An Update on Inherited Colon Cancer and Gastrointestinal Polyposis
Authors:
Pavlína Plevová
Authors‘ workplace:
Katedra biomedicínských oborů, LF Ostravské univerzity Oddělení lékařské genetiky, FN Ostrava
Published in:
Klin Onkol 2019; 32(Supplementum2): 97-108
Category:
Review
doi:
https://doi.org/10.14735/amko2019S97
Overview
Background: It is estimated that 5–10% of colorectal cancers arise due to a known genetic syndrome. Individuals with these cancer syndromes are also at risk of extracolonic cancers. Polyposis and nonpolyposis hereditary syndromes are generally recognized. Inclusion of next-generation sequencing technology, especially multiple-gene panel testing, in routine laboratory practice has made identifying the causes of these diseases significantly easier.
Purpose: To summarize current knowledge of the causes, clinical manifestations, diagnostic criteria, and recommendations for presymptomatic screening of individuals at risk of hereditary gastrointestinal polyposis and colorectal cancer syndromes. We dicuss currently defined syndromes detected by multiple-gene panel next-generation sequencing; these include constitutional mismatch repair deficiency (biallelic MLH1, MSH2, MSH6, PMS2 gene mutations), gastric adenocarcinoma and proximal polyposis of the stomach (APC gene), NTHL1-associated polyposis, polymerase proofreading-associated polyposis (POLD1, POLE genes), juvenile polyposis (SMAD4, BMPR1A genes), and serrated polyposis syndromes. Another aim is to summarize recent knowledge about well-known syndromes, including hereditary nonpolyposis colon cancer (Lynch syndrome), familial adenomatous polyposis, MUTYH-associated polyposis, and Peutz–Jeghers and Cowden/PTEN hamartoma tumor syndromes.
Conclusion: Awareness of hereditary polyposis/colon cancer syndromes enables early diagnosis and prevention of cancer in affected individuals and their relatives. Genetic counseling, presymptomatic testing of at-risk individuals, and efficient screening may be beneficial for affected families.
Thank to Lenka Foretová, M.D., PhD, (Masaryk Memorial Cancer Institute, Brno) for a critical review of the manuscript and valuable advices.
The author declares she has no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE recommendation for biomedical papers.
Submitted: 1. 3. 2019
Accepted: 6. 6. 2019
Keywords:
genes – colonic polyps – Stomach – polyps – secondary prevention
Sources
1. Jasperson KW, Tuohy TM, Neklason DW et al. Hereditary and familial colon cancer. Gastroenterology 2010; 138 (6): 2044–2058. doi: 10.1053/j.gastro.2010.01.054.
2. Wells K, Wise P. Hereditary colorectal cancer syndromes. Surg Clin N Am 2017; 97 (3): 605–625. doi: 10.1016/j.suc.2017.01.009.
3. Plevová P, Novotný J, Šachlová M et al. Hereditární nepolypózní kolorektální karcinom (HNPCC, Lynchův syndrom). Klin Onkol 2009; 22 (Supp l): S12–S15.
4. Plevová P, Štekrová J, Kohoutová M et al. Familiární adenomatózní polypóza. Klin Onkol 2009; 22 (Suppl 1): S16–S19.
5. Puchmajerová A, Vasovčák P, Křepelová A. Peutz-Jeghersův syndrom. Klin Onkol 2009; 22 (Suppl 1): S36–S37.
6. Puchmajerová A, Vasovčák P, Křepelová A et al. Cowdenův syndrom Klin Onkol 2009; 22 (Suppl 1): S56–S57.
7. Spoto CPE, Gullo I, Carneiro F et al. Hereditary gastrointestinal carcinomas and their precursors: an algorithm for genetic testing. Semin Diagn Pathol 2018; 35 (3): 170–183. doi: 10.1053/j.semdp.2018.01.004.
8. de la Chapelle A. The incidence of Lynch syndrome. Fam Cancer 2005; 4 (3): 233–237. 10.1007/s10689-004-5811-3.
9. Dunlop MG, Farrington SM, Carothers AD et al. Cancer risk associated with germline DNA mismatch repair gene mutations. Hum Mol Genet 1997; 6 (1): 105–110. doi: 10.1093/hmg/6.1.105.
10. Guillem JG, Calle JPL, Cellini C et al. Varying features of early age-of-onset “sporadic” and hereditary nonpolyposis colorectal cancer patients. Dis Colon Rectum 1999; 42 (1): 36–42.
11. Provenzale D, Gupta S, Ahnen DJ et al. Genetic/familial high-risk assessment: colorectal version 1.2016, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 2016; 14 (8): 1010–1030.
12. Burt RW, Leppert MF, Slattery ML et al. Genetic testing and phenotype in a large kindred with attenuated familial adenomatous polyposis. Gastroenterology 2004; 127 (2): 444–451.
13. Vogt S, Jones N, Christian D et al. Expanded extracolonic tumor spectrum. Gastroenterology 2009; 137 (6): 1976–1985. doi: 10.1053/j.gastro.2009.08.052.
14. Lee SE, Kang SY, Cho J et al. Pyloric gland adenoma in Lynch syndrome. Am J Surg Pathol 2014; 38 (6): 784–792. doi: 10.1097/PAS.0000000000000185.
15. Palomaki GE, McClain MR, Melillo S et al. EGAPP supplementary evidence review: DNA testing strategies aimed at reducing morbidity and mortality from Lynch syndrome. Genet Med 2009; 11 (1): 42–65. doi: 10.1097/GIM.0b013e31818fa2db.
16. Pinto D, Pinto C, Guerra J et al. Contribution of MLH1 constitutional methylation for Lynch syndrome diagnosis in patients with tumor MLH1 downregulation. Cancer Med 2018; 7 (2): 433–444. doi: 10.1002/cam4.1285.
17. Castillejo A, Hernández-Illán E, Rodriguez-Soler M et al. Prevalence of MLH1 constitutional epimutations as a cause of Lynch syndrome in unselected versus selected consecutive series of patients with colorectal cancer. J Med Genet 2015; 52 (7): 498–502. doi: 10.1136/jmedgenet-2015-103076.
18. Hesson LB, Packham D, Kwok CT et al. Lynch syndrome associated with two MLH1 promoter variants and allelic imbalance of MLH1 expression. Hum Mutat 2014; 36 (6): 622–630. doi: 10.1002/humu.22785.
19. Ligtenberg MJ, Kuiper RP, Chan TL et al. Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3’ exons of TACSTD1. Nat Genet 2009; 41 (1): 112–117. doi: 10.1038/ng.283.
20. Hitchins MP. The role of epigenetics in lynch syndrome. Fam Cancer 2013; 12 (2): 189–205. doi: 10.1007/s10689-013-9613-3.
21. Berg M, Hagland HR, Søreide K. Comparison of CpG island methylator phenotype (CIMP) frequency in colon cancer using different probe and gene specific scoring alternatives on recommended multigene panels. PLoS ONE 2014; 9 (1): e86657. doi: 10.1371/journal.pone.0086657.
22. Grothey A, Venook AP. Optimizing adjuvant therapy for localized colon cancer and treatment selection in advanced colorectal cancer. J Natl Compr Canc Netw 2018; 16 (Suppl 5): 611–615. doi: 10.6004/jnccn.2018.0038.
23. Shia J. Immunohistochemistry versus microsatellite instability testing for screening colorectal cancer patients at risk for hereditary nonpolyposis colorectal cancer syndrome. Part I. The utility of immunohistochemistry. J Mol Diagn 2008; 10 (4): 293–300. doi: 10.2353/jmoldx.2008.080031.
24. Lindor NM, Petersen GM, Hadley DW et al. Recommendations for the care of individuals with an inherited predisposition to Lynch syndrome: a systematic review. JAMA 2006; 296 (12): 1507–1517. doi: 10.1001/jama.296.12.1507.
25. Bouzourene H, Hutter P, Losi L et al. Selection of patients with germline MLH1 mutated Lynch syndrome by determination of MLH1 methylation and BRAF mutation. Fam Cancer 2009; 9 (2): 167–172. doi: 10.1007/s10689-009-9302-4.
26. Veigl ML, Kasturi L, Olechnowicz J et al. Biallelic inactivation of hMLH1 by epigenetic gene silencing, a novel mechanism causing human MSI cancers. Proc Natl Acad Sci USA 1998; 95 (15): 8698–8702. doi: 10.1073/pnas.95.15.8698.
27. Koinuma K, Shitoh K, Miyakura Y et al. Mutations of BRAF are associated with extensive hMLH1 promoter methylation in sporadic colorectal carcinomas. Int J Cancer 2004; 108 (2): 237–242. doi: 10.1002/ijc.11523.
28. Syngal S, Brand RE, Church JM et al. ACG clinical guideline: genetic testing and management of hereditary gastrointestinal cancer syndromes. Am J Gastroenterol 2015; 110 (2): 223–262. doi: 10.1038/ajg.2014.435.
29. Wimmer K, Kratz CP, Vasen HF et al. European consortium “care for CMMRD” (C4CMMRD). J Med Genet 2014; 51 (6): 355–365. doi: 10.1136/jmedgenet-2014-102284.
30. Valle L. Recent discoveries in the genetics of familial colorectal cancer and polyposis. Clin Gastroenterol Hepatol 2017; 15 (6): 809–819. doi: 10.1016/j.cgh.2016.09.148.
31. Durno CA, Sherman PM, Aronson M et al. Phenotypic and genotypic characterisation of biallelic mismatch repair deficiency (BMMR-D) syndrome. Eur J Cancer 2015; 51 (8): 977–983. doi: 10.1016/j.ejca.2015.02.008.
32. Vasen HF, Ghorbanoghli Z, Bourdeaut F et al. Guidelines for surveillance of individuals with constitutional mismatch repair-deficiency proposed by the European Consortium “Care for CMMR-D” (C4CMMR-D). J Med Genet 2014; 51 (5): 283–293. doi: 10.1136/jmedgenet-2013-102238.
33. Ramchander NC, Ryan NA, Crosbie EJ et al. Homozygous germ-line mutation of the PMS2 mismatch repair gene: a unique case report of constitutional mismatch repair deficiency (CMMRD). BMC Med Genet 2017; 18 (1): 40. doi: 10.1186/s12881-017-0391-x.
34. Bouffet E, Larouche V, Campbell BB et al. Immune checkpoint inhibition for hypermutant glioblastoma multiforme resulting from germline biallelic mismatch repair deficiency. J Clin Oncol 2016; 34 (19): 2206–2211. doi: 10.1200/JCO.2016.66.6552.
35. Nebot-Bral L, Brandao D, Verlingue L et al. Hypermutated tumours in the era of immunotherapy: the paradigm of personalised medicine. Eur J Cancer 2017; 84: 290–303. doi: 10.1016/j.ejca.2017.07.026.
36. Guastadisegni C, Colafranceschi M, Ottini L et al. Microsatellite instability as a marker of prognosis and response to therapy: a meta-analysis of colorectal cancer survival data. Eur J Cancer 2010; 46 (15): 2788–2798. doi: 10.1016/j.ejca.2010.05.009.
37. Abedalthagafi M. Constitutional mismatch repair-deficiency: current problems and emerging therapeutic strategies. Oncotarget 2018; 9 (83): 35458–35469. doi: 10.18632/oncotarget.26249.
38. Pavelka Z, Zitterbart K, Nosková H et al. Effective Immunotherapy of glioblastoma in an adolescent with constitutional mismatch repair-deficiency syndrome. Klin Onkol 2019; 32 (1): 70–74. doi: 10.14735/amko201970.
39. Genetics Home Reference. U.S. National Library of Medicine. c2018 [online]. Available from: https: //ghr.nlm.nih.gov/condition/familial-adenomatous-polyposis.
40. Järvinen HJ. Epidemiology of familial adenomatous polyposis in Finland: impact of family screening on the colorectal cancer rate and survival. Gut 1992; 33 (3): 357–360. doi: 10.1136/gut.33.3.357.
41. Bisgaard ML, Fenger K, Bülow S et al. Familial adenomatous polyposis (FAP): frequency, penetrance, and mutation rate. Hum Mutat 1994; 3 (2): 121–123. doi: 10.1002/humu.1380030206.
42. Wood LD, Salaria SN, Cruise MW et al. Upper GI tract lesions in familial adenomatous polyposis (FAP): enrichment of pyloric gland adenomas and other gastric and duodenal neoplasms. Am J Surg Pathol 2014; 38 (3): 389–393. doi: 10.1097/PAS.0000000000000146.
43. Brosens LA, Keller JJ, Offerhaus GJ et al. Prevention and management of duodenal polyps in familial adenomatous polyposis. Gut 2005; 54 (7): 1034–1043. doi: 10.1136/gut.2004.053843.
44. Li J, Woods S, Healey S et al. Point mutations in exon 1B of APC reveal gastric adenocarcinoma and proximal polyposis of the stomach as a familial adenomatous polyposis variant. Am J Hum Genet 2016; 98 (5): 830–842. doi: 10.1016/j.ajhg.2016.03.001.
45. Arnason T, Liang WY, Alfaro E et al. Morphology and natural history of familial adenomatous polyposis-associated dysplastic fundic gland polyps. Histopathology 2014; 65 (3): 353–362. doi: 10.1111/his.12393.
46. Garrean S, Hering J, Saied A et al. Gastric adenocarcinoma arising from fundic gland polyps in a patient with familial adenomatous polyposis syndrome. Am Surg 2008; 74 (1): 79–83.
47. Talseth-Palmer BA. The genetic basis of colonic adenomatous polyposis syndromes. Hered Cancer Clin Pract 2017; 15: 5. doi: 10.1186/s13053-017-0065-x.
48. Worthley DL, Phillips KD, Wayte N et al. Gastric adenocarcinoma and proximal polyposis of the stomach (GAPPS): a new autosomal dominant syndrome. Gut 2012; 61 (5): 774–779. doi: 10.1136/gutjnl-2011-300348.
49. Repak R, Kohoutova D, Podhola M et al. The first European family with gastrin adenocarcinoma and proximal polyposis of the stomach: case report and review of the literature. Gastrointest Endosc 2016; 84 (4): 718–725. doi: 10.1016/j.gie.2016.06.023.
50. Genta RM, Schuler CM, Robiou CI et al. No association between gastric fundic gland polyps and gastrointestinal neoplasia in a study of over 100,000 patients. Clin Gastroenterol Hepatol 2009; 7 (8): 849–854. doi: 10.1016/j.cgh.2009.05.015.
51. Huang CZ, Lai RX, Mai L et al. Relative risk factors associated with the development of fundic gland polyps. Eur J Gastroenterol Hepatol 2014; 26 (11): 1217–1221. doi: 10.1097/MEG.0000000000000199.
52. Stolte M, Vieth M, Ebert MP. High-grade dysplasia in sporadic fundic gland polyps: clinically relevant or not? Eur J Gastroenterol Hepatol 2003; 15 (11): 1153–1156. doi: 10.1097/01.meg.0000085495.01212.1c.
53. Lin Y, Lin S, Baxter MD et al. Novel APC promoter and exon 1B deletion and allelic silencing in three mutation-negative classic familial adenomatous polyposis families. Genome Med 2015; 7 (1): 42. doi: 10.1186/s13073-015-0148-0.
54. Snow AK, Tuohy TM, Sargent NR et al. APC promoter 1B deletion in seven American families with familial adenomatous polyposis. Clin Genet 2015; 88 (4): 360–365. doi: 10.1111/cge.12503.
55. Groves C, Lamlum H, Crabtree M et al. Mutation cluster region, association between germline and somatic mutations and genotype-phenotype correlation in upper gastrointestinal familial adenomatous polyposis. Am J Pathol 2002; 160 (6): 2055–2061. doi: 10.1016/S0002-9440 (10) 61155-8.
56. Atlas of Genetics and Cytogenetics in Oncology and Haematology. Institut de l‘Information Scientifique et Technique. c2018. [online]. Available from: http: //atlasgeneticsoncology.org/Kprones/MYHpolypID10121.html.
57. Papp J, Kovacs ME, Matrai Z et al. Contribution of APC and MUTYH mutations to familial adenomatous polyposis susceptibility in Hungary. Fam Cancer 2016; 15 (1): 85–97. doi: 10.1007/s10689-015-9845-5.
58. Nielsen M, Lynch H, Infante E et al. MUTYH-associated polyposis. GeneReviews. University of Washington. c1993–2019. [online]. Available from: https: //www.ncbi.nlm.nih.gov/books/NBK107219/.
59. Nielsen M, Poley JW, Verhoef S et al. Duodenal carcinoma in MUTYH-associated polyposis. J Clin Pathol 2006; 59 (11): 1212–1215. doi: 10.1136/jcp.2005.031757.
60. Morak M, Heidenreich B, Keller G et al. Biallelic MUTYH mutations can mimic Lynch syndrome. Eur J Hum Genet 2014; 22 (11): 1334–1337. doi: 10.1038/ejhg.2014.15.
61. Win AK, Dowty JG, Cleary SP et al. Risk of colorectal cancer for carriers of mutations in MUTYH, with and without a family history of cancer. Gastroenterology 2014; 146 (5): 1208–1211. doi: 10.1053/j.gastro.2014.01.022.
62. Win AK, Reece JC, Dowty JG et al. Risk of extracolonic cancers for people with biallelic and monoallelic mutations in MUTYH. Int J Cancer 2016; 139 (7): 1557–1563. doi: 10.1002/ijc.30197.
63. Lipton L, Halford SE, Johnson V et al. Carcinogenesis in MYH-associated polyposis follows a distinct genetic pathway. Cancer Res 2003; 63 (22): 7595–7599.
64. Weren RD, Ligtenberg MJ, Kets CM et al. A germline homozygous mutation in the base-excision repair gene NTHL1 causes adenomatous polyposis and colorectal cancer. Nat Genet 2015; 47 (6): 668–671. doi: 10.1038/ng.3287.
65. Grolleman JE, de Voer RM, Elsayed FA et al. Mutational signature analysis reveals NTHL1 deficiency to cause a multi-tumor phenotype. Cancer Cell 2019; 35 (2): 256–266. doi: 10.1016/j.ccell.2018.12.011.
66. Weren RD, Ligtenberg MJ, Geurts van Kessel A et al. NTHL1 and MUTYH polyposis syndromes: two sides of the same coin? J Pathol 2018; 244 (2): 135–142. doi: 10.1002/path.5002.
67. Bellido F, Pineda M, Aiza G et al. POLE and POLD1 mutations in 529 kindred with familial colorectal cancer and/or polyposis: review of reported cases and recommendations for genetic testing and surveillance. Genet Med 2016; 18 (4): 325–332. doi: 10.1038/gim.2015.75.
68. Nicolas E, Golemis EA, Arora S. POLD1: Central mediator of DNA replication and repair, and implication in cancer and other pathologies. Gene 2016; 590 (1): 128–141. doi: 10.1016/j.gene.2016.06.031.
69. Hansen MF, Johansen J, Bjornevoll I et al. A novel POLE mutation associated with cancers of colon, pancreas, ovaries and small intestine. Fam Cancer 2015; 14 (3): 437–448. doi: 10.1007/s10689-015-9803-2.
70. Rohlin A, Zagoras T, Nilsson S et al. A mutation in POLE predisposing to a multi-tumour phenotype. Int J Oncol 2014; 45 (1): 77–81. doi: 10.3892/ijo.2014.2410.
71. Wimmer K, Beilken A, Nustede R et al. A novel germline POLE mutation causes an early onset cancer prone syndrome mimicking constitutional mismatch repair deficiency. Fam Cancer 2017; 16 (1): 67–71. doi: 10.1007/s10689-016-9925-1.
72. Palles C, Cazier JB, Howarth KM et al. Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas. Nat Genet 2013; 45 (2): 136–144. doi: 10.1038/ng.2503.
73. Buchanan DD, Stewart JR, Clendenning M et al. Risk of colorectal cancer for carriers of a germline mutation in POLE or POLD1. Genet Med 2018; 20 (8): 890–895. doi: 10.1038/gim.2017.185.
74. Heitzer E, Tomlinson I. Replicative DNA polymerase mutations in cancer. Curr Opin Genet Dev 2014; 24: 107–113. doi: 10.1016/j.gde.2013.12.005.
75. Rashid M, Fischer A, Wilson CH et al. Adenoma development in familial adenomatous polyposis and MUTYH-associated polyposis: somatic landscape and driver genes. J Pathol 2016; 238 (1): 98–108. doi: 10.1002/path. 4643.
76. Elsayed FA, Kets CM, Ruano D et al. Germline variants in POLE are associated with early onset mismatch repair deficient colorectal cancer. Eur J Hum Genet 2015; 23 (8): 1080–1084. doi: 10.1038/ejhg.2014.242.
77. Jansen AM, van Wezel T, van den Akker BE et al. Combined mismatch repair and POLE/POLD1 defects explain unresolved suspected Lynch syndrome cancers. Eur J Hum Genet 2016; 24 (7): 1089–1092. doi: 10.1038/ejhg.2015.252.
78. Weedon MN, Ellard S, Prindle MJ et al. An in-frame deletion at the polymerase active site of POLD1 causes a multisystem disorder with lipodystrophy. Nat Genet 2013; 45: 947–950. doi: 10.1038/ng.2670.
79. Sasaki H, Yanagi K, Ugi S et al. Definitive diagnosis of mandibular hypoplasia, deafness, progeroid features and lipodystrophy (MDPL) syndrome caused by a recurrent de novo mutation in the POLD1 gene. Endocr J 2018; 65 (2): 227–238. doi: 10.1507/endocrj.EJ17-0287.
80. Beggs AD, Latchford AR, Vasen HF et al. Peutz-Jeghers syndrome: a systematic review and recommendations for management. Gut 2010; 59 (7): 975–986. doi: 10.1136/gut.2009.198499.
81. van Lier MG, Wagner A, Mathus-Vliegen EM. High cancer risk in Peutz-Jeghers syndrome: a systematic review and surveillance recommendations. Am J Gastroenterol 2010; 105 (6): 1258–1264. doi: 10.1038/ajg.2009.725.
82. Tse JY, Wu S, Shinagare SA et al. Peutz-Jeghers syndrome: a critical look at slonic Peutz-Jeghers polyps. Mod Pathol 2013; 26 (9): 1235–1240. doi: 10.1038/modpathol.2013.44.
83. Lam-Himlin D, Park JY, Cornish TC et al. Morphologic characterization of syndromic gastric polyps. Am J Surg Pathol 2010; 34 (11): 1656–1662. doi: 10.1097/PAS.0b013e3181f2b1f1.
84. Orpha.net. French National Institute for Health and Medical Research. c1977–2019. [online]. Available from: https: //www.orpha.net/consor/cgi-bin/index.php.
85. Borowsky J, Setia N, Lauwers G et al. Gastrointestinal tract pathology in PTEN Hamartoma tumour syndrome: a review of 43 cases. Mod Pathol 2015; 28 (Suppl 2): 149A.
86. Agarwal R, Liebe S, Turski ML et al. Targeted therapy for genetic cancer syndromes: Von Hippel-Lindau disease, Cowden syndrome, and Proteus syndrome. Discov Med 2015; 19 (103): 109–116.
87. Ma H, Brosensi LA, Offerhausi GJ et al. Pathology and genetics of hereditary colorectal cancer. Pathology 2018; 50 (1): 49–59. doi: 10.1016/j.pathol.2017.09.004.
88. Brosens LA, van Hattem A, Hylind LM et al. Risk of colorectal cancer in juvenilie polyposis. Gut 2007; 56 (7): 965–967. doi: 10.1136/gut.2006.116913.
89. Howe JR, Mitros FA, Summers RW. The risk of gastrointestinal carcinoma in familial juvenile polyposis. Ann Surg Oncol 1998; 5 (8): 751–756.
90. Schreibman IR, Baker M, Amos C et al. The hamartomatous polyposis syndromes: a clinical and molecular review. Am J Gastroenterol 2005; 100 (2): 476–490. doi: 10.1111/j.1572-0241.2005.40237.x.
91. van Hattem WA, Langeveld D, de Leng WW et al. Histologic variations in juvenilie polyp phenotype correlate with genetic defect underlying juvenile polyposis. Am J Surg Pathol 2011; 35 (4): 530–536. doi: 10.1097/PAS.0b013e318211cae1.
92. Brosens LA, Langeveld D, van Hattem WA et al. Juvenile polyposis syndrome. World J Gastroenterol 2011; 17 (44): 4839–4844. doi: 10.3748/wjg.v17.i44.4839.
93. van Hattem WA, Brosens LA, de Leng WW et al. Large genomic deletions of SMAD4, BMPR1A and PTEN in juvenile polyposis. Gut 2008; 57 (5): 623–627. doi: 10.1136/gut.2007.142927.
94. Massague J. TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 1996; 85 (7): 947–950.
95. Calva-Cerqueira D, Dahdaleh FS, Woodfield G et al. Discovery of the BMPR1A promoter and germline mutations that cause juvenile polyposis. Hum Mol Genet 2010; 19 (23): 4654–4662. doi: 10.1093/hmg/ddq 396.
96. Rodriguez-Moranta F, Rodriguez-Alonso L, Guardiola Capon J. Serrated polyposis syndrome. Cir Esp 2014; 92 (10): 643–644. doi: 10.1016/j.ciresp.2014.03.003.
97. Edelstein DL, Cruz-Correa M, Soto-Salgado M et al. Risk of colorectal and other cancers in patients with serrated polyposis. Clin Gastroenterol Hepatol 2015; 13 (9): 1697–1699. doi: 10.1016/j.cgh.2015.02.003.
98. Boparai KS, Mathus-Vliegen EM, Koornstra JJ et al. Increased colorectal cancer risk during follow-up in patients with hyperplastic polyposis syndrome: a multicentre cohort study. Gut 2010; 59 (8): 1094–1100. doi: 10.1136/gut.2009.185884.
99. Rosty C, Walsh MD, Walters RJ et al. Multiplicity and molecular heterogeneity of colorectal carcinomas in individuals with serrated polyposis. Am J Surg Pathol 2013; 37 (3): 434–442. doi: 10.1097/PAS.0b013e318270f748.
100. Crowder CD, Sweet K, Lehman A et al. Serrated polyposis is an underdiagnosed and unclear syndrome: the surgical pathologist has a role in improving detection. Am J Surg Pathol 2012; 36 (8): 1178–1185. doi: 10.1097/PAS.0b013e3182597f41.
101. Rosty C, Parry S, Young JP. Serrated polyposis: an enigmatic model of colorectal cancer predisposition. Patholog Res Int 2011; 2011: 157073. doi: 10.4061/2011/157073.
102. Anderson JC. Pathogenesis and management of serrated polyps: current status and future directions. Gut Liver 2014; 8 (6): 582–589. doi: 10.5009/gnl14248.
103. IJspeert JE, Bossuyt PM, Kuipers EJ et al. Smoking status informs about the risk of advanced serrated polyps in a screening population. Endosc Int Open 2016; 4 (1): E73–E78. doi: 10.1055/s-0034-1393361.
104. Valle L. Recent discoveries in the genetics of familial colorectal cancer and polyposis. Clin Gastroenterol Hepatol 2017; 15 (5): 809–819. doi: 10.1016/j.cgh.2016.09.148.
105. Gala MK, Mizukami Y, Le LP et al. Germline mutations in oncogene induced senescence pathways are associated with multiple sessile serrated adenomas. Gastroenterology 2014; 146 (2): 520–529. doi: 10.1053/j.gastro.2013.10.045.
106. Omim.org. McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine. c1966–2019. [online]. Available from: https: //www.omim.org.
107. Buchanan DD, Clendenning M, Zhuoer L et al. Lack of evidence for germline RNF43 mutations in patients with serrated polyposis syndrome from a large multinational study. Gut 2017; 66 (6): 1170–1172. doi: 10.1136/gutjnl-2016-312773.
108. Snover DC, Ahnen DJ, Burt RW et al. Serrated polyps of the colon and rectum and serrated polyposis. In: Bosman FT, Carneiro F, Hruban RH, Theise ND (eds). WHO classification of tumours of the digestive system. Lyon: IARC Press 2010: 160–165.
109. You YN, Borras E, Chang K et al. Detection of pathogenic germline variants among patients with advanced colorectal cancerundergoing tumor genomic profiling for precision medicine. Dis Colon Rectum 2019; 62 (4): 429–437. doi: 10.1097/DCR.0000000000001322.
110. Agaimy A, Schaefer IM, Kotzina L et al. Juvenile-like (inflammatory/hyperplastic) mucosal polyps of the gastrointestinal tract in neurofibromatosis type 1. Histopathology 2014; 64 (6): 777–786. doi: 10.1111/his.12325.
111. Brosens LA, Offerhaus GJ, Canto MI et al. Simultaneous juvenile polyposis syndrome and neurofibromatosis type 1. Histopathology 2016; 68 (2): 313–315. doi: 10.1111/his.12734.
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