Clinical Endoscopy

Original Article

Acute Gastrointestinal Bleeding in COVID-19 Patients: A Systematic Review and Meta-Analysis: Umair Iqbal, Hafsa Anwar, Hafiz Umair Siddiqui, Muhammad Ali Khan, Faisal Kamal, Bradley D. Confer, Harshit S. Khara; Clin Endosc 2021;54(4):534-541. Published online June 25, 2021; DOI: https://doi.org/10.5946/ce.2021.071

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Background
/Aims: More than 100 million people to date have been affected by the coronavirus disease-2019 (COVID-19) pandemic. Patients with COVID-19 have a higher risk of bleeding complications. We performed a systematic review and meta-analysis to evaluate the outcomes of COVID-19 patients with signs and symptoms of acute gastrointestinal bleeding (GIB).
Methods
A systematic literature search was carried out for articles published until until November 11, 2020, in the Embase, MEDLINE, Web of Science, and Cochrane Library databases. We included studies on COVID-19 patients with signs and symptoms of GIB.
Results
Our search yielded 49 studies, of which eight with a collective 127 patients (86 males and 41 females) met our inclusion criteria. Conservative management alone was performed in 59% of the patients, endoscopic evaluation in 31.5%, and interventional radiology (IR) embolization in 11%. Peptic ulcer disease was the most common endoscopic finding, diagnosed in 47.5% of the patients. Pooled overall mortality was 19.1% (95% confidence interval [CI]; 12.7%-27.6%) and pooled mortality secondary to GIB was 3.5% (95% CI; 1.3%–9.1%). The pooled risk of rebleeding was 11.3% (95% CI; 6.8%–18.4%).
Conclusions
The majority of COVID-19 patients with GIB responded to conservative management, with a low mortality rate associated with GIB and the risk of rebleeding. Thus, we suggest limiting endoscopic and IR interventions to those with hemodynamic instability and those for whom conservative management was unsuccessful.

Citations

Citations to this article as recorded by

Incidence and Outcomes of Upper GI Bleeding in Hospitalized SARS‐CoV‐2 Patients
Erin Sanzone, Katherine Gheysens, Krystal Hunter, Adib Chaaya, Sangita Phadtare, Tatsuya Toyokawa
Gastroenterology Research and Practice.2025;[Epub] CrossRef
Prevalence and outcomes of upper gastrointestinal bleeding in COVID‐19: A systematic review and meta‐analysis
Sawai Singh Rathore, Zario Shai Wint, Aman Goyal, Bijay Mukesh Jeswani, Ameer Mustafa Farrukh, María Alejandra Nieto‐Salazar, Thanmai Reddy Thugu, Snigdha Erva, Raafay Mehmood, Adriana Carolina Toro‐velandia, Hamam Aneis, Sunny Ratnani, Ibrahim Marouf Yas
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Inpatient outcomes of inflammatory bowel disease in hospitalized patients with COVID-19: analysis of a nationally representative sample
Mohammad Aldiabat, Saqr Alsakarneh, Tyrell Daniel, Muhammad Ali Butt, Balaji Jagdish, James Rock, Aarushi Sudan, Majd Al-Ahmad, Ahmad Jabri, Yassine Kilani, Tarek Odah, Laith Alhuneafat, Mir Zulqarnain, Jana G. Hashash, Hassan Ghoz
Baylor University Medical Center Proceedings.2024; 37(2): 239. CrossRef
Rates, Risk Factors, and Outcomes of Nonvariceal Upper Gastrointestinal Bleeding in Patients Hospitalized for COVID-19 in the United States
Mohammad Aldiabat, Wesam Aleyadeh, Taimur Muzammil, Kemi Adewuyi, Majd Alahmad, Ahmad Jabri, Laith Alhuneafat, Yassine Kilani, Saqr Alsakarneh, Mohammad Bilal
Current Medical Science.2024; 44(6): 1202. CrossRef
Increasing inpatient mortality of nonvariceal upper gastrointestinal bleeding during the COVID-19 pandemic: a nationwide retrospective cohort study
Waqas Rasheed, Gnanashree Dharmarpandi, Ola Al-Jobory, Anass Dweik, Muhammad Anil, Sameer Islam
Baylor University Medical Center Proceedings.2023; 36(3): 286. CrossRef
Outcomes in Patients Admitted for Upper Gastrointestinal Bleeding and COVID-19 Infection: A Study of Two Years of the Pandemic
Sergiu Cazacu, Daniela Burtea, Vlad Iovănescu, Dan Florescu, Sevastița Iordache, Adina Turcu-Stiolica, Victor Sacerdotianu, Bogdan Ungureanu
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Prevalence, causes, medical interventions, and mortality outcome of acute gastrointestinal bleeding among COVID-19 inpatients
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Gastrointestinal Bleeding in Patients With New Coronavirus Infection COVID-19
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Clinical and Endoscopic Outcomes in COVID-19 Patients With Gastrointestinal Bleeding
Hassan Ashktorab, Tiziano Russo, Gholamreza Oskrochi, Giovanni Latella, Sara Massironi, Martina Luca, Lakshmi G. Chirumamilla, Adeyinka O. Laiyemo, Hassan Brim
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Clinical Characteristics of Hospitalized COVID-19 Patients Who Have Gastrointestinal Bleeds Requiring Intervention: A Case-Control Study
Ahmad Abulawi, Ali Al-Tarbsheh, Annie Leamon, Paul Feustel, Amit Chopra, Asra Batool
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Mari R. Thomas, Marie Scully
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Mortality Rate in Upper Gastrointestinal Bleeding Associated with Anti-Thrombotic Therapy Before and During Covid-19 Pandemic
Petrica Popa, Sevastita Iordache, Dan Nicolae Florescu, Vlad Florin Iovanescu, Alexandru Vieru, Valentin Barbu, Maria-Cristina Bezna, Dragos Ovidiu Alexandru, Bogdan Silviu Ungureanu, Sergiu Marian Cazacu
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Mark A. Anderson, Mark A. Khauli, Reece J. Goiffon, Avinash Kambadakone
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The frequency of ulcerative-erosive defects and ulcerative bleeding of the gastroduodenal zone in patients with coronavirus infection COVID-19
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Follow-up after Double Balloon Enteroscopy in Patients with Suspected Small Bowel Bleeding: Focused on the Rebleeding Rate: Sun-Jin Boo, M.D., Jeong-Sik Byeon, M.D., Kee Don Choi, M.D., Byong Duk Ye, M.D., Dong-Hoon Yang, M.D., Soon Man Yoon, M.D., Kyung-Jo Kim, M.D., Seung-Jae Myung, M.D., Suk-Kyun Yang, M.D. and Jin-Ho Kim, M.D.; Korean J Gastrointest Endosc 2010;40(3):157-163. Published online March 30, 2010

Abstract PDF: Background
/Aims: Double balloon enteroscopy (DBE) is an effective modality for making the diagnosis and managing suspected small bowel bleeding. However, there is limited data on the follow-up results after DBE. The aim of this study was to evaluate the long-term clinical outcome after DBE in patients with suspected small bowel bleeding.
Methods
We retrospectively analyzed the rebleeding rate of 60 consecutive patients (M：F=39：21, age: 13∼85 years) who underwent DBE because of suspected small bowel bleeding at Asan Medical Center during a 3 year period.
Results
The median follow-up period was 552 days. Bleeding sources were detected by DBE in 41 patients. The cumulative rebleeding rate at 6, 12 and 24 months was 22%, 27% and 30%, respectively. There was no significant difference in the cumulative rebleeding rate between the patients with bleeding sources detected by the initial DBE and those without bleeding sources detected by the initial DBE. The cumulative rebleeding rate at 6 and 12 months was significantly higher for the patients with vascular or superficial mucosal lesions than for the patients with tumors or other lesions (p=0.013).
Conclusions
The rebleeding risk after DBE is not low for patients with suspected small bowel bleeding. The rebleeding risk is especially high for patients with vascular or superficial mucosal lesions, and this may necessitate careful follow-up. (Korean J Gastrointest Endosc 2010;40:157-163)

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Predictors of Rebleeding after Hemoclip Therapy for Treating High-risk Bleeding Ulcers: Hemoclip Therapy Alone was Comparable to Combination Treatmentwith Epinephrine Injection: Hyo Jeong Oh, M.D., Tae Hyeon Kim, M.D., Geom Seog Seo, M.D., Chang Soo Choi, M.D., Eun Young Cho, M.D., Ki Hoon Kim, M.D., Sung O Seo, M.D., Ji Hye Kweon, M.D., Han Seung Ryu, M.D.,Suck Chei Choi, M.D., Haak Cheoul Kim, M.D. and Sae Ron Shin, M.D.*; Korean J Gastrointest Endosc 2008;37(2):83-89. Published online August 30, 2008

Abstract PDF: Background/Aims: Active bleeding and non-bleeding visible vessels in patients with bleeding peptic ulcer are associated with a high risk of rebleeding. The aim of our study was to define the risk factors associated with failure of endoscopic hemostasis and rebleeding in patients with active peptic ulcer bleeding. Methods: We retrospectively reviewed 119 patients (90 men and 29 women; mean age, 60.14±14.67 years) with active peptic ulcer bleeding (spurting, oozing and/or non-bleeding visible vessel) and who were treated in Wonkwang Medical Center from January 2002 to January 2007. They were classified to endoscopic hemoclipping alone group (n=75) or endoscopic hemoclipping combined with epinephrine injection group (n=44), according to the therapeutic modality. Results: Initial hemostasis was achieved in the two groups (100%), and permanent hemostasis was achieved 71.4% in all the patients. Operation was done in eight patients (6.7%), and six patients (5%) in the two groups, respectively, died within 1 month after initial hemostasis because of bleeding related complications. Recurrent bleeding, the duration of the hospital stay, blood transfusion requirements, complications and the operation and mortality rates were not statistically different between the hemoclip alone and combination groups. Univariate analysis showed that rebleeding was related to the presence of shock on admission (p=0.01), complication (p=0.00), the pulse rate (＞100/min) on admission (p=0.04), single ulcer (p=0.032), the level of hemoglobin (＜8 g/dL) (p=0.02) and the volume of transfusion (＞3 units) after the procedure (p=0.005) in all the patients. On the multivariate analysis that was adjusted for age and gender, the hemoglobin level (＜8 g/dL) (odds ratio = 10.5) was the only significant predictor for early rebleeding. Conclusions: This result may suggest that the combination method does not provide a substantial advantage over hemoclipping alone for the hemostatic management of active peptic ulcers bleeding. A low hemoglobin level on admission may be useful to predict rebleeding after initial endoscopic hemostasis in patients with active peptic ulcer. However, this study was designed retrospectively, so the comparison between these two groups should be re-evaluated prospectively in a large, multicenter trial. (Korean J Gastrointest Endosc 2008;37:83-89)

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The Effect of Second Look Endoscopy in Patients with Peptic Ulcer Bleeding: Seung Yup Lee, M.D.*, Ji Hyun Park, M.D., Jong Hyup Lee, M.D., Se Hwan Kim, M.D.*, Chang Keun Park, M.D.*, Chang Min Cho, M.D., Won Young Tak, M.D., Young Oh Kweon, M.D., Sung Kook Kim, M.D. and Yong Hwan Choi, M.D.; Korean J Gastrointest Endosc 2007;34(6):304-311. Published online June 30, 2007

Abstract PDF: Background/Aims: Performing second look endoscopy has been suggested in order to reduce recurrent bleeding. We assessed whether second look endoscopy reduces the risks of recurrent bleeding and the mortality rate for patients suffering with peptic ulcer bleeding. Methods: From February 2003 to June 2004, we have performed a prospective, randomized, controlled study of 141 patients with bleeding peptic ulcers, and these patients had been admitted to Kyungpook National University Hospital. Seventy patients in the study group were randomized to receive scheduled second look endoscopy. Seventy one patients in the control group were observed closely. Results: Seventeen of the admitted 141 patients were found to have rebleeding after initial therapeutic endoscopy. The overall rebleeding rate was 12.1%. Although the duration of the hospital stay was significantly lower for the study group than for the control group (p＜0.05), the rebleeding rate was similar for both groups (p＞0.05). The two groups were similar in respect to the mortality during the period of hospitalization, the volume of hypertonic saline epinephrine that was injected and the number of hemoclips that were used. Conclusions: From these results, we can conclude that scheduled second look endoscopy with retreatment did not reduce the risk of recurrent bleeding for patients with peptic ulcer bleeding. Therefore, scheduled second look endoscopy should be selectively performed for the patients who are at a high risk for peptic ulcer bleeding.

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Risk Factors for Upper Gastrointestinal Rebleeding in Critically Ill Patients: Seong Joon Koh, M.D., Jae Hee Cheon, M.D., Joo Sung Kim, M.D., Byong Duk Ye, M.D., Hae Yeon Kang, M.D., Bo Hyun Kim, M.D., Jeong Hoon Lee, M.D., Ki Young Yang, M.D., Sang Gyun Kim, M.D., Hyun Chae Jung, M.D. and In Sung Song, M.D.; Korean J Gastrointest Endosc 2006;32(5):320-325. Published online May 30, 2006

Abstract PDF: Background
/Aims: To determine the incidence and risk factors associated with rebleeding after upper gastrointestinal bleeding (UGIB) in critically ill patients. Methods: This study retrospectively reviewed the medical records of 60 patients undergoing bedside esophagogastroduodenoscopy between April 2000 and February 2004 for UGIB that developed whilst in the intensive care unit (ICU). Results: Eight out of 60 patients died within 7 days, and an additional 7 patients died within 30 days after the initial bleeding. Two of these 15 patients (13.3%), died from GI bleeding. The 7-day and 30-day rebleeding rates were 34.6% (18/52 patients), and 51.1% (23/45 patients), respectively. Multiple logistic regression using the significant variables revealed, anemia (Hb＜9.0 g/dL) and hypoalbuminemia (＜3.0 g/dL) to be significant factor for 7-day rebleeding, and hypoxia (＜80 mmHg), anemia (Hb＜9.0 g/dL), blood transfusion (≥3 units) to be significant independent risk factor for 30-day rebleeding. Conclusions: The rebleeding rates in the ICU setting were as high as 34.6% at 7 days and 51.1% at 30 days. This suggests that the underlying conditions of the critically ill patients affect the rebleeding rate more than the endoscopic features. Therefore, adequate general ICU care including the prevention and correction of hypoxia, anemia, and hypoalbuminemia, and minimizing blood loss can reduce the risk of rebleeding after UGIB in an ICU setting. (Korean J Gastrointest Endosc 2006;32:320⁣325)

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Clinical Findings of Upper Gastrointestinal Bleeding and Risk Factors for Early Rebleeding in Patients with Bleeding Peptic Ulcers: Hyeon Yong Park, M.D., Jin Wook Hur, M.D., Paul Choi, M.D., Nam Young Park, M.D., Jee Yeon Kim, M.D., Dong Wan Kim, M.D., Jee Young Lee, M.D., Ki Hwan Kim, M.D., Moo In Park, M.D., Seun Ja Park, M.D. and Ja Young Koo, M.D.; Korean J Gastrointest Endosc 2003;27(2):57-63. Published online August 30, 2003

Abstract PDF: Background
/Aims: Upper gastrointestinal (UGI) bleeding may have serious complications. Endoscopic therapy is effective in the hemostasis of active bleeding. We analysed the causes of UGI bleeding and evaluated risk factors and rate of rebleeding in patients with bleeding peptic ulcer. Methods: Records from 326 patients admitted with upper gastrointestinal bleeding between January 1998 and December 2002 were reviewed. We retrospectively analyzed clinical findings and rebleeding risk factors of peptic ulcers. Results: Common causes of UGI bleeding were esophageal varix (38.0%), peptic ulcer (36.9%), Mallory-Weiss tear (13.8%), stomach cancer (6.4%). Early rebleeding of bleeding peptic ulcer after hemostasis occurred in 23 cases (19.2%). On the basis of univariate analysis, significant predictive factors for early rebleeding were old age (＞65) (p=0.034), size of ulcer (＞2 cm) (p=0.002), number of ulcer (＞1) (p=0.059). In multivariate analysis, old age (odds ratio, OR=2.3), size of ulcer (OR=3.3), number of ulcer (OR=2.6) were independent risk factors of rebleeding. Conclusions: Common causes of UGI bleeding are esophageal varix, peptic ulcer, Mallory-Weiss tear. Predictive risk factors for early rebleeding in bleeding peptic ulcer may be old age, size of ulcer and number of ulcer. (Korean J Gastrointest Endosc 2003;27:57⁣63)

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소화성궤양 출혈의 내시경적 지혈술 후의 조기 재출혈에 관한 우험 인자 분석 ( Risk Factors for Early Rebleeding after Initial Endoscopic Hemostasis in Patients with Bleeding Peptic Ulcers ): Korean J Gastrointest Endosc 2000;21(6):898-908. Published online November 30, 1999

Abstract PDF: Backgrund/Aims: Rebleeding rate after initial endoscopic hemostasis in patients with ulcer hemorrhage has been reported in 20-30%, Identification of patients who are at high risk for rebleeding would be expected to improve the outcome of endoscopic hemostasis. The purpose of this study was to evaluate risk factors for early rebleeding after initial hemostasis in the view of clinical and endoscopic characteristics. Methods: We reviewed 99 patients who presented with bleeding peptie ulcers and were treated with endoscopic hemostasis including hypertonic saline injection, electrocautery and clipping. We compared the clinical variables (age, pulse rate, hemoglobin), endoscopic characteristics of ulcer (size, number, and location of ulcer, clots on the base, bleeding stigmata, size and color of exposed vessel) between the patients who bled early (n=22) and who didnt bleed (n=77) within 5 days. Results: The statistically significant correlates with early rebleeding after hemostasis were number of comorbid illness (≥2) (p=0.031), volume of transfusion (≥5 units) (p=0.001), size of ulcer (>1 cm) (p=0.038), multiple ulcers (p=O.O2O), presence of blood clots on ulcer base (p=0.012), stigmata (active bleeding and visible vessels) (p=0.010), size of exposed vessel (>1 mm) (p<0.0001). In multivariate analysis, volume of transfusion (odds ratio[OR] 14.4), size of ulcer (OR 11.7), multiple ulcers (OR 5.5) and size of exposed vessel (OR 13.2) were significant risk factors. Conclusions: The risk factors for early rebleeding after hemostasis in bleeding peptic ulcer can be predicted by clinical variables and endoscopic findings. Early identifieation of risk factors such as transfusion over 5 units, large-sized ulcer, multiple ulcers, bleeding stigmata and size of exposed vessei over 1 mm can predict the prognosis of peptic ulcer bleeding.

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원저 : 소화성 궤양 출혈에서 열탐침 지혈법 후 재출혈의 위험인자 (The Risk Factors for Rebleeding with Heat Probe Thermocoagulation in Bleeding Peptie Ulcer Patients: Korean J Gastrointest Endosc 2000;20(6):431-436. Published online November 30, 1999

Abstract PDF: Background
/Aims: The precise rebleeding rate and risk factors of rebleeding after heat probe thermocoagulation in peptic ulcer patients with bleeding are not clear and still need to be evaluated. If we could identify the pre-dictors for rebleeding, the mortality rate might be loweted with early retreatment or surgery in these high risk group. Methods: The 94 patients in whom heat probe was applied were enrolled and the 18 patients with bleeding tendencies. Initial hemostasis was defined as hemostasis persisting for 24 hours post-treatment and permanent hemostasis as absence of bleeding for 7 days after therapy. Rebleedig was defined as oozing or spurting hemorrhage in the ulcer base and/or unstable vital signs and continuting tarry or bloody stool or hematemesis after therapy. Results: In 35 patients with active bleeding sign, initial hemostasis was obtained in 30 (85.7%) patients. After having achieved initial hemostasis, 9 (30.0%) patients rebled. In 41 ulcer patients with non-bleeding visible vessel, 40 cases (97.6%) achieved successful pre-vention of rebleeding. No evident complication was observed. With univariate analysis, bleeding ulcer patients with spurting and oozing hemorrhage had a higher re-bleeding rate than those with non-bleeding visible vessel. Conclusions: The heat probe thermocoagulaton is relative safe and effective procedure to protect bleeding in pectic ulcer patients with non-bleeding visible vessel, but insufficient to hemostasis in bleeding peptic ulcer patients with spurting or oozing in ulcer base. Spurting and oozing hemorrhage are the only risk factors of rebleeding after initial hemostasis with heat probe thermocoagulation in peptic ulcer patients with bleeding.

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식도정맥류에 대한 내시경적 정맥류 결찰요법 후 재출혈 및 재발과 연관된 위험인자들 ( Risk Factors Associated with Rebleeding and Recurrence Following Endoscopic Variceal Ligation ): Korean J Gastrointest Endosc 1999;19(1):1-8. Published online November 30, 1998

Abstract PDF: the first EVL was associated with rebleeding (p=0.01); whereas, age, Child class, grade and extent of varices, presence of gastric varices and/or portal hypertensive gastropathy, total number of bands and sessions for successful EVL were not (p ＞0.05). Persistence of esophageal ulcer at 2 weeks after the first EVL was associated with rebleeding also in multivariate analysis (relative risk 5.87, p=0.01). 3) In univariate analysis, grade (p=0.01) and extent (p=0.01) of varices were related to recurrence; whereas, age, Child class, presence of gastric varices and/or portal hypertensive gastropathy, total number of bands and sessions for successful EVL were not (p ＞0.05). In multivariate analysis, grade of varices was the only risk factor associated with recurrence (relative risk 3.76, p=0.01). Conclusions: 1) Persistence of esophageal ulcer at second week after the first EVL was associated with rebleeding. 2) Frequent follow-up endoscopic examinations are necessary in patients who present with high grade of varices since risk of recurrence is high even after successful EVL. (Korean J Gastrointest Endosc 19: 1 ∼8, 1999)

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원저 : 식도 위장관 ; 소화성 궤양의 재출혈 위험인자 및 에탄올 주입치료의 효과에 관한 연구 ( Original Articles : Esophagus , Stomach & Intestine ; The Risk Factors of Re-bleeding in Peptic Ulcer Patients and the Efficacy of Ethanol Injection Therapy ): Korean J Gastrointest Endosc 1998;18(4):485-498. Published online November 30, 1997

Abstract PDF: Background
/Aims: Acute peptic ulcer bleeding is the most common cause of upper gastrointestinal bleeding, and needs urgent management in cases including large amounts of blood loss. Ernergency endoscopy was performed and evaluation was made on the risk factors of rebleeding in peptic ulcer patients and the efficacy of ethanol injection therapy. Methods: The clinical and endoscopic variables were evaluated according to the rebleeding rates and the efficacy of ethanol injection therapy for hemostasis and prevention of rebleeding in 161 cases including gastric ulcers (GU) with bleeding (M: F 134: 27, mean age 56.5 years) and 136 cases including duodenal ulcers (DU) with bleeding (M: F 111: 25, mean age 40.7 years). (Korean J Gastrointest Endosc 18: 485-498, 1998) (continue)

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