염증성 장질환 환자에서 바이러스 간염 = Viral Hepatitis in Patients with Inflammatory Bowel Disease

다국어 초록 (Multilingual Abstract)

There has been a rise in the incidence of inflammatory bowel disease (IBD) in developing countries, including South Korea.
Consequently, the use of immunosuppressive agents such as immunomodulators or biologics has also increased. Due to immunosuppression, patients on these agents are at increased risk of various opportunistic infections during treatment, which may sometimes lead to serious adverse outcomes. Viral hepatitis, especially hepatitis B, is one of the infectious conditions that can be reactivated during immunosuppressive therapy, and adequate strategies for monitoring and prophylaxis are needed to prevent it.
South Korea is one of the countries with intermediate endemicity for hepatitis A and B. Thus, taking adequate precautions against viral hepatitis could prevent new infections or reactivation of these conditions in patients with IBD on immunosuppressive therapy.
In this review article, we have summarized the latest evidence on viral hepatitis in patients with IBD that would be of assistance in clinical practice.

참고문헌 (Reference)

1 Ng SC, "Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century : a systematic review of population-based studies" 390 : 2769-2778, 2017

2 Hou JK, "Viral hepatitis and inflammatory bowel disease" 16 : 925-932, 2010

3 Terrault NA, "Update on prevention, diagnosis, and treatment of chronic hepatitis B : AASLD 2018hepatitis B guidance" 67 : 1560-1599, 2018

4 Ajit Sood ; Kirandeep Kaur ; Arshdeep Singh ; Vandana Midha ; Ramit Mahajan ; Namita Bansal ; Varun Mehta ; Dharmatma Singh, "Trends of inflammatory bowel disease at a tertiary care center in northern India" 대한장연구학회 19 (19): 282-290, 2021

5 GBD 2017 Inflammatory Bowel Disease Collaborators, "The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990-2017 : a systematic analysis for the Global Burden of Disease Study 2017" 5 : 17-30, 2020

6 임선영 ; 김지훈, "The epidemiology of hepatitis B virus infection in Korea" 대한내과학회 34 (34): 945-953, 2019

7 Bell BP, "The diverse patterns of hepatitis A epidemiology in the United States-implications for vaccination strategies" 178 : 1579-1584, 1998

8 Haruhiko Ogata ; Takashi Hagiwara ; Takeshi Kawaberi ; Mariko Kobayashi ; Toshifumi Hibi, "Safety and effectiveness of adalimumab in the treatment of ulcerative colitis: results from a large-scale, prospective, multicenter, observational study" 대한장연구학회 19 (19): 419-429, 2021

9 Ting SW, "Risk of hepatitis B reactivation in patients with psoriasis on ustekinumab" 38 : 873-880, 2018

10 Ahn Soo Min ; Choi Jonggi ; Ye Byong Duk ; Yang Suk-Kyun ; Oh Ji Seon ; Kim Yong‑Gil ; Lee Chang-Keun ; Yoo Bin ; Park Sang Hyoung ; Hong Seokchan, "Risk of Hepatitis B Virus (HBV) Reactivation in Patients with Immune-Mediated Inflammatory Diseases Receiving Biologics: Focus on the Timing of Biologics after Anti-HBV Treatment" 거트앤리버 소화기연관학회협의회 16 (16): 567-574, 2022

11 Alameel T, "Risk of HBV reactivation among IBD patients with occult hepatitis B virus infection" 19 : 621-622, 2021

12 Soo-Kyung Park ; Chang Hwan Choi ; 천재영 ; Heeyoung Lee ; Eun Sun Kim ; Jae Jun Park ; Chan Hyuk Park ; Bo-In Lee ; 정윤호 ; 박동일 ; Do Young Kim ; Hana Park ; 진윤태 ; the IBD Research Group of the Korean Association for the Study of Intestinal Diseases, "Prevention and management of viral hepatitis in inflammatory bowel disease: a clinical practice guideline by the Korean Association for the Study of Intestinal Diseases" 대한장연구학회 18 (18): 18-33, 2020

13 Parnita Harsh ; Vipin Gupta ; Saurabh Kedia ; Sawan Bopanna ; Sucharita Pilli ; Surendernath ; Govind Kumar Makharia ; Vineet Ahuja, "Prevalence of hepatitis B, hepatitis C and human immunodeficiency viral infections in patients with inflammatory bowel disease in north India" 대한장연구학회 15 (15): 97-102, 2017

14 Chevaux JB, "Prevalence of hepatitis B and C and risk factors for nonvaccination in inflammatory bowel disease patients in Northeast France" 16 : 916-924, 2010

15 Papa A, "Prevalence and natural history of hepatitis B and C infections in a large population of IBD patients treated with anti-tumor necrosis factor-α agents" 7 : 113-119, 2013

16 Huang ML, "Prevalence and factors related to hepatitis B and C infection in inflammatory bowel disease patients in China : a retrospective study" 8 : 282-287, 2014

17 Loras C, "Prevalence and factors related to hepatitis B and C in inflammatory bowel disease patients in Spain : a nationwide, multicenter study" 104 : 57-63, 2009

18 Kim YJ, "Possible reactivation of potential hepatitis B virus occult infection by tumor necrosis factor-alpha blocker in the treatment of rheumatic diseases" 37 : 346-350, 2010

19 Melmed GY, "Patients with inflammatory bowel disease are at risk for vaccine-preventable illnesses" 101 : 1834-1840, 2006

20 Dave M, "Opportunistic infections due to inflammatory bowel disease therapy" 20 : 196-212, 2014

21 Madonia S, "Occult hepatitis B and infliximab-induced HBV reactivation" 13 : 508-509, 2007

22 여승재 ; Hyun Seok Lee ; Byung Ik Jang ; Eun Soo Kim ; 전성우 ; 김성국 ; Kyeong Ok Kim ; Yoo Jin Lee ; Hyun Jik Lee ; Kyung Sik Park ; Yun Jin Jung ; 김은영 ; 양창헌, "Nonimmunity against hepatitis B virus infection in patients newly diagnosed with inflammatory bowel disease" 대한장연구학회 16 (16): 400-408, 2018

23 Axiaris G, "Management of hepatitis B virus infection in patients with inflammatory bowel disease under immunosuppressive treatment" 27 : 3762-3779, 2021

24 Sahil Khanna, "Management of Clostridioides difficile infection in patients with inflammatory bowel disease" 대한장연구학회 19 (19): 265-274, 2021

25 Tadakazu Hisamatsu ; Yasuo Suzuki ; Mariko Kobayashi ; Takashi Hagiwara ; Takeshi Kawaberi ; Haruhiko Ogata ; Toshiyuki Matsui ; Mamoru Watanabe ; Toshifumi Hibi, "Long-term safety and effectiveness of adalimumab in Japanese patients with Crohn’s disease: 3-year results from a real-world study" 대한장연구학회 19 (19): 408-418, 2021

26 오신주 ; 신가영 ; Soh Hosim ; 이재곤 ; 임종필 ; Eun Chang Soo ; 이강문 ; 박동일 ; Han Dong Soo ; 김효종 ; 이창균, "Long-term outcomes of infliximab in a real-world multicenter cohort of patients with acute severe ulcerative colitis" 대한장연구학회 19 (19): 323-331, 2021

27 Loras C, "Liver dysfunction related to hepatitis B and C in patients with inflammatory bowel disease treated with immunosuppressive therapy" 59 : 1340-1346, 2010

28 Moon HW, "Laboratory characteristics of recent hepatitis A in Korea : ongoing epidemiological shift" 16 : 1115-1118, 2010

29 "Korean National Health and Nutrition Examination Survey (KNHANES). [Internet]"

30 Lan JL, "Kinetics of viral loads and risk of hepatitis B virus reactivation in hepatitis B core antibody-positive rheumatoid arthritis patients undergoing anti-tumour necrosis factor alpha therapy" 70 : 1719-1725, 2011

31 Gisbert JP, "Kinetics of anti-hepatitis B surface antigen titers after hepatitis B vaccination in patients with inflammatory bowel disease" 19 : 554-558, 2013

32 Korean Association for the Study of the Liver (KASL), "KASL clinical practice guidelines for management of chronic hepatitis B" 대한간학회 25 (25): 93-159, 2019

33 The Korean Association for the Study of the Liver, "KASL clinical practice guidelines for management of chronic hepatitis B" 대한간학회 28 (28): 276-331, 2022

34 The Korean Association for the Study of the Liver, "KASL clinical practice guidelines for liver cirrhosis: Ascites and related complications" 대한간학회 24 (24): 169-229, 2018

35 Korean Association for the Study of the Liver, "KASL clinical practice guidelines : management of hepatitis C" 22 : 76-139, 2016

36 Pratt PK Jr, "Improved antibody response to three additional hepatitis B vaccine doses following primary vaccination failure in patients with inflammatory bowel disease" 64 : 2031-2038, 2019

37 Loras C, "Impact of surveillance of hepatitis b and hepatitis c in patients with inflammatory bowel disease under anti-TNF therapies : multicenter prospective observational study(REPENTINA 3)" 8 : 1529-1538, 2014

38 Aygen B, "Immunosuppressive therapy and the risk of hepatitis B reactivation : consensus report" 29 : 259-269, 2018

39 Cossio-Gil Y, "Immunogenicity of hepatitis B vaccine in patients with inflammatory bowel disease and the benefits of revaccination" 30 : 92-98, 2015

40 Bell BP, "Immunogenicity of an inactivated hepatitis A vaccine in infants and young children" 26 : 116-122, 2007

41 Jiang HY, "Immune response to hepatitis B vaccination among people with inflammatory bowel diseases : a systematic review and meta-analysis" 35 : 2633-2641, 2017

42 Kochhar GS, "Hepatitis-B vaccine response in inflammatory bowel disease patients : a systematic review and meta-analysis" 27 : 1610-1619, 2021

43 Ghany MG, "Hepatitis C guidance 2019 update : American Association for the Study of Liver Diseases-Infectious Diseases Society of America recommendations for testing, managing, and treating hepatitis C virus infection" 71 : 686-721, 2020

44 Millman AJ, "Hepatitis C : review of the epidemiology, clinical care, and continued challenges in the direct acting antiviral era" 4 : 174-185, 2017

45 World Health Organization, "Hepatitis B vaccines: WHO position paper, July 2017 - Recommendations" 37 : 223-225, 2019

46 Coates T, "Hepatitis B vaccines : assessment of the seroprotective efficacy of two recombinant DNA vaccines" 23 : 392-403, 2001

47 Loomba R, "Hepatitis B reactivation associated with immune suppressive and biological modifier therapies : current concepts, management strategies, and future directions" 152 : 1297-1309, 2017

48 Irving GJ, "Hepatitis A immunisation in persons not previously exposed to hepatitis A" 2012 : CD009051-, 2012

49 Van Damme P, "Hepatitis A booster vaccination : is there a need?" 362 : 1065-1071, 2003

50 "Global hepatitis report 2017. [Internet]"

51 Hollinger FB, "Fields virology" Lippincott-Raven 1996

52 Cardona AM, "Evaluation of the safety and effectiveness of direct-acting antiviral drugs in the treatment of hepatitis C in patients with inflammatory bowel disease : national multicenter study(ENEIDA registry). MIC project" 16 (16): i321-i322, 2022

53 Korea Centers for Disease Control and Prevention, "Epidemiology and management of vaccine preventable disease" Korea Centers for Disease Control and Prevention 2017

54 Kwak MS, "Emerging trends of inflammatory bowel disease in South Korea : a nationwide population-based study" 34 : 1018-1026, 2019

55 Park SH, "Efficacy of hepatitis A vaccination and factors impacting on seroconversion in patients with inflammatory bowel disease" 20 : 69-74, 2014

56 Toshifumi Hibi ; Isao Kamae ; Philippe Pinton ; Lyann Ursos ; Ryuichi Iwakiri ; Greg Hather ; Haridarshan Patel, "Efficacy of biologic therapies for biologic-naïve Japanese patients with moderately to severely active ulcerative colitis: a network meta-analysis" 대한장연구학회 19 (19): 53-61, 2021

57 Choon Jin Ooi ; Ida Normiha Hilmi ; 김효종 ; Umesh Jalihal ; Deng Chyang Wu ; Dirk Demuth ; Dirk Lindner ; Shashi Adsul, "Efficacy and safety of vedolizumab in ulcerative colitis in patients from Asian countries in the GEMINI 1 study" 대한장연구학회 19 (19): 71-82, 2021

58 Rupa Banerjee ; Sai Wei Chuah ; Ida Normiha Hilmi ; Deng Chyang Wu ; 양석균 ; Dirk Demuth ; Dirk Lindner ; Shashi Adsul, "Efficacy and safety of vedolizumab in Crohn’s disease in patients from Asian countries in the GEMINI 2 study" 대한장연구학회 19 (19): 83-94, 2021

59 Tadakazu Hisamatsu ; 김효종 ; Satoshi Motoya ; Yasuo Suzuki ; Yoshifumi Ohnishi ; Noriyuki Fujii ; Nobuko Matsushima ; Richuan Zheng ; Colleen W. Marano, "Efficacy and safety of ustekinumab in East Asian patients with moderately to severely active ulcerative colitis: a subpopulation analysis of global phase 3 induction and maintenance studies (UNIFI)" 대한장연구학회 19 (19): 386-397, 2021

60 Morisco F, "Effect of immunosuppressive therapy on patients with inflammatory bowel diseases and hepatitis B or C virus infection" 20 : 200-208, 2013

61 Kucharzik T, "ECCO guidelines on the prevention, diagnosis, and management of infections in inflammatory bowel disease" 15 : 879-913, 2021

62 European Association for the Study of the Liver, "EASL recommendations on treatment of hepatitis C : Final update of the series" 73 : 1170-1218, 2020

63 European Association for the Study of the Liver, "EASL 2017 clinical practice guidelines on the management of hepatitis B virus infection" 67 : 370-398, 2017

64 김유선, "Does cytomegalovirus load predict the outcome of acute severe ulcerative colitis?" 대한장연구학회 19 (19): 357-359, 2021

65 Gisbert JP, "Comparison of the effectiveness of two protocols for vaccination(standard and double dosage)against hepatitis B virus in patients with inflammatory bowel disease" 35 : 1379-1385, 2012

66 Park SH, "Clinical courses of chronic hepatitis B virus infection and inflammatory bowel disease in patients with both diseases" 18 : 2004-2010, 2012

67 Lee Ji Min ; Wei Shu-Chen ; Lee Kang-Moon ; Ye Byong Duk ; Mao Ren ; 김현수 ; Park Soo Jung ; Park Sang Hyoung ; Oh Eun Hye ; Im Jong Pil ; Jang Byung Ik ; Kim Dae Bum ; Takeuchi Ken, "Clinical Course of Hepatitis B Viral Infection in Patients Undergoing Anti-Tumor Necrosis Factor α Therapy for Inflammatory Bowel Disease" 거트앤리버 소화기연관학회협의회 16 (16): 396-403, 2022

68 Esteve M, "Chronic hepatitis B reactivation following infliximab therapy in Crohn's disease patients : need for primary prophylaxis" 53 : 1363-1365, 2004

69 Perrillo RP, "American Gastroenterological Association Institute technical review on prevention and treatment of hepatitis B virus reactivation during immunosuppressive drug therapy" 148 : 221-244.e3, 2015

70 Reddy KR, "American Gastroenterological Association Institute guideline on the prevention and treatment of hepatitis B virus reactivation during immunosuppressive drug therapy" 148 : 215-e17-, 2015

71 Farraye FA, "ACG clinical guideline : preventive care in inflammatory bowel disease" 112 : 241-258, 2017

72 Park SH, "A 30-year trend analysis in the epidemiology of inflammatory bowel disease in the Songpa-Kangdong district of Seoul, Korea in 1986-2015" 13 : 1410-1417, 2019

73 Rubin LG, "2013 IDSA clinical practice guideline for vaccination of the immunocompromised host" 58 : 309-318, 2014