Dra. Lara Arias
Hospital Universitario de Burgos
Dra. Raquel Vicente
Hospital Universitario Miguel Servet. Zaragoza
Dra. Beatriz Sicilia
Hospital Universitario de Burgos

INTRODUCTION

Patients with ulcerative colitis (UC) and Crohn’s Disease (CD) involving at least one third of the colon are at greater risk of developing colorectal cancer (CRC), although incidence rates have decreased from 4.29/1000 patients/year according to studies published in the 1950s to 1.21/1000 patients/year in studies from the last decade, as reported by the meta-analysis issued in 2014 by the Hospital de la Princesa group1. These percentages are much lower than those reported in classic meta-analyses, which showed a cumulative risk of CRC in patients with UC of 2% at 10 years, 8% at 20 years and 18% at 30 years2.

Furthermore, the screening of patients with IBD using endoscopic follow-up has shown to reduce the incidence of CRC, as published in a systematic review and meta-analysis of the Cochrane group3, when compared with the incidence of CRC in patients with IBD outside the endoscopic screening programme. This follow-up should be carried out using high-definition endoscopes and chromoendoscopy, whether virtual (VCE) or dye-based (DCE), and with targeted biopsies, according to the recommendations of scientific societies4.

In this chapter we are going to review how to perform an optical diagnosis of the lesions, which endoscopic resection we should use depending on this optical diagnosis, and the follow-up of our patients with IBD where dysplasia has been detected.

Optical diagnosis

According to the recommendations of the SCENIC Consensus published in 20155 for the diagnosis and follow-up of IBD patients, we must consider the interpretation of the pit pattern and the morphology of the lesion.

Pit pattern interpretation

For pit pattern interpretation we follow the Kudo Classification6, via chromoendoscopy, which differentiates between lesions with dysplasia or hyperplastic lesions. Recent publications have shown a sensitivity of around 93-100% with a specificity of 88 to 97%4,7 with negative and positive predictive values of 88% and 46% respectively (Fig 1). We can therefore classify the lesions according to 5 different patterns: Kudo 1 and 2 corresponding to non-neoplastic patterns, IIIs, IIIl and IV patterns, which match intramucosal neoplasms and type V, with distorted ridges or amorphous surface, which represents carcinoma (Table 1).

Section III.1. Table 1: Anatomical-pathological correspondence of Kudo patterns and treatment recommendations.

The negative predictive values for DCE and VCE (Narrow band image – NBI) were comparable, raising doubts as to whether these results could be extrapolated if colonoscopy without magnification was performed by untrained endoscopists. The Spanish IBD group (GEICYL)8 has published its results in a population-based dysplasia incidence programme with DCE, and although no good correlation has been shown between lesions with a Kudo pit pattern type ≥III pattern and dysplasia, the Kudo pit pattern type I and II lesions have been correctly identified, showing a high negative predictive value (92%), even when performed by non-expert endoscopists.

A new classification has recently been validated by an international group of experts, The Frankfurt Advanced Chromoendoscopic IBD LEsions Classification (FACILE), to improve prediction of dysplasia in detected lesions that include the assessment of the pit pattern (round, regular or irregular villi pattern, unstructured) and of the vascular pattern (non-visible, regular or irregular). The 4 predictive features of dysplasia include non-polypoid morphology of the lesion, irregular pit pattern, irregular vascular pattern and signs of inflammation in the lesion9.

Morphology of the lesion

Based on the SCENIC Consensus5, we are going to classify the lesions based on their morphology using the Modified Paris Classification as illustrated in Table 2:

  • Polypoid lesion (Type I): lesion that protrudes >2.5mm above the mucosa (reference: 2.5mm= height of a closed clamp).
    • Pedunculated polypoid lesion (Paris type Ip)
    • Sessile polypoid lesion (Paris type Is)
  • Non-polypoid sessile lesion (type II)
    • Elevated or protruding lesions<2.5mm (type IIa)
    • Flat or non-elevated lesions (type IIb)
    • Depressed lesions (type IIc), which sometimes involve ulceration, are more difficult or cannot be removed endoscopically.

Section III.1. Table 2: Morphology of the lesions. Paris classification and equivalence. Laine L, Kaltenbach T, Barkun A, et al. SCENIC Guideline Development Panel. SCENIC international consensus statement on surveillance and management of dysplasia in inflammatory bowel disease. Gastroenterology. 2015; 148:639–51. E28

Resection of lesions

Overall the resection of lesions in patients with IBD is no different to the resection of lesions with similar characteristics in patients without IBD, and will basically depend on the morphological classification and pit pattern:

I. Polypoid lesion (Type I): lesion that protrudes >2.5mm above the mucosa (reference: 2.5mm= height of a closed clamp).

  • Pedunculated polypoid lesion (Paris type Ip)
  • Sessile polypoid lesion (Paris type Is)

These polypoid lesions, regardless of whether they exhibit a pit pattern suggestive of dysplasia (Kudo III, IV) should be completely removed by endoscopic resection (confirmed by a histological study and with the tissue surrounding the lesion excised free of dysplasia, using staining or magnification techniques) and subsequent follow-up with chromoendoscopy (DCE) using a high-definition endoscope. The absence of other lesions with dysplasia in the rest of the colon must be verified, especially in HGD lesion5,10,11,12.

Section III.I. Video 1:  Patient with long-standing UC on maintenance treatment with Infliximab. Pedunculated polypoid lesion of approximately 1 cm. Paris IP type classification. Kudo Pattern III. There are no other dysplastic lesions in the rest of the colon. Complete endoscopic resection is performed, taking biopsies of the eschar and surrounding mucosa that do not present any alterations.

A particular situation in this scenario are pseudopolyps, as they are raised lesions, but with Kudo 1 pit patterns and which may exist in large numbers along the entire length of the colon. In this case they can be left unresected5 thus preventing complications, as the optical diagnosis of these lesions with chromoendoscopy allows dysplasia to be ruled out with a high negative predictive value.

II. Non-polypoid sessile lesion (type II)

  • Elevated or protruding lesions<2.5mm (type IIa)
  • Flat or non-elevated lesions (type IIb)
  • Depressed lesions (type IIc), which sometimes involve ulceration, are more difficult or cannot be removed endoscopically.

Combined lesions, e.g. elevated sessile or non-polypoid lesions accompanied by a flat lesion (Is+IIb/ IIa+IIb) are common. In all cases and especially in combined lesions, the lesion should be assessed for ulceration and the edges of the lesion well defined (staining/magnification techniques) to differentiate them from the surrounding mucosa and to allow for complete resection4. When they grow horizontally, they give rise to what we call laterally spreading tumours (LST), which in turn are classified in 2 types: granular type (LST-G), with nodules on the tumour surface, and non-granular type (LST-NG)13, with a flat, smooth surface. There are differences between the 2 types with respect to the risk of malignant degeneration and submucosal invasion. Non-granular LST have a higher risk of malignant submucosal invasion (14%) compared to granular LST (7%). The granular LST are divided into 2 subtypes: homogeneous and nodular mixed (with dominant nodules), with the latter being more at risk of deep invasion in large nodules (>10mm) and in depressed areas. In the non-granular the risk of invasion of the submucosa is directly related to size; the “non-lifting” sign and the V Kudo pattern is also more common in depressed areas14.

The visualisation of these lesions, especially flat or depressed (IIb and IIc) is enhanced by performing chromoendoscopy (CE) techniques with high-definition endoscopes (HDWLE). The SCENIC Consensus does not consider the association between the type of lesion and the likelihood of predicting dysplastic or invasive lesions, but subsequent publications report a higher frequency of occurrence of HGD in non-polypoid lesions with described Kudo patterns (III-V) when studied under endoscopic magnification4,12.

In this type of slightly raised or flat lesions, complete resection may be particularly difficult given the basal fibrosis of patients with IBD15, and the technique to be used will depend on the optical diagnosis (pit patterns based on the Kudo Classification) and the size of the lesion. Endoscopic mucosal resection (EMR) or endoscopic submucosal dissection (ESD) may be performed, attempting en bloc resection whenever possible. In order to perform EMR and ESD, prior raising of the lesion is required, via the injection of substances underneath in order to separate it from the muscularis propria and reduce the risk of perforation. Although the fluid most commonly used is saline, it has the disadvantage that the cushion thus created is short-lived, calling for repeated injections during the procedure (Video 2). Other more viscous substances are available that last longer and are thus preferable; these include glycerol (10% glycerine and 5% fructose in saline), hyaluronic acid and hydroxypropyl methylcellulose, among others16. A small amount of indigo carmine or methylene blue can be added to all of the above. It is important to make sure that the polyp is properly and fully lifted, as this indicates the absence of submucosal neoplastic invasion. Failure to lift can sometimes be due to the presence of fibrosis under the lesion which, according to Japanese experts would indicate the use of ESD rather than EMR. Fibrosis may be induced by biopsy collection, a tattoo very close to the lesion, or a prior attempt at excision. All of this should be taken into account when these lesions are identified in order to try to avoid procedures that might hinder or prevent subsequent endoscopic resection.

Section III.1. Video 2: Long-term ulcerative colitis. A type IIa sessile lesion is observed in the sigma, elevated, 1.5 cm, with well-defined edges, without ulcerations in the lesion. The lesion is elevated to facilitate resection using a diathermy loop. After polypectomy, coagulation of the edges of the lesion is performed.

In mucosal resection, once the lesion is elevated, one proceeds to a piecemeal removal by means of partial resections with a polypectomy snare, starting from one edge until complete resection is achieved (Fig. 2). Each fragment should not exceed 10-15 mm in size. The first fragment should include a small margin of normal mucosa, and subsequent fragments should include the edge of the previous one. Air aspiration can sometimes be useful during snare closure in order to reduce the risk of said snare slipping over the surface of the polyp without catching any tissue. Before applying electric current, once the fragment is caught, gas insufflation must be repeated in order to confirm safe conduct of the procedure. The endoscope should be positioned in a manner such that the lesion is located at 6 o’clock, in line with the working channel. One can use either pure coagulation current or EndoCut. After capturing each fragment with the snare and before applying current, said fragment must be must drawn away from the wall to reduce the risk of perforation17.

Endoscopic submucosal dissection seeks to remove the lesion in one piece regardless of its size, thereby facilitating histological assessment and improving the rate of curative resections. This method is particularly useful in the case of IBD, since the presence of prolonged inflammatory activity can cause mucosal and submucosal fibrosis; because it hinders proper elevation after fluid injection, this desmoplastic reaction can interfere with mucosal resection. The development of specific instruments has made dissection of fibrotic tissue and en bloc excision possible, ensuring healing. In fact, fibrosis is considered an indication for ESD.

The criteria confirming that en bloc resection via ESD can be considered curative are18:

  • Tumour-free edges of the resected fragment.
  • *Well-differentiated histopathological type*.
  • A depth of invasion less than 1,000 microns (up to the superficial submucosal layer or sm1).
  • Absence of lymphovascular invasion.
  • Absence of budding grade 2–3.

ESD is superior to EMR in that it allows en bloc resection of the lesion, resulting in a higher percentage of complete resections and a lower incidence of recurrence. By contrast, ESD takes much longer to perform, is technically more difficult and carries a higher risk for complications, especially perforation19.

Endoscopic submucosal dissection is particularly difficult in the rectum and colon, for the following reasons20:

  • The wall of the colon is very thin and is therefore at a greater risk of perforation than other locations.
  • Endoscopic control is more difficult in some parts of the colon because of paradoxical movements.
  • Retroflexion of the endoscope may be difficult due to the narrow lumen.
  • The lesions to be removed may be located either in or behind the folds of the colon.
  • If perforation occurs, there is a high risk of peritonitis, which requires surgical treatment.

ESD starts with a circumferential cut around a portion of the lesion and, as in EMR, after elevation thereof. This procedure normally makes use of an EndoCut current. Then, using coagulation and with the help of a translucent cap placed on the end of the endoscope, which serves to separate the fragment from the wall, the submucosal plane is carefully dissected, taking care not to reach the muscle layer until total removal is achieved. A range of accessories are available for this purpose, such as the Dual Knife, Hook Knife, Mucosectomy, Flex Knife, Hybrid Knife and Flush Knife, among others. The latter 2 are special in that liquid injection can be performed with the instrument itself, achieving a faster dissection. The use of one piece of equipment over another depends on the characteristics of the lesion and the individual preferences of the endoscopist. Moreover, and due to the characteristics of the colon and location of the lesions, it is often preferable to use small calibre endoscopes such as conventional gastroscopes or paediatric colonoscopes, as they are more manoeuvrable and allow easier retroflexion16,19.

Sometimes, a mixed or “hybrid” technique is used, which combines initial submucosal dissection with final en bloc snare resection, with results that are similar to those of traditional ESD.

After surgical excision, it is important to ensure haemostasis of the eschar via electrocoagulation of the visible vessels with specific forceps such as the Coag Grasper or argon gas, thus reducing the risk of delayed bleeding. Also, one can electocoagulate the edges of the eschar and any area suspected of constituting residual adenoma in order to reduce the risk of recurrence17.

The specimen must be sent to the pathology laboratory en bloc and spread on a soft surface with the help of pins in order to allow the pathologist to perform a rigorous study and assess the depth of invasion and infiltration of the edges (Fig. 3).

A meta-analysis21 has recently been published that assesses the efficacy and safety of EMR and ESD in polypoid and non-polypoid lesions, including 11 studies on 506 patients with IBD and 610 lesions with an average size of 23 mm. The percentage of complete resection of the lesions was 97.9%, with 0.8% risk of perforation [IC95% 0.1-2.2%] and a local recurrence rate in patients for whom endoscopic follow-up was decided of 4.9% [IC95% 1%-10.7%] during an average follow-up of 33 months. 6.6% of patients after the endoscopic technique were referred directly to surgery [IC95% 3.6%-10.2%]. To conclude, endoscopic resection (EMR or ESD) can prevent surgery in 93.4% of patients with dysplasia and IBD and is safe, with adverse effects in 0.2% of cases. And although both techniques have similar percentages of complete resection, as occurs outside the scope of IBD22, maybe for large lesions (>2cm) with high probability of submucosal invasion ESD “en bloc” could be the technique of choice to ensure full endoscopic healing without needing surgery (e.g.. LST-NG with depression or LST-G with large nodules)14.

Numerous and at times large lesions with Kudo I and II pit patterns can be seen in rectum and sigma8,23,24,25. Given the high negative predictive value (NPV) shown by the Kudo Classification thus proving to be highly accurate in excluding dysplasia, as well as the fact that most of the lesions with dysplasia are located in the proximal colon, resection of Kudo I and maybe Kudo II lesions in rectum and sigma could be avoided. This could prevent endoscopic complications in patients who are often asymptomatic and also save procedural time. In the GEICYL series the lesions located in the rectum and sigma were protective factors for dysplasia8. Although lesions with a Kudo pit pattern type II in most cases correspond to hyperplastic lesions, in some cases they could refer to serrated lesions with possible neoplastic potential. In the Iacucci series26, 80% of the serrated adenomas were located in the proximal colon, and were flat lesions with an irregular spiral vascular pattern. In the next few years further studies evaluating the natural history of these lesions in inflammatory bowel disease will be needed.

Below we will analyse the risk of progression once the lesion has been removed, which shall establish the follow-up intervals.

Dysplasia follow-up

Dysplasia or “intraepithelial neoplasia” is a neoplastic change in the cells of the intestinal epithelium limited to the basement membrane, without invasion of the lamina propria. The appearance of a series of molecular or histological changes in the context of associated chronic inflammation conditions the development of CRC generally linked to the following sequence: inflammation, dysplasia (indefinite, low or high grade) and carcinoma. Dysplasia is the marker linked to the increase of risk of malignancy in more than 90% of cases, forming part of the endoscopic follow-up strategies in IBD11. Certain limitations to this sequence have to be considered, as 10-15% of cancers can develop without a history of dysplasia or directly from low-grade dysplasia (LGD) in the absence of high-grade dysplasia (HGD). The presence of indefinite dysplasia highlights the problems of identifying dysplasia, describing a variable progression to HGD and CRC from 13-28%27.

On the other hand, dysplasia detected during patient follow-up (incidental dysplasia) has a lower associated risk than this diagnosis at initial colonoscopy (prevalent dysplasia) where the risk of HGD and CRC is greater (29% vs 16%). Recurring dysplasia (LGD in 2 consecutive colonoscopies) has a major impact on the indication of colectomy, as does findings of multifocal dysplasia (especially when HGD is involved).

Currently the most commonly used microscopic classification in Europe is the Vienna Classification, which stratifies dysplasia into 5 categories: negative for dysplasia, indefinite for dysplasia, LGD, HGD and invasive neoplasia. The greatest diagnostic difficulties are associated with the differentiation between regenerative changes and HGD and early invasive carcinoma, so a second assessment by an expert pathologist is crucial before any decision on patient management is made (11,28). In our usual practice we should use the macroscopic classification of dysplasia that since 2015 has followed the standards and definitions adopted in the International Consensus (SCENIC) adapted to the descriptive terms of the Paris Classification to its potential endoscopic resectability5,12 (Table 2).

Section III.1. Table 3: Histological classification of dysplasias. Comparison of the Vienna classification with the Riddell classification. LEGEND: *Does not exceed the basement membrane; **It surpasses the basement membrane; ***Invasion of the lamina propria to the muscularis mucosa; ****Invasion of the submucosa or beyond

The estimated incidence of CRC in these patients following endoscopic resection of polypoid lesions with dysplasia is approximately 0.5/100 patients/year, similar to incidence after polypectomy in patients without associated colitis29. Subsequent studies reflect a progression of cancer between 0% and 4.5% to 2 years and between 0% and 13.6% at 4 years30. With this evidence and following the recommendations of the consensus led by the Spanish Working Group on Crohn’s Disease and Ulcerative Colitis (Grupo Español de Trabajo en Enfermedad de Crohn y Colitis Ulcerosa – GETECCU), in dysplasia screening of patients with IBD31, when such lesions are resected, irrespective of findings of HGD or LGD, follow-up can be endoscopic and should be performed using DCE/VCE a year after excision (algorithm 1).

Data on progression to CRC of non-polypoid lesions is limited and comes from observational studies and case series where there is no clear differentiation between HGD and LGD30. These studies show a wide variability (40-100%) in the percentage of complete lesion resection with dysplasia-free margins (R0) conditioning the follow-up prognosis. Most recent follow-up studies include resections R0 < 70%, given the presence of large lesions with a high percentage of fibrosis32,33. This results in a high degree of heterogeneity and inconsistency when carrying out meta-analysis of published studies30. Overall, less current progression to advanced lesions is detected than in previous studies after the introduction of DCE and high-definition endoscopy from 2012 onwards; studies that report a R0 >70-80% progression to HGD and CCR (even 0%), although with short periods of follow-up (2 years)30. If we take as an example a multicentre, consecutive study of 69 patients, using DCE and high-definition endoscopy during 2000 and 2014, progression to advanced lesions is observed after resection of HGD at a rate of 1.34 per 100 patients/year with a mean follow-up of 3.3 years34. A recent Belgian study35 of retrospective follow-up of 410 patients over more than 20 years describes a lower risk of the appearance of advanced lesions (CRC and HGD) compared to previous studies36 with a risk of progression in the case of resection of lesions with LGD of 2.3% after 1 year of follow-up (0.5% of CRC) and 13.8% (8.5% of CRC) at 10 years, with the risk of CRC after prior resection of lesions with HGD of 9.1% at 1 year and 24.3% at 10 years. 19% of patients colectomised for dysplasia had CRC in the surgical specimen (5 with associated stenosis) and 42% patients colectomised for HGD had cancer in the specimen. The presence of metachronous lesions, PSC, colonic stenosis and a history of lesions with non-polypoid dysplasia >1cm are associated with a RR of 15 for the subsequent development of CRC35,36.

With this evidence and following the recommendations of the consensus led by the Spanish Group on Crohn’s Disease and Ulcerative Colitis (Grupo Español de Trabajo en Enfermedad de Crohn y Colitis Ulcerosa – GETECCU) in dysplasia screening of patients with IBD31, when such flat or slightly over-elevated lesions are resected with HGD, follow-up can be endoscopic with VCE/DCE 6 months after excision. On the other hand, if the dysplasia is of high grade (HGD), endoscopic follow-up could also be performed after 3-6 months but colectomy should always be considered, especially if the patient has other associated risk factors (primary sclerosing cholangitis/previous dysplasia) or with more evidence if multifocal HGD is present (algorithm 1)

Section III. 1. Algorithm 1: Monitoring of lesions with dysplasia. Sicilia B, Vicente R, Arias L. Recommendations of the Spanish Working Group on Crohn’s disease and Ulcerative Colitis (GETECCU) on dysplasia screening in inflammatory bowel disease patients. GastroenterolHepatol. 2021 Jun-Jul;44(6):435-447. CAPTION: *Tattoo if Kudo ≥3 | DCE: dye-based chromoendoscopy | LGD: low-grade dysplasia | HGD: high-grade dysplasia

When dysplasia is detected in randomised biopsies, it is called invisible dysplasia. We have previously commented that these lesions are now generally visible. There are 8 studies in the literature with small numbers of patients, limited follow-up and heterogeneous cohorts including patients with high risk of CRC (PSC and multifocal dysplasia) that report rates of progression of this type of dysplasia from 2.3-13% at 1 year and 4.6-44% at 2 years30 with percentages of progression to CRC of between 0% and 28% with an average follow-up of 2 years. The detection of lesions with LGD using DCE or high-definition endoscopes is greater, with only 12% of lesions being observed with invisible LGD compared to 88% of previous invisible lesions34. In terms of follow-up, the rates of progression are also lower with figures of 2.29/100 patients/year and only 3.8% development of CRC with an average follow-up of 5 years.

Conclusions

1. It is important to correctly describe the morphology of the pits (Kudo Classification) as well as the morphology of the lesion (Modified Paris Classification) to decide which therapeutic strategy to use, aiming for en bloc resection for lesions < 2 cm; and for lesions larger than 2 cm, depending on the likelihood of submucosal invasion, use EMR or ESD, always assessing the surgical option if deep invasion is suspected (non-lifting sign / Kudo pit pattern type V)

2. With limited evidence using chromoendoscopy techniques, the rate of progression to dysplasia appears to be lower than with low-definition endoscopes and without chromoendoscopy, and the presence of dysplasia, whether LGD or HGD, has a different meaning if it is diagnosed on a raised or flat lesion, with the latter requiring close monitoring with DCE/VCE by experts, assessing the possibility of colectomy in patients at high risk or with multifocal high-grade dysplasia.

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SIGUIENTE: >> III.2 Manejo endoscópico de las estenosis en la Enfermedad Inflamatoria Intestinal
ÍNDICE: << Volver al Índice ENDI