1932

Abstract

For decades, conventional adenomas were the only known precursor lesions of colorectal cancer (CRC). Accordingly, education and research regarding CRC prevention were mainly focused on adenomas. The groundbreaking discovery that serrated polyps (SPs) also have the potential to develop into CRCs, and seem to account for a considerable proportion of sporadic CRCs, has led to a paradigm shift in the prevention, diagnosis, and treatment of CRC. Studies in recent years have led to our current understanding of SPs and associated CRC, but a lot of work is still to be done to further improve knowledge about this serrated neoplasia pathway and the clinical management of SPs and serrated polyposis syndrome (SPS). In this review, we reflect on the current understanding of SPs with respect to terminology, detection, resection, and surveillance and reflect on the management of SPS.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-med-042220-024703
2022-01-27
2024-10-07
Loading full text...

Full text loading...

/deliver/fulltext/med/73/1/annurev-med-042220-024703.html?itemId=/content/journals/10.1146/annurev-med-042220-024703&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Torlakovic E, Snover DC. 1996.. Serrated adenomatous polyposis in humans. . Gastroenterology 110:(3):74855
    [Google Scholar]
  2. 2. 
    Longacre TA, Fenoglio-Preiser CM. 1990.. Mixed hyperplastic adenomatous polyps/serrated adenomas. A distinct form of colorectal neoplasia. . Am. J. Surg. Pathol. 14:(6):52437
    [Google Scholar]
  3. 3. 
    Teoh HH, Delahunt B, Isbister WH. 1989.. Dysplastic and malignant areas in hyperplastic polyps of the large intestine. . Pathology 21:(2):13842
    [Google Scholar]
  4. 4. 
    Nagtegaal ID, Arends MJ, Odze RD, Lam AK. 2019.. Colorectal serrated lesions and polyps. . In WHO Classification of Tumours of the Digestive System, ed. RK Pai, MJ Mäkinen, C Rosty . Lyon, France:: Int. Agency Res. Cancer
    [Google Scholar]
  5. 5. 
    Hazewinkel Y, de Wijkerslooth TR, Stoop EM, et al. 2014.. Prevalence of serrated polyps and association with synchronous advanced neoplasia in screening colonoscopy. . Endoscopy 46:(3):21924
    [Google Scholar]
  6. 6. 
    IJspeert JE, Madani A, Overbeek LI, et al. 2017.. Implementation of an e-learning module improves consistency in the histopathological diagnosis of sessile serrated lesions within a nationwide population screening programme. . Histopathology 70:(6):92937
    [Google Scholar]
  7. 7. 
    O'Brien MJ, Yang S, Mack C, et al. 2006.. Comparison of microsatellite instability, CpG island methylation phenotype, BRAF and KRAS status in serrated polyps and traditional adenomas indicates separate pathways to distinct colorectal carcinoma end points. . Am. J. Surg. Pathol. 30:(12):1491501
    [Google Scholar]
  8. 8. 
    Spring KJ, Zhao ZZ, Karamatic R, et al. 2006.. High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy. . Gastroenterology 131:(5):14007
    [Google Scholar]
  9. 9. 
    Vennelaganti S, Cuatrecasas M, Vennalaganti P, et al. 2020.. Moderate inter-observer agreement among pathologists in differentiation of sessile serrated from hyperplastic polyps. . Gastroenterology 160:(1):45254
    [Google Scholar]
  10. 10. 
    Bettington M, Walker N, Rosty C, et al. 2014.. Critical appraisal of the diagnosis of the sessile serrated adenoma. . Am. J. Surg. Pathol. 38:(2):15866
    [Google Scholar]
  11. 11. 
    Dada M, Wang LM, Chetty R. 2013.. Incidence and review of sessile serrated polyp reporting in a district general hospital in the UK. . Virchows Arch. 463:(5):63336
    [Google Scholar]
  12. 12. 
    Paskett ED, Reeves KW, Pineau B, et al. 2005.. The association between cigarette smoking and colorectal polyp recurrence (United States). . Cancer Causes Control 16:(9):102133
    [Google Scholar]
  13. 13. 
    Figueiredo JC, Crockett SD, Snover DC, et al. 2015.. Smoking-associated risks of conventional adenomas and serrated polyps in the colorectum. . Cancer Causes Control 26:(3):37786
    [Google Scholar]
  14. 14. 
    Bosman FT, Carneiro F, Hruban RH, Theise ND. 2010.. Serrated polyps of the colon and rectum and serrated polyposis. . In WHO Classification of Tumours of the Digestive System, ed. DC Snover, DJ Ahnen, RW Burt, RD Odze , pp. 16065. Lyon, France:: Int. Agency Res. Cancer
    [Google Scholar]
  15. 15. 
    IJspeert JEG, de Wit K, van der Vlugt M, et al. 2016.. Prevalence, distribution and risk of sessile serrated adenomas/polyps at a center with a high adenoma detection rate and experienced pathologists. . Endoscopy 48:(8):74046
    [Google Scholar]
  16. 16. 
    Abdeljawad K, Vemulapalli KC, Kahi CJ, et al. 2015.. Sessile serrated polyp prevalence determined by a colonoscopist with a high lesion detection rate and an experienced pathologist. . Gastrointest. Endosc. 81:(3):51724
    [Google Scholar]
  17. 17. 
    Bettington M, Walker N, Rosty C, et al. 2017.. Clinicopathological and molecular features of sessile serrated adenomas with dysplasia or carcinoma. . Gut 66:(1):97106
    [Google Scholar]
  18. 18. 
    Liu C, Walker NI, Leggett BA, et al. 2017.. Sessile serrated adenomas with dysplasia: morphological patterns and correlations with MLH1 immunohistochemistry. . Mod. Pathol. 30:(12):172838
    [Google Scholar]
  19. 19. 
    Bettington ML, Walker NI, Rosty C, et al. 2015.. A clinicopathological and molecular analysis of 200 traditional serrated adenomas. . Mod. Pathol. 28:(3):41427
    [Google Scholar]
  20. 20. 
    Toyota M, Ahuja N, Ohe-Toyota M, et al. 1999.. CpG island methylator phenotype in colorectal cancer. . PNAS 96:(15):868186
    [Google Scholar]
  21. 21. 
    Snover DC. 2011.. Update on the serrated pathway to colorectal carcinoma. . Hum. Pathol. 42::110
    [Google Scholar]
  22. 22. 
    Arain MA, Sawhney M, Sheikh S, et al. 2010.. CIMP status of interval colon cancers: another piece to the puzzle. . Am. J. Gastroenterol. 105:(5):118995
    [Google Scholar]
  23. 23. 
    Samadder NJ, Curtin K, Tuohy TMF, et al. 2014.. Characteristics of missed or interval colorectal cancer and patient survival: a population-based study. . Gastroenterology 146:(4):95060
    [Google Scholar]
  24. 24. 
    Kambara T, Simms LA, Whitehall VL, et al. 2004.. BRAF mutation is associated with DNA methylation in serrated polyps and cancers of the colorectum. . Gut 53:(8):113744
    [Google Scholar]
  25. 25. 
    Rad R, Cadiñanos J, Rad L, et al. 2013.. A genetic progression model of Braf(V600E)-induced intestinal tumorigenesis reveals targets for therapeutic intervention. . Cancer Cell 24:(1):1529
    [Google Scholar]
  26. 26. 
    Lannagan TRM, Lee YK, Wang T, et al. 2019.. Genetic editing of colonic organoids provides a molecularly distinct and orthotopic preclinical model of serrated carcinogenesis. . Gut 68:(4):68492
    [Google Scholar]
  27. 27. 
    Liu C, Fennell LJ, Bettington ML, et al. 2019.. DNA methylation changes that precede onset of dysplasia in advanced sessile serrated adenomas. . Clin. Epigenet. 11:(1):90
    [Google Scholar]
  28. 28. 
    Kane MF, Loda M, Gaida GM, et al. 1997.. Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. . Cancer Res. 57:(5):80811
    [Google Scholar]
  29. 29. 
    Bond CE, Umapathy A, Ramsnes I, et al. 2012.. p53 mutation is common in microsatellite stable, BRAF mutant colorectal cancers. . Int. J. Cancer 130:(7):156776
    [Google Scholar]
  30. 30. 
    Phipps AI, Alwers E, Harrison T, et al. 2020.. Association between molecular subtypes of colorectal tumors and patient survival, based on pooled analysis of 7 international studies. . Gastroenterology 158:(8):215868.e4
    [Google Scholar]
  31. 31. 
    Kopetz S, Grothey A, Yaeger R, et al. 2019.. Encorafenib, binimetinib, and cetuximab in BRAF V600E-mutated colorectal cancer. . N. Engl. J. Med. 381:(17):163243
    [Google Scholar]
  32. 32. 
    André T, Shiu KK, Kim TW, et al. 2020.. Pembrolizumab in microsatellite-instability-high advanced colorectal cancer. . N. Engl. J. Med. 383:(23):220718
    [Google Scholar]
  33. 33. 
    Guinney J, Dienstmann R, Wang X, et al. 2015.. The consensus molecular subtypes of colorectal cancer. . Nat. Med. 21:(11):135056
    [Google Scholar]
  34. 34. 
    Imperiale TF, Ransohoff DF, Itzkowitz SH, et al. 2014.. Multitarget stool DNA testing for colorectal-cancer screening. . N. Engl. J. Med. 370:(14):128797
    [Google Scholar]
  35. 35. 
    van Rijn JC, Reitsma JB, Stoker J, et al. 2006.. Polyp miss rate determined by tandem colonoscopy: a systematic review. . Am. J. Gastroenterol. 101:(2):34350
    [Google Scholar]
  36. 36. 
    Zhao S, Wang S, Pan P, et al. 2019.. Magnitude, risk factors, and factors associated with adenoma miss rate of tandem colonoscopy: a systematic review and meta-analysis. . Gastroenterology 156:(6):166174.e11
    [Google Scholar]
  37. 37. 
    Clark BT, Laine L. 2016.. High-quality bowel preparation is required for detection of sessile serrated polyps. . Clin. Gastroenterol. Hepatol. 14:(8):115562
    [Google Scholar]
  38. 38. 
    de Wijkerslooth TR, Stoop EM, Bossuyt PM, et al. 2013.. Differences in proximal serrated polyp detection among endoscopists are associated with variability in withdrawal time. . Gastrointest. Endosc. 77:(4):61723
    [Google Scholar]
  39. 39. 
    Butterly L, Robinson CM, Anderson JC, et al. 2014.. Serrated and adenomatous polyp detection increases with longer withdrawal time: results from the New Hampshire Colonoscopy Registry. . Am. J. Gastroenterol. 109:(3):41726
    [Google Scholar]
  40. 40. 
    Roelandt P, Demedts I, Willekens H, et al. 2019.. Impact of endoscopy system, high definition, and virtual chromoendoscopy in daily routine colonoscopy: a randomized trial. . Endoscopy 51:(3):23743
    [Google Scholar]
  41. 41. 
    Hurt C, Ramaraj R, Farr A, et al. 2019.. Feasibility and economic assessment of chromocolonoscopy for detection of proximal serrated neoplasia within a population-based colorectal cancer screening programme (CONSCOP): an open-label, randomised controlled non-inferiority trial. . Lancet Gastroenterol. Hepatol. 4:(5):36475
    [Google Scholar]
  42. 42. 
    Atkinson NSS, Ket S, Bassett P, et al. 2019.. Narrow-band imaging for detection of neoplasia at colonoscopy: a meta-analysis of data from individual patients in randomized controlled trials. . Gastroenterology 157:(2):46271
    [Google Scholar]
  43. 43. 
    Omata F, Ohde S, Deshpande GA, et al. 2014.. Image-enhanced, chromo, and cap-assisted colonoscopy for improving adenoma/neoplasia detection rate: a systematic review and meta-analysis. . Scand. J. Gastroenterol. 49:(2):22237
    [Google Scholar]
  44. 44. 
    Bleijenberg AGC, van Leerdam ME, Bargeman M, et al. 2020.. Substantial and sustained improvement of serrated polyp detection after a simple educational intervention: results from a prospective controlled trial. . Gut 69:(12):215058
    [Google Scholar]
  45. 45. 
    Particip. Paris Worksh. 2003.. The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002. . Gastrointest. Endosc. 58:(6 Suppl.):S343
    [Google Scholar]
  46. 46. 
    Kudo S, Hirota S, Nakajima T, et al. 1994.. Colorectal tumours and pit pattern. . J. Clin. Pathol. 47:(10):88085
    [Google Scholar]
  47. 47. 
    Hewett DG, Kaltenbach T, Sano Y, et al. 2012.. Validation of a simple classification system for endoscopic diagnosis of small colorectal polyps using narrow-band imaging. . Gastroenterology 143:(3):599607.e1
    [Google Scholar]
  48. 48. 
    Singh R, Jayanna M, Navadgi S, et al. 2013.. Narrow-band imaging with dual focus magnification in differentiating colorectal neoplasia. . Dig. Endosc. 25:(Suppl. 2):1620
    [Google Scholar]
  49. 49. 
    IJspeert JE, Bastiaansen BA, van Leerdam ME, et al. 2016.. Development and validation of the WASP classification system for optical diagnosis of adenomas, hyperplastic polyps and sessile serrated adenomas/polyps. . Gut 65:(6):96370
    [Google Scholar]
  50. 50. 
    Meester RGS, van Herk M, Lansdorp-Vogelaar I, Ladabaum U. 2020.. Prevalence and clinical features of sessile serrated polyps: a systematic review. . Gastroenterology 159:(1):10518
    [Google Scholar]
  51. 51. 
    Hazewinkel Y, López-Cerón M, East JE, et al. 2013.. Endoscopic features of sessile serrated adenomas: validation by international experts using high-resolution white-light endoscopy and narrow-band imaging. . Gastrointest. Endosc. 77:(6):91624
    [Google Scholar]
  52. 52. 
    Rex DK, Rahmani EY. 1999.. New endoscopic finding associated with hyperplastic polyps. . Gastrointest. Endosc. 50:(5):7046
    [Google Scholar]
  53. 53. 
    Crockett SD, Nagtegaal ID. 2019.. Terminology, molecular features, epidemiology, and management of serrated colorectal neoplasia. . Gastroenterology 157:(4):94966.e4
    [Google Scholar]
  54. 54. 
    Burgess NG, Tutticci NJ, Pellise M, Bourke MJ. 2014.. Sessile serrated adenomas/polyps with cytologic dysplasia: a triple threat for interval cancer. . Gastrointest. Endosc. 80:(2):30710
    [Google Scholar]
  55. 55. 
    Farrar WD, Sawhney MS, Nelson DB, et al. 2006.. Colorectal cancers found after a complete colonoscopy. . Clin. Gastroenterol. Hepatol. 4:(10):125964
    [Google Scholar]
  56. 56. 
    Morris EJ, Rutter MD, Finan PJ, et al. 2015.. Post-colonoscopy colorectal cancer (PCCRC) rates vary considerably depending on the method used to calculate them: a retrospective observational population-based study of PCCRC in the English National Health Service. . Gut 64:(8):124856
    [Google Scholar]
  57. 57. 
    Kaminski MF, Regula J, Kraszewska E, et al. 2010.. Quality indicators for colonoscopy and the risk of interval cancer. . N. Engl. J. Med. 362:(19):1795803
    [Google Scholar]
  58. 58. 
    Corley DA, Jensen CD, Marks AR, et al. 2014.. Adenoma detection rate and risk of colorectal cancer and death. . N. Engl. J. Med. 370:(14):1298306
    [Google Scholar]
  59. 59. 
    Vennelaganti S, Cuatrecasas M, Vennalaganti P, et al. 2021.. Interobserver agreement among pathologists in the differentiation of sessile serrated from hyperplastic polyps. . Gastroenterology 160:(1):45254.e1
    [Google Scholar]
  60. 60. 
    IJspeert JE, van Doorn SC, van der Brug YM, et al. 2015.. The proximal serrated polyp detection rate is an easy-to-measure proxy for the detection rate of clinically relevant serrated polyps. . Gastrointest. Endosc. 82:(5):87077
    [Google Scholar]
  61. 61. 
    Kahi CJ, Hewett DG, Norton DL, et al. 2011.. Prevalence and variable detection of proximal colon serrated polyps during screening colonoscopy. . Clin. Gastroenterol. Hepatol. 9:(1):4246
    [Google Scholar]
  62. 62. 
    Lee JK, Liles EG, Bent S, et al. 2014.. Accuracy of fecal immunochemical tests for colorectal cancer: systematic review and meta-analysis. . Ann. Intern. Med. 160:(3):171
    [Google Scholar]
  63. 63. 
    Carethers JM. 2020.. Fecal DNA testing for colorectal cancer screening. . Annu. Rev. Med. 71::5969
    [Google Scholar]
  64. 64. 
    Hassan C, Spadaccini M, Iannone A, et al. 2020.. Performance of artificial intelligence in colonoscopy for adenoma and polyp detection: a systematic review and meta-analysis. . Gastrointest. Endosc. 93:(1):7785.e6
    [Google Scholar]
  65. 65. 
    Rex DK, Kahi C, O'Brien M, et al. 2011.. The American Society for Gastrointestinal Endoscopy PIVI (Preservation and Incorporation of Valuable Endoscopic Innovations) on real-time endoscopic assessment of the histology of diminutive colorectal polyps. . Gastrointest. Endosc. 73:(3):41922
    [Google Scholar]
  66. 66. 
    Pohl H, Srivastava A, Bensen SP, et al. 2013.. Incomplete polyp resection during colonoscopy-results of the complete adenoma resection (CARE) study. . Gastroenterology 144:(1):7480.e1
    [Google Scholar]
  67. 67. 
    Tate DJ, Awadie H, Bahin FF, et al. 2018.. Wide-field piecemeal cold snare polypectomy of large sessile serrated polyps without a submucosal injection is safe. . Endoscopy 50:(3):24852
    [Google Scholar]
  68. 68. 
    van Hattem WA, Shahidi N, Vosko S, et al. 2021.. Piecemeal cold snare polypectomy versus conventional endoscopic mucosal resection for large sessile serrated lesions: a retrospective comparison across two successive periods. . Gut 70:(9):169197
    [Google Scholar]
  69. 69. 
    Thoguluva Chandrasekar V, Aziz M, Patel HK, et al. 2020.. Efficacy and safety of endoscopic resection of sessile serrated polyps 10 mm or larger: a systematic review and meta-analysis. . Clin. Gastroenterol. Hepatol. 18:(11):244855.e3
    [Google Scholar]
  70. 70. 
    Erichsen R, Baron JA, Hamilton-Dutoit SJ, et al. 2016.. Increased risk of colorectal cancer development among patients with serrated polyps. . Gastroenterology 150:(4):895902.e5
    [Google Scholar]
  71. 71. 
    Holme Ø, Bretthauer M, Eide TJ, et al. 2015.. Long-term risk of colorectal cancer in individuals with serrated polyps. . Gut 64:(6):92936
    [Google Scholar]
  72. 72. 
    He X, Hang D, Wu K, et al. 2020.. Long-term risk of colorectal cancer after removal of conventional adenomas and serrated polyps. . Gastroenterology 158:(4):85261.e4
    [Google Scholar]
  73. 73. 
    Yoon JY, Kim HT, Hong SP, et al. 2015.. High-risk metachronous polyps are more frequent in patients with traditional serrated adenomas than in patients with conventional adenomas: a multicenter prospective study. . Gastrointest. Endosc. 82:(6):108793.e3
    [Google Scholar]
  74. 74. 
    Gupta S, Lieberman D, Anderson JC, et al. 2020.. Recommendations for follow-up after colonoscopy and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. . Am. J. Gastroenterol. 115:(3):41534
    [Google Scholar]
  75. 75. 
    Rutter MD, East J, Rees CJ, et al. 2020.. British Society of Gastroenterology/Association of Coloproctology of Great Britain and Ireland/Public Health England post-polypectomy and post-colorectal cancer resection surveillance guidelines. . Gut 69:(2):20123
    [Google Scholar]
  76. 76. 
    Hassan C, Antonelli G, Dumonceau JM, et al. 2020.. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline—Update 2020. . Endoscopy 52:(8):687700
    [Google Scholar]
  77. 77. 
    Rosty C, Brosens LAA, Dekker E, Nagtegaal ID. 2019.. Genetic tumour syndromes of the digestive system. . In WHO Classification of Tumours: Genetic Tumour Syndromes of the Digestive System, Vol. 1, ed. MJ Arends, F Carneiro, SF Lax, AJ Lazar , pp. 2426. Lyon, France:: Int. Agency Res. Cancer, 5th ed..
    [Google Scholar]
  78. 78. 
    IJspeert JEG, Bevan R, Senore C, et al. 2017.. Detection rate of serrated polyps and serrated polyposis syndrome in colorectal cancer screening cohorts: a European overview. . Gut 66:(7):122532
    [Google Scholar]
  79. 79. 
    IJspeert JEG, Rana SA, Atkinson NS, et al. 2017.. Clinical risk factors of colorectal cancer in patients with serrated polyposis syndrome: a multicentre cohort analysis. . Gut 66:(2):27884
    [Google Scholar]
  80. 80. 
    Carballal S, Rodríguez-Alcalde D, Moreira L, et al. 2016.. Colorectal cancer risk factors in patients with serrated polyposis syndrome: a large multicentre study. . Gut 65:(11):182937
    [Google Scholar]
  81. 81. 
    Bleijenberg AG, IJspeert JE, van Herwaarden YJ, et al. 2020.. Personalised surveillance for serrated polyposis syndrome: results from a prospective 5-year international cohort study. . Gut 69:(1):11221
    [Google Scholar]
  82. 82. 
    van Leerdam ME, Roos VH, van Hooft JE, et al. 2019.. Endoscopic management of polyposis syndromes: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. . Endoscopy 51:(9):87795
    [Google Scholar]
  83. 83. 
    East JE, Atkin WS, Bateman AC, et al. 2017.. British Society of Gastroenterology position statement on serrated polyps in the colon and rectum. . Gut 66:(7):118196
    [Google Scholar]
  84. 84. 
    Buchanan DD, Clendenning M, Zhuoer L, et al. 2017.. Lack of evidence for germline RNF43 mutations in patients with serrated polyposis syndrome from a large multinational study. . Gut 66:(6):117072
    [Google Scholar]
  85. 85. 
    Yan HHN, Lai JCW, Ho SL, et al. 2017.. RNF43 germline and somatic mutation in serrated neoplasia pathway and its association with BRAF mutation. . Gut 66:(9):164556
    [Google Scholar]
  86. 86. 
    Boparai KS, Reitsma JB, Lemmens V, et al. 2010.. Increased colorectal cancer risk in first-degree relatives of patients with hyperplastic polyposis syndrome. . Gut 59:(9):122225
    [Google Scholar]
/content/journals/10.1146/annurev-med-042220-024703
Loading
/content/journals/10.1146/annurev-med-042220-024703
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error