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Original article
Serological response to vaccines against SARS-CoV-2 in patients with inflammatory bowel disease
Respuesta serológica a las vacunas frente a SARS-CoV-2 en pacientes con enfermedad inflamatoria intestinal
Alicia Algabaa,
Corresponding author
alicia_algaba@hotmail.com

Corresponding author.
, Sara Romeroa, Alicia Granjaa, Daniel Garzaa, Mar Allera, Sara Barreroa, Iván Guerraa, Marina Gila, Nazaret Pizarroa, Paloma Ruiza, Santiago Prietob, Belén Hernándezc, Aranzazu Pouc, Fernando Bermejoa
a Servicio de Digestivo, Hospital Universitario de Fuenlabrada, Madrid, Spain
b Servicio de Laboratorio, Hospital Universitario de Fuenlabrada, Madrid, Spain
c Servicio de Farmacia, Hospital Universitario de Fuenlabrada, Madrid, Spain
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detecting that 10&#46;2&#37; of the patients had had SARS-CoV-2 infection in the first wave&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> We also recently reported on how the incidence of COVID-19 had evolved in our patients in the 2nd and 3rd waves&#46;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> In a joint communication with the patients&#8217; Asociaciones de Crohn y Colitis Ulcerosa &#40;ACCU&#41; &#91;Crohn&#8217;s and Ulcerative Colitis Associations&#41; and the Grupo Enfermero de Trabajo en Enfermedad Inflamatoria Intestinal &#40;GETEII&#41; &#91;Nursing Working Group on Inflammatory Bowel Disease&#93;&#41;&#44; the Grupo Espa&#241;ol de Trabajo en Enfermedad de Crohn y Colitis Ulcerosa &#40;GETECCU&#41; &#91;Spanish Working Group on Crohn&#8217;s Disease and Ulcerative Colitis&#93; explains that the vaccine is safe in patients with IBD&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> There is no evidence to suggest an increased risk in other immune-based diseases or patients on steroid&#44; immunosuppressive or biological treatment&#46; GETECCU&#44; GETEII and ACCU recommend vaccinating all patients with IBD against SARS-CoV-2&#44; regardless of their IBD treatment&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">In general&#44; most of Spain&#8217;s autonomous regions did not establish any preference or priority when vaccinating patients with IBD and in many cases&#44; Madrid Region included&#44; they were vaccinated by age groups along with the rest of the population&#46; As with other vaccines&#44; such as hepatitis B&#44;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> immunosuppressive or biological treatment could potentially decrease the efficacy of the vaccines for COVID-19 infection&#46; In addition&#44; the vaccines may have less efficacy in these patients than reported in the general population in the pivotal studies already published&#46;<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5&#8211;8&#44;10</span></a> For all the above reasons&#44; it is appropriate to perform post-vaccination serology in the clinical scenario of a patient with IBD&#44; as we routinely do in hepatitis B immunisation&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">The efficacy of the SARS-CoV-2 vaccines may be lower in patients with IBD&#46; Our aim was to study the serological response &#40;SR&#41; and the tolerability of the COVID-19 vaccine in patients with IBD and the relationship of these aspects with the IBD treatment and type of vaccine&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Methods</span><p id="par0025" class="elsevierStylePara elsevierViewall">Observational&#44; single-centre&#44; cross-sectional study in patients with IBD followed up at the Hospital de Fuenlabrada Unit in Madrid&#44; Spain&#46; We included patients over 18 years of age with IBD&#44; vaccinated with any type of vaccine for COVID-19 with the regimen administered and having had the second dose &#40;except patients vaccinated with Ad26&#46;COV2-S&#174; &#91;Janssen Pharmaceutica&#44; JANSSEN CILAG SA&#44; Johnson &#38; Johnson subsidiary&#93; who had only received a single dose&#41; of the vaccine three months&#8239;&#177;&#8239;one month prior to inclusion&#46; Patients with known COVID-19 infection prior to vaccination &#40;confirmed by PCR&#44; antigen test or serology&#41; or with diseases other than IBD causing immunosuppression &#40;for example human immunodeficiency virus or agammaglobulinaemia&#41; were excluded&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">The SR to the vaccine was analysed by determining specific IgG antibodies against the receptor-binding domain &#40;RBD&#41; of the virus spike protein subunit S1&#46; Chemiluminescence technique &#40;DxI-Beckman Coulter analyser&#41; for measurement of specific IgG antibodies against the RBD of the virus spike protein subunit S1 and standardised against the 1st ISNIBSC 20&#47;136&#46; These antibodies appear post-vaccination for SARS CoV-2 or post-COVID-19 infection&#46; Therefore&#44; any positive response in the absence of proven infection was considered a positive vaccine response&#46; In this study&#44; any value higher than 30&#8239;IU&#47;mL was considered as a positive vaccine response &#40;manufacturer&#8217;s data&#58; Beckman Coulter&#44; Inc&#46;&#41;&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">IBD activity was measured by clinical &#40;Harvey-Bradshaw for Crohn&#8217;s disease and Mayo partial score for ulcerative colitis&#41; and biological &#40;C-reactive protein or faecal calprotectin&#41; indices&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">Tolerability was studied using specific questionnaires to determine the occurrence of any adverse effects &#40;AE&#41; related to the vaccine&#46; Other clinical data were reviewed by telephone interview and review of the medical records&#46; An AE was considered serious if it led to the hospital admission or death of the patient&#46;</p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Statistical analysis</span><p id="par0045" class="elsevierStylePara elsevierViewall">Calculations were made to determine the sample size for the study&#46; Considering the number of patients seen in the IBD clinic &#40;around 800&#41; and estimating that 20&#37; of patients would not be candidates for inclusion&#44; mainly because they had previously had COVID-19 infection&#44; plus allowing a 5&#37; margin of error and a 95&#37; confidence interval &#40;CI&#41;&#44; we calculated that the overall sample size should be 230 patients&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">For the statistical analysis&#44; we carried out a descriptive analysis with the qualitative variables being represented by percentages and 95&#37; CI&#46; The Kolmogorov-Smirnov test was performed to assess the normality of continuous variables&#46; Quantitative variables were expressed as mean and standard deviation or median and interquartile range if the variable did not follow a normal distribution&#46; In the bivariate study&#44; categorical variables were compared using the chi-square test &#40;&#967;<span class="elsevierStyleSup">2</span>&#41; and comparisons between quantitative and qualitative variables were made using Student&#8217;s <span class="elsevierStyleItalic">t</span>-test or the Mann-Whitney <span class="elsevierStyleItalic">U</span> test if the variables did not follow a normal distribution&#46; The percentage of efficacy of the vaccine was calculated stratifying by type of drug and by type of vaccine&#46;</p><p id="par0055" class="elsevierStylePara elsevierViewall">Multivariate analysis was performed to identify potential risk factors for decreased vaccine efficacy using a logistic regression model&#46; The IBM&#174; SPSS&#174; Statistics program was used to carry out the analysis&#46;</p></span></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Results</span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Baseline characteristics of the patients included</span><p id="par0060" class="elsevierStylePara elsevierViewall">We included 280 patients with IBD&#46; The baseline characteristics of these 280 patients are shown in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46; When they were vaccinated&#44; 24&#46;6&#37; had IBD activity&#46; The IBD treatments patients were receiving at the time of inclusion were as follows&#58; 1&#41; anti-TNF biological agents&#58; 26&#46;4&#37; &#40;N&#8239;&#61;&#8239;74&#41;&#59; 2&#41; non-anti-TNF biological agents&#58; 11&#46;8&#37; &#40;N&#8239;&#61;&#8239;33&#41;&#59; 3&#41; immunosupressors 37&#46;1&#37; &#40;N&#8239;&#61;&#8239;104&#41;&#59; and 4&#41; aminosalicylates 21&#46;1&#37; &#40;N&#8239;&#61;&#8239;59&#41;&#46; Only five patients &#40;1&#46;8&#37;&#41; were receiving combined biological and immunosuppressant therapy&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Serological response to vaccines for SARS-CoV-2 in patients with inflammatory bowel disease</span><p id="par0065" class="elsevierStylePara elsevierViewall">The distribution of the different types of vaccines was as follows&#58; Comirnaty&#174; 68&#46;8&#37; &#40;N&#8239;&#61;&#8239;192&#41;&#59; Spikevax&#174; 10&#46;8&#37; &#40;30&#41;&#59; Vaxzevria&#174; 18&#46;3&#37; &#40;51&#41;&#59; and Ad26&#46;COV2-S&#174; 2&#46;1&#37;&#46;6 Overall&#44; 51&#46;3&#37; had AE with the vaccine &#40;N&#8239;&#61;&#8239;135&#41;&#44; all of which were mild&#44; the most common being pain at the vaccination site &#40;45&#46;9&#37;&#41;&#44; asthenia &#40;25&#46;9&#37;&#41;&#44; fever &#40;25&#46;9&#37;&#41;&#44; headache &#40;16&#46;3&#37;&#41;&#44; myalgia &#40;14&#46;1&#37;&#41; and general malaise &#40;15&#46;6&#37;&#41;&#46; After being vaccinated&#44; 65&#37; &#40;N&#8239;&#61;&#8239;174&#41; developed IgG antibodies&#46; <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> shows the efficacy and AE according to the specific type of vaccine&#46; Vaccines with mRNA technology had a higher SR than vector-based vaccines with adenovirus &#40;Comirnaty&#174; &#91;Pfizer-BioNTech&#93;&#47;Spikevax&#174; &#91;Moderna&#93; 72&#46;8&#37; vs Vaxzevria&#174;&#47;Ad26&#46;COV2-S&#174; &#91;Ad26&#46;COV2-S&#58; Janssen-Cilag International&#93; 37&#46;5&#37;&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;0001&#41;&#46; The AE rate was higher with vaccines based on mRNA technology &#40;55&#46;0&#37; vs 37&#46;0&#37;&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;018&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">The SR to the vaccine was related to age&#44; such that the patients who generated antibodies after the vaccine were younger than those who had no response &#40;50&#8239;&#177;&#8239;12 vs 56&#8239;&#177;&#8239;13 years&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001&#41;&#46; The efficacy of the vaccine was not related to the type of IBD treatment&#46; The percentage efficacy of the vaccine was as follows&#58; patients on no treatment or only on aminosalicylates&#44; 65&#46;4&#37;&#59; patients on immunosuppressive treatment&#44; 61&#46;4&#37;&#59; patients on anti-TNF treatment&#44; 65&#46;8&#37;&#59; and patients on treatment with non-anti-TNF biological drugs&#44; 68&#46;7&#37; &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;9&#41;&#46; Efficacy was also not related to IBD activity &#40;percentage efficacy in patients in remission&#44; 65&#46;8&#37; vs patients with IBD activity at the time of vaccination&#44; 65&#46;6&#37;&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;72&#41;&#44; gender &#40;64&#46;0&#37; efficacy in females vs 66&#46;2&#37; in males&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;2&#41;&#44; type of IBD &#40;efficacy in patients with Crohn&#8217;s disease 63&#46;7&#37; vs patients with ulcerative colitis&#44; 67&#46;7&#37;&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;967&#41;&#59; or previous comorbidities &#40;percentage efficacy in patients with comorbidities&#44; 63&#46;0&#37;&#44; vs 89&#46;2&#37; in patients without comorbidities&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;08&#41;&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">In the multivariate analysis&#44; only age was considered a factor related to SR&#59; patients under the age of 60 had a higher SR than patients over 60 &#40;OR&#58; 3&#46;8&#44; 95&#37; CI&#44; 1&#46;9&#8211;7&#46;0&#59; <span class="elsevierStyleItalic">p</span>&#8239;&#60;&#8239;&#46;001&#41;&#46;</p></span></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Discussion</span><p id="par0080" class="elsevierStylePara elsevierViewall">Published studies on the efficacy of the initial vaccination schedule for SARS-CoV-2 in the general population place it at around 90&#37; in terms of infection prevention&#46;<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5&#44;7&#44;10&#44;11</span></a> The available vaccines are not sterilising&#44; but they do reduce the severity and mortality rates of the different variants of SARS-CoV-2&#46;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;9</span></a> Our approach was to find out the SR to the available vaccines in patients with IBD and the possible influence of the base treatments on this response&#46; The SR in our study was 65&#37; and was higher for mRNA-based vaccines&#59; Comirnaty&#174;&#47;Spikevax&#174; 72&#46;8&#37; vs Vaxzevria&#174;&#47;Ad26&#46;COV2-S&#174; 37&#46;5&#37;&#46; The phase I-II trial of the Janssen Ad26&#46;COV2-S&#174; vaccine obtained 97&#37;&#8211;100&#37; seroconversion with the different doses used in the trial in patients aged 18&#8211;65&#44; while the seroconversion rate was lower in patients over 65 &#40;75&#37;&#8211;77&#37;&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> The SR in our study was also related to the age of the patients&#59; the patients who generated antibodies after the vaccine were younger than those who did not&#46; Other studies carried out with the vaccines for the hepatitis B virus and flu had similar findings&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#44;12</span></a> Intrinsic changes in B cells with age could contribute to reduced antibody response&#44; such as that seen with the influenza vaccine&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">12</span></a></p><p id="par0085" class="elsevierStylePara elsevierViewall">Also&#44; simply having IBD&#44; IBD activity at the time of vaccination or the treatments used to control the disease could affect the development of antibodies after vaccination&#46; Studies conducted in patients with liver or kidney transplants found that these patients develop a substantially lower immune response to the mRNA-based vaccine &#40;Comirnaty&#174;&#41; than controls&#46; All the control patients generated antibodies against the vaccine compared to 47&#46;5&#37; of liver transplant patients and 37&#46;5&#37; of kidney transplant patients&#46; Age was also among the predictors of worse SR to the vaccine&#46;<a class="elsevierStyleCrossRefs" href="#bib0075"><span class="elsevierStyleSup">13&#44;14</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">As in previous studies&#44; we found that disease activity did not seem to be related to a better or worse response to the vaccine&#46;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">15</span></a> Although around a quarter of the patients had IBD activity at the time of vaccination&#44; they did not have a lower SR than the rest&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">With regard to the treatments used&#44; it was reported that patients treated with infliximab may have attenuated immunogenicity with a single dose of the BNT162b2 &#40;Comirnaty&#174;&#41; and ChAdOx1 nCoV-19 &#40;Vaxzevria&#174;&#41; vaccines and vaccination was urged after SARS-CoV-2 infection&#44; or not delaying a second dose&#44; in these patients&#46;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">16</span></a> In our case&#44; seroconversion after vaccination was not related to the type of IBD treatment&#44; with very similar percentages of positive IgG antibodies in all treatment groups&#44; in line with other recently published data&#46;<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">17&#44;18</span></a> Vaccination therefore continues to be an effective option in all IBD patients regardless of the treatment they are receiving&#44; including immunosuppressive or biological drugs&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">In their article published in <span class="elsevierStyleItalic">Lancet Rheumatology</span>&#44; Mahil et al&#46; found that methotrexate may have decreased the SR to the Pfizer vaccine &#40;Comirnaty&#174;&#41; in a group of 17 patients with rheumatic diseases&#44; but immunosuppressive and biological treatments did not &#40;27 patients with anti-TNF therapies and 25 patients with anti-IL-23&#41;&#44; although they concluded that verification is needed from more pharmacovigilance studies with real-life data&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">19</span></a></p><p id="par0105" class="elsevierStylePara elsevierViewall">Other studies also reporting data from patients with rheumatological and musculoskeletal diseases on biological therapy with anti-TNF found&#44; like us&#44; that these therapies did not affect the generation of antibodies after vaccination&#46; However&#44; they did find that treatment with corticosteroids&#44; rituximab or abatacept were associated with lower immunity after receiving the vaccine&#46; In our study&#44; only three patients were receiving corticosteroid therapy at the time of vaccination&#44; so we cannot confirm these findings&#46;<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">20&#8211;22</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">Regarding the safety of the vaccine&#44; previous studies in the IBD population with vaccines using mRNA technology&#44; such as the study by Botwin et al&#46;&#44; reported that 62&#37; of the patients suffered AE after the second dose of the vaccine&#44; with the most common being pain at the administration site &#40;56&#37;&#41;&#44; asthenia &#40;45&#37;&#41;&#44; headache &#40;34&#37;&#41; and fever &#40;29&#37;&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0125"><span class="elsevierStyleSup">23&#44;24</span></a> These data are in line with ours&#59; in our study&#44; 51&#46;3&#37; of the patients overall had AE associated with the vaccine&#44; with a higher rate of AE in patients who received mRNA vaccines than in those given adenovirus vector-based vaccines&#46; In our case&#44; the most common AE were pain at the vaccination site &#40;45&#46;9&#37;&#41;&#44; asthenia &#40;25&#46;9&#37;&#41;&#44; fever &#40;25&#46;9&#37;&#41;&#44; headache &#40;16&#46;3&#37;&#41;&#44; myalgia &#40;14&#46;1&#37;&#41; and malaise &#40;15&#46;6&#37;&#41;&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">In our study all of the AE were mild&#46; However&#44; in the previously mentioned study&#44; 24 out of 246 patients had 53 serious AE after the second dose&#46; This may be due to the definition of severity&#44; as these authors considered severe AE to be those which limited daily activities&#44; although only three of the 24 patients who actually suffered AE required hospital admission for that reason&#46; In our case&#44; the criteria were stricter&#44; as we only considered as severe AE those which led to the hospitalisation or death of the patient&#44; neither of which occurred with any of our patients&#46; Therefore&#44; although development of AE was common&#44; they were manageable and outweighed the possible complications associated with a SARS-CoV-2 infection&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">Lastly&#44; regarding the limitations of the study&#44; we cannot rule out with complete certainty that some of the positive IgG results were due to post-vaccination infection&#44; as serology for envelope or nucleocapsid and protease was not performed in these patients&#46; We can confirm&#44; however&#44; that none of the patients had or had had symptoms compatible with the infection or previous positive diagnostic tests &#40;antigen test&#44; PCR or serology&#41; at the time of the measurement&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">Additionally&#44; it has to be taken into account that this series was carried out before the appearance of the Omicron variant&#44; at a time when the incidence of infection in the reference population was low&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Conclusions</span><p id="par0130" class="elsevierStylePara elsevierViewall">One third of patients with IBD failed to develop antibodies with the initial vaccination regimen for SARS-CoV-2&#46; The response to mRNA-based vaccines was greater and was related to age&#44; being better in younger patients&#46; The type of treatment used for IBD did not affect the SR&#46; Immunosuppressive and biological drugs did not decrease SR&#46; Although more than half of the patients developed AE with the vaccine&#44; they were mild in all cases&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">This work was carried out in accordance with the World Medical Association&#8217;s Code of Ethics &#40;Declaration of Helsinki&#41; for experiments with humans&#46; All the patients included in the study had signed the specific Informed Consent Form for telematic contact for reasons of their IBD&#46; They were also informed verbally and in writing in comprehensible language of the objectives and requirements of the study&#46; The explanations the participants received included full information about the nature&#44; purpose and possible risks and benefits of the study&#46; They were able to ask any questions they had and informed that they were completely free to withdraw from the study at any time&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">This study was approved by the Hospital Universitario de Fuenlabrada Ethics Committee&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Funding</span><p id="par0145" class="elsevierStylePara elsevierViewall">This study received no specific funding from public&#44; private or non-profit organisations&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Conflicts of interest</span><p id="par0150" class="elsevierStylePara elsevierViewall">A&#46; Algaba has been a speaker and has received a research grant or consultancy fees from MSD&#44; Lilly&#44; Roche&#44; Takeda and Janssen&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">F&#46; Bermejo has been a speaker&#44; consultant and advisory member or has received research funding from MSD&#44; Abbvie&#44; Takeda&#44; Janssen&#44; Pfizer&#44; Biogen&#44; Amgen&#44; Ferring&#44; Faes Farma&#44; Tillotts Pharma&#44; Chiesi and Gebro Pharma&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">I&#46; Guerra has served as a speaker or consultant for Takeda&#44; Kern Pharma&#44; Abbvie and Janssen&#46;</p><p id="par0165" class="elsevierStylePara elsevierViewall">None of the declared conflicts of interest is directly related to this manuscript&#46;</p></span></span>"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Objective</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">To study the serological response &#40;SR&#41; and tolerability of COVID-19 vaccine in patients with inflammatory bowel disease &#40;IBD&#41; and its relation with IBD treatment and type of vaccine&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Observational&#44; cross-sectional study in patients with IBD vaccinated against COVID-19 without known previous infection&#46; SR was analyzed by the determination of IgG antibodies against the S1 subunit&#46; Safety was studied using a questionnaire to identify adverse effects &#40;AE&#41;&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">280 patients with IBD were included&#46; Type of vaccines&#58; Comirnaty&#174; 68&#46;8&#37;&#59; Spikevax&#174; 10&#46;8&#37;&#44; Vaxzevria&#174; 18&#46;3&#37;&#44; Ad26&#46;COV2-S&#174; 2&#46;2&#37;&#46; 51&#46;3&#37; had AE&#44; being 100&#37; mild&#46; 65&#37; developed IgG antibodies after vaccination&#46; The SR was higher for vaccines with mRNA technology &#40;100&#37; Spikevax&#174;&#44; 68&#46;5&#37; Comirnaty&#174;&#41; compared to those based on adenovirus vector &#40;38&#46;0&#37; Vaxzevria&#174;&#44; 33&#46;3&#37; Ad26&#46;COV2-S&#174;&#41; &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001&#41;&#46; In the multivariate analysis&#44; SR was related to age &#40;&#60;60 years&#59; OR&#58; 3&#46;8&#44; 95&#37; CI 1&#46;9&#8211;7&#46;0&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001&#41;&#46; The SR in patients with aminosalicylates was 65&#46;4&#37;&#44; 61&#46;4&#37; with immunosuppressants&#44; 65&#46;8&#37; with anti-TNF&#44; and 68&#46;7&#37; with non-anti-TNF biologicals &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;9&#41;&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">One third of patients with IBD did not develop antibodies with the initial vaccination against SARS-CoV-2&#46; The SR to vaccines based on mRNA technology was higher&#44; and it was related to age &#40;higher in younger patients&#41;&#46; Immunosuppressants and biologicals did not decrease SR&#46; More than half of the patients presented AD&#44; being mild in all cases&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "abst0005"
            "titulo" => "Objective"
          ]
          1 => array:2 [
            "identificador" => "abst0010"
            "titulo" => "Methods"
          ]
          2 => array:2 [
            "identificador" => "abst0015"
            "titulo" => "Results"
          ]
          3 => array:2 [
            "identificador" => "abst0020"
            "titulo" => "Conclusions"
          ]
        ]
      ]
      "es" => array:3 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Objetivo</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Estudiar la respuesta serol&#243;gica &#40;RS&#41; y tolerabilidad frente a la vacuna COVID-19 en pacientes con enfermedad inflamatoria intestinal &#40;EII&#41; y su relaci&#243;n con el tratamiento de la EII y tipo de vacuna&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todos</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Estudio observacional&#44; transversal en pacientes con EII vacunados contra COVID-19 sin infecci&#243;n previa conocida&#46; La RS se analiz&#243; mediante la determinaci&#243;n de anticuerpos IgG frente a la subunidad S1&#46; La seguridad se estudi&#243; mediante cuestionario para identificaci&#243;n de efectos adversos &#40;EA&#41;&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Se incluyeron 280 pacientes con EII&#46; Tipo de vacunas&#58; Comirnaty&#174; 68&#44;8&#37;&#59; Spikevax&#174; 10&#44;8&#37;&#44; Vaxzevria&#174; 18&#44;3&#37;&#44; Ad26&#46;COV2-S&#174; 2&#44;2&#37;&#46; Un 51&#44;3&#37; tuvo EA&#44; siendo el 100&#37; leves&#46; Un 65&#37; desarroll&#243; anticuerpos IgG tras la vacunaci&#243;n&#46; La RS fue superior para vacunas con tecnolog&#237;a ARNm &#40;100&#37; Spikevax&#174;&#44; 68&#44;5&#37; Comirnaty&#174;&#41; frente a las basadas en vector con adenovirus &#40;38&#44;0&#37; Vaxzevria&#174;&#44; 33&#44;3&#37; Ad26&#46;COV2-S&#174;&#41; &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#44;001&#41;&#46; En el an&#225;lisis multivariante la RS se relacion&#243; con la edad &#40;&#60;60 a&#241;os&#59; OR&#58; 3&#44;8&#44; IC 95&#37; 1&#44;9&#8211;7&#44;0&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#44;001&#41;&#46; La RS en pacientes con aminosalicilatos fue del 65&#44;4&#37;&#44; 61&#44;4&#37; con inmunosupresor&#44; 65&#44;8&#37; con anti-TNF y 68&#44;7&#37; con biol&#243;gicos no anti-TNF &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#44;9&#41;&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Un tercio de pacientes con EII no desarroll&#243; anticuerpos con la pauta vacunal inicial frente a SARS-CoV-2&#46; La RS a las vacunas basadas en tecnolog&#237;a ARNm fue superior&#44; y estuvo relacionada con la edad &#40;mayor en pacientes m&#225;s j&#243;venes&#41;&#46; Los inmunosupresores y biol&#243;gicos no disminuyeron la RS&#46; M&#225;s de la mitad de los pacientes presentaron EA&#44; leves en todos los casos&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "abst0025"
            "titulo" => "Objetivo"
          ]
          1 => array:2 [
            "identificador" => "abst0030"
            "titulo" => "M&#233;todos"
          ]
          2 => array:2 [
            "identificador" => "abst0035"
            "titulo" => "Resultados"
          ]
          3 => array:2 [
            "identificador" => "abst0040"
            "titulo" => "Conclusiones"
          ]
        ]
      ]
    ]
    "multimedia" => array:2 [
      0 => array:8 [
        "identificador" => "tbl0005"
        "etiqueta" => "Table 1"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0005"
            "detalle" => "Table "
            "rol" => "short"
          ]
        ]
        "tabla" => array:1 [
          "tablatextoimagen" => array:1 [
            0 => array:1 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">N&#8239;&#61;&#8239;280&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Gender</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Male&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">150 &#40;53&#46;6&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Age</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Mean&#8239;&#177;&#8239;standard deviation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">52&#8239;&#177;&#8239;13 years&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Smoking</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">55 &#40;22&#46;1&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Tipo de enfermedad inflamatoria intestinal</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Crohn&#8217;s disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">166 &#40;59&#46;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Ulcerative colitis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">106 &#40;37&#46;9&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Unclassified&#47;indeterminate colitis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">8 &#40;2&#46;9&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Age at diagnosis &#40;Crohn&#8217;s disease&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>A1 &#40;age&#8239;&#8804;&#8239;16&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 &#40;6&#46;2&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>A2 &#40;aged 17&#8211;40&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">99 &#40;61&#46;5&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>A3 &#40;age&#8239;&#62;&#8239;40&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">52 &#40;32&#46;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Location &#40;Crohn&#8217;s disease&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>L1 terminal ileum&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">56 &#40;36&#46;4&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>L2 colon&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">25 &#40;16&#46;2&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>L3 ileocolic&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">72 &#40;46&#46;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>L1&#8239;&#43;&#8239;L4 &#40;upper gastrointestinal tract&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&#8211;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>L2&#8239;&#43;&#8239;L4&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1 &#40;0&#46;6&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Disease behaviour&#44; n &#40;&#37;&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B1 inflammatory&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">74 &#40;57&#46;8&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B2 stenosing&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">22 &#40;17&#46;2&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>B3 fistulising&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">32 &#40;25&#46;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Location &#40;ulcerative colitis&#41;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Extended&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">42 &#40;39&#46;6&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Left-sided colitis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">55 &#40;51&#46;9&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Proctitis&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 &#40;9&#46;4&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Type of treatment for the inflammatory bowel disease</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Mesalazine&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">59 &#40;21&#46;1&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Azathioprine&#47;mercaptopurine&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">89 &#40;31&#46;8&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Tofacitinib&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6 &#40;2&#46;1&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Methotrexate&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9 &#40;3&#46;2&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Infliximab&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">33 &#40;11&#46;8&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Adalimumab&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">36 &#40;12&#46;9&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Golimumab&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5 &#40;1&#46;8&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Ustekinumab&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">24 &#40;8&#46;6&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Vedolizumab&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">9 &#40;3&#46;2&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Corticosteroids&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3 &#40;1&#46;1&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Open-label clinical trial &#40;mirikizumab&#44; etrolizumab&#44; filgotinib&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">14 &#40;5&#46;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Comorbidities</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Yes&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">162 &#40;62&#46;5&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Type of comorbidity</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Chronic kidney disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 &#40;3&#46;7&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Chronic obstructive pulmonary disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">37 &#40;14&#46;6&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Congestive heart failure&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 &#40;0&#46;8&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Coronary heart disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5 &#40;2&#46;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Diabetes mellitus&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">33 &#40;12&#46;9&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Hypertension&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">74 &#40;29&#46;1&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Dyslipidaemia&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">87 &#40;34&#46;0&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Cancer&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">23 &#40;9&#46;1&#37;&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Liver disease&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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es en pt

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