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Multicenter Study
. 2021 Feb;8(1):e000578.
doi: 10.1136/bmjgast-2020-000578.

Gastrointestinal mucosal damage in patients with COVID-19 undergoing endoscopy: an international multicentre study

Giuseppe Vanella  1 , Gabriele Capurso  1 , Cesare Burti  2 , Lorella Fanti  3 , Luigi Ricciardiello  4 , Andre Souza Lino  5 , Ivo Boskoski  6   7 , Michiel Bronswijk  8 , Amy Tyberg  9 , Govind Krishna Kumar Nair  10 , Stefano Angeletti  11 , Aurelio Mauro  12 , Fabiana Zingone  13 , Kofi W Oppong  14 , Daniel de la Iglesia-Garcia  15 , Lieven Pouillon  16 , Ioannis S Papanikolaou  17 , Pierluigi Fracasso  18 , Fabio Ciceri  19 , Patrizia Rovere-Querini  20 , Carolina Tomba  2 , Edi Viale  3 , Leonardo Henry Eusebi  4 , Maria Elena Riccioni  6   7 , Schalk van der Merwe  8   21 , Haroon Shahid  9 , Avik Sarkar  9 , Jin Woo Gene Yoo  10 , Emanuele Dilaghi  11 , R Alexander Speight  14 , Francesco Azzolini  3 , Francesco Buttitta  4 , Serena Porcari  6   7 , Maria Chiara Petrone  1 , Julio Iglesias-Garcia  15 , Edoardo V Savarino  13 , Antonio Di Sabatino  12 , Emilio Di Giulio  11 , James J Farrell  10 , Michel Kahaleh  9 , Philip Roelandt  8   21 , Guido Costamagna  6   7 , Everson Luiz de Almeida Artifon  5 , Franco Bazzoli  4 , Per Alberto Testoni  3 , Salvatore Greco  2 , Paolo Giorgio Arcidiacono  22
Affiliations
Multicenter Study

Gastrointestinal mucosal damage in patients with COVID-19 undergoing endoscopy: an international multicentre study

Giuseppe Vanella et al. BMJ Open Gastroenterol. 2021 Feb.

Abstract

Background: Although evidence suggests frequent gastrointestinal (GI) involvement during coronavirus disease 2019 (COVID-19), endoscopic findings are scarcely reported.

Aims: We aimed at registering endoscopic abnormalities and potentially associated risk factors among patients with COVID-19.

Methods: All consecutive patients with COVID-19 undergoing endoscopy in 16 institutions from high-prevalence regions were enrolled. Mann-Whitney U, χ2 or Fisher's exact test were used to compare patients with major abnormalities to those with negative procedures, and multivariate logistic regression to identify independent predictors.

Results: Between February and May 2020, during the first pandemic outbreak with severely restricted endoscopy activity, 114 endoscopies on 106 patients with COVID-19 were performed in 16 institutions (men=70.8%, median age=68 (58-74); 33% admitted in intensive care unit; 44.4% reporting GI symptoms). 66.7% endoscopies were urgent, mainly for overt GI bleeding. 52 (45.6%) patients had major abnormalities, whereas 13 bled from previous conditions. The most prevalent upper GI abnormalities were ulcers (25.3%), erosive/ulcerative gastro-duodenopathy (16.1%) and petechial/haemorrhagic gastropathy (9.2%). Among lower GI endoscopies, 33.3% showed an ischaemic-like colitis.Receiver operating curve analysis identified D-dimers >1850 ng/mL as predicting major abnormalities. Only D-dimers >1850 ng/mL (OR=12.12 (1.69-86.87)) and presence of GI symptoms (OR=6.17 (1.13-33.67)) were independently associated with major abnormalities at multivariate analysis.

Conclusion: In this highly selected cohort of hospitalised patients with COVID-19 requiring endoscopy, almost half showed acute mucosal injuries and more than one-third of lower GI endoscopies had features of ischaemic colitis. Among the hospitalisation-related and patient-related variables evaluated in this study, D-dimers above 1850 ng/mL was the most useful at predicting major mucosal abnormalities at endoscopy.

Trial registration number: ClinicalTrial.gov (ID: NCT04318366).

Keywords: covid-19; endoscopy; gastrointestinal tract; mucosal infection.

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Conflict of interest statement

Competing interests: GV received travel grants from Mylan and Alfasigma. GC is a consultant for Mylan. IB is consultant for Apollo Endosurgery, Cook Medical and Boston Scientific; board member for Endo Tools; research grant recipient from Apollo Endosurgery; had food and beverage compensation from Apollo Endosurgery, Cook Medical, Boston Scientific and Endo Tools. LR is a consultant for Cancer Prevention Pharmaceuticals; has received research grants from SLA Pharma AG and Takeda and receives funds from the Italian Association for Cancer Research (IG21723). MB received travel grants from Takeda, Taewoong Medical and Prion Medical. KWO has received lecture fees from Olympus, Medtronic and Mylan. He has received a research grant from Medtronic. LP received advisory board fees from Janssen and Takeda; presentation fees from AbbVie and Ferring; and personal fees from AbbVie, Ferring, Norgine and Takeda. SWVdM holds the Cook chair in interventional endoscopy and holds consultancy agreements with Boston Scientific, Cook, Pentax and Olympus. ES has received lecture or consultancy fees from Medtronic, Reckitt Benckiser, Takeda, Merck & Co, Bristol Myers Squibb, AbbVie, Amgen, Novartis, Fresenius Kabi, Sandoz, Sofar, Malesci, Janssen, Grifols, Aurora Pharma, Innovamedica, Johnson & Johnson, SILA, Unifarco, Alfasigma, Shire, EG Stada Group. MK has done consulting work for Boston Scientific, Interscope Med and AbbVie. He has received research grants from Boston Scientific, Emcision, Conmed, Pinnacle, Cook, Gore, Merit and Olympus. PR is supported by Clinical Mandate from Belgian Foundation against Cancer (Stichting tegen Kanker) and receives speaking and consultancy fees from MSD Belgium. GC is consultant for and had food and beverage compensation from Cook Medical, Boston Scientific and Olympus.

Figures

Figure 1
Figure 1
Upper GI tract. A patient admitted in intensive care unit underwent upper GI endoscopy on day 15 after admission for haematemesis. Digested blood was found in the stomach and duodenum, together with a superficial ulcer with irregular margins with flat pigmentation (IIc according to Forrest classification) in the lesser curvature, on a pale and dystrophic background mucosa (A, B). In the second duodenal portion, small ulcers were found on an atrophic background mucosa (C). Histology of the ulcer showed ischaemic damage with sporadic endocapillary microthrombi. GI, gastrointestinal.
Figure 2
Figure 2
Gastroduodenal damage in a patient undergoing upper GI endoscopy for melena after being admitted for COVID-19. Gastroscopy showed diffuse erythema, antral erosions and one non-bleeding prepyloric ulcer (A). In the bulb a dystrophic mucosa showed diffuse congestion, petechiae (submucosal haemorrhages) and a blackish appearance of some disepithelialised areas (B). GI, gastrointestinal
Figure 3
Figure 3
Small intestine. A patient without medical history or chronic therapy, admitted in a non-intensive ward, underwent a CT scan for persistent abdominal pain, showing thickened jejunal walls; enteroscopy performed 44 days after admission showed multiple erosions and ulcers on a background atrophic mucosa with shortened villi. Histology reported acute inflammation, ulcerations and granulation tissue, with abundant eosinophils, without definite aetiology (all cultural exams negative including immunohistochemistry for Cytomegalovirus and PCR for SARS-CoV-2).
Figure 4
Figure 4
Colon. Endoscopy appearance of ischaemic-like colopathy. (A, B) An elderly patient was admitted with diarrhoea and COVID-19 pneumonia in a non-intensive ward. Five days after admission he underwent a colonoscopy showing friable mucosa with ulcers and pseudomembranes in the sigmoid and descending colon (B); the pathognomonic ‘single stripe’ sign (a linear ulcer extending longitudinally along the antimesenteric bowel wall) was visible in the sigmoid (A). Histology was compatible with ischaemic damage. (C, D) A patient without relevant comorbidities or chronic therapy, underwent a colonoscopy for bloody diarrhoea 30 days after intensive care unit admission. Colonoscopy found petechiae, oedema and easily friable mucosa (C) with small erosions (D) with a patchy and segmental distribution in the left ‘watershed’ area (sigmoid).
Figure 5
Figure 5
An elderly hospitalised patient with COVID-19 with diabetes, kidney failure and atrial fibrillation underwent urgent proctosigmoidoscopy for rectal bleeding. Endoscopy was interrupted due to the presence of abundant coagulated blood. Rinsing of clots showed a fragile, dusky, cyanotic and black mucosa with severe ulcerations, compatible with severe ischaemic/necrotic colitis.
Figure 6
Figure 6
A middle-age patient, with a history of dyslipidaemia, was admitted following an episode of abdominal discomfort, rectal blood loss and a vasovagal syncope. On admission COVID-19-screening came back positive. Subsequent flexible sigmoidoscopy revealed unilateral ulcerations in the left colon with rectal sparing (A, B). Histopathology showed patchy atrophic changes, mucus depletion, signs of regeneration and infiltration by polymorphonuclear neutrophils, typical for an ischaemia-type colitis. COVID-19-antibody-staining was positive on various enterocytes (C, D arrows).
Figure 7
Figure 7
Colonoscopy of a young patient performed for persisting diarrhoea 2 months after being discharged from a COVID-19 ward. In the rectum, a fragile and dystrophic mucosa with diffuse petechiae was seen (A, B). The mucosa of the distal sigmoid colon appeared severely oedematous, congested, with diffuse aphthous erosions (C, D). Histology of the whole colon showed intense lymphocytic and granulomatous infiltration.
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