- Email: [email protected]
The not so NICE classification
Letters to the editor
REFERENCES 1. Triantafyllou K, Viazis N, Tsibouris P, et al. Colon capsule endoscopy is feasible to perform after incomplete colonoscopy and guides further workup in clinical practice. Gastrointest Endosc 2014;79:307-16. 2. Rembacken B, Hassan C, Riemann JF, et al. Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE). Endoscopy 2012;44:957-68. 3. Schoofs N, Devière J, Van Gossum A. PillCam colon capsule endoscopy compared with colonoscopy for colorectal tumor diagnosis: a prospective pilot study. Endoscopy 2006;38:971-7. http://dx.doi.org/10.1016/j.gie.2014.01.011
Response We thank our Portuguese colleagues for their interest in our publication.1 We respond to their comments, as follows: 1. The rate of colonoscopy completion in our study population is within the rates reported in clinical practice.2 Moreover, different colon capsule endoscopy (CCE) accuracy is not statistically expected in a population with a higher rate of cecal intubation. The accuracy, usefulness, and consensus of our study results are strongly supported by the literature3 and by the recently presented results of studies on the use of the secondgeneration Given Imaging colon capsule endoscope to complement incomplete colonoscopy.4-6 Irrespective of the population mix of the studies, the CCE complementation rate is 86% to 98%.1,3-6 2. The issue that arises from the lack of marking the site where colonoscopy stopped has been acknowledged and extensively discussed as a study limitation in our publication1 and previously.3 3. The potential need for further workup after CCE was discussed with the study participants during the informed consent procedure. Therefore, our reported procedure acceptance rate is not flawed by this issue. 4. Finally, we cannot disagree that the follow-up period might have been inadequate to allow for the identification of missed preneoplastic lesions. However, our endpoint was focused on the identification of missed cancers.
2. Shah H, Paszat LF, Saskin R, et al. Factors associated with incomplete colonoscopy: a population-based study. Gastroenterology 2007;132: 2297-303. 3. Alarcón-Fernández O, Ramos L, Adrián-de-Ganzo Z, et al. Effects of colon capsule endoscopy on medical decision making in patients with incomplete colonoscopies. Clin Gastroenterol Hepatol 2013;11:534-40. 4. Baltes P, Bota M, Albert J, et al. PillCam Colon2 after incomplete colonoscopy: first preliminary results of a multicenter study. United Eur Gastroenterol J 2013;1(Suppl 1):A190. 5. Spada C, Hassan C, Barbaro B, et al. Colon capsule endoscopy versus colonography in the evaluation of patients with incomplete traditional colonoscopy: a prospective comparative trial. United Eur Gastroenterol J 2013;1(Suppl 1):A126. 6. Nogales O, Lujan M, Nicolas D, et al. Utility of colon capsule endoscopy after an incomplete colonoscopy. Multicentric Spanish study. United Eur Gastroenterol J 2013;1(Suppl 1):A344. http://dx.doi.org/10.1016/j.gie.2014.02.002
The not so NICE classification To the Editor:
1. Triantafyllou K, Viazis N, Tsibouris P, et al. Colon capsule endoscopy is feasible to perform after incomplete colonoscopy and guides further workup in clinical practice. Gasrointest Endosc 2014;79:307-16.
We read with great interest the article by Kumar et al1 in the December issue of GIE in which they retrospectively analyzed the use of Narrow-Band Imaging International Colorectal Endoscopic (NICE) classification by community gastroenterologists for predicting polyp histology. They showed that 37% of sessile serrated adenomas (SSAs) had all 3 features of hyperplastic polyps (HPs), whereas 61% of SSAs had all 3 features of adenomas. They suggested that as many as one third of SSAs could be erroneously classified as innocuous HPs by community gastroenterologists using the NICE classification. The study evaluated a large number of polyps, and the endoscopists evaluating the images were trained in narrow-band imaging and the use of the NICE classification. It highlights the evolving role of optical tools in making management decisions for patients undergoing colonoscopy for colorectal cancer screening. However, we believe that there are several factors that limit the applicability of the study’s conclusions to current standard clinical practice and should be considered before further studies to address similar questions are designed. There are currently no standardized imaging criteria for the identification of sessile serrated adenomas/polyps (SSAs/SSPs). The NICE classification was developed by an international group (Colon Tumor NBI Interest Group), which included Japanese, U.S., French, and U.K. endoscopists. It differentiates colonic lesions based on differences in the color, vessels, and surface pattern without magnifying endoscopy into 3 categories: HPs, adenomas, and submucosally invading carcinomas.2 This study demonstrated the limitations of the NICE classification because it was not developed to differentiate SSAs/SSPs; therefore, there is some overlap of the features found in both HPs and adenomatous polyps. We previously showed that the SSAs/SSPs are difficult to diagnose endoscopically and can be easily
1030 GASTROINTESTINAL ENDOSCOPY Volume 79, No. 6 : 2014
www.giejournal.org
Konstantinos Triantafyllou, MD, PhD Hepatogastroenterology Unit Second Department of Internal Medicine and Research Institute Attikon University General Hospital Medical School, Athens University Athens, Greece
REFERENCES
Letters to the editor
classified as HPs based on endoscopic features, even with the use of narrow-band imaging (NBI).3 Recently, with increasing recognition of the role of serrated lesions in colon cancer, multiple studies have attempted to characterize the endoscopic features of SSAs/ SSPs (both white-light endoscopy and NBI with or without magnification).4 Singh et al5 used NBI with magnification and the Sano classification to successfully differentiate HPs, SSAs/SSPs, and tubular adenomas with 96% accuracy. Kahi et al6 and Hetzel et al7 previously showed that the SSA/SSP detection rates are highly variable and endoscopist dependent. The study by Kumar et al again highlights that endoscopists who are not aware of SSAs/SSPs and are not looking for these lesions will definitely miss these or classify these SSAs/SSPs with malignant potential as relatively benign HPs. The endoscopists in the Kumar et al study, even though trained in NBI and the NICE classification, did not make real-time diagnoses of SSAs/SSPs. The investigators documented the features of the polyp, and these features were then correlated with the diagnosis as determined by surgical pathology. Future studies of interest would involve experts in NBI as well as community gastroenterologists using NBI with magnification to differentiate HPs, SSAs, and adenomas in real time and compare the results of optical biopsies with the histological diagnosis. Furthermore, the authors use the term SSAs for the lesions of interest, which has been interchangeably used with SSPs. This has led to some confusion as to the histology of these lesions. The World Health Organization and an expert panel have recommended using SSAs/ SSPs to represent these lesions and prevent any confusion.8 This study also highlights important limitations in our current understanding and management of serrated lesions of the colon. Even though the NICE classification is helpful in detecting HPs, a unified classification system that differentiates HPs, SSAs/SSPs, and adenomas is needed before we can achieve any success in reaching the goals of the “resect and discard” strategy.
DISCLOSURE All authors disclosed no financial relationships relevant to this publication. Ajaypal Singh, MBBS Vani J. Konda, MD Section of Gastroenterology Uzma D. Siddiqui, MD Center for Endoscopic Research and Therapeutics Section of Gastroenterology University of Chicago, Chicago Illinois, USA www.giejournal.org
REFERENCES 1. Kumar S, Fioritto A, Mitani A, et al. Optical biopsy of sessile serrated adenomas: do these lesions resemble hyperplastic polyps under narrow-band imaging? Gastrointest Endosc 2013;78:902-9. 2. Oba S, Tanaka S, Sano Y, et al. Current status of narrow-band imaging magnifying colonoscopy for colorectal neoplasia in Japan. Digestion 2011;83:167-72. 3. Rogart JN, Jain D, Siddiqui UD, et al. Narrow-band imaging without high magnification to differentiate polyps during real-time colonoscopy: improvement with experience. Gastrointestinal Endoscopy. Gastrointest Endosc 2008;68:1136-45. 4. Hazewinkel Y, López-Cerón M, East JE, et al. Endoscopic features of sessile serrated adenomas: validation by international experts using high-resolution white-light endoscopy and narrow-band imaging. Gastrointest Endosc 2013;77:916-24. 5. Singh R, Jayanna M, Navadgi S, et al. Narrow-band imaging with dual focus magnification in differentiating colorectal neoplasia. Dig Endosc 2013;25:16-20. 6. Kahi CJ, Hewett DG, Norton DL, et al. Prevalence and variable detection of proximal colon serrated polyps during screening colonoscopy. Clin Gastroenterol Hepatol 2011;9:42-6. 7. Hetzel JT, Huang CS, Coukos JA, et al. Variation in the detection of serrated polyps in an average risk colorectal cancer screening cohort. Am J Gastroenterol 2010;105:2656-64. 8. Rex DK, Ahnen DJ, Baron JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012;107:1315-29. http://dx.doi.org/10.1016/j.gie.2014.01.025
Response: We thank Singh et al for their interest in our article investigating the narrow-band imaging (NBI) characteristics of sessile serrated adenomas (SSAs).1 We agree with Singh et al that the details of our study design must be kept in mind in the interpretation of the results. We performed a retrospective analysis of prospectively collected data in which we assessed the Narrow Band Imaging International Colorectal Endoscopic (NICE) classification features2 that were observed in SSAs by endoscopists who were being trained in the use of NBI to identify polyps as either adenomatous or hyperplastic. As Singh et al point out, the NICE classification2 was not developed to differentiate hyperplastic polyps or adenomas from SSAs, and the endoscopists in our study did not set out to make NBI-based real-time diagnoses of SSA. Based in part on our clinical experience and in part on past publications3 as cited by Singh et al in their letter, we hypothesized that the endoscopists in our study would tend to observe the NICE features of hyperplastic polyps in those lesions that were later read by pathologists as SSAs. Instead, these endoscopists observed a profile of NICE features that was intermediate to the profile observed for hyperplastic polyps and adenomas. However, given that these endoscopists had proven proficiency in the ex vivo but not yet the in vivo application of the NICE classification, these results may not represent the NICE features of SSAs in the eyes of observers with more experience in NBI. Volume 79, No. 6 : 2014 GASTROINTESTINAL ENDOSCOPY 1031
REFERENCES 1. Triantafyllou K, Viazis N, Tsibouris P, et al. Colon capsule endoscopy is feasible to perform after incomplete colonoscopy and guides further workup in clinical practice. Gastrointest Endosc 2014;79:307-16. 2. Rembacken B, Hassan C, Riemann JF, et al. Quality in screening colonoscopy: position statement of the European Society of Gastrointestinal Endoscopy (ESGE). Endoscopy 2012;44:957-68. 3. Schoofs N, Devière J, Van Gossum A. PillCam colon capsule endoscopy compared with colonoscopy for colorectal tumor diagnosis: a prospective pilot study. Endoscopy 2006;38:971-7. http://dx.doi.org/10.1016/j.gie.2014.01.011
Response We thank our Portuguese colleagues for their interest in our publication.1 We respond to their comments, as follows: 1. The rate of colonoscopy completion in our study population is within the rates reported in clinical practice.2 Moreover, different colon capsule endoscopy (CCE) accuracy is not statistically expected in a population with a higher rate of cecal intubation. The accuracy, usefulness, and consensus of our study results are strongly supported by the literature3 and by the recently presented results of studies on the use of the secondgeneration Given Imaging colon capsule endoscope to complement incomplete colonoscopy.4-6 Irrespective of the population mix of the studies, the CCE complementation rate is 86% to 98%.1,3-6 2. The issue that arises from the lack of marking the site where colonoscopy stopped has been acknowledged and extensively discussed as a study limitation in our publication1 and previously.3 3. The potential need for further workup after CCE was discussed with the study participants during the informed consent procedure. Therefore, our reported procedure acceptance rate is not flawed by this issue. 4. Finally, we cannot disagree that the follow-up period might have been inadequate to allow for the identification of missed preneoplastic lesions. However, our endpoint was focused on the identification of missed cancers.
2. Shah H, Paszat LF, Saskin R, et al. Factors associated with incomplete colonoscopy: a population-based study. Gastroenterology 2007;132: 2297-303. 3. Alarcón-Fernández O, Ramos L, Adrián-de-Ganzo Z, et al. Effects of colon capsule endoscopy on medical decision making in patients with incomplete colonoscopies. Clin Gastroenterol Hepatol 2013;11:534-40. 4. Baltes P, Bota M, Albert J, et al. PillCam Colon2 after incomplete colonoscopy: first preliminary results of a multicenter study. United Eur Gastroenterol J 2013;1(Suppl 1):A190. 5. Spada C, Hassan C, Barbaro B, et al. Colon capsule endoscopy versus colonography in the evaluation of patients with incomplete traditional colonoscopy: a prospective comparative trial. United Eur Gastroenterol J 2013;1(Suppl 1):A126. 6. Nogales O, Lujan M, Nicolas D, et al. Utility of colon capsule endoscopy after an incomplete colonoscopy. Multicentric Spanish study. United Eur Gastroenterol J 2013;1(Suppl 1):A344. http://dx.doi.org/10.1016/j.gie.2014.02.002
The not so NICE classification To the Editor:
1. Triantafyllou K, Viazis N, Tsibouris P, et al. Colon capsule endoscopy is feasible to perform after incomplete colonoscopy and guides further workup in clinical practice. Gasrointest Endosc 2014;79:307-16.
We read with great interest the article by Kumar et al1 in the December issue of GIE in which they retrospectively analyzed the use of Narrow-Band Imaging International Colorectal Endoscopic (NICE) classification by community gastroenterologists for predicting polyp histology. They showed that 37% of sessile serrated adenomas (SSAs) had all 3 features of hyperplastic polyps (HPs), whereas 61% of SSAs had all 3 features of adenomas. They suggested that as many as one third of SSAs could be erroneously classified as innocuous HPs by community gastroenterologists using the NICE classification. The study evaluated a large number of polyps, and the endoscopists evaluating the images were trained in narrow-band imaging and the use of the NICE classification. It highlights the evolving role of optical tools in making management decisions for patients undergoing colonoscopy for colorectal cancer screening. However, we believe that there are several factors that limit the applicability of the study’s conclusions to current standard clinical practice and should be considered before further studies to address similar questions are designed. There are currently no standardized imaging criteria for the identification of sessile serrated adenomas/polyps (SSAs/SSPs). The NICE classification was developed by an international group (Colon Tumor NBI Interest Group), which included Japanese, U.S., French, and U.K. endoscopists. It differentiates colonic lesions based on differences in the color, vessels, and surface pattern without magnifying endoscopy into 3 categories: HPs, adenomas, and submucosally invading carcinomas.2 This study demonstrated the limitations of the NICE classification because it was not developed to differentiate SSAs/SSPs; therefore, there is some overlap of the features found in both HPs and adenomatous polyps. We previously showed that the SSAs/SSPs are difficult to diagnose endoscopically and can be easily
1030 GASTROINTESTINAL ENDOSCOPY Volume 79, No. 6 : 2014
www.giejournal.org
Konstantinos Triantafyllou, MD, PhD Hepatogastroenterology Unit Second Department of Internal Medicine and Research Institute Attikon University General Hospital Medical School, Athens University Athens, Greece
REFERENCES
Letters to the editor
classified as HPs based on endoscopic features, even with the use of narrow-band imaging (NBI).3 Recently, with increasing recognition of the role of serrated lesions in colon cancer, multiple studies have attempted to characterize the endoscopic features of SSAs/ SSPs (both white-light endoscopy and NBI with or without magnification).4 Singh et al5 used NBI with magnification and the Sano classification to successfully differentiate HPs, SSAs/SSPs, and tubular adenomas with 96% accuracy. Kahi et al6 and Hetzel et al7 previously showed that the SSA/SSP detection rates are highly variable and endoscopist dependent. The study by Kumar et al again highlights that endoscopists who are not aware of SSAs/SSPs and are not looking for these lesions will definitely miss these or classify these SSAs/SSPs with malignant potential as relatively benign HPs. The endoscopists in the Kumar et al study, even though trained in NBI and the NICE classification, did not make real-time diagnoses of SSAs/SSPs. The investigators documented the features of the polyp, and these features were then correlated with the diagnosis as determined by surgical pathology. Future studies of interest would involve experts in NBI as well as community gastroenterologists using NBI with magnification to differentiate HPs, SSAs, and adenomas in real time and compare the results of optical biopsies with the histological diagnosis. Furthermore, the authors use the term SSAs for the lesions of interest, which has been interchangeably used with SSPs. This has led to some confusion as to the histology of these lesions. The World Health Organization and an expert panel have recommended using SSAs/ SSPs to represent these lesions and prevent any confusion.8 This study also highlights important limitations in our current understanding and management of serrated lesions of the colon. Even though the NICE classification is helpful in detecting HPs, a unified classification system that differentiates HPs, SSAs/SSPs, and adenomas is needed before we can achieve any success in reaching the goals of the “resect and discard” strategy.
DISCLOSURE All authors disclosed no financial relationships relevant to this publication. Ajaypal Singh, MBBS Vani J. Konda, MD Section of Gastroenterology Uzma D. Siddiqui, MD Center for Endoscopic Research and Therapeutics Section of Gastroenterology University of Chicago, Chicago Illinois, USA www.giejournal.org
REFERENCES 1. Kumar S, Fioritto A, Mitani A, et al. Optical biopsy of sessile serrated adenomas: do these lesions resemble hyperplastic polyps under narrow-band imaging? Gastrointest Endosc 2013;78:902-9. 2. Oba S, Tanaka S, Sano Y, et al. Current status of narrow-band imaging magnifying colonoscopy for colorectal neoplasia in Japan. Digestion 2011;83:167-72. 3. Rogart JN, Jain D, Siddiqui UD, et al. Narrow-band imaging without high magnification to differentiate polyps during real-time colonoscopy: improvement with experience. Gastrointestinal Endoscopy. Gastrointest Endosc 2008;68:1136-45. 4. Hazewinkel Y, López-Cerón M, East JE, et al. Endoscopic features of sessile serrated adenomas: validation by international experts using high-resolution white-light endoscopy and narrow-band imaging. Gastrointest Endosc 2013;77:916-24. 5. Singh R, Jayanna M, Navadgi S, et al. Narrow-band imaging with dual focus magnification in differentiating colorectal neoplasia. Dig Endosc 2013;25:16-20. 6. Kahi CJ, Hewett DG, Norton DL, et al. Prevalence and variable detection of proximal colon serrated polyps during screening colonoscopy. Clin Gastroenterol Hepatol 2011;9:42-6. 7. Hetzel JT, Huang CS, Coukos JA, et al. Variation in the detection of serrated polyps in an average risk colorectal cancer screening cohort. Am J Gastroenterol 2010;105:2656-64. 8. Rex DK, Ahnen DJ, Baron JA, et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012;107:1315-29. http://dx.doi.org/10.1016/j.gie.2014.01.025
Response: We thank Singh et al for their interest in our article investigating the narrow-band imaging (NBI) characteristics of sessile serrated adenomas (SSAs).1 We agree with Singh et al that the details of our study design must be kept in mind in the interpretation of the results. We performed a retrospective analysis of prospectively collected data in which we assessed the Narrow Band Imaging International Colorectal Endoscopic (NICE) classification features2 that were observed in SSAs by endoscopists who were being trained in the use of NBI to identify polyps as either adenomatous or hyperplastic. As Singh et al point out, the NICE classification2 was not developed to differentiate hyperplastic polyps or adenomas from SSAs, and the endoscopists in our study did not set out to make NBI-based real-time diagnoses of SSA. Based in part on our clinical experience and in part on past publications3 as cited by Singh et al in their letter, we hypothesized that the endoscopists in our study would tend to observe the NICE features of hyperplastic polyps in those lesions that were later read by pathologists as SSAs. Instead, these endoscopists observed a profile of NICE features that was intermediate to the profile observed for hyperplastic polyps and adenomas. However, given that these endoscopists had proven proficiency in the ex vivo but not yet the in vivo application of the NICE classification, these results may not represent the NICE features of SSAs in the eyes of observers with more experience in NBI. Volume 79, No. 6 : 2014 GASTROINTESTINAL ENDOSCOPY 1031