A revised classification system and recommendations from the Baltimore consensus meeting for neoplastic precursor lesions in the pancreas

American Journal of Surgical Pathology

Volumn 39, Issue 12, 2015, Pages 1730-1741

  Basturk, Olca ^a   Hong, Seung Mo ^e   Wood, Laura D ^b   Adsay, N Volkan ^c   Albores Saavedra, Jorge ^f   Biankin, Andrew V ^g   Brosens, Lodewijk A A ^h   Fukushima, Noriyoshi ⁱ   Goggins, Michael ^b   Hruban, Ralph H ^b   Kato, Yo ^j   Klimstra, David S ^a   Klöppel, Günter ^m   Krasinskas, Alyssa ^c   Longnecker, Daniel S ^d   Matthaei, Hanno ⁿ   Offerhaus, G Johan A ^h   Shimizu, Michio ^k   Takaori, Kyoichi ^l   Terris, Benoit ^p   Yachida, Shinichi ^k   Esposito, Irene ^o   Furukawa, Toru ^k   more..

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c EMORY UNIVERSITY HOSPITAL   (United States)

^d DARTMOUTH HITCHCOCK MEDICAL CENTER   (United States)

^e University of Ulsan   (South Korea)

^f LIVER RESEARCH UNIT   (Mexico)

^g UNIVERSITY OF GLASGOW   (United Kingdom)

^h UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

ⁱ JICHI MEDICAL UNIVERSITY   (Japan)

^j CANCER INSTITUTE   (Japan)

^k TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^l KYOTO UNIVERSITY   (Japan)

^m TECHNICAL UNIVERSITY OF MUNICH   (Germany)

ⁿ UNIVERSITY OF BONN   (Germany)

^o UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^p Hôpital Cochin ^*  (France)

more..

Author keywords

adenocarcinoma; atypical flat lesions (AFL); intraductal papillary mucinous neoplasm (IPMN); mucinous cystic neoplasm (MCN); pancreatic intraepithelial neoplasia (PanIN); precursor

Indexed keywords

BIOPSY; CANCER GRADING; CARCINOMA IN SITU; CHEMISTRY; CLASSIFICATION; CONSENSUS; CONSENSUS DEVELOPMENT; COOPERATION; HUMAN; INTERNATIONAL COOPERATION; NEOPLASM; NOMENCLATURE; PANCREAS CARCINOMA; PANCREAS TUMOR; PATHOLOGY; PRECANCER; PREDICTIVE VALUE; TUMOR INVASION; TUMOR VOLUME;

BIOPSY; CARCINOMA IN SITU; CARCINOMA, PANCREATIC DUCTAL; CONSENSUS; COOPERATIVE BEHAVIOR; HUMANS; INTERNATIONAL COOPERATION; NEOPLASM GRADING; NEOPLASM INVASIVENESS; NEOPLASMS, CYSTIC, MUCINOUS, AND SEROUS; PANCREATIC NEOPLASMS; PRECANCEROUS CONDITIONS; PREDICTIVE VALUE OF TESTS; TERMINOLOGY AS TOPIC; TUMOR BURDEN;

EID: 84948695938     PISSN: 01475185     EISSN: 15320979     Source Type: Journal    
DOI: 10.1097/PAS.0000000000000533     Document Type: Conference Paper

References (114)

1. Hruban RH, Adsay NV, Albores-Saavedra J, et al. Pancreatic intraepithelial neoplasia: a new nomenclature and classification system for pancreatic duct lesions. Am J Surg Pathol. 2001; 25: 579-586
2. Hruban RH, Takaori K, Klimstra DS, et al. An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillary mucinous neoplasms. Am J Surg Pathol. 2004; 28: 977-987
3. Hruban RH, Pitman MB, Klimstra DS. Tumors of the Pancreas. Washington, DC: American Registry of Pathology
4. Adsay NV, Fukushima N, Furukawa T, et al. Intraductal neoplasms of the pancreas. In: Bosman FT, Hruban RH, Carneiro F, et al, eds. WHO Classification of Tumours of the Digestive System. Lyon: IARC; 2010: 304-313
5. Hruban RH, Adsay NV, Albores-Saavedra J, et al. Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations. Cancer Res. 2006; 66: 95-106
6. Wada K. p16 and p53 gene alterations and accumulations in the malignant evolution of intraductal papillary-mucinous tumors of the pancreas. J Hepatobiliary Pancreat Surg. 2002; 9: 76-85
7. Fujii H, Inagaki M, Kasai S, et al. Genetic progression and heterogeneity in intraductal papillary-mucinous neoplasms of the pancreas. Am J Pathol. 1997; 151: 1447-1454
8. Mueller J, Gansauge S, Mattfeldt T. P53 mutation but not p16/MTS1 mutation occurs in intraductal papillary mucinous tumors of the pancreas. Hepatogastroenterology. 2003; 50: 541-544
9. Fukushima N, Sato N, Ueki T, et al. Aberrant methylation of preproenkephalin and p16 genes in pancreatic intraepithelial neoplasia and pancreatic ductal adenocarcinoma. Am J Pathol. 2002; 160: 1573-1581
10. Lohr M, Kloppel G, Maisonneuve P, et al. Frequency of K-ras mutations in pancreatic intraductal neoplasias associated with pancreatic ductal adenocarcinoma and chronic pancreatitis: a meta-Analysis. Neoplasia. 2005; 7: 17-23
11. Seki M, Ninomiya E, Hayashi K, et al. Widespread and multifocal carcinomas in situ (CISs) through almost the entire pancreas: report of a case with preoperative cytological diagnosis. Langenbecks Arch Surg. 2010; 395: 589-592
12. Kawada N, Uehara H, Takada R, et al. Microinvasion of highgrade pancreatic intraepithelial neoplasia. Case Rep Gastroenterol. 2013; 7: 30-36
13. Konstantinidis IT, Vinuela EF, Tang LH, et al. Incidentally discovered pancreatic intraepithelial neoplasia: what is its clinical significance?. Ann Surg Oncol. 2013; 20: 3643-3647
14. Lami G, Biagini MR, Galli A. Endoscopic ultrasonography for surveillance of individuals at high risk for pancreatic cancer. World J Gastrointest Endosc. 2014; 6: 272-285
15. LeBlanc JK, Chen JH, Al-Haddad M, et al. Can endoscopic ultrasound predict pancreatic intraepithelial neoplasia lesions in chronic pancreatitis?: a retrospective study of pathologic correlation. Pancreas. 2014; 43: 849-854
16. Ito H, Kawaguchi Y, Kawashima Y, et al. A case of pancreatic intraepithelial neoplasia that was difficult to diagnose preoperatively. Case Rep Oncol. 2015; 8: 30-36
17. Matsuda Y, Ishiwata T, Izumiyama-Shimomura N, et al. Gradual telomere shortening and increasing chromosomal instability among PanIN grades and normal ductal epithelia with and without cancer in the pancreas. PLoS One. 2015; 10: e0117575
18. Rebours V, Gaujoux S, d'Assignies G, et al. Obesity and fatty pancreatic infiltration are risk factors for pancreatic precancerous lesions (PanIN). Clin Cancer Res. 2015; 21: 3522-3528
19. Bartsch DK, Dietzel K, Bargello M, et al. Multiple small imaging branch-duct type intraductal papillary mucinous neoplasms (IPMNs) in familial pancreatic cancer: indicator for concomitant high grade pancreatic intraepithelial neoplasia?. Fam Cancer. 2013; 12: 89-96
20. Fritz S, Fernandez-del Castillo C, Mino-Kenudson M, et al. Global genomic analysis of intraductal papillary mucinous neoplasms of the pancreas reveals significant molecular differences compared to ductal adenocarcinoma. Ann Surg. 2009; 249: 440-447
21. Jones S, Zhang X, Parsons DW, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science. 2008; 321: 1801-1806
22. Wu J, Jiao Y, Dal Molin M, et al. Whole-exome sequencing of neoplastic cysts of the pancreas reveals recurrent mutations in components of ubiquitin-dependent pathways. Proc Natl Acad Sci USA. 2011; 108: 21188-21193
23. Furukawa T, Kuboki Y, Tanji E, et al. Whole-exome sequencing uncovers frequent GNAS mutations in intraductal papillary mucinous neoplasms of the pancreas. Sci Rep. 2011; 1: 161
24. Yachida S, Vakiani E, White CM, et al. Small cell and large cell neuroendocrine carcinomas of the pancreas are genetically similar and distinct from well-differentiated pancreatic neuroendocrine tumors. Am J Surg Pathol. 2012; 36: 173-184
25. Jiao Y, Yonescu R, Offerhaus GJ, et al. Whole-exome sequencing of pancreatic neoplasms with acinar differentiation. J Pathol. 2014; 232: 428-435
26. Park M, Kim M, Hwang D, et al. Characterization of gene expression and activated signaling pathways in solid-pseudopapillary neoplasm of pancreas. Mod Pathol. 2014; 27: 580-593
27. Furlan D, Sahnane N, Bernasconi B, et al. APC alterations are frequently involved in the pathogenesis of acinar cell carcinoma of the pancreas, mainly through gene loss and promoter hypermethylation. Virchows Arch. 2014; 464: 553-564
28. Garcia-Carracedo D, Chen ZM, Qiu W, et al. PIK3CA mutations in mucinous cystic neoplasms of the pancreas. Pancreas. 2014; 43: 245-249
29. Tanaka M, Fernandez-del Castillo C, Adsay V, et al. International consensus guidelines 2012 for the management of IPMN and MCN of the pancreas. Pancreatology. 2012; 12: 183-197
30. Matthaei H, Hong SM, Mayo SC, et al. Presence of pancreatic intraepithelial neoplasia in the pancreatic transection margin does not influence outcome in patients with R0 resected pancreatic cancer. Ann Surg Oncol. 2011; 18: 3493-3499
31. Andea A, Sarkar F, Adsay VN. Clinicopathological correlates of pancreatic intraepithelial neoplasia: a comparative analysis of 82 cases with and 152 cases without pancreatic ductal adenocarcinoma. Mod Pathol. 2003; 16: 996-1006
32. Winter JM, Cameron JL, Lillemoe KD, et al. Periampullary and pancreatic incidentaloma: a single institution's experience with an increasingly common diagnosis. Ann Surg. 2006; 243: 673-680
33. Laffan TA, Horton KM, Klein AP, et al. Prevalence of unsuspected pancreatic cysts on MDCT. Am J Roentgenol. 2008; 191: 802-807
34. Kent TS, Jr CM, Callery MP. Intraductal papillary mucinous neoplasm and the pancreatic incidentaloma. World J Gastrointest Surg. 2010; 2: 319-323
35. Abraham SC, Wilentz RE, Yeo CJ, et al. Pancreaticoduodenectomy (Whipple resections) in patients without malignancy: are they all'chronic pancreatitis'?. Am J Surg Pathol. 2003; 27: 110-120
36. Allen PJ, D'Angelica M, Gonen M, et al. A selective approach to the resection of cystic lesions of the pancreas: results from 539 consecutive patients. Ann Surg. 2006; 244: 572-582
37. Furukawa T, Kloppel G, Volkan Adsay N, et al. Classification of types of intraductal papillary-mucinous neoplasm of the pancreas: a consensus study. Virchows Arch. 2005; 447: 794-799
38. Adsay V, Mino-Kenudson M, Furukawa T, et al. Pathologic evaluation and reporting of intraductal papillary mucinous neoplasms of the pancreas and other tumoral intraepithelial neoplasms of pancreatobiliary tract: recommendations of Verona Consensus Meeting. Ann Surg. 2015. [Epub ahead of print]
39. Ammori JB, Do RK, Brennan MF, et al. Uncinate duct dilation in intraductal papillary mucinous neoplasms of the pancreas: a radiographic finding with potentially increased malignant potential. J Gastrointest Surg. 2014; 18: 911-916
40. Shimizu Y, Yamaue H, Maguchi H, et al. Predictors of malignancy in intraductal papillary mucinous neoplasm of the pancreas: analysis of 310 pancreatic resection patients at multiple highvolume centers. Pancreas. 2013; 42: 883-888
41. Ohno E, Itoh A, Kawashima H, et al. Malignant transformation of branch duct-Type intraductal papillary mucinous neoplasms of the pancreas based on contrast-enhanced endoscopic ultrasonography morphological changes: focus on malignant transformation of intraductal papillary mucinous neoplasm itself. Pancreas. 2012; 41: 855-862
42. Hwang DW, Jang JY, Lim CS, et al. Determination of malignant and invasive predictors in branch duct type intraductal papillary mucinous neoplasms of the pancreas: a suggested scoring formula. J Korean Med Sci. 2011; 26: 740-746
43. Tomimaru Y, Takeda Y, Tatsumi M, et al. Utility of 2-[18F] fluoro-2-deoxy-D-glucose positron emission tomography in differential diagnosis of benign and malignant intraductal papillarymucinous neoplasm of the pancreas. Oncol Rep. 2010; 24: 613-620
44. Mimura T, Masuda A, Matsumoto I, et al. Predictors of malignant intraductal papillary mucinous neoplasm of the pancreas. J Clin Gastroenterol. 2010; 44: e224-e229
45. Shimamoto T, Tani M, Kawai M, et al. MUC1 is a useful molecular marker for malignant intraductal papillary mucinous neoplasms in pancreatic juice obtained from endoscopic retrograde pancreatography. Pancreas. 2010; 39: 879-883
46. Bausch D, Mino-Kenudson M, Fernandez-Del Castillo C, et al. Plectin-1 is a biomarker of malignant pancreatic intraductal papillary mucinous neoplasms. J Gastrointest Surg. 2009; 13: 1948-1954
47. Le H, Ziogas A, Rhee JM, et al. A population-based, descriptive analysis of malignant intraductal papillary mucinous neoplasms of the pancreas. Cancer Epidemiol Biomarkers Prev. 2008; 17: 2737-2741
48. Cone MM, Rea JD, Diggs BS, et al. Predicting malignant intra ductal papillary mucinous neoplasm: a single-center review. Am J Surg. 2011; 201: 575-579
49. Fritz S, Hackert T, Hinz U, et al. Role of serum carbohydrate antigen 19-9 and carcinoembryonic antigen in distinguishing between benign and invasive intraductal papillary mucinous neoplasm of the pancreas. Br J Surg. 2011; 98: 104-110
50. Simons JP, Ng SC, Shah SA, et al. Malignant intraductal papillary mucinous neoplasm: are we doing the right thing?. J Surg Res. 2011; 167: 251-257
51. Lee CJ, Scheiman J, Anderson MA, et al. Risk of malignancy in resected cystic tumors of the pancreas or=3 cm in size: is it safe to observe asymptomatic patients?. A multi-institutional report. J Gastrointest Surg. 2008; 12: 234-242
52. Kawamoto S, Horton KM, Lawler LP, et al. Intraductal papillary mucinous neoplasm of the pancreas: can benign lesions be differentiated from malignant lesions with multidetector CT?. Radiographics. 2005; 25: 1451-1468
53. Manfredi R, Graziani R, Motton M, et al. Main pancreatic duct intraductal papillary mucinous neoplasms: accuracy of MR imaging in differentiation between benign and malignant tumors compared with histopathologic analysis. Radiology. 2009; 253: 106-115
54. Klöppel G, Bommer G, Ruckert K, et al. Intraductal proliferation in the pancreas and its relationship to human and experimental carcinogenesis. Virchows Arch A Pathol Anat Histol. 1980; 387: 221-233
55. Pour PM, Sayed S, Sayed G. Hyperplastic preneoplastic and neoplastic lesions found in 83 human pancreases. Am J Clin Pathol. 1982; 77: 137-152
56. Detlefsen S, Sipos B, Feyerabend B, et al. Pancreatic fibrosis associated with age and ductal papillary hyperplasia. Virchows Arch. 2005; 447: 800-805
57. Ito R, Kondo F, Yamaguchi T, et al. Pancreatic intraepithelial neoplasms in the normal appearing pancreas: on their precise relationship with age. Hepatogastroenterology. 2008; 55: 1103-1106
58. Hruban RH, Klimstra DS. Adenocarcinoma of the pancreas. Semin Diagn Pathol. 2014; 31: 443-451
59. Brat DJ, Lillemoe KD, Yeo CJ, et al. Progression of pancreatic intraductal neoplasias to infiltrating adenocarcinoma of the pancreas. Am J Surg Pathol. 1998; 22: 163-169
60. McCarthy DM, Brat DJ, Wilentz RE, et al. Pancreatic intraepithelial neoplasia and infiltrating adenocarcinoma: analysis of progression and recurrence by DPC4 immunohistochemical labeling. Hum Pathol. 2001; 32: 638-642
61. Fujii T, Kato K, Kodera Y, et al. Prognostic impact of pancreatic margin status in the intraductal papillary mucinous neoplasms of the pancreas. Surgery. 2010; 148: 285-290
62. Nakagohri T, Kinoshita T, Konishi M, et al. Surgical outcome of intraductal papillary mucinous neoplasms of the pancreas. Ann Surg Oncol. 2007; 14: 3174-3180
63. Raut CP, Cleary KR, Staerkel GA, et al. Intraductal papillary mucinous neoplasms of the pancreas: effect of invasion and pancreatic margin status on recurrence and survival. Ann Surg Oncol. 2006; 13: 582-594
64. Leng KM, Wang ZD, Zhao JB, et al. Impact of pancreatic margin status and lymph node metastases on recurrence after resection for invasive and noninvasive intraductal papillary mucinous neoplasms of the pancreas: a meta-Analysis. Dig Surg. 2012; 29: 213-225
65. Frankel TL, LaFemina J, Bamboat ZM, et al. Dysplasia at the surgical margin is associated with recurrence after resection of non-invasive intraductal papillary mucinous neoplasms. HPB (Oxford). 2013; 15: 814-821
66. White R, D'Angelica M, Katabi N, et al. Fate of the remnant pancreas after resection of noninvasive intraductal papillary mucinous neoplasm. J Am Coll Surg. 2007; 204: 987-993. discussion 993-985
67. Kang MJ, Jang JY, Lee KB, et al. Long-Term prospective cohort study of patients undergoing pancreatectomy for intraductal papillary mucinous neoplasm of the pancreas: implications for postoperative surveillance. Ann Surg. 2014; 260: 356-363
68. Dejean NM, Dumitra S, Barkun JS. Recurrence of non-invasive intraductal papillary municious neoplasm seven years following total pancreatectomy. Int J Surg Case Rep. 2013; 4: 789-791
69. Tanno S, Nakano Y, Sugiyama Y, et al. Incidence of synchronous and metachronous pancreatic carcinoma in 168 patients with branch duct intraductal papillary mucinous neoplasm. Pancreatology. 2010; 10: 173-178
70. Eguchi H, Ishikawa O, Ohigashi H, et al. Role of intraoperative cytology combined with histology in detecting continuous and skip type intraductal cancer existence for intraductal papillary mucinous carcinoma of the pancreas. Cancer. 2006; 107: 2567-2575
71. Cioc AM, Ellison EC, Proca DM, et al. Frozen section diagnosis of pancreatic lesions. Arch Pathol Lab Med. 2002; 126: 1169-1173
72. Gigot JF, Deprez P, Sempoux C, et al. Surgical management of intraductal papillary mucinous tumors of the pancreas: the role of routine frozen section of the surgical margin, intraoperative endoscopic staged biopsies of the Wirsung duct, and pancreaticogastric anastomosis. Arch Surg. 2001; 136: 1256-1262
73. Nakanuma Y, Curado M-P, Franceschi S, et al. Intrahepatic cholangiocarcinoma. In: Bosman FT, Hruban RH, Carneiro F, et al, eds. WHO Classification of Tumours of the Digestive System. Lyon: IARC 2010 217-224
74. Wu J, Matthaei H, Maitra A, et al. Recurrent GNAS mutations define an unexpected pathway for pancreatic cyst development. Sci Transl Med. 2011; 3: 92ra66
75. Kanda M, Matthaei H, Wu J, et al. Presence of somatic mutations in most early-stage pancreatic intraepithelial neoplasia. Gastroenterology. 2012; 142: 730-733. e739
76. Matthaei H, Wu J, Dal Molin M, et al. GNAS sequencing identifies IPMN-specific mutations in a subgroup of diminutive pancreatic cysts referred to as incipient IPMNs. Am J Surg Pathol. 2014; 38: 360-363
77. Yamaguchi K, Ohuchida J, Ohtsuka T, et al. Intraductal papillarymucinous tumor of the pancreas concomitant with ductal carcinoma of the pancreas. Pancreatology. 2002; 2: 484-490
78. Yamaguchi K, Kanemitsu S, Hatori T, et al. Pancreatic ductal adenocarcinoma derived from IPMN and pancreatic ductal adenocarcinoma concomitant with IPMN. Pancreas. 2011; 40: 571-580
79. Ideno N, Ohtsuka T, Kono H, et al. Intraductal papillary mucinous neoplasms of the pancreas with distinct pancreatic ductal adenocarcinomas are frequently of gastric subtype. Ann Surg. 2013; 258: 141-151
80. Yamasaki S, Suda K, Nobukawa B, et al. Intraductal spread of pancreatic cancer. Clinicopathologic study of 54 pancreatectomized patients. Pancreatology. 2002; 2: 407-412
81. Kosmahl M, Egawa N, Schroder S, et al. Mucinous nonneoplastic cyst of the pancreas: a novel nonneoplastic cystic change?. Mod Pathol. 2002; 15: 154-158
82. Krasinskas A, Oakley GJ, Bagci P, et al. Cystic mucinous duct lesion of the pancreas: a clinicopathologic analysis of 40 examples of a diagnostically challenging and terminologically controversial entity. Mod Pathol. 2012; 25: 445A
83. Murtaugh LC, Leach SD. A case of mistaken identity?. Nonductal origins of pancreatic ductal cancers. Cancer Cell. 2007; 11: 211-213
84. Willemer S, Adler G. Histochemical and ultrastructural characteristics of tubular complexes in human acute pancreatitis. Dig Dis Sci. 1989; 34: 46-55
85. Bockman DE, Guo J, Buchler P, et al. Origin and development of the precursor lesions in experimental pancreatic cancer in rats. Lab Invest. 2003; 83: 853-859
86. Shi G, DiRenzo D, Qu C, et al. Maintenance of acinar cell organization is critical to preventing Kras-induced acinar-ductal metaplasia. Oncogene. 2013; 32: 1950-1958
87. De La OJ, Emerson LL, Goodman JL, et al. Notch and Kras reprogram pancreatic acinar cells to ductal intraepithelial neoplasia. Proc Natl Acad Sci USA. 2008; 105: 18907-18912
88. Guerra C, Schuhmacher AJ, Canamero M, et al. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell. 2007; 11: 291-302
89. Habbe N, Shi G, Meguid RA, et al. Spontaneous induction of murine pancreatic intraepithelial neoplasia (mPanIN) by acinar cell targeting of oncogenic Kras in adult mice. Proc Natl Acad Sci USA. 2008; 105: 18913-18918
90. Ray KC, Bell KM, Yan J, et al. Epithelial tissues have varying degrees of susceptibility to Kras(G12D)-initiated tumorigenesis in a mouse model. PLoS One. 2011; 6: e16786
91. Kopp JL, von Figura G, Mayes E, et al. Identification of Sox9-dependent acinar-To-ductal reprogramming as the principal mechanism for initiation of pancreatic ductal adenocarcinoma. Cancer Cell. 2012; 22: 737-750
92. Bockman DE, Boydston WR, Anderson MC. Origin of tubular complexes in human chronic pancreatitis. Am J Surg. 1982; 144: 243-249
93. Parsa I, Longnecker DS, Scarpelli DG, et al. Ductal metaplasia of human exocrine pancreas and its association with carcinoma. Cancer Res. 1985; 45: 1285-1290
94. Esposito I, Seiler C, Bergmann F, et al. Hypothetical progression model of pancreatic cancer with origin in the centroacinar-Acinar compartment. Pancreas. 2007; 35: 212-217
95. Shi C, Hong SM, Lim P, et al. KRAS2 mutations in human pancreatic acinar-ductal metaplastic lesions are limited to those with PanIN: implications for the human pancreatic cancer cell of origin. Mol Cancer Res. 2009; 7: 230-236
96. Brune K, Abe T, Canto M, et al. Multifocal neoplastic precursor lesions associated with lobular atrophy of the pancreas in patients having a strong family history of pancreatic cancer. Am J Surg Pathol. 2006; 30: 1067-1076
97. Aichler M, Seiler C, Tost M, et al. Origin of pancreatic ductal adenocarcinoma from atypical flat lesions: a comparative study in transgenic mice and human tissues. J Pathol. 2012; 226: 723-734
98. Konukiewitz B, Schlitter AM, Berchtold S, et al. Characterization of putative precursor lesions of familial pancreatic cancer. Pancreatology. 2013; 13: S14
99. Akita H, Takeda Y, Hoshino H, et al. Mural nodule in branch duct-Type intraductal papillary mucinous neoplasms of the pancreas is a marker of malignant transformation and indication for surgery. Am J Surg. 2011; 202: 214-219
100. Salvia R, Fernandez-del Castillo C, Bassi C, et al. Main-duct intraductal papillary mucinous neoplasms of the pancreas: clinical predictors of malignancy and long-Term survival following resection. Ann Surg. 2004; 239: 678-685
101. Sugiyama M, Izumisato Y, Abe N, et al. Predictive factors for malignancy in intraductal papillary-mucinous tumours of the pancreas. Br J Surg. 2003; 90: 1244-1249
102. Terris B, Ponsot P, Paye F, et al. Intraductal papillary mucinous tumors of the pancreas confined to secondary ducts show less aggressive pathologic features as compared with those involving the main pancreatic duct. Am J Surg Pathol. 2000; 24: 1372-1377
103. Irie H, Yoshimitsu K, Aibe H, et al. Natural history of pancreatic intraductal papillary mucinous tumor of branch duct type: follow-up study by magnetic resonance cholangiopancreatography. J Comput Assist Tomogr. 2004; 28: 117-122
104. Sadakari Y, Ienaga J, Kobayashi K, et al. Cyst size indicates malignant transformation in branch duct intraductal papillary mucinous neoplasm of the pancreas without mural nodules. Pancreas. 2010; 39: 232-236
105. Maguchi H, Tanno S, Mizuno N, et al. Natural history of branch duct intraductal papillary mucinous neoplasms of the pancreas: a multicenter study in Japan. Pancreas. 2011; 40: 364-370
106. Salvia R, Crippa S, Falconi M, et al. Branch-duct intraductal papillary mucinous neoplasms of the pancreas: to operate or not to operate?. Gut. 2007; 56: 1086-1090
107. Tanno S, Nakano Y, Nishikawa T, et al. Natural history of branch duct intraductal papillary-mucinous neoplasms of the pancreas without mural nodules: long-Term follow-up results. Gut. 2008; 57: 339-343
108. Reid BJ, Haggitt RC, Rubin CE, et al. Observer variation in the diagnosis of dysplasia in Barrett's esophagus. Hum Pathol. 1988; 19: 166-178
109. Fenger C, Bak M, Kronborg O, et al. Observer reproducibility in grading dysplasia in colorectal adenomas: comparison between two different grading systems. J Clin Pathol. 1990; 43: 320-324
110. Jensen P, Krogsgaard MR, Christiansen J, et al. Observer variability in the assessment of type and dysplasia of colorectal adenomas, analyzed using kappa statistics. Dis Colon Rectum. 1995; 38: 195-198
111. Epstein JI, Grignon DJ, Humphrey PA, et al. Interobserver reproducibility in the diagnosis of prostatic intraepithelial neoplasia. Am J Surg Pathol. 1995; 19: 873-886
112. Waxman AG, Chelmow D, Darragh TM, et al. Revised terminology for cervical histopathology and its implications for management of high-grade squamous intraepithelial lesions of the cervix. Obstet Gynecol. 2012; 120: 1465-1471
113. Darragh TM, Colgan TJ, Thomas Cox J, et al. The Lower Anogenital Squamous Terminology Standardization project for HPV-Associated lesions: background and consensus recommendations from the College of American Pathologists and the American Society for Colposcopy and Cervical Pathology. Int J Gynecol Pathol. 2013; 32: 76-115
114. Furukawa T, Chiba R, Kobari M, et al. Varying grades of epithelial atypia in the pancreatic ducts of humans. Classification based on morphometry and multivariate analysis and correlated with positive reactions of carcinoembryonic antigen. Arch Pathol Lab Med. 1994; 118: 227-234.