Association of endoscopic and histological remission with clinical course in patients of ulcerative colitis

Vikram Narang; Ravneet Kaur; Bhavna Garg; Ramit Mahajan; Vandana Midha; Neena Sood; Ajit Sood

doi:10.5217/ir.2018.16.1.55

Articles

Page Path: HOME > Intest Res > Volume 16(1); 2018 > Article

Original Article Association of endoscopic and histological remission with clinical course in patients of ulcerative colitis: Vikram Narang¹, Ravneet Kaur¹, Bhavna Garg¹, Ramit Mahajan², Vandana Midha³, Neena Sood¹, Ajit Sood²; Intestinal Research 2018;16(1):55-61.
DOI: https://doi.org/10.5217/ir.2018.16.1.55
Published online: January 18, 2018

¹Department of Pathology, Dayanand Medical College and Hospital, Ludhiana, India.

²Department of Gastroentrology, Dayanand Medical College and Hospital, Ludhiana, India.

³Department of Internal Medicine, Dayanand Medical College and Hospital, Ludhiana, India.

Correspondence to Vikram Narang, Department of Pathology, Dayanand Medical College and Hospital, Tagore Nagar, Civil Lines, Ludhiana 141001, India. Tel: +91-1614687619, drvikramnarang@yahoo.com

• Received: April 12, 2017 • Revised: June 10, 2017 • Accepted: June 16, 2017

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

prev next

8,444 Views
133 Download
69 Web of Science
70 Crossref
72 Scopus

Full Article

Download PDF

Abstract
INTRODUCTION
METHODS
RESULTS
DISCUSSION
NOTES
REFERENCES

Abstract

Background/Aims
The therapeutic goal for treating ulcerative colitis (UC) patients has shifted to achieving mucosal healing over the past few years. However, at present, limited data is available on the correlation between endoscopic findings and histological remission in patients with endoscopic mucosal healing.
Methods
This was a prospective observational study conducted over a period of 18 months (January 2014 to June 2015) at Dayanand Medical College and Hospital, Ludhiana, Punjab, India. Patients diagnosed with UC who had been in clinical remission (n=76) for at least 6 months were evaluated for endoscopic remission. Those in endoscopic remission (Mayo score ≤1; 46/76, 60.5%) were subjected to multiple biopsies from the rectosigmoid region and histological remission, which was then defined as grade 0/1 as per the Geboes criteria.
Results
Of the 46 patients in endoscopic remission (age, 18–73 years; male:female=1.5:1.0), majority had E1 (proctitis) disease (21/46, 45.6%) followed by E2 (left sided colitis) (18/46, 39.1%) and E3 disease (pancolitis) (7/46, 15.2%) at baseline. Histological remission was noted in 67.3% (31/46) of the patients, while 32.7% (15/46) still retained the histologically active disease in the form of infiltration of the lamina propria by eosinophils and neutrophils (13/15, 86.6%), cryptitis (14/15, 93.3%), and crypt abscesses (8/15, 53.3%). On follow-up, after 1 year, 87.1% (27/31) of the patients who had been in histological remission remained clinically asymptomatic, while 12.9% (4/31) had relapsed. Among the 15 histologically active patients, 46.6% (7/15) remained in clinical remission, while 53.3% (8/15) had relapsed.
Conclusions
Histological remission, rather than endoscopic remission, predicts a sustained clinical remission and allows monitoring of therapy for the subsequent disease course in patients with UC.
Keywords: Mucosal healing; Histological remission; Colitis, ulcerative

INTRODUCTION

Ulcerative colitis (UC) is a chronic IBD with a relapsing and remitting course. The optimal goal of treatment of IBD is the complete resolution of the inflammatory process, and this is achieved only when patients in clinical remission have a corresponding mucosal healing. Mucosal healing may be observed on both endoscopic and histological aspects, and at present a standardized definition of mucosal healing for IBD patients does not exist. Although most studies on mucosal healing focus on endoscopic scores, some experts have suggested histological inflammation is a better predictor of future clinical relapse than endoscopic appearance alone.1 2 The present analysis was planned to evaluate the association between clinical remission, endoscopic remission, and histopathological parameters. Current practice in UC patients is to achieve endoscopic mucosal healing and no guidelines mention histological remission. To the best of our knowledge, this is the first study from Asia highlighting the discrepancy between endoscopic and histologic remission.

METHODS

1. Setting

This was a prospective, observational study assessing the association between the histological remission and long-term clinical course in patients with UC, conducted in the Departments of Gastroenterology and Pathology, Dayanand Medical College and Hospital, Ludhiana, between January 2014 to June 2015 (18 months) and subsequently followed up for 1 year.

2. Patients and Treatment

The diagnosis of UC was based on accepted clinical, endoscopic, and histological criteria. Clinical remission was defined as a Simple Clinical Colitis Activity Index ≤2 for at least 6 months and endoscopic remission (normal with clearly visible vascular pattern or erythema with decreased vascular pattern but no bleeding, i.e., Mayo score ≤1). Patients with active disease on endoscopy (Mayo ≥2) were excluded.

3. Histological Evaluation

Patients who were in clinical remission (n=76) for at least 6 months were subjected to ileocolonoscopy. Patients who were in endoscopic remission (46/76, 60.5%) were subjected to 4 biopsies from the rectosigmoid region to evaluate histological activity. As per Geboes criteria (2000), grade 0/1 was defined as histological remission.3 All the biopsies were evaluated by 1 gastrointestinal pathologist (N.S.). The patient characteristics (age, gender, endoscopic findings, duration of disease, duration of remission, and histopathology) were recorded (Fig. 1). Written consent was obtained from the patients and ethical approval from the Institutional Review Board of Dayanand Medical College and Hospital (ECR/715/Inst/PB/2015) was also obtained in April/May 2013.

4. Follow-up

The patients showing endoscopic remission were maintained on a stable dose of mesalamine and azathioprine/6-mercaptoprine and were followed up for 1 year to observe the clinical course. Patients on steroids, biological therapies, rectal mesalamine, or steroid enemas were not included in the present study.

5. Statistical Analysis

The data collected were subjected to statistical analysis. Mean and standard deviation were computed and paired t- and Z-tests were applied to evaluate the association between the 2 variables and to compare the means of the 2 groups. A significance difference was defined at an appropriate degree of freedom at the 1% and 5% levels of significance (P<0.05).

RESULTS

1. Baseline Characteristics

Seventy-six patients had a sustained clinical remission during 2014 to 2015, the duration of which ranged from 6 months to >5 years. Of these 76 patients, 46 were in endoscopic remission (age, 18–73 years; male:female=1.5:1.0). Prior to starting treatment, these patients had E1 disease (proctitis) in 45.6% (21/46) followed by E2 (left sided colitis; 18/46, 39.1%) and E3 (extensive colitis; 7/46, 15.2%) disease. According to the average duration of remission at the time of analysis, the patients were grouped as follows: 6 months to <2 years (38/46, 82.6%), 2 to 5 years (6/46, 13.0%), and >5 years (2/46, 4.3%) (Table 1).

2. Histopathological Parameters

The patients in endoscopic remission were subjected to endoscopic biopsies from the rectosigmoid region. Histological remission was noted in 67.3% of patients (31/46), while 15 (32.7%) patients still had histologically active disease in the form of infiltration of the lamina propria by eosinophils and neutrophils (13/15, 86.6%), cryptitis (14/15, 93.3%), and crypt abscesses (8/15, 53.3%) (Fig. 2). The histological grades of these patients are summarized in Table 2. Of the 31 patients in histological remission, 16 (51.6%) had mild structural changes while 14 (41.9%) had no structural changes according to the Geboes criteria, and 21 (67.7%) of the patients in histological remission had mild chronic inflammatory cells in the lamina propria while 11/15 patients (73.3%) in the histologically active category had moderate increases and 13.3% had marked increases in chronic inflammatory infiltrates into the lamina propria (Table 2). Histological remission did not depend on the duration (P=0.807) or extent (P=0.360) of the disease but the Mayo score (0/1) was significant in predicting remission (P=0.047) (Table 3). There was no clinical significance for the presence of basal lymphoid aggregates or basal plasmacytosis (P=1.000) (Table 2).

3. Follow-up

When followed up for 1 year, nearly twice the number of patients in histological remission remained in clinical remission when compared with those with histological activity (87.1% vs. 46.6%, respectively, P=0.006). As seen in Table 4, relapses defined by the histological score (P=0.001) did not depend on patient factors like age or sex, or duration of clinical remission, disease extent, or Mayo endoscopic score.

DISCUSSION

Although the concept of “deep remission” has developed in CD, it has not been replicated in those with UC. Most studies on mucosal healing focus on endoscopic scores, and the data from various trials suggests that patients with Mayo score 0 (complete mucosal healing) have longer-lasting remissions. However, patients with UC who are in clinical and endoscopic remission may still have histologically active disease and are at a high risk of having a relapse,2 4 thus suggesting the need for repeat biopsy and histopathology once mucosal healing has been achieved. Current practice in UC patients is focused on achieving endoscopic mucosal healing and to date there is no consensus about when to include histological remission in the definition of mucosal healing. These observations make this analysis pertinent and are the first from Asia highlighting the discrepancy between endoscopic and histological remission for clinical outcomes of UC patients.

Of the 46 patients who were in endoscopic remission in our study, 67.3% patients (31/46) were in histological remission, but 32.6% (15/46) still had histologically active disease. When the long-term clinical outcomes were assessed after 1 year, the rate of a sustained clinical remission was significantly higher in patients who attained histological remission than among those who showed signs of active inflammation on histopathology (87.1% vs. 46.6%, P=0.006). A recent study from the United Kingdom also reported moderate concordance between endoscopic and histological remission with 24% of patients with endoscopic remission having persistent mucosal inflammation on biopsy.4 These findings highlight the fact that histological remission is distinct from endoscopic mucosal healing and it is a better predictor of a sustained clinical remission. Thus, histological remission may be a better endpoint for assessing long-term clinical outcomes including risk of colon cancer, as well as effectiveness of a drug in a clinical trial.

When patients with endoscopically quiescent disease are subjected to biopsy, the histopathology may show features that suggest disease activity. These include the presence of neutrophilic infiltrates in the lamina propria, epithelial cell damage (loss of cells, mucin depletion, cryptitis, crypt abscesses, and erosion), and an increase in lymphocytes and plasma cells. The presence of neutrophils is a reliable indicator of disease activity, with a good inter-observer agreement in various studies. Histology may also predict relapse or dysplasia. Histological findings predictive of ensuing clinical relapse in patients with quiescent disease are the persistence of neutrophils, basal plasmacytosis, mildly active disease, and an elevated number of eosinophils.2 3 4 5

In our study, more than 70% of patients in endoscopic remission showed mild crypt distortion and mild to moderate increases in chronic inflammatory cells in the lamina propria. The presence of eosinophils and neutrophils in the lamina propria, cryptitis, and crypt abscesses were seen only in the histologically active group. Thus, the presence of acute inflammatory infiltrates and crypt destruction were predictors of activity and relapse. These findings are consistent with other studies.5 6

In a multivariate analysis of data from 74 patients with inactive UC, relapse was also predicted by the presence of basal plasmacytosis.7 Although we observed basal plasmacytosis and basal lymphoid aggregates in biopsies of our UC patients, they failed to reach statistical significance to predict relapse. Similar observations were made by our group in a small prospective analysis previously and therefore we believe that some of these changes can be focal and serial step sectioning and better orientation of the specimen might be required.8 This problem has considerable implications for the precision of scoring. Some index items, such as basal plasmacytosis, require perpendicular sections of well-oriented samples for accurate interpretation. Section thickness may also affect the interpretation of results. Similar observations were made by Riley et al.5 who in a study of 82 patients with UC in symptomatic and sigmoidoscopic remission found an acute inflammatory cell infiltrate, presence of crypt abscesses, and mucin depletion to be associated with an increased risk of relapse. Most recently, in a retrospective analysis of a cohort of 75 patients with UC, Bessissow et al.7 showed that despite normal endoscopy, histologic investigation showed inflammatory activity (Geboes score ≥3.1) in 40% of patients, and basal plasmacytosis in 21% of patients.

Factors such as age, gender, extent of disease, and duration of clinical remission were not found to be statistically significant in predicting relapse. We attribute this to the smaller number of patients in the analysis. A limitation of our study is that we did not analyze any of the available biological parameters but during our previous analysis these were not statistically significant.8 Bessissow et al.7 showed that on univariate analysis, the only serologic marker that favored clinical remission was CRP ≤5 mg/L, but this effect did not remain significant on multivariate analysis, which was most likely related to the fact that the inflammation was only limited to the mucosa. In addition, Schoepfer et al.9 demonstrated that CRP is an inadequate biomarker of endoscopic disease activity in UC. It is also not surprising that albumin and hemoglobin were not predictive of relapse, because in patients with prolonged mucosal healing, one would expect them to be normalized.1

Though achievement of histological healing provides a more accurate picture of recovery and improves the disease outcomes, it seems to be a relatively difficult goal to achieve. In addition to this, there are certain unresolved issues. Most of the scoring systems for endoscopy and histological features are either not validated or only partially validated.3 4 10 There are no standard guidelines on how often one should perform colonoscopy and biopsy inpatients in clinical remission. Also, the inflammatory process in UC may be discontinuous during the natural course of the disease or after medical treatment, thus suggesting a need for several targeted biopsies, the number and method of acquisition of which is yet not clearly defined. Also, H&E can identify neutrophils and lymphocytes accurately but cannot determine the activation status of lymphocytes, for which immunochemistry is needed.

Thus, in conclusion, histological remission and healing serves as a better marker of treatment efficacy in patients with UC and is a better predictor of sustained remission in patients than endoscopic remission. Histologic remission and healing is an area of increased research focus and has the promise of being an important marker of treatment efficacy in UC, with the potential to guide treatment decisions in the future.

In conclusion, mucosal healing is associated with better clinical outcomes in patients with UC; however, histologic parameters may provide a more accurate picture of the recovery of the mucosa and further improve disease outcomes. This study indicates that histologic healing may be associated with better outcomes in UC thus providing a rationale for making this a treatment goal. The present analysis is small but is a progressive step towards better defining remission in UC.

NOTES

FINANCIAL SUPPORT: The authors received no financial support for the research, authorship, and/or publication of this article.

CONFLICT OF INTEREST: No potential conflict of interest relevant to this article was reported.

AUTHOR CONTRIBUTION: V.N., manuscript writing and data analysis; R.K., manuscript design and data analysis; B.G., manuscript review and editing; R.M., manuscript editing and Manuscript de sign; V.M., manuscript editing; N.S. and A.S., supervison, manuscript edit ing, manuscript design.

REFERENCES

1. D'Haens G, Sandborn WJ, Feagan BG, et al. A review of activity indices and efficacy end points for clinical trials of medical therapy in adults with ulcerative colitis. Gastroenterology 2007;132:763–786.PMID: 17258735.Article PubMed
2. Travis SP, Higgins PD, Orchard T, et al. Review article: defining remission in ulcerative colitis. Aliment Pharmacol Ther 2011;34:113–124.PMID: 21615435.Article PubMed
3. Geboes K, Riddell R, Ost A, Jensfelt B, Persson T, Löfberg R. A reproducible grading scale for histological assessment of inflammation in ulcerative colitis. Gut 2000;47:404–409.PMID: 10940279.Article PubMed PMC
4. Bryant RV, Burger DC, Delo J, et al. Beyond endoscopic mucosal healing in UC: histological remission better predicts corticosteroid use and hospitalisation over 6 years of follow-up. Gut 2016;65:408–414.PMID: 25986946.Article PubMed
5. Riley SA, Mani V, Goodman MJ, Dutt S, Herd ME. Microscopic activity in ulcerative colitis: what does it mean? Gut 1991;32:174–178.PMID: 1864537.Article PubMed PMC
6. Bitton A, Peppercorn MA, Antonioli DA, et al. Clinical, biological, and histologic parameters as predictors of relapse in ulcerative colitis. Gastroenterology 2001;120:13–20.PMID: 11208709.Article PubMed
7. Bessissow T, Lemmens B, Ferrante M, et al. Prognostic value of serologic and histologic markers on clinical relapse in ulcerative colitis patients with mucosal healing. Am J Gastroenterol 2012;107:1684–1692.PMID: 23147523.Article PubMed PDF
8. Azad S, Sood N, Sood A. Biological and histological parameters as predictors of relapse in ulcerative colitis: a prospective study. Saudi J Gastroenterol 2011;17:194–198.PMID: 21546723.Article PubMed PMC
9. Schoepfer AM, Beglinger C, Straumann A, Trummler M, Renzulli P, Seibold F. Ulcerative colitis: correlation of the Rachmilewitz endoscopic activity index with fecal calprotectin, clinical activity, C-reactive protein, and blood leukocytes. Inflamm Bowel Dis 2009;15:1851–1858.PMID: 19462421.Article PubMed
10. Geboes K, Dalle I. Influence of treatment on morphological features of mucosal inflammation. Gut 2002;50(Suppl 3): III37–III42.PMID: 11953331.Article PubMed PMC

Fig. 1

Flow diagram depicting the patients enrolled and their long-term clinical follow-up.

Fig. 2

(A) Endoscopy Mayo score 0; (B) histopathological examination of the same patient exhibiting mild crypt distortion only (Geboes grade, 0.1) (H&E, ×200). (C) Endoscopy Mayo score 1; (D) histopathological examination of the same patient showing significant acute inflammatory infiltrates in the lamina propria along with evidence of cryptitis (Geboes grade, 3.1) (H&E, ×400).

Table 1

Baseline Characteristics of the Patients

Values are presented as number (%).

Table 2

Histological Parameters as per Geboes Criteria

Table 3

Factors Predicting Histological Remission

MES, mayo endoscpoic subscore.

Table 4

Factors Predicting Relapse in Patients

MES, mayo endoscopic subscore.

Figure & Data

REFERENCES

Citations

Citations to this article as recorded by

Advanced Endoscopic Imaging for Assessing Mucosal Healing and Histologic Remission in Inflammatory Bowel Diseases
Tommaso Pessarelli, Gian Eugenio Tontini, Helmut Neumann
Gastrointestinal Endoscopy Clinics of North America.2025; 35(1): 159. CrossRef
Predictive accuracy of fecal calprotectin for histologic remission in ulcerative colitis
Arshdeep Singh, Arshia Bhardwaj, Riya Sharma, Bhavjeet Kaur Kahlon, Ashvin Singh Dhaliwal, Dharmatma Singh, Simranjeet Kaur, Devanshi Jain, Namita Bansal, Ramit Mahajan, Kirandeep Kaur, Aminder Singh, Vikram Narang, Harpreet Kaur, Vandana Midha, Ajit Sood
Intestinal Research.2025; 23(2): 144. CrossRef
Fatigue in Patients with Inflammatory Bowel Disease in Remission One Year After Diagnosis (the IBSEN III Study)
Kristina A Holten, Tomm Bernklev, Randi Opheim, Bjørn C Olsen, Trond Espen Detlie, Vibeke Strande, Petr Ricanek, Raziye Boyar, May-Bente Bengtson, Tone B Aabrekk, Øyvind Asak, Svein Oskar Frigstad, Vendel A Kristensen, Milada Hagen, Magne Henriksen, Gert
Journal of Crohn's and Colitis.2025;[Epub] CrossRef
The Diagnostic Significance of SLC26A2 and Its Potential Role in Ulcerative Colitis
Lijuan Qian, Shuo Hu, Haizhou Zhao, Ye Han, Chenguang Dai, Xinquan Zan, Qiaoming Zhi, Chunfang Xu
Biomedicines.2025; 13(2): 461. CrossRef
Histologic healing and clinical outcomes in ulcerative colitis
Raymond Fueng-Hin Liang, Huiyu Lin, Cora Yuk-Ping Chau, Wee Chian Lim
Intestinal Research.2025; 23(2): 182. CrossRef
Histological Remission Placebo Rates in Ulcerative Colitis Trials: A Systematic Review and Meta-analysis
Michael Youssef, Kelly Dong, So Jeong Lee, Neeraj Narula
Inflammatory Bowel Diseases.2024; 30(1): 125. CrossRef
Histological Disease Activity as Predictor of Clinical Relapse, Hospitalization, and Surgery in Inflammatory Bowel Disease: Systematic Review and Meta-Analysis
Mohammad Shehab, Sahad Al Akram, Amro Hassan, Fatema Alrashed, Vipul Jairath, Talat Bessissow
Inflammatory Bowel Diseases.2024; 30(4): 563. CrossRef
Disease Clearance as a New Outcome in Ulcerative Colitis: a Systematic Review and Expert Consensus
Ferdinando D’Amico, Fernando Magro, Britta Siegmund, Taku Kobayashi, Paulo Gustavo Kotze, Virginia Solitano, Benedicte Caron, Sameer Al Awadhi, Ailsa Hart, Vipul Jairath, Axel Dignass, Laurent Peyrin-Biroulet, Silvio Danese
Inflammatory Bowel Diseases.2024; 30(6): 1009. CrossRef
Histological Outcomes and JAK-STAT Signalling in Ulcerative Colitis Patients Treated with Tofacitinib
Sara van Gennep, Ivan C N Fung, Djuna C de Jong, Rishand K Ramkisoen, Esmé Clasquin, Jitteke de Jong, Leonie C S de Vries, Wouter J de Jonge, Krisztina B Gecse, Mark Löwenberg, John C Woolcott, Aart Mookhoek, Geert R D’Haens
Journal of Crohn's and Colitis.2024; 18(8): 1283. CrossRef
Etrolizumab as an induction and maintenance therapy for ulcerative colitis: A systematic review and meta‐analysis of randomized controlled trials
Othman Saleh, Mohamed T. Abuelazm, Islam Mohamed, Alaa Ramadan, Mohammad Assaf, Ahmad Alzoubi, Majd M. AlBarakat, Basel Abdelazeem
JGH Open.2024;[Epub] CrossRef
Adequacy of sigmoidoscopy as compared to colonoscopy for assessment of disease activity in patients of ulcerative colitis: a prospective study
Sameet Tariq Patel, Anuraag Jena, Sanjay Chandnani, Shubham Jain, Pankaj Nawghare, Saurabh Bansal, Harsh Gandhi, Rishikesh Malokar, Jay Chudasama, Prasanta Debnath, Seemily Kahmei, Rima Kamat, Sangeeta Kini, Qais Q Contractor, Pravin M Rathi
Intestinal Research.2024; 22(3): 310. CrossRef
Deep mucosal healing in ulcerative colitis: how deep is better?
Xin Jin, Yan You, Gechong Ruan, Weixun Zhou, Ji Li, Jingnan Li
Frontiers in Medicine.2024;[Epub] CrossRef
Histologic improvement predicts endoscopic remission in patients with ulcerative colitis
Ji Eun Kim, Minjee Kim, Min-Ji Kim, Eun Ran Kim, Sung Noh Hong, Dong Kyung Chang, Sang Yun Ha, Young-Ho Kim
Scientific Reports.2024;[Epub] CrossRef
Epithelial neutrophil localization and tight junction Claudin‐2 expression are innovative outcome predictors in inflammatory bowel disease
Irene Zammarchi, Giovanni Santacroce, Miguel Puga‐Tejada, Brian Hayes, Rory Crotty, Elaine O’Driscoll, Snehali Majumder, Wiktoria Kaczmarczyk, Yasuharu Maeda, Jane McCarthy, Kathleen Sugrue, Caitriona O’Sullivan, Louise Burke, Subrata Ghosh, Marietta Iacu
United European Gastroenterology Journal.2024; 12(9): 1155. CrossRef
Predictive Model for Outcomes in Inflammatory Bowel Disease Patients Receiving Maintenance Infliximab Therapy
Rochelle Wong, Paris Charilaou, Amy Hemperly, Lihui Qin, Yushan Pan, Prerna Mathani, Randy Longman, Brigid S Boland, Parambir S Dulai, Ariela K Holmer, Dana Lukin, Siddharth Singh, Mark A Valasek, William J Sandborn, Ellen Scherl, Niels Vande Casteele, Ro
Crohn's & Colitis 360.2024;[Epub] CrossRef
Histologic Activity and Steroid Use History Are Risk Factors of Clinical Relapse in Ulcerative Colitis With Mayo Endoscopic Subscore of 0 or 1
Gyeol Seong, Joo Hye Song, Ji Eun Kim, Tae Jun Kim, Eun Ran Kim, Sung Noh Hong, Dong Kyung Chang, Seok-Hyung Kim, Sang Yun Ha, Young-Ho Kim
Inflammatory Bowel Diseases.2023; 29(2): 238. CrossRef
(Re)Appraising Remission in Ulcerative Colitis
Ajit Sood, Arshdeep Singh, Ramit Mahajan, Vandana Midha, Charles N Bernstein, David T Rubin
Inflammatory Bowel Diseases.2023; 29(8): 1317. CrossRef
Artificial Intelligence Enables Quantitative Assessment of Ulcerative Colitis Histology
Fedaa Najdawi, Kathleen Sucipto, Pratik Mistry, Stephanie Hennek, Christina K.B. Jayson, Mary Lin, Darren Fahy, Shawn Kinsey, Ilan Wapinski, Andrew H. Beck, Murray B. Resnick, Archit Khosla, Michael G. Drage
Modern Pathology.2023; 36(6): 100124. CrossRef
Impaired Intestinal Permeability Assessed by Confocal Laser Endomicroscopy—A New Potential Therapeutic Target in Inflammatory Bowel Disease
Stefan Chiriac, Catalin Victor Sfarti, Horia Minea, Carol Stanciu, Camelia Cojocariu, Ana-Maria Singeap, Irina Girleanu, Tudor Cuciureanu, Oana Petrea, Laura Huiban, Cristina Maria Muzica, Sebastian Zenovia, Robert Nastasa, Remus Stafie, Adrian Rotaru, Er
Diagnostics.2023; 13(7): 1230. CrossRef
HISTOPATHOLOGICAL FEATURES IN RELAPSE OF ULCERATIVE COLITIS.
Saroash Iqbal, Aman Ur Rehman, Nausheen Henna, Zara Madiha, Sahar Moeed, Uzma Aslam
JAIMC: Journal of Allama Iqbal Medical College.2023;[Epub] CrossRef
Mucosal Atrophy Predicts Poorer Outcomes in Pediatric Ulcerative Colitis—A National Inception Cohort Study
Emily Stenke, Lorraine Stallard, Sarah Cooper, Anna Dominik, Abigail Pilkington, Sheila Sugrue, Maureen O’Sullivan, Michael McDermott, Shoana Quinn, Annemarie Broderick, Billy Bourke, Séamus Hussey
Journal of Pediatric Gastroenterology and Nutrition.2023; 76(5): 603. CrossRef
Automating Ground Truth Annotations for Gland Segmentation Through Immunohistochemistry
Tushar Kataria, Saradha Rajamani, Abdul Bari Ayubi, Mary Bronner, Jolanta Jedrzkiewicz, Beatrice S. Knudsen, Shireen Y. Elhabian
Modern Pathology.2023; 36(12): 100331. CrossRef
Evaluation of Disease Activity in Inflammatory Bowel Disease: Diagnostic Tools in the Assessment of Histological Healing
Alina Ecaterina Jucan, Otilia Gavrilescu, Mihaela Dranga, Iolanda Valentina Popa, Ioana-Ruxandra Mihai, Vasile-Claudiu Mihai, Gabriela Stefanescu, Vasile Liviu Drug, Cristina Cijevschi Prelipcean, Radu-Alexandru Vulpoi, Oana-Bogdana Barboi, Irina Ciortesc
Biomedicines.2023; 11(11): 3090. CrossRef
Selected Cytokines and Metalloproteinases in Inflammatory Bowel Disease
Barbara Sosna, David Aebisher, Angelika Myśliwiec, Klaudia Dynarowicz, Dorota Bartusik-Aebisher, Piotr Oleś, Grzegorz Cieślar, Aleksandra Kawczyk-Krupka
International Journal of Molecular Sciences.2023; 25(1): 202. CrossRef
Utilizing Deep Learning to Analyze Whole Slide Images of Colonic Biopsies for Associations Between Eosinophil Density and Clinicopathologic Features in Active Ulcerative Colitis
Niels Vande Casteele, Jonathan A Leighton, Shabana F Pasha, Frank Cusimano, Aart Mookhoek, Catherine E Hagen, Christophe Rosty, Reetesh K Pai, Rish K Pai
Inflammatory Bowel Diseases.2022; 28(4): 539. CrossRef
Randomised clinical trial: a phase 1b study of GB004, an oral HIF‐1α stabiliser, for treatment of ulcerative colitis
Silvio Danese, Barrett G. Levesque, Brian G. Feagan, Alina Jucov, Bal Raj Bhandari, Rish K. Pai, Kristen Taylor Meadows, Brian J. Kirby, Jean‐Marie Bruey, Allan Olson, Robin Osterhout, Courtney Van Biene, Julia Ford, Richard Aranda, Kartik Raghupathi, Wil
Alimentary Pharmacology & Therapeutics.2022; 55(4): 401. CrossRef
PICaSSO Histologic Remission Index (PHRI) in ulcerative colitis: development of a novel simplified histological score for monitoring mucosal healing and predicting clinical outcomes and its applicability in an artificial intelligence system
Xianyong Gui, Alina Bazarova, Rocìo del Amor, Michael Vieth, Gert de Hertogh, Vincenzo Villanacci, Davide Zardo, Tommaso Lorenzo Parigi, Elin Synnøve Røyset, Uday N Shivaji, Melissa Anna Teresa Monica, Giulio Mandelli, Pradeep Bhandari, Silvio Danese, Jos
Gut.2022; 71(5): 889. CrossRef
Systematic review and meta-analysis: the advantage of endoscopic Mayo score 0 over 1 in patients with ulcerative colitis
Angelo Viscido, Marco Valvano, Gianpiero Stefanelli, Annalisa Capannolo, Chiara Castellini, Eugenia Onori, Antonio Ciccone, Filippo Vernia, Giovanni Latella
BMC Gastroenterology.2022;[Epub] CrossRef
Appendiceal Orifice Inflammation Is Associated with Lower Rate of Complete Endoscopic Remission in Patients with Ulcerative Colitis
Chang Kyo Oh, Han Hee Lee, Jin Su Kim, Bo-In Lee, Young-Seok Cho
Journal of Personalized Medicine.2022; 12(5): 748. CrossRef
ECCO Position on Harmonisation of Crohn’s Disease Mucosal Histopathology
F Magro, J Sabino, F Rosini, M Tripathi, P Borralho, P Baldin, S Danese, A Driessen, I O Gordon, M Iacucci, N Noor, M Svrcek, L Peyrin-Biroulet, R Feakins
Journal of Crohn's and Colitis.2022; 16(6): 876. CrossRef
Constrained multiple instance learning for ulcerative colitis prediction using histological images
Rocío del Amor, Pablo Meseguer, Tommaso Lorenzo Parigi, Vincenzo Villanacci, Adrián Colomer, Laëtitia Launet, Alina Bazarova, Gian Eugenio Tontini, Raf Bisschops, Gert de Hertogh, Jose G. Ferraz, Martin Götz, Xianyong Gui, Bu’Hussain Hayee, Mark Lazarev,
Computer Methods and Programs in Biomedicine.2022; 224: 107012. CrossRef
Ulcerative colitis: Impact of early disease clearance on long‐term outcomes ‐ A multicenter cohort study
Ferdinando D’Amico, Gionata Fiorino, Virginia Solitano, Eugenia Massarini, Lucas Guillo, Mariangela Allocca, Federica Furfaro, Alessandra Zilli, Stefanos Bonovas, Fernando Magro, Laurent Peyrin‐Biroulet, Silvio Danese
United European Gastroenterology Journal.2022; 10(7): 775. CrossRef
Efficacy and safety of ozanimod for ulcerative colitis (review)
M. V. Shapina, A. V. Poletova, T. A. Baranova
Koloproktologia.2022; 21(3): 119. CrossRef
Deep learning-based automated quantification of goblet cell mucus using histological images as a predictor of clinical relapse of ulcerative colitis with endoscopic remission
Jun Ohara, Tetsuo Nemoto, Yasuharu Maeda, Noriyuki Ogata, Shin-ei Kudo, Toshiko Yamochi
Journal of Gastroenterology.2022; 57(12): 962. CrossRef
Clinical Predictors of Response to Faecal Microbiota Transplantation in Patients with Active Ulcerative Colitis
Ajit Sood, Arshdeep Singh, Ramit Mahajan, Vandana Midha, Kirandeep Kaur, Dharmatma Singh, Namita Bansal, Khushdeep Dharni
Journal of Crohn's and Colitis.2021; 15(2): 238. CrossRef
Therapeutic drug monitoring of anti‐tumour necrosis factor‐α agents in inflammatory bowel disease: Limits and improvements
José María Giráldez‐Montero, Jaime Gonzalez‐Lopez, Manuel Campos‐Toimil, María Jesús Lamas‐Díaz
British Journal of Clinical Pharmacology.2021; 87(5): 2216. CrossRef
Histologic Features of Colon Biopsies (Geboes Score) Associated With Progression of Ulcerative Colitis for the First 36 Months After Biopsy
Fernando Magro, Catarina Alves, Joanne Lopes, Susana Lopes, Helena Tavares de Sousa, José Cotter, Vitor Macedo da Silva, Paula Lago, Ana Vieira, Mariana Brito, Maria A.M. Duarte, Francisco Portela, João P. Silva, Paula Ministro, Bruno Arroja, Liliana Carv
Clinical Gastroenterology and Hepatology.2021; 19(12): 2567. CrossRef
Treat to Target: The Role of Histologic Healing in Inflammatory Bowel Diseases: A Systematic Review and Meta-analysis
Akshita Gupta, Amy Yu, Laurent Peyrin-Biroulet, Ashwin N. Ananthakrishnan
Clinical Gastroenterology and Hepatology.2021; 19(9): 1800. CrossRef
Fecal calprotectin as a noninvasive test to predict deep remission in patients with ulcerative colitis
Ludimilla dos Reis Malvão, Kalil Madi, Barbara Cathalá Esberard, Renata Fernandes de Amorim, Kelly dos Santos Silva, Katia Farias e Silva, Heitor Siffert Pereira de Souza, Ana Teresa Pugas Carvalho
Medicine.2021; 100(3): e24058. CrossRef
Real-life evaluation of histologic scores for Ulcerative Colitis in remission
Christian Børde Arkteg, Sveinung Wergeland Sørbye, Lene Buhl Riis, Stig Manfred Dalen, Jon Florholmen, Rasmus Goll, Valérie Pittet
PLOS ONE.2021; 16(3): e0248224. CrossRef
Long-Term Efficacy and Safety of Ozanimod in Moderately to Severely Active Ulcerative Colitis: Results From the Open-Label Extension of the Randomized, Phase 2 TOUCHSTONE Study
William J Sandborn, Brian G Feagan, Stephen Hanauer, Severine Vermeire, Subrata Ghosh, Wenzhong J Liu, AnnKatrin Petersen, Lorna Charles, Vivian Huang, Keith Usiskin, Douglas C Wolf, Geert D’Haens
Journal of Crohn's and Colitis.2021; 15(7): 1120. CrossRef
Ultra-high Magnification Endocytoscopy and Molecular Markers for Defining Endoscopic and Histologic Remission in Ulcerative Colitis—An Exploratory Study to Define Deep Remission
Marietta Iacucci, Louisa Jeffery, Animesh Acharjee, Olga Maria Nardone, Davide Zardo, Samuel C L Smith, Alina Bazarova, Rosanna Cannatelli, Uday N Shivaji, John Williams, Georgios Gkoutos, Subrata Ghosh
Inflammatory Bowel Diseases.2021; 27(11): 1719. CrossRef
Raman spectroscopy accurately differentiates mucosal healing from non-healing and biochemical changes following biological therapy in inflammatory bowel disease
Samuel C. L. Smith, Carl Banbury, Davide Zardo, Rosanna Cannatelli, Olga M. Nardone, Uday N. Shivaji, Subrata Ghosh, Pola Goldberg Oppenheimer, Marietta Iacucci, Pradeep Dudeja
PLOS ONE.2021; 16(6): e0252210. CrossRef
Accurate diagnosis of endoscopic mucosal healing in ulcerative colitis using deep learning and machine learning
Tien-Yu Huang, Shan-Quan Zhan, Peng-Jen Chen, Chih-Wei Yang, Henry Horng-Shing Lu
Journal of the Chinese Medical Association.2021; 84(7): 678. CrossRef
Is histological remission of ulcerative colitis achievable?
Oleg V. Knyazev, Anna V. Kagramanova, Sergei G. Khomeriki, Asfold I. Parfenov
Terapevticheskii arkhiv.2021; 93(8): 975. CrossRef
Current Trends in IBD—Development of Mucosal-Based Biomarkers and a Novel Minimally Invasive Recoverable Sampling System
Yunki Y Yau, Valerie C Wasinger, Robert P Hirten, Emil Chuang, Merodean Huntsman, Jack Stylli, Jeff Shimizu, Vijay Yajnik, Jeffrey Smith, Shaoying N Lee, Sharat Singh, Christopher Wahl, Rupert W Leong, Bruce E Sands
Inflammatory Bowel Diseases.2021; 27(Supplement): S17. CrossRef
Histological remission of ulcerative colitis with combined anti-cytokine and cell therapy
Oleg V. Knyazev, Sergey G. Khomeriki, Аnna V. Kagramanova, Albina A. Lishchinskaya, Olga A. Smirnova, Karina K. Noskova, Asfold I. Parfenov
Terapevticheskii arkhiv.2021; 93(12): 1435. CrossRef
Histologic Activity and Steroid Use History are Risk Factors of Clinical Relapse in Ulcerative Colitis with Endoscopic Remission
Gyeol Seong, Joo Hye Song, Ji Eun Kim, Tae Jun Kim, Eun Ran Kim, Sung Noh Hong, Dong Kyung Chang, Seok-Hyung Kim, Sang Yun Ha, Young-Ho Kim
SSRN Electronic Journal .2021;[Epub] CrossRef
Relationship between Mayo endoscopic score and histological scores in ulcerative colitis: A prospective study
Jimil Shah, Usha Dutta, Ashim Das, Vishal Sharma, Harshal Mandavdhare, Pankaj Sharma, Dimple Kalsi, Priyanka Popli, Rakesh Kochhar
JGH Open.2020; 4(3): 382. CrossRef
Complete Resolution of Mucosal Neutrophils Associates With Improved Long-Term Clinical Outcomes of Patients With Ulcerative Colitis
Rish K. Pai, Douglas J. Hartman, Claudia Ramos Rivers, Miguel Regueiro, Marc Schwartz, David G. Binion, Reetesh K. Pai
Clinical Gastroenterology and Hepatology.2020; 18(11): 2510. CrossRef
Prostaglandin E-major urinary metabolite versus fecal immunochemical occult blood test as a biomarker for patient with ulcerative colitis
Natsuki Ishida, Takahiro Miyazu, Ryosuke Takano, Satoshi Tamura, Shinya Tani, Takuma Kagami, Mihoko Yamade, Yasushi Hamaya, Moriya Iwaizumi, Satoshi Osawa, Takahisa Furuta, Hiroaki Miyajima, Ken Sugimoto
BMC Gastroenterology.2020;[Epub] CrossRef
ECCO Position Paper: Harmonization of the Approach to Ulcerative Colitis Histopathology
Fernando Magro, Glen Doherty, Laurent Peyrin-Biroulet, Magali Svrcek, Paula Borralho, Alissa Walsh, Fatima Carneiro, Francesca Rosini, Gert de Hertogh, Luc Biedermann, Lieven Pouillon, Michael Scharl, Monika Tripathi, Silvio Danese, Vincenzo Villanacci, R
Journal of Crohn's and Colitis.2020; 14(11): 1503. CrossRef
Fecal calprotectin: current and future perspectives for inflammatory bowel disease treatment
Lorenzo Bertani, Maria Gloria Mumolo, Gherardo Tapete, Eleonora Albano, Giovanni Baiano Svizzero, Federico Zanzi, Linda Ceccarelli, Massimo Bellini, Santino Marchi, Francesco Costa
European Journal of Gastroenterology & Hepatology.2020; 32(9): 1091. CrossRef
What is the appropriate cut-off value of CRP to predict endoscopic remission in patients with ulcerative colitis in clinical remission?
Jongbeom Shin, Sung Min Kong, Gyeol Seong, Young-Ho Kim
International Journal of Colorectal Disease.2020; 35(12): 2249. CrossRef
Treat to target or ‘treat to clear’ in inflammatory bowel diseases: one step further?
Arianna Dal Buono, Giulia Roda, Marjorie Argollo, Eirini Zacharopoulou, Laurent Peyrin-Biroulet, Silvio Danese
Expert Review of Gastroenterology & Hepatology.2020; 14(9): 807. CrossRef
Incremental Benefit of Achieving Endoscopic and Histologic Remission in Patients With Ulcerative Colitis: A Systematic Review and Meta-Analysis
Hyuk Yoon, Sushrut Jangi, Parambir S. Dulai, Brigid S. Boland, Larry J. Prokop, Vipul Jairath, Brian G. Feagan, William J. Sandborn, Siddharth Singh
Gastroenterology.2020; 159(4): 1262. CrossRef
Assessing Severity of Disease in Patients with Ulcerative Colitis
Baldeep Singh Pabla, David Allen Schwartz
Gastroenterology Clinics of North America.2020; 49(4): 671. CrossRef
Colitis and Crohn’s Foundation (India) consensus statements on use of 5-aminosalicylic acid in inflammatory bowel disease
Ajit Sood, Vineet Ahuja, Vandana Midha, Saroj Kant Sinha, C. Ganesh Pai, Saurabh Kedia, Varun Mehta, Sawan Bopanna, Philip Abraham, Rupa Banerjee, Shobna Bhatia, Karmabir Chakravartty, Sunil Dadhich, Devendra Desai, Manisha Dwivedi, Bhabhadev Goswami, Kir
Intestinal Research.2020; 18(4): 355. CrossRef
‘Treat to Target’ in Mild to Moderate Ulcerative Colitis: Evidence to Support this Strategy
Arianna Dal Buono, Giulia Roda, Marjorie Argollo, Kristine Paridaens, Laurent Peyrin-Biroulet, Silvio Danese
Current Drug Targets.2020; 22(1): 117. CrossRef
What is the role of histopathology in the evaluation of disease activity in Crohn’s Disease?
Rish K. Pai, Vipul Jairath
Best Practice & Research Clinical Gastroenterology.2019;[Epub] CrossRef
Vedolizumab Trough Levels and Histological Healing During Maintenance Therapy in Ulcerative Colitis
Lieven Pouillon, Hélène Rousseau, Hélène Busby-Venner, Marcelo De Carvalho Bittencourt, Myriam Choukour, Guillaume Gauchotte, Camille Zallot, Silvio Danese, Cédric Baumann, Laurent Peyrin-Biroulet
Journal of Crohn's and Colitis.2019; 13(8): 970. CrossRef
Prediction of treatment outcome and relapse in inflammatory bowel disease
Jun Kato, Takeichi Yoshida, Sakiko Hiraoka
Expert Review of Clinical Immunology.2019; 15(6): 667. CrossRef
Role of Faecal Microbiota Transplantation for Maintenance of Remission in Patients With Ulcerative Colitis: A Pilot Study
Ajit Sood, Ramit Mahajan, Arshdeep Singh, Vandana Midha, Varun Mehta, Vikram Narang, Tarundeep Singh, Anmol Singh Pannu
Journal of Crohn's and Colitis.2019; 13(10): 1311. CrossRef
Mucosal healing in inflammatory bowel disease: Expanding horizon
Jimil Shah, Manik Lal Thakur, Usha Dutta
Indian Journal of Gastroenterology.2019; 38(2): 98. CrossRef
A Treat-to-Target Update in Ulcerative Colitis: A Systematic Review
Ryan Ungaro, Jean-Frédéric Colombel, Trevor Lissoos, Laurent Peyrin-Biroulet
American Journal of Gastroenterology.2019; 114(6): 874. CrossRef
A Simplified Definition of Histologic Improvement in Ulcerative Colitis and its Association With Disease Outcomes up to 30 Weeks from Initiation of Therapy: Post Hoc Analysis of Three Clinical Trials
Katherine Li, Richard Strauss, Colleen Marano, Linda E Greenbaum, Joshua R Friedman, Laurent Peyrin-Biroulet, Carrie Brodmerkel, Gert De Hertogh
Journal of Crohn's and Colitis.2019; 13(8): 1025. CrossRef
Can advanced endoscopic techniques for assessment of mucosal inflammation and healing approximate histology in inflammatory bowel disease?
Olga Maria Nardone, Rosanna Cannatelli, Davide Zardo, Subrata Ghosh, Iacucci Marietta
Therapeutic Advances in Gastroenterology.2019;[Epub] CrossRef
The emerging role of histologic disease activity assessment in ulcerative colitis
Rish K. Pai, Vipul Jairath, Niels Vande Casteele, Florian Rieder, Claire E. Parker, Gregory Y. Lauwers
Gastrointestinal Endoscopy.2018; 88(6): 887. CrossRef
Temporal clinical, proteomic, histological and cellular immune responses of dextran sulfate sodium-induced acute colitis
Natalia Schneider Nunes, Saejeong Kim, Maggie Sundby, Parwathy Chandran, Scott Robert Burks, Ana Helena Paz, Joseph Alan Frank
World Journal of Gastroenterology.2018; 24(38): 4341. CrossRef
Can histologic remission be a better prognostic factor and therapeutic target beyond endoscopic mucosal healing in patients with ulcerative colitis?
Hyo Jun Ahn, Sang-Bum Kang
Intestinal Research.2018; 16(1): 1. CrossRef

PubReader
ePub Link

Cite

CITE: export Copy Download Format; Close

Download Citation

Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

Format:

RIS — For EndNote, ProCite, RefWorks, and most other reference management software
BibTeX — For JabRef, BibDesk, and other BibTeX-specific software

Include:

Citation for the content below
Citation and abstract for the content below

Association of endoscopic and histological remission with clinical course in patients of ulcerative colitis

Intest Res. 2018;16(1):55-61. Published online January 18, 2018

DOI: https://doi.org/10.5217/ir.2018.16.1.55

XML Download

Figure

Related articles

Association of endoscopic and histological remission with clinical course in patients of ulcerative colitis

Fig. 1 Flow diagram depicting the patients enrolled and their long-term clinical follow-up.

Fig. 2 (A) Endoscopy Mayo score 0; (B) histopathological examination of the same patient exhibiting mild crypt distortion only (Geboes grade, 0.1) (H&E, ×200). (C) Endoscopy Mayo score 1; (D) histopathological examination of the same patient showing significant acute inflammatory infiltrates in the lamina propria along with evidence of cryptitis (Geboes grade, 3.1) (H&E, ×400).