Intest Res.  2022 Oct;20(4):431-444. 10.5217/ir.2021.00111.

Korean Association for the Study of Intestinal Diseases guidance for clinical practice of adult inflammatory bowel disease during the coronavirus disease 2019 pandemic: expert consensus statements

• Park YE
• Lee YJ
• Chang JY
• Song HJ
• Kim DH
• Yang YJ
• Kim BC
• Lee JG
• Yang HC
• Choi M
• Kim SE
• Myung SJ

• KMID: 2535817
• DOI: http://doi.org/10.5217/ir.2021.00111

Abstract

Many unexpected problems have resulted from the unprecedented coronavirus disease 2019 (COVID-19) pandemic. The optimal management of patients with inflammatory bowel disease (IBD) during the COVID-19 pandemic has also been a challenge. Therefore, the Korean Association for the Study of Intestinal Diseases (KASID) developed a consensus statement of experts regarding the management of IBD during the COVID-19 pandemic. This consensus statement made recommendations regarding the risk and treatment of COVID-19 in IBD patients. This statement emphasizes that IBD is not a risk factor for COVID-19, and care should be taken not to exacerbate IBD in patients in remission state by maintaining their medications, except for corticosteroids.

Keyword

SARS-CoV-2; COVID-19; Inflammatory bowel disease; Management

Reference

1. Perlman S. Another decade, another coronavirus. N Engl J Med. 2020; 382:760–762.

2. Sohrabi C, Alsafi Z, O’Neill N, et al. World Health Organization declares global emergency: a review of the 2019 novel coronavirus (COVID-19). Int J Surg. 2020; 76:71–76.

3. Bezzio C, Saibeni S, Variola A, et al. Outcomes of COVID-19 in 79 patients with IBD in Italy: an IG-IBD study. Gut. 2020; 69:1213–1217.

4. Chen N, Zhou M, Dong X, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020; 395:507–513.

5. Nair R, Aggarwal R, Khanna D. Methods of formal consensus in classification/diagnostic criteria and guideline development. Semin Arthritis Rheum. 2011; 41:95–105.

6. Hong KS, Ko SB, Yu KH, et al. Update of the Korean clinical practice guidelines for endovascular recanalization therapy in patients with acute ischemic stroke. J Stroke. 2016; 18:102–113.

7. Choi CH, Moon W, Kim YS, et al. Second Korean guideline for the management of ulcerative colitis. Korean J Gastroenterol. 2017; 69:1–28.

8. Park JJ, Yang SK, Ye BD, et al. Second Korean guidelines for the management of Crohn’s disease. Korean J Gastroenterol. 2017; 69:29–54.

9. Kim JM, Cheon JH. Pathogenesis and clinical perspectives of extraintestinal manifestations in inflammatory bowel diseases. Intest Res. 2020; 18:249–264.

10. Winthrop KL, Melmed GY, Vermeire S, et al. Herpes zoster infection in patients with ulcerative colitis receiving tofacitinib. Inflamm Bowel Dis. 2018; 24:2258–2265.

11. Pauly MP, Tucker LY, Szpakowski JL, et al. Incidence of hepatitis B virus reactivation and hepatotoxicity in patients receiving long-term treatment with tumor necrosis factor antagonists. Clin Gastroenterol Hepatol. 2018; 16:1964–1973.

12. Ooi CJ, Hilmi I, Banerjee R, et al. Best practices on immunomodulators and biologic agents for ulcerative colitis and Crohn’s disease in Asia. J Gastroenterol Hepatol. 2019; 34:1296–1315.

13. Attauabi M, Poulsen A, Theede K, et al. Prevalence and outcomes of COVID-19 among patients with inflammatory bowel disease: a Danish prospective population-based cohort study. J Crohns Colitis. 2021; 15:540–550.

14. Derikx LA, Lantinga MA, de Jong DJ, et al. Clinical outcomes of COVID-19 in patients with inflammatory bowel disease: a nationwide cohort study. J Crohns Colitis. 2021; 15:529–539.

15. Aziz M, Fatima R, Haghbin H, Lee-Smith W, Nawras A. The incidence and outcomes of COVID-19 in IBD patients: a rapid review and meta-analysis. Inflamm Bowel Dis. 2020; 26:e132–e133.

16. Singh S, Khan A, Chowdhry M, Bilal M, Kochhar GS, Clarke K. Risk of severe coronavirus disease 2019 in patients with inflammatory bowel disease in the United States: a multicenter research network study. Gastroenterology. 2020; 159:1575–1578.

17. Lukin DJ, Kumar A, Hajifathalian K, et al. Baseline disease activity and steroid therapy stratify risk of COVID-19 in patients with inflammatory bowel disease. Gastroenterology. 2020; 159:1541–1544.

18. Brenner EJ, Ungaro RC, Gearry RB, et al. Corticosteroids, but not TNF antagonists, are associated with adverse COVID-19 outcomes in patients with inflammatory bowel diseases: results from an international registry. Gastroenterology. 2020; 159:481–491.

19. Rodríguez-Lago I, Ramírez de la Piscina P, Elorza A, Merino O, Ortiz de Zárate J, Cabriada JL. Characteristics and prognosis of patients with inflammatory bowel disease during the SARS-CoV-2 pandemic in the Basque Country (Spain). Gastroenterology. 2020; 159:781–783.

20. Allocca M, Fiorino G, Zallot C, et al. Incidence and patterns of COVID-19 among inflammatory bowel disease patients from the Nancy and Milan Cohorts. Clin Gastroenterol Hepatol. 2020; 18:2134–2135.

21. Taxonera C, Sagastagoitia I, Alba C, Mañas N, Olivares D, Rey E. 2019 novel coronavirus disease (COVID-19) in patients with inflammatory bowel diseases. Aliment Pharmacol Ther. 2020; 52:276–283.

22. Gubatan J, Levitte S, Balabanis T, Patel A, Sharma A, Habtezion A. SARS-CoV-2 testing, prevalence, and predictors of COVID-19 in patients with inflammatory bowel disease in Northern California. Gastroenterology. 2020; 159:1141–1144.

23. Guan WJ, Ni ZY, Hu Y, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020; 382:1708–1720.

24. Zhou F, Yu T, Du R, et al. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020; 395:1054–1062.

25. Yang J, Zheng Y, Gou X, et al. Prevalence of comorbidities and its effects in patients infected with SARS-CoV-2: a systematic review and meta-analysis. Int J Infect Dis. 2020; 94:91–95.

26. Vardavas CI, Nikitara K. COVID-19 and smoking: a systematic review of the evidence. Tob Induc Dis. 2020; 18:20.

27. Wenham C, Smith J, Morgan R; Gender and COVID-19 Working Group. COVID-19: the gendered impacts of the outbreak. Lancet. 2020; 395:846–848.

28. Patrì A, Pinchera B, Spirito L, et al. Gastrointestinal tract diseases as a risk factor for SARS-CoV2 rectal shedding? An Italian report on 10 COVID-19 patients. Intest Res. 2021; 19:354–356.

29. Barbosa da Luz B, de Oliveira NM, França Dos Santos IW, et al. An overview of the gut side of the SARS-CoV-2 infection. Intest Res. 2021; 19:379–385.

30. Hoffmann M, Kleine-Weber H, Schroeder S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020; 181:271–280.

31. Park J, Jeong D, Chung YW, Kim DH, Cheon JH, Ryu JH. Quantitative proteomic analysis of the expression of SARS-CoV-2 receptors in the gut of patients with chronic enterocolitis. Yonsei Med J. 2020; 61:891–894.

32. Burgueño JF, Reich A, Hazime H, et al. Expression of SARS-CoV-2 entry molecules ACE2 and TMPRSS2 in the gut of patients with IBD. Inflamm Bowel Dis. 2020; 26:797–808.

33. Rubin DT, Feuerstein JD, Wang AY, Cohen RD. AGA clinical practice update on management of inflammatory bowel disease during the COVID-19 pandemic: expert commentary. Gastroenterology. 2020; 159:350–357.

34. Kennedy NA, Jones GR, Lamb CA, et al. British Society of Gastroenterology guidance for management of inflammatory bowel disease during the COVID-19 pandemic. Gut. 2020; 69:984–990.

35. Aysha AA, Rentsch C, Prentice R, et al. Practical management of inflammatory bowel disease patients during the COVID-19 pandemic: expert commentary from the Gastroenterological Society of Australia Inflammatory Bowel Disease faculty. Intern Med J. 2020; 50:798–804.

36. Ludvigsson JF, Axelrad J, Halfvarson J, et al. Inflammatory bowel disease and risk of severe COVID-19: a nationwide population-based cohort study in Sweden. United European Gastroenterol J. 2021; 9:177–192.

37. Toruner M, Loftus EV Jr, Harmsen WS, et al. Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology. 2008; 134:929–936.

38. Singh AK, Jena A, Kumar-M P, Jha DK, Sharma V. Clinical presentation of COVID-19 in patients with inflammatory bowel disease: a systematic review and meta-analysis. Intest Res. 2021; Jan. 18. [Epub]. https://doi.org/10.5217/ir.2020.00108.

39. Tian Y, Rong L, Nian W, He Y. Review article: gastrointestinal features in COVID-19 and the possibility of faecal transmission. Aliment Pharmacol Ther. 2020; 51:843–851.

40. Redd WD, Zhou JC, Hathorn KE, et al. Prevalence and characteristics of gastrointestinal symptoms in patients with severe acute respiratory syndrome coronavirus 2 infection in the United States: a multicenter cohort study. Gastroenterology. 2020; 159:765–767.

41. Wang D, Hu B, Hu C, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA. 2020; 323:1061–1069.

42. Han C, Duan C, Zhang S, et al. Digestive symptoms in COVID-19 patients with mild disease severity: clinical presentation, stool viral RNA testing, and outcomes. Am J Gastroenterol. 2020; 115:916–923.

43. Cheung KS, Hung IF, Chan PP, et al. Gastrointestinal manifestations of SARS-CoV-2 infection and virus load in fecal samples from a Hong Kong cohort: systematic review and meta-analysis. Gastroenterology. 2020; 159:81–95.

44. Harmer D, Gilbert M, Borman R, Clark KL. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett. 2002; 532:107–110.

45. Goyal P, Choi JJ, Pinheiro LC, et al. Clinical characteristics of COVID-19 in New York city. N Engl J Med. 2020; 382:2372–2374.

46. Britton GJ, Chen-Liaw A, Cossarini F, et al. Limited intestinal inflammation despite diarrhea, fecal viral RNA and SARS-CoV-2-specific IgA in patients with acute COVID-19. Sci Rep. 2021; 11:13308.

47. Rahier JF, Magro F, Abreu C, et al. Second European evidencebased consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohns Colitis. 2014; 8:443–468.

48. Magro F, Rahier JF, Abreu C, et al. Inflammatory bowel disease management during the COVID-19 outbreak: the ten do’s and don’ts from the ECCO-COVID Taskforce. J Crohns Colitis. 2020; 14(14 Suppl 3):S798–S806.

49. Hrusak O, Kalina T, Wolf J, et al. Flash survey on severe acute respiratory syndrome coronavirus-2 infections in paediatric patients on anticancer treatment. Eur J Cancer. 2020; 132:11–16.

50. Bussalino E, De Maria A, Russo R, Paoletti E. Immunosuppressive therapy maintenance in a kidney transplant recipient with SARS-CoV-2 pneumonia: a case report. Am J Transplant. 2020; 20:1922–1924.

51. D’Antiga L. Coronaviruses and immunosuppressed patients: the facts during the third epidemic. Liver Transpl. 2020; 26:832–834.

52. Blanco JL, Ambrosioni J, Garcia F, et al. COVID-19 in patients with HIV: clinical case series. Lancet HIV. 2020; 7:e314–e316.

53. Ungaro RC, Brenner EJ, Gearry RB, et al. Effect of IBD medications on COVID-19 outcomes: results from an international registry. Gut. 2021; 70:725–732.

54. Agrawal M, Brenner EJ, Zhang X, et al. Characteristics and outcomes of IBD patients with COVID-19 on tofacitinib therapy in the SECURE-IBD Registry. Inflamm Bowel Dis. 2021; 27:585–589.

55. An P, Ji M, Ren H, et al. Protection of 318 inflammatory bowel disease patients from the outbreak and rapid spread of COVID-19 infection in Wuhan, China. SSRN. [Preprint]. 2020 [cited 2021 Jul 28]. https://ssrn.com/abstract=3543590.

56. Ni YN, Chen G, Sun J, Liang BM, Liang ZA. The effect of corticosteroids on mortality of patients with influenza pneumonia: a systematic review and meta-analysis. Crit Care. 2019; 23:99.

57. Stockman LJ, Bellamy R, Garner P. SARS: systematic review of treatment effects. PLoS Med. 2006; 3:e343.

58. Lansbury L, Rodrigo C, Leonardi-Bee J, Nguyen-Van-Tam J, Lim WS. Corticosteroids as adjunctive therapy in the treatment of influenza. Cochrane Database Syst Rev. 2019; 2–CD010406.

59. Arabi YM, Mandourah Y, Al-Hameed F, et al. Corticosteroid therapy for critically ill patients with Middle East respiratory syndrome. Am J Respir Crit Care Med. 2018; 197:757–767.

60. World Health Organization. Clinical management of severe acute respiratory infection when novel coronavirus (2019-nCoV) infection is suspected: interim guidance, 28 January 2020 [Internet]. c2000 [cited 2021 Jul 28]. https://apps.who.int/iris/handle/10665/330893.

61. Lim HW, Schuster IP, Rajapakse R, Monzur F, Khan S, Sultan K. The impact of corticosteroid use on inpatients with inflammatory bowel disease and positive polymerase chain reaction for Clostridium difficile. Intest Res. 2019; 17:244–252.

62. Cline JC, Davis SM. Risks of infection or reactivation of tuberculosis associated with chronic corticosteroid therapy. Ann Pharmacother. 1997; 31:775–776.

63. Ling KL, Hilmi I, Raja Ali RA, et al. Asian Pacific Association of Gastroenterology (APAGE) Inflammatory Bowel Disease (IBD) Working Party guidelines on IBD management during the COVID-19 pandemic. JGH Open. 2020; 4:320–323.

64. Kim KO, Jang BI. Management of inflammatory bowel disease in the COVID-19 era. Intest Res. 2022; 20:3–10.

65. Zingone F, Savarino EV. Viral screening before initiation of biologics in patients with inflammatory bowel disease during the COVID-19 outbreak. Lancet Gastroenterol Hepatol. 2020; 5:525.

66. D’Amico F, Danese S, Peyrin-Biroulet L; ECCO COVID taskforce. Inflammatory bowel disease management during the coronavirus-19 outbreak: a survey from the European Crohn’s and Colitis Organization. Gastroenterology. 2020; 159:14–19.

67. Dotan I, Panaccione R, Kaplan GG, O’Morain C, Lindsay JO, Abreu MT. Best practice guidance for adult infusion centres during the COVID-19 pandemic: report from the COVID-19 International Organization for the Study of IBD [IOIBD] Task Force. J Crohns Colitis. 2020; 14(14 Suppl 3):S785–S790.

68. Van Assche G, Vermeire S, Ballet V, et al. Switch to adalimumab in patients with Crohn’s disease controlled by maintenance infliximab: prospective randomised SWITCH trial. Gut. 2012; 61:229–234.

69. Heida A, Dijkstra A, Muller Kobold A, et al. Efficacy of home telemonitoring versus conventional follow-up: a randomized controlled trial among teenagers with inflammatory bowel disease. J Crohns Colitis. 2018; 12:432–441.

70. Lewin S, Lees C, Regueiro M, Hart A, Mahadevan U. International Organization for the Study of Inflammatory Bowel Disease: global strategies for telemedicine and inflammatory bowel diseases. J Crohns Colitis. 2020; 14(14 Suppl 3):S780–S784.

71. Silasi M, Cardenas I, Kwon JY, Racicot K, Aldo P, Mor G. Viral infections during pregnancy. Am J Reprod Immunol. 2015; 73:199–213.

72. Di Mascio D, Khalil A, Saccone G, et al. Outcome of coronavirus spectrum infections (SARS, MERS, COVID-19) during pregnancy: a systematic review and meta-analysis. Am J Obstet Gynecol MFM. 2020; 2:100107.

73. Wong SF, Chow KM, Leung TN, et al. Pregnancy and perinatal outcomes of women with severe acute respiratory syndrome. Am J Obstet Gynecol. 2004; 191:292–297.

74. Jeong SY, Sung SI, Sung JH, et al. MERS-CoV infection in a pregnant woman in Korea. J Korean Med Sci. 2017; 32:1717–1720.

75. Meijer WJ, van Noortwijk AG, Bruinse HW, Wensing AM. Influenza virus infection in pregnancy: a review. Acta Obstet Gynecol Scand. 2015; 94:797–819.

76. Collin J, Byström E, Carnahan A, Ahrne M. Public Health Agency of Sweden’s Brief Report: pregnant and postpartum women with severe acute respiratory syndrome coronavirus 2 infection in intensive care in Sweden. Acta Obstet Gynecol Scand. 2020; 99:819–822.

77. Rosen MH, Axelrad J, Hudesman D, Rubin DT, Chang S. Management of acute severe ulcerative colitis in a pregnant woman with COVID-19 infection: a case report and review of the literature. Inflamm Bowel Dis. 2020; 26:971–973.

78. Alsheef MA, Alabbad AM, Albassam RA, et al. Pregnancy and venous thromboembolism: risk factors, trends, management, and mortality. Biomed Res Int. 2020; 2020:4071892.

79. De Lima-Karagiannis A, Juillerat P, Sebastian S, Pedersen N, Bar-Gil Shitrit A, van der Woude CJ. Management of pregnant inflammatory bowel disease patients during the COVID-19 pandemic. J Crohns Colitis. 2020; 14(14 Suppl 3):S807–S814.

80. Vassilopoulou E, Feketea G, Koumbi L, Mesiari C, Berghea EC, Konstantinou GN. Breastfeeding and COVID-19: from nutrition to immunity. Front Immunol. 2021; 12:661806.

81. Zhu C, Liu W, Su H, et al. Breastfeeding risk from detectable severe acute respiratory syndrome coronavirus 2 in breastmilk. J Infect. 2020; 81:452–482.

82. World Health Organization. Breastfeeding and COVID-19: scientific brief, 23 June 2020 [Internet]. c2020 [cited 2021 Jul 28]. https://apps.who.int/iris/handle/10665/332639.

83. Meyer A, Semenzato L, Zureik M, Weill A, Carbonnel F, Dray-Spira R. Risk of severe COVID-19 in patients treated with IBD medications: a French nationwide study. Aliment Pharmacol Ther. 2021; 54:160–166.

84. Siegel CA, Christensen B, Kornbluth A, et al. Guidance for restarting inflammatory bowel disease therapy in patients who withheld immunosuppressant medications during COVID-19. J Crohns Colitis. 2020; 14(14 Suppl 3):S769–S773.

85. Allez M, Fleshner P, Gearry R, Lakatos PL, Rubin DT. Care of the patient with IBD requiring hospitalisation during the COVID-19 pandemic. J Crohns Colitis. 2020; 14(14 Suppl 3):S774–S779.

86. Arons MM, Hatfield KM, Reddy SC, et al. Presymptomatic SARS-CoV-2 infections and transmission in a skilled nursing facility. N Engl J Med. 2020; 382:2081–2090.