World J Gastroenterol 2015 March 14; 21(10): 2896-2904 ISSN 1007-9327 (print) ISSN 2219-2840 (online)
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MINIREVIEWS
Endoscopic and histologic characteristics of serrated lesions Driffa Moussata, Gilles Boschetti, Marion Chauvenet, Karine Stroeymeyt, Stéphane Nancey, Françoise Berger, Thierry Lecomte, Bernard Flourié serrated pathway and includes three types of polyp, characterised by a serrated appearance of the crypts: hyperplastic polyps (HP), sessile serrated adenomas (SSA) or lesions, and traditional serrated adenomas. Each lesion has its own genetic, as well as macroscopic and microscopic morphological features. Because of their flat aspect, their detection is easier with chromoendoscopy (carmin indigo or narrow-band imaging). However, as we show in this review, the distinction between SSA and HP is quite difficult. It is now recommended to resect in one piece as it is possible the serrated polyps with a control in a delay depending on the presence or not of dysplasia. These different types of lesion are described in detail in the present review in general population, in polyposis and in inflammatory bowel diseases patients. This review highlights the need to improve characterization and understanding of this way of colorectal cancerogenesis.
Driffa Moussata, Gilles Boschetti, Marion Chauvenet, Karine Stroeymeyt, Stéphane Nancey, Bernard Flourié, Department of Gastroenterology, Lyon Sud Hospital, 69310 Pierre Bénite, France Driffa Moussata, Inserm Unit CREATIS - UMR5220 INSERM1044, Lyon University, 69100 Villeurbanne, France Françoise Berger, Department of Pathology, Hôpital Lyon Sud, 69310 Pierre Bénite, France Thierry Lecomte, Department of Gastroenterology, Tours Hospital, 37000 Tours, France Author contributions: Moussata D has written the review; Boschetti G, Chauvenet M and Stroeymeyt K have contributed to conception and acquisition of data; Berger F has revised the pathologic data; Flourié B, Nancey S and Lecomte T have revised and approved the final version to be published. Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/ licenses/by-nc/4.0/ Correspondence to: Driffa Moussata, MD, PhD, Department of Gastroenterology, Lyon Sud Hospital, 165 chemin du Grand Revoyet, 69310 Pierre Bénite, France. [email protected] Telephone: +33-478-861290 Fax: +33-478-861063 Received: July 7, 2014 Peer-review started: July 7, 2014 First decision: August 6, 2014 Revised: August 25, 2014 Accepted: October 14, 2014 Article in press: October 15, 2014 Published online: March 14, 2015
Key words: Hyperplastic polyp; Traditional serrated adenoma; Serrated polyposis; Sessile serrated adenoma; Endoscopy; Endomicroscopy; Histology © The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
Core tip: The serrated lesions belong to a new carcinogenesis way of colorectal cancer which is important to know and detect. Even though endoscopic techniques have improved, some difficulties remain in terms of detection because of the lesions’ shape and aspect and the fact that the endoscopists have to be aware of some characteristics. However, we argue in this article that the endoscopists have to be trained so the recognition of these pre-neoplastic lesions can be improved. Furthermore, there is a necessity to communicate well with the pathologists. This article is a review of the knowledge we currently have of serrated lesions, and their endoscopic and histologic aspects which every gastroenterologist needs to know.
Abstract In recent years, a second pathway for colonic carcinogenesis, distinct from the adenomatous pathway, has been explored. This is referred to as
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Moussata D et al . Review of serrated polyps of the crypts in the proliferative zone for the other types of SP. As a consequence, with the maturation zones extending onto both sides of the proliferative zone, the cryptic “branched” type of architecture associated with an accumulation of cells at the surface [13] produces this serrated appearance . In 2010, a new World Health Organisation (WHO) histological classification was elaborated, to improve the inter-observer reproducibility of pathological [14] diagnosis . Although the kappa has been significantly increased, the global kappa remains middle (k = 0.55), in a European study involving expert anatomic [15] pathologists . This low reproducibility can be explained by the small size of the samples and the difficulty in orienting the crypts, with respect to the basal membrane, which is not always present on the samples.
Moussata D, Boschetti G, Chauvenet M, Stroeymeyt K, Nancey S, Berger F, Lecomte T, Flourié B. Endoscopic and histologic characteristics of serrated lesions. World J Gastroenterol 2015; 21(10): 2896-2904 Available from: URL: http://www.wjgnet. com/1007-9327/full/v21/i10/2896.htm DOI: http://dx.doi. org/10.3748/wjg.v21.i10.2896
INTRODUCTION Conventionally, dysplastic lesions and non-neoplastic lesions (hyperplastic or metaplastic) were distinguished [1] by their degenerative potential. In 1983, Jass was one of the first to defend the idea that there could be a link between hyperplastic polyps (HP) and colorectal cancer. Since then, it has been demonstrated that HP have proliferative, but not necessarily dysplastic anomalies, which are related to mutations of genes [2,3] such as the KRAS or BRAF . HP belong to a heterogeneous group of lesions, which are said to be serrated, because of the jagged appearance of their crypts, and which also include sessile serrated adenomas (SSA) and traditional sessile serrated adenomas (TSA). They represent [4] approximately 36% of polyps , and cancers arising from the serrated pathway are thought to represent around 20% of all colorectal cancers and more than [5,6] 30% of intervallic cancers . The risk factors associated with the occurrence of serrated polyps (SP) are similar to those described in the case of conventional adenomas. Tobacco appears to have a greater influence on the number of SP, but paradoxically has no influence on cancer cases, [7,8] which may develop from them . In addition, it has been shown that the presence of SP could increase, by a factor of three, the risk of an advanced-stage adenoma (villous or supra-centimeter adenoma, or adenoma with high-grade dysplasia) or a synchronous [9,10] or metachronous cancer . There are thus two advantages of detecting SP, as a consequence resulting not only from their own degenerative potential, but also from the aforementioned association.
CARCINOGENIC PATHWAY The molecular alterations observed in SP include mainly Braf mutations (V600E) and Kras mutations (codon 12 and 13), associated with a hyper-methylation of the region, which promotes some genes referred to as CIMP (CpG Island Methylation Promoter). The CpG islets are di-nucleotide regions, rich in cytosine [2,16] guanine at the level of region 5’ . This phenomenon can alter the expression of the genes involved in oncogenesis, such as p16, MGMT ‘MethylGuanine DNA [2,16] Methyltransferase) or MLH1 . The CIMP pathway is thought to be involved in approximately 30% of [17] colorectal cancer cases and nearly 90% of CIMP+ [16] colorectal cancers have a Braf or Kras mutation . The prevalence of these anomalies varies according to the type of SP (Table 1). Braf and Kras mutations activate the MAPK-ERK pathway leading to decreased apoptosis and cellular proliferation with at least the formation [18] of hyperplastic crypts . This is counteracted by a protective phenomen called oncogene-induced [19] senescence (Figure 1 ). Schematically, there appear to be 2 parallel pathways, depending on the gene involved: (1) braf mutation, often associated with CIMP+, presenting a satellite stability or instability depending on the involvement of MLH1; and (2) Kras mutation, often associated with a low level of microsatellite instability, [20] and inactivation of the MGMT gene . In the first case, the tumours are very often located in the proximal colon, like SSA, and in the second case they are often located in the distal colon, like TSA. It is interesting to note that whereas MLH1 methylation occurs frequently, a high level of microsatellite instability is rare, probably because this event occurs late during the [21] carcinogenesis of SP . However, that would not be so simple because, recently, some authors have shown that SSA as HP could be associated with TSA, that would suggest that they could be precursor-lesions of TSA. In this case, TSA present a lower and a higher frequency of Kras and Braf mutations, respectively,
PHYSIOPATHOLOGY The intestinal epithelium is made up of two major types of cell: absorptive cells (colonocytes) and secreting cells (goblet cells, endocrine cells and Paneth cells) originating from stem cells situated in the lower third of the crypts. These cells are differentiated by their migration towards the surface of the crypts, except in the case of Paneth cells, which reside at the base of the crypts. Hyperplasia of the crypts is the result of the equilibrium established between a level [11] [12] of proliferation and apoptosis . Torlakovic et al have shown that HP are caused by an extension of the proliferative zone beyond the lower third of the crypts, and displacement or ectopic formation along the length
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Moussata D et al . Review of serrated polyps Table 1 Serrated polyps characteristics
Frequency among polyps Dominant sex Macroscopy Size Paris classification Localization Pit pattern « Kudo » Microscopy Crypts
Hyperplastic polyps
Sessile serrated adenoma
Traditional serrated adenoma
28 à 42% Male
9% Female
1% No ascendancy
< 5 mm Ⅱa distal, rectum Ⅱ
> 5 mm Ⅰs, Ⅱa proximal, 27% distal Ⅱ-O (Open)
> 5 mm Ⅰp, Ⅰs distal Ⅱ-Ⅲs or ⅢL
Serrated aspect on the superior half of the crypts
Upper third serrated aspect of crypts, horizontalization of the third inferior of crypts aspect of “boot” or L Important mucus, small nuclear modifications Increased proliferative index with degenerative risk Braf (82%), CIMP-H, méthylation MLH1
Aspect serrated on all the crypt, ectopique crypts
Epithelium
Cylindrical
Maturation, degenerative potential Molecular
Normal index of proliferation, no degenerative potential +/- Braf, Kras, MSI (29%)
tubulo-villous dysplasia (37%), carcinoma (11%) Increased proliférative index with degenerative risk Kras (30%-80%), CIMP-L, méthylation MGMT
MSI: Microsatellites instability; CIMP-H, CIMP-L: CpG island methylation promotor-high, CIMP-bas; MLH1: MutL homolog 1; MGMT: MethylGuanine DNA methyltransferase.
MAPK ↑
BRAF mutation
KRAS mutation
Apoptosis ↓ SSA
TSA
CpG island methylation
MLH1 meth
MGMT meth CpG island methylation
P16 meth
Serration
CIMP-H
BRAF mut CIMP-H MSS
BRAF mut CIMP-H MSI
CIMP-L
Molecular profile
KRAS mut CIMP-L MSI-L
KRAS mut CIMP-L MSS
Figure 1 Schematic representation of the sessile and traditional serrated pathways[18]. MSI: Microsatellites instability; CIMP-H, CIMP-L: CpG island methylation promotor-high, CIMP-bas; MLH1: MutL homolog 1; MGMT: MethylGuanine DNA methyltransferase; SSA: Sessile serrated adenomas.
Endoscopic aspect
[22]
compared with TSA with no precursor lesion
.
Their macroscopic appearance is very often of type Ⅱa in Paris classification, and they are smaller than 5 mm in size.
MORPHOLOGY OF SERRATED LESIONS HP
HP are the most frequently encountered serrated lesions (75%-80%) and represent 28% to 42% of endoscopically detected polyps, with a higher [4] prevalence in men (Table 2). They are located mainly in the distal colon and the rectum.
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Chromo-endoscopy: The crypt opening is star-shaped, [23] corresponding to type Ⅱ in the Kudo classification . Narrow-band imaging: On the basis of 3 criteria (color, shape of the pits and pattern of vessels), NICE
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Sessile serrated lesions or SSA
Table 2 Endoscopic follow-up according to United States Multi[39] Society Task Force on Colorectal Cancer and European [40] Society of Gastrointestinal Endoscopy Serrated polyps HP SSA without dysplasia SSA with dysplasia TSA Serrated polyposis
With a frequency of occurrence corresponding to 15% to 20% of SP and 9% of all types of polyp, SSA are the most common lesions following HP. Just like TSA, the use of an adenomatous denomination leads to confusion, since they do not necessarily present dysplasia. However, some authors persist in using this designation in order to emphasize their degenerative risk. They are most commonly detected in women at an average age of approximately 60 years.
Follow-up according to United Follow-up according [39] [40] States multi-society to ESGE 5 yr, if > 10 mm or proximal < 3 lesions, < 1 cm: 5 yr ≥ 3, > 1 cm: 3 yr 3 yr
10 yr 10 yr
3 yr 1 yr
3 yr 1 yr
3 yr
Endoscopic aspect
In a retrospective study, more than 4000 polyps labelled as HP were revisited, and from multivariate analysis, a size > 5 mm and a location in the proximal colon were identified as discriminating criteria in favour [31] of SSA . They are very commonly of type IIa in Paris classification, and standard endoscopic screening is not straightforward as a consequence of their irregular boundaries and fuzzy appearance, which arise from the abundant presence of mucous (Figure 3). However, some authors have shown that education and training of the endoscopists could improve the recognition of these lesions, even with conventional whitelight [32] colonoscopies (worldwide available) . Rightside location, flat morphology, red-colored surface and presence of a mucus cap were independently associated with SSA histology. Recognition of these features during conventional colonoscopy may improve [33] the SSA detection rate .
ESGE: European Society of Gastrointestinal Endoscopy; HP: Hyperplastic polyps; SSA: Sessile serrated adenomas.
[24]
classification characterizes HP lesions with the same color or lighter than the background and without any vessel. They could also present dark or white spots of uniform size. Endomicroscopy: The confocal endomicroscopy (CEM) is an endoscopic technique, which enables us to perform an in-vivo histologic diagnosis during the endoscopy after fluoroscein has been injected intravenously. Several studies have shown that CEM has a [25,26] good correlation with histology and increases the dysplastic yield of biopsies particularly in inflammatory [27] bowel diseases (IBD) patients . However, no data is available about the different types of serrated polyps. In our experience, CEM (EC3870K Pentax, Tokyo), which can explore the mucosa from the surface to a depth of 270 microns, the crypts of HP lesions present anomalies at the surface with a lumen of the crypts larger with a stellar shape, whereas deeper, the crypts and the lumen are round, as in normal mucosa.
Chromoendoscopy: In addition to conventional type [23] Ⅱ pit pattern according to Kudo’s classification , [34] Kimura et al has reported that the surface architecture of the lesions was also broadly categorized as type Ⅱ-Open (type Ⅱ-O), type Ⅱ-Long (type Ⅱ-L), or type Ⅳ-Serrated (type Ⅳ-S). Ishigooka has shown that either type Ⅱ-O alone or partial type Ⅱ-O is the basic architecture, with SSA/Ps histology evident in 83.7% of cases. Others have shown that the type Ⅱ-O is highly specific (97%) but of low sensitivity (65%). This corresponds to the association of the star-shaped and very broad appearance of the crypts, which is probably related to the abundant presence of [31] mucous (Figure 3).
Histology
Microscopically, they are characterised by enlarged crypts, of which the upper half has a serrated architecture. The proliferative zone is located at the base of the crypts, which have a regular appearance. Homogeneous nuclei are located at the base of the cells. These lesions can be classified into several subtypes: (1) micro-vesicular HP, 2 times more common than; (2) HP rich in caliciform cells and 25 times more [28] common than; and (3) low mucin content cells . As this distinction currently has no clinical significance, it is not described in detail by pathologists, but makes it possible to understand why their endoscopic appearance can be so different (Figure 2). In addition, it has been shown that the presence of several HP in the distal colon is often associated with an increased [29] risk of serrated lesions in the proximal colon . Finally, some authors have suggested considering HP to be neoplastic lesions, since in 29% of cases microsatellite instability is observed, and depending on their HP sub[30] type, Braf or Kras mutations are detected .
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Narrow-band imaging: According to narrow-band imaging (NBI) International Colorectal Endoscopic classification system (NICE), SSA present a mixed [24] spectrum of features between HP and adenomas and that is why some authors concluded that this classification is insufficient to accurately distinguish [35] [36] SSA from HP . Hazewinkel et al have reported in a retrospective study that in white-light endoscopy, indistinctive borders and cloud-like surface are 2 independent predictive characteristics of SSA with 2 others features in NBI as an irregular shape and dark spots inside the crypts. A sensitivity, specificity
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A
B
C
Figure 2 Hyperplastic polyp in chromoendoscopy (A), histology (B) and confocal endomicroscopy (C).
A
B
C
Figure 3 Sessile serrated adenoma in chromoendoscopy (A), confocal endomicroscopy (B) and histology (C)
and overall accuracy of, respectively, 75%, 79% and 77% on WLE and 89%, 96% and 93%on NBI were [36] obtained .
fact, their proliferation zone can be located at the midheight of the crypts, with mature goblet cells located at their base. SSA are distinguished from HP using the following characteristics: (1) a serrated appearance at the base of the crypts, together with a more jagged appearance at the surface; (2) horizontalization of the crypts with more collaterally branched crypts; (3) dilatation of the crypts; (4) an increase in epitheliumstroma ratio > 50%; (5) mitoses on the surface of the crypts; and (6) cellular atypia such as an enlarged nucleus and overproduction of mucin (Figure 3). One consensus suggests that at least 2 of the 6 criteria should be present on at least 2 well-separated crypts. These criteria were validated in a study involving several pathologists, with good inter-observer
Confocal endomicroscopy: The architecture of the crypts is modified and dilated by the presence of a great deal of mucous, which appears in black on the endomicroscopic images. The lumen is enlarged and presents a stellar shape as in histology. In practice, in endomicroscopy, it is easier to recognize SSA than HP.
Histology
Like HP, SSA do not systematically present with cytological signs of dysplasia, however unlike HP, they have an abnormal architecture and proliferation. In
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A
B
C
Figure 4 Traditional serrated polyp in chromoendoscopy (A), confocal endomicroscopy (B) and histology (C). [15]
agreement
.
longer in contact with the muscularis propria, thus distinguishing them from SSA (Figure 4). They are characterised by an abundant eosinophilic cytoplasm [28] and elongated nuclei .
TSA These represent approximately 6% of SP, i.e., 1% [37] of all polyps, and are more common in Asia . They can be pedunculated or serrated, or even flat, and are more common in the distal colon (60%) and in patients whose age is close to 60 years, with no [4] distinction of sex .
SPECIAL CASE OF SERRATED POLYPOSIS
Endomicroscopy: In the literature, there is no specific description of these polyps in endomicroscopy, probably because of the low frequency. However, on endomicrosocpy, the crypts appear tubular as in adenoma lesions with low grade dysplasia and horizontalized that is characterized these lesions. The lumen is dilated and has a stellar shape. At the surface, the aspect is like a lace with cellular proliferation.
The diagnostic criteria for serrated polyposis were initially defined by Burt and Jass in 2000, and have recently been updated under the name of serrated [14] polyposis . Its definition is based on at least one of the following criteria: (1) at least 5 SP situated in the proximal colon, as far as the sigmoid colon, of which 2 are at least supra-centimetric; (2) whatever st the number of HP, a history of one 1 degree relative presenting with serrated polyposis; and (3) more than 20 HP, whatever their size or location. [29] Its incidence is estimated to be 1 per 100000 . It affects both sexes and is often diagnosed at around [21] the age of 55-65 years . The risk of cancer is 5 times higher than in general population. Two variants are described: type 1: serrated polyposis including the different serrated types, associated with adenomas; type 2: including the conventional hyperplastic polyps (< 5 mm), with a low risk of cancer. As a result of various different definitions, it has been suggested that each type could correspond to a different genetic pathway, with no possibility at the present time of stating whether the transmission is [39] recessive or dominant . Surgery is indicated in the case of cancer or when it is impossible to carry out an endoscopic inspection, with yearly monitoring. Family screening should of course be adopted as a standard st procedure for 1 degree relatives after the age of 40, [30] or 10 years prior to the age of the cancer .
HISTOLOGY
IBD
Microscopically, they show signs of dysplasia in 37% of cases, associated with an intramucosal carcinoma in 11% of cases. They have serrated crypts aligned perpendicularly to the crypt axis, characteristic of these lesions, with the presence of ectopic crypts no
In 1967, Morson et al were the first to describe flat pre-cancerous lesions with a pseudo-villous appearance, occurring in association with IBD. Histologically, they observed that the crypts lost their parallelism with a poorly positioned proliferation zone removed from the
Endoscopic aspect
Chromoendoscopy: In chromoendoscopy, TSA associate type Ⅱ with types Ⅲs or ⅡL and a [4] slightly textured or lobular surface (Figure 4) . The [38] characteristics of TSAs are often reddish in color . A further characteristic that was not included in this study is that some flat lesions show a surface architecture that can be described as highly protruding [34] double elevation, pinecone-shaped, or coral-shaped . In Ishigooka’s study, TSAs accounted for 76.9% (30/39) of lesions with a basic architecture of type Ⅳ-S pit pattern, and lesions without type Ⅳ-S pit pattern could be classified as non-TSAs with 96.7% sensitivity and 88.9% specificity. The authors concluded that type Ⅳ-S pit pattern can be considered a characteristic [38] finding of TSAs .
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[40]
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B
C
Figure 5 Endoscopic (A), endomicroscopic (B) and histologic (C) characteristics of serrated lesions in patients with inflammatory bowel disease.
muscularis mucosa and closer to the surface. Kilgore identified mucosa with a hyperplastic appearance surrounding and further away from the cancer, on surgical specimens from the colon of Crohn’s disease patients, in 30% of cancer patients, as opposed to [41] [42] 10% in the control group . Rubio et al compared the appearance of tissue surrounding carcinomatous lesions in IBD patients with that in control patients (sporadic adenocarcinoma). They observed a serrated appearance in 22% (11/50) of IBD cases, as opposed to 2% (1/50) in the control group. The same authors have reported a strong prevalence (34.5%) of serrated lesions in patients having IBD in the absence of [43] carcinoma . It has been hypothesised that a chronic inflammation could lead to exaggerated proliferation at the level of the basal portion of the crypts, associated with abnormal regeneration phenomena, producing these serrated lesions, with dysplasia at the base [42] of the crypts . From our own experience, a wellidentified serrated appearance is indeed observed under endomicroscopy, corresponding exactly to the aforementioned descriptions, but remaining quite different from sporadic SP (HP, SSA and TSA), in terms of their macroscopic appearance, when viewed endoscopically (Figure 5). In fact, according to our own unpublished data, their macroscopic appearance corresponds to type Ⅱb, and is very often characterised by larger dimensions than in a [44] population of non-IBD patients . At the molecular level, the genetic signatures are not well identified. It appears that there is very often a Kras mutation
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in 18% of UC cases with cancer, and 9% of Braf [45] mutations . However, little data is available and we need more studies to understand the serrated pathway in IBD patients.
ENDOSCOPIC SURVEILLANCE Some authors have reported a faster development [46,47] of these lesions whereas, on the contrary, a large cohort study has shown that the median age of patients carrying SSA was 61 years, whereas that of patients presenting with cancer was 76 years, thus [48] suggesting very slow progression . For this reason, the recent recommendations from the United States Multi-Society Task Force on Colorectal Cancer and [49,50] European Society of Gastrointestinal Endoscopy advocate an endoscopic control adapted to the size, number and presence of dysplasia (Table 2). As in the case of adenomas, factors such as withdrawal duration and the preparation or experience of the endoscopists, [51] are correlated with the rate of SP detections . Consequently, as in the case of adenomas, the question arises as to the role of new technologies, such as chromoendoscopy for the optimisation of screening and characterisation according to Kudo classification, in the detection of these lesions. In a retrospective study including patients with serrated polyposis, high resolution endoscopy and NBI made it possible to show that a fuzzy and irregular appearance of the polyps’ edges supported SSA, with a sensitivity, specificity [36] and accuracy of 89%, 96% and 93%, respectively .
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Although the inter-observer reproducibility for the fuzzy appearance under NBI was good (k = 0.67), as [52] in Tadepalli study (k = 0.8) , this should be evaluated in more extensive studies. Endomicroscopy associated with chromoendoscopy has been evaluated and has revealed an increase in detection sensitivity (91% vs [39] 77%; p = 0.01), and exactly the same specificity .
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CONCLUSION Under the denomination of serrated polyps, different types of lesions can be encountered, thus requiring a more accurate characterisation. This depends not only on the endoscopists, who must be able to recognise and describe these lesions in order to resect them in one piece, but also on the pathologists, who requires an accurate description and an oriented resected peace. This collaboration is essential in order to improve current knowledge and understanding.
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REFERENCES 1 2 3
4
5
6 7
8
9
10
11
17
Jass JR. Relation between metaplastic polyp and carcinoma of the colorectum. Lancet 1983; 1: 28-30 [PMID: 6129371 DOI: 10.1016/S0140-6736(83)91564-7] Chan TL, Zhao W, Leung SY, Yuen ST. BRAF and KRAS mutations in colorectal hyperplastic polyps and serrated adenomas. Cancer Res 2003; 63: 4878-4881 [PMID: 12941809] Preto A, Figueiredo J, Velho S, Ribeiro AS, Soares P, Oliveira C, Seruca R. BRAF provides proliferation and survival signals in MSI colorectal carcinoma cells displaying BRAF(V600E) but not KRAS mutations. J Pathol 2008; 214: 320-327 [PMID: 18098337 DOI: 10.1002/path.2295] Limketkai BN, Lam-Himlin D, Arnold MA, Arnold CA. The cutting edge of serrated polyps: a practical guide to approaching and managing serrated colon polyps. Gastrointest Endosc 2013; 77: 360-375 [PMID: 23410696 DOI: 10.1016/j.gie.2012.11.013] Jass JR. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 2007; 50: 113-130 [PMID: 17204026 DOI: 10.1111/j.1365-2559. 2006.02549.x] Leggett B, Whitehall V. Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology 2010; 138: 2088-2100 [PMID: 20420948 DOI: 10.1053/j.gastro.2009.12.066] Ji BT, Weissfeld JL, Chow WH, Huang WY, Schoen RE, Hayes RB. Tobacco smoking and colorectal hyperplastic and adenomatous polyps. Cancer Epidemiol Biomarkers Prev 2006; 15: 897-901 [PMID: 16702367 DOI: 10.1158/1055-9965.EPI-05-0883] Morimoto LM, Newcomb PA, Ulrich CM, Bostick RM, Lais CJ, Potter JD. Risk factors for hyperplastic and adenomatous polyps: evidence for malignant potential? Cancer Epidemiol Biomarkers Prev 2002; 11: 1012-1018 [PMID: 12376501] Hiraoka S, Kato J, Fujiki S, Kaji E, Morikawa T, Murakami T, Nawa T, Kuriyama M, Uraoka T, Ohara N, Yamamoto K. The presence of large serrated polyps increases risk for colorectal cancer. Gastroenterology 2010; 139: 1503-1510, 1510.e1-3 [PMID: 20643134] Schreiner MA, Weiss DG, Lieberman DA. Proximal and large hyperplastic and nondysplastic serrated polyps detected by colonoscopy are associated with neoplasia. Gastroenterology 2010; 139: 1497-1502 [PMID: 20633561 DOI: 10.1053/j.gastro.2010.06.074] Snover DC, Jass JR, Fenoglio-Preiser C, Batts KP. Serrated polyps of the large intestine: a morphologic and molecular review of an evolving concept. Am J Clin Pathol 2005; 124: 380-391 [PMID: 16191506 DOI: 10.1309/V2EPTPLJRB3FGHJL]
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23
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25
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Torlakovic EE, Gomez JD, Driman DK, Parfitt JR, Wang C, Benerjee T, Snover DC. Sessile serrated adenoma (SSA) vs. traditional serrated adenoma (TSA). Am J Surg Pathol 2008; 32: 21-29 [PMID: 18162766 DOI: 10.1097/PAS.0b013e318157f002] Snover DC. Update on the serrated pathway to colorectal carcinoma. Hum Pathol 2011; 42: 1-10 [PMID: 20869746 DOI: 10.1016/j.humpath.2010.06.002] Snover DC, Ahnen DJ, Burt RW, Odze RD. Serrated polyps of the colon and rectum and serrated polyposis. In: Bosman FT, Carneiro CF, Hruban RH; Theise ND, editors. WHO Classification of Tumours of the Digestive System World Health Organization classification of tumours. Lyon, France: IARC Press, 2010: 160-165 Ensari A, Bilezikçi B, Carneiro F, Doğusoy GB, Driessen A, Dursun A, Flejou JF, Geboes K, de Hertogh G, Jouret-Mourin A, Langner C, Nagtegaal ID, Offerhaus J, Orlowska J, Ristimäki A, Sanz-Ortega J, Savaş B, Sotiropoulou M, Villanacci V, Kurşun N, Bosman F. Serrated polyps of the colon: how reproducible is their classification? Virchows Arch 2012; 461: 495-504 [PMID: 23052370 DOI: 10.1007/s00428-012-1319-7] Kambara T, Simms LA, Whitehall VL, Spring KJ, Wynter CV, Walsh MD, Barker MA, Arnold S, McGivern A, Matsubara N, Tanaka N, Higuchi T, Young J, Jass JR, Leggett BA. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut 2004; 53: 1137-1144 [PMID: 15247181 DOI: 10.1136/gut.2003.037671] Young J, Barker MA, Simms LA, Walsh MD, Biden KG, Buchanan D, Buttenshaw R, Whitehall VL, Arnold S, Jackson L, Kambara T, Spring KJ, Jenkins MA, Walker GJ, Hopper JL, Leggett BA, Jass JR. Evidence for BRAF mutation and variable levels of microsatellite instability in a syndrome of familial colorectal cancer. Clin Gastroenterol Hepatol 2005; 3: 254-263 [PMID: 15765445 DOI: 10.1016/S1542-3565] Yamane L, Scapulatempo-Neto C, Reis RM, Guimarães DP. Serrated pathway in colorectal carcinogenesis. World J Gastroenterol 2014; 20: 2634-2640 [PMID: 24627599 DOI: 10.3748/wjg.v20.i10.2634] Patai AV, Molnár B, Tulassay Z, Sipos F. Serrated pathway: alternative route to colorectal cancer. World J Gastroenterol 2013; 19: 607-615 [PMID: 23431044 DOI: 10.3748/wjg.v19.i5.607] Huang CS, Farraye FA, Yang S, O’Brien MJ. The clinical significance of serrated polyps. Am J Gastroenterol 2011; 106: 229-240; quiz 241 [PMID: 21045813 DOI: 10.1038/ajg.2010.429] Rosty C, Parry S, Young JP. Serrated polyposis: an enigmatic model of colorectal cancer predisposition. Patholog Res Int 2011; 2011: 157073 [PMID: 21660283] Kim MJ, Lee EJ, Suh JP, Chun SM, Jang SJ, Kim do S, Lee DH, Lee SH, Youk EG. Traditional serrated adenoma of the colorectum: clinicopathologic implications and endoscopic findings of the precursor lesions. Am J Clin Pathol 2013; 140: 898-911 [PMID: 24225759 DOI: 10.1309/AJCPDJC9VC5KTYUS] Kudo S, Tamura S, Nakajima T, Yamano H, Kusaka H, Watanabe H. Diagnosis of colorectal tumorous lesions by magnifying endoscopy. Gastrointest Endosc 1996; 44: 8-14 [PMID: 8836710 DOI: 10.1016/S0016-5107(96)70222-5] Kumar S, Fioritto A, Mitani A, Desai M, Gunaratnam N, Ladabaum U. Optical biopsy of sessile serrated adenomas: do these lesions resemble hyperplastic polyps under narrow-band imaging? Gastrointest Endosc 2013; 78: 902-909 [PMID: 23849819 DOI: 10.1016/j.gie.2013.06.004] Buchner AM, Shahid MW, Heckman MG, Krishna M, Ghabril M, Hasan M, Crook JE, Gomez V, Raimondo M, Woodward T, Wolfsen HC, Wallace MB. Comparison of probe-based confocal laser endomicroscopy with virtual chromoendoscopy for classification of colon polyps. Gastroenterology 2010; 138: 834-842 [PMID: 19909747 DOI: 10.1053/j.gastro.2009.10.053] Sanduleanu S, Driessen A, Gomez-Garcia E, Hameeteman W, de Bruïne A, Masclee A. In vivo diagnosis and classification of colorectal neoplasia by chromoendoscopy-guided confocal laser endomicroscopy. Clin Gastroenterol Hepatol 2010; 8: 371-378
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[PMID: 19683597 DOI: 10.1016/j.cgh.2009.08.006] Kiesslich R, Goetz M, Lammersdorf K, Schneider C, Burg J, Stolte M, Vieth M, Nafe B, Galle PR, Neurath MF. Chromoscopy-guided endomicroscopy increases the diagnostic yield of intraepithelial neoplasia in ulcerative colitis. Gastroenterology 2007; 132: 874-882 [PMID: 17383417 DOI: 10.1053/j.gastro.2007.01.048] Torlakovic E, Skovlund E, Snover DC, Torlakovic G, Nesland JM. Morphologic reappraisal of serrated colorectal polyps. Am J Surg Pathol 2003; 27: 65-81 [PMID: 12502929 DOI: 10.1097/0000047 8-200301000-00008] Orlowska J. Serrated lesions and hyperplastic (serrated) polyposis relationship with colorectal cancer: classification and surveillance recommendations. Gastrointest Endosc 2013; 77: 858-871 [PMID: 23684091 DOI: 10.1016/j.gie.2013.02.016] Rex DK, Ahnen DJ, Baron JA, Batts KP, Burke CA, Burt RW, Goldblum JR, Guillem JG, Kahi CJ, Kalady MF, O’Brien MJ, Odze RD, Ogino S, Parry S, Snover DC, Torlakovic EE, Wise PE, Young J, Church J. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012; 107: 1315-1329; quiz 1314, 1330 [PMID: 22710576 DOI: 10.1038/ajg.2012.161] Singh H, Bay D, Ip S, Bernstein CN, Nugent Z, Gheorghe R, Wightman R. Pathological reassessment of hyperplastic colon polyps in a city-wide pathology practice: implications for polyp surveillance recommendations. Gastrointest Endosc 2012; 76: 1003-1008 [PMID: 23078924 DOI: 10.1016/j.gie.2012.07.026] Freedman JS, Harari DY, Bamji ND, Bodian CA, Kornacki S, Cohen LB, Miller KM, Aisenberg J. The detection of premalignant colon polyps during colonoscopy is stable throughout the workday. Gastrointest Endosc 2011; 73: 1197-1206 [PMID: 21396640 DOI: 10.1016/j.gie.2011.01.019] Pereyra L, Gómez EJ, González R, Fischer C, Eraña GB, Torres AG, Correa L, Mella JM, Panigadi GN, Luna P, Pedreira SC, Cimmino DG, Boerr LA. Finding sessile serrated adenomas: is it possible to identify them during conventional colonoscopy? Dig Dis Sci 2014; 59: 3021-3026 [PMID: 25073956 DOI: 10.1007/ s10620-014-3295-z] Kimura T, Yamamoto E, Yamano HO, Suzuki H, Kamimae S, Nojima M, Sawada T, Ashida M, Yoshikawa K, Takagi R, Kato R, Harada T, Suzuki R, Maruyama R, Kai M, Imai K, Shinomura Y, Sugai T, Toyota M. A novel pit pattern identifies the precursor of colorectal cancer derived from sessile serrated adenoma. Am J Gastroenterol 2012; 107: 460-469 [PMID: 22233696 DOI: 10.1038/ajg.2011.457] Wallace MB. Not so NICE to be serrated. Gastrointest Endosc 2013; 78: 910-911; quiz 912-912.e7 [PMID: 24237946 DOI: 10.1016/j.gie.2013.07.053] Hazewinkel Y, López-Cerón M, East JE, Rastogi A, Pellisé M, Nakajima T, van Eeden S, Tytgat KM, Fockens P, Dekker E. Endoscopic features of sessile serrated adenomas: validation by international experts using high-resolution white-light endoscopy and narrow-band imaging. Gastrointest Endosc 2013; 77: 916-924 [PMID: 23433877] Kim KM, Lee EJ, Kim YH, Chang DK, Odze RD. KRAS mutations in traditional serrated adenomas from Korea herald an aggressive phenotype. Am J Surg Pathol 2010; 34: 667-675 [PMID: 20305537] Ishigooka S, Nomoto M, Obinata N, Oishi Y, Sato Y, Nakatsu S, Suzuki M, Ikeda Y, Maehata T, Kimura T, Watanabe Y, Nakajima T, Yamano HO, Yasuda H, Itoh F. Evaluation of magnifying colonoscopy in the diagnosis of serrated polyps. World J Gastroenterol 2012; 18: 4308-4316 [PMID: 22969193 DOI: 10.3748/wjg.v18.i32.4308]
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Guarinos C, Sánchez-Fortún C, Rodríguez-Soler M, Alenda C, Payá A, Jover R. Serrated polyposis syndrome: molecular, pathological and clinical aspects. World J Gastroenterol 2012; 18: 2452-2461 [PMID: 22654442 DOI: 10.3748/wjg.v18.i20.2452] Morson BC, Pang LS. Rectal biopsy as an aid to cancer control in ulcerative colitis. Gut 1967; 8: 423-434 [PMID: 6057771 DOI: 10.1136/gut.8.5.423] Kilgore SP, Sigel JE, Goldblum JR. Hyperplastic-like mucosal change in Crohn’s disease: an unusual form of dysplasia? Mod Pathol 2000; 13: 797-801 [PMID: 10912940 DOI: 10.1038/ modpathol.3880138] Rubio CA, Befrits R, Jaramillo E, Nesi G, Amorosi A. Villous and serrated adenomatous growth bordering carcinomas in inflammatory bowel disease. Anticancer Res 2000; 20: 4761-4764 [PMID: 11205214] Rubio CA. Serrated neoplasias and de novo carcinomas in ulcerative colitis: a histological study in colectomy specimens. J Gastroenterol Hepatol 2007; 22: 1024-1031 [PMID: 17559365 DOI: 10.1111/j.1440-1746.2007.04944.x] Moussata D, Boschetti G, Chauvenet M, Stroeymeyt K, Nancey S, Berger F, Flourie B. Serrated polyps in patients with inflammatory bowel disease: endoscopic characteristics different from serrated polyps in the general population. Gastroenterology 2014; 146: S-424 [DOI: 10.1016/S0016-5085(14)61527-4] Aust DE, Haase M, Dobryden L, Markwarth A, Löhrs U, Wittekind C, Baretton GB, Tannapfel A. Mutations of the BRAF gene in ulcerative colitis-related colorectal carcinoma. Int J Cancer 2005; 115: 673-677 [PMID: 15704157 DOI: 10.1002/ijc.20925] Lazarus R, Junttila OE, Karttunen TJ, Mäkinen MJ. The risk of metachronous neoplasia in patients with serrated adenoma. Am J Clin Pathol 2005; 123: 349-359 [PMID: 15716230 DOI: 10.1309/ VBAGV3BR96N2EQTR] Oono Y, Fu K, Nakamura H, Iriguchi Y, Yamamura A, Tomino Y, Oda J, Mizutani M, Takayanagi S, Kishi D, Shinohara T, Yamada K, Matumoto J, Imamura K. Progression of a sessile serrated adenoma to an early invasive cancer within 8 months. Dig Dis Sci 2009; 54: 906-909 [PMID: 18688718 DOI: 10.1007/s10620-008-0407-7] Lash RH, Genta RM, Schuler CM. Sessile serrated adenomas: prevalence of dysplasia and carcinoma in 2139 patients. J Clin Pathol 2010; 63: 681-686 [PMID: 20547691 DOI: 10.1136/ jcp.2010.075507] Lieberman DA, Rex DK, Winawer SJ, Giardiello FM, Johnson DA, Levin TR; United States Multi-Society Task Force on Colorectal Cancer. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US MultiSociety Task Force on Colorectal Cancer. Gastroenterology 2012; 143: 844-857 [PMID: 22763141 DOI: 10.1053/ j.gastro.2012.06.001] Hassan C, Quintero E, Dumonceau JM, Regula J, Brandão C, Chaussade S, Dekker E, Dinis-Ribeiro M, Ferlitsch M, GimenoGarcía A, Hazewinkel Y, Jover R, Kalager M, Loberg M, Pox C, Rembacken B, Lieberman D. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2013; 45: 842-851 [PMID: 24030244 DOI: 10.1055/s-0033-1344548] Liang JJ, Bissett I, Kalady M, Bennet A, Church JM. Importance of serrated polyps in colorectal carcinogenesis. ANZ J Surg 2013; 83: 325-330 [PMID: 23078414] Tadepalli US, Feihel D, Miller KM, Itzkowitz SH, Freedman JS, Kornacki S, Cohen LB, Bamji ND, Bodian CA, Aisenberg J. A morphologic analysis of sessile serrated polyps observed during routine colonoscopy (with video). Gastrointest Endosc 2011; 74: 1360-1368 [PMID: 22018553 DOI: 10.1016/j.gie.2011.08.008]
P- Reviewer: Kopacova M, Seicean A, Tellez-Avila F, Tomizawa M, Zavoral M S- Editor: Ma YJ L- Editor: A E- Editor: Ma S
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MINIREVIEWS
Endoscopic and histologic characteristics of serrated lesions Driffa Moussata, Gilles Boschetti, Marion Chauvenet, Karine Stroeymeyt, Stéphane Nancey, Françoise Berger, Thierry Lecomte, Bernard Flourié serrated pathway and includes three types of polyp, characterised by a serrated appearance of the crypts: hyperplastic polyps (HP), sessile serrated adenomas (SSA) or lesions, and traditional serrated adenomas. Each lesion has its own genetic, as well as macroscopic and microscopic morphological features. Because of their flat aspect, their detection is easier with chromoendoscopy (carmin indigo or narrow-band imaging). However, as we show in this review, the distinction between SSA and HP is quite difficult. It is now recommended to resect in one piece as it is possible the serrated polyps with a control in a delay depending on the presence or not of dysplasia. These different types of lesion are described in detail in the present review in general population, in polyposis and in inflammatory bowel diseases patients. This review highlights the need to improve characterization and understanding of this way of colorectal cancerogenesis.
Driffa Moussata, Gilles Boschetti, Marion Chauvenet, Karine Stroeymeyt, Stéphane Nancey, Bernard Flourié, Department of Gastroenterology, Lyon Sud Hospital, 69310 Pierre Bénite, France Driffa Moussata, Inserm Unit CREATIS - UMR5220 INSERM1044, Lyon University, 69100 Villeurbanne, France Françoise Berger, Department of Pathology, Hôpital Lyon Sud, 69310 Pierre Bénite, France Thierry Lecomte, Department of Gastroenterology, Tours Hospital, 37000 Tours, France Author contributions: Moussata D has written the review; Boschetti G, Chauvenet M and Stroeymeyt K have contributed to conception and acquisition of data; Berger F has revised the pathologic data; Flourié B, Nancey S and Lecomte T have revised and approved the final version to be published. Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/ licenses/by-nc/4.0/ Correspondence to: Driffa Moussata, MD, PhD, Department of Gastroenterology, Lyon Sud Hospital, 165 chemin du Grand Revoyet, 69310 Pierre Bénite, France. [email protected] Telephone: +33-478-861290 Fax: +33-478-861063 Received: July 7, 2014 Peer-review started: July 7, 2014 First decision: August 6, 2014 Revised: August 25, 2014 Accepted: October 14, 2014 Article in press: October 15, 2014 Published online: March 14, 2015
Key words: Hyperplastic polyp; Traditional serrated adenoma; Serrated polyposis; Sessile serrated adenoma; Endoscopy; Endomicroscopy; Histology © The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
Core tip: The serrated lesions belong to a new carcinogenesis way of colorectal cancer which is important to know and detect. Even though endoscopic techniques have improved, some difficulties remain in terms of detection because of the lesions’ shape and aspect and the fact that the endoscopists have to be aware of some characteristics. However, we argue in this article that the endoscopists have to be trained so the recognition of these pre-neoplastic lesions can be improved. Furthermore, there is a necessity to communicate well with the pathologists. This article is a review of the knowledge we currently have of serrated lesions, and their endoscopic and histologic aspects which every gastroenterologist needs to know.
Abstract In recent years, a second pathway for colonic carcinogenesis, distinct from the adenomatous pathway, has been explored. This is referred to as
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Moussata D et al . Review of serrated polyps of the crypts in the proliferative zone for the other types of SP. As a consequence, with the maturation zones extending onto both sides of the proliferative zone, the cryptic “branched” type of architecture associated with an accumulation of cells at the surface [13] produces this serrated appearance . In 2010, a new World Health Organisation (WHO) histological classification was elaborated, to improve the inter-observer reproducibility of pathological [14] diagnosis . Although the kappa has been significantly increased, the global kappa remains middle (k = 0.55), in a European study involving expert anatomic [15] pathologists . This low reproducibility can be explained by the small size of the samples and the difficulty in orienting the crypts, with respect to the basal membrane, which is not always present on the samples.
Moussata D, Boschetti G, Chauvenet M, Stroeymeyt K, Nancey S, Berger F, Lecomte T, Flourié B. Endoscopic and histologic characteristics of serrated lesions. World J Gastroenterol 2015; 21(10): 2896-2904 Available from: URL: http://www.wjgnet. com/1007-9327/full/v21/i10/2896.htm DOI: http://dx.doi. org/10.3748/wjg.v21.i10.2896
INTRODUCTION Conventionally, dysplastic lesions and non-neoplastic lesions (hyperplastic or metaplastic) were distinguished [1] by their degenerative potential. In 1983, Jass was one of the first to defend the idea that there could be a link between hyperplastic polyps (HP) and colorectal cancer. Since then, it has been demonstrated that HP have proliferative, but not necessarily dysplastic anomalies, which are related to mutations of genes [2,3] such as the KRAS or BRAF . HP belong to a heterogeneous group of lesions, which are said to be serrated, because of the jagged appearance of their crypts, and which also include sessile serrated adenomas (SSA) and traditional sessile serrated adenomas (TSA). They represent [4] approximately 36% of polyps , and cancers arising from the serrated pathway are thought to represent around 20% of all colorectal cancers and more than [5,6] 30% of intervallic cancers . The risk factors associated with the occurrence of serrated polyps (SP) are similar to those described in the case of conventional adenomas. Tobacco appears to have a greater influence on the number of SP, but paradoxically has no influence on cancer cases, [7,8] which may develop from them . In addition, it has been shown that the presence of SP could increase, by a factor of three, the risk of an advanced-stage adenoma (villous or supra-centimeter adenoma, or adenoma with high-grade dysplasia) or a synchronous [9,10] or metachronous cancer . There are thus two advantages of detecting SP, as a consequence resulting not only from their own degenerative potential, but also from the aforementioned association.
CARCINOGENIC PATHWAY The molecular alterations observed in SP include mainly Braf mutations (V600E) and Kras mutations (codon 12 and 13), associated with a hyper-methylation of the region, which promotes some genes referred to as CIMP (CpG Island Methylation Promoter). The CpG islets are di-nucleotide regions, rich in cytosine [2,16] guanine at the level of region 5’ . This phenomenon can alter the expression of the genes involved in oncogenesis, such as p16, MGMT ‘MethylGuanine DNA [2,16] Methyltransferase) or MLH1 . The CIMP pathway is thought to be involved in approximately 30% of [17] colorectal cancer cases and nearly 90% of CIMP+ [16] colorectal cancers have a Braf or Kras mutation . The prevalence of these anomalies varies according to the type of SP (Table 1). Braf and Kras mutations activate the MAPK-ERK pathway leading to decreased apoptosis and cellular proliferation with at least the formation [18] of hyperplastic crypts . This is counteracted by a protective phenomen called oncogene-induced [19] senescence (Figure 1 ). Schematically, there appear to be 2 parallel pathways, depending on the gene involved: (1) braf mutation, often associated with CIMP+, presenting a satellite stability or instability depending on the involvement of MLH1; and (2) Kras mutation, often associated with a low level of microsatellite instability, [20] and inactivation of the MGMT gene . In the first case, the tumours are very often located in the proximal colon, like SSA, and in the second case they are often located in the distal colon, like TSA. It is interesting to note that whereas MLH1 methylation occurs frequently, a high level of microsatellite instability is rare, probably because this event occurs late during the [21] carcinogenesis of SP . However, that would not be so simple because, recently, some authors have shown that SSA as HP could be associated with TSA, that would suggest that they could be precursor-lesions of TSA. In this case, TSA present a lower and a higher frequency of Kras and Braf mutations, respectively,
PHYSIOPATHOLOGY The intestinal epithelium is made up of two major types of cell: absorptive cells (colonocytes) and secreting cells (goblet cells, endocrine cells and Paneth cells) originating from stem cells situated in the lower third of the crypts. These cells are differentiated by their migration towards the surface of the crypts, except in the case of Paneth cells, which reside at the base of the crypts. Hyperplasia of the crypts is the result of the equilibrium established between a level [11] [12] of proliferation and apoptosis . Torlakovic et al have shown that HP are caused by an extension of the proliferative zone beyond the lower third of the crypts, and displacement or ectopic formation along the length
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Moussata D et al . Review of serrated polyps Table 1 Serrated polyps characteristics
Frequency among polyps Dominant sex Macroscopy Size Paris classification Localization Pit pattern « Kudo » Microscopy Crypts
Hyperplastic polyps
Sessile serrated adenoma
Traditional serrated adenoma
28 à 42% Male
9% Female
1% No ascendancy
< 5 mm Ⅱa distal, rectum Ⅱ
> 5 mm Ⅰs, Ⅱa proximal, 27% distal Ⅱ-O (Open)
> 5 mm Ⅰp, Ⅰs distal Ⅱ-Ⅲs or ⅢL
Serrated aspect on the superior half of the crypts
Upper third serrated aspect of crypts, horizontalization of the third inferior of crypts aspect of “boot” or L Important mucus, small nuclear modifications Increased proliferative index with degenerative risk Braf (82%), CIMP-H, méthylation MLH1
Aspect serrated on all the crypt, ectopique crypts
Epithelium
Cylindrical
Maturation, degenerative potential Molecular
Normal index of proliferation, no degenerative potential +/- Braf, Kras, MSI (29%)
tubulo-villous dysplasia (37%), carcinoma (11%) Increased proliférative index with degenerative risk Kras (30%-80%), CIMP-L, méthylation MGMT
MSI: Microsatellites instability; CIMP-H, CIMP-L: CpG island methylation promotor-high, CIMP-bas; MLH1: MutL homolog 1; MGMT: MethylGuanine DNA methyltransferase.
MAPK ↑
BRAF mutation
KRAS mutation
Apoptosis ↓ SSA
TSA
CpG island methylation
MLH1 meth
MGMT meth CpG island methylation
P16 meth
Serration
CIMP-H
BRAF mut CIMP-H MSS
BRAF mut CIMP-H MSI
CIMP-L
Molecular profile
KRAS mut CIMP-L MSI-L
KRAS mut CIMP-L MSS
Figure 1 Schematic representation of the sessile and traditional serrated pathways[18]. MSI: Microsatellites instability; CIMP-H, CIMP-L: CpG island methylation promotor-high, CIMP-bas; MLH1: MutL homolog 1; MGMT: MethylGuanine DNA methyltransferase; SSA: Sessile serrated adenomas.
Endoscopic aspect
[22]
compared with TSA with no precursor lesion
.
Their macroscopic appearance is very often of type Ⅱa in Paris classification, and they are smaller than 5 mm in size.
MORPHOLOGY OF SERRATED LESIONS HP
HP are the most frequently encountered serrated lesions (75%-80%) and represent 28% to 42% of endoscopically detected polyps, with a higher [4] prevalence in men (Table 2). They are located mainly in the distal colon and the rectum.
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Chromo-endoscopy: The crypt opening is star-shaped, [23] corresponding to type Ⅱ in the Kudo classification . Narrow-band imaging: On the basis of 3 criteria (color, shape of the pits and pattern of vessels), NICE
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Sessile serrated lesions or SSA
Table 2 Endoscopic follow-up according to United States Multi[39] Society Task Force on Colorectal Cancer and European [40] Society of Gastrointestinal Endoscopy Serrated polyps HP SSA without dysplasia SSA with dysplasia TSA Serrated polyposis
With a frequency of occurrence corresponding to 15% to 20% of SP and 9% of all types of polyp, SSA are the most common lesions following HP. Just like TSA, the use of an adenomatous denomination leads to confusion, since they do not necessarily present dysplasia. However, some authors persist in using this designation in order to emphasize their degenerative risk. They are most commonly detected in women at an average age of approximately 60 years.
Follow-up according to United Follow-up according [39] [40] States multi-society to ESGE 5 yr, if > 10 mm or proximal < 3 lesions, < 1 cm: 5 yr ≥ 3, > 1 cm: 3 yr 3 yr
10 yr 10 yr
3 yr 1 yr
3 yr 1 yr
3 yr
Endoscopic aspect
In a retrospective study, more than 4000 polyps labelled as HP were revisited, and from multivariate analysis, a size > 5 mm and a location in the proximal colon were identified as discriminating criteria in favour [31] of SSA . They are very commonly of type IIa in Paris classification, and standard endoscopic screening is not straightforward as a consequence of their irregular boundaries and fuzzy appearance, which arise from the abundant presence of mucous (Figure 3). However, some authors have shown that education and training of the endoscopists could improve the recognition of these lesions, even with conventional whitelight [32] colonoscopies (worldwide available) . Rightside location, flat morphology, red-colored surface and presence of a mucus cap were independently associated with SSA histology. Recognition of these features during conventional colonoscopy may improve [33] the SSA detection rate .
ESGE: European Society of Gastrointestinal Endoscopy; HP: Hyperplastic polyps; SSA: Sessile serrated adenomas.
[24]
classification characterizes HP lesions with the same color or lighter than the background and without any vessel. They could also present dark or white spots of uniform size. Endomicroscopy: The confocal endomicroscopy (CEM) is an endoscopic technique, which enables us to perform an in-vivo histologic diagnosis during the endoscopy after fluoroscein has been injected intravenously. Several studies have shown that CEM has a [25,26] good correlation with histology and increases the dysplastic yield of biopsies particularly in inflammatory [27] bowel diseases (IBD) patients . However, no data is available about the different types of serrated polyps. In our experience, CEM (EC3870K Pentax, Tokyo), which can explore the mucosa from the surface to a depth of 270 microns, the crypts of HP lesions present anomalies at the surface with a lumen of the crypts larger with a stellar shape, whereas deeper, the crypts and the lumen are round, as in normal mucosa.
Chromoendoscopy: In addition to conventional type [23] Ⅱ pit pattern according to Kudo’s classification , [34] Kimura et al has reported that the surface architecture of the lesions was also broadly categorized as type Ⅱ-Open (type Ⅱ-O), type Ⅱ-Long (type Ⅱ-L), or type Ⅳ-Serrated (type Ⅳ-S). Ishigooka has shown that either type Ⅱ-O alone or partial type Ⅱ-O is the basic architecture, with SSA/Ps histology evident in 83.7% of cases. Others have shown that the type Ⅱ-O is highly specific (97%) but of low sensitivity (65%). This corresponds to the association of the star-shaped and very broad appearance of the crypts, which is probably related to the abundant presence of [31] mucous (Figure 3).
Histology
Microscopically, they are characterised by enlarged crypts, of which the upper half has a serrated architecture. The proliferative zone is located at the base of the crypts, which have a regular appearance. Homogeneous nuclei are located at the base of the cells. These lesions can be classified into several subtypes: (1) micro-vesicular HP, 2 times more common than; (2) HP rich in caliciform cells and 25 times more [28] common than; and (3) low mucin content cells . As this distinction currently has no clinical significance, it is not described in detail by pathologists, but makes it possible to understand why their endoscopic appearance can be so different (Figure 2). In addition, it has been shown that the presence of several HP in the distal colon is often associated with an increased [29] risk of serrated lesions in the proximal colon . Finally, some authors have suggested considering HP to be neoplastic lesions, since in 29% of cases microsatellite instability is observed, and depending on their HP sub[30] type, Braf or Kras mutations are detected .
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Narrow-band imaging: According to narrow-band imaging (NBI) International Colorectal Endoscopic classification system (NICE), SSA present a mixed [24] spectrum of features between HP and adenomas and that is why some authors concluded that this classification is insufficient to accurately distinguish [35] [36] SSA from HP . Hazewinkel et al have reported in a retrospective study that in white-light endoscopy, indistinctive borders and cloud-like surface are 2 independent predictive characteristics of SSA with 2 others features in NBI as an irregular shape and dark spots inside the crypts. A sensitivity, specificity
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Figure 2 Hyperplastic polyp in chromoendoscopy (A), histology (B) and confocal endomicroscopy (C).
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Figure 3 Sessile serrated adenoma in chromoendoscopy (A), confocal endomicroscopy (B) and histology (C)
and overall accuracy of, respectively, 75%, 79% and 77% on WLE and 89%, 96% and 93%on NBI were [36] obtained .
fact, their proliferation zone can be located at the midheight of the crypts, with mature goblet cells located at their base. SSA are distinguished from HP using the following characteristics: (1) a serrated appearance at the base of the crypts, together with a more jagged appearance at the surface; (2) horizontalization of the crypts with more collaterally branched crypts; (3) dilatation of the crypts; (4) an increase in epitheliumstroma ratio > 50%; (5) mitoses on the surface of the crypts; and (6) cellular atypia such as an enlarged nucleus and overproduction of mucin (Figure 3). One consensus suggests that at least 2 of the 6 criteria should be present on at least 2 well-separated crypts. These criteria were validated in a study involving several pathologists, with good inter-observer
Confocal endomicroscopy: The architecture of the crypts is modified and dilated by the presence of a great deal of mucous, which appears in black on the endomicroscopic images. The lumen is enlarged and presents a stellar shape as in histology. In practice, in endomicroscopy, it is easier to recognize SSA than HP.
Histology
Like HP, SSA do not systematically present with cytological signs of dysplasia, however unlike HP, they have an abnormal architecture and proliferation. In
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Figure 4 Traditional serrated polyp in chromoendoscopy (A), confocal endomicroscopy (B) and histology (C). [15]
agreement
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longer in contact with the muscularis propria, thus distinguishing them from SSA (Figure 4). They are characterised by an abundant eosinophilic cytoplasm [28] and elongated nuclei .
TSA These represent approximately 6% of SP, i.e., 1% [37] of all polyps, and are more common in Asia . They can be pedunculated or serrated, or even flat, and are more common in the distal colon (60%) and in patients whose age is close to 60 years, with no [4] distinction of sex .
SPECIAL CASE OF SERRATED POLYPOSIS
Endomicroscopy: In the literature, there is no specific description of these polyps in endomicroscopy, probably because of the low frequency. However, on endomicrosocpy, the crypts appear tubular as in adenoma lesions with low grade dysplasia and horizontalized that is characterized these lesions. The lumen is dilated and has a stellar shape. At the surface, the aspect is like a lace with cellular proliferation.
The diagnostic criteria for serrated polyposis were initially defined by Burt and Jass in 2000, and have recently been updated under the name of serrated [14] polyposis . Its definition is based on at least one of the following criteria: (1) at least 5 SP situated in the proximal colon, as far as the sigmoid colon, of which 2 are at least supra-centimetric; (2) whatever st the number of HP, a history of one 1 degree relative presenting with serrated polyposis; and (3) more than 20 HP, whatever their size or location. [29] Its incidence is estimated to be 1 per 100000 . It affects both sexes and is often diagnosed at around [21] the age of 55-65 years . The risk of cancer is 5 times higher than in general population. Two variants are described: type 1: serrated polyposis including the different serrated types, associated with adenomas; type 2: including the conventional hyperplastic polyps (< 5 mm), with a low risk of cancer. As a result of various different definitions, it has been suggested that each type could correspond to a different genetic pathway, with no possibility at the present time of stating whether the transmission is [39] recessive or dominant . Surgery is indicated in the case of cancer or when it is impossible to carry out an endoscopic inspection, with yearly monitoring. Family screening should of course be adopted as a standard st procedure for 1 degree relatives after the age of 40, [30] or 10 years prior to the age of the cancer .
HISTOLOGY
IBD
Microscopically, they show signs of dysplasia in 37% of cases, associated with an intramucosal carcinoma in 11% of cases. They have serrated crypts aligned perpendicularly to the crypt axis, characteristic of these lesions, with the presence of ectopic crypts no
In 1967, Morson et al were the first to describe flat pre-cancerous lesions with a pseudo-villous appearance, occurring in association with IBD. Histologically, they observed that the crypts lost their parallelism with a poorly positioned proliferation zone removed from the
Endoscopic aspect
Chromoendoscopy: In chromoendoscopy, TSA associate type Ⅱ with types Ⅲs or ⅡL and a [4] slightly textured or lobular surface (Figure 4) . The [38] characteristics of TSAs are often reddish in color . A further characteristic that was not included in this study is that some flat lesions show a surface architecture that can be described as highly protruding [34] double elevation, pinecone-shaped, or coral-shaped . In Ishigooka’s study, TSAs accounted for 76.9% (30/39) of lesions with a basic architecture of type Ⅳ-S pit pattern, and lesions without type Ⅳ-S pit pattern could be classified as non-TSAs with 96.7% sensitivity and 88.9% specificity. The authors concluded that type Ⅳ-S pit pattern can be considered a characteristic [38] finding of TSAs .
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Figure 5 Endoscopic (A), endomicroscopic (B) and histologic (C) characteristics of serrated lesions in patients with inflammatory bowel disease.
muscularis mucosa and closer to the surface. Kilgore identified mucosa with a hyperplastic appearance surrounding and further away from the cancer, on surgical specimens from the colon of Crohn’s disease patients, in 30% of cancer patients, as opposed to [41] [42] 10% in the control group . Rubio et al compared the appearance of tissue surrounding carcinomatous lesions in IBD patients with that in control patients (sporadic adenocarcinoma). They observed a serrated appearance in 22% (11/50) of IBD cases, as opposed to 2% (1/50) in the control group. The same authors have reported a strong prevalence (34.5%) of serrated lesions in patients having IBD in the absence of [43] carcinoma . It has been hypothesised that a chronic inflammation could lead to exaggerated proliferation at the level of the basal portion of the crypts, associated with abnormal regeneration phenomena, producing these serrated lesions, with dysplasia at the base [42] of the crypts . From our own experience, a wellidentified serrated appearance is indeed observed under endomicroscopy, corresponding exactly to the aforementioned descriptions, but remaining quite different from sporadic SP (HP, SSA and TSA), in terms of their macroscopic appearance, when viewed endoscopically (Figure 5). In fact, according to our own unpublished data, their macroscopic appearance corresponds to type Ⅱb, and is very often characterised by larger dimensions than in a [44] population of non-IBD patients . At the molecular level, the genetic signatures are not well identified. It appears that there is very often a Kras mutation
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in 18% of UC cases with cancer, and 9% of Braf [45] mutations . However, little data is available and we need more studies to understand the serrated pathway in IBD patients.
ENDOSCOPIC SURVEILLANCE Some authors have reported a faster development [46,47] of these lesions whereas, on the contrary, a large cohort study has shown that the median age of patients carrying SSA was 61 years, whereas that of patients presenting with cancer was 76 years, thus [48] suggesting very slow progression . For this reason, the recent recommendations from the United States Multi-Society Task Force on Colorectal Cancer and [49,50] European Society of Gastrointestinal Endoscopy advocate an endoscopic control adapted to the size, number and presence of dysplasia (Table 2). As in the case of adenomas, factors such as withdrawal duration and the preparation or experience of the endoscopists, [51] are correlated with the rate of SP detections . Consequently, as in the case of adenomas, the question arises as to the role of new technologies, such as chromoendoscopy for the optimisation of screening and characterisation according to Kudo classification, in the detection of these lesions. In a retrospective study including patients with serrated polyposis, high resolution endoscopy and NBI made it possible to show that a fuzzy and irregular appearance of the polyps’ edges supported SSA, with a sensitivity, specificity [36] and accuracy of 89%, 96% and 93%, respectively .
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Although the inter-observer reproducibility for the fuzzy appearance under NBI was good (k = 0.67), as [52] in Tadepalli study (k = 0.8) , this should be evaluated in more extensive studies. Endomicroscopy associated with chromoendoscopy has been evaluated and has revealed an increase in detection sensitivity (91% vs [39] 77%; p = 0.01), and exactly the same specificity .
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CONCLUSION Under the denomination of serrated polyps, different types of lesions can be encountered, thus requiring a more accurate characterisation. This depends not only on the endoscopists, who must be able to recognise and describe these lesions in order to resect them in one piece, but also on the pathologists, who requires an accurate description and an oriented resected peace. This collaboration is essential in order to improve current knowledge and understanding.
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REFERENCES 1 2 3
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Jass JR. Relation between metaplastic polyp and carcinoma of the colorectum. Lancet 1983; 1: 28-30 [PMID: 6129371 DOI: 10.1016/S0140-6736(83)91564-7] Chan TL, Zhao W, Leung SY, Yuen ST. BRAF and KRAS mutations in colorectal hyperplastic polyps and serrated adenomas. Cancer Res 2003; 63: 4878-4881 [PMID: 12941809] Preto A, Figueiredo J, Velho S, Ribeiro AS, Soares P, Oliveira C, Seruca R. BRAF provides proliferation and survival signals in MSI colorectal carcinoma cells displaying BRAF(V600E) but not KRAS mutations. J Pathol 2008; 214: 320-327 [PMID: 18098337 DOI: 10.1002/path.2295] Limketkai BN, Lam-Himlin D, Arnold MA, Arnold CA. The cutting edge of serrated polyps: a practical guide to approaching and managing serrated colon polyps. Gastrointest Endosc 2013; 77: 360-375 [PMID: 23410696 DOI: 10.1016/j.gie.2012.11.013] Jass JR. Classification of colorectal cancer based on correlation of clinical, morphological and molecular features. Histopathology 2007; 50: 113-130 [PMID: 17204026 DOI: 10.1111/j.1365-2559. 2006.02549.x] Leggett B, Whitehall V. Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology 2010; 138: 2088-2100 [PMID: 20420948 DOI: 10.1053/j.gastro.2009.12.066] Ji BT, Weissfeld JL, Chow WH, Huang WY, Schoen RE, Hayes RB. Tobacco smoking and colorectal hyperplastic and adenomatous polyps. Cancer Epidemiol Biomarkers Prev 2006; 15: 897-901 [PMID: 16702367 DOI: 10.1158/1055-9965.EPI-05-0883] Morimoto LM, Newcomb PA, Ulrich CM, Bostick RM, Lais CJ, Potter JD. Risk factors for hyperplastic and adenomatous polyps: evidence for malignant potential? Cancer Epidemiol Biomarkers Prev 2002; 11: 1012-1018 [PMID: 12376501] Hiraoka S, Kato J, Fujiki S, Kaji E, Morikawa T, Murakami T, Nawa T, Kuriyama M, Uraoka T, Ohara N, Yamamoto K. The presence of large serrated polyps increases risk for colorectal cancer. Gastroenterology 2010; 139: 1503-1510, 1510.e1-3 [PMID: 20643134] Schreiner MA, Weiss DG, Lieberman DA. Proximal and large hyperplastic and nondysplastic serrated polyps detected by colonoscopy are associated with neoplasia. Gastroenterology 2010; 139: 1497-1502 [PMID: 20633561 DOI: 10.1053/j.gastro.2010.06.074] Snover DC, Jass JR, Fenoglio-Preiser C, Batts KP. Serrated polyps of the large intestine: a morphologic and molecular review of an evolving concept. Am J Clin Pathol 2005; 124: 380-391 [PMID: 16191506 DOI: 10.1309/V2EPTPLJRB3FGHJL]
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18
19 20 21 22
23
24
25
26
2903
Torlakovic EE, Gomez JD, Driman DK, Parfitt JR, Wang C, Benerjee T, Snover DC. Sessile serrated adenoma (SSA) vs. traditional serrated adenoma (TSA). Am J Surg Pathol 2008; 32: 21-29 [PMID: 18162766 DOI: 10.1097/PAS.0b013e318157f002] Snover DC. Update on the serrated pathway to colorectal carcinoma. Hum Pathol 2011; 42: 1-10 [PMID: 20869746 DOI: 10.1016/j.humpath.2010.06.002] Snover DC, Ahnen DJ, Burt RW, Odze RD. Serrated polyps of the colon and rectum and serrated polyposis. In: Bosman FT, Carneiro CF, Hruban RH; Theise ND, editors. WHO Classification of Tumours of the Digestive System World Health Organization classification of tumours. Lyon, France: IARC Press, 2010: 160-165 Ensari A, Bilezikçi B, Carneiro F, Doğusoy GB, Driessen A, Dursun A, Flejou JF, Geboes K, de Hertogh G, Jouret-Mourin A, Langner C, Nagtegaal ID, Offerhaus J, Orlowska J, Ristimäki A, Sanz-Ortega J, Savaş B, Sotiropoulou M, Villanacci V, Kurşun N, Bosman F. Serrated polyps of the colon: how reproducible is their classification? Virchows Arch 2012; 461: 495-504 [PMID: 23052370 DOI: 10.1007/s00428-012-1319-7] Kambara T, Simms LA, Whitehall VL, Spring KJ, Wynter CV, Walsh MD, Barker MA, Arnold S, McGivern A, Matsubara N, Tanaka N, Higuchi T, Young J, Jass JR, Leggett BA. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. Gut 2004; 53: 1137-1144 [PMID: 15247181 DOI: 10.1136/gut.2003.037671] Young J, Barker MA, Simms LA, Walsh MD, Biden KG, Buchanan D, Buttenshaw R, Whitehall VL, Arnold S, Jackson L, Kambara T, Spring KJ, Jenkins MA, Walker GJ, Hopper JL, Leggett BA, Jass JR. Evidence for BRAF mutation and variable levels of microsatellite instability in a syndrome of familial colorectal cancer. Clin Gastroenterol Hepatol 2005; 3: 254-263 [PMID: 15765445 DOI: 10.1016/S1542-3565] Yamane L, Scapulatempo-Neto C, Reis RM, Guimarães DP. Serrated pathway in colorectal carcinogenesis. World J Gastroenterol 2014; 20: 2634-2640 [PMID: 24627599 DOI: 10.3748/wjg.v20.i10.2634] Patai AV, Molnár B, Tulassay Z, Sipos F. Serrated pathway: alternative route to colorectal cancer. World J Gastroenterol 2013; 19: 607-615 [PMID: 23431044 DOI: 10.3748/wjg.v19.i5.607] Huang CS, Farraye FA, Yang S, O’Brien MJ. The clinical significance of serrated polyps. Am J Gastroenterol 2011; 106: 229-240; quiz 241 [PMID: 21045813 DOI: 10.1038/ajg.2010.429] Rosty C, Parry S, Young JP. Serrated polyposis: an enigmatic model of colorectal cancer predisposition. Patholog Res Int 2011; 2011: 157073 [PMID: 21660283] Kim MJ, Lee EJ, Suh JP, Chun SM, Jang SJ, Kim do S, Lee DH, Lee SH, Youk EG. Traditional serrated adenoma of the colorectum: clinicopathologic implications and endoscopic findings of the precursor lesions. Am J Clin Pathol 2013; 140: 898-911 [PMID: 24225759 DOI: 10.1309/AJCPDJC9VC5KTYUS] Kudo S, Tamura S, Nakajima T, Yamano H, Kusaka H, Watanabe H. Diagnosis of colorectal tumorous lesions by magnifying endoscopy. Gastrointest Endosc 1996; 44: 8-14 [PMID: 8836710 DOI: 10.1016/S0016-5107(96)70222-5] Kumar S, Fioritto A, Mitani A, Desai M, Gunaratnam N, Ladabaum U. Optical biopsy of sessile serrated adenomas: do these lesions resemble hyperplastic polyps under narrow-band imaging? Gastrointest Endosc 2013; 78: 902-909 [PMID: 23849819 DOI: 10.1016/j.gie.2013.06.004] Buchner AM, Shahid MW, Heckman MG, Krishna M, Ghabril M, Hasan M, Crook JE, Gomez V, Raimondo M, Woodward T, Wolfsen HC, Wallace MB. Comparison of probe-based confocal laser endomicroscopy with virtual chromoendoscopy for classification of colon polyps. Gastroenterology 2010; 138: 834-842 [PMID: 19909747 DOI: 10.1053/j.gastro.2009.10.053] Sanduleanu S, Driessen A, Gomez-Garcia E, Hameeteman W, de Bruïne A, Masclee A. In vivo diagnosis and classification of colorectal neoplasia by chromoendoscopy-guided confocal laser endomicroscopy. Clin Gastroenterol Hepatol 2010; 8: 371-378
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[PMID: 19683597 DOI: 10.1016/j.cgh.2009.08.006] Kiesslich R, Goetz M, Lammersdorf K, Schneider C, Burg J, Stolte M, Vieth M, Nafe B, Galle PR, Neurath MF. Chromoscopy-guided endomicroscopy increases the diagnostic yield of intraepithelial neoplasia in ulcerative colitis. Gastroenterology 2007; 132: 874-882 [PMID: 17383417 DOI: 10.1053/j.gastro.2007.01.048] Torlakovic E, Skovlund E, Snover DC, Torlakovic G, Nesland JM. Morphologic reappraisal of serrated colorectal polyps. Am J Surg Pathol 2003; 27: 65-81 [PMID: 12502929 DOI: 10.1097/0000047 8-200301000-00008] Orlowska J. Serrated lesions and hyperplastic (serrated) polyposis relationship with colorectal cancer: classification and surveillance recommendations. Gastrointest Endosc 2013; 77: 858-871 [PMID: 23684091 DOI: 10.1016/j.gie.2013.02.016] Rex DK, Ahnen DJ, Baron JA, Batts KP, Burke CA, Burt RW, Goldblum JR, Guillem JG, Kahi CJ, Kalady MF, O’Brien MJ, Odze RD, Ogino S, Parry S, Snover DC, Torlakovic EE, Wise PE, Young J, Church J. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012; 107: 1315-1329; quiz 1314, 1330 [PMID: 22710576 DOI: 10.1038/ajg.2012.161] Singh H, Bay D, Ip S, Bernstein CN, Nugent Z, Gheorghe R, Wightman R. Pathological reassessment of hyperplastic colon polyps in a city-wide pathology practice: implications for polyp surveillance recommendations. Gastrointest Endosc 2012; 76: 1003-1008 [PMID: 23078924 DOI: 10.1016/j.gie.2012.07.026] Freedman JS, Harari DY, Bamji ND, Bodian CA, Kornacki S, Cohen LB, Miller KM, Aisenberg J. The detection of premalignant colon polyps during colonoscopy is stable throughout the workday. Gastrointest Endosc 2011; 73: 1197-1206 [PMID: 21396640 DOI: 10.1016/j.gie.2011.01.019] Pereyra L, Gómez EJ, González R, Fischer C, Eraña GB, Torres AG, Correa L, Mella JM, Panigadi GN, Luna P, Pedreira SC, Cimmino DG, Boerr LA. Finding sessile serrated adenomas: is it possible to identify them during conventional colonoscopy? Dig Dis Sci 2014; 59: 3021-3026 [PMID: 25073956 DOI: 10.1007/ s10620-014-3295-z] Kimura T, Yamamoto E, Yamano HO, Suzuki H, Kamimae S, Nojima M, Sawada T, Ashida M, Yoshikawa K, Takagi R, Kato R, Harada T, Suzuki R, Maruyama R, Kai M, Imai K, Shinomura Y, Sugai T, Toyota M. A novel pit pattern identifies the precursor of colorectal cancer derived from sessile serrated adenoma. Am J Gastroenterol 2012; 107: 460-469 [PMID: 22233696 DOI: 10.1038/ajg.2011.457] Wallace MB. Not so NICE to be serrated. Gastrointest Endosc 2013; 78: 910-911; quiz 912-912.e7 [PMID: 24237946 DOI: 10.1016/j.gie.2013.07.053] Hazewinkel Y, López-Cerón M, East JE, Rastogi A, Pellisé M, Nakajima T, van Eeden S, Tytgat KM, Fockens P, Dekker E. Endoscopic features of sessile serrated adenomas: validation by international experts using high-resolution white-light endoscopy and narrow-band imaging. Gastrointest Endosc 2013; 77: 916-924 [PMID: 23433877] Kim KM, Lee EJ, Kim YH, Chang DK, Odze RD. KRAS mutations in traditional serrated adenomas from Korea herald an aggressive phenotype. Am J Surg Pathol 2010; 34: 667-675 [PMID: 20305537] Ishigooka S, Nomoto M, Obinata N, Oishi Y, Sato Y, Nakatsu S, Suzuki M, Ikeda Y, Maehata T, Kimura T, Watanabe Y, Nakajima T, Yamano HO, Yasuda H, Itoh F. Evaluation of magnifying colonoscopy in the diagnosis of serrated polyps. World J Gastroenterol 2012; 18: 4308-4316 [PMID: 22969193 DOI: 10.3748/wjg.v18.i32.4308]
40 41
42
43
44
45
46
47
48
49
50
51 52
Guarinos C, Sánchez-Fortún C, Rodríguez-Soler M, Alenda C, Payá A, Jover R. Serrated polyposis syndrome: molecular, pathological and clinical aspects. World J Gastroenterol 2012; 18: 2452-2461 [PMID: 22654442 DOI: 10.3748/wjg.v18.i20.2452] Morson BC, Pang LS. Rectal biopsy as an aid to cancer control in ulcerative colitis. Gut 1967; 8: 423-434 [PMID: 6057771 DOI: 10.1136/gut.8.5.423] Kilgore SP, Sigel JE, Goldblum JR. Hyperplastic-like mucosal change in Crohn’s disease: an unusual form of dysplasia? Mod Pathol 2000; 13: 797-801 [PMID: 10912940 DOI: 10.1038/ modpathol.3880138] Rubio CA, Befrits R, Jaramillo E, Nesi G, Amorosi A. Villous and serrated adenomatous growth bordering carcinomas in inflammatory bowel disease. Anticancer Res 2000; 20: 4761-4764 [PMID: 11205214] Rubio CA. Serrated neoplasias and de novo carcinomas in ulcerative colitis: a histological study in colectomy specimens. J Gastroenterol Hepatol 2007; 22: 1024-1031 [PMID: 17559365 DOI: 10.1111/j.1440-1746.2007.04944.x] Moussata D, Boschetti G, Chauvenet M, Stroeymeyt K, Nancey S, Berger F, Flourie B. Serrated polyps in patients with inflammatory bowel disease: endoscopic characteristics different from serrated polyps in the general population. Gastroenterology 2014; 146: S-424 [DOI: 10.1016/S0016-5085(14)61527-4] Aust DE, Haase M, Dobryden L, Markwarth A, Löhrs U, Wittekind C, Baretton GB, Tannapfel A. Mutations of the BRAF gene in ulcerative colitis-related colorectal carcinoma. Int J Cancer 2005; 115: 673-677 [PMID: 15704157 DOI: 10.1002/ijc.20925] Lazarus R, Junttila OE, Karttunen TJ, Mäkinen MJ. The risk of metachronous neoplasia in patients with serrated adenoma. Am J Clin Pathol 2005; 123: 349-359 [PMID: 15716230 DOI: 10.1309/ VBAGV3BR96N2EQTR] Oono Y, Fu K, Nakamura H, Iriguchi Y, Yamamura A, Tomino Y, Oda J, Mizutani M, Takayanagi S, Kishi D, Shinohara T, Yamada K, Matumoto J, Imamura K. Progression of a sessile serrated adenoma to an early invasive cancer within 8 months. Dig Dis Sci 2009; 54: 906-909 [PMID: 18688718 DOI: 10.1007/s10620-008-0407-7] Lash RH, Genta RM, Schuler CM. Sessile serrated adenomas: prevalence of dysplasia and carcinoma in 2139 patients. J Clin Pathol 2010; 63: 681-686 [PMID: 20547691 DOI: 10.1136/ jcp.2010.075507] Lieberman DA, Rex DK, Winawer SJ, Giardiello FM, Johnson DA, Levin TR; United States Multi-Society Task Force on Colorectal Cancer. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US MultiSociety Task Force on Colorectal Cancer. Gastroenterology 2012; 143: 844-857 [PMID: 22763141 DOI: 10.1053/ j.gastro.2012.06.001] Hassan C, Quintero E, Dumonceau JM, Regula J, Brandão C, Chaussade S, Dekker E, Dinis-Ribeiro M, Ferlitsch M, GimenoGarcía A, Hazewinkel Y, Jover R, Kalager M, Loberg M, Pox C, Rembacken B, Lieberman D. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2013; 45: 842-851 [PMID: 24030244 DOI: 10.1055/s-0033-1344548] Liang JJ, Bissett I, Kalady M, Bennet A, Church JM. Importance of serrated polyps in colorectal carcinogenesis. ANZ J Surg 2013; 83: 325-330 [PMID: 23078414] Tadepalli US, Feihel D, Miller KM, Itzkowitz SH, Freedman JS, Kornacki S, Cohen LB, Bamji ND, Bodian CA, Aisenberg J. A morphologic analysis of sessile serrated polyps observed during routine colonoscopy (with video). Gastrointest Endosc 2011; 74: 1360-1368 [PMID: 22018553 DOI: 10.1016/j.gie.2011.08.008]
P- Reviewer: Kopacova M, Seicean A, Tellez-Avila F, Tomizawa M, Zavoral M S- Editor: Ma YJ L- Editor: A E- Editor: Ma S
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