Geography Influences Susceptibility to SARS-CoV-2 Serological Response in Patients With Inflammatory Bowel Disease: Multinational Analysis From the ICARUS-IBD Consortium

Author:

Wong Serre-Yu1,Wellens Judith2,Helmus Drew1,Marlow Luke3,Brann Stephanie3,Martinez Pazos Vicky1,Weinberg Alan4,Moran Hunter R1,McGregor Colleen3,Vermeire Séverine2,Watanabe Kenji5,Kamikozuru Koji5,Ahuja Vineet6,Vermani Shubi6,Lindsay James O7,Kingston Ashley7,Dutta Usha8,Kaur Harmandeep8,Silverberg Mark S9,Milgrom Raquel9,Chien Ng Siew10,Mak Joyce Wing Yan10,Cadwell Ken111213,Thompson Craig14,Colombel Jean-Frédéric1,Satsangi Jack3,Ambrose Tim15,Brain Oliver15,Walsh Alissa15,Klenerman Paul15,Travis Simon15,Edmans Matthew15,Dixon Rebekah16,Navalurkar Reema17,Gold Stephanie16,Lacoste Joshua16,Chen Clara18,Halfvarson Jonas19,Bergemalm Daniel19,Rubin David T20,Abreu Maria T21,Allez Matthieu22,Anne Neil Jessica23,Sota Stela23,Ku Jang Kyung23,Ching Krystal23,Venzon Mericien23,Yao Xiaomin23,Bernard Lucie23,Cowger Tori L24,Accorsi Emma24,Wiseman Dean16,Riggs Alexa16,Stanley Stephanie16,Reyes-Mercedes Pamela16,Mendiolaza Michelle16,Nunez Sara16,Phillipe Brianne16,Chen Xin16,Tankelevich Michael16,Jimenez Darwin16,Ramos Julio16,Kedia Saurabh6,Yokoyama Yoko25,Kawai Mikio25,Sato Toshiyuki25,Kojima Kentaro25,Nagase Kazuko25,Nakamura Shiro25,Miyazaki Takako25,Kakimoto Kazuki25,Kamata Noriko25,Hosomi Shuhei25,Nishishita Masakazu25,Chan Alicia26,Sharma Vishal8,Singh Kumar Anupam8,Samanta Jayanta8,Shah Jimil8,Sinha S K8,Cipriano Bessie27,Lee Irish27,Ruocco Giuseppe27,Garcia Nicole20,Choi Natalie20,Alejandra Quintero Maria21,

Affiliation:

1. Henry D. Janowitz Division of Gastroenterology, Icahn School of Medicine at Mount Sinai , New York, NY , USA

2. Department of Gastroenterology and Hepatology, Leuven University Hospitals , Leuven , Belgium

3. Translational Gastroenterology Unit, Nuffield Department of Medicine, University of Oxford , Oxford , United Kingdom

4. Department of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai , New York, NY , USA

5. Center for Inflammatory Bowel Disease, Division of Internal Medicine, Hyogo College of Medicine , Nishinomiya , Japan

6. Department of Gastroenterology, All India Institute of Medical Sciences , New Delhi , India

7. Center for Immunobiology, Blizard Institute, Queen Mary University of London – Barts Health NHS Trust , London , United Kingdom

8. Postgraduate Institute of Medical Education and Research , Chandigarh , India

9. Division of Gastroenterology, Department of Medicine, Mount Sinai Hospital, University of Toronto , Toronto, Ontario , Canada

10. Division of Gastroenterology and Hepatology, Prince of Wales Hospital, The Chinese University of Hong Kong , Hong Kong , China

11. Division of Gastroenterology and Hepatology, Department of Medicine, Perelman School of Medicine of the University of Pennsylvania , Pennsylvania, PA , USA

12. Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine of the University of Pennsylvania , Pennsylvania, PA , USA

13. Department of Pathology and Laboratory Medicine, Perelman School of Medicine of the University of Pennsylvania , Pennsylvania, PA , USA

14. Division of Biomedical Sciences, Warwick Medical School, University of Warwick , Warwick , United Kingdom

15. Translational Gastroenterology Unit, Nuffield Department of Medicine, University of Oxford , Oxford , UK

16. The Henry D. Janowitz Division of Gastroenterology, Icahn School of Medicine at Mount Sinai , New York , USA

17. University of Washington , Washington , USA

18. Department of Medicine, Stony Brook University Hospital , Stony Brook, New York , USA

19. Örebro University Hospital , Örebro , Sweden

20. University of Chicago Inflammatory Bowel Disease Center , Chicago , USA

21. University of Miami , Miami , USA

22. Assistance Publique, Hopitaux De Paris, Hopital Saint-Louis , Paris , France

23. Department of Microbiology, New York University Grossman School of Medicine , New York , USA

24. Center for Communicable Disease Dynamics, Department of Epidemiology, Harvard T.H. Chan School of Public Health , Boston, MA , USA

25. Center for Inflammatory Bowel Disease, Division of Internal Medicine, Hyogo College of Medicine , Japan

26. Division of Gastroenterology and Hepatology, The Chinese University of Hong Kong - Prince of Wales Hospital , Hong Kong

27. Center for Immunobiology, Blizard Institute, Queen Mary University of London - Barts Health NHS Trust , London , UK

Abstract

Abstract Background Beyond systematic reviews and meta-analyses, there have been no direct studies of serological response to COVID-19 in patients with inflammatory bowel disease (IBD) across continents. In particular, there has been limited data from Asia, with no data reported from India. The ICARUS-IBD (International study of COVID-19 Antibody Response Under Sustained immunosuppression in IBD) consortium assessed serological response to SARS-CoV-2 in patients with IBD in North America, Europe, and Asia. Methods The ICARUS-IBD study is a multicenter observational cohort study spanning sites in 7 countries. We report seroprevalence data from 2303 patients with IBD before COVID-19 vaccination between May 2020 and November 2021. SARS-CoV-2 anti-spike and anti-nucleocapsid antibodies were analyzed. Results The highest and lowest SARS-CoV-2 anti-spike seropositivity rates were found in Asia (81.2% in Chandigarh and 57.9% in Delhi, India; and 0% in Hong Kong). By multivariable analysis, country (India: odds ratio [OR], 18.01; 95% confidence interval [CI], 12.03-26.95; P < .0001; United Kingdom: OR, 2.43; 95% CI, 1.58-3.72; P < .0001; United States: OR, 2.21; 95% CI, 1.27-3.85; P = .005), male sex (OR, 1.46; 95% CI, 1.07-1.99; P = .016), and diabetes (OR, 2.37; 95% CI, 1.04-5.46; P = .039) conferred higher seropositivity rates. Biological therapies associated with lower seroprevalence (OR, 0.22; 95% CI, 0.15-0.33; P < .0001). Multiple linear regression showed associations between anti-spike and anti-nucleocapsid titers with medications (P < .0001) but not with country (P = .3841). Conclusions While the effects of medications on anti-SARS-CoV-2 antibody titers in patients with IBD were consistent across sites, geographical location conferred the highest risk of susceptibility to serologically detectable SARS-CoV-2 infection. Over half of IBD patients in India were seropositive prior to vaccination. These insights can help to inform shielding advice, therapeutic choices, and vaccine strategies in IBD patients for COVID-19 and future viral challenges.

Funder

Chandigarh Institutional Ethics Committee

Digestive System in Children and Adults

Postgraduate Institute of Medical Education and Research

All India Institute of Medical Sciences Institute

Publisher

Oxford University Press (OUP)

Subject

Gastroenterology,Immunology and Allergy

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