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THE RISK OF MILD, MODERATE AND SEVERE INFECTIONS IN IBD PATIENTS: RESULTS FROM A PROSPECTIVE, MULTICENTRE, OBSERVATIONAL COHORT STUDY - PRIQ

Ashkan Rezazadeh Ardabili 1, Dirk van Esser 1, Dion S.J. Wintjens 1, Mia Cilissen 1, Debbie S. Deben 2, Zlatan Mujagic 1, Fritzi Russ 2, Laurents Stassen 1, Adriaan A. Van Bodegraven 2, Dennis R. Wong 2, Bjorn Winkens 3, Daisy Mae Jonkers 1, Marielle Romberg-Camps 2, Marieke Pierik 1

Affiliations

1 Maastricht University Medical Center+, Maastricht, Netherlands

2 Zuyderland Medical Centre, Sittard-Geleen, Netherlands

3 Maastricht University, Maastricht, Netherlands

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Abstract

Introduction

Immunomodulators and biologicals play an essential role in current IBD management, but are associated with increased risk of infections. In light of the growing number of treatment options, the benefit-risk balance of drugs is becoming increasingly important in clinical decision making. Post-marketing surveillance studies are pivotal to assess infection risk, yet mainly focus on severe infections. As a result, data on mild and moderate infections are scarce. However, mild and moderate infections take longer to clear in immunosuppressed patients, have been reported to be the most burdensome adverse drug reaction according to patients, and can negatively influence drug adherence.

Aims & Methods

Aim: To assess the incidence of all infections and identify risk factors for the development of infections in IBD patients.
Methods: We previously developed and validated a Patient-Reported Infections Questionnaire (PRIQ), with excellent diagnostic accuracy, covering 15 infection categories with a 3-month recall period. [1] The current prospective, multicentre, observational cohort study was performed between Jun, 1 2020 and Jul, 1 2021, enrolling consecutive IBD patients and using the PRIQ which was implemented in myIBDcoach, an established telemedicine platform. Infection severity was defined as mild (self-limiting or topical treatment), moderate (oral antibiotics, antivirals or antifungals) or severe (hospitalization or IV treatment). Incidence rates (IR) were calculated for all infections, stratified for severity and subtype. Multivariable logistic regression, adjusting for relevant confounders, was performed to identify risk factors for infections.

Results

In total, 629 IBD patients (n=346 CD, n=283 UC, 58.3% female, mean age at cohort entry 48.3 years [SD 14.8], mean disease duration 12.4 years [SD 10.8]) were included which completed 2391 PRIQs during 572 person-years (PY) of follow-up. This resulted in 990 reported infections, corresponding to IRs of 17.3, 11.8, 5.1, and 0.4 per 10PY for all, mild, moderate, and severe infections, respectively. Upper respiratory tract (IR 26.9/100PY) and urinary tract infections (IR 14.8/100PY) were the most commonly reported mild and moderate infections types, respectively (Table 1). Compared to patients without treatment, patients on immunosuppressive treatment more frequently experienced infections of any severity (mild vs. no treatment: IR ratio (IRR) 1.57 [95%CI 1.21-2.06] p<0.001, moderate vs. no treatment: IRR 1.42 [95%CI 1.20-1.69] p<0.001). On multivariable logistic regression, female sex (mild adjusted odds ratio [aOR] 1.96 [95%CI 1.38-2.79]; moderate aOR 1.71 [95%CI 1.15-2.54]), smoking status (mild aOR 1.66 [95%CI 1.15-2.41]; moderate aOR 1.86 [95%CI 1.05-3.28]), higher BMI (moderate aOR 1.05 [95%CI 1.02-2.00]), and more comorbidities (mild aOR 2.41 [95%CI 1.46-3.98]; moderate aOR 1.82 [95%CI 1.07-3.11]) were all significantly associated with the development of mild and moderate infections.

Table 1. Incidence rates for all infections, and stratified for infection type and infection severity per 100 PY.
	All infections		Mild infections		Moderate infections		Severe infections
Infection type^†	n	IR [95% CI]	n	IR [95% CI]	n	IR [95% CI]	n	IR [95% CI]
All Influenza URTI LRTI COVID-19 Eye Oral Cold sore Gastrointestinal Urinary tract Genital Skin Shingles Warts Tuberculosis Meningitis Hepatitis Other	990 131 205 48 46 58 76 102 18 95 33 80 10 68 0 0 3 17	173.0 [162.4-184.0] 22.9 [19.2-27.1] 35.8 [31.2-41.0] 8.4 [6.3-11.0] 8.0 [6.0-10.6] 10.1 [7.8-13.0] 13.3 [10.5-16.5] 17.8 [14.6-21.5] 3.1 [1.9-4.9] 16.6 [13.5-20.2] 5.8 [4.0-8.0] 14.0 [11.2-17.3] 1.7 [0.9-3.1] 11.9 [9.3-15.0] N/A N/A 0.5 [0.1-1.4] 3.0 [1.8-4.7]	673 102 154 14 38 53 58 98 2 8 19 50 1 68 0 0 0 8	118.0 [108.9-126.7] 17.8 [14.6-21.5] 26.9 [22.9-31.4] 2.4 [1.4-4.0] 6.6 [4.8-9.0] 9.3 [7.0-12.0] 10.1 [7.8-13.0] 17.0 [14.0-20.8] 0.3 [0.06-1.2] 1.4 [0.6-2.7] 3.3 [2.0-5.1] 8.7 [6.6-11.4] 0.2 [0.009-0.9] 11.9 [9.3-15.0] N/A N/A N/A 1.4 [0.6-2.6]	292 25 48 31 6 5 17 4 8 85 14 30 9 0 0 0 2 8	51.0 [45.4-57.1] 4.4 [2.9-6.4] 8.4 [6.3-11.0] 5.4 [3.7-7.6] 1.0 [0.4-2.2] 0.9 [0.3-1.9] 3.0 [1.8-4.7] 0.7 [0.2-1.7] 1.4 [0.6-2.6] 14.8 [12.0-18.3] 2.4 [1.4-4.0] 5.2 [3.6-7.4] 1.6 [0.8-2.9] N/A N/A N/A 0.3 [0.06-1.2] 1.4 [0.6-2.7]	25 4 3 3 2 0 1 0 8 2 0 0 0 0 0 0 1 1	4.0 [2.9-6.4] 0.7 [0.2-1.7] 0.5 [0.1-1.4] 0.5 [0.1-1.4] 0.3 [0.06-1.2] N/A 0.2 [0.009-0.9] N/A 1.4 [0.6-2.6] 0.3 [0.06-1.2] N/A N/A N/A N/A N/A N/A 0.2 [0.009-0.9] 0.2 [0.009-0.9]
_n,_{number of infectious events; IR, incidence rate; PY, person-years; CI, confidence interval; URTI, upper respiratory tract infection; LRTI, lower respiratory tract infection. 95%CI calculated using Mid-P exact test} _{^†Elaboration on infection types:}_{URTI includes nasal cold, laryngitis, tonsillitis, sinus infection, ear infection and ‘common’ cold. LRTI includes pneumonia and bronchitis.} _{Time at risk (572.5 PY) based on follow up of 629 IBD patients during 1 year.}

Conclusion

In this real-world prospective study, immune suppressive therapy was associated with mild and moderate infections of any kind in IBD patients. These infections particularly occur in females, smokers, patients with higher BMI and more comorbidities. This information should be considered in personalised treatment selection.

References

[1] Rezazadeh Ardabili A, van Esser D, Wintjens D, et al. Development and validation of a remote monitoring tool for assessment of mild, moderate, and severe infections in Inflammatory Bowel Disease [published online ahead of print, 2023 Feb 16]. J Crohns Colitis. 2023;jjad023. doi:10.1093/ecco-jcc/jjad023

Disclosure

M.P. reports grants and non-financial support from Falk Pharma, grants from European commission, grants from ZonMw (Dutch national research fund), grants and non-financial support from Takeda, grants and non-financial support from Johnson and Johnson, grants and non-financial support from Abbvie, non-financial support from Ferring, non-financial support from Immunodiagnostics, non-financial support from MSD, all outside the submitted work. D.J. reports grants from Top Knowledge Institute (Well on Wheat), grants from Horizon 2020 DISCOvERIE, grants from NWO-CCC Partnership program (Carbokinetics), all outside the submitted work. Z.M. reports grants form MLDS, Niels Stensen Fellowship and Galapagos. A.v.B. has served as speaker, adviser and/or principal investigator for AbbVie, Arandal, Arena, Celgene, Ferring, Galapagos, Janssen, MSD, Pfizer, Roche, Takeda, TEVA, and received research grants from Pfizer, TEVA, Eurostars funding, ZonMw, all outside the submitted work.
The other authors have nothing to disclose relevant to this publication.

Conference

UEG Week Copenhagen 2023

Topics

IBD

Submission format

Abstract

Session

PP 05 IBD (Posters)

Citation

United European Gastroenterology Journal 2023; 11 (Supplement 8)

Published

2023

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Henrik Albæk Jacobsen

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POPULATION-WIDE STUDY IDENTIFIES HLA-DRB1*01:03 AS A STRONG RISK FACTOR FOR SEVERE ULCERATIVE COLITIS DISEASE COURSE

Marie Vestergaard 1, Kristine Allin 1,2, Anne Krogh Nøhr* 1, Jesus Vicente Torresano Lominchar 1, Heidi Søgaard Christensen 1, Rasmus Froberg Brøndum 1, Martin Bøgsted 1, Henrik Bygum Krarup 2, Kaspar René Nielsen 3, Henrik Albæk Jacobsen 1, Lone Larsen 1,2, Aleksejs Sazonovs 1, Tine Jess 1,2

Affiliations

1 Center for Molecular Prediction of Inflammatory Bowel Disease (PREDICT), Aalborg University Copenhagen, Copenhagen, Denmark

2 Aalborg University Hospital, Aalborg, Denmark

3 Zealand University Hospital, Roskilde, Denmark

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Abstract

Introduction

We lack reliable biomarkers to identify patients with inflammatory bowel disease (IBD) at a greater risk of severe disease course. With emerging evidence that early step-down treatment in severe patients leads to better disease outcomes, alongside worries about overtreatment of mild patients, there is a clinical need to identify such biomarkers.

Aims & Methods

In this study, we explore genetic variants associated with severe disease course for ulcerative colitis (UC) in a nationwide cohort of 4491 patients from Denmark.
We genotyped 4491 patients with UC (4153 from Danish birth blood spot archive; 338 from NorDIBD regional cohort), linking them with registry data capturing medical interactions throughout patients’ lifetimes. Patients who required 2+ IBD-related hospitalizations, 2+ IBD-related major surgeries, 1 IBD-related hospitalization and 1 IBD-related major surgery or use of systemic corticosteroids (≥5000 mg) in the first 3 years of diagnosis were defined as severe. We conducted a genome-wide association study comparing severe patients (N=1203) to those with a less severe disease course (N=3288).

Results

The GWAS identified a signal within the HLA region, with the HLA-DRB1*01:03 allele driving the association (OR=3.30 [2.23-4.87], P=2.08×10^-9, UC carriage rate=2.8%). We did not observe an association with CD severity in a similarly ascertained cohort of 3688 individuals (P=0.79).
Remarkably, carriage of DRB1*01:03 was associated with a seven-fold increase of major surgery risk (OR=7.05 [4.55-10.91], P=2.31×10^-16) (Table 1). At the point of diagnosis, carriage of DRB1*01:03 was associated with higher CRP levels (β=2.68, P=1.70×10^-7), f-cal levels (β=1.92, P=4.42×10^-3) and a higher rate of hospitalization at diagnosis (OR=1.64, P=0.014), suggesting that the effect on severity is not limited to disease progression.

Outcome	N	OR [95% CI]	P-value
Main analysis	1203 vs. 3288	3.30 [2.23 - 4.87]	2.08E-09
≥5000 mg corticosteroids	821 vs. 3288	2.29 [1.42 - 3.69]	1.06E-03
≥2 hospitalizations	692 vs. 3288	5.16 [3.44 - 7.73]	1.72E-14
≥2 hospitalizations without major surgery	555 vs. 3288	5.93 [3.71 - 9.49]	2.28E-12
≥2 major surgeries	242 vs. 3288	7.24 [4.35 - 12.04]	1.49E-12
Major surgery	358 vs. 3266	7.05 [4.55 - 10.91]	2.31E-16
Intestinal resection	210 vs. 3266	7.42 [4.46 - 12.32]	2.33E-12
Enterostomy	151 vs. 3266	8.38 [4.67 - 15.03]	1.54E-10
Colectomy	338 vs. 3266	7.34 [4.73 - 11.40]	8.23E-17

Table 1: HLA-DRB1*01:03 has a consistent direction of effect and magnitude across different conditions that define patient severity; it is associated with multifaceted patient severity, rather than one particular factor entirely driving the association.

Conclusion

In this large-scale, unselected nationwide cohort study, we find that HLA-DRB1*01:03 is a biomarker of UC disease course that is associated with a more severe presentation at diagnosis, as well as higher subsequent risk of surgery and hospitalization. Demonstrating the association at a genome-wide significance level for the first time, this study revitalizes findings from smaller studies at the beginning of the genetic era which explicitly recruited severe patients and made estimating carriage effects difficult.
While HLA-DRB1*01:03 is a low-frequency allele, patients who carry it are at a much higher risk of severe UC. As the cost of typing a single HLA allele is low (under 50 EUR) and several pharmacogenetic variants are beginning to be tested at diagnosis, we argue that it is a valuable addition to the arsenal of personalized healthcare tools.

Conference

UEG Week Vienna 2024

Topics

IBD

Submission format

Abstract

Session

IBD risk factors and outcomes (Posters)

Citation

United European Gastroenterology Journal 2024; 12 (Supplement 8)

Published

2024

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	%(n)
Nausea	25(49)
Diarrhoea	37(70)
Abdominal Pain	44(84)
Distension	42(80)
Sensation of food getting stuck in bowel	9(18)
Hair Falling out	13(25)
Mouth Ulcers	18(35)
Glossitis	4(7)
Angular stomatitis	6(11)

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