increase in 2021.

Table 3.

A Year-Wise Comparison of the Number of Patients Who Underwent Operations^a for Colorectal Cancers in South Korea on a Monthly Basis

Fig. 3.

A year-wise comparison of the monthly number of patients who underwent surgery for colorectal cancers in South Korea.

Compared to those in April 2019, the monthly number of patients operated for CRC in men decreased by 27.8% in April 2020, when the impact of COVID-19 maximized for operations, and by 8.6% in April 2021. In women, it decreased by 18.3% in April 2020 and increased by 6.6% in April 2021 (Supplementary Fig. 3). The number of patients who underwent surgery for CRC in April 2020 and 2021 decreased by 30.2% and 3.4%, respectively, at secondary care centers and decreased by 21.0% and 2.1%, respectively, in tertiary care centers compared with those in April 2019 (Supplementary Table 4).

4. Treatment of CRC

The annual number of patients treated for CRC in South Korea decreased by 2.8% in 2020 and increased by 4.4% in 2021 compared to that in 2019 (Table 4). For the monthly number of patients treated for CRC, there was an 11.3% decrease in March 2020, but an 8.4% increase in March 2021. The observed change was within 10% for the rest of the months (Fig. 4).

Table 4.

A Year-Wise Comparison of the Monthly Number of Patients Claimed to Have Colorectal Cancers^a in South Korea

Fig. 4.

A year-wise comparison of the monthly number of patients who claimed to have colorectal cancer in South Korea.

Compared to that in March 2019, the monthly number of patients with any treatment for CRC in men decreased by 9.9% in March 2020 and increased by 8.5% in March 2021. For women, it decreased by 13.4% in March 2020, and increased by 8.4% in March 2021 (Supplementary Fig. 4). The number of patients receiving treatment as an outpatient decreased by 11.4% in March 2020 and increased by 11.6% in March 2021 and that of those as inpatients decreased by 8.0% and 2.7% in both years, respectively (Supplementary Table 5). The number of patients receiving treatment in the primary, secondary, and tertiary care centers decreased by 1.2%, 12.1%, and 11.3%, respectively in March 2020, and increased by 27.1%, 1.9%, and 11.7% in March 2021, respectively.

To analyze the claims data in more detail, we made a monthly comparison of the number of hospital visits, length of hospital stay, and total medical expenses per person in March (Table 5). The number of hospital visits per person in March increased from 2.39 times in 2019 to 2.53 times in 2020. Those in the remaining months of 2020 had fewer hospital visits than those in March. The length of hospital stay per person in March also increased from 5.08 days in 2019 to 5.39 days in 2020 and decreased by 4.79 days in 2021. An increase in the total medical expenses per person from KRW 1,443,000 in March 2019 to KRW 1,602,000 in March 2020 and a decrease by KRW 1,525,000 in March 2021 was noted. Primary, secondary, and tertiary care centers showed the same trend in total medical expenses in March, which was at a cost of KRW 159,000 in 2019, 187,000 in 2020, and 172,000 in 2021 in primary care centers; KRW 1,312,000, 1,388,000, and 1,304,000 in secondary care centers; and KRW 1,461,000, 1,673,000, and 1,605,000 in tertiary care centers (Supplementary Table 6).

Table 5.

A Year-Wise Comparison of the Details of Claims Data for Treatment of Colorectal Cancer^a in South Korea

DISCUSSION

This nationwide study is the first to provide real data, rather than modelled estimates, for the changes of clinical practices related to CRC during COVID-19 pandemic. The number of people receiving diagnostic colonoscopy, therapeutic colonoscopy, and any treatment for CRC decreased the most in March 2020, the first surge of COVID-19; additionally, the number of patients undergoing CRC surgery decreased the most in April 2020, with a 1-month delay, as compared to the monthly number in 2019, the pre-COVID-19 era. Since then, the COVID-19 pandemic has continued globally without any reduction in infectivity; however, the clinical practices related to CRC recovered to the level as before the pandemic 3 months later in June 2020 and exceeded that of the pre-pandemic numbers almost every month by 2021. Notably, the highest number of hospital visits, the longest length of hospital stays, and the highest medical cost per person among patients treated for CRC was recorded in March 2020.

In comparison to the corresponding month of each year, our Korean national data reported a 43.8% reduction in the number of diagnostic colonoscopies and a 37.5% reduction in that of therapeutic colonoscopies in March 2020. Another Korean study from a single center in Daegu City, the epicenter of the first serious outbreak, reported a 70.8% reduction (from 380 to 111 cases) in non-emergent colonoscopy between February 19 and March 28, 2020 [13]. Western countries also showed that a reduction in colonoscopy volume during the COVID-19 pandemic was over 90% in the New York metropolitan area [14], up to 85.6% using the French national health data [15], 92% based on 4 population-based datasets of England [16], and 59% in the population-based study from Hong Kong compared to those prior to COVID-19 [17]. Our study showed that a reduction in colonoscopy volume in South Korea was relatively smaller than those in other countries. This might be explained by the fact that the Korean government has implemented strict quarantine measures, but has not implemented lockdown, while most countries had locked down to prevent COVID-19 transmission. Since the WHO declared COVID-19 a global pandemic on March 11, the largest decline in clinical practice affected by COVID-19 occurred in April 2020 in most countries, while it occurred 1 month earlier, in March 2020, in our study [14-20]. We assumed that the Korean government determined the rapid implementation of a strict infection control policy, which resulted in an earlier decrease in the number of endoscopic procedures compared to that in other countries. Comparing data from South Korea and other countries on COVID-19, the policy decision to lock down the community in response to an infection outbreak has a significant impact on the medical use behavior of the population.

Our notable finding was that the number of CRC patients screened and treated quickly bounced back after March 2020, the first surge, catching up since June 2020, and then started to exceed and outgrow throughout 2021, the second year, compared to that in the pre-COVID-19 era despite the ongoing COVID-19 pandemic. This phenomenon may be explained as follows. At the beginning of the COVID-19 pandemic, no direct evidence on the safety of colonoscopic procedures for viral transmission was identified, and the possibility of COVID-19 spread by aerosolization generated during colonoscopy was raised.3 However, the data accumulated to date showed that there are no cases of SARS-CoV-2 transmission through colonoscopy [21,22]. This suggests that resuming colonoscopy may pose a very low risk of SARS-CoV-2 transmission in the real world. As the COVID-19 pandemic was long-lasting, the demand for colonoscopy seems to have revived quickly. An alternative explanation is that declining COVID-19 severity and mortality over time have improved adherence to colonoscopy and surgery and visiting the hospital for treatments. A previous study demonstrated that higher perceived seriousness and lower perceived barriers are important factors influencing good adherence to colonoscopy [23]. As the pandemic continues, perceived seriousness, namely concern about the possibility of missing potential malignancies, has grown more and more than the perceived barriers and fear of potential risk of COVID-19 infection.

We also observed that the range of change in the number of colonoscopies in women was wider than that in men during the COVID-19 pandemic. Although the number of both diagnostic and therapeutic colonoscopies in 2020 decreased more in women than in men, the numbers increased even more in women in 2021 as per our data. This could be due to the differences with respect to sex in health behavior between women and men, because women are more interested in health-related information and might pay more attention to potential worldwide pandemics of COVID-19 than men [24]. Furthermore, women showed sex differences in the COVID-19 attitudes and health behaviors as they are more likely to perceive the pandemic as a very serious health problem and agree with restraining measures [25,26]. Our findings may indicate that health care resources should consider the sex difference in estimating the impact of infectious pandemics on screening and treatment of CRC.

A study conducted in the United States with health insurance claims data showed that face-to-face office visits decreased by 68% and telemedicine increased by 40.8% in April 2020 compared to that in April 2019 [19]. In our data, there was only a small reduction (11.3%) in face-to-face visits among those diagnosed with CRC. It is speculated that the seriousness of CRC was more than concerns regarding COVID-19 infection due to lower severity and mortality in Korean COVID-19 [27]. Contrastingly, our data showed the longest length of hospital stays and the highest medical cost per person visiting a hospital due to CRC in March 2020. This implies that CRC patients who visit hospitals even during a pandemic, despite the possibility of COVID-19 transmission, may have more severe disease conditions in terms of severity and comorbidities. In addition, our data revealed that the number of diagnostic and therapeutic colonoscopies and CRC operations at tertiary centers decreased lesser than those performed at primary or secondary centers during the pandemic, and the inpatient-based procedure decreased lesser than the outpatient-based procedure, suggesting that essential care for the diagnosis and treatment of CRC is relatively less affected by the COVID-19 pandemic.

Several studies have reported concern over the pause and delay in CRC screening due to COVID-19, which leads to increased healthcare burden afterwards, subsequent staging at diagnosis, and mortality of CRC [18,28-31]. Several researchers have assumed that the decline in CRC screening will continue for a significant period of time. Several modeling studies predicting the consequences of a delayed CRC diagnosis were conducted with the assumption that the postponement in CRC screening due to the COVID-19 pandemic would be maintained for 5 years in a U.K. study [18], for 3 years in a U.S. study [6], for 2 years in a Canadian study [32], and for 6 months without catching up of missed screens in a Netherlands study [33]. To minimize pandemic-driven CRC screening disruption, several strategies were devised, including an approach depending on individual risk stratification for developing CRC [34,35], open access colonoscopy, which serves as a scheduled colonoscopy without pre-evaluation before the procedure for fewer hospital visits [36], fecal immunochemical test kit delivered using postal mail for eliminating unnecessary visits for patients with negative results [37], and the active application of telemedicine or smartphone apps [38,39]. This evidence was derived from population data during the early period of the COVID-19 pandemic. These situations might have been overestimated in terms of the actual long-term impact of the COVID-19 pandemic on the backlog of screening procedures and surveillance outcomes relating to CRC because they should have considered lowered severity and mortality of COVID-19 obtained from widely available vaccines and therapeutic agents, lesser fear of colonoscopy-induced transmission of COVID-19 based on the accumulation of data, and compensation for the postponed examination in the following year, as shown in our data. Our data indicate that if healthcare providers manage to sustain the colonoscopy capacity, the backlog related to CRC may be cleared by the mid-2021 despite the interference of COVID-19 in the Asian-Pacific region, where there were fewer cases and deaths from COVID-19.

The use of HIRA enabled us to perform the largest study to date that assessed the impact of COVID-19 on CRC, and the results are virtually free from referral bias and readily generalizable owing to the population-based design. However, this study has some limitations. The data derived from administrative coding systems have inherent limitations in terms of miscoding or data entry errors. We also concede that one of the limitations of our study pertains to secondary data with limited information for the indication of each colonoscopy and operation for CRC and no specific details of the clinical information for the patients in the HIRA. In addition, we could not analyze the differences in stage of CRC, overall survival and disease-free survival of CRC before and after COVID-19. Additional research on these topics may improve our understanding of the impact of the pandemic crisis of COVID-19 on clinical practice of CRC. Finally, as cases and deaths of COVID-19, healthcare systems and pandemic responses differ across countries, our findings cannot be generalized to other countries.

In conclusion, our nationwide study showed that negative impacts of the COVID-19 pandemic on clinical practices related to CRC completely recovered within second year of the pandemic. It could be considered for the development of an optimal strategy on CRC management in response to the pandemic-driven crisis.

Supplementary Material

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

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