Effectiveness and Safety of Ustekinumab in Pediatric Ulcerative Colitis: A Multi-center Retrospective Study from the Pediatric IBD Porto Group of ESPGHAN.


Journal

Paediatric drugs
ISSN: 1179-2019
Titre abrégé: Paediatr Drugs
Pays: Switzerland
ID NLM: 100883685

Informations de publication

Date de publication:
23 May 2024
Historique:
accepted: 14 04 2024
medline: 23 5 2024
pubmed: 23 5 2024
entrez: 23 5 2024
Statut: aheadofprint

Résumé

Current data on ustekinumab therapy in children with ulcerative colitis (UC) or unclassified inflammatory bowel disease (IBDU) are limited. We aimed to evaluate the effectiveness and safety of ustekinumab in pediatric UC and IBDU. This multicenter retrospective study included 16 centers affiliated with the IBD Interest and Porto groups of ESPGHAN. Children with UC or IBDU treated with ustekinumab were enrolled. Demographic, clinical, laboratory, endoscopic, and imaging data as well as adverse events were recorded. Analyses were all based on the intention-to-treat principle. Fifty-eight children (39 UC and 19 IBDU, median age 14.5 [IQR 11.5-16.5] years) were included. All had failed biologic therapies, and 38 (66%) had failed two or more biologics. Corticosteroid-free clinical remission (CFR) was observed in 27 (47%), 33 (57%), and 37 (64%) children at 16, 26, and 52 weeks, respectively. Normalization of C-reactive protein and calprotectin < 150 μg/g were achieved in 60% and 52%, respectively, by 52 weeks. Endoscopic and radiologic remissions were reached in 8% and 23%, respectively. The main predictors of CFR were diagnosis of UC compared with IBDU (hazard ratio [HR] 2.2, 95% CI 1.03-4.85; p = 0.041) and no prior vedolizumab therapy (HR 2.1, 95% CI 1.11-4.27; p = 0.023). Ustekinumab serum levels were not associated with disease activity. Adverse events were recorded in six (10%) children, leading to discontinuation of the drug in three. Based on these findings, ustekinumab appears as an effective therapy for pediatric refractory UC and IBDU. The potential efficacy should be weighed against the risks of serious adverse events.

Sections du résumé

BACKGROUND AND OBJECTIVES OBJECTIVE
Current data on ustekinumab therapy in children with ulcerative colitis (UC) or unclassified inflammatory bowel disease (IBDU) are limited. We aimed to evaluate the effectiveness and safety of ustekinumab in pediatric UC and IBDU.
METHODS METHODS
This multicenter retrospective study included 16 centers affiliated with the IBD Interest and Porto groups of ESPGHAN. Children with UC or IBDU treated with ustekinumab were enrolled. Demographic, clinical, laboratory, endoscopic, and imaging data as well as adverse events were recorded. Analyses were all based on the intention-to-treat principle.
RESULTS RESULTS
Fifty-eight children (39 UC and 19 IBDU, median age 14.5 [IQR 11.5-16.5] years) were included. All had failed biologic therapies, and 38 (66%) had failed two or more biologics. Corticosteroid-free clinical remission (CFR) was observed in 27 (47%), 33 (57%), and 37 (64%) children at 16, 26, and 52 weeks, respectively. Normalization of C-reactive protein and calprotectin < 150 μg/g were achieved in 60% and 52%, respectively, by 52 weeks. Endoscopic and radiologic remissions were reached in 8% and 23%, respectively. The main predictors of CFR were diagnosis of UC compared with IBDU (hazard ratio [HR] 2.2, 95% CI 1.03-4.85; p = 0.041) and no prior vedolizumab therapy (HR 2.1, 95% CI 1.11-4.27; p = 0.023). Ustekinumab serum levels were not associated with disease activity. Adverse events were recorded in six (10%) children, leading to discontinuation of the drug in three.
CONCLUSION CONCLUSIONS
Based on these findings, ustekinumab appears as an effective therapy for pediatric refractory UC and IBDU. The potential efficacy should be weighed against the risks of serious adverse events.

Identifiants

pubmed: 38780740
doi: 10.1007/s40272-024-00631-z
pii: 10.1007/s40272-024-00631-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Turner D, Ruemmele FM, Orlanski-Meyer E, et al. Management of paediatric ulcerative colitis, part 1: ambulatory care-an evidence-based guideline from European Crohn’s and Colitis Organization and European Society of Paediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr. 2018;67(2):257–91.
doi: 10.1097/MPG.0000000000002035 pubmed: 30044357
Hyams J, Damaraju L, Blank M, et al. Induction and maintenance therapy with infliximab for children with moderate to severe ulcerative colitis. Clin Gastroenterol Hepatol. 2012;10(4):391-399.e1.
doi: 10.1016/j.cgh.2011.11.026 pubmed: 22155755
Croft NM, Faubion WA Jr, Kugathasan S, et al. Efficacy and safety of adalimumab in paediatric patients with moderate-to-severe ulcerative colitis (ENVISION I): a randomised, controlled, phase 3 study. Lancet Gastroenterol Hepatol. 2021;6(8):616–27.
doi: 10.1016/S2468-1253(21)00142-4 pubmed: 34153231
Breton J, Kastl A, Conrad M, et al. Positioning biologic therapies in the management of pediatric inflammatory bowel disease. Gastroenterol Hepatol. 2020;16:400–14.
Atia O, Shavit-Brunschwig Z, Mould DR, et al. Outcomes, dosing, and predictors of vedolizumab treatment in children with inflammatory bowel disease (VEDOKIDS): a prospective, multicentre cohort study. Lancet Gastroenterol Hepatol. 2023;8(1):31–42.
doi: 10.1016/S2468-1253(22)00307-7 pubmed: 36306803
Feagan BG, Sandborn WJ, Gasink C, et al. Ustekinumab as induction and maintenance therapy for Crohn’s disease. N Engl J Med. 2016;375(20):1946–60.
doi: 10.1056/NEJMoa1602773 pubmed: 27959607
Sandborn WJ, Rebuck R, Wang Y, et al. Five-year efficacy and safety of ustekinumab treatment in crohn’s disease: the IM-UNITI Trial. Clin Gastroenterol Hepatol. 2022;20(3):578–90.
doi: 10.1016/j.cgh.2021.02.025 pubmed: 33618023
Engel T, Yung DE, Ma C, et al. Effectiveness and safety of Ustekinumab for Crohn’s disease; systematic review and pooled analysis of real-world evidence. Dig Liver Dis. 2019;51(9):1232–40.
doi: 10.1016/j.dld.2019.05.002 pubmed: 31202609
Sands BE, Sandborn WJ, Panaccione R, et al. Ustekinumab as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2019;381(13):1201–14.
doi: 10.1056/NEJMoa1900750 pubmed: 31553833
Abreu MT, Rowbotham DS, Danese S, et al. Efficacy and safety of maintenance ustekinumab for ulcerative colitis through 3 years: UNIFI long-term extension. J Crohns Colitis. 2022;16(8):1222–34.
doi: 10.1093/ecco-jcc/jjac030 pubmed: 35239968 pmcid: 9426670
Fumery M, Filippi J, Abitbol V, et al. Effectiveness and safety of ustekinumab maintenance therapy in 103 patients with ulcerative colitis: a GETAID cohort study. Aliment Pharmacol Ther. 2021;54(7):944–51.
doi: 10.1111/apt.16544 pubmed: 34296456
Chiappetta MF, Viola A, Mastronardi M, et al. One-year effectiveness and safety of ustekinumab in ulcerative colitis: a multicenter real-world study from Italy. Expert Opin Biol Ther. 2021;21(11):1483–9.
doi: 10.1080/14712598.2021.1981855 pubmed: 34521307
Honap S, Al-Hillawi L, Baillie S, et al. Ustekinumab for the treatment of moderate to severe ulcerative colitis: a multicentre UK cohort study. Frontline Gastroenterol. 2022;13(6):517–23.
doi: 10.1136/flgastro-2022-102168 pubmed: 36250172 pmcid: 9555129
Chaparro M, Garre A, Iborra M, et al. Effectiveness and safety of ustekinumab in ulcerative colitis: real-world evidence from the ENEIDA Registry. J Crohns Colitis. 2021;15(11):1846–51.
doi: 10.1093/ecco-jcc/jjab070 pubmed: 33860795
Thunberg J, Björkqvist O, Hedin CRH, et al. Ustekinumab treatment in ulcerative colitis: real-world data from the Swedish inflammatory bowel disease quality register. United Eur Gastroenterol J. 2022;10(7):631–9.
doi: 10.1002/ueg2.12275
Dhaliwal J, McKay HE, Deslandres C, et al. One-year outcomes with ustekinumab therapy in infliximab-refractory paediatric ulcerative colitis: a multicentre prospective study. Aliment Pharmacol Ther. 2021;53(12):1300–8.
doi: 10.1111/apt.16388 pubmed: 33909911
Levine A, Koletzko S, Turner D, et al. ESPGHAN revised porto criteria for the diagnosis of inflammatory bowel disease in children and adolescents. J Pediatr Gastroenterol Nutr. 2014;58:795–806.
doi: 10.1097/MPG.0000000000000239 pubmed: 24231644
Levine A, Griffiths A, Markowitz J, et al. Pediatric modification of the Montreal classification for inflammatory bowel disease: the Paris classification. Inflamm Bowel Dis. 2011;17(6):1314–21.
doi: 10.1002/ibd.21493 pubmed: 21560194
Turner D, Otley AR, Mack D, et al. Development, validation, and evaluation of a pediatric ulcerative colitis activity index: a prospective multicenter study. Gastroenterology. 2007;133:423–32.
doi: 10.1053/j.gastro.2007.05.029 pubmed: 17681163
Schroeder MKW, Tremaine WJ, Ilstrup DM. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. N Engl J Med. 1987;317(26):1625–9.
doi: 10.1056/NEJM198712243172603 pubmed: 3317057
Danese S, Sands BE, Abreu MT, et al. Early symptomatic improvement after ustekinumab therapy in patients with ulcerative colitis: 16-week data from the UNIFI Trial. Clin Gastroenterol Hepatol. 2022;20(12):2858–67.
doi: 10.1016/j.cgh.2022.02.050 pubmed: 35276329
Afif W, Arasaradnam RP, Abreu MT, et al. Efficacy and safety of ustekinumab for ulcerative colitis through 4 years: final results of the UNIFI long-term maintenance study. Am J Gastroenterol. 2023. https://doi.org/10.14309/ajg.0000000000002621 . (Online ahead of print).
doi: 10.14309/ajg.0000000000002621 pubmed: 38095692 pmcid: 11062601
Meyer A, Fumery M, Peyrin-Biroulet L, et al. Comparative real-world effectiveness of vedolizumab and ustekinumab for patients with ulcerative colitis: a GETAID multicentre cohort study. Scand J Gastroenterol. 2022;57(12):1454–62.
doi: 10.1080/00365521.2022.2095668 pubmed: 35819361
Dalal RS, Esckilsen S, Barnes EL, et al. Predictors and outcomes of ustekinumab dose intensification in ulcerative colitis: a multicenter cohort study. Clin Gastroenterol Hepatol. 2022;20(10):2399–401.
doi: 10.1016/j.cgh.2021.03.028 pubmed: 33775893
Taxonera C, Olivares D, López-García ON, et al. Meta-analysis: Real-world effectiveness and safety of ustekinumab in patients with ulcerative colitis. Aliment Pharmacol Ther. 2023;57(6):610–9.
doi: 10.1111/apt.17386 pubmed: 36645145
Alsoud D, De Hertogh G, Compernolle G, et al. Real-world endoscopic and histological outcomes are correlated with ustekinumab exposure in patients with ulcerative colitis. J Crohns Colitis. 2022;16(10):1562–70.
doi: 10.1093/ecco-jcc/jjac067 pubmed: 35533353
Uchida G, Nakamura M, Yamamura T, et al. Real-world effectiveness and risk factors for discontinuation of ustekinumab in ulcerative colitis. Inflamm Intest Dis. 2023;8(2):60–8.
doi: 10.1159/000531497 pubmed: 37901340 pmcid: 10601947
Zhdanava M, Zhao R, Manceur AM, et al. Persistence and dose escalation during maintenance phase and use of nonbiologic medications among patients with ulcerative colitis initiated on ustekinumab in the United States. Crohns Colitis 360. 2023;5(3):otad045.
doi: 10.1093/crocol/otad045 pubmed: 37671391 pmcid: 10476877
Gisbert JP, Parody-Rúa E, Chaparro M. Efficacy, effectiveness, and safety of ustekinumab for the treatment of ulcerative colitis: a systematic review. Inflamm Bowel Dis. 2023;30(2):292–302. https://doi.org/10.1093/ibd/izac275 . (Online ahead of print).
doi: 10.1093/ibd/izac275 pmcid: 10834158

Auteurs

Shlomi Cohen (S)

Pediatric Gastroenterology Institute, "Dana-Dwek" Children's Hospital, Tel Aviv Sourasky Medical Center and the Faculty of Medicine, Tel Aviv University, 6 Weizmann Street, 6423906, Tel Aviv, Israel. shlomico@tlvmc.gov.il.

Helena Rolandsdotter (H)

Department of Clinical Science and Education and Department of Gastroenterology, Sachs Children and Youth Hospital, Karolinska Institute, Stockholm, Sweden.
Department of Gastroenterology, Sachs' Children and Youth Hospital, Stockholm, Sweden.

Kaija-Leena Kolho (KL)

Department of Paediatric Gastroenterology, Children's Hospital and Tampere University, HUS and University of Helsinki, Helsinki, Finland.
Tampere University, Tampere, Finland.

Dan Turner (D)

The Juliet Keiden Institute of Pediatric Gastroenterology and Nutrition, The Eisenberg R&D Authority, Shaare Zedek Medical Center, The Hebrew University of Jerusalem, Jerusalem, Israel.

Christos Tzivinikos (C)

Department of Pediatric Gastroenterology, Al Jalila Children's Specialty Hospital, Mohamed Bin Rashid University of Medicine and Health Sciences, Dubai, United Arab Emirates.

Matteo Bramuzzo (M)

Gastroenterology, Digestive Endoscopy and Nutrition Unit, Institute for Maternal and Child Health, IRCCS "Burlo Garofolo", Trieste, Italy.

Gemma Pujol-Muncunill (G)

Department of Paediatric Gastroenterology, Hepatology and Nutrition, Hospital Sant Joan de Déu, Barcelona, Spain.

Luca Scarallo (L)

Gastroenterology and Nutrition Unit, Meyer Children's Hospital IRCCS, Florence, Italy.

Darja Urlep (D)

Department of Gastroenterology, Hepatology and Nutrition, University Children's Hospital Ljubljana, 1000, Ljubljana, Slovenia.

Firas Rinawi (F)

Pediatric Gastroenterology Unit and Faculty of Medicine Technion, Haifa, Emek Medical Centre, Afula, Israel.
Faculty of Medicine Technion, Haifa, Israel.

Maya Granot (M)

Pediatric Gastroenterology and nutrition Unit, Edmond and Lily Safra Children's Hospital and the Faculty of Medicine, Tel Aviv University, Sheba Medical Center, Ramat Gan, Israel.
The Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.

Ben Kang (B)

Department of Pediatrics, School of Medicine, Kyungpook National University, Daegu, Korea.

Ylva Longueville (Y)

Pediatric Gastroenterology Unit, Karolinska University Hospital, Stockholm, Sweden.

Marta Velasco Rodríguez-Belvís (MV)

Paediatric Gastroenterology, Hepatology and Nutrition, Hospital Infantil Universitario Niño Jesús, Madrid, Spain.

Yael Weintraub (Y)

Schneider Children's Medical Center and the Faculty of Medicine, Institute of Gastroenterology, Nutrition and Liver Diseases, Tel Aviv University, Tel Aviv, Israel.

Víctor Manuel Navas-López (VM)

Pediatric Gastroenterology and Nutrition Unit, Hospital Regional Universitario de Málaga, Málaga, Spain.

Anat Yerushalmy-Feler (A)

Pediatric Gastroenterology Institute, "Dana-Dwek" Children's Hospital, Tel Aviv Sourasky Medical Center and the Faculty of Medicine, Tel Aviv University, 6 Weizmann Street, 6423906, Tel Aviv, Israel.

Classifications MeSH