Progress in the Application of Transmural Healing as an Indicator to Evaluate the Remission of Crohn's Disease

doi:10.12114/j.issn.1007-9572.2020.00.061

Abstract

Abstract: Crohn's Disease （CD） is a chronic nonspecific inflammatory disease involving the entire digestive tract.There has always been controversy in the academic circle about the therapeutic target of CD.The remission of clinical symptoms and endoscopic mucosal healing of the intestinal tract were all used as the therapeutic target of CD.With the popularization of enterography （CTE），magnetic resonance enterography （MRE），intestinal ultrasound （IUS） and other related imaging technologies in the diagnosis and treatment of CD，transmural healing has received increasing attention.As an indicator to evaluate the alleviation of inflammation of full-thickness intestinal wall by means of imaging examination，transmural healing is expected to become one of the new therapeutic targets for CD.This paper reviewed the imaging features of CD and the definition and scoring criteria related to transmural healing，analyzed the role of transmural healing in the evaluation of curative effect in patients with CD，and proposed the existing problems in the evaluation of CD treatment with transmural healing，in order to provide more information for clinicians.

Key words: Crohn disease, Transmural healing, Treatment outcome, Ultrasonography, Magnetic resonance imaging

摘要： 克罗恩病（CD）是一种累及全消化道的慢性非特异性炎性疾病。关于CD的治疗目标学术界一直存在争议，临床症状的缓解、内镜下肠道的黏膜愈合均曾作为CD的治疗目标。随着小肠影像学检查如计算机断层扫描小肠成像（CTE）、磁共振小肠成像（MRE）、肠道超声检查（IUS）等相关影像技术在CD诊疗中的普及，透壁愈合日益受到重视。作为一种借助影像学检查手段评估全层肠壁炎症缓解的指标，透壁愈合有望成为新的CD治疗目标之一。本文综述了CD的影像学表现和透壁愈合相关定义及评分标准，分析了透壁愈合在CD患者疗效评估中的作用，并提出目前使用透壁愈合评估CD治疗情况尚存在的问题，旨在为临床医生治疗CD提供更多参考。

关键词: Crohn病, 透壁愈合, 治疗结果, 超声检查, 磁共振成像

ZHANG Ming,JIANG Chonghui. Progress in the Application of Transmural Healing as an Indicator to Evaluate the Remission of Crohn's Disease　[J]. Chinese General Practice, 2020, 23(30): 3884-3887. DOI: 10.12114/j.issn.1007-9572.2020.00.061.
张明,蒋崇慧. 透壁愈合作为评估克罗恩病缓解指标的应用进展[J]. 中国全科医学, 2020, 23(30): 3884-3887. DOI: 10.12114/j.issn.1007-9572.2020.00.061.

References

［1］GOWER-ROUSSEAU C，SARTER H，SAVOYE G，et al．Validation of the Inflammatory Bowel Disease Disability Index in a population-based cohort［J］．Gut，2017，66（4）：588-596．DOI：10.1136/gutjnl-2015-310151.
［2］COLOMBEL J F，NARULA N，PEYRIN-BIROULET L.Management strategies to improve outcomes of patients with inflammatory bowel diseases［J］．Gastroenterology，2017，152（2）：351-361.e5．DOI：10.1053/j.gastro.2016.09.046.
［3］DANESE S，FIORINO G，PEYRIN-BIROULET L.Early intervention in Crohn's disease：towards disease modification trials［J］．Gut，2017，66（12）：2179-2187．DOI：10.1136/gutjnl-2017-314519.
［4］SIEGEL C A，WHITMAN C B，SPIEGEL B M R，et al．Development of an index to define overall disease severity in IBD［J］．Gut，2018，67（2）：244-254．DOI：10.1136/gutjnl-2016-312648.
［5］中华医学会消化病学分会炎症性肠病学组.炎症性肠病诊断与治疗的共识意见（2012年?广州）［J］．中华内科杂志，2012，51（10）：818-831．DOI：10.3760/cma.j.issn.0578-1426.2012.10.024.
［6］张明，王新颖.组织愈合在炎症性肠病诊治中的应用［J］．中华消化杂志，2017，37（1）：68-70．DOI：10.3760/cma.j.issn.0254-1432.2017.01.021.
［7］PEYRIN-BIROULET L，SANDBORN W，SANDS B E，et al．Selecting therapeutic targets in inflammatory bowel disease （STRIDE）：determining therapeutic goals for treat-to-target［J］．Am J Gastroenterol，2015，110（9）：1324-1338．DOI：10.1038/ajg.2015.233.
［8］ZORZI F，STASI E，BEVIVINO G，et al．A sonographic lesion index for Crohn's disease helps monitor changes in transmural bowel damage during therapy［J］．Clin Gastroenterol Hepatol，2014，12（12）：2071-2077．DOI：10.1016/j.cgh.2014.04.036.
［9］CIVITELLI F，NUTI F，OLIVA S，et al．Looking beyond mucosal healing：effect of biologic therapy on transmural healing in pediatric Crohn's disease［J］．Inflamm Bowel Dis，2016，22（10）：2418-2424．DOI：10.1097/MIB.0000000000000897.
［10］FERNANDES S R，RODRIGUES R V，BERNARDO S，et al．Transmural healing is associated with improved long-term outcomes of patients with Crohn's disease［J］．Inflamm Bowel Dis，2017，23（8）：1403-1409．DOI：10.1097/MIB.0000000000001143.
［11］DEEPAK P，FLETCHER J G，FIDLER J L，et al．Radiological response is associated with better long-term outcomes and is a potential treatment target in patients with small bowel Crohn's disease［J］．Am J Gastroenterol，2016，111（7）：997-1006．DOI：10.1038/ajg.2016.177.
［12］LATERZA L，PISCAGLIA A C，MINORDI L M，et al．Multiparametric evaluation predicts different mid-term outcomes in Crohn's disease［J］．Dig Dis，2018，36（3）：184-193．DOI：10.1159/000487589.
［13］PANéS J，RIMOLA J.Is the objective of treatment for Crohn's disease mucosal or transmural healing?［J］．Clin Gastroenterol Hepatol，2018，16（7）：1037-1039．DOI：10.1016/j.cgh.2018.03.034.
［14］BRUINING D H，ZIMMERMANN E M，LOFTUS E V Jr，et al．Consensus recommendations for evaluation，interpretation，and utilization of computed tomography and magnetic resonance enterography in patients with small bowel Crohn's disease［J］．Gastroenterology，2018，154（4）：1172-1194．DOI：10.1053/j.gastro.2017.11.274.
［15］MACONI G，NYLUND K，RIPOLLES T，et al．EFSUMB recommendations and clinical guidelines for intestinal ultrasound （GIUS） in inflammatory bowel diseases［J］．Ultraschall Med，2018，39（3）：304-317．DOI：10.1055/s-0043-125329.
［16］SHAH S C，COLOMBEL J F，SANDS B E，et al．Systematic review with meta-analysis：mucosal healing is associated with improved long-term outcomes in Crohn's disease［J］．Aliment Pharmacol Ther，2016，43（3）：317-333．DOI：10.1111/apt.13475.
［17］MACONI G，ARMUZZI A.Beyond remission and mucosal healing in Crohn's disease.Exploring the deep with cross sectional imaging［J］．Dig Liver Dis，2017，49（5）：457-458．DOI：10.1016/j.dld.2017.04.009.
［18］DAPERNO M，CASTIGLIONE F，DE RIDDER L，et al．Results of the 2nd part Scientific Workshop of the ECCO.Ⅱ：Measures and markers of prediction to achieve，detect，and monitor intestinal healing in inflammatory bowel disease［J］．J Crohns Colitis，2011，5（5）：484-498．DOI：10.1016/j.crohns.2011.07.003.
［19］CASTIGLIONE F，TESTA A，REA M，et al．Transmural healing evaluated by bowel sonography in patients with Crohn's disease on maintenance treatment with biologics［J］．Inflamm Bowel Dis，2013，19（9）：1928-1934．DOI：10.1097/MIB.0b013e31829053ce.
［20］EDER P，KATULSKA K，KRELA-KAZMIERCZAK I，et al．The influence of anti-TNF therapy on the magnetic resonance enterographic parameters of Crohn's disease activity［J］．Abdom Imaging，2015，40（7）：2210-2218．DOI：10.1007/s00261-015-0466-0.
［21］PREZZI D，BHATNAGAR G，VEGA R，et al．Monitoring Crohn's disease during anti-TNF-α therapy：validation of the magnetic resonance enterography global score （MEGS） against a combined clinical reference standard［J］．Eur Radiol，2016，26（7）：2107-2117．DOI：10.1007/s00330-015-4036-1.
［22］STOPPINO L P，DELLA VALLE N，RIZZI S，et al．Magnetic resonance enterography changes after antibody to tumor necrosis factor （anti-TNF） alpha therapy in Crohn's disease：correlation with SES-CD and clinical-biological markers［J］．BMC Med Imaging，2016，16（1）：37．DOI：10.1186/s12880-016-0139-7.
［23］KANG B，CHOI S Y，CHI S，et al．Baseline wall thickness is lower in mucosa-healed segments 1 year after infliximab in pediatric crohn disease patients［J］．J Pediatr Gastroenterol Nutr，2017，64（2）：279-285．DOI：10.1097/MPG.0000000000001222.
［24］HUH J，KIM K J，PARK S H，et al．Diffusion-weighted MR enterography to monitor bowel inflammation after medical therapy in Crohn's disease：a prospective longitudinal study［J］．Korean J Radiol，2017，18（1）：162-172．DOI：10.3348/kjr.2017.18.1.162.
［25］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［J］．Dig Liver Dis，2017，49（5）：484-489．DOI：10.1016/j.dld.2017.02.014.
［26］KUCHARZIK T，WITTIG B M，HELWIG U，et al．Use of intestinal ultrasound to monitor Crohn's disease activity［J］．Clin Gastroenterol Hepatol，2017，15（4）：535-542.e2．DOI：10.1016/j.cgh.2016.10.040.
［27］DILLMAN J R，DEHKORDY S F，SMITH E A，et al．Defining the ultrasound longitudinal natural history of newly diagnosed pediatric small bowel Crohn disease treated with infliximab and infliximab-azathioprine combination therapy［J］．Pediatr Radiol，2017，47（8）：924-934．DOI：10.1007/s00247-017-3848-3.
［28］LOPES S，ANDRADE P，CUNHA R，et al．Transmural healing in Crohn's disease：beyond mural findings［J］．Dig Liver Dis，2018，50（1）：103-104．DOI：10.1016/j.dld.2017.09.134.
［29］STURM A，MAASER C，CALABRESE E，et al．ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 2：IBD scores and general principles and technical aspects［J］．J Crohns Colitis，2019，13（3）：273-284．DOI：10.1093/ecco-jcc/jjy114.
［30］TAKENAKA K，OHTSUKA K，KITAZUME Y，et al．Correlation of the endoscopic and magnetic resonance scoring systems in the deep small intestine in Crohn's disease［J］．Inflamm Bowel Dis，2015，21（8）：1832-1838．DOI：10.1097/MIB.0000000000000449.
［31］RIMOLA J，ORDáS I，RODRIGUEZ S，et al．Magnetic resonance imaging for evaluation of Crohn's disease：validation of parameters of severity and quantitative index of activity［J］．Inflamm Bowel Dis，2011，17（8）：1759-1768．DOI：10.1002/ibd.21551.
［32］RIPOLLéS T，PAREDES J M，MARTíNEZ-PéREZ M J，et al．Ultrasonographic changes at 12 weeks of anti-TNF drugs predict 1-year sonographic response and clinical outcome in Crohn's disease：A multicenter study［J］．Inflamm Bowel Dis，2016，22（10）：2465-2473．DOI：10.1097/MIB.0000000000000882.
［33］SAUER C G，KUGATHASAN S，MARTIN D R，et al．Medical radiation exposure in children with inflammatory bowel disease estimates high cumulative doses［J］．Inflamm Bowel Dis，2011，17（11）：2326-2332．DOI：10.1002/ibd.21626.

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