Introduction

The outbreak of the coronavirus disease 2019 (COVID-19) pandemic has had a substantial influence on healthcare systems worldwide. Many countries have implemented strict measures, including lockdowns and stay-at-home orders, to contain the spread of the virus. These measures have had a pivotal influence on the treatment of surgical diseases, including acute appendicitis (AA) [1-5]. However, Korea has implemented a unique response to the COVID-19 pandemic, which has allowed for the continuation of elective surgeries and prompt treatment of emergency cases without needing a lockdown [6,7].

AA is one of the most common surgical emergencies. Delaying its treatment can lead to life-threatening complications such as perforation and peritonitis. The COVID-19 pandemic has raised concerns about the management of AA, as hospitals have had to balance the need to provide timely surgical interventions and the need to prevent COVID-19 transmission [8-10].

This study aimed to evaluate the impact of the COVID-19 pandemic on the treatment of AA in Korea, a country without a lockdown. We analyzed changes in timing of surgery, severity of disease, and outcomes of surgery during the pre-pandemic period and the pandemic period.

Methods

Ethical statements: The protocol was approved by the Institutional Review Board of Kosin University Gospel Hospital (No. KUGH 2021-09-025). This study was performed in accordance with the Declaration of Helsinki. Informed consent was waived by the IRB.

This retrospective study was conducted at Kosin University Gospel Hospital, Korea. We identified all adults and pediatric patients diagnosed with AA and treated with a surgical procedure after they visited the emergency department. The primary outcome of this study was to determine the proportion of patients with complicated AA during the pre-pandemic period and the pandemic period.

1. Study population

We reviewed records of all patients who were treated with a surgical procedure for AA during two discretionary time periods: a control period from January 1, 2019, to February 28, 2020; and a COVID-19 period from March 1, 2020, to April 30, 2021. The COVID-19 period was set immediately after the COVID-19 real-time polymerase chain reaction (RT-PCR) test was performed on all febrile (37.5 °C) patients visiting the emergency department in Korea.

2. Definition

Most cases of AA were diagnosed using computed tomography (CT). For pregnant women and young children, ultrasonography was used. The severity of AA was determined only according to the operational records by the surgeon. Complicated AA was defined as inflammation of the appendix with presence of gangrene, evident necrosis, or perforation with local or generalized peritonitis written in operational records. Diagnostic delay time was defined as the time from the emergency room visit to the CT or ultrasonography examination. Preoperative delay time was defined as the time from the emergency room visit to the start of surgical procedure (Fig. 1).

3. Emergency surgery during COVID-19 period

Since March 2020, patients who visited the emergency department with symptoms of upper respiratory tract infection or fever underwent RT-PCR testing for COVID-19 in Korea. Patients without these symptoms were excluded from the COVID-19 test according to the emergency department specialist’s judgment and the selective procedure protocol for COVID-19. Patients with a fever or symptoms of upper respiratory tract infection underwent surgery and hospitalization only if the COVID-19 test result was negative. However, if emergency surgery was required before COVID-19 test results were available, a separate operating room was used, in accordance with the center's emergency surgery protocol. All medical staff participating in the surgery wore level D coveralls and surgical gowns, N95 respirators, goggles or face shields, double gloves, and overshoes. Medical personnel in charge of anesthesia and circulation nursing also wore surgical gowns, N95 respirators, surgical caps, surgical gloves, and overshoes (Fig. 2). The number of participants was minimized. After surgery, patients were transferred to a negative pressure isolation room of the surgical intensive care unit instead of the recovery room.

4. Statistical analysis

Data analyzed included demographics, presentation variables, preoperative assessments, and postoperative hospital stay. Before comparative analyses, continuous variables were evaluated for distribution normality using a Shapiro-Wilk statistic and normality plots to guide nonparametric testing. Data were then analyzed using independent t-test, Mann-Whitney U test, or Fisher exact testing. Results containing continuous variables are presented as means with standard deviations or medians with interquartile ranges based on normal distribution. Odds ratios (ORs) and 95% confidence intervals (CIs) are provided for pertinent categorical comparisons. To quantify the possible association for complicated AA during the COVID-19 period, a multivariate logistic regression analysis was performed for the outcomes having p-values less than 0.05 in univariate analysis. Statistical significance was assumed at p<0.05. Data analyses were performed using IBM SPSS for Macintosh version 27 (IBM Corp.) [11].

Results

We identified a total of 254 patients who underwent surgical procedures for AA during the two study periods. A total of 33 patients (13%) were excluded, including 26 who had previous abdominal surgery, five patients who underwent interval appendectomy, and two patients who were diagnosed with advanced gastric cancer during AA surgery. A total of 139 of the 221 eligible patients with AA were included in the COVID-19 cohort and 82 of the 221 eligible patients were included in the control cohort. The study flow diagram is shown in Fig. 3.

In the COVID-19 period, we collected data from 139 patients who underwent surgery for AA compared to 82 patients in the control period. We observed that the rate of AA patients who visited this center during the COVID-19 period was increased by 69%. Comparisons between the two groups showed no significant differences in variables such as age, sex, American Society of Anesthesiologists score, or severity of AA. Diagnostic delay time, postoperative hospital stays, surgical type, and surgical extent were also similar between the two periods. However, preoperative delay time, operative time, postoperative complication rate, and other hospital diagnosis rates significantly increased during the COVID-19 period compared to those during the control period (p=0.01, p=0.01, p=0.02, and p=0.01, respectively) (Table 1).

1. Analysis according to the fever

Since COVID-19 RT-PCR tests were performed for patients with a fever of 37.5 °C or higher, a case of 37.5 °C or higher was defined as fever. Those with the presence of fever and those with absence of fever were compared. Characteristics of the cohort of patients stratified according to the fever are summarized in Table 2.

For AA patients with body temperature 37.5 °C or higher, operative time was significantly longer during the COVID-19 period group (p<0.01). However, surgical procedure, surgery extent, diagnostic delay time, preoperative delay time, and postoperative hospital stay were not significantly different between the two periods. There was no significant difference in the rate of postoperative complication or other hospital diagnosis between the two periods either.

For the patients with AA whose body temperature at the time of emergency department visit was 37.5 °C or higher, the rate of complicated AA was significantly higher in the COVID-19 period than in the control period (p<0.01). Diagnostic delay time, preoperative delay time, and postoperative hospital stay were significantly longer in the COVID-19 period than in the control period (p<0.05) (Fig. 4). Postoperative complication rate and other hospital diagnosis rate were also significantly higher in the COVID-19 period group than in the control period group (p<0.01). However, there was no significant difference in the surgical procedure or the extent of surgery between two periods.

2. Multivariable logistic regression model for odds of the complicated AA

To ascertain what factor could predict for a complicated AA, multivariate analysis was performed. As shown in Table 3, age (p=0.019; 1.023; 95% CI, 0.49–2.93) and presence of fever (p<0.01;OR, 8.108; 95% CI, 6.92–67.34) were independent risk factors for a complicated AA. Receiver operating characteristic curve analysis revealed that the optimal cutoff of was 44 years for the occurrence of complicated AA, showing a sensitivity of 58.6% and a specificity of 65.2% (Fig. 5).

Discussion

COVID-19 has affected the world. In some countries, lockdowns and stay-at home orders by health authorities have affected the treatment of surgical disease requiring emergency surgery [1,10]. However, unlike other countries, Korea has implemented a thorough quarantine system since the early days of COVID-19 with a national system for treating COVID-19 patients at designated hospitals. Thus, it is estimated that the treatment of other diseases has not been affected by the COVID-19 pandemic in most private hospitals [6,7]. However, there is not much research on the direction of treatment or the results of treatment for AA during the COVID-19 period. Thus, it is necessary to highlight the special situation unique to Korea, different from other countries.

In Korea, surgical treatment is a standard treatment for AA [8,12]. Although Salminen et al. [13] reported that medical treatment for uncomplicated AA is feasible, the likelihood of surgery for recurrent appendicitis within 1 year was 27.3% and the likelihood of surgery within 5 years was 39.1%. Moreover, the cost for appendectomy and the total costs per patient for AA in Korea were approximately 1,300,000 KRW (1,100 USD) and 3,000,000 KRW (2,500 USD), respectively, which are not high compared to other developed countries, providing a basis for prioritizing surgical treatment. Additionally, during the decision-making process for AA, patients often prefer surgical treatment if a joint decision is made about surgical or medical treatment [14-16].

Several retrospective studies have reported that numbers of AA admissions and surgical procedures are significantly decreased during the COVID-19 period compared to those before the COVID-19 period with the same duration [3,9,17,18]. However, reasons for such decrease are not entirely clear. They may be related to changes in healthcare-seeking behavior, delayed or missing diagnoses, and other factors [18,19]. Bayissa et al. [20] have suggested that some cases of simple appendicitis might resolve spontaneously due to a change in the gut microbiome caused by the pandemic-related changes in diet and lifestyle.

Several studies conducted in Korea, distinct from other investigations within COVID-19 lockdown countries, have revealed that there is no notable variance in the incidence of AA throughout the pandemic when compared to the corresponding period in the previous year [21,22]. In our study, however, during the COVID-19 period, the number of patients who visited the emergency department for AA and received surgical treatment increased. Other studies have estimated that uncomplicated appendicitis could resolve spontaneously while staying at home during the COVID-19 pandemic [18,19]. However, Korea has never conducted a lockdown. Most of COVID-19 confirmed patients were treated at national-designated hospitals. The proportion of COVID-19 confirmed patients in local hospitals was extremely low [6,7]. Also, since Korea has better access to medical care and lower medical costs than other developed countries, it is estimated that there would be no significant obstacles to finding a hospital with AA during the COVID-19 pandemic [14]. Furthermore, the majority of doctors in Korea acknowledge that the primary treatment for AA is surgery. In addition, the general public in Korea perceives AA as a minor condition that can be resolved with little medical intervention or surgery. Therefore, it is speculated that the incidence of AA patients would not decrease during the pandemic in Korea and that surgeries for AA might have even increased in tertiary care facilities where surgical intervention is available.

Furthermore, it is thought that our hospital had its own reasons for the influx of AA patients during the COVID-19 period. In Korea, almost all abdominal emergency surgeries are performed by board certified surgical specialists. During the control period, there was a shortage of surgeons who could perform emergency surgery at Kosin University Gospel Hospital. From January 1, 2020, a new division called Emergency Surgery or Acute Care Surgery Team was created and three surgical specialists worked a total of 24 hours a day, allowing more emergency surgeries than before.

The majority of studies in the lockdown countries suggest that even though the incidence of AA decreased, the severity of AA increased during the COVID-19 period, with a higher incidence of complicated and perforated appendicitis, longer hospital stays, and high rates of postoperative complications. The delay in seeking medical care and delayed surgical intervention might have contributed to the worse outcomes observed during the pandemic period [3-5,9,17].

However, in Korea, a country that did not enforce a strict lockdown, the incidence of AA did not significantly decrease. A study in Korea found that delayed surgical treatment due to COVID-19 protocols resulted in a higher incidence of complicated AA and postoperative complications [22]. However, another study in Korea reported that surgical outcomes and postoperative complications were not significantly different between the pandemic period and the pre-pandemic period [23].

In our study, there was no significant difference in the frequency of complicated AA during the COVID-19 period compared to that in the control period. However, in the case of fever, the frequency of patients with complicated AA was increased during the COVID-19 period compared to that in control period.

AA is known to lead to gangrenous change, perforation, abscess, and peritonitis as inflammation progresses over time. In a recent study, a delay of 12 to 24 hours did not affect the postoperative outcome [12,24,25]. In our study, there was an average delay of 139 minutes until surgery in the COVID-19 period compared to the control period. However, it did not affect complex appendicitis. In the group with fever, the mean duration was 758 minutes (12.6 hours). Patients with AA, especially those with high fever, are known to have perforation potential [20]. There was no significant difference in the preoperative delay time in the two groups without fever. The significant difference in the preoperative delay time in the fever group is considered to be the main cause. Prehospital delay is considered to be very important during the time from symptom onset to surgery. However, prehospital delay was not included in this study because it was difficult to find out the exact time from patients’ medical records due to limitations of the retrospective study.

According to our study, the diagnostic delay time and preoperative delay time in patients with AA who had a fever of 37.5 °C or higher were significantly increased during the COVID-19 period compared to those during the control period. During the COVID-19 period, the waiting time for surgery for all AA patients increased compared to that during the control period. However, emergency room stay time, including the diagnostic delay time in patients with a fever of AA, was significantly longer during the COVID-19 period than that during the control period. Since March 2020, when patients with symptoms such as fever or respiratory infections visited the emergency room, a COVID-19 test was performed. During this time, all processes that required contact with patients were carried out very carefully to protect hospitals and medical staff. If a patient had a fever but was judged to have no association with respiratory infections, the diagnosis for conditions such as AA proceeded based on the decision of the emergency medicine specialist before confirming results of the COVID-19 test. This series of decision-making processes between medical staff protection and patient safety was very challenging.

Furthermore, if a patient with AA confirmed after a CT scan had a fever, according to surgical room response manual, surgery could only be performed after wearing protective gear or postponing surgery and hospitalization until COVID-19 PCR test results were obtained. Among all patients during the COVID-19 period, three patients underwent surgery while wearing level D personal equipment due to the need to wait for COVID-19 test results, which was expected to worsen the patient's condition. Two of the three cases were pregnant women with AA and the other was a pediatric patient with AA progressing with systemic inflammatory response syndrome accompanied by fever. The number of cases wearing level D coveralls during surgery was lower than the total number of AA surgery patients with fever during the COVID-19 period, which was attributed to the physical burden of wearing protective gear on surgeons and scopist. When performing a surgery while wearing protective gear, medical staff had to cope with intense heat, uncomfortable vision, and other difficulties. Additionally, according to the response manual, isolation in a single room is required after surgery. If a room for the patient was not available after surgery, the surgery had to be postponed.

According to our study, the frequency of postoperative complications was significantly increased during the COVID-19 period compared to that during the control period. There was no significant difference in the incidence of severe complications (Clavien-Dindo class 3 or higher) between the two periods. However, when subgroup analysis was performed based on the presence or absence of fever, there was no statistically significant difference in the frequency of complications between the two groups in the absence of fever. On the other hand, in patients with fever, the COVID-19 group had a significantly higher incidence of complications. The time elapsed before surgery in patients with AA accompanied by fever during the COVID-19 period might have increased the severity of patient’s condition. There were a total of four severe complications among all patients, including one case of percutaneous drainage for intraabdominal abscess, one case of postoperative bleeding, surgical repair for wound infection and dehiscence each, and one case of death.

In our study, we observed an increase in the number of patients diagnosed with AA at other local hospitals and transferred to our tertiary hospital during the COVID-19 pandemic. During the COVID-19 pandemic period, local hospitals might have hesitated to provide care for patients with fever. In fact, when a patient with fever visited the emergency room of a local hospital, some hospitals initially performed a COVID-19 RT-PCR test. After confirming a negative result, additional tests related to AA were conducted [7]. Even when diagnosed with AA after a CT scan, there were cases where patients were transferred to tertiary hospitals for treatment [6]. For these reasons, the frequency of patients diagnosed in other hospitals during the COVID-19 period might have increased since the control period.

Some studies have shown that older patients (usually those over the age of 60) have a higher risk of perforation and complications from AA than younger patients. This might be due to changes in the morphological and functional characteristics of the appendix with age, as well as differences in immune responses to infection [26-28]. Furthermore, in some studies, a higher fever has been associated with a more severe form of AA, such as perforation or gangrene [25,29]. Similarly, our multivariate analysis also confirmed that complicated appendicitis increased with age and the presence of fever.

As mentioned earlier, three patients with AA underwent laparoscopic appendectomy, wearing level D personal protective equipment. Outfitted on level D protective gear during surgery made it difficult to see the surgical field and caused significant discomfort due to the high temperature. Therefore, major surgeries that require more time and put physical strain on medical staff would be almost impossible.

Our study found that older patients and those with fever had a higher likelihood of increased severity of AA. In times of infectious disease outbreaks such as the COVID-19 pandemic, there is a serious need for discussion and consideration regarding surgical interventions for elderly patients with fever. It is necessary for us to understand and analyze our most vulnerable areas to cope with new diseases that may arise in the future.

The retrospective nature of this single-center study may pose limitations, such as selection bias. However, it is noteworthy as it analyzes a relatively large number of AA cases at a tertiary hospital in Korea during the COVID-19 pandemic. Subsequent multicenter studies may provide more robust and generalizable findings.

Article information

Conflicts of interest

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

Funding

None.

Author contributions

Conceptualization: YC, YK. Data curation: YK. Formal analysis: YC. Investigation: YK. Methodology: YC. Project administration: YK. Resources: YK. Software: YC. Supervision: YK. Validation: YK. Visualization: YC. Writing - original draft: YC. Writing - review & editing: YK. All authors read and approved the final manuscript.

Fig. 1.

COVID-19 and hospital delays. COVID-19, coronavirus disease 2019; ER, emergency room; CT, computed tomography; OP operation.

Fig. 2.

Level D coveralls and surgical gowns, N95 respirators, goggles or face shields, double gloves, and overshoes.

Fig. 3.

Diagram for the study.

Fig. 4.

(A, B) Diagnostic delay time and preoperative delay time were significantly longer in COVID-19 group in according to fever. (C, D) Postoperative hospital stay was significantly longer in COVID-9 group according to fever. COVID-19, coronavirus disease 2019.

Fig. 5.

Receiver operating characteristic (ROC) curve analysis to identify the occurrence of complicated acute appendicitis that the optimal cutoffs for age was 44 years, yielding 58.6% sensitivity and 65.2% specificity.

References

• 1. COVIDSurg Collaborative. Elective surgery cancellations due to the COVID-19 pandemic: global predictive modelling to inform surgical recovery plans. Br J Surg 2020;107:1440–9.ArticlePubMedPDF
• 2. Brindle ME, Gawande A. Managing COVID-19 in surgical systems. Ann Surg 2020;272:e1–2.ArticlePubMed
• 3. Sartori A, Podda M, Botteri E, Passera R, Agresta F, Arezzo A, et al. Appendectomy during the COVID-19 pandemic in Italy: a multicenter ambispective cohort study by the Italian Society of Endoscopic Surgery and new technologies (the CRAC study). Updates Surg 2021;73:2205–13.ArticlePubMedPMC
• 4. Orthopoulos G, Santone E, Izzo F, Tirabassi M, Perez-Caraballo AM, Corriveau N, et al. Increasing incidence of complicated appendicitis during COVID-19 pandemic. Am J Surg 2021;221:1056–60.ArticlePubMed
• 5. Fisher JC, Tomita SS, Ginsburg HB, Gordon A, Walker D, Kuenzler KA. Increase in pediatric perforated appendicitis in the New York city metropolitan region at the epicenter of the COVID-19 outbreak. Ann Surg 2021;273:410–5.ArticlePubMed
• 6. Kang J, Jang YY, Kim J, Han SH, Lee KR, Kim M, et al. South Korea’s responses to stop the COVID-19 pandemic. Am J Infect Control 2020;48:1080–6.ArticlePubMedPMC
• 7. Her M. How is COVID-19 affecting South Korea? What is our current strategy? Disaster Med Public Health Prep 2020;14:684–6.ArticlePubMed
• 8. Choi JH, Choi YI. Initial experience with single incision laparoscopic appendectomy by surgical resident. J Minim Invasive Surg 2018;21:65–9.Article
• 9. Kohler F, Muller S, Hendricks A, Kastner C, Reese L, Boerner K, et al. Changes in appendicitis treatment during the COVID-19 pandemic: a systematic review and meta-analysis. Int J Surg 2021;95:106148.ArticlePubMedPMC
• 10. Grossi U, Gallo G, Ortenzi M, Piccino M, Salimian N, Guerrieri M, et al. Changes in hospital admissions and complications of acute appendicitis during the COVID-19 pandemic: a systematic review and meta-analysis. Health Sci Rev (Oxf) 2022;3:100021.ArticlePubMedPMC
• 11. Kang G, Kim SE. How to write an original article in medicine and medical science. Kosin Med J 2022;37:96–101.ArticlePDF
• 12. Kim SH, Park SJ, Park YY, Choi SI. Delayed appendectomy is safe in patients with acute nonperforated appendicitis. Int Surg 2015;100:1004–10.ArticlePubMedPMCPDF
• 13. Salminen P, Tuominen R, Paajanen H, Rautio T, Nordstrom P, Aarnio M, et al. Five-year follow-up of antibiotic therapy for uncomplicated acute appendicitis in the APPAC randomized clinical trial. JAMA 2018;320:1259–65.ArticlePubMedPMC
• 14. Kim JW, Shin DW, Chae JJ, Kim JY, Park SG. Impact of the new payment system on laparoscopic appendectomy in Korea. J Surg Res 2015;199:338–44.ArticlePubMed
• 15. Haijanen J, Sippola S, Tuominen R, Gronroos J, Paajanen H, Rautio T, et al. Cost analysis of antibiotic therapy versus appendectomy for treatment of uncomplicated acute appendicitis: 5-year results of the APPAC randomized clinical trial. PLoS One 2019;14:e0220202.ArticlePubMedPMC
• 16. Newhall K, Albright B, Tosteson A, Ozanne E, Trus T, Goodney PP. Cost-effectiveness of prophylactic appendectomy: a Markov model. Surg Endosc 2017;31:3596–604.ArticlePubMedPDF
• 17. Willms AG, Oldhafer KJ, Conze S, Thasler WE, von Schassen C, Hauer T, et al. Appendicitis during the COVID-19 lockdown: results of a multicenter analysis in Germany. Langenbecks Arch Surg 2021;406:367–75.ArticlePubMedPMCPDF
• 18. Tankel J, Keinan A, Blich O, Koussa M, Helou B, Shay S, et al. The decreasing incidence of acute appendicitis during COVID-19: a retrospective multi-centre study. World J Surg 2020;44:2458–63.ArticlePubMedPMCPDF
• 19. Dick L, Green J, Brown J, Kennedy E, Cassidy R, Othman S, et al. Changes in emergency general surgery during COVID-19 in Scotland: a prospective cohort study. World J Surg 2020;44:3590–4.ArticlePubMedPMCPDF
• 20. Bayissa BB, Miressa F, Abulkadir A, Fekadu G. Predictors of complicated appendicitis among patients presented to public referral hospitals in Harari region, Eastern Ethiopia: a case-control study. Surg Pract Sci 2022;9:100072.Article
• 21. Choi HG, Kang HS, Lim H, Kim JH, Kim JH, Cho SJ, et al. Changes in the incidence rates of gastrointestinal diseases due to the COVID-19 pandemic in South Korea: A Long-Term Perspective. J Pers Med 2022;12:1144.ArticlePubMedPMC
• 22. Choi YS, Yi JW, Chung CTY, Shin WY, Choi SK, Heo YS. Clinical experience of emergency appendectomy under the COVID-19 pandemic in a single institution in South Korea. Medicina (Kaunas) 2022;58:783.ArticlePubMedPMC
• 23. Kim CW, Lee SH. Impact of COVID-19 on the care of acute appendicitis: a single-center experience in Korea. Ann Surg Treat Res 2021;101:240–6.ArticlePubMedPMCPDF
• 24. Shin CS, Roh YN, Kim JI. Delayed appendectomy versus early appendectomy in the treatment of acute appendicitis: a retrospective study. World J Emerg Surg 2014;9:8.ArticlePubMedPMCPDF
• 25. Drake FT, Mottey NE, Farrokhi ET, Florence MG, Johnson MG, Mock C, et al. Time to appendectomy and risk of perforation in acute appendicitis. JAMA Surg 2014;149:837–44.ArticlePubMedPMC
• 26. Lunca S, Bouras G, Romedea NS. Acute appendicitis in the elderly patient: diagnostic problems, prognostic factors and outcomes. Rom J Gastroenterol 2004;13:299–303.PubMed
• 27. Korner H, Sondenaa K, Soreide JA, Andersen E, Nysted A, Lende TH, et al. Incidence of acute nonperforated and perforated appendicitis: age-specific and sex-specific analysis. World J Surg 1997;21:313–7.ArticlePubMedPDF
• 28. Reinisch A, Reichert M, Ondo Meva CC, Padberg W, Ulrich F, Liese J. Frailty in elderly patients with acute appendicitis. Eur J Trauma Emerg Surg 2022;48:3033–42.ArticlePubMedPMCPDF
• 29. Sirikurnpiboon S, Amornpornchareon S. Factors associated with perforated appendicitis in elderly patients in a tertiary care hospital. Surg Res Pract 2015;2015:847681.ArticlePubMedPMCPDF

Figure & Data

References

Citations

Citations to this article as recorded by  

• Acute appendicitis surgery in the COVID-19 era: delays without deterioration of outcomes
  Sang-Yong Son
  Kosin Medical Journal.2025; 40(1): 1.     CrossRef