Abstract
Objectives:
This study evaluated the endoscopic management and clinical outcomes of patients with colonic diverticular bleeding (CDB) during the coronavirus disease 2019 (COVID-19) pandemic.
Methods:
A total of 388 hospitalized patients diagnosed with CDB at two hospitals during (April 2020-March 2023) and before (April 2017-March 2020) the pandemic were enrolled in the study. We performed one-to-one propensity score matching (PSM) on the participants. We analyzed endoscopic management and clinical outcomes before and during the pandemic using a total of 264 patients matched in a PSM analysis.
Results:
A total of 213 (1.3%) and 172 (1.2%) colonoscopies were performed before and during the pandemic, respectively in patients with CDB (P = 0.70). After PSM, the number of early colonoscopies (63.6% vs. 76.5%, P = 0.03) and colonoscopies performed outside regular working hours (23.8% vs. 47.7%, P < 0.01) was significantly lower during the pandemic than before it. A univariate logistic regression analysis revealed that the risks of rebleeding within 30 days (odds ratio [OR]: 0.81, P = 0.42) and composite outcome (OR: 0.90, P = 0.69) were not increased during the pandemic.
Conclusions:
During the pandemic, the number of early colonoscopies and colonoscopies performed outside regular working hours decreased; however, this decrease did not influence rebleeding and composite outcome in patients with CDB.
Keywords: coronavirus disease-2019, emergency, colonoscopy, colonic diverticular bleeding, pandemic
Introduction
The coronavirus disease 2019 (COVID-19) has severely disrupted medical care worldwide. Although COVID-19 is primarily transmitted via droplets and aerosols[1,2], the potential for fecal-oral transmission[3,4] cannot be denied; therefore, the recommendation was to avoid unnecessary endoscopies to prevent transmission between patients and medical staff during the COVID-19 pandemic[5-7].
Owing to the global outbreak of respiratory infection during the COVID-19 pandemic, screening and emergency colonoscopies have decreased by 75-90%[8,9] and 62%[10,11], respectively. Thus, the COVID-19 pandemic has brought dramatic changes to endoscopic practices.
Colonic diverticular bleeding (CDB) is the most common cause of acute lower gastrointestinal bleeding (ALGIB), accounting for 26-64% of all ALGIB cases[12-16]. CDB has rebleeding and mortality rates of 20-35%[16-19] and 0.2-3.9%[16,20,21], respectively, during hospitalization. It is potentially life-threatening and requires medical intervention, including emergency endoscopy. Therefore, a decrease in colonoscopies may affect the clinical outcomes of patients with CDB.
Several studies have reported the endoscopic management and clinical outcomes of patients with upper gastrointestinal bleeding (UGIB) during the COVID-19 pandemic[22-24]. In a retrospective study of 1,192 patients with UGIB, no significant differences were found in mortality (4.2% vs. 3.9%) and rebleeding (10.7% vs. 10.0%) rates[22]. Moreover, a study including 332 patients reported that although the time from hospital arrival to endoscopy was longer during the pandemic than it was before, it did not affect the clinical outcomes[25]. However, there have been few reports on the endoscopic management and clinical outcomes of ALGIB during the COVID-19 pandemic[10,11]. In previous reports, although a decrease in endoscopy for ALGIB has been reported during the COVID-19 pandemic[10,11], endoscopic management that may influence the risk of rebleeding and mortality in ALGIB, such as the time from arrival to emergency endoscopy and the timeslot of the day the endoscopy was performed, has not been fully evaluated.
Therefore, this two-center study aimed to evaluate the endoscopic management and clinical outcomes of patients with CDB during the COVID-19 pandemic in Japan.
Methods
Patient selection
This retrospective cohort study was conducted at two tertiary centers in Japan. The participants were patients aged ≥20 years who presented with the chief complaint of acute hematochezia and were urgently hospitalized with CDB between April 2017 and March 2023. During the study period, 31,777 patients underwent colonoscopies; among them, those aged ≤20 years (n=183) and those who underwent screening endoscopies (n=31,206) were excluded. Thus, 388 hospitalized patients diagnosed with CDB were included in this study. Based on when the first COVID-19 State of Emergency was announced in Japan (at the start of April 2020), the study period was divided into two parts: April 2020 to March 2023 (during the pandemic) and April 2017 to March 2020 (before the pandemic) (Figure 1).
Figure 1.
Study flowchart.
COVID-19, coronavirus disease 2019; CDB, colonic diverticular bleeding
The study was conducted in accordance with the principles of the Declaration of Helsinki. The Ethics Committee of our hospital approved the study protocol (approval number: 6229). The details of the study were posted on the hospital websites, and informed consent was obtained via an opt-out method.
Data collection
Data were collected from the electronic medical records and endoscopy databases. Using these registries, we evaluated baseline characteristics, including anthropometric factors, sex, age, body mass index, performance status, comorbidities, drinking and smoking habits, vital signs, NOBLADS score[26], medication use, and initial laboratory test results. Comorbidities included hypertension, diabetes mellitus, cerebrovascular disease, myocardial infarction, heart failure, peripheral vascular disease, chronic kidney disease, respiratory disease, liver disease, collagen disease, malignant disease, and CDB. Furthermore, the comorbidities were assessed using the Charlson Comorbidity Index (CCI)[27]. Drinker was defined as a regular or occasional drinker. The Shock Index, defined as the ratio of heart rate to systolic blood pressure[28], was evaluated as a vital sign upon arrival. We evaluated the NOBLADS score as a risk-scoring system for the severity of ALGIB[26]. Regarding medication use, we evaluated the use of non-steroidal anti-inflammatory drugs (NSAIDs) and antithrombotic drugs. Antithrombotic agent use was defined as the use of low-dose aspirin, thienopyridine, other antiplatelet agents (e.g., cilostazol), direct oral anticoagulants, or warfarin. In terms of examination at hospital arrival, we evaluated the rate of computed tomography (CT) performance and the positivity rate of extravasation on contrast-enhanced CT. We evaluated the percentage of patients receiving red blood cells (RBC) transfusion. Furthermore, we also evaluated the length of hospitalization.
Endoscopic management
Among patients admitted for ALGIB, all patients suspected to have CDB based on physical, abdominal, and CT findings underwent emergency endoscopy unless the patient refused or was in poor general condition. Early colonoscopy within 24 hours[29] was performed for patients with a shock index ≥ 1 or patients for whom contrast-enhanced CT scan showed positive extravasation[30]. Colonoscopies were performed by 10 experts or eight trainees supervised by experts with more than 10 years of experience in endoscopy. A colonoscope (PCF-Q260AZI or PCF-290AZI) with a water jet device and an attachment cap (Olympus Co., LTD, Tokyo, Japan) was used for the colonoscopies. Standard precautions before the COVID-19 pandemic included the use of gloves, unwoven masks, and gowns. During the COVID-19 pandemic, endoscopists used complete personal protective equipment (PPE), including gloves, N95 masks, eye goggles, face shields, and gowns[31].
We evaluated the colonoscopy and early colonoscopy rates. Regarding the timing of endoscopy, we evaluated the time to colonoscopy and the timeslot of the day when the colonoscopy was performed. Time to colonoscopy was defined as the time from hospital arrival to the start of scope insertion. The timeslot of the day when colonoscopy was performed was classified as either within regular working hours (9:00 AM to 16:59 PM on weekdays) or outside regular working hours (17:00 PM to 8:59 AM on weekdays or all hours on weekends and holidays).
The identification rate of the stigmata of recent hemorrhage (SRH)[32], location of the SRH (from the ileum to rectum), and presence or absence of active bleeding were evaluated as endoscopic findings. When SRH was identified, endoscopic hemostasis was performed using hemoclips (HX-610-135S or HX-610-135; Olympus Co. Ltd.). We mainly used direct clipping at our institution; the indirect clipping method was only used when the direct clipping method was difficult to perform[33]. Interventional radiology (IVR) or surgery was performed when endoscopic hemostasis failed.
Clinical outcomes
We evaluated rebleeding rates, mortality rates, the need for IVR, and composite outcome within 30 days. Rebleeding was defined as large amounts of fresh, bloody, or wine-colored stools after admission, regardless of achieving endoscopic hemostasis[13]. The composite outcome comprised the following endpoints: rebleeding, mortality within 30 days, and the need for IVR for hemostasis[34]. Causes of death were determined using blood test results, multiple imaging studies, or autopsies.
Statistical analyses
The Fisher's exact test was used to compare categorical variables, while the Wilcoxon rank sum test was used to compare continuous variables. PSM was employed to adjust for differences between the groups before and during COVID-19. We used a logistic regression model to estimate the propensity score, with during COVID-19 as a function of the patient's baseline characteristics. The propensity score model included 38 factors such as anthropometric factors, comorbidities, daily habits, hemodynamic status, NOBLADS score, medication use, laboratory tests, examination, and the percentage of patients receiving RBC transfusion. A one-to-one PSM was performed between before and during the COVID-19 groups using the nearest neighbor method within a caliper width of 0.2 of the standard deviation of the logit of the propensity score. The area under the receiver operating characteristic curve for propensity scores for during the COVID-19 group was 0.744 (95% confidence interval [CI]: 0.695-0.793) before matching. Following the matching, we compared the endoscopic factors between the two groups. Next, we compared the clinical outcomes between the two groups using univariate logistic regression models. P < 0.05 was considered statistically significant. The statistical analysis was performed using SAS version 9.4 (SAS Institute Inc., Cary, NC, USA).
Results
Patient characteristics
The characteristics of all patients (n=388) and the propensity score-matched patients (n=264) are summarized in Table 1. One-to-one PSM identified 132 pairs of patients with matched baseline characteristics from groups before and during the COVID-19 pandemic (Figure 1). The median age of the patients was 77.0 (interquartile range: 68.0-84.0) years; 183 were male, and 81 were female. There were no significant differences in comorbidities, use of oral medications, or NOBLADS scores for the severity of ALGIB between the two groups. Patients with a Shock Index ≥ 1 were included at a rate of 9% in both the groups.
Table 1.
Patient Characteristics.
| Characteristics | All patients (N = 388) | Propensity score-matched patients (N = 264) | ||||
|---|---|---|---|---|---|---|
| During COVID-19 (N = 175) |
Before COVID-19 (N = 213) |
Standardized difference |
During COVID-19 (N = 132) |
Before COVID-19 (N = 132) |
Standardized difference |
|
| Anthropometric factors, n (%) | ||||||
| Sex (male/female) | 123 (70.3)/52 (29.7) | 151 (70.9)/62 (29.1) | -0.001 | 90 (68.2)/42 (31.8) | 93 (70.5)/39 (29.5) | 0.050 |
| Age (median [IQR]) | 78.0 (70.0-84.0) | 76.0 (68.0-83.0) | 0.186 | 77.5 (69.0-84.0) | 76.0 (68.0-84.0) | 0.076 |
| BMI (median [IQR]) | 23.0 (21.0-25.0) | 22.6 (20.7-25.1) | 0.016 | 22.9 (21.0-24.6) | 22.6 (20.7-25.2) | -0.037 |
| PS > 2 | 12 (6.9) | 19 (8.9) | 0.048 | 10 (7.6) | 8 (6.1) | -0.057 |
| Comorbidity, n (%) | ||||||
| Hypertension | 108 (61.7) | 133 (62.4) | 0.009 | 76 (57.6) | 83 (62.9) | 0.109 |
| Diabetes mellitus | 43 (24.6) | 33 (15.5) | -0.224 | 27 (20.5) | 22 (16.7) | -0.095 |
| Cerebrovascular disease | 30 (17.1) | 46 (21.6) | 0.123 | 23 (17.4) | 20 (15.2) | -0.057 |
| Myocardial infarction | 40 (22.9) | 32 (15.0) | -0.210 | 27 (20.5) | 26 (19.7) | -0.019 |
| Heart failure | 21 (12.0) | 43 (20.2) | 0.223 | 20 (15.2) | 18 (13.6) | -0.041 |
| Peripheral vascular disease | 4 (2.3) | 7 (3.3) | 0.037 | 2 (1.5) | 3 (2.3) | 0.047 |
| Chronic kidney disease | 21 (12.0) | 50 (23.5) | 0.293 | 20 (15.2) | 20 (15.2) | 0.000 |
| Respiratory disease | 2 (1.1) | 8 (3.8) | 0.174 | 2 (1.5) | 1 (0.8) | -0.048 |
| Liver disease | 1 (0.6) | 7 (3.3) | 0.203 | 1 (0.8) | 1 (0.8) | 0.000 |
| Collagen disease | 14 (8.0) | 13 (6.1) | -0.071 | 10 (7.6) | 10 (7.6) | 0.000 |
| Malignant disease | 11 (6.3) | 23 (10.8) | 0.169 | 10 (7.6) | 11 (8.3) | 0.027 |
| Colonic diverticular bleeding | 83 (47.4) | 87 (40.8) | -0.129 | 62 (47.0) | 58 (43.9) | -0.061 |
| CCI > 3 | 31 (17.7) | 48 (22.5) | 0.119 | 25 (18.9) | 22 (16.7) | -0.056 |
| Daily habits, n (%) | ||||||
| Drinker | 83 (47.4) | 87 (40.8) | -0.129 | 62 (47.0) | 58 (43.9) | -0.061 |
| Current smoker | 48 (27.4) | 49 (23.0) | -0.117 | 31 (23.5) | 33 (25.0) | 0.035 |
| Hemodynamic status, n (%) | ||||||
| Shock index ≥ 1 | 17 (9.7) | 20 (9.4) | 0.014 | 12 (9.1) | 12 (9.1) | 0.000 |
| NOBLADS Score (median [IQR]) | 3.0 (2.0-4.0) | 3.0 (2.0-4.0) | -0.077 | 3.0 (2.0-4.0) | 3.0 (2.0-4.0) | 0.000 |
| Medication use, n (%) | ||||||
| Antithrombotic agents | 92 (52.6) | 97 (45.5) | -0.138 | 65 (49.2) | 61 (46.2) | -0.061 |
| Antiplatelet drugs | 65 (37.1) | 66 (31.0) | -0.131 | 46 (34.8) | 43 (32.6) | -0.048 |
| Aspirin | 36 (20.6) | 51 (23.9) | 0.080 | 29 (22.0) | 29 (22.0) | 0.000 |
| Thienopyridine | 27 (15.4) | 27 (12.7) | -0.074 | 15 (11.4) | 16 (12.1) | 0.022 |
| NSAIDs | 18 (10.3) | 26 (12.2) | 0.068 | 16 (12.1) | 17 (12.9) | 0.024 |
| DOACs | 23 (13.1) | 25 (11.7) | -0.037 | 16 (12.1) | 15 (11.4) | -0.023 |
| Warfarin | 9 (5.1) | 13 (6.1) | 0.046 | 8 (6.1) | 7 (5.3) | -0.032 |
| Laboratory tests (median [IQR]) | ||||||
| White blood cells (cells/μL) | 7,400 (5,900-9,000) | 7,200 (6,000-8,900) | 0.067 | 7,300 (5,900-8,900) | 7,150 (6,100-8,800) | 0.021 |
| Hemoglobin (g/L) | 10.8 (9.2-12.7) | 11.5 (9.8-12.9) | -0.198 | 10.8 (9.4-12.7) | 11.4 (9.9-12.6) | -0.096 |
| Hematocrit (%) | 32.7 (27.9-38.2) | 34.3 (29.0-39.3) | -0.121 | 32.8 (28.2-38.4) | 34.4 (30.1-37.8) | -0.092 |
| Platelets (×104/μL) | 20.4 (16.8-25.0) | 20.8 (17.3-25.9) | -0.036 | 20.6 (17.0-24.9) | 20.3 (17.4-25.6) | -0.037 |
| PT-INR (s) | 1.1 (1.0-1.1) | 1.0 (1.0-1.1) | -0.018 | 1.1 (1.0-1.1) | 1.0 (1.0-1.1) | 0.094 |
| Albumin (g/dL) | 3.7 (3.4-4.0) | 3.8 (3.4-4.0) | -0.005 | 3.7 (3.4-4.0) | 3.8 (3.5-4.0) | -0.067 |
| C-reactive protein (mg/dL) | 0.1 (0.0-0.4) | 0.1 (0.0-0.3) | 0.166 | 0.1 (0.0-0.5) | 0.1 (0.0-0.3) | 0.023 |
| Examination, n (%) | ||||||
| Computed tomography | 172 (98.3) | 211 (99.1) | 0.067 | 132 (100.0) | 130 (98.5) | -0.131 |
| Extravasation positive | 45 (25.7) | 57 (26.8) | 0.047 | 30 (22.7) | 35 (26.5) | 0.086 |
| Transfusion, n (%) | ||||||
| Received an RBC transfusion | 78 (44.6) | 73 (34.3) | -0.210 | 52 (39.4) | 48 (36.4) | -0.062 |
Note: NOBLADS comprises NSAIDs, no diarrhea, no abdominal tenderness, blood pressure (≤100 mm Hg), antiplatelet drug use (non-aspirin), albumin (<3.0 g/dL), disease score of 2 or greater, and syncope.
BMI and PT-INR were missing for 5 (1.3%), and 5 (1.3%) patients, respectively.
Categorical data were compared using the Fisher’s exact test. Continuous data were compared using the Wilcoxon rank sum test.
Abbreviations: COVID-19, coronavirus disease 2019; BMI, body mass index; PS, performance status; CCI, Charlson Comorbidity Index; NSAIDs, non-steroidal anti-inflammatory drugs; DOACs, direct oral anticoagulants; PT-INR, prothrombin time-international normalized ratio; RBC, red blood cell; IQR, interquartile range
Therapeutic intervention, timing and findings of endoscopy
Before PSM, of the 16,964 and 14,242 screening colonoscopies conducted before and during the COVID-19 pandemic, respectively, 213 (1.3%) and 172 (1.2%) were emergency colonoscopies (P = 0.70), showing no significant difference.
Therapeutic intervention, timing and findings of endoscopy, and length of hospitalization before and during the COVID-19 pandemic after PSM are summarized in Table 2. After PSM, the rate of early colonoscopy was significantly lower (63.6% vs. 76.5%, P = 0.03), the median time from presentation to colonoscopy was significantly longer (20.0 vs. 12.0 hours; P < 0.01), and the number of colonoscopies performed outside of regular working hours was significantly lower (23.8% vs. 47.7%, P < 0.01) during the COVID-19 pandemic than before it. In the location of SRH, the transverse colon was significantly more common during the COVID-19 pandemic than before it (P = 0.04). There was no statistically significant difference in the rate of endoscopic hemostasis before and during the pandemic.
Table 2.
Therapeutic Intervention, Timing and Findings of Endoscopy, and Length of Hospitalization.
| During COVID-19 (N = 132) |
Before COVID-19 (N = 132) |
P-value | |
|---|---|---|---|
| Therapeutic intervention, n (%) | |||
| Colonoscopy | 130 (98.5) | 132 (100.0) | 0.50 |
| Early colonoscopy | 84 (63.6) | 101 (76.5) | 0.03 |
| Time from presentation to colonoscopy (median [IQR]) (hours) | 20.0 (8.0-28.0) | 12.0 (4.0-24.0) | <0.01 |
| Time slot of endoscopy, n (%) | |||
| Regular working hours (9:00 AM to 16:59 PM) | 99 (76.2) | 69 (52.3) | <0.01 |
| Outside regular working hours (17:00 PM to 8:59 AM) | 31 (23.8) | 63 (47.7) | - |
| Endoscopic findings, n (%) | |||
| SRH identification | 66 (50.0) | 59 (44.7) | 0.46 |
| Location of SRH | |||
| Ileum | 1 (0.8) | 2 (1.5) | 1.00 |
| Cecum | 6 (4.5) | 4 (3.0) | 0.75 |
| Ascending colon | 25 (18.9) | 35 (26.5) | 0.19 |
| Transverse colon | 8 (6.1) | 1 (0.8) | 0.04 |
| Descending colon | 5 (3.8) | 3 (2.3) | 0.72 |
| Sigmoid colon | 20 (15.2) | 14 (10.6) | 0.36 |
| Rectum | 1 (0.8) | 0 (0.0) | 1.00 |
| Active bleeding | 21 (15.9) | 34 (25.8) | 0.07 |
| Endoscopic hemostasis | 65 (49.2) | 59 (44.7) | 0.54 |
| Direct clipping method | 60 (45.5) | 55 (41.7) | 0.62 |
| Indirect clipping method | 5 (3.8) | 4 (3.0) | 1.00 |
| Length of hospitalization (median [IQR]) (days) | 8.0 (6.0-12.0) | 8.5 (7.0-11.0) | 0.32 |
Note: Early colonoscopy is colonoscopy performed within 24 h of the initial visit.
The number of the time slot of endoscopy was missing for 2 (1.5%) (During COVID-19 group).
Categorical data were compared using the Fisher’s exact test. Continuous data were compared using the Wilcoxon rank sum test.
Abbreviations: COVID-19, coronavirus disease 2019; SRH, stigmata of recent hemorrhage; IQR, interquartile range
Clinical outcomes
The results of the univariate logistic regression analysis for clinical outcomes after PSM are summarized in Table 3. Rebleeding rates within 30 days were 32.6% and 28.0% (P = 0.42), mortality rates within 30 days were 0% and 0.8% (P = 0.96), the need for IVR was 3.8% and 6.8% (P = 0.28), and the composite outcome rates within 30 days were 34.1% and 31.8% (P = 0.69), respectively, before and during the COVID-19 pandemic.
Table 3.
Univariate Logistic Regression Analysis for Clinical Outcomes.
| During COVID-19 (N = 132) |
Before COVID-19 (N = 132) |
OR (95% CI) |
P-value | |
|---|---|---|---|---|
| Rebleeding within 30 days, n (%) | 37 (28.0) | 43 (32.6) | 0.81 (0.48-1.36) | 0.42 |
| Mortality within 30 days, n (%) | 1 (0.8) | 0 (0.0) | † | 0.96 |
| Interventional radiology, n (%) | 9 (6.8) | 5 (3.8) | 1.86 (0.61-5.70) | 0.28 |
| Composite outcome within 30 days, n (%) | 42 (31.8) | 45 (34.1) | 0.90 (0.54-1.51) | 0.69 |
Note: The composite outcome comprises the following endpoints: rebleeding, mortality within 30 days, and the need for IVR for hemostasis.
†Quasi-complete separation of data points was detected.
Abbreviations: COVID-19, coronavirus disease 2019; OR, odds ratio; CI, confidence interval; IVR, interventional radiology
Discussion
This study focused on the endoscopic management and clinical outcomes of patients with CDB before and during the COVID-19 pandemic and revealed the following findings. First, before PSM, 1.3% (213/16,964) and 1.2% (172/14,242) of colonoscopies performed before and during the COVID-19 pandemic, respectively, were emergency colonoscopies for patients with CDB. Thus, the number of emergency colonoscopies did not decrease significantly during the pandemic. Second, after PSM, although the number of early colonoscopy and colonoscopies performed outside regular working hours significantly decreased and the time from presentation to colonoscopy was significantly longer during the COVID-19 pandemic (Table 2), it did not affect the rebleeding, mortality, need for IVR, or composite outcome rates (Table 3). These results indicate that the time delays in endoscopic management during the pandemic did not affect the rebleeding or mortality rates in patients with CDB. Applying this information in the management of emergency colonoscopies for ALGIB during the infectious disease pandemic could help providers protect medical staff from the transmission of infections and ensure adequate allocation of limited medical resources, including endoscopists.
In this study, the colonoscopy rates for CDB did not significantly differ before and during the COVID-19 pandemic. However, a previous report from Western countries showed that the number of emergency colonoscopies performed for LGIB during the COVID-19 pandemic decreased to 62%[10,11], and these results differed from ours. There are three possible reasons for this. First, the participating institutions were tertiary centers in Japan that could promptly provide patients with antigen/polymerase chain reaction tests and CT scans. Second, endoscopists were available for 24 h and could promptly provide emergency colonoscopies. Third, the hospital was equipped with appropriate infection control measures such as appropriate ventilation and full PPE.
In our study, during the COVID-19 pandemic period, there was a significant decrease in the number of colonoscopies performed outside regular working hours and in early colonoscopies, and the time from presentation to colonoscopy was significantly longer than it was before the pandemic. This is because human and material medical resources were concentrated in emergency departments to deal with respiratory infections, and colonoscopies were performed less frequently outside regular working hours. Therefore, colonoscopies were performed more frequently during regular working hours when medical resources were more readily available. Notably, although there was a decrease in early colonoscopies and a longer time from presentation to colonoscopy, there was no statistically significant difference in rebleeding rates, mortality rates, the need for IVR, and composite outcome rates in patients with CDB before and during the COVID-19 pandemic. This suggests that, during the COVID-19 pandemic, by appropriately selecting only the most urgent cases, including the shock status or extravasation-positive cases, and performing colonoscopies at the appropriate time, important clinical outcomes for patients with CDB may not be affected. In addition, if the emergency priority level is high, IVR with a lower risk of infection can be selected as an option. This endoscopic management will have two advantages. First, we can allow adequate time to test for infections to prevent its transmission to medical staff. Second, unnecessary emergency colonoscopies outside regular working hours can be reduced. Consequently, endoscopists with limited resources will not have to use them outside regular working hours, which will allow for a change in work style reform.
This study had several limitations. First, this was a retrospective and historical control study involving a small number of patients. Thus, the presence of unmeasured confounding factors could not be ruled out. However, we strove to minimize the risk of bias by conducting PSM and selecting cases for analysis. Furthermore, although Japanese guidelines recommend early colonoscopy for ALGIB[18], several negative results regarding its usefulness have been reported in recent years[35,36]. Therefore, regarding the timing of the colonoscopy, it cannot be ruled out that physicians may have been influenced by the latest studies regarding colonoscopy timing. Second, this study was conducted at tertiary centers with 24-h emergency endoscopy capability. Third, we were unable to investigate changes in patients' lifestyle habits before and during the COVID-19 pandemic in this study. Reportedly, an increase in alcohol consumption was noted during the COVID-19 pandemic compared with before[37], and changes in lifestyle habits[38] contributed to an increase in obese people[39]. The possibility cannot be ruled out that such changes in lifestyle might have affected the incidence and severity of CDB.
Conclusion
During the COVID-19 pandemic, a decrease in early colonoscopy and colonoscopies outside regular working hours did not affect the rebleeding, mortality, IVR, and composite outcome risks in patients with CDB. In future infectious disease outbreaks, these results could help providers involved in the endoscopic management of ALGIB reduce unnecessary emergency colonoscopies, protect medical staff from the transmission of infections, and ensure adequate allocation of limited medical resources, including endoscopists.
Conflicts of Interest
There are no conflicts of interest.
Author Contributions
Y.S. was the principal investigator who designed and conducted the study. Material preparation and data collection were performed by T.K., Y.S., K.T., J.I., Y.N., M.K., H.K., and Y.Y. Data analysis was performed by T.K., K.T. and Y.S. The first draft of the manuscript was written by T.K. and Y.S. Furthermore, Y.K., T.M., H.Y., N.M., and K.T. supervised and provided input regarding the manuscript preparation. All authors had access to the study data, commented on previous versions of the manuscript, and read and approved the final manuscript.
Approval by Institutional Review Board (IRB)
This study protocol was reviewed and approved by the Medical Ethics Committee, Clinical Research Section at St. Marianna University (approval number 6229).
Informed Consent
The details of the study were posted on the hospital websites, and informed consent was obtained via an opt-out method.
Data Availability Statement
All data analyzed in this study are incorporated within the manuscript. If data disclosure is requested, it can be disclosed. For any further inquiries, please reach out to the corresponding author.
Acknowledgements
We thank Editage (www.editage.com) for their assistance in manuscript translation and editing.
References
- 1.Riou J, Althaus CL. Pattern of early human-to-human transmission of Wuhan 2019 novel coronavirus (2019-nCoV), December 2019 to January 2020. Euro Surveill. 2020 Jan; 25(4): 2000058. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Parry J. China coronavirus: cases surge as official admits human to human transmission. BMJ. 2020 Jan; 368: m236. [DOI] [PubMed] [Google Scholar]
- 3.Cuicchi D, Lazzarotto T, Poggioli G. Fecal-oral transmission of SARS-CoV-2: review of laboratory-confirmed virus in gastrointestinal system. Int J Colorectal Dis. 2021 Mar; 36(3): 437-44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Wang W, Xu Y, Gao R, et al. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA. 2020 May; 323(18): 1843-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Irisawa A, Furuta T, Matsumoto T, et al. Gastrointestinal endoscopy in the era of the acute pandemic of coronavirus disease 2019: recommendations by Japan Gastroenterological Endoscopy Society (Issued on April 9th, 2020). Dig Endosc. 2020 Jul; 32(5): 648-50. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Chiu PWY, Ng SC, Inoue H, et al. Practice of endoscopy during COVID-19 pandemic: position statements of the Asian Pacific Society for Digestive Endoscopy (APSDE-COVID statements). Gut. 2020 Jun; 69(6): 991-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Gralnek IM, Hassan C, Beilenhoff U, et al. ESGE and ESGENA Position Statement on gastrointestinal endoscopy and the COVID-19 pandemic. Endoscopy. 2020 Jun; 52(6): 483-90. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Blanco GDV, Troncone E, Grasso E, et al. The impact of COVID-19 on elective and urgent digestive endoscopic procedures: a report on a year of pandemic in a gastroenterology centre in Italy. Prz Gastroenterol. 2022; 17(4): 301-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Alboraie M, Piscoya A, Tran QT, et al. The global impact of COVID-19 on gastrointestinal endoscopy units: an international survey of endoscopists. Arab J Gastroenterol. 2020 Sep; 21(3): 156-61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Bujanda L, Arratibel P, Gil I, et al. Surgery and emergency gastrointestinal endoscopy during the Covid-19 pandemic. Gastroenterol Hepatol. 2021 Apr; 44(4): 294-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Chiriac S, Stanciu C, Cojocariu C, et al. The Impact of the COVID-19 pandemic on gastrointestinal endoscopy activity in a tertiary care center from Northeastern Romania. Healthcare (Basel). 2021 Jan; 9(1): 100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Oakland K, Guy R, Uberoi R, et al. Acute lower GI bleeding in the UK: patient characteristics, interventions and outcomes in the first nationwide audit. Gut. 2018 Apr; 67(4): 654-62. [DOI] [PubMed] [Google Scholar]
- 13.Strate LL, Orav EJ, Syngal S. Early predictors of severity in acute lower intestinal tract bleeding. Arch Intern Med. 2003 Apr; 163(7): 838-43. [DOI] [PubMed] [Google Scholar]
- 14.Lanas Á, Carrera-Lasfuentes P, Arguedas Y, et al. Risk of upper and lower gastrointestinal bleeding in patients taking nonsteroidal anti-inflammatory drugs, antiplatelet agents, or anticoagulants. Clin Gastroenterol Hepatol. 2015 May; 13(5): 906-12.e2. [DOI] [PubMed] [Google Scholar]
- 15.Nagata N, Niikura R, Aoki T, et al. Lower GI bleeding risk of nonsteroidal anti-inflammatory drugs and antiplatelet drug use alone and the effect of combined therapy. Gastrointest Endosc. 2014 Dec; 80(6): 1124-31. [DOI] [PubMed] [Google Scholar]
- 16.Nagata N, Kobayashi K, Yamauchi A, et al. Identifying bleeding etiologies by endoscopy affected outcomes in 10,342 cases with hematochezia: CODE BLUE-J Study. Am J Gastroenterol. 2021 Nov; 116(11): 2222-34. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Niikura R, Nagata N, Yamada A, et al. Recurrence of colonic diverticular bleeding and associated risk factors. Colorectal Dis. 2012 Mar; 14(3): 302-5. [DOI] [PubMed] [Google Scholar]
- 18.Nagata N, Ishii N, Manabe N, et al. Guidelines for colonic diverticular bleeding and colonic diverticulitis: Japan Gastroenterological Association. Digestion. 2019; 99: 1-26. [DOI] [PubMed] [Google Scholar]
- 19.Ito Y, Sakata Y, Yoshida H, et al. High cost of hospitalization for colonic diverticular bleeding depended on repeated bleeding and blood transfusion: analysis with diagnosis procedure combination data in Japan. Digestion. 2017; 96(2): 76-80. [DOI] [PubMed] [Google Scholar]
- 20.Niikura R, Yasunaga H, Yamaji Y, et al. Factors affecting in-hospital mortality in patients with lower gastrointestinal tract bleeding: a retrospective study using a national database in Japan. J Gastroenterol. 2015 May; 50(5): 533-40. [DOI] [PubMed] [Google Scholar]
- 21.Strate LL, Ayanian JZ, Kotler G, et al. Risk factors for mortality in lower intestinal bleeding. Clin Gastroenterol Hepatol. 2008 Sep; 6(9): 1004-10; quiz 955. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Khan R, Saha S, Gimpaya N, et al. Outcomes for upper gastrointestinal bleeding during the first wave of the COVID-19 pandemic in the Toronto area. J Gastroenterol Hepatol. 2022 May; 37(5): 878-82. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Kim J, Doyle JB, Blackett JW, et al. Effect of the coronavirus 2019 pandemic on outcomes for patients admitted with gastrointestinal bleeding in New York City. Gastroenterology. 2020 Sep; 159(3): 1155-7.e1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Adekunle AD, Rubens M, Sedarous M, et al. Trends in gastrointestinal disease hospitalizations and outcomes during the first year of the coronavirus pandemic. World J Gastroenterol. 2023 Jan; 29(4): 744-57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Komatsu T, Sato Y, Kuroki Y, et al. Impact of the COVID-19 pandemic on the time to emergency endoscopy and clinical outcomes in patients with upper gastrointestinal bleeding. DEN Open. 2023 Nov; 4(1): e310. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Aoki T, Nagata N, Shimbo T, et al. Development and validation of a risk scoring system for severe acute lower gastrointestinal bleeding. Clin Gastroenterol Hepatol. 2016 Nov; 14(11): 1562-70.e2. [DOI] [PubMed] [Google Scholar]
- 27.Charlson ME, Pompei P, Ales KL, et al. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987; 40(5): 373-83. [DOI] [PubMed] [Google Scholar]
- 28.Allgöwer M, Burri C. “Schockindex” [“Shock index”]. Dtsch Med Wochenschr. 1967; 92(43): 1947-50. [DOI] [PubMed] [Google Scholar]
- 29.Niikura R, Nagata N, Yamada A, et al. Efficacy and safety of early vs elective colonoscopy for acute lower gastrointestinal bleeding. Gastroenterology. 2020 Jan; 158(1): 168-175.e6. [DOI] [PubMed] [Google Scholar]
- 30.Oakland K, Chadwick G, East JE, et al. Diagnosis and management of acute lower gastrointestinal bleeding: guidelines from the British Society of Gastroenterology. Gut. 2019 May; 68(5): 776-89. [DOI] [PubMed] [Google Scholar]
- 31.World Health Organization. Rational use of personal protective equipment (PPE) for coronavirus disease (COVID-19): WHO/2019-nCoV/IPC PPE_use/2020.2; 2020. [Google Scholar]
- 32.Jensen DM, Machicado GA, Jutabha R, et al. Urgent colonoscopy for the diagnosis and treatment of severe diverticular hemorrhage. N Engl J Med. 2000 Jan; 342(2): 78-82. [DOI] [PubMed] [Google Scholar]
- 33.Kishino T, Nagata N, Kobayashi K, et al. Endoscopic direct clipping versus indirect clipping for colonic diverticular bleeding: a large multicenter cohort study. United European Gastroenterol J. 2022 Feb; 10(1): 93-103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Kherad O, Restellini S, Martel M, et al. Outcomes following restrictive or liberal red blood cell transfusion in patients with lower gastrointestinal bleeding. Aliment Pharmacol Ther. 2019 Apr; 49(7): 919-25. [DOI] [PubMed] [Google Scholar]
- 35.Nigam N, Ham SA, Sengupta N. Early colonoscopy for diverticular bleeding does not reduce risk of postdischarge recurrent bleeding: a propensity score matching analysis. Clin Gastroenterol Hepatol. 2019 May; 17(6): 1105-11.e1. [DOI] [PubMed] [Google Scholar]
- 36.Shiratori Y, Ishii N, Aoki T, et al. Timing of colonoscopy in acute lower GI bleeding: a multicenter retrospective cohort study. Gastrointest Endosc. 2023 Jan; 97(1): 89-99. [DOI] [PubMed] [Google Scholar]
- 37.Pomazal R, Malecki KMC, McCulley L, et al. Changes in alcohol consumption during the COVID-19 pandemic: evidence from Wisconsin. Int J Environ Res Public Health. 2023 Mar; 20(7): 5301. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Rubio-Tomás T, Skouroliakou M, Ntountaniotis D. Lockdown due to COVID-19 and its consequences on diet, physical activity, lifestyle, and other aspects of daily life worldwide: a narrative review. Int J Environ Res Public Health. 2022 Jun; 19(11): 6832. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Akter T, Zeba Z, Hosen I, et al. Impact of the COVID-19 pandemic on BMI: Its changes in relation to socio-demographic and physical activity patterns based on a short period. PLoS One. 2022 Mar; 17(3): e0266024. [DOI] [PMC free article] [PubMed] [Google Scholar]

