Consensus guidelines of ECCO/ESPGHAN on the medical management of pediatric Crohn’s disease
Open accessAbstract
Children and adolescents with Crohn's disease (CD) present often with a more complicated disease course compared to adult patients. In addition, the potential impact of CD on growth, pubertal and emotional development of patients underlines the need for a specific management strategy of pediatric-onset CD. To develop the first evidenced based and consensus driven guidelines for pediatric-onset CD an expert panel of 33 IBD specialists was formed after an open call within the European Crohn's and Colitis Organisation and the European Society of Pediatric Gastroenterolog, Hepatology and Nutrition. The aim was to base on a thorough review of existing evidence a state of the art guidance on the medical treatment and long term management of children and adolescents with CD, with individualized treatment algorithms based on a benefit-risk analysis according to different clinical scenarios. In children and adolescents who did not have finished their growth, exclusive enteral nutrition (EEN) is the induction therapy of first choice due to its excellent safety profile, preferable over corticosteroids, which are equipotential to induce remission. The majority of patients with pediatric-onset CD require immunomodulator based maintenance therapy. The experts discuss several factors potentially predictive for poor disease outcome (such as severe perianal fistulizing disease, severe stricturing/penetrating disease, severe growth retardation, panenteric disease, persistent severe disease despite adequate induction therapy), which may incite to an anti-TNF-based top down approach. These guidelines are intended to give practical (whenever possible evidence-based) answers to (pediatric) gastroenterologists who take care of children and adolescents with CD; they are not meant to be a rule or legal standard, since many different clinical scenario exist requiring treatment strategies not covered by or different from these guidelines.
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There is limited evidence for the role of diet and other types of CAMs in inducing and maintaining disease remission in IBD, excluding exclusive enteral nutrition in pediatric Crohn's disease.
“This interest and use of CAM is common in pediatric IBD, despite being limited evidence for the role of diet and other types of CAMs in inducing and maintaining disease remission in IBD (excluding exclusive enteral nutrition in pediatric Crohn’s disease) [22,23,24].”
From Online Acceptance and Commitment Therapy and Nutrition Workshop for Parents of Children with Inflammatory Bowel Disease: Feasibility, Acceptability, and Initial Effectiveness. (2021) · cites this paper as [22]
Section 2.1 recommends exclusive enteral nutrition to induce remission in children with Crohn’s disease, while Statement 21 finds no significant maintenance benefit from probiotics and Statement 20 does not recommend omega-3 preparations. These passages support the exception and limited evidence for some alternatives, but the guidelines do not establish the broader claim about diet and other CAMs across IBD or that CAM use is common in pediatric IBD. (LLM, conf=0.86)
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Levine, A., Weizman, Z., Broide, E., Shamir, R., Shaoul, R. R., Pacht, A., Dinari, G., On, A., Weiss, B., & Bujanover, Y. (2003) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200302000-00017 · Cited by 81 · see citing works
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Optimum Duration of Treatment With 6-Mercaptopurine for Crohn's Disease
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Torres, J., Mehandru, S., Colombel, J., & Peyrin‐Biroulet, L. (2016) · The Lancet · doi:10.1016/s0140-6736(16)31711-1 · Cited by 2,722 · see citing works
The Medical Management of Paediatric Crohn’s Disease: an ECCO-ESPGHAN Guideline Update
van Rheenen, P. F., Aloi, M., Assa, A., Bronský, J., Escher, J. C., Fagerberg, U. L., Gasparetto, M., Gerasimidis, K., Griffiths, A. M., Henderson, P., et al. (2020) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjaa161 · Cited by 756 · see citing works
The Diagnostic Approach to Monogenic Very Early Onset Inflammatory Bowel Disease
Uhlig, H. H., Schwerd, T., Koletzko, S., Shah, N., Kammermeier, J., Elkadri, A. A., Ouahed, J., Wilson, D. C., Travis, S. P. L., Turner, D., et al. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.07.023 · Cited by 716 · see citing works
Levine, A., Wine, E., Assa, A., Boneh, R. S., Shaoul, R. R., Kori, M., Cohen, S., Peleg, S., Shamaly, H., On, A., et al. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.04.021 · Cited by 673 · see citing works
ESPEN guideline: Clinical nutrition in inflammatory bowel disease
Forbes, A., Escher, J., Hébuterne, X., Kłęk, S., Krznaric, Z., Schneider, S., Shamir, R., Stardelova, K., Wierdsma, N., Wiskin, A. E., et al. (2017) · Clinical Nutrition · doi:10.1016/j.clnu.2016.12.027 · Cited by 625 · see citing works
“Overall, the panel did not find enough evidence to make firm recommendations over and above previous European recommendations [13,137].”
BackgroundMethodInfluentialSelf-citationRetractedAn Update on Inflammatory Bowel Disease
Sairenji, T., Collins, K. L., & Evans, D. (2017) · Primary Care Clinics in Office Practice · doi:10.1016/j.pop.2017.07.010 · Cited by 501 · see citing works
“Data on the safety and efficacy of thalidomide treatment in children are still insufficient.(95) Anti-TNF therapies (such as infliximab and adalimumab) are commonly used in children and can be used for induction or maintenance of remission.”
BackgroundInfluentialYu, Y. R., & Rodriguez, J. R. (2017) · Seminars in Pediatric Surgery · doi:10.1053/j.sempedsurg.2017.10.003 · Cited by 396 · see citing works
Evolving role of diet in the pathogenesis and treatment of inflammatory bowel diseases
Levine, A., Boneh, R. S., & Wine, E. (2018) · Gut · doi:10.1136/gutjnl-2017-315866 · Cited by 384 · see citing works
ESPEN guideline on Clinical Nutrition in inflammatory bowel disease
Bischoff, S. C., Bager, P., Escher, J. C., Forbes, A., Hébuterne, X., Hvas, C. L., Joly, F., Kłęk, S., Krznarić, Ž., Ockenga, J., et al. (2023) · Clinical Nutrition · doi:10.1016/j.clnu.2022.12.004 · Cited by 399 · see citing works
“…pediatric gastroenterology and nutrition, ECCO and ESPGHAN, have advised on the possible use of partial maintenance EN in patients with very mild disease or low risk of relapse, preferring polymeric feeds, with elemental feeds being advised only in the case of allergy to cow's milk proteins [406].”
BackgroundESPEN practical guideline: Clinical Nutrition in inflammatory bowel disease
Bischoff, S. C., Escher, J., Hébuterne, X., Kłęk, S., Krznaric, Z., Schneider, S., Shamir, R., Stardelova, K., Wierdsma, N., Wiskin, A. E., et al. (2020) · Clinical Nutrition · doi:10.1016/j.clnu.2019.11.002 · Cited by 351 · see citing works
“The ECCO-ESPGHAN guidelines on the medical management of pediatric CD advise oral administration of folate in patients on methotrexate, 5 mg once weekly 24e72 h after the methotrexate, or 1 mg daily for five days per week [181].”
BackgroundMethodSvolos, V., Hansen, R., Nichols, B., Quince, C., Ijaz, U. Z., Papadopoulou, R., Edwards, C. A., Watson, D. G., Alghamdi, A., Brejnrod, A., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.12.002 · Cited by 320 · see citing works
Inflammation and malnutrition in inflammatory bowel disease
Massironi, S., Viganò, C., Palermo, A., Pirola, L., Mulinacci, G., Allocca, M., Peyrin‐Biroulet, L., & Danese, S. (2023) · The Lancet. Gastroenterology & hepatology · doi:10.1016/s2468-1253(23)00011-0 · Cited by 320 · see citing works
Enteral nutritional therapy for induction of remission in Crohn's disease
Narula, N., Dhillon, A. S., Zhang, D., Sherlock, M. E., Tondeur, M. C., & Zachos, M. (2018) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd000542.pub3 · Cited by 306 · see citing works
The metabolic nature of inflammatory bowel diseases
Adolph, T. E., Meyer, M., Schwärzler, J., Mayr, L., Grabherr, F., & Tilg, H. (2022) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-022-00658-y · Cited by 305 · see citing works
Agrawal, M., Spencer, E. A., Colombel, J., & Ungaro, R. C. (2021) · Gastroenterology · doi:10.1053/j.gastro.2021.04.063 · Cited by 272 · see citing works
Fecal Microbiota in Pediatric Inflammatory Bowel Disease and Its Relation to Inflammation
Kolho, K., Korpela, K., Jaakkola, T., Pichai, M. V. A., Zoetendal, E. G., Salonen, A., & de Vos, W. M. (2015) · The American Journal of Gastroenterology · doi:10.1038/ajg.2015.149 · Cited by 244 · see citing works
Deneau, M. R., El‐Matary, W., Valentino, P. L., Abdou, R., Alqoaer, K., Amin, M., Amir, A. Z., Auth, M., Bazerbachi, F., Broderick, A., et al. (2017) · Hepatology · doi:10.1002/hep.29204 · Cited by 230 · see citing works
“Physicians generally followed established practice guidelines for these diseases.((11-13)) Patients with PSC generally did not receive immunosuppression outside of that mandated by coexisting IBD, AIH, or other immune-mediated diseases.”
MethodSelf-citationBile Acid–Gut Microbiota Axis in Inflammatory Bowel Disease: From Bench to Bedside
Yang, M., Gu, Y., Li, L., Liu, T., Song, X., Sun, Y., Cao, X., Wang, B., Jiang, K., & Cao, H. (2021) · Nutrients · doi:10.3390/nu13093143 · Cited by 216 · see citing works
Boneh, R. S., Shabat, C. S., Yanai, H. A., Chermesh, I., Avraham, S. B., Boaz, M., & Levine, A. (2017) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjx071 · Cited by 205 · see citing works
Wang, S., Martins, R., Sullivan, M. C., Friedman, E. S., Misic, A. M., El‐Fahmawi, A., Martinis, E. C. P. D., O’Brien, K. M., Chen, Y., Bradley, C. W., et al. (2019) · Microbiome · doi:10.1186/s40168-019-0740-4 · Cited by 200 · see citing works
Miele, E., Shamir, R., Aloi, M., Assa, A., Braegger, C., Bronsky, J., de Ridder, L., Escher, J. C., Hojsak, I., Kolaček, S., et al. (2018) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001896 · Cited by 191 · see citing works
Abramson, A., Frederiksen, M. R., Vegge, A., Jensen, B., Poulsen, M. H., Mouridsen, B., Jespersen, M. O., Kirk, R. K., Windum, J., Hubálek, F., et al. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-01024-0 · Cited by 186 · see citing works
Wasilewski, A., Zielińska, M., Storr, M., & Fichna, J. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000364 · Cited by 186 · see citing works
“To date, the role of VSL#3 in the treatment of CD has not been investigated.(52,53) However, VSL#3 was found to increase the variety of bacteria species in GIT of patients with IBD.”
BackgroundBryant, R. V., Friedman, A. B., Wright, E. K., Taylor, K. M., Begun, J., Maconi, G., Maaser, C., Novak, K. L., Kucharzik, T. F., Atkinson, N. S. S., et al. (2018) · Gut · doi:10.1136/gutjnl-2017-315655 · Cited by 179 · see citing works
Review article: the gut microbiome in inflammatory bowel disease—avenues for microbial management
Mcilroy, J. R., Ianiro, G., Mukhopadhya, I., Hansen, R., & Hold, G. L. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.14384 · Cited by 175 · see citing works
“The focus has therefore fallen on enteral nutrition in CD, with recognition that exclusive liquid diets for periods of 6- 8 weeks are highly effective in inducing remission in ~80% of paedi- atric patients with active luminal CD, leading to exclusive enteral nutrition being promoted as first-line therapy in paediatric…”
BackgroundThe Role of Environmental Factors in the Pathogenesis of Inflammatory Bowel Diseases
Shouval, D. S., & Rufo, P. A. (2017) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2017.2571 · Cited by 174 · see citing works
Swaminath, A. C., Feathers, A., Ananthakrishnan, A. N., Falzon, L., & Ferry, S. (2017) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.14253 · Cited by 175 · see citing works
“Corticosteroids are the most commonly used medication to induce remission in the USA,(4) but can pose particular risks in a paediatric population including: growth retardation, low bone mineral density, adrenal suppression and body image dissatisfaction.(5) As an alternative, gastroenterologists sometimes elect to use…”
BackgroundWang, Y., Gao, X., Ghozlane, A., Hu, H., Li, X., Xiao, Y., Li, D., Yu, G., & Zhang, T. (2017) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjx153 · Cited by 173 · see citing works
Lee, D. Y., Baldassano, R. N., Otley, A. R., Albenberg, L. G., Griffiths, A. M., Compher, C. W., Chen, E. Z., Li, H., Gilroy, E. D., Nessel, L. A., et al. (2015) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000426 · Cited by 170 · see citing works
“Although immunosuppressive therapies, such as anti-tumor necrosis factor alpha (anti-TNF) therapy, are the primary treatment of pediatric CD in the United States, enteral nutritional (EN) therapy is commonly used to induce remission in children from Canada, Australia, Japan, and Europe.(4,5) Both exclusive enteral nut…”
BackgroundAleksandrova, K., Romero-Mosquera, B., & Hernández, V. (2017) · Nutrients · doi:10.3390/nu9090962 · Cited by 169 · see citing works
Olén, O., Askling, J., Sachs, M. C., Frumento, P., Neovius, M., Smedby, K., Ekbom, A., Malmborg, P., & Ludvigsson, J. F. (2017) · BMJ · doi:10.1136/bmj.j3951 · Cited by 159 · see citing works
Diagnosis and management of inflammatory bowel disease in children
Oliveira, S. B. D. C., & Monteiro, I. M. (2017) · BMJ · doi:10.1136/bmj.j2083 · Cited by 152 · see citing works
The Role of Carrageenan and Carboxymethylcellulose in the Development of Intestinal Inflammation
Martino, J. V., Limbergen, J. V., & Cahill, L. E. (2017) · Frontiers in Pediatrics · doi:10.3389/fped.2017.00096 · Cited by 150 · see citing works
“Exclusive enteral nutrition (EEN) is recommended as a firstline therapy in pediatric CD and involves the use of a liquid formula diet as the only source of nutrition over several weeks (8, 60).”
BackgroundThe Impact of Inflammatory Bowel Disease in Canada 2018: Children and Adolescents with IBD
Carroll, M. W., Kuenzig, M. E., Mack, D. R., Otley, A. R., Griffiths, A. M., Kaplan, G. G., Bernstein, C. N., Bitton, A., Murthy, S. K., Nguyen, G. C., et al. (2018) · Journal of the Canadian Association of Gastroenterology · doi:10.1093/jcag/gwy056 · Cited by 150 · see citing works
“Specific to children with IBD is the ability to use exclusive enteral nutrition (EEN) as an alternative to corticosteroids in Crohn’s disease to induce remission (54).”
BackgroundDiet therapy for inflammatory bowel diseases: The established and the new
Durchschein, F., Petritsch, W., & Hammer, H. F. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i7.2179 · Cited by 146 · see citing works
Exclusive enteral nutrition in Crohn's disease: Evidence and practicalities
Ashton, J. J., Gavin, J., & Beattie, R. M. (2018) · Clinical Nutrition · doi:10.1016/j.clnu.2018.01.020 · Cited by 148 · see citing works
The Role of Diet and Gut Microbiota in Regulating Gastrointestinal and Inflammatory Disease
Gill, P. A., Inniss, S., Kumagai, T., Rahman, F. Z., & Smith, A. M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.866059 · Cited by 149 · see citing works
Mechanisms of Pediatric Inflammatory Bowel Disease
Peloquin, J. M., Goel, G., Villablanca, E. J., & Xavier, R. J. (2016) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032414-112151 · Cited by 139 · see citing works
Pigneur, B., Lepage, P., Mondot, S., Schmitz, J., Goulet, O., Dore, J. M., & Ruemmele, F. M. (2018) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjy207 · Cited by 139 · see citing works
Dietary management of adults with IBD — the emerging role of dietary therapy
Fitzpatrick, J. A., Melton, S. L., Yao, C. K., Gibson, P. R., & Halmos, E. P. (2022) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-022-00619-5 · Cited by 138 · see citing works
Sieczkowska, J., Jarzębicka, D., Banaszkiewicz, A., Plocek, A., Gawrońska, A., Toporowska‐Kowalska, E., Oracz, G., Meglicka, M., & Kierkuś, J. (2015) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjv233 · Cited by 136 · see citing works
Jongsma, M., Aardoom, M. A., Cozijnsen, M. A., van Pieterson, M., de Meij, T. G. J., Groeneweg, M., Norbruis, O. F., Wolters, V. M., van Wering, H. M., Hojsak, I., et al. (2020) · Gut · doi:10.1136/gutjnl-2020-322339 · Cited by 134 · see citing works
Pediatric Inflammatory Bowel Disease
Bouhuys, M., Lexmond, W. S., & van Rheenen, P. F. (2022) · PEDIATRICS · doi:10.1542/peds.2022-058037 · Cited by 136 · see citing works
The Role of Diet in the Pathogenesis and Management of Inflammatory Bowel Disease: A Review
Wark, G., Samocha‐Bonet, D., Ghaly, S., & Danta, M. (2020) · Nutrients · doi:10.3390/nu13010135 · Cited by 127 · see citing works
“In the paediatric setting, active disease has the ability to impact upon growth potential as well as pubertal and emotional development [3].”
BackgroundProbiotics, Prebiotics and Synbiotics in Inflammatory Bowel Diseases
Akutko, K., & Stawarski, A. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10112466 · Cited by 125 · see citing works
“Taking into account that so far no statistically significant benefits of using probiotics to induce or maintain remission compared to standard therapy have been found, probiotics should not be used in the treatment of patients with CD [44,59,60].”
BackgroundFatty acids and lipid mediators in inflammatory bowel disease: from mechanism to treatment
Yan, D., Ye, S., He, Y., Wang, S., Xiao, Y., Xiang, X., Deng, M., Luo, W., Chen, X., & Wang, X. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1286667 · Cited by 129 · see citing works
The Impact of Exclusive Enteral Nutrition (EEN) on the Gut Microbiome in Crohn’s Disease: A Review
MacLellan, A. L., Connors, J., Grant, S., Cahill, L. E., Langille, M. G. I., & Limbergen, J. V. (2017) · Nutrients · doi:10.3390/nu9050447 · Cited by 118 · see citing works
“Because adults struggle more with compliance to EEN, studies demonstrating the efficacy of EEN in adult CD patients have been less conclusive [12,16].”
MethodResultYu, Y., Chen, K., & Chen, J. (2019) · World Journal of Pediatrics · doi:10.1007/s12519-018-0204-0 · Cited by 123 · see citing works
Brooks, A. J., Smith, P. J., Cohen, R., COLLINS, P. D., Douds, A. C., Forbes, V., Gaya, D. R., Johnston, B. T., McKiernan, P. J., Murray, C. D., et al. (2017) · Gut · doi:10.1136/gutjnl-2016-313000 · Cited by 118 · see citing works
Campmans-Kuijpers, M. J. E., & Dijkstra, G. D. H. (2021) · Nutrients · doi:10.3390/nu13041067 · Cited by 116 · see citing works
“is currently the primary induction treatment in paediatric CD; partly because steroid therapy has adverse effects and growth has to be maintained in children [5,6].”
BackgroundEndoscopy in Pediatric Inflammatory Bowel Disease
Oliva, S., Thomson, M. A., de Ridder, L., de Carpi, J. M., Biervliet, S. V., Braegger, C., Dias, J. A., Kolaček, S., Miele, E., Buderus, S., et al. (2018) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000002092 · Cited by 113 · see citing works
“It is important to note that for the purpose of MH, a risk to increase the frequency of endoscopic procedures may exist, making it likely that pediatric IBD patients will undergo multiple episodes of GA (61).”
BackgroundDiederen, K., Li, J. V., Donachie, G. E., de Meij, T. G. J., de Waart, D. R., Hakvoort, T. B. M., Kindermann, A., Wagner, J., Auyeung, V. P. W., Velde, A. A. T., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-75306-z · Cited by 113 · see citing works
Boneh, R. S., Levine, A., Lomer, M. C. E., Wierdsma, N., Allan, P., Fiorino, G., Gatti, S., Jonkers, D. M. A. E., Kierkuś, J., Katsanos, K. H., et al. (2017) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjx109 · Cited by 112 · see citing works
Ungaro, R. C., Aggarwal, S., Topaloglu, Ö., Lee, W., Clark, R., & Colombel, J. (2020) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15685 · Cited by 111 · see citing works
“Bolia, J Pediatr Gastroenterol Nutr, 2017a ,56 Observational Paediatric 73 1 y IFX w/o IM in early versus nonearly CD Time interval between diagnosis and introduction of IFX (mon): Loss of response group: 28 (4-90); No loss of response group: 12.”
BackgroundUse of thiopurines in inflammatory bowel disease: an update
Singh, A., Mahajan, R., Kedia, S., Dutta, A. K., Anand, A., Bernstein, C. N., Desai, D., Pai, C. G., Makharia, G. K., Tevethia, H. V., et al. (2021) · Intestinal Research · doi:10.5217/ir.2020.00155 · Cited by 111 · see citing works
A Review on the Use of Anti-TNF in Children and Adolescents with Inflammatory Bowel Disease
Aardoom, M. A., Veereman, G., & de Ridder, L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20102529 · Cited by 109 · see citing works
“In addition, based on consensus, the top-down strategy should be considered in children with CD suffering from extensive disease, significant growth retardation, deep ulcerations in the colon seen at endoscopy, severe osteoporosis and stenosing or penetrating disease at diagnosis [12].”
BackgroundResultInfluentialThe Use of Fecal Calprotectin Testing in Paediatric Disorders
Ribes‐Koninckx, C., Donat, E., Benninga, M. A., Broekaert, I. J., Gottrand, F., Kolho, K., Lionetti, P., Miele, E., Orel, R., Papadopoulou, A., et al. (2021) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000003046 · Cited by 109 · see citing works
Surgical Management of Crohn Disease in Children
Dias, J. A., Kolaček, S., Turner, D., Pærregaard, A., Rintala, R. J., Afzal, N. A., Karolewska‐Bochenek, K., Bronský, J., Chong, S. K. F., Fell, J. M. E., et al. (2017) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001562 · Cited by 102 · see citing works
The role of diet in the prevention and treatment of Inflammatory Bowel Diseases.
Reddavide, R., Rotolo, O., Caruso, M. G., Stasi, E., Notarnicola, M., Miraglia, C., Nouvenne, A., Meschi, T., Angelis, G. L. D., Mario, F. D., et al. (2018) · Acta bio-medica dell'Ateneo parmense/Acta biomedica · doi:10.23750/abm.v89i9-s.7952 · Cited by 100 · see citing works
Nutritional Treatment in Crohn’s Disease
Caio, G., Lungaro, L., Caputo, F., Zoli, E., Giancola, F., Chiarioni, G., GIORGIO, R. D., & Zoli, G. (2021) · Nutrients · doi:10.3390/nu13051628 · Cited by 103 · see citing works
“In the attempt to make the EEN more palatable, a partial EEN has been proposed, where EEN has been combined with ad libitum solid food; however, this approach did not guarantee a similar rate of remission as total EEN [1,57].”
BackgroundRole of Diet in Inflammatory Bowel Disease
Ruemmele, F. M. (2016) · Annals of Nutrition and Metabolism · doi:10.1159/000445392 · Cited by 97 · see citing works
Perioperative dietary therapy in inflammatory bowel disease.
Adamina, M., Gerasimidis, K., Sigall-Boneh, R., Zmora, O., van Overstraeten, A. D. B., Campmans-Kuijpers, M., Ellul, P., Katsanos, K., Kotze, P., Noor, N., et al. (2019) · Journal of Crohn's & Colitis · doi:10.1093/ecco-jcc/jjz160 · Cited by 86 · see citing works
Nutrition in Patients with Inflammatory Bowel Diseases: A Narrative Review
Roncoroni, L., Gori, R., Elli, L., Tontini, G. E., Doneda, L., Norsa, L., Cuomo, M., Lombardo, V., Scricciolo, A., Caprioli, F., et al. (2022) · Nutrients · doi:10.3390/nu14040751 · Cited by 99 · see citing works
“Due to its excellent safety profile and its equipotential to corticosteroids in inducing remission, the European Crohn’s and Colitis Organization (ECCO) and the ESPGHAN recommend EEN as the first-line therapy for mild-to-moderate pediatric CD to induce remission, both in the first flare-up and during relapses of sympt…”
BackgroundClinical Use and Molecular Action of Corticosteroids in the Pediatric Age
Ferrara, G., Petrillo, M. G., Giani, T., Marrani, E., Filippeschi, C., Oranges, T., Simonini, G., & Cimaz, R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020444 · Cited by 97 · see citing works
“In distal colonic disease, steroid-based enemas may be used, as in adult patients [113].”
Logan, M., Gkikas, K., Svolos, V., Nichols, B., Milling, S. W. F., Gaya, D. R., Seenan, J. P., MacDonald, J. C., Hansen, R., Ijaz, U. Z., et al. (2020) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15695 · Cited by 95 · see citing works
Inflammatory Bowel Disease in Pediatric Patients
Buderus, S., Scholz, D., Behrens, R., Claßen, M., de Laffolie, J., Keller, K., Zimmer, K., & Koletzko, S. (2015) · Deutsches Ärzteblatt international · doi:10.3238/arztebl.2015.0121 · Cited by 94 · see citing works
“Their use is controversial according to the new guidelines and is only recommended for mild cases (27).”
BackgroundBoneh, R. S., Limbergen, J. V., Wine, E., Assa, A., Shaoul, R. R., Millman, P. N., Cohen, S., Kori, M., Peleg, S., On, A., et al. (2020) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2020.04.006 · Cited by 94 · see citing works
Infliximab in young paediatric IBD patients: it is all about the dosing
Jongsma, M., Winter, D. A., Huynh, H. Q., Norsa, L., Hussey, S., Kolho, K., Bronský, J., Assa, A., Cohen, S., Lev‐Tzion, R., et al. (2020) · European Journal of Pediatrics · doi:10.1007/s00431-020-03750-0 · Cited by 93 · see citing works
Dunn, K. A., Moore-Connors, J., MacIntyre, B., Stadnyk, A. W., Thomas, N. A., Noble, A. J., Mahdi, G., Rashid, M., Otley, A. R., Bielawski, J. P., et al. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000956 · Cited by 93 · see citing works
Ghiboub, M., Verburgt, C. M., Sovran, B., Benninga, M. A., de Jonge, W. J., & Limbergen, J. V. (2020) · Nutrients · doi:10.3390/nu12092846 · Cited by 94 · see citing works
The Genetics of Inflammatory Bowel Disease
Hadad, J. E., Schreiner, P., Vavricka, S. R., & Greuter, T. (2023) · Molecular Diagnosis & Therapy · doi:10.1007/s40291-023-00678-7 · Cited by 96 · see citing works
“Pre-treatment genotyping is endorsed by the European Crohn’s and Colitis Organisation guidelines [76], but does not substitute monitoring of drug toxicity under treatment.”
MethodInflammatory Bowel Disease: The Classic Gastrointestinal Autoimmune Disease
Kaistha, A., & Levine, J. J. (2014) · Current problems in pediatric and adolescent health care · doi:10.1016/j.cppeds.2014.10.003 · Cited by 89 · see citing works
“4 g/day.(21,22) A purine analog, 6-MP, impairs lymphocyte proliferation by inhibiting DNA synthesis.”
InfluentialValdés-Mas, R., Leshem, A., Zheng, D., Cohen, Y., Kern, L., Zmora, N., He, Y., Katina, C., Eliyahu-Miller, S., Yosef-Hevroni, T., et al. (2025) · Cell · doi:10.1016/j.cell.2024.12.016 · Cited by 89 · see citing works
Cohen-Dolev, N., Sładek, M., Hussey, S., Turner, D., Veres, G., Koletzko, S., de Carpi, J. M., Staiano, A., Shaoul, R. R., Lionetti, P., et al. (2017) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjx150 · Cited by 88 · see citing works
Intestinal Behçet and Crohn’s disease: two sides of the same coin
Valenti, S., Gallizzi, R., Vivo, D. D., & Romano, C. (2017) · Pediatric Rheumatology · doi:10.1186/s12969-017-0162-4 · Cited by 88 · see citing works
Efficacy of exclusive enteral nutrition in complicated Crohn’s disease
Yang, Q., Gao, X., Chen, H., Li, M., Wu, X., Zhi, M., Lan, P., & Hu, P. (2017) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.2017.1335770 · Cited by 86 · see citing works
“Exclusive enteral nutrition (EEN) has been recommended as an alternative strategy to induce disease remission in CD patients [3,4].”
BackgroundKakuta, Y., Kinouchi, Y., & Shimosegawa, T. (2017) · Journal of Gastroenterology · doi:10.1007/s00535-017-1416-0 · Cited by 83 · see citing works
Logan, M., Clark, C., Ijaz, U. Z., Gervais, L., Duncan, H., Garrick, V., Curtis, L., Buchanan, E., Cardigan, T., Armstrong, L., et al. (2019) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.15425 · Cited by 82 · see citing works
Beres, N. J., Szabó, D., Kocsis, D., Szűcs, D., Kiss, Z., Müller, K. E., Lendvai, G., Kiss, A., Arató, A., Sziksz, E., et al. (2016) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000687 · Cited by 81 · see citing works
“This complex biological role explains the efficacy of anti-TNF-a therapy, representing a significant therapeutic tool in the management of the hard-to-treat patients, showing a good clinical outcome and leading to mucosal healing.(15) Recent evidence suggests that epigenetic factors are also potent modulators of IBD.”
BackgroundAntibiotics in IBD: Still a Role in the Biological Era?
Ledder, O., & Turner, D. (2018) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izy067 · Cited by 81 · see citing works
WFUMB Position Paper. Learning Gastrointestinal Ultrasound: Theory and Practice
Atkinson, N. S. S., Bryant, R. V., Dong, Y., Maaser, C., Kucharzik, T. F., Maconi, G., Asthana, A. K., Blaivas, M., Goudie, A., Gilja, O. H., et al. (2016) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2016.08.026 · Cited by 80 · see citing works
“ECCO affirms that the diagnosis of IBD is confirmed by clinical evaluation and a combination of other investigation modalities (Dignass et al. 2012; Ruemmele et al. 2014; Turner et al. 2012; van Assche et al. 2010).”
Clock Gene Disruption Is an Initial Manifestation of Inflammatory Bowel Diseases
Weintraub, Y., Cohen, S., Chapnik, N., Ben‐Tov, A., Yerushalmy‐Feler, A., Dotan, I., Tauman, R., & Froy, O. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2019.04.013 · Cited by 79 · see citing works
Connors, J., Dunn, K. A., Allott, J., Bandsma, R., Rashid, M., Otley, A. R., Bielawski, J. P., & Limbergen, J. V. (2019) · The ISME Journal · doi:10.1038/s41396-019-0560-3 · Cited by 79 · see citing works
Inflammatory Bowel Disease in Childhood and Adolescence
Däbritz, J., Gerner, P., Enninger, A., Claßen, M., & Radke, M. H. (2017) · Deutsches Ärzteblatt international · doi:10.3238/arztebl.2017.0331 · Cited by 79 · see citing works
“Ruemmele FM, Veres G, Kolho KL, et al.: Consensus guidelines of ECCO/ESPGHAN on the medical management of pediatric Crohn‘s disease.”
BackgroundMethodInfluentialCozijnsen, M. A., Shoham, A. B., Kang, B., Choe, B., Choe, Y. H., Jongsma, M., Russell, R. K., Ruemmele, F. M., Escher, J. C., de Ridder, L., et al. (2019) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2019.04.012 · Cited by 78 · see citing works
Sturm, A., Stallmach, A., Atreya, R. N., Bettenworth, D., Bokemeyer, B., Dignass, A. U., Ehehalt, R., Germer, C. T., Grunert, P., Helwig, U., et al. (2022) · Zeitschrift für Gastroenterologie · doi:10.1055/a-1713-3941 · Cited by 77 · see citing works
Microbiota in Inflammatory Bowel Disease Pathogenesis and Therapy
Serban, D. E. (2015) · Nutrition in Clinical Practice · doi:10.1177/0884533615606898 · Cited by 77 · see citing works
“EEN is recommended as first-line therapy to induce remission in children with active luminal CD, over 6–8 weeks, having a safety profile.(41,144) EEN is not useful in UC.”
Wall, C. L., Gearry, R. B., & Day, A. S. (2017) · Inflammatory Intestinal Diseases · doi:10.1159/000489630 · Cited by 76 · see citing works
Sahu, P., Kedia, S., Vuyyuru, S. K., Bajaj, A., Markandey, M., Singh, N., Singh, M. K., Kante, B., Kumar, P., Ranjan, M. K., et al. (2021) · Alimentary Pharmacology & Therapeutics · doi:10.1111/apt.16249 · Cited by 76 · see citing works
“Duration of hospitalisation (days) 10 (8-17) 13 (8-24) 0.”
BackgroundMethodInfluentialNovel approaches in IBD therapy: targeting the gut microbiota-bile acid axis
Pan, Y., Zhang, H., Li, M., He, T., Guo, S., Zhu, L., Tan, J., & Wang, B. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2356284 · Cited by 78 · see citing works
“159,160 EEN therapy is based on direct anti-inflammatory effects, which improve the composition of gut microbiota, reduce barrier permeability, and modulate the immune system.”
BackgroundMack, D. R., Benchimol, E. I., Critch, J., deBruyn, J. C. C., Tse, F., Moayyedi, P., Church, P. C., Deslandres, C., El‐Matary, W., Huynh, H. Q., et al. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.03.022 · Cited by 74 · see citing works
Nutritional Interventions in the Patient with Inflammatory Bowel Disease
Limketkai, B. N., Wolf, A., & Parian, A. M. (2017) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2017.09.007 · Cited by 74 · see citing works
Targeting mucosal healing in Crohn’s disease: what the clinician needs to know
Klenske, E., Bojarski, C., Waldner, M. J., Räth, T., Neurath, M. F., & Atreya, R. N. (2019) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756284819856865 · Cited by 73 · see citing works
Swedish Inflammatory Bowel Disease Register (SWIBREG) – a nationwide quality register
Ludvigsson, J. F., Andersson, M., Bengtsson, J., Eberhardson, M., Fagerberg, U. L., Grip, O., Halfvarson, J., Hjortswang, H., Jäghult, S., Karling, P., et al. (2019) · Scandinavian Journal of Gastroenterology · doi:10.1080/00365521.2019.1660799 · Cited by 74 · see citing works
“EEN is highly effective in newly diagnosed paediatric CD [52].”
BackgroundInfluence of Environmental Factors in the Development and Outcomes of Inflammatory Bowel Disease.
Vedamurthy, A., & Ananthakrishnan, A. N. (2019) · Europe PMC (PubMed Central) · Cited by 73 · see citing works
Perianal Crohn Disease in a Large Multicenter Pediatric Collaborative
Adler, J., Dong, S., Eder, S. J., Dombkowski, K. J., & System, I. P. I. L. H. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001447 · Cited by 73 · see citing works
Personalising medicine in inflammatory bowel disease—current and future perspectives
Ashton, J. J., Mossotto, E., Ennis, S., & Beattie, R. M. (2019) · Translational Pediatrics · doi:10.21037/tp.2018.12.03 · Cited by 72 · see citing works
“What is clear is that interpretation of results must account for the definition of a therapeutic endpoint as this is likely to be highly variable, despite ECCO/ESPGHAN published guidance (2,3).”
BackgroundInfluentialAdherence to Oral Maintenance Treatment in Adolescents with Inflammatory Bowel Disease
Spekhorst, L. M., Hummel, T. Z., Benninga, M. A., van Rheenen, P. F., & Kindermann, A. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000924 · Cited by 71 · see citing works
“IBD management involves multiple medications prescribed in the first instance (1,2).”
BackgroundEnteral Nutrition in the Management of Pediatric and Adult Crohn’s Disease
Hansen, T. M., & Duerksen, D. R. (2018) · Nutrients · doi:10.3390/nu10050537 · Cited by 71 · see citing works
“Enteral nutrition has shown efficacy in controlling disease activity, maintaining clinical remission, and addressing malnutrition in pediatric and adult CD patients with active disease [4,5].”
BackgroundDamas, O. M., Garces, L. C., & Abreu, M. T. (2019) · Current Treatment Options in Gastroenterology · doi:10.1007/s11938-019-00231-8 · Cited by 71 · see citing works
- Authors
- Ruemmele, F. M., Veres, G., Kolho, K. L., Griffiths, A., Levine, A., Escher, J. C., Amil Dias, J., Barabino, A., Braegger, C. P., Bronsky, J., Buderus, S., Martín-de-Carpi, J., De Ridder, L., Fagerberg, U. L., Hugot, J. P., Kierkus, J., Kolacek, S., Koletzko, S., Lionetti, P., Miele, E., Navas López, V. M., Paerregaard, A., Russell, R. K., Serban, D. E., Shaoul, R., Van Rheenen, P., Veereman, G., Weiss, B., Wilson, D., Dignass, A., Eliakim, A., Winter, H., & Turner, D.
- Affiliations
- Hôpital Necker-Enfants Malades (FR)
- Semmelweis University (HU)
- Helsinki University Hospital (FI)
- University of Toronto (CA)
- Tel Aviv University (IL)
- Erasmus MC (NL)
- Unit of Paediatric Gastroenterology, Hospital S. João, A Hernani Monteiro, 4202-451, Porto, Portugal
- Istituto Giannina Gaslini (IT)
- University Children's Hospital Zurich (CH)
- Department of Pediatrics, University Hospital Motol, Uvalu 84, 150 06 Prague, Czech Republic
- St. Marien-Hospital Bonn (DE)
- Department of Paediatric Gastroenterolgoy, Hepatology and Nutrition, Hospital Sant Joan de Déu, Paseo Sant Joan de Déu 2, 08950 Barcelona, Spain
- Department of Paediatric Gastroenterology, Erasmus Medical Center, Wytemaweg 80, 3015 CN Rotterdam, Netherlands
- Karolinska Institutet (SE)
- Sorbonne Paris Cité (FR)
- Department of Gastroenterology, Hepatology and Feeding Disorders, Instytut Pomnik Centrum Zdrowia Dziecka, Ul. Dzieci Polskich 20, 04-730 Warsaw, Poland
- Department of Paediatric Gastroenterology, Children's Hospital, University of Zagreb Medical School, Klaićeva 16, 10000 Zagreb, Croatia
- Department of Paediatric Gastroenterology, Dr. von Hauner Children's Hospital, Lindwurmstr. 4, 80337 Munich, Germany
- Meyer Children's Hospital (IT)
- University of Naples Federico II (IT)
- Paediatric Gastroenterology and Nutrition Unit, Hospital Materno Infantil, Avda. Arroyo de los Ángeles s/n, 29009 Málaga, Spain
- Department of Paediatrics 460, Hvidovre University Hospital, Kettegård Allé 30, 2650 Hvidovre, Denmark
- Department of Paediatric Gastroenterology, Yorkhill Hospital, Dalnair Street, Glasgow G3 8SJ, United Kingdom
- Iuliu Hațieganu University of Medicine and Pharmacy (RO)
- Rambam Health Care Campus (IL)
- Department of Paediatric Gastroenterology, Hepatology and Nutrition, University Medical Center Groningen, P.O. Box 30001, 9700 RB Groningen, Netherlands
- Queen Fabiola Children's University Hospital (BE)
- Sheba Medical Center (IL)
- Royal Hospital for Sick Children (GB)
- Agaplesion Markus Hospital (DE)
- Massachusetts General Hospital (US)
- Hebrew University of Jerusalem (IL)
- Corresponding author
- Ruemmele, F.M.
- ORCID
- Venue
- Journal of Crohn s and Colitis
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-10-01
- Volume
- 8
- Issue
- 10
- Pages
- 1179-1207
- ISSN
- 1873-9946 (ISSN-L)
- 1876-4479
- OpenAlex
- W2135936774
- Cited by
- 1,083
- References
- 293
- Citations by year
- 2026: 61 · 2025: 60 · 2024: 71 · 2023: 97 · 2022: 83 · 2021: 123 · 2020: 117 · 2019: 136 · 2018: 92 · 2017: 122 · 2016: 61 · 2015: 52 · 2014: 5 · 2012: 2
- FWCI
- 52.41
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Crohn s and Colitis (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- BOA (University of Milano-Bicocca) (submittedVersion, cc-by-nc-nd)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion)
- Florence Research (University of Florence) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion)
- VUBIR (Vrije Universiteit Brussel) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Ophthalmology › Ocular Diseases and Behçet’s Syndrome
- Health Sciences › Medicine › Surgery › Anorectal Disease Treatments and Outcomes
- Keywords
- pediatric Crohn's disease, medical management
- MeSH terms
- Adalimumab, Infliximab, Adolescent, Adrenal Cortex Hormones, Algorithms, Aminosalicylic Acids, Anti-Inflammatory Agents, Non-Steroidal, Anti-Bacterial Agents, Antibodies, Monoclonal, Azathioprine, Child, Crohn Disease, Enteral Nutrition, Humans, Immunosuppressive Agents, Methotrexate, Remission Induction, Thalidomide, Tumor Necrosis Factor-alpha, Mercaptopurine, Maintenance Chemotherapy, Antibodies, Monoclonal, Humanized
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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