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Koppelman LJM, Oyugi AA, Maljaars PWJ, van der Meulen-de Jong AE. Modifiable Factors Influencing Disease Flares in Inflammatory Bowel Disease: A Literature Overview of Lifestyle, Psychological, and Environmental Risk Factors. J Clin Med 2025; 14:2296. [PMID: 40217745 PMCID: PMC11989426 DOI: 10.3390/jcm14072296] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/29/2025] [Revised: 03/21/2025] [Accepted: 03/24/2025] [Indexed: 04/14/2025] Open
Abstract
Background: A significant concern for patients with Inflammatory Bowel Disease (IBD) is predicting and managing disease flares. While healthcare providers rely on biomarkers, providing conclusive patient advice remains challenging. This review explores the role of lifestyle, psychological health, and environmental exposures in the prediction and management of IBD flares. Methods: This review followed PRISMA guidelines (2020). A structured search was conducted in PubMed for articles published between 2012 and 2024, using free and Medical Subject Heading (MeSH) terms for predicting factors in IBD. Inclusion criteria included studies reporting primary data on modifiable clinical or environmental predictors of IBD relapse, excluding studies on post-operative investigations, treatment cessation, and pediatric or pregnant populations. The Mixed Method Appraisal Tool (MMAT) was used to assess the quality of the studies. Results: Out of 2287 identified citations, 58 articles were included. Several modifiable factors influencing disease flares were identified, including psychological stress, sleep disturbances, smoking, and nutrition. Poor sleep quality and mental health were linked to increased flare risks, while smoking was associated with higher relapse rates in Crohn's disease. Environmental exposures, such as heat waves and high-altitude regions, also contributed. Predictive models integrating clinical, lifestyle, and psychological factors showed promising accuracy but require further refinement. Limitations of this review include the potential for publication bias, variability in flare definitions, and limited sample sizes Conclusions: Key predictors of IBD flares include dietary factors, psychological stress, poor sleep quality, and pharmacological influences. Personalized approaches integrating these predictors can optimize disease control and improve patient outcomes.
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Affiliation(s)
- Lola J. M. Koppelman
- Department of Gastroenterology and Hepatology, Leiden University Medical Centre, 2333 ZA Leiden, The Netherlands
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2
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Rinebold E, Huang AL, Hahn SJ. How to Approach the Difficult Perineum in Crohn's Disease. Clin Colon Rectal Surg 2025; 38:148-159. [PMID: 39944307 PMCID: PMC11813606 DOI: 10.1055/s-0044-1786377] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 05/09/2025]
Abstract
Crohn's disease (CD) is a chronic, inflammatory bowel disease with a wide range of presentations, including perianal disease. Presentation is variable, ranging from skin tags to complex fistulas, strictures, and nonhealing wounds. Symptoms of perianal CD can be devastating and may impact quality of life. Optimal management requires coordinated medical and surgical therapy. When possible, conservative treatment of perianal disease should be attempted. However, surgical treatment is often required, and some patients may ultimately require total proctocolectomy with permanent diversion due to the severity of disease. Even with close attention and treatment, disease can be recurrent, and complications of treatment are sometimes worse than the initial presentation. Novel treatments, including use of mesenchymal stem cells and autologous fat grafting, hold some promise, but are not yet widely available. Thorough knowledge of treatment options, careful patient selection, coordination between medical and surgical providers, and setting realistic expectations are important in the successful treatment of difficult perineal CD.
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Affiliation(s)
- Emily Rinebold
- Division of Colon and Rectal Surgery, Department of Surgery, Icahn School of Medicine at Mount Sinai, Mount Sinai Hospital, New York, New York
| | - Alex L. Huang
- Division of Colon and Rectal Surgery, Department of Surgery, Icahn School of Medicine at Mount Sinai, Mount Sinai Hospital, New York, New York
| | - Sue J. Hahn
- Division of Colon and Rectal Surgery, Department of Surgery, Icahn School of Medicine at Mount Sinai, Mount Sinai Hospital, New York, New York
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Rossier LN, Décosterd NP, Matter CB, Staudenmann DA, Moser A, Egger B, Seibold FW. SARS-CoV-2 vaccination in inflammatory bowel disease patients is not associated with flares: a retrospective single-centre Swiss study. Ann Med 2024; 56:2295979. [PMID: 38289017 PMCID: PMC10829820 DOI: 10.1080/07853890.2023.2295979] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/27/2023] [Accepted: 12/12/2023] [Indexed: 02/01/2024] Open
Abstract
INTRODUCTION Vaccination hesitancy is an important barrier to vaccination among IBD patients. The development of adverse events is the main concern reported. The purpose of this monocentric study was to assess SARS-CoV-2 vaccination safety in IBD patients by evaluating the postvaccination flare risk and incidence of overall adverse events. METHODS Surveys were handed out on three consecutive months to each patient presenting at the Crohn-Colitis Centre, where they documented their vaccination status and any side effects experienced after vaccination.Dates of flares occurring in 2021 were recorded from their electronic medical records. Baseline and IBD characteristics and flare incidence were compared between the vaccinated and unvaccinated patients, and among the vaccinated population before and after their vaccination doses. The characteristics of patients who developed side effects and of those who did not were compared. RESULTS We enrolled 396 IBD patients, of whom 91% were vaccinated. The proportion of patients who experienced flares was statistically not different between the vaccinated and the unvaccinated population (1.8 vs 2.6 flares per 100 person-months (p = 0.28)). Among vaccinated patients, there was no difference across the prevaccination, 1 month post any vaccination, and more than 1 month after any vaccination periods, and between the Spikevax and Cominarty subgroups. Overall, 46% of patients reported vaccination side effects, mostly mild flu-like symptoms. CONCLUSION SARS-CoV-2 vaccination with mRNA vaccines seems safe, with mostly mild side effects. The IBD flare risk is not increased in the month following any vaccination.
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Affiliation(s)
- Laura N. Rossier
- Intesto, Gastroenterology and Crohn-Colitis Center, Fribourg and Berne, Switzerland
- Faculty of Medicine, University of Fribourg, Switzerland
| | - Natalie P. Décosterd
- Intesto, Gastroenterology and Crohn-Colitis Center, Fribourg and Berne, Switzerland
| | - Christoph B. Matter
- Intesto, Gastroenterology and Crohn-Colitis Center, Fribourg and Berne, Switzerland
| | - Dominic A. Staudenmann
- Intesto, Gastroenterology and Crohn-Colitis Center, Fribourg and Berne, Switzerland
- Faculty of Medicine, University of Fribourg, Switzerland
| | | | - Bernhard Egger
- Faculty of Medicine, University of Fribourg, Switzerland
- Department of Surgery, Cantonal Hospital Fribourg
| | - Frank W. Seibold
- Intesto, Gastroenterology and Crohn-Colitis Center, Fribourg and Berne, Switzerland
- Faculty of Medicine, University of Fribourg, Switzerland
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4
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Classen JM, Muzalyova A, Römmele C, Nagl S, Ebigbo A, Schnoy E. Antibody Response to SARS-CoV-2 before and after the Third Vaccination in Patients with Inflammatory Bowel Disease. Dig Dis 2024; 43:19-27. [PMID: 39616993 DOI: 10.1159/000542353] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/15/2024] [Accepted: 10/27/2024] [Indexed: 12/25/2024]
Abstract
INTRODUCTION Patients with inflammatory bowel disease (IBD) receiving immunosuppressive therapy might have an increased risk of developing a severe course of SARS-CoV-2 infection. The aim of this study was to investigate the development of antibodies in immunosuppressed patients with IBD compared to a healthy control group and to determine the effect of immunomodulators on the level of anti-SARS-CoV-2 IgG antibody levels before and after a third vaccination against SARS-CoV-2. METHODS This is a single-center study with a retrospective observational design. Seventy-one IBD patients matched by propensity score to 71 healthy employees (control group) were included. Blood was taken from both groups at predetermined times before and after the third booster vaccination. RESULTS All patients with IBD (n = 71, 100%) received immunomodulatory therapy. The mean antibody level before the third vaccination was 1,352.88 U/mL (SD = 1,011.489) in the IBD group and was not lower compared to the control group (p = 0.088). Gender, age, and disease duration had no significant impact on the development of antibody levels. Patients with TNF-alpha blockers had significantly lower antibody titers (p = 0.011) compared to the control group. Patients with integrin inhibitor therapy had significantly higher antibody titers (p = 0.003) than the controls. After the third vaccination, an increase in antibody titers was recorded in all patients in the IBD group. CONCLUSION We recorded an antibody titer in all patients with IBD that was not significantly lower compared to healthy controls despite immunomodulatory therapy. The booster vaccination led to an increase in antibody levels in all patients with IBD.
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Affiliation(s)
| | - Anna Muzalyova
- Internal Medicine III, University Hospital Augsburg, Augsburg, Germany
| | - Christoph Römmele
- Internal Medicine III, University Hospital Augsburg, Augsburg, Germany
| | - Sandra Nagl
- Internal Medicine III, University Hospital Augsburg, Augsburg, Germany
| | - Alanna Ebigbo
- Internal Medicine III, University Hospital Augsburg, Augsburg, Germany
| | - Elisabeth Schnoy
- Internal Medicine III, University Hospital Augsburg, Augsburg, Germany,
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5
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Vitus ES, Mann S, Lees CW, Jess T, Elmahdi R. A Systematic Review and Meta-Analysis: Adverse Inflammatory Bowel Disease Outcomes Following Acute COVID-19. GASTRO HEP ADVANCES 2024; 4:100581. [PMID: 39926204 PMCID: PMC11803825 DOI: 10.1016/j.gastha.2024.10.021] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 06/03/2024] [Accepted: 10/18/2024] [Indexed: 02/11/2025]
Abstract
Background and Aims Respiratory viral infections have been implicated in the exacerbation of immune-mediated inflammatory diseases such as inflammatory bowel disease (IBD). To understand the impact of early SARS-CoV-2 variants on the risk of adverse IBD outcomes, we aimed to perform a meta-analysis of high-quality studies. Methods Cohort studies investigating adverse IBD outcomes (IBD flares, change in disease activity, change in medication, IBD-related hospitalization, and surgery) following COVID-19 were retrieved from MEDLINE and Embase. The Risk Of Bias In Nonrandomized Studies-of Exposure tool was used to assess risk of bias. Random effects model meta-analysis was used to calculate the hazard ratio (HR) for risk of adverse outcomes. Subgroup analysis was performed to estimate risk of outcomes for ulcerative colitis and Crohn's disease patients. Metaregression was performed for sex and duration of follow-up. Results Of the 3119 identified studies, 5 were included in the meta-analysis. A total of 34,977 IBD patients with COVID-19 and 53,270 IBD patients without recorded COVID-19 infection were identified. Two of the studies showed a high risk of bias. The random effects model did not show a statistically significant increase in the risk of adverse IBD outcomes following COVID infection (HR:1.05 [0.75-1.46]). There was no significant difference in adverse outcomes between Crohn's disease (HR: 0.91 [0.82-1.02]) and ulcerative colitis patients (HR: 0.83 [0.76-0.90]). Neither the proportion of male participants nor the mean duration of follow-up were found to be significant predictors of effect size. Conclusion In this systematic review and meta-analysis, we find that COVID-19 did not increase the risk of adverse IBD outcomes.
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Affiliation(s)
- Evangelin Shaloom Vitus
- Department of Clinical Medicine, PREDICT Center for Molecular Prediction of Inflammatory Bowel Disease, Aalborg University, Copenhagen, Denmark
| | - Simran Mann
- Department of Anesthetics, St Peter’s Hospital, Ashford and St Peter’s NHS Trust, Chertsey, UK
| | - Charlie W. Lees
- Centre for Genomics and Experimental Medicine, University of Edinburgh, Edinburgh, Scotland
- Department of Gastroenterology and Hepatology, the Western General Hospital, Edinburgh, Scotland
| | - Tine Jess
- Department of Clinical Medicine, PREDICT Center for Molecular Prediction of Inflammatory Bowel Disease, Aalborg University, Copenhagen, Denmark
- Department of Gastroenterology and Hepatology, Aalborg University Hospital, Aalborg, Denmark
| | - Rahma Elmahdi
- Department of Clinical Medicine, PREDICT Center for Molecular Prediction of Inflammatory Bowel Disease, Aalborg University, Copenhagen, Denmark
- Department of Gastroenterology and Hepatology, Aalborg University Hospital, Aalborg, Denmark
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Long MD, Parlett L, Lewis JD, Haynes K, Adimadhyam S, Hou L, Wolfe A, Toh S, Burris J, Dorand J, Kappelman MD. Corticosteroids but not Anti-TNF Are Associated With Increased COVID-19 Complications in Patients With Inflammatory Bowel Disease. Inflamm Bowel Dis 2024; 30:1345-1352. [PMID: 37611117 DOI: 10.1093/ibd/izad176] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/28/2022] [Indexed: 08/25/2023]
Abstract
BACKGROUND AND AIMS Immunosuppressed individuals are at higher risk for COVID-19 complications, yet data in patients with inflammatory bowel disease (IBD) are limited. We evaluated the risk of COVID-19- severe sequelae by medication utilization in a large cohort of patients with IBD. METHODS We conducted a retrospective cohort study utilizing insurance claims data between August 31, 2019, and August 31, 2021.We included IBD patients identified by diagnosis and treatment codes. Use of IBD medications was defined in the 90 days prior to cohort entry. Study outcomes included COVID-19 hospitalization, mechanical ventilation, and inpatient death. Patients were followed until the outcome of interest, outpatient death, disenrollment, or end of study period. Due to the aggregate nature of available data, we were unable to perform multivariate analyses. RESULTS We included 102 986 patients (48 728 CD, 47 592 UC) with a mean age of 53 years; 55% were female. Overall, 412 (0.4%) patients were hospitalized with COVID-19. The incidence of hospitalization was higher in those on corticosteroids (0.6% vs 0.3%; P < .0001; 13.6 per 1000 person-years; 95% confidence interval [CI], 10.8-16.9) and lower in those receiving anti-tumor necrosis factor α therapy (0.2% vs 0.5%; P < .0001; 3.9 per 1000 person-years; 95% CI, 2.7-5.4). Older age was associated with increased hospitalization with COVID-19. Overall, 71 (0.07%) patients required mechanical ventilation and 52 (0.05%) died at the hospital with COVID-19. The proportion requiring mechanical ventilation (1.9% vs 0.05%; P < .0001; 3.9 per 1000 person-years; 95% CI, 2.5-5.9) was higher among users of corticosteroids. CONCLUSIONS Among patients with IBD, those on corticosteroids had more hospitalizations and mechanical ventilation with COVID-19. Anti-tumor necrosis factor α therapy was associated with a decreased risk of hospitalization. These findings reinforce previous guidance to taper and/or discontinue corticosteroids in IBD.
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Affiliation(s)
- Millie D Long
- Department of Medicine and Department of Pediatrics, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
| | | | - James D Lewis
- Department of Medicine, Perlman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
| | | | - Sruthi Adimadhyam
- Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA
| | - Laura Hou
- Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA
| | - Audrey Wolfe
- Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA
| | - Sengwee Toh
- Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA
| | | | | | - Michael D Kappelman
- Department of Medicine and Department of Pediatrics, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA
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7
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Mercuri C, Catone M, Bosco V, Guillari A, Rea T, Doldo P, Simeone S. Motivational Interviewing as a Strategy to Improve Adherence in IBD Treatment: An Integrative Review Amidst COVID-19 Disruptions. Healthcare (Basel) 2024; 12:1210. [PMID: 38921325 PMCID: PMC11204356 DOI: 10.3390/healthcare12121210] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/18/2024] [Revised: 04/25/2024] [Accepted: 06/15/2024] [Indexed: 06/27/2024] Open
Abstract
Aims and Objectives: This review aims to analyze the effectiveness of motivational interviewing (MI) in enhancing therapeutic adherence and compliance in adult patients with inflammatory bowel disease (IBD), especially considering the disruptions caused by the COVID-19 pandemic. Background: IBD, which includes conditions such as ulcerative colitis and Crohn's disease, affects over 10 million people globally. It significantly impacts both physical and psychological well-being, leading to challenges in therapeutic adherence. Only 25-47% of patients with IBD adequately follow prescribed treatments. Design and Methods: An integrative methodology that combines qualitative and quantitative research was utilized, following a 7-step framework. This framework encompasses identifying the research question, devising a search strategy, performing a critical appraisal, summarizing findings, extracting data, conducting an analysis, and drawing conclusions. Results: Poor adherence to therapy among patients with IBD can exacerbate disease progression and result in complications. MI has been identified as a promising approach to improving both adherence and treatment outcomes. Studies, including those predating the COVID-19 pandemic, have demonstrated MI's effectiveness in enhancing adherence among patients with IBD. Conclusions: MI shows promise in enhancing adherence among adult patients with IBD. Although initial results are promising, additional research is needed to thoroughly understand its effectiveness across various clinical contexts. Relevance to Clinical Practice: The findings underscore the potential of MI as an integral component of IBD treatment strategies, suggesting that its implementation could enhance patient-provider interactions and lead to better overall health outcomes.
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Affiliation(s)
- Caterina Mercuri
- Clinical and Experimental Medicine Department, Magna Graecia University, 88100 Catanzaro, Italy; (C.M.); (P.D.); (S.S.)
| | - Maria Catone
- Department of Public Health, University of Naples Federico II, 80138 Naples, Italy; (M.C.); (T.R.)
| | - Vincenzo Bosco
- Department of Medical and Surgical Sciences, University Hospital Mater Domini, Magna Graecia University, 88100 Catanzaro, Italy;
| | - Assunta Guillari
- Department of Public Health, University of Naples Federico II, 80138 Naples, Italy; (M.C.); (T.R.)
| | - Teresa Rea
- Department of Public Health, University of Naples Federico II, 80138 Naples, Italy; (M.C.); (T.R.)
| | - Patrizia Doldo
- Clinical and Experimental Medicine Department, Magna Graecia University, 88100 Catanzaro, Italy; (C.M.); (P.D.); (S.S.)
| | - Silvio Simeone
- Clinical and Experimental Medicine Department, Magna Graecia University, 88100 Catanzaro, Italy; (C.M.); (P.D.); (S.S.)
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Schmidt C, Stallmach A, Sturm A, Bachmann O, Helwig U, Koletzko S, Lynen P, Schnoy E, Dignass A, Kucharzik T, Blumenstein I. [Update: Addendum to S3-Guidelines Crohn disease and ulcerative colitis: Management of Patients with Inflammatory Bowel Disease with regard to COVID-19 (version 2.0)]. ZEITSCHRIFT FUR GASTROENTEROLOGIE 2024; 62:517-534. [PMID: 38599579 DOI: 10.1055/a-2255-7184] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 04/12/2024]
Affiliation(s)
- Carsten Schmidt
- Medizinischen Klinik II (Gastroenterologie, Hepatologie, Endokrinologie, Diabetologie und Infektiologie), Klinikum Fulda, Universitätsmedizin Marburg-Campus Fulda, Fulda
- Medizinische Fakultät der Friedrich-Schiller-Universität, Jena
| | - Andreas Stallmach
- Klinik für Innere Medizin IV (Gastroenterologie, Infektiologie und Hepatologie), Universitätsklinikum Jena, Jena
| | - Andreas Sturm
- Klinik für Innere Medizin, Schwerpunkt Gastroenterologie, DRK Kliniken Berlin | Westend, Berlin
| | - Oliver Bachmann
- Klinik für Innere Medizin 1, Siloah St. Trudpert Klinikum, Pforzheim
| | - Ulf Helwig
- Internistische Praxengemeinschaft Oldenburg, Oldenburg
| | - Sibylle Koletzko
- Ehem. Kinderklinik und Kinderpoliklinik im Dr. von Hauner Kinderspital, LMU Klinikum der Universität München, München
| | - Petra Lynen
- Deutsche Gesellschaft für Gastroenterologie, Verdauungs- und Stoffwechselkrankheiten, Berlin
| | - Elisabeth Schnoy
- III. Medizinische Klinik, Universitätsklinikum Augsburg, Augsburg
| | - Axel Dignass
- Medizinischen Klinik I, Agaplesion Markus Krankenhaus, Frankfurt
| | - Torsten Kucharzik
- Klinik für Innere Medizin & Gastroenterologie, Klinikum Lüneburg, Lüneburg
| | - Irina Blumenstein
- Goethe-Universität Frankfurt, Universitätsklinikum, Medizinische Klinik 1, Frankfurt am Main
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9
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Martínez-Domínguez SJ, García-Mateo S, Sainz-Arnal P, Martínez-García J, Gallego-Llera B, Lozano-Limones MJ, Hidalgo S, Gargallo-Puyuelo CJ, Latre-Santos M, Nocito-Colon MML, Martínez-Lostao L, Refaie E, Arroyo-Villarino MT, Del Rio-Nechaevsky M, Ramirez-Labrada A, Pardo J, Gomollón F, Baptista PM. Unravelling the cellular response to the SARS-COV-2 vaccine in inflammatory bowel disease patients on biologic drugs. Sci Rep 2023; 13:23061. [PMID: 38155275 PMCID: PMC10754931 DOI: 10.1038/s41598-023-50537-y] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/09/2023] [Accepted: 12/21/2023] [Indexed: 12/30/2023] Open
Abstract
Suboptimal vaccine response is a significant concern in patients with Inflammatory Bowel Disease (IBD) receiving biologic drugs. This single-center observational study involved 754 patients with IBD. In Phase I (October 2020-April 2021), 754 IBD participants who had not previously received the SARS-CoV-2 vaccine, underwent blood extraction to assess the seroprevalence of SARS-CoV-2 infection and IBD-related factors. Phase II (May 2021-October 2021) included a subgroup of 52 IBD participants with confirmed previous SARS-CoV-2 infection, who were studied for humoral and cellular response to the SARS-CoV-2 vaccine. In Phase I, treatment with anti-TNF was associated with lower rates of seroconversion (aOR 0.25 95% CI [0.10-0.61]). In Phase II, a significant increase in post-vaccination IgG levels was observed regardless of biologic treatment. However, patients treated with anti-TNF exhibited significantly lower IgG levels compared to those without IBD therapy (5.32 ± 2.47 vs. 7.99 ± 2.59 U/ml, p = 0.042). Following vaccination, a lymphocyte, monocyte, and NK cell activation pattern was observed, with no significant differences between patients receiving biologic drugs and those without IBD treatment. Despite lower seroprevalence and humoral response to the SARS-CoV-2 vaccine in patients treated with anti-TNF, the cellular response to the vaccine did not differ significantly from that patients without IBD therapy.
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Affiliation(s)
- Samuel J Martínez-Domínguez
- Digestive Diseases Department, University Hospital "Lozano Blesa", Av. San Juan Bosco, nº 15. PC: 50009, Zaragoza, Spain.
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain.
- University of Zaragoza, Zaragoza, Spain.
| | - Sandra García-Mateo
- Digestive Diseases Department, University Hospital "Lozano Blesa", Av. San Juan Bosco, nº 15. PC: 50009, Zaragoza, Spain
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
| | | | - Javier Martínez-García
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
| | | | | | - Sandra Hidalgo
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
| | - Carla J Gargallo-Puyuelo
- Digestive Diseases Department, University Hospital "Lozano Blesa", Av. San Juan Bosco, nº 15. PC: 50009, Zaragoza, Spain
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
| | - Marta Latre-Santos
- Digestive Diseases Department, University Hospital "Lozano Blesa", Av. San Juan Bosco, nº 15. PC: 50009, Zaragoza, Spain
| | | | - Luis Martínez-Lostao
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
- Immunology Department, University Hospital "Lozano Blesa", Zaragoza, Spain
- Institute of Nanoscience and Material of Aragón (INMA), Zaragoza, Spain
| | - Engy Refaie
- Scuola di Specializzazione in Chirurgia Generale, Università Degli Studi di Pavia Fondazione IRCCS Policlinico San Matteo, Pavia, Italy
| | - Maria Teresa Arroyo-Villarino
- Digestive Diseases Department, University Hospital "Lozano Blesa", Av. San Juan Bosco, nº 15. PC: 50009, Zaragoza, Spain
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
| | - Marcela Del Rio-Nechaevsky
- CIBEREnfermedadesRaras (CIBERER), Madrid, Spain
- Biomedical Engineering Department, Universidad Carlos III de Madrid, Madrid, Spain
- IIS-Fundación Jiménez Díaz, Madrid, Spain
| | - Ariel Ramirez-Labrada
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
- CIBER Enfermedades Infecciosas (CIBERINFEC), Madrid, Spain
| | - Julián Pardo
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
- CIBER Enfermedades Infecciosas (CIBERINFEC), Madrid, Spain
| | - Fernando Gomollón
- Digestive Diseases Department, University Hospital "Lozano Blesa", Av. San Juan Bosco, nº 15. PC: 50009, Zaragoza, Spain
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- University of Zaragoza, Zaragoza, Spain
- CIBER Enfermedades Hepáticas y Digestivas (CIBEREHD), Madrid, Spain
| | - Pedro M Baptista
- Aragón Health Research Institute (IIS Aragón), Zaragoza, Spain
- Biomedical Engineering Department, Universidad Carlos III de Madrid, Madrid, Spain
- CIBER Enfermedades Hepáticas y Digestivas (CIBEREHD), Madrid, Spain
- Fundación ARAID, Zaragoza, Spain
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10
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Papa A, Covino M, De Lucia SS, Del Gaudio A, Fiorani M, Polito G, Settanni CR, Piccioni A, Franceschi F, Gasbarrini A. Impact of COVID-19 in individuals with and without pre-existent digestive disorders with a particular focus on elderly patients. World J Gastroenterol 2023; 29:4099-4119. [PMID: 37475841 PMCID: PMC10354572 DOI: 10.3748/wjg.v29.i26.4099] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/27/2022] [Revised: 01/10/2023] [Accepted: 03/20/2023] [Indexed: 07/10/2023] Open
Abstract
Coronavirus disease 2019 (COVID-19) has several extrapulmonary symptoms. Gastrointestinal (GI) symptoms are among the most frequent clinical manifestations of COVID-19, with severe consequences reported in elderly patients. Furthermore, the impact of COVID-19 on patients with pre-existing digestive diseases still needs to be fully elucidated, particularly in the older population. This review aimed to investigate the impact of COVID-19 on the GI tract, liver, and pancreas in individuals with and without previous digestive diseases, with a particular focus on the elderly, highlighting the distinctive characteristics observed in this population. Finally, the effectiveness and adverse events of the anti-COVID-19 vaccination in patients with digestive disorders and the peculiarities found in the elderly are discussed.
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Affiliation(s)
- Alfredo Papa
- CEMAD, Center for Diagnosis and Treatment of Digestive Diseases, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Roma 00168, Italy
- CEMAD, Università Cattolica del Sacro Cuore, Roma 00168, Italy
| | - Marcello Covino
- Department of Emergency, Università Cattolica del Sacro Cuore - Fondazione Policlinico Universitario A. Gemelli, IRCCS, Rome 00168, Italy
- Emergency Medicine, Università Cattolica del Sacro Cuore, Roma 00168, Italy
| | - Sara Sofia De Lucia
- CEMAD, Center for Diagnosis and Treatment of Digestive Diseases, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Roma 00168, Italy
| | - Angelo Del Gaudio
- CEMAD, Center for Diagnosis and Treatment of Digestive Diseases, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Roma 00168, Italy
| | - Marcello Fiorani
- CEMAD, Center for Diagnosis and Treatment of Digestive Diseases, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Roma 00168, Italy
| | - Giorgia Polito
- CEMAD, Center for Diagnosis and Treatment of Digestive Diseases, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Roma 00168, Italy
| | - Carlo Romano Settanni
- Digestive Disease Center, Fondazione Policlinico Universitario A. Gemelli IRCCS - Università Cattolica del Sacro Cuore, Rome 00168, Italy
| | - Andrea Piccioni
- Department of Emergency, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Roma 00168, Italy
| | - Francesco Franceschi
- Department of Emergency, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Roma 00168, Italy
- Department of Emergency, Università Cattolica del Sacro Cuore, Roma 00168, Italy
| | - Antonio Gasbarrini
- CEMAD, Center for Diagnosis and Treatment of Digestive Diseases, Fondazione Policlinico Universitario A. Gemelli, IRCCS, Roma 00168, Italy
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11
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Candel FJ, Barreiro P, Salavert M, Cabello A, Fernández-Ruiz M, Pérez-Segura P, San Román J, Berenguer J, Córdoba R, Delgado R, España PP, Gómez-Centurión IA, González Del Castillo JM, Heili SB, Martínez-Peromingo FJ, Menéndez R, Moreno S, Pablos JL, Pasquau J, Piñana JL, On Behalf Of The Modus Investigators Adenda. Expert Consensus: Main Risk Factors for Poor Prognosis in COVID-19 and the Implications for Targeted Measures against SARS-CoV-2. Viruses 2023; 15:1449. [PMID: 37515137 PMCID: PMC10383267 DOI: 10.3390/v15071449] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/30/2023] [Revised: 06/17/2023] [Accepted: 06/23/2023] [Indexed: 07/30/2023] Open
Abstract
The clinical evolution of patients infected with the Severe Acute Respiratory Coronavirus type 2 (SARS-CoV-2) depends on the complex interplay between viral and host factors. The evolution to less aggressive but better-transmitted viral variants, and the presence of immune memory responses in a growing number of vaccinated and/or virus-exposed individuals, has caused the pandemic to slowly wane in virulence. However, there are still patients with risk factors or comorbidities that put them at risk of poor outcomes in the event of having the coronavirus infectious disease 2019 (COVID-19). Among the different treatment options for patients with COVID-19, virus-targeted measures include antiviral drugs or monoclonal antibodies that may be provided in the early days of infection. The present expert consensus is based on a review of all the literature published between 1 July 2021 and 15 February 2022 that was carried out to establish the characteristics of patients, in terms of presence of risk factors or comorbidities, that may make them candidates for receiving any of the virus-targeted measures available in order to prevent a fatal outcome, such as severe disease or death. A total of 119 studies were included from the review of the literature and 159 were from the additional independent review carried out by the panelists a posteriori. Conditions found related to strong recommendation of the use of virus-targeted measures in the first days of COVID-19 were age above 80 years, or above 65 years with another risk factor; antineoplastic chemotherapy or active malignancy; HIV infection with CD4+ cell counts < 200/mm3; and treatment with anti-CD20 immunosuppressive drugs. There is also a strong recommendation against using the studied interventions in HIV-infected patients with a CD4+ nadir <200/mm3 or treatment with other immunosuppressants. Indications of therapies against SARS-CoV-2, regardless of vaccination status or history of infection, may still exist for some populations, even after COVID-19 has been declared to no longer be a global health emergency by the WHO.
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Affiliation(s)
- Francisco Javier Candel
- Clinical Microbiology & Infectious Diseases, Transplant Coordination, Hospital Clínico Universitario San Carlos, 28040 Madrid, Spain
| | - Pablo Barreiro
- Regional Public Health Laboratory, Infectious Diseases, Internal Medicine, Hospital General Universitario La Paz, 28055 Madrid, Spain
- Department of Medical Specialities and Public Health, Universidad Rey Juan Carlos, 28922 Madrid, Spain
| | - Miguel Salavert
- Infectious Diseases, Internal Medicine, Hospital Universitario y Politécnico La Fe, 46026 Valencia, Spain
| | - Alfonso Cabello
- Internal Medicine, Hospital Universitario Fundación Jiménez Díaz, 28040 Madrid, Spain
| | - Mario Fernández-Ruiz
- Unit of Infectious Diseases, Hospital Universitario "12 de Octubre", Instituto de Investigación Sanitaria Hospital "12 de Octubre" (imas12), Centro de Investigación Biomédica en Red de Enfermedades Infecciosas (CIBERINFEC), Instituto de Salud Carlos III (ISCIII), 28041 Madrid, Spain
| | - Pedro Pérez-Segura
- Medical Oncology, Hospital Clínico Universitario San Carlos, 28040 Madrid, Spain
| | - Jesús San Román
- Department of Medical Specialities and Public Health, Universidad Rey Juan Carlos, 28922 Madrid, Spain
| | - Juan Berenguer
- Instituto de Investigación Sanitaria Gregorio Marañón (IiSGM), Centro de Investigación Biomédica en Red de Enfermedades Infecciosas (CIBERINFEC), 28007 Madrid, Spain
| | - Raúl Córdoba
- Haematology and Haemotherapy, Hospital Universitario Fundación Jiménez Díaz, 28040 Madrid, Spain
| | - Rafael Delgado
- Clinical Microbiology, Hospital Universitario "12 de Octubre", Instituto de Investigación Sanitaria Hospital "12 de Octubre" (imas12), 28041 Madrid, Spain
| | - Pedro Pablo España
- Pneumology, Hospital Universitario de Galdakao-Usansolo, 48960 Vizcaya, Spain
| | | | | | - Sarah Béatrice Heili
- Intermediate Respiratory Care Unit, Hospital Universitario Fundación Jiménez Díaz, 28040 Madrid, Spain
| | - Francisco Javier Martínez-Peromingo
- Department of Medical Specialities and Public Health, Universidad Rey Juan Carlos, 28922 Madrid, Spain
- Geriatrics, Hospital Universitario Rey Juan Carlos, 28933 Madrid, Spain
| | - Rosario Menéndez
- Pneumology, Hospital Universitario y Politécnico La Fe, 46026 Valencia, Spain
| | - Santiago Moreno
- Infectious Diseases, Hospital Universitario Ramón y Cajal, 28034 Madrid, Spain
| | - José Luís Pablos
- Rheumatology, Hospital Universitario "12 de Octubre", Instituto de Investigación Sanitaria Hospital "12 de Octubre" (imas12), 28041 Madrid, Spain
| | - Juan Pasquau
- Infectious Diseases, Hospital Universitario Virgen de las Nieves, 18014 Granada, Spain
| | - José Luis Piñana
- Haematology and Haemotherapy, Hospital Clínico Universitario de Valencia, 46010 Valencia, Spain
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12
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Scalzo N, Ungaro RC. Managing IBD in the COVID-19 era. Therap Adv Gastroenterol 2023; 16:17562848231176450. [PMID: 37337593 PMCID: PMC10273097 DOI: 10.1177/17562848231176450] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/30/2023] [Accepted: 05/01/2023] [Indexed: 06/21/2023] Open
Abstract
Over the last 2 years the lives of millions have changed because of the emergence of Coronavirus disease 2019 (COVID-19). Patients living with inflammatory bowel disease (IBD) represent a sizable population with their own sets of challenges to providers in the wake of so much uncertainty. The Centers for Disease Control considers immunocompromised individuals at higher risk of infection and complications from COVID-19. Early in the pandemic, the specific risks for IBD patients were unclear as guidance was based on expert opinion regarding the management of IBD during a COVID-19 era. Fortunately, after considerable work in the field, the overwhelming evidence suggests that IBD patients as a whole do not appear to be at increased risk for more severe disease from COVID-19. Certain risk factors such as age, steroids, comorbidities, combination immunomodulatory therapy, and IBD disease activity have been associated with worse outcomes. Most IBD medications are low risk, with the exception of immunomodulator monotherapy and combination therapy with thiopurine and anti-TNF. Vaccination remains safe and effective for all IBD patients, although additional booster doses may be necessary, particularly in patients taking anti-TNF agents.
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Affiliation(s)
- Nicholas Scalzo
- Department of Medicine, Icahn School of Medicine at Mount Sinai, One Gustave L Levy Place, Department of Medicine Box 1118, New York, NY 10029-6574, USA
| | - Ryan C. Ungaro
- The Dr. Henry D. Janowitz Division of Gastroenterology, Icahn School of Medicine at Mount Sinai, New York, NY, USA
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13
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Kwon HJ, Panagos K, Alizadeh M, Bell M, Bourmaf M, Zisman E, Paul P, Sibel L, Wong U. Patients with inflammatory bowel disease are more hesitant about Coronavirus disease 2019 vaccination. Front Med (Lausanne) 2022; 9:1005121. [PMID: 36457565 PMCID: PMC9707735 DOI: 10.3389/fmed.2022.1005121] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/27/2022] [Accepted: 10/12/2022] [Indexed: 11/16/2022] Open
Abstract
Despite the impact of the Coronavirus Disease 2019 (COVID-19) pandemic, vaccine hesitancy remains common in the general public and patients with Inflammatory Bowel Diseases (IBD). We sought to examine the reasons for vaccine hesitancy in patients with IBD. In this case-control study, we performed a retrospective chart review of 1,349 IBD patients and 215 non-IBD patients seen at University of Maryland Medical Center, a tertiary referral medical center, between March 2020 and October 2021. Data obtained included demographics, vaccination records, disease history, number of IBD-related surgeries, and IBD medications. 813/1,349 (60.3%) IBD patients received at least one dose of either the Pfizer/BioNTech, Moderna, or Johnson & Johnson vaccines. In a multivariate logistic regression, COVID vaccination was found to be positively associated with older age (p-value = 1.65e-5), female sex (p = 0.00194), Asian and White races (p = 0.02330, 0.00169), number of clinic visits (p = 1.11e-08), and biologic use (p = 7.82e-5). There was no association between vaccination and other types of vaccination nor with the use of other IBD medications. There was a negative association between vaccination status and the total number of IBD related surgeries (p = 0.02857). In non-IBD patients, only the number of clinic visits was positively associated with COVID-19 vaccination. Although the majority of IBD patients are immunosuppressed, COVID-19 vaccination rate was only 60.3%. Younger adults, males, African Americans, and those requiring IBD-related surgeries were less likely to receive COVID-19 vaccine. Healthcare providers need to recognize these potential risk factors for COVID-19 vaccine hesitancy.
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Affiliation(s)
- Hyuk Joon Kwon
- Department of Internal Medicine, University of Maryland Medical Center, Baltimore, MD, United States
| | - Katherine Panagos
- Department of Internal Medicine, University of Maryland Medical Center, Baltimore, MD, United States,*Correspondence: Katherine Panagos
| | - Madeline Alizadeh
- Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, MD, United States
| | - Mack Bell
- Department of Internal Medicine, University of Maryland Medical Center, Baltimore, MD, United States
| | - Mohammad Bourmaf
- Department of Internal Medicine, University of Maryland Medical Center, Baltimore, MD, United States
| | - Erin Zisman
- Department of Internal Medicine, University of Maryland Medical Center, Baltimore, MD, United States
| | - Pinkle Paul
- Department of Internal Medicine, University of Maryland Medical Center, Baltimore, MD, United States
| | - Lauren Sibel
- Department of Internal Medicine, University of Maryland Medical Center, Baltimore, MD, United States
| | - Uni Wong
- Department of Gastroenterology and Hepatology, University of Maryland School of Medicine, Baltimore, MD, United States,Department of Gastroenterology and Hepatology, Veterans Affairs Maryland Health Care System, Baltimore, MD, United States
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14
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Chen L, Hu K, Cheng C, Hu Q, Zhang L, An T, Guo Y, Chen S, Duan G. Risk of adverse outcomes in inflammatory bowel disease patients infected with SARS-CoV-2: a systematic review and meta-analysis. Int J Colorectal Dis 2022; 37:2277-2289. [PMID: 36271206 PMCID: PMC9589854 DOI: 10.1007/s00384-022-04265-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Accepted: 10/06/2022] [Indexed: 02/04/2023]
Abstract
BACKGROUND Between people with and without inflammatory bowel disease (IBD), there was no statistically significant difference in the probability of contracting the severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). However, the risk of adverse outcomes in IBD patients after virus infection remains unclear. METHODS Eligible studies conducted from January 1, 2020 to March 17, 2022 were obtained by searching PubMed, Embase, and Web of Science. Information was collected in tables from the included studies. Random-effects and fixed-effects models were used as measures for the pooled estimates. All data were estimated by R version 4.1.3. RESULTS Twenty-four studies were included. The risk ratio (RR) of adverse outcomes in COVID-19 patients with IBD increased by 32% (RR 1.32; 95% CI 1.06-1.66) relative to COVID-19 patients without IBD. The RR of mortality was higher in COVID-19 patients with IBD from Europe (RR 1.72; 95% CI 1.11-2.67) than in those that were not from Europe (RR 1.00; 95% CI 0.79-1.26; χ2 = 4.67; P = 0.03). Patients with ulcerative colitis were at higher risk of adverse outcomes after SARS-CoV-2 infection than patients with Crohn's disease patients (RR1.38; 95% CI 1.27-1.50). The IBD drugs treatment was associated with the risk of adverse outcomes, the pooled odds ratio (OR) of mesalazine (1.79; 95% CI 1.59-2.02), immunomodulators (1.30; 95% CI 1.10-1.53), and anti-TNF (0.47; 95% CI 0.41-0.53) were assessed. CONCLUSION COVID-19 patients with IBD had an increased risk of adverse outcomes than those without IBD, whereas anti-TNF treatment might reduce the risk.
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Affiliation(s)
- Long Chen
- Department of Epidemiology, College of Public Health, Zhengzhou University, Zhengzhou, 450001, China
| | - Kai Hu
- Henan Academy of Medical Sciences, Zhengzhou, Henan, 450046, China
| | - Cheng Cheng
- Department of Epidemiology, College of Public Health, Zhengzhou University, Zhengzhou, 450001, China
| | - Quanman Hu
- Department of Epidemiology, College of Public Health, Zhengzhou University, Zhengzhou, 450001, China
| | - Liang Zhang
- Department of Epidemiology, College of Public Health, Zhengzhou University, Zhengzhou, 450001, China
| | - Tongyan An
- Department of Epidemiology, College of Public Health, Zhengzhou University, Zhengzhou, 450001, China
| | - Yongjun Guo
- Henan Academy of Medical Sciences, Zhengzhou, Henan, 450046, China
| | - Shuaiyin Chen
- Department of Epidemiology, College of Public Health, Zhengzhou University, Zhengzhou, 450001, China.
| | - Guangcai Duan
- Department of Epidemiology, College of Public Health, Zhengzhou University, Zhengzhou, 450001, China
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15
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Bezzio C, Fiorino G, Ribaldone DG, Armuzzi A, Saibeni S, IG-IBD COVID-19 Study Group
VerneroMartaFurfaroFedericaPuglieseDanielaManesGianpieroPastorelliLucaGerardiVivianaViganòChiaraVariolaAngelaCaprioliFabioZingoneFabianaScucchiLudovicaArdizzoneSandroBaroniStefaniaRicciChiaraOnaliSaraBalestrieriPaolaRoselliJennyBodiniGiorgiaDapernoMarcoLentiMarcoBaldoniMoniaCarparelliSoniaCasiniValentinaFeliceCarlaCortelezziClaudioAmatoArnaldoMazzuoliSilviaCoppiniFrancescaSartiniAlessandroSorianoAlessandraViscidoAngeloBudaAndreaGrossiLaurinoAlloccaMariangelaPriviteraGiuseppeArmandiAngelo. IBD Flare in the COVID-19 Pandemic: Therapy Discontinuation Is to Blame. Inflamm Bowel Dis 2022; 29:834-836. [PMID: 35972338 PMCID: PMC9384797 DOI: 10.1093/ibd/izac173] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/01/2022] [Indexed: 01/28/2023]
Abstract
Lay Summary
This prospective case-control study investigated the impact of severe acute respiratory syndrome coronavirus 2 infection on inflammatory bowel disease course and looked for risk factors associated with flares. In the severe acute respiratory syndrome coronavirus 2 pandemic era, inflammatory bowel disease course is not influenced by infection, while therapy discontinuation is a risk factor for disease flare.
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Affiliation(s)
- Cristina Bezzio
- Address correspondence to: Cristina Bezzio, MD, PhD, Gastroenterology Unit, Rho Hospital, ASST Rhodense, Corso Europa 250, 20017 Rho, Milan, Italy ()
| | - Gionata Fiorino
- Gastroenterology and Endoscopy, IRCCS Ospedale San Raffaele, University Vita-Salute San Raffaele, Milan, Italy
| | - Davide G Ribaldone
- Division of Gastroenterology, Department of Medical Sciences, Università di Torino, Turin, Italy
| | - Alessandro Armuzzi
- IBD Unit, IRCCS Humanitas Research Hospital, Rozzano, Italy,Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Italy
| | - Simone Saibeni
- Gastroenterology Unit, Rho Hospital, ASST Rhodense, Rho, Italy
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16
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Lin S, Lau LH, Chanchlani N, Kennedy NA, Ng SC. Recent advances in clinical practice: management of inflammatory bowel disease during the COVID-19 pandemic. Gut 2022; 71:1426-1439. [PMID: 35477864 PMCID: PMC9185820 DOI: 10.1136/gutjnl-2021-326784] [Citation(s) in RCA: 23] [Impact Index Per Article: 7.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/27/2022] [Accepted: 04/14/2022] [Indexed: 01/28/2023]
Abstract
The COVID-19 pandemic has raised considerable concerns that patients with inflammatory bowel disease (IBD), particularly those treated with immunosuppressive therapies, may have an increased risk of SARS-CoV-2 acquisition, develop worse outcomes following COVID-19, and have suboptimal vaccine response compared with the general population. In this review, we summarise data on the risk of COVID-19 and associated outcomes, and latest guidance on SARS-CoV-2 vaccines in patients with IBD. Emerging evidence suggests that commonly used medications for IBD, such as corticosteroids but not biologicals, were associated with adverse outcomes to COVID-19. There has been no increased risk of de novo, or delayed, IBD diagnoses, however, an overall decrease in endoscopy procedures has led to a rise in the number of missed endoscopic-detected cancers during the pandemic. The impact of IBD medication on vaccine response has been a research priority recently. Data suggest that patients with IBD treated with antitumour necrosis factor (TNF) medications had attenuated humoral responses to SARS-CoV-2 vaccines, and more rapid antibody decay, compared with non-anti-TNF-treated patients. Reassuringly, rates of breakthrough infections and hospitalisations in all patients who received vaccines, irrespective of IBD treatment, remained low. International guidelines recommend that all patients with IBD treated with immunosuppressive therapies should receive, at any point during their treatment cycle, three primary doses of SARS-CoV-2 vaccines with a further booster dose as soon as possible. Future research should focus on our understanding of the rate of antibody decay in biological-treated patients, which patients require additional doses of SARS-CoV-2 vaccine, the long-term risks of COVID-19 on IBD disease course and activity, and the potential risk of long COVID-19 in patients with IBD.
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Affiliation(s)
- Simeng Lin
- Department of Gastroenterology, Royal Devon and Exeter NHS Foundation Trust, Exeter, UK
- Exeter Inflammatory Bowel Disease and Pharmacogenetics Research Group, University of Exeter, Exeter, UK
| | - Louis Hs Lau
- Department of Medicine and Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China
| | - Neil Chanchlani
- Department of Gastroenterology, Royal Devon and Exeter NHS Foundation Trust, Exeter, UK
- Exeter Inflammatory Bowel Disease and Pharmacogenetics Research Group, University of Exeter, Exeter, UK
| | - Nicholas A Kennedy
- Department of Gastroenterology, Royal Devon and Exeter NHS Foundation Trust, Exeter, UK
- Exeter Inflammatory Bowel Disease and Pharmacogenetics Research Group, University of Exeter, Exeter, UK
| | - Siew C Ng
- Department of Medicine and Therapeutics, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong SAR, China
- Microbiota I-Center (MagIC), Hong Kong, Hong Kong SAR, China
- State Key Laboratory of Digestive Disease, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Hong Kong, Hong Kong SAR, China
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17
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Esposito S, Caminiti C, Giordano R, Argentiero A, Ramundo G, Principi N. Risks of SARS-CoV-2 Infection and Immune Response to COVID-19 Vaccines in Patients With Inflammatory Bowel Disease: Current Evidence. Front Immunol 2022; 13:933774. [PMID: 35812420 PMCID: PMC9260046 DOI: 10.3389/fimmu.2022.933774] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/01/2022] [Accepted: 05/26/2022] [Indexed: 02/05/2023] Open
Abstract
Inflammatory bowel diseases (IBD), including Crohn's disease, ulcerative colitis, and unclassified inflammatory bowel disease, are a group of chronic, immune mediated conditions that are presumed to occur in genetically susceptible individuals because of a dysregulated intestinal immune response to environmental factors. IBD patients can be considered subjects with an aberrant immune response that makes them at increased risk of infections, particularly those due to opportunistic pathogens. In many cases this risk is significantly increased by the therapy they receive. Aim of this narrative review is to describe the impact of SARS-CoV-2 infection and the immunogenicity of COVID-19 vaccines in patients with IBD. Available data indicate that patients with IBD do not have an increased susceptibility to infection with SARS-CoV-2 and that, if infected, in the majority of the cases they must not modify the therapy in place because this does not negatively affect the COVID-19 course. Only corticosteroids should be reduced or suspended due to the risk of causing severe forms. Furthermore, COVID-19 seems to modify the course of IBD mainly due to the impact on intestinal disease of the psychological factors deriving from the measures implemented to deal with the pandemic. The data relating to the immune response induced by SARS-CoV-2 or by COVID-19 vaccines can be considered much less definitive. It seems certain that the immune response to disease and vaccines is not substantially different from that seen in healthy subjects, with the exception of patients treated with anti-tumor necrosis factor alone or in combination with other immunosuppressants who showed a reduced immune response. How much, however, this problem reduces induced protection is not known. Moreover, the impact of SARS-CoV-2 variants on IBD course and immune response to SARS-CoV-2 infection and COVID-19 vaccines has not been studied and deserves attention. Further studies capable of facing and solving unanswered questions are needed in order to adequately protect IBD patients from the risks associated with SARS-CoV-2 infection.
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Affiliation(s)
- Susanna Esposito
- Pediatric Clinic, Department of Medicine and Surgery, University of Parma, Parma, Italy
| | - Caterina Caminiti
- Research and Innovation Unit, University Hospital of Parma, Parma, Italy
| | | | - Alberto Argentiero
- Pediatric Clinic, Department of Medicine and Surgery, University of Parma, Parma, Italy
| | - Greta Ramundo
- Pediatric Clinic, Department of Medicine and Surgery, University of Parma, Parma, Italy
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18
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Impact of SARS-CoV-2 Infection on the Course of Inflammatory Bowel Disease in Patients Treated with Biological Therapeutic Agents: A Case-Control Study. Biomedicines 2022; 10:biomedicines10040843. [PMID: 35453593 PMCID: PMC9029341 DOI: 10.3390/biomedicines10040843] [Citation(s) in RCA: 6] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/03/2022] [Revised: 03/30/2022] [Accepted: 03/31/2022] [Indexed: 01/27/2023] Open
Abstract
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection has raised concerns in patients with inflammatory bowel disease (IBD), not only due to consequences of coronavirus disease 2019 itself but also as a possible cause of IBD relapse. The main objective of this study was to assess the role of SARS-CoV-2 in IBD clinical recurrence in a cohort of patients undergoing biological therapy. Second, we evaluated the difference in C-reactive protein (CRP) levels between the start and end of the follow-up period (ΔCRP) and the rate of biological therapy discontinuation. Patients with IBD positive for SARS-CoV-2 infection were compared with non-infected patients. IBD recurrence was defined as the need for intensification of current therapy. We enrolled 95 IBD patients with SARS-CoV-2 infection and 190 non-infected patients. During follow-up, 11 of 95 (11.6%) SARS-CoV-2-infected patients experienced disease recurrence compared to 21 of 190 (11.3%) in the control group (p = 0.894). Forty-six (48.4%) SARS-CoV-2-infected patients discontinued biological therapy versus seven (3.7%) in the control group (p < 0.01). In the multivariate analysis, biological agent discontinuation (p = 0.033) and ΔCRP (p = 0.017), but not SARS-CoV-2 infection (p = 0.298), were associated with IBD recurrence. SARS-CoV-2 infection was not associated with increased IBD recurrence rates in this cohort of patients treated with biological agents.
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19
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Zabana Y, Marín-Jiménez I, Rodríguez-Lago I, Vera I, Martín-Arranz MD, Guerra I, Gisbert JP, Mesonero F, Benítez O, Taxonera C, Ponferrada-Díaz Á, Piqueras M, Lucendo AJ, Caballol B, Mañosa M, Martínez-Montiel P, Bosca-Watts M, Gordillo J, Bujanda L, Manceñido N, Martínez-Pérez T, López A, Rodríguez-Gutiérrez C, García-López S, Vega P, Rivero M, Melcarne L, Calvo M, Iborra M, Barreiro de-Acosta M, Sicilia B, Barrio J, Pérez JL, Busquets D, Pérez-Martínez I, Navarro-Llavat M, Hernández V, Argüelles-Arias F, Ramírez Esteso F, Meijide S, Ramos L, Gomollón F, Muñoz F, Suris G, de Zarate JO, Huguet JM, Llaó J, García-Sepulcre MF, Sierra M, Durà M, Estrecha S, Fuentes Coronel A, Hinojosa E, Olivan L, Iglesias E, Gutiérrez A, Varela P, Rull N, Gilabert P, Hernández-Camba A, Brotons A, Ginard D, Sesé E, Carpio D, Aceituno M, Cabriada JL, González-Lama Y, Jiménez L, Chaparro M, López-San Román A, Alba C, Plaza-Santos R, Mena R, Tamarit-Sebastián S, Ricart E, Calafat M, Olivares S, Navarro P, Bertoletti F, Alonso-Galán H, Pajares R, Olcina P, Manzano P, Domènech E, Esteve M, on behalf of the ENEIDA registry of GETECCU. Nationwide COVID-19-EII Study: Incidence, Environmental Risk Factors and Long-Term Follow-Up of Patients with Inflammatory Bowel Disease and COVID-19 of the ENEIDA Registry. J Clin Med 2022; 11:421. [PMID: 35054116 PMCID: PMC8781643 DOI: 10.3390/jcm11020421] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/09/2021] [Revised: 12/23/2021] [Accepted: 01/06/2022] [Indexed: 02/04/2023] Open
Abstract
We aim to describe the incidence and source of contagion of COVID-19 in patients with IBD, as well as the risk factors for a severe course and long-term sequelae. This is a prospective observational study of IBD and COVID-19 included in the ENEIDA registry (53,682 from 73 centres) between March-July 2020 followed-up for 12 months. Results were compared with data of the general population (National Centre of Epidemiology and Catalonia). A total of 482 patients with COVID-19 were identified. Twenty-eight percent were infected in the work environment, and 48% were infected by intrafamilial transmission, despite having good adherence to lockdown. Thirty-five percent required hospitalization, 7.9% had severe COVID-19 and 3.7% died. Similar data were reported in the general population (hospitalisation 19.5%, ICU 2.1% and mortality 4.6%). Factors related to death and severe COVID-19 were being aged ≥ 60 years (OR 7.1, 95% CI: 1.8-27 and 4.5, 95% CI: 1.3-15.9), while having ≥2 comorbidities increased mortality (OR 3.9, 95% CI: 1.3-11.6). None of the drugs for IBD were related to severe COVID-19. Immunosuppression was definitively stopped in 1% of patients at 12 months. The prognosis of COVID-19 in IBD, even in immunosuppressed patients, is similar to that in the general population. Thus, there is no need for more strict protection measures in IBD.
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Affiliation(s)
- Yamile Zabana
- Hospital Universitari Mútua Terrassa, 08221 Terrassa, Spain; (O.B.); (M.A.); (P.M.); (M.E.)
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
| | | | - Iago Rodríguez-Lago
- Gastroenterology Department, Hospital Universitario de Galdakao, 48960 Galdakao, Spain; (I.R.-L.); (J.L.C.)
- Biocruces Bizkaia Health Research Institute, 48960 Galdakao, Spain
| | - Isabel Vera
- Hospital Universitario Puerta de Hierro, 28222 Majadahonda, Spain; (I.V.); (Y.G.-L.)
| | | | - Iván Guerra
- Hospital Universitario de Fuenlabrada, 28942 Fuenlabrada, Spain; (I.G.); (L.J.)
- Instituto de Investigación Hospital Universitario La Paz (IdiPaz), 28046 Madrid, Spain
| | - Javier P. Gisbert
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Department of Gastroenterology, Hospital Universitario de La Princesa, Universidad Autónoma de Madrid (UAM), 28049 Madrid, Spain
- Instituto de Investigación Sanitaria Princesa (IIS-IP), 28006 Madrid, Spain
| | - Francisco Mesonero
- Hospital Universitario Ramón y Cajal, 28034 Madrid, Spain; (F.M.); (A.L.-S.R.)
| | - Olga Benítez
- Hospital Universitari Mútua Terrassa, 08221 Terrassa, Spain; (O.B.); (M.A.); (P.M.); (M.E.)
| | - Carlos Taxonera
- Hospital Clínico San Carlos, 28040 Madrid, Spain; (C.T.); (C.A.)
- Instituto de Investigación del Hospital Clínico San Carlos [IdISSC], 28040 Madrid, Spain
| | | | - Marta Piqueras
- Consorci Sanitari de Terrassa, 08227 Terrassa, Spain; (M.P.); (R.M.)
| | - Alfredo J. Lucendo
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Instituto de Investigación Sanitaria Princesa (IIS-IP), 28006 Madrid, Spain
- Hospital General de Tomelloso, 13700 Tomelloso, Spain;
| | - Berta Caballol
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital Clínic de Barcelona-IDIBAPS, 08036 Barcelona, Spain
| | - Míriam Mañosa
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital Universitari Germans Trias i Pujol, 08916 Badalona, Spain
| | - Pilar Martínez-Montiel
- Fundación Hospital Universitario Doce de Octubre, 28041 Madrid, Spain; (P.M.-M.); (S.O.)
| | - Maia Bosca-Watts
- Hospital Clinic Universitari de Valencia, 46010 Valencia, Spain; (M.B.-W.); (P.N.)
| | - Jordi Gordillo
- Hospital de la Santa Creu i Sant Pau, 08041 Barcelona, Spain; (J.G.); (F.B.)
| | - Luis Bujanda
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital Universitario Donostia, Instituto Biodonostia, 20014 San Sebastián, Spain;
- Universidad del País Vasco (UPV/EHU), 48940 Leioua, Spain
| | - Noemí Manceñido
- Hospital Universitario Infanta Sofía, 28703 San Sebastián de los Reyes, Spain; (N.M.); (R.P.)
| | | | - Alicia López
- Institut Hospital del Mar d’Investigacions Mèdiques (IMIM), Hospital del Mar, 08003 Barcelona, Spain;
| | | | | | - Pablo Vega
- Complexo Hospitalario Universitario de Ourense, 32005 Ourense, Spain;
| | - Montserrat Rivero
- Instituto de Investigación Sanitaria Valdecilla (IDIVAL), Hospital Universitario Marqués de Valdecilla, 39008 Santander, Spain;
| | - Luigi Melcarne
- Hospital Universitari Parc Taulí, 08208 Sabadell, Spain;
| | - Maria Calvo
- Hospital San Pedro-Logroño, 26006 Logroño, Spain;
| | - Marisa Iborra
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital Universitario y Politécnico de la Fe de Valencia, 46026 Valencia, Spain
| | | | | | - Jesús Barrio
- Hospital Universitario Río Hortega (HURH), 47012 Valladolid, Spain;
| | - José Lázaro Pérez
- Hospital Universitario Fundación de Alcorcón, 28922 Alcorcón, Spain;
| | - David Busquets
- Hospital Universitari de Girona Doctor Josep Trueta, 17007 Girona, Spain;
| | - Isabel Pérez-Martínez
- Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Hospital Universitario Central de Asturias, 33011 Oviedo, Spain;
| | | | | | | | | | - Susana Meijide
- Hospital Universitario de Cruces, 48903 Barakaldo, Spain;
| | - Laura Ramos
- Hospital Universitario de Canarias, 38320 San Cristobal de la Laguna, Spain;
| | - Fernando Gomollón
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital Clínico Universitario “Lozano Blesa” and IIS Aragón, 50009 Zaragoza, Spain
| | - Fernando Muñoz
- Hospital Universitario de Salamanca, 37007 Salamanca, Spain;
| | - Gerard Suris
- Hospital Universitari de Bellvitge, 08907 L’Hospitalet de Llobregat, Spain;
| | | | - José María Huguet
- Consorcio Hospital General Universitario de Valencia, 46014 Valencia, Spain;
| | - Jordina Llaó
- Althaia Xarxa Assistencial Universitària de Manresa, 08243 Manresa, Spain;
| | | | - Mónica Sierra
- Complejo Asistencial Universitario de León, 24071 León, Spain;
| | - Miguel Durà
- Hospital Clínico de Valladolid, 47003 Valladolid, Spain;
| | | | | | | | | | - Eva Iglesias
- Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Hospital Universitario Reina Sofía de Córdoba, 14004 Cordoba, Spain;
| | - Ana Gutiérrez
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital General Universitario de Alicante, 03010 Alicante, Spain
| | - Pilar Varela
- Hospital Universitario de Cabueñes, 33394 Gijón, Spain;
| | - Núria Rull
- Hospital Universitario Son Llàtzer, 07198 Palma, Spain;
| | - Pau Gilabert
- Hospital de Viladecans, 08840 Viladecans, Spain;
| | | | | | - Daniel Ginard
- Hospital Universitario Son Espases, 07120 Palma, Spain;
| | - Eva Sesé
- Hospital Universitari Arnau de Vilanova de Lleida, 25198 Lleida, Spain;
| | - Daniel Carpio
- Complexo Hospitalario de Pontevedra, 36071 Pontevedra, Spain;
| | - Montserrat Aceituno
- Hospital Universitari Mútua Terrassa, 08221 Terrassa, Spain; (O.B.); (M.A.); (P.M.); (M.E.)
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
| | - José Luis Cabriada
- Gastroenterology Department, Hospital Universitario de Galdakao, 48960 Galdakao, Spain; (I.R.-L.); (J.L.C.)
- Biocruces Bizkaia Health Research Institute, 48960 Galdakao, Spain
| | - Yago González-Lama
- Hospital Universitario Puerta de Hierro, 28222 Majadahonda, Spain; (I.V.); (Y.G.-L.)
| | - Laura Jiménez
- Hospital Universitario de Fuenlabrada, 28942 Fuenlabrada, Spain; (I.G.); (L.J.)
- Instituto de Investigación Hospital Universitario La Paz (IdiPaz), 28046 Madrid, Spain
| | - María Chaparro
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Department of Gastroenterology, Hospital Universitario de La Princesa, Universidad Autónoma de Madrid (UAM), 28049 Madrid, Spain
- Instituto de Investigación Sanitaria Princesa (IIS-IP), 28006 Madrid, Spain
| | | | - Cristina Alba
- Hospital Clínico San Carlos, 28040 Madrid, Spain; (C.T.); (C.A.)
- Instituto de Investigación del Hospital Clínico San Carlos [IdISSC], 28040 Madrid, Spain
| | - Rocío Plaza-Santos
- Hospital Universitario Infanta Leonor, 28031 Madrid, Spain; (Á.P.-D.); (R.P.-S.)
| | - Raquel Mena
- Consorci Sanitari de Terrassa, 08227 Terrassa, Spain; (M.P.); (R.M.)
| | | | - Elena Ricart
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital Clínic de Barcelona-IDIBAPS, 08036 Barcelona, Spain
| | - Margalida Calafat
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital Universitari Germans Trias i Pujol, 08916 Badalona, Spain
| | - Sonsoles Olivares
- Fundación Hospital Universitario Doce de Octubre, 28041 Madrid, Spain; (P.M.-M.); (S.O.)
| | - Pablo Navarro
- Hospital Clinic Universitari de Valencia, 46010 Valencia, Spain; (M.B.-W.); (P.N.)
| | - Federico Bertoletti
- Hospital de la Santa Creu i Sant Pau, 08041 Barcelona, Spain; (J.G.); (F.B.)
| | - Horacio Alonso-Galán
- Hospital Universitario Donostia, Instituto Biodonostia, 20014 San Sebastián, Spain;
- Universidad del País Vasco (UPV/EHU), 48940 Leioua, Spain
| | - Ramón Pajares
- Hospital Universitario Infanta Sofía, 28703 San Sebastián de los Reyes, Spain; (N.M.); (R.P.)
| | - Pablo Olcina
- Hospital Virgen de la Luz, 16002 Cuenca, Spain; (T.M.-P.); (P.O.)
| | - Pamela Manzano
- Hospital Universitari Mútua Terrassa, 08221 Terrassa, Spain; (O.B.); (M.A.); (P.M.); (M.E.)
| | - Eugeni Domènech
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
- Hospital Universitari Germans Trias i Pujol, 08916 Badalona, Spain
| | - Maria Esteve
- Hospital Universitari Mútua Terrassa, 08221 Terrassa, Spain; (O.B.); (M.A.); (P.M.); (M.E.)
- Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBEREHD), 28029 Madrid, Spain; (J.P.G.); (A.J.L.); (B.C.); (M.M.); (L.B.); (M.I.); (F.G.); (A.G.); (M.C.); (E.R.); (M.C.); (E.D.)
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Dai C, Dong ZY, Wang YN, Huang YH, Jiang M. Impact of SARS-CoV-2 vaccination in inflammatory bowel disease patients with different biological agents: a systematic review and meta-analysis. REVISTA ESPAÑOLA DE ENFERMEDADES DIGESTIVAS 2022; 114. [DOI: 10.17235/reed.2022.9264/2022] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/10/2022]
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