Tom 15, Nr 1 (2023)
Artykuł przeglądowy
Opublikowany online: 2024-05-28
Wyświetlenia strony
76
Wyświetlenia/pobrania artykułu
6
Monitorowanie pacjentów z czynną chorobą zapalną jelit
DOI: 10.5603/gek.100659
Gastroenterologia Kliniczna 2023;15(1):52-69.
Streszczenie
W erze leczenia prowadzonego do uzyskania celu terapeutycznego coraz większego znaczenia nabiera ścisłe monitorowanie pacjentów z chorobą zapalną jelit (IBD). Nie można pomijać parametrów skuteczności leczenia ocenianych przez pacjenta (PROM), jednak ich ograniczone związek z parametrami biochemicznymi, histologicznymi i endoskopowymi podkreśla potrzebę opracowania dodatkowych strategii monitorowania. Remisja endoskopowa i histologiczna wiąże się z lepszymi wynikami długoterminowymi, ale wymaga bardziej inwazyjnych metod oceny. W związku z tym coraz bardziej istotne stają się nieinwazyjne metody monitorowania, a coraz więcej dowodów wskazuje na dodatkową wartość kliniczną oceny przezściennej, zarówno u pacjentów z chorobą Leśniowskiego-Crohna, jak i wrzodziejącym zapaleniem jelita grubego. W niniejszym przeglądzie przedstawiono wiele celów terapeutycznych w leczeniu pacjentów z IBD, koncentrując się w szczególności na coraz większym znaczeniu ultrasonografii jelit. Zaproponowano też możliwy algorytm monitorowania pacjentów z IBD w codziennej praktyce klinicznej i wskazano obszary, które należy uwzględnić w przyszłych badaniach dotyczących strategii monitorowania pacjentów z IBD.
Słowa kluczowe: monitorowanieultrasonografia jelitchoroba zapalna jelit (IBD)enterografia rezonansu magnetycznego (MRE)biomarkergojenie przezściennegojenie błony śluzowej (MH)remisja endoskopowa (ER)
Referencje
- Khanna R, Zou G, D'Haens G, et al. A retrospective analysis: the development of patient reported outcome measures for the assessment of Crohn's disease activity. Aliment Pharmacol Ther. 2015; 41(1): 77–86.
- Arias MT, Vande Casteele N, Vermeire S, et al. A panel to predict long-term outcome of infliximab therapy for patients with ulcerative colitis. Clin Gastroenterol Hepatol. 2015; 13(3): 531–538.
- Dubinsky MC, Newton L, Delbecque L, et al. Exploring disease remission and bowel urgency severity among adults with moderate to severe ulcerative colitis: a qualitative study. Patient Relat Outcome Meas. 2022; 13: 287–300.
- Kulyk A, Shafer LA, Graff LA, et al. Urgency for bowel movements is a highly discriminatory symptom of active disease in persons with IBD (the Manitoba Living with IBD study). Aliment Pharmacol Ther. 2022; 56(11-12): 1570–1580.
- Sudhakar P, Wellens J, Verstockt B, et al. Holistic healthcare in inflammatory bowel disease: time for patient-centric approaches? Gut. 2023; 72(1): 192–204.
- Ghosh S, Louis E, Beaugerie L, et al. Development of the IBD disk: a visual self-administered tool for assessing disability in inflammatory bowel diseases. Inflamm Bowel Dis. 2017; 23(3): 333–340.
- Tadbiri S, Nachury M, Bouhnik Y, et al. GETAID-IBD-disk study group. The IBD-disk is a reliable tool to assess the daily-life burden of patients with inflammatory bowel disease. J Crohns Colitis. 2021; 15(5): 766–773.
- Turner D, Ricciuto A, Lewis A, et al. International Organization for the Study of IBD. STRIDE-II: an update on the selecting therapeutic targets in inflammatory bowel disease (STRIDE) initiative of the International Organization for the Study of IBD (IOIBD): determining therapeutic goals for treat-to-target strategies in IBD. Gastroenterology. 2021; 160(5): 1570–1583.
- Restellini S, Chao CY, Martel M, et al. Clinical parameters correlate with endoscopic activity of ulcerative colitis: a systematic review. Clin Gastroenterol Hepatol. 2019; 17(7): 1265–1275.e8.
- Munkholm P, Langholz E, Davidsen M, et al. Disease activity courses in a regional cohort of Crohn's disease patients. Scand J Gastroenterol. 1995; 30(7): 699–706.
- Colombel JF, Narula N, Peyrin-Biroulet L. Management strategies to improve outcomes of patients with inflammatory bowel diseases. Gastroenterology. 2017; 152(2): 351–361.e5.
- Naftali T, Bar-Lev Schleider L, Dotan I, et al. Cannabis induces a clinical response in patients with Crohn's disease: a prospective placebo-controlled study. Clin Gastroenterol Hepatol. 2013; 11(10): 1276–1280.e1.
- Modigliani R, Mary JY, Simon JF, et al. Groupe d'Etude Thérapeutique des Affections Inflammatoires Digestives.. Clinical, biological, and endoscopic picture of attacks of Crohn's disease. Evolution on prednisolone. Gastroenterology. 1990; 98(4): 811–818.
- Peyrin-Biroulet L, Reinisch W, Colombel JF, et al. Clinical disease activity, C-reactive protein normalisation and mucosal healing in Crohn's disease in the SONIC trial. Gut. 2014; 63(1): 88–95.
- Verstockt B, Pouillon L, Ballaux F, et al. Patient-reported outcomes and disability are associated with histological disease activity in patients with ulcerative colitis: results from the APOLLO study. J Crohns Colitis. 2023; 17(7): 1046–1054.
- Narula N, Alshahrani AA, Yuan Y, et al. Patient-Reported outcomes and endoscopic appearance of ulcerative colitis: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2019; 17(3): 411–418.e3.
- de Jong MJ, Huibregtse R, Masclee AdAM, et al. Patient-Reported outcome measures for use in clinical trials and clinical practice in inflammatory bowel diseases: a systematic review. Clin Gastroenterol Hepatol. 2018; 16(5): 648–663.e3.
- Colombel JF, Panaccione R, Bossuyt P, et al. Effect of tight control management on Crohn's disease (CALM): a multicentre, randomised, controlled phase 3 trial. Lancet. 2017; 390(10114): 2779–2789.
- Suk Danik J, Chasman DI, Cannon CP, et al. Influence of genetic variation in the C-reactive protein gene on the inflammatory response during and after acute coronary ischemia. Ann Hum Genet. 2006; 70(Pt 6): 705–716.
- Vermeire S, Van Assche G, Rutgeerts P. Laboratory markers in IBD: useful, magic, or unnecessary toys? Gut. 2006; 55(3): 426–431.
- Yoon JY, Park SJ, Hong SP, et al. Correlations of C-reactive protein levels and erythrocyte sedimentation rates with endoscopic activity indices in patients with ulcerative colitis. Dig Dis Sci. 2014; 59(4): 829–837.
- Sollelis E, Quinard RM, Bouguen G, et al. Combined evaluation of biomarkers as predictor of maintained remission in Crohn's disease. World J Gastroenterol. 2019; 25(19): 2354–2364.
- Stallmach A, Langbein C, Atreya R, et al. Vedolizumab provides clinical benefit over 1 year in patients with active inflammatory bowel disease - a prospective multicenter observational study. Aliment Pharmacol Ther. 2016; 44(11-12): 1199–1212.
- Levine A, Turner D, Pfeffer Gik T, et al. Comparison of outcomes parameters for induction of remission in new onset pediatric Crohn's disease: evaluation of the porto IBD group "growth relapse and outcomes with therapy" (GROWTH CD) study. Inflamm Bowel Dis. 2014; 20(2): 278–285.
- Cornillie F, Hanauer SB, Diamond RH, et al. Postinduction serum infliximab trough level and decrease of C-reactive protein level are associated with durable sustained response to infliximab: a retrospective analysis of the ACCENT I trial. Gut. 2014; 63(11): 1721–1727.
- Theede K, Holck S, Ibsen P, et al. Level of fecal calprotectin correlates with endoscopic and histologic inflammation and identifies patients with mucosal healing in ulcerative colitis. Clin Gastroenterol Hepatol. 2015; 13(11): 1929–19236.e1.
- Schoepfer AM, Beglinger C, Straumann A, et al. Fecal calprotectin correlates more closely with the Simple Endoscopic Score for Crohn's disease (SES-CD) than CRP, blood leukocytes, and the CDAI. Am J Gastroenterol. 2010; 105(1): 162–169.
- Schoepfer AM, Beglinger C, Straumann A, et al. Fecal calprotectin more accurately reflects endoscopic activity of ulcerative colitis than the Lichtiger Index, C-reactive protein, platelets, hemoglobin, and blood leukocytes. Inflamm Bowel Dis. 2013; 19(2): 332–341.
- D'Haens G, Ferrante M, Vermeire S, et al. Fecal calprotectin is a surrogate marker for endoscopic lesions in inflammatory bowel disease. Inflamm Bowel Dis. 2012; 18(12): 2218–2224.
- Rokkas T, Portincasa P, Koutroubakis IE. Fecal calprotectin in assessing inflammatory bowel disease endoscopic activity: a diagnostic accuracy meta-analysis. J Gastrointestin Liver Dis. 2018; 27(3): 299–306.
- Mosli MH, Zou G, Garg SK, et al. C-reactive protein, fecal calprotectin, and stool lactoferrin for detection of endoscopic activity in symptomatic inflammatory bowel disease patients: a systematic review and meta-analysis. Am J Gastroenterol. 2015; 110(6): 802–819; quiz 820.
- Gecse KB, Brandse JF, van Wilpe S, et al. Impact of disease location on fecal calprotectin levels in Crohn's disease. Scand J Gastroenterol. 2015; 50(7): 841–847.
- Buisson A, Mak WY, Andersen MJ, et al. Fecal calprotectin is highly effective to detect endoscopic ulcerations in Crohn's disease regardless of disease location. Inflamm Bowel Dis. 2021; 27(7): 1008–1016.
- Sakuraba A, Nemoto N, Hibi N, et al. Extent of disease affects the usefulness of fecal biomarkers in ulcerative colitis. BMC Gastroenterol. 2021; 21(1): 197.
- D'Amico F, Rubin DT, Kotze PG, et al. International consensus on methodological issues in standardization of fecal calprotectin measurement in inflammatory bowel diseases. United European Gastroenterol J. 2021; 9(4): 451–460.
- Heida A, Park KT, van Rheenen PF. Clinical utility of fecal calprotectin monitoring in asymptomatic patients with inflammatory bowel disease: a systematic review and practical guide. Inflamm Bowel Dis. 2017; 23(6): 894–902.
- Cozijnsen MA, Ben Shoham A, Kang B, et al. Development and validation of the mucosal inflammation noninvasive index for pediatric Crohn's disease. Clin Gastroenterol Hepatol. 2020; 18(1): 133–140.e1.
- Minderhoud IM, Steyerberg EW, van Bodegraven AdA, et al. Predicting endoscopic disease activity in Crohn's disease: a new and validated noninvasive disease activity index (the utrecht activity index). Inflamm Bowel Dis. 2015; 21(10): 2453–2459.
- Molander P, af Björkesten CG, Mustonen H, et al. Fecal calprotectin concentration predicts outcome in inflammatory bowel disease after induction therapy with TNFα blocking agents. Inflamm Bowel Dis. 2012; 18(11): 2011–2017.
- Battat R, Dulai PS, Vande Casteele N, et al. Biomarkers are associated with clinical and endoscopic outcomes with vedolizumab treatment in ulcerative colitis. Inflamm Bowel Dis. 2019; 25(2): 410–420.
- Boschetti G, Garnero P, Moussata D, et al. Accuracies of serum and fecal S100 proteins (calprotectin and calgranulin C) to predict the response to TNF antagonists in patients with Crohn's disease. Inflamm Bowel Dis. 2015; 21(2): 331–336.
- Guidi L, Marzo M, Andrisani G, et al. Faecal calprotectin assay after induction with anti-tumour necrosis factor α agents in inflammatory bowel disease: prediction of clinical response and mucosal healing at one year. Dig Liver Dis. 2014; 46(11): 974–979.
- Theede K, Holck S, Ibsen P, et al. Level of fecal calprotectin correlates with endoscopic and histologic inflammation and identifies patients with mucosal healing in ulcerative colitis. Clin Gastroenterol Hepatol. 2015; 13(11): 1929–19236.e1.
- Park KT, Heida A, van Rheenen PF, et al. Clinical utility of fecal calprotectin monitoring in asymptomatic patients with inflammatory bowel disease: a systematic review and practical guide. Inflamm Bowel Dis. 2017; 23(6): 894–902.
- Maaser C, Sturm A, Vavricka SR, et al. European Crohn’s and Colitis Organisation [ECCO] and the European Society of Gastrointestinal and Abdominal Radiology [ESGAR]. ECCO-ESGAR guideline for diagnostic assessment in IBD part 1: initial diagnosis, monitoring of known IBD, detection of complications. J Crohns Colitis. 2019; 13(2): 144–164.
- Zhulina Y, Cao Y, Amcoff K, et al. The prognostic significance of faecal calprotectin in patients with inactive inflammatory bowel disease. Aliment Pharmacol Ther. 2016; 44(5): 495–504.
- Ankersen DV, Weimers P, Marker D, et al. Individualized home-monitoring of disease activity in adult patients with inflammatory bowel disease can be recommended in clinical practice: A randomized-clinical trial. World J Gastroenterol. 2019; 25(40): 6158–6171.
- Louis E, Mary JY, Vernier-Massouille G, et al. Groupe D'etudes Thérapeutiques Des Affections Inflammatoires Digestives. Maintenance of remission among patients with Crohn's disease on antimetabolite therapy after infliximab therapy is stopped. Gastroenterology. 2012; 142(1): 63–70.e5; quiz e31.
- Wong ECL, Dulai PS, Marshall JK, et al. How do we treat inflammatory bowel diseases to aim for endoscopic remission? Clin Gastroenterol Hepatol. 2020; 18(6): 1300–1308.
- Ha C, Kornbluth A. Mucosal healing in inflammatory bowel disease: where do we stand? Curr Gastroenterol Rep. 2010; 12(6): 471–478.
- Rutgeerts P, Vermeire S, Van Assche G. Mucosal healing in inflammatory bowel disease: impossible ideal or therapeutic target? Gut. 2007; 56(4): 453–455.
- Yoon H, Jangi S, Dulai PS, et al. Incremental benefit of achieving endoscopic and histologic remission in patients with ulcerative colitis: a systematic review and meta-analysis. Gastroenterology. 2020; 159(4): 1262–1275.e7.
- Danese S, Vermeire S, D'Haens G, et al. STARDUST Study Group. Treat to target versus standard of care for patients with Crohn's disease treated with ustekinumab (STARDUST): an open-label, multicentre, randomised phase 3b trial. Lancet Gastroenterol Hepatol. 2022; 7(4): 294–306.
- Peyrin-Biroulet L, Vermeire S, D’Haens GR, et al. DOP90 Efficacy of the treat-to-target approach in modifying disease course with ustekinumab in patients with moderate-to-severe Crohn’s Disease: Results from the STARDUST trial. J Crohn’s Colitis. 2022; 16(Suppl_1): i132–i134.
- Jairath V, Khanna R, Guizzetti L, et al. Cluster-randomised controlled trial of an enhanced treatment algorithm for the mangement of Crohn’s diseaes: REACT-2. United Eur Gastroenterol J. 2022; 10(Suppl 8).
- Rimola J, Alfaro I, Fernández-Clotet A, et al. Persistent damage on magnetic resonance enterography in patients with Crohn's disease in endoscopic remission. Aliment Pharmacol Ther. 2018; 48(11-12): 1232–1241.
- Weinstein-Nakar I, Focht G, Church P, et al. ImageKids study group. Associations among mucosal and transmural healing and fecal level of calprotectin in children with crohn's disease. Clin Gastroenterol Hepatol. 2018; 16(7): 1089–1097.e4.
- Civitelli F, Nuti F, Oliva S, et al. Looking beyond mucosal healing: effect of biologic therapy on transmural healing in pediatric Crohn's disease. Inflamm Bowel Dis. 2016; 22(10): 2418–2424.
- Sands BE, Sandborn WJ, Panaccione R, et al. UNIFI Study Group. Ustekinumab as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2019; 381(13): 1201–1214.
- Sandborn WJ, Feagan BG, D'Haens G, et al. True North Study Group. Ozanimod as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2021; 385(14): 1280–1291.
- Feagan BG, Danese S, Loftus EV, et al. Filgotinib as induction and maintenance therapy for ulcerative colitis (SELECTION): a phase 2b/3 double-blind, randomised, placebo-controlled trial. Lancet. 2021; 397(10292): 2372–2384.
- Danese S, Vermeire S, Zhou W, et al. Upadacitinib as induction and maintenance therapy for moderately to severely active ulcerative colitis: results from three phase 3, multicentre, double-blind, randomised trials. Lancet. 2022; 399(10341): 2113–2128.
- Gupta A, Yu A, Peyrin-Biroulet L, et al. Treat to target: the role of histologic healing in inflammatory bowel diseases: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2021; 19(9): 1800–1813.e4.
- Daniluk U, Daniluk J, Krasnodebska M, et al. The combination of fecal calprotectin with ESR, CRP and albumin discriminates more accurately children with Crohn's disease. Adv Med Sci. 2019; 64(1): 9–14.
- D'Amico F, Fiorino G, Solitano V, et al. Ulcerative colitis: Impact of early disease clearance on long-term outcomes — a multicenter cohort study. United European Gastroenterol J. 2022; 10(7): 775–782.
- Christensen B, Erlich J, Gibson PR, et al. Histologic healing is more strongly associated with clinical outcomes in ileal Crohn's disease than endoscopic healing. Clin Gastroenterol Hepatol. 2020; 18(11): 2518–2525.e1.
- Castiglione F, Mainenti P, Testa A, et al. Cross-sectional evaluation of transmural healing in patients with Crohn's disease on maintenance treatment with anti-TNF alpha agents. Dig Liver Dis. 2017; 49(5): 484–489.
- Zacharopoulou E, Craviotto V, Fiorino G, et al. Targeting the gut layers in Crohn's disease: mucosal or transmural healing? Expert Rev Gastroenterol Hepatol. 2020; 14(9): 775–787.
- Wilkens R, Novak KL, Maaser C, et al. Relevance of monitoring transmural disease activity in patients with Crohn's disease: current status and future perspectives. Therap Adv Gastroenterol. 2021; 14: 17562848211006672.
- Maconi G, Armuzzi A. Beyond remission and mucosal healing in Crohn's disease. Exploring the deep with cross sectional imaging. Dig Liver Dis. 2017; 49(5): 457–458.
- Zorzi F, Ghosh S, Chiaramonte C, et al. Response assessed by ultrasonography as target of biological treatment for Crohn's disease. Clin Gastroenterol Hepatol. 2020; 18(9): 2030–2037.
- Lafeuille P, Hordonneau C, Vignette J, et al. Transmural healing and MRI healing are associated with lower risk of bowel damage progression than endoscopic mucosal healing in Crohn's disease. Aliment Pharmacol Ther. 2021; 53(5): 577–586.
- Fernandes SR, Rodrigues RV, Bernardo S, et al. Transmural healing is associated with improved long-term outcomes of patients with Crohn's disease. Inflamm Bowel Dis. 2017; 23(8): 1403–1409.
- Fernandes SR. Transmural remission and long-term clinical outcome in Crohn’s disease. UEG (2022) MP286.
- Castiglione F, Imperatore N, Testa A, et al. One-year clinical outcomes with biologics in Crohn's disease: transmural healing compared with mucosal or no healing. Aliment Pharmacol Ther. 2019; 49(8): 1026–1039.
- Vaughan R, Tjandra D, Patwardhan A, et al. Toward transmural healing: sonographic healing is associated with improved long-term outcomes in patients with Crohn's disease. Aliment Pharmacol Ther. 2022; 56(1): 84–94.
- Horsthuis K, Bipat S, Bennink RJ, et al. Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis of prospective studies. Radiology. 2008; 247(1): 64–79.
- Panés J, Bouzas R, Chaparro M, et al. Systematic review: the use of ultrasonography, computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn's disease. Aliment Pharmacol Ther. 2011; 34(2): 125–145.
- Bruining DH, Zimmermann EM, Loftus EV, et al. Society of Abdominal Radiology Crohn’s Disease-Focused Panel. Consensus recommendations for evaluation, interpretation, and Utilization of computed tomography and magnetic resonance enterography in patients with small bowel crohn's disease. Gastroenterology. 2018; 154(4): 1172–1194.
- Kucharzik T, Tielbeek J, Carter D, et al. ECCO-ESGAR topical review on optimizing reporting for cross-sectional imaging in inflammatory bowel disease. J Crohns Colitis. 2022; 16(4): 523–543.
- Taylor SA, Mallett S, Bhatnagar G, et al. METRIC study investigators. Diagnostic accuracy of magnetic resonance enterography and small bowel ultrasound for the extent and activity of newly diagnosed and relapsed Crohn's disease (METRIC): a multicentre trial. Lancet Gastroenterol Hepatol. 2018; 3(8): 548–558.
- Puylaert CAJ, Tielbeek JAW, Bipat S, et al. Grading of Crohn's disease activity using CT, MRI, US and scintigraphy: a meta-analysis. Eur Radiol. 2015; 25(11): 3295–3313.
- Buisson A, Pereira B, Goutte M, et al. Magnetic resonance index of activity (MaRIA) and Clermont score are highly and equally effective MRI indices in detecting mucosal healing in Crohn's disease. Dig Liver Dis. 2017; 49(11): 1211–1217.
- Allocca M, Fiorino G, Bonifacio C, et al. Comparative accuracy of bowel ultrasound versus magnetic resonance enterography in combination with colonoscopy in assessing Crohn's disease and guiding clinical decision-making. J Crohns Colitis. 2018; 12(11): 1280–1287.
- Buisson A, Gonzalez F, Poullenot F, et al. ACCEPT study group. Comparative acceptability and perceived clinical utility of monitoring tools: a nationwide survey of patients with inflammatory bowel disease. Inflamm Bowel Dis. 2017; 23(8): 1425–1433.
- Ilvemark JF, Hansen T, Goodsall TM, et al. Defining transabdominal intestinal ultrasound treatment response and remission in inflammatory bowel disease: systematic review and expert consensus statement. J Crohns Colitis. 2022; 16(4): 554–580.
- Goodsall TM, Jairath V, Feagan BG, et al. Standardisation of intestinal ultrasound scoring in clinical trials for luminal Crohn's disease. Aliment Pharmacol Ther. 2021; 53(8): 873–886.
- Novak KL, Nylund K, Maaser C, et al. Expert consensus on optimal acquisition and development of the International Bowel Ultrasound Segmental Activity Acore [IBUS-SAS]: a reliability and inter-rater variability study on intestinal ultrasonography in Crohn's disease. J Crohns Colitis. 2021; 15(4): 609–616.
- Kucharzik T, Wittig BM, Helwig U, et al. TRUST study group. Use of intestinal ultrasound to monitor Crohn's disease activity. Clin Gastroenterol Hepatol. 2017; 15(4): 535–542.e2.
- Helwig U, Fischer I, Hammer L, et al. Transmural response and transmural healing defined by intestinal ultrasound: new potential therapeutic targets? J Crohns Colitis. 2022; 16(1): 57–67.
- Kucharzik T, Wilkens R, D'Agostino MA, et al. STARDUST Intestinal Ultrasound study group. Early ultrasound response and progressive transmural remission after treatment with ustekinumab in Crohn's disease. Clin Gastroenterol Hepatol. 2023; 21(1): 153–163.e12.
- Maaser C, Petersen F, Helwig U, et al. German IBD Study Group and the TRUST&UC study group, German IBD Study Group and TRUST&UC study group. Intestinal ultrasound for monitoring therapeutic response in patients with ulcerative colitis: results from the TRUST&UC study. Gut. 2020; 69(9): 1629–1636.
- Ilvemark JF, Wilkens R, Thielsen P, et al. Early intestinal ultrasound predicts intravenous corticosteroid response in hospitalised patients with severe ulcerative colitis. J Crohns Colitis. 2022; 16(11): 1725–1734.
- de Voogd F, van Wassenaer EA, Mookhoek A, et al. Intestinal ultrasound is accurate to determine endoscopic response and remission in patients with moderate to severe ulcerative colitis: a longitudinal prospective cohort study. Gastroenterology. 2022; 163(6): 1569–1581.
- Sagami S, Kobayashi T, Aihara K, et al. Transperineal ultrasound predicts endoscopic and histological healing in ulcerative colitis. Aliment Pharmacol Ther. 2020; 51(12): 1373–1383.
- Allocca M, Filippi E, Costantino A, et al. Milan ultrasound criteria are accurate in assessing disease activity in ulcerative colitis: external validation. United European Gastroenterol J. 2021; 9(4): 438–442.
- Kucharzik T, Helwig U, Seibold F, et al. IBD patients with early clinical and sonographic improvements achieve better long-term outcomes than patients with clinical improvements alone — one-year interim results of the TRUST BEYOND study ECCO. Gastroenterology. 2022; 162(7): S610–S611.
- Calabrese E, Rispo A, Zorzi F, et al. Ultrasonography tight control and monitoring in Crohn's disease during different biological therapies: a multicenter study. Clin Gastroenterol Hepatol. 2022; 20(4): e711–e722.
- Allocca M, Craviotto V, Bonovas S, et al. Predictive value of bowel ultrasound in Crohn's disease: a 12-month prospective study. Clin Gastroenterol Hepatol. 2022; 20(4): e723–e740.
