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Xiao A, Yozu M, Kővári BP, Yassan L, Liao X, Salomao M, Westerhoff M, Sejben A, Lauwers GY, Choi WT. Nonconventional Dysplasia is Frequently Associated With Goblet Cell Deficient and Serrated Variants of Colonic Adenocarcinoma in Inflammatory Bowel Disease. Am J Surg Pathol 2024; 48:691-698. [PMID: 38546105 DOI: 10.1097/pas.0000000000002217] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 05/16/2024]
Abstract
Various subtypes of nonconventional dysplasia have been recently described in inflammatory bowel disease (IBD). We hypothesized that goblet cell deficient dysplasia and serrated dysplasia may be the primary precursor lesions for goblet cell deficient (GCDAC) and serrated (SAC) variants of colonic adenocarcinoma, respectively. Clinicopathologic features of 23 GCDAC and 10 SAC colectomy cases were analyzed. All dysplastic lesions found adjacent to the colorectal cancers (n = 22 for GCDACs and n = 10 for SACs) were subtyped as conventional, nonconventional, or mixed-type dysplasia. As controls, 12 IBD colectomy cases with well to moderately differentiated adenocarcinoma that lacked any mucinous, signet ring cell, low-grade tubuloglandular, or serrated features while retaining goblet cells throughout the tumor (at least 50% of the tumor) were evaluated. The cohort consisted of 19 (58%) men and 14 (42%) women, with a mean age of 53 years and a long history of IBD (mean duration: 18 y). Twenty-seven (82%) patients had ulcerative colitis. GCDACs (57%) were more often flat or invisible than SACs (10%) and controls (25%; P = 0.023). The GCDAC and SAC groups were more likely to show lymphovascular invasion (GCDAC group: 52%, SAC group: 50%, control group: 0%, P = 0.001) and lymph node metastasis (GCDAC group: 39%, SAC group: 50%, control group: 0%, P = 0.009) than the control group. Notably, GCDACs and SACs were more frequently associated with nonconventional dysplasia than controls (GCDAC group: 77%, SAC group: 40%, control group: 0%, P < 0.001). Goblet cell deficient dysplasia (73%) was the most prevalent dysplastic subtype associated with GCDACs ( P = 0.049), whereas dysplasias featuring a serrated component (60%) were most often associated with SACs ( P = 0.001). The GCDAC group (75%) had a higher rate of macroscopically flat or invisible synchronous dysplasia compared with the SAC (20%) and control (33%) groups ( P = 0.045). Synchronous dysplasia demonstrated nonconventional dysplastic features more frequently in the GCDAC (69%) and SAC (40%) groups compared with the control group (0%; P = 0.016). In conclusion, goblet cell deficient dysplasia and dysplasias featuring a serrated component could potentially serve as high-risk markers for GCDACs and SACs, respectively.
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Affiliation(s)
- Andrew Xiao
- Department of Pathology, University of California, San Francisco, CA
| | - Masato Yozu
- Department of Histopathology, Middlemore Hospital, Auckland, New Zealand
| | - Bence P Kővári
- Department of Pathology, H. Lee Moffitt Cancer Center, Tampa, FL
| | - Lindsay Yassan
- Department of Pathology, University of Chicago, Chicago, IL
| | - Xiaoyan Liao
- Department of Pathology, University of Rochester, Rochester, NY
| | | | | | - Anita Sejben
- Department of Pathology, Albert Szent-Györgyi Medical School, Szeged, Hungary
| | | | - Won-Tak Choi
- Department of Pathology, University of California, San Francisco, CA
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Enea D, Lauwers G, Svrcek M. [Conventional and non-conventional dysplasia in patients with inflammatory bowel disease]. Ann Pathol 2023:S0242-6498(23)00049-4. [PMID: 36906454 DOI: 10.1016/j.annpat.2023.02.006] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/03/2023] [Revised: 02/16/2023] [Accepted: 02/20/2023] [Indexed: 03/11/2023]
Abstract
Compared to the general population, patients with inflammatory bowel disease (IBD), both ulcerative colitis (UC) or Crohn's disease (CD), are at increased risk of developing some cancers, particularly colorectal cancers (CRC). CRCs, the vast majority of which are adenocarcinomas, develop from a precancerous lesion called dysplasia (or intraepithelial neoplasia) via an inflammation-dysplasia-adenocarcinoma sequence. The advancements of new endoscopic techniques, including visualisation and resection techniques, has led to a reclassification of dysplasia lesions into visible and invisible lesions and their therapeutic management, with a more conservative approach to the colorectal setting. In addition, besides conventional dysplasia, of intestinal phenotype, classically described in IBD, non-conventional dysplasias (as opposed to conventional dysplasia of intestinal phenotype) are now described, including at least seven subtypes. Recognition of these unconventional subtypes, which are still poorly known from pathologists, is becoming crucial, as some of these subtypes appear to be at high risk of developing advanced neoplasia (i.e. high-grade dysplasia or CRC). This review briefly describes the macroscopic features of dysplastic lesions in IBD, as well as their therapeutic management, followed by the clinicopathological features of these dysplastic lesions, with particular emphasis on the new subtypes of unconventional dysplasia, both from a morphological and molecular point of view.
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Affiliation(s)
- Diana Enea
- Sorbonne université, Assistance publique-Hôpitaux de Paris, hôpital Saint-Antoine, service d'anatomie et cytologie pathologiques, SIRIC CURAMUS, Paris, France
| | - Grégory Lauwers
- Department of Pathology, H. Lee Moffitt Cancer Center and Research Institute and Departments of Pathology and Oncologic Sciences, University of South Florida, Tampa, FL, États-Unis
| | - Magali Svrcek
- Sorbonne université, Assistance publique-Hôpitaux de Paris, hôpital Saint-Antoine, service d'anatomie et cytologie pathologiques, SIRIC CURAMUS, Paris, France.
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Li Y, Wang HL. Influence of SCENIC recommendations on terminology used for histopathologic diagnosis of inflammatory bowel disease-associated dysplasia. World J Gastrointest Oncol 2022; 14:1375-1387. [PMID: 36160744 PMCID: PMC9412923 DOI: 10.4251/wjgo.v14.i8.1375] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/27/2022] [Revised: 07/18/2022] [Accepted: 08/06/2022] [Indexed: 02/05/2023] Open
Abstract
BACKGROUND Published in 2015, the International Consensus Recommendations on Surveillance for Colorectal Endoscopic Neoplasia Detection and Management in Inflammatory Bowel Disease Patients (SCENIC) recommended abandoning the use of diagnostic term "dysplasia-associated lesion or mass (DALM)" for polypoid dysplastic lesions detected in patients with inflammatory bowel disease (IBD). The aim of this study was to investigate whether this recommendation had any influence on diagnostic terminologies used by pathologists in their practice. METHODS We retrospectively reviewed all pathology reports for surveillance colonoscopic biopsies from ulcerative colitis (UC) patients in our institution during 1/2012-12/2014 (pre-SCENIC) and 1/2016-12/2018 (post-SCENIC). These included 1203 biopsies from 901 UC patients during the pre-SCENIC period and 1273 biopsies from 977 UC patients during the post-SCENIC period. Their corresponding endoscopic findings and histopathologic diagnoses were recorded. Clinical indications for total colectomy for UC patients and corresponding histopathologic findings in colectomy specimens were also recorded and compared. RESULTS A total of 347 and 419 polyps/polypoid lesions were identified during the pre-SCENIC and post-SCENIC periods, among which 60 and 104 were dysplastic/adenomatous, respectively. More polypoid dysplastic lesions were simply diagnosed as "adenoma" during the post-SCENIC period in comparison with the pre-SCENIC period (97.1% vs 65.0%; P < 0.001). The number of cases with a comment in pathology reports regarding the distinction between DALM and sporadic adenoma was also significantly decreased during the post-SCENIC period (5.8% vs 38.3%; P < 0.001). In addition, the term "dysplasia" was more consistently used for random biopsies during the post-SCENIC period. Furthermore, the terms "sessile serrated adenoma/polyp" (SSA/P) and "serrated epithelial change" (SEC) were more consistently used for polypoid lesions and random biopsies, respectively, during the post-SCENIC period, although these were not specifically addressed in the SCENIC recommendations. The indications for colectomy remained unchanged, however, despite the standardization of diagnostic terminologies. CONCLUSION The SCENIC recommendations relieve pathologists from the burden of distinguishing DALM from sporadic adenoma in IBD patients, which helps the standardization of diagnostic terminologies used by pathologists. The consistent use of the diagnostic terminologies may help reduce potential confusions to clinicians and patients.
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Affiliation(s)
- Yuan Li
- Department of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, CA 90095, United States
- Department of Pathology, Molecular Pathology Research Center, Peking Union Medical College Hospital, Chinese Academy of Medical Science, Beijing 100730, China
| | - Hanlin L Wang
- Department of Pathology and Laboratory Medicine, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, CA 90095, United States
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Choi WT, Kővári BP, Lauwers GY. The Significance of Flat/Invisible Dysplasia and Nonconventional Dysplastic Subtypes in Inflammatory Bowel Disease: A Review of Their Morphologic, Clinicopathologic, and Molecular Characteristics. Adv Anat Pathol 2022; 29:15-24. [PMID: 34469911 DOI: 10.1097/pap.0000000000000316] [Citation(s) in RCA: 15] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/26/2022]
Abstract
Patients with inflammatory bowel disease are at significantly increased risk of dysplasia and colorectal cancer (CRC). The early detection, histologic grading, and removal of dysplasia plays a critical role in preventing the development of CRC. With advances in endoscopic visualization and resection techniques, colectomy is no longer recommended to manage dysplasia, unless surveillance colonoscopy detects flat/invisible dysplasia (either high-grade dysplasia or multifocal low-grade dysplasia) or an endoscopically unresectable lesion. Although there are numerous review articles and book chapters on the morphologic criteria of conventional (intestinal type) dysplasia, the most well-recognized form of dysplasia, at least 7 distinct nonconventional morphologic patterns of epithelial dysplasia have been recently described in inflammatory bowel disease. Most practicing pathologists are not familiar with these nonconventional subtypes and thus, may even overlook some of these dysplastic lesions as benign or reactive. However, the recognition of these subtypes is important, as some of them appear to have a high risk of developing advanced neoplasia (high-grade dysplasia or CRC) and often show molecular alterations characteristic of advanced neoplasia. This review briefly describes the morphologic criteria of conventional dysplasia but predominantly focuses on all 7 nonconventional subtypes as well as our understanding of their clinicopathologic and molecular features that can assist in their risk stratification.
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Affiliation(s)
- Won-Tak Choi
- Department of Pathology, University of California at San Francisco, San Francisco, CA
| | - Bence P Kővári
- Department of Pathology, H. Lee Moffitt Cancer Center, Tampa, FL
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Choi WT. Non-conventional dysplastic subtypes in inflammatory bowel disease: a review of their diagnostic characteristics and potential clinical implications. J Pathol Transl Med 2021; 55:83-93. [PMID: 33677953 PMCID: PMC7987516 DOI: 10.4132/jptm.2021.02.17] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/15/2021] [Accepted: 02/17/2021] [Indexed: 12/26/2022] Open
Abstract
The early detection and grading of dysplasia is the current standard of care to minimize mortality from colorectal cancer (CRC) in patients with inflammatory bowel disease. With the development of advanced endoscopic resection techniques, colectomy is now reserved for patients with invisible/flat dysplasia (either high-grade [HGD] or multifocal low-grade dysplasia) or endoscopically unresectable lesions. Although most pathologists are familiar with the morphologic criteria of conventional (intestinal type) dysplasia, the most well-recognized form of dysplasia, an increasing number of diagnostic material has led to the recognition of several different morphologic patterns of epithelial dysplasia. The term “non-conventional” dysplasia has been coined to describe these changes, but to date, the recognition and full appreciation of these novel forms of dysplasia by practicing pathologists is uneven. The recognition of these non-conventional subtypes is becoming increasingly important, as some of them appear to have a higher risk of developing HGD or CRC than conventional dysplasia or sporadic adenomas. This review describes the morphologic characteristics of all seven non-conventional subtypes that have been reported to date as well as our current understanding of their clinicopathologic and molecular features that distinguish them from conventional dysplasia or sporadic adenomas.
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Affiliation(s)
- Won-Tak Choi
- Department of Pathology, University of California at San Francisco, San Francisco, CA, USA
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Pereira D, Kővári B, Brown I, Chaves P, Choi WT, Clauditz T, Ghayouri M, Jiang K, Miller GC, Nakanishi Y, Kim KM, Kim BH, Kumarasinghe MP, Kushima R, Ushiku T, Yozu M, Srivastava A, Goldblum JR, Pai RK, Lauwers GY. Non-conventional dysplasias of the tubular gut: a review and illustration of their histomorphological spectrum. Histopathology 2021; 78:658-675. [PMID: 33124049 DOI: 10.1111/his.14294] [Citation(s) in RCA: 10] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/06/2023]
Abstract
The increasing use of gastrointestinal endoscopic procedures has led to the recognition by histopathologists of non-conventional (or special-type) dysplasias of the gastrointestinal tract. These lesions can be recognised in association with prevalent underlying gastrointestinal conditions, such as Barrett oesophagus, chronic atrophic gastritis, and inflammatory bowel disease. The diagnosis of these special types can be challenging, and their biological behaviours are not fully characterised. The aim of this review is to provide a global view of non-conventional dysplastic lesions observed in the various segments of the tubular gastrointestinal tract and describe their salient features. Furthermore, as the clinical implications of these various subtypes have not been broadly tested in practice and are not represented in most management guidelines, we offer guidance on the best management practices for these lesions.
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Affiliation(s)
- Daniela Pereira
- Serviço de Anatomia Patológica, Instituto Português de Oncologia de Lisboa de Francisco Gentil-EPE (IPOLFG EPE), Lisboa, Portugal.,Faculdade de Ciências da Saúde, Universidade da Beira Interior (FCS UBI), Covilhã, Portugal
| | - Bence Kővári
- Department of Pathology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA.,Department of Pathology, University of Szeged, Szeged, Hungary.,Albert Szent-Györgyi Health Centre, Szeged, Hungary
| | - Ian Brown
- Envoi Specialist Pathologists, Brisbane, Qld, Australia.,Faculty of Medicine, University of Queensland, Brisbane, Qld, Australia
| | - Paula Chaves
- Serviço de Anatomia Patológica, Instituto Português de Oncologia de Lisboa de Francisco Gentil-EPE (IPOLFG EPE), Lisboa, Portugal.,Faculdade de Ciências da Saúde, Universidade da Beira Interior (FCS UBI), Covilhã, Portugal
| | - Won-Tak Choi
- Department of Pathology, University of California at San Francisco, San Francisco, CA, USA
| | - Till Clauditz
- Department of Pathology, University-Medical Centre Hamburg-Eppendorf, Hamburg, Germany
| | - Masoumeh Ghayouri
- Department of Pathology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA.,Department of Pathology and Cell Biology, University of South Florida, Tampa, FL, USA.,Department of Oncological Sciences, University of South Florida, Tampa, FL, USA
| | - Kun Jiang
- Department of Pathology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA.,Department of Pathology and Cell Biology, University of South Florida, Tampa, FL, USA.,Department of Oncological Sciences, University of South Florida, Tampa, FL, USA
| | - Gregory C Miller
- Envoi Specialist Pathologists, Brisbane, Qld, Australia.,Faculty of Medicine, University of Queensland, Brisbane, Qld, Australia
| | - Yukihiro Nakanishi
- Department of Pathology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA.,Department of Pathology and Cell Biology, University of South Florida, Tampa, FL, USA.,Department of Oncological Sciences, University of South Florida, Tampa, FL, USA
| | - Kyoung M Kim
- Department of Pathology, Samsung Medical Centre, Seoul, Korea
| | - Baek H Kim
- Department of Pathology, Korea University Guro Hospital, Seoul, Korea
| | | | - Ryoji Kushima
- Department of Pathology, Shiga University of Medical Science, Otsu, Japan
| | - Tetsuo Ushiku
- Department of Pathology, The University of Tokyo, Tokyo, Japan
| | - Masato Yozu
- Histopathology Department, Middlemore Hospital, Auckland, New Zealand
| | | | - John R Goldblum
- Department of Anatomic Pathology, Cleveland Clinic, Cleveland, OH, USA
| | - Rish K Pai
- Department of Laboratory Medicine and Pathology, Mayo Clinic Arizona, Scottsdale, AZ, USA
| | - Gregory Y Lauwers
- Department of Pathology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA.,Department of Pathology and Cell Biology, University of South Florida, Tampa, FL, USA.,Department of Oncological Sciences, University of South Florida, Tampa, FL, USA
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