Introduction

Colorectal cancer is the second most common cause of cancer-related death in the world [1]. To improve the survival rate of colorectal cancer patients, many efforts and developments have been made in various fields such as early detection, surgical methods, and chemotherapy [2-7]. Surgical treatment is one of the most important treatments for colorectal cancer. Depending on the timing of diagnosis and state of the colorectal cancer, surgical methods may vary, including elective or emergency surgery, laparoscopic or open surgery. Also, variations were also observed in other treatment methods, including radiation and chemotherapy, as well as in operative outcomes such as operation time and postoperative complications.

Considering the rapid transmission rate and the high morbidity and mortality, the World Health Organization declared coronavirus disease 2019 (COVID-19) a pandemic in March 2020 [8]. The COVID-19 pandemic has had a significant global impact on all diseases, including colorectal cancer [9]. It has been reported that the COVID-19 pandemic has affected the entire clinical process, including screening, treatment, and surgical and oncological outcomes of colorectal cancer [10-15]. Some studies have reported delays in treatment and increased related mortality in colorectal cancer during the COVID-19 pandemic [13-15]. Most studies have focused on management of the inevitable delay in surgery and have suggested the application of preoperative (neoadjuvant) treatment as an alternative [13,14,16].

Though COVID-19 has become endemic, the effects of potential emergence of other such infectious diseases on other various diseases, including colorectal cancer, must be considered. Analyzing the effect of the past COVID-19 pandemic on the treatment of colorectal cancer is essential to better prepare for similar future situations. Therefore, the aim of this study is to review the changes in the surgical treatment of colorectal cancer caused by the COVID-19 pandemic at a local tertiary medical institution in Korea.

Methods

Ethical statements: The study protocol was approved by the Institutional Review Board (IRB) of the Kosin University Gospel Hospital (IRB No. KUGH 2024-11-012) and conducted in accordance with the principles outlined in the Declaration of Helsinki. The requirement for informed consent was waived by the IRB.

A total of 757 patients who underwent colorectal cancer surgery at Kosin University Gospel Hospital from January 2019 to December 2021 was enrolled. Patients were divided into the pre-pandemic (321 cases, January 2019–February 2020) and pandemic (436 cases, March 2020–December 2021) groups. Medical records were reviewed retrospectively for demographics, diagnostics (asymptomatic vs. symptomatic), tumor location (right-side colon, left-side colon, and rectum), preoperative serum carcinoembryonic antigen (CEA) level, obstruction and perforation status, operation methods, adjacent organ invasion, combined organ resection, postoperative complications, and pathology results.

Asymptomatic diagnosis was defined as cases diagnosed through health screening or incidentally during other medical processes. Symptomatic diagnosis was defined as cases diagnosed based on symptoms related to colorectal cancer. Tumor location was divided into three groups: the right-side colon (including the cecum, ascending colon, hepatic flexure colon, and transverse colon), the left-side colon (including the splenic flexure colon, descending colon, sigmoid colon, and rectosigmoid colon), and the rectum. In the pathologic results, carcinoma in situ cases were classified as stage 0 and T-stage 0.

Statistical analysis was performed with IBM SPSS ver. 22.0 (IBM Corp.). Student t-test was used to compare normally distributed variables. Comparisons between groups of discrete variables were performed using Wilcoxon rank-sum test or chi-square test as appropriate. All p-values <0.05 were considered statistically significant.

Results

Demographics are summarized in Table 1. The mean age (66.09 years vs. 67.22 years) and sex distribution showed no significant differences. Additionally, there were no significant differences in diagnostic processes (asymptomatic vs. symptomatic), tumor location (right-side colon, left-side colon, and rectum), preoperative serum CEA level (<10 ng/dL vs. ≥10 ng/dL), or cases of obstruction or perforation. However, asymptomatic diagnosis showed a decreasing trend in the pandemic group (48.9% vs. 44.0%; p=0.239). Cases of obstruction or perforation were similar in the two groups.

Surgical treatment patterns are summarized in Table 2. The proportion of emergent operations was similar in the two groups (2.8% vs. 1.1%; p=0.094). Laparoscopic operation was performed more frequently during the pandemic period (73.8% vs. 80.8%). Combined organ resection trended toward greater frequency in the pandemic group but the difference was not significant (6.2% vs. 13.5%; p=0.06). The most commonly resected organ in the non-pandemic group was the urinary bladder (5 cases), while those in the pandemic group were the uterus and ovary (13 cases).

Pathologic data are presented in Table 3. Compared to cancer of stages 2, 3, and 4, cancer at stages 0 and 1 was significantly less frequent in the pandemic group (25.8% vs. 18.3%; p=0.008), as was T-stage 0 (2.8% vs. 0.4%; p=0.041).

Discussion

This study analyzed changes in the surgical treatment of colorectal cancer caused by the COVID-19 pandemic at a local tertiary medical institution. In this study, asymptomatic diagnosis showed a decreasing trend in the pandemic group (48.9% vs. 44.0%; p=0.239). Similarly, surgeries for stages 0 and 1 colorectal cancer showed a declining trend during the COVID-19 pandemic period. This suggests that the number of presenting early-stage colorectal cancer cases decreased compared to the pre-pandemic period due to factors such as reduced accessibility to hospitals, decreased medical health screening, and delayed surgeries.

Shaukat and Church [10] reported that screening rates for colorectal cancer decreased during the COVID-19 pandemic in the USA. With the decline in number of medical health screenings, it was expected that symptomatic diagnosis and presenting advanced colorectal cancer cases would increase. With limited hospital accessibility and delays in surgery, an increase in surgeries for advanced cancer was anticipated. However, Kim et al. [17] have reported that the diagnostic pathway and non-screening (symptomatic diagnosis) rate were not different significantly (64.1% vs. 63.6%; p=0.710) during the COVID-19 pandemic. They also reported that a diagnosis due to clinical symptoms (symptomatic diagnosis) was associated with a more advanced stage (TNM stage 3 or 4) at diagnosis. In this study, there was no significant difference in the proportion of diagnostic processes (asymptomatic vs. symptomatic). However, asymptomatic diagnosis showed a decreasing trend in the pandemic group (48.9% vs. 44.0%; p=0.239). This result showed that diagnosis through health screening and presenting cases of early-stage colorectal cancer decreased during the COVID-19 pandemic.

It can be hypothesized that preoperative serum CEA levels will increase as the incidence of detected early colorectal cancer decreases. Lim et al. [18] reported that preoperative serum CEA level was higher in the COVID-19 pandemic period (8.59 ng/mL vs. 14.7 ng/mL; p=0.021), though there was no significant difference in the proportion of elevated preoperative serum CEA level (≥5 ng/mL; 61.8% vs. 69.1%; p=0.163). The present study showed a similar result (≥10 ng/dL; 19.0% vs. 22.2%; p=0.278).

As hospital accessibility was poor and surgery was delayed during the COVID-19 pandemic, it was expected that the number of obstruction or perforation cases would increase. However, in this study, the proportion of obstruction or perforation cases in colorectal cancer surgery did not differ significantly, in agreement with other previous studies [16,18,19]. Choi et al. [16] reported that perforation, abscess, or obstruction cases did not differ significantly in a no-preoperative chemoradiation group before and during the pandemic (5.8% vs. 4.8%; p=0.4111). Lim et al. [18] reported similar results for obstruction (15.4% vs. 14.5%; p=0.577) and perforation (1.2% vs. 1.5%; p=0.524).

In Korea, there are limited reports on emergent operations for colorectal cancer during the COVID-19 pandemic period. Lim et al. [18] reported that emergent operations did not increase in cases of curative surgery without neoadjuvant therapy (0.3% vs. 0.2%; p>0.999). Park et al. [19] reported comparable results (4.3% vs. 0%), attributing them to referral of emergent or urgent cases to other hospitals due to disruption of normal medical management. The present study showed no significant difference in the proportion of emergent operation (2.8% vs. 1.1%; p=0.094).

Choi et al. [16] reported a significant increase in the number of adjacent organ resection surgeries (2.8% vs. 4.8%; p=0.017), in similar results of the present study (6.2% vs. 13.5%; p=0.06). The most commonly resected organs in combined surgeries were the uterus and ovary, bladder, and small bowel.

In this study, early-stage colorectal cancer of stage 0 or 1 was significantly decreased in the pandemic group (25.8% vs. 18.3%; p=0.008). Similarly, T-stage 0 was lower in the pandemic group (2.8% vs. 0.4%; p=0.041). Although the impact was minimal, it can be attributed to the reduced access to medical facilities and delays in medical procedures during the pandemic. However, other studies have reported different results. Kim et al. [17] reported a larger proportion of early-stage cases (TNM stage 1 or 2) during the pandemic period and a lower risk of diagnosis with an advanced stage compared to the pre-pandemic period (odds ratio, 0.768; 95% confidence interval, 0.647–0.911). Choi et al. [16] reported no significant difference in the pathological TNM stage distribution between pre-COVID and COVID periods. The proportions of patients with tumors limited to the bowel (Tis to T2) were similar at 34.5% during the pre-COVID period and 35.4% during the COVID period. The authors provided an explanation for why there was no stage upshift at diagnosis or treatment delay in Korea. Unlike many other countries, Korea did enforce national or regional lockdowns, apart from a short-term localized lockdown. As a result, the impact of stage shifts caused by cancellations of cancer screenings or delays in cancer diagnosis due to medical facility closures or restrictions on social mobility was insignificant. However, Choi et al. [16] reported a significantly larger proportion of stage IV patients who were initially unresectable in the COVID group compared to the pre-COVID group (82.8% vs. 91.0%; p<0.05). The differing results among studies suggests that multi-institutional analyses including a larger number of subjects or studies using big data should be performed in the future.

In conclusion, during the COVID-19 pandemic, the proportion of asymptomatic diagnoses and surgeries for early-stage colorectal cancer (stage 0 and 1) decreased, while combined adjacent organ resection increased pattern. These changes in surgical treatment are likely to influence oncologic outcomes. Further long-term follow-up studies are necessary to evaluate the impact on colorectal cancer patients treated during the pandemic period.

Article information

Conflicts of interest

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

Funding

None.

Author contributions

Conceptualization; Formal analysis: YM, Seung Hyun Lee. Data curation: YM. Investigation; Methodology: all authors. Project administration; Resources; Supervision; Validation: Seung Hyun Lee. Visualization: YM. Writing-original draft: YM. Writing-review & editing: all authors. All authors read and approved the final manuscript.

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