Precursor lesions of pancreatic cancer: Molecular pathology and clinical implications

Pancreatology

Volumn 7, Issue 1, 2007, Pages 9-19

  Singh, Mansher ^a   Maitra, Anirban ^a  

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

Author keywords

Intraductal papillary mucinous neoplasm; Mucinous cystic neoplasm; Pancreatic cancer, precursor lesions; Pancreatic intraepithelial neoplasia

Indexed keywords

MUCIN; PROTEIN P53;

ALGORITHM; ASPIRATION BIOPSY; CANCER GENETICS; CANCER GROWTH; CANCER RISK; CANCER SURVIVAL; DIAGNOSTIC ACCURACY; DIAGNOSTIC IMAGING; ENDOSCOPIC RETROGRADE CHOLANGIOPANCREATOGRAPHY; FAMILIAL CANCER; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HIGH RISK PATIENT; HISTOLOGY; HUMAN; INVASIVE CARCINOMA; MEDICAL LITERATURE; ONCOGENE K RAS; PANCREAS ADENOCARCINOMA; PANCREAS CYST; PANCREAS INTRADUCTAL PAPILLARY MUCINOUS NEOPLASIA; PANCREAS INTRAEPITHELIAL NEOPLASIA; PANCREAS MUCINOUS CYSTIC NEOPLASIA; PANCREATOGRAPHY; PATHOLOGY; PRECANCER; PRIORITY JOURNAL; PROGNOSIS; REVIEW; SENSITIVITY AND SPECIFICITY;

EID: 34248204213     PISSN: 14243903     EISSN: 14243911     Source Type: Journal    
DOI: 10.1159/000101873     Document Type: Article

References (100)

1. Yeo TP, Hruban RH, Leach SD, Wilentz RE, Sohn TA, Kern SE, Iacobuzio-Donahue CA, Maitra A, Goggins M, Canto MI, Abrams RA, Laheru D, Jaffee EM, Hidalgo M, Yeo CJ: Pancreatic cancer. Curr Probl Cancer 2002;26:176-275.
2. Li D, Xie K, Wolff R, Abbruzzese JL: Pancreatic cancer. Lancet 2004;363:1049-1057.
3. Sohn TA, Yeo CJ, Cameron JL, Koniaris L, Kaushal S, Abrams RA, Sauter PK, Coleman J, Hruban RH, Lillemoe KD: Resected adenocarcinoma of the pancreas - 616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg 2000;4:567-579.
4. Pisters PW, Wolff RA, Crane CH, Evans DB: Combined-modality treatment for operable pancreatic adenocarcinoma. Oncology (Williston Park) 2005;19:393-404, 409; discussion 409-410, 412-416.
5. Canto MI, Goggins M, Hruban RH, Petersen GM, Giardiello FM, Yeo C, Fishman EK, Brune K, Axilbund J, Griffin C, Ali S, Richman J, Jagannath S, Kantsevoy SV, Kalloo AN: Screening for early pancreatic neoplasia in high-risk individuals: a prospective controlled study. Clin Gastroenterol Hepatol 2006;4:766-781; quiz 665.
6. Charpentier KP, Brentnall TA, Bronner MP, Byrd D, Marsh C: A new indication for pancreas transplantation: high-grade pancreatic dysplasia. Clin Transplant 2004;18:105-107.
7. Smith RA, Cokkinides V, Eyre HJ: American Cancer Society guidelines for the early detection of cancer, 2006. CA Cancer J Clin 2006;56:11-25; quiz 49-50.
8. Negm RS, Verma M, Srivastava S: The promise of biomarkers in cancer screening and detection. Trends Mol Med 2002;8:288-293.
9. Hulst SP: Zur Kenntnis der Genese des Adenokarzinoms und Karzinoms des Pankreas. Virchows Arch 1905;180:288-316.
10. Takaori K, Hruban RH, Maitra A, Tanigawa N: Pancreatic intraepithelial neoplasia. Pancreas 2004;28:257-262.
11. Klimstra DS, Longnecker DS: K-ras mutations in pancreatic ductal proliferative lesions. Am J Pathol 1994;145:1547-1550.
12. Hruban RH, Adsay NV, Albores-Saavedra J, Compton C, Garrett ES, Goodman SN, Kern SE, Klimstra DS, Kloppel G, Longnecker DS, Luttges J, Offerhaus GJ: Pancreatic intraepithelial neoplasia: a new nomenclature and classification system for pancreatic duct lesions. Am J Surg Pathol 2001;25:579-586.
13. Hruban RH, Takaori K, Klimstra DS, Adsay NV, Albores-Saavedra J, Biankin AV, Biankin SA, Compton C, Fukushima N, Furukawa T, Goggins M, Kato Y, Kloppel G, Longnecker DS, Luttges J, Maitra A, Offerhaus GJ, Shimizu M, Yonezawa S: An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillary mucinous neoplasms. Am J Surg Pathol 2004;28:977-987.
14. Kern SE, Hruban RH, Hidalgo M, Yeo CJ: An introduction to pancreatic adenocarcinoma genetics, pathology and therapy. Cancer Biol Ther 2002;1:607-613.
15. Doi R, Ikeda H, Kobayashi H, Kogire M, Imamura M: Carcinoma in the remnant pancreas after distal pancreatectomy for carcinoma. Eur J Surg Suppl 2003(588):62-65.
16. McCarthy DM, Brat DJ, Wilentz RE, Yeo CJ, Cameron JL, Kern SE, Hruban RH: Pancreatic intraepithelial neoplasia and infiltrating adenocarcinoma: analysis of progression and recurrence by dpc4 immunohistochemical labeling. Hum Pathol 2001;32:638-642.
17. Hruban RH, Wilentz RE, Goggins M, Offerhaus GJ, Yeo CJ, Kern SE: Pathology of incipient pancreatic cancer. Ann Oncol 1999;10:9-11.
18. Maitra A, Fukushima N, Takaori K, Hruban RH: Precursors to invasive pancreatic cancer. Adv Anat Pathol 2005;12:81-91.
19. Maitra A, Adsay NV, Argani P, Iacobuzio-Donahue C, De Marzo A, Cameron JL, Yeo CJ, Hruban RH: Multicomponent analysis of the pancreatic adenocarcinoma progression model using a pancreatic intraepithelial neoplasia tissue microarray. Mod Pathol 2003;16:902-912.
20. Luttges J, Kloppel G: Precancerous conditions of pancreatic carcinoma. J Hepatobiliary Pancreat Surg 2000;7:568-574.
21. Biankin AV, Kench JG, Dijkman FP, Biankin SA, Henshall SM: Molecular pathogenesis of precursor lesions of pancreatic ductal adenocarcinoma. Pathology 2003;35:14-24.
22. Moskaluk CA, Hruban RH, Kern SE: P16 and k-ras gene mutations in the intraductal precursors of human pancreatic adenocarcinoma. Cancer Res 1997;57:2140-2143.
23. Deramaudt T, Rustgi AK: Mutant KRAS in the initiation of pancreatic cancer. Biochim Biophys Acta 2005;1756:97-101.
24. Sherr CJ: Cell cycle control and cancer. Harvey Lect 2000;96:73-92.
25. Caldas C, Hahn SA, da Costa LT, Redston MS, Schutte M, Seymour AB, Weinstein CL, Hruban RH, Yeo CJ, Kern SE: Frequent somatic mutations and homozygous deletions of the p16 (mts1) gene in pancreatic adenocarcinoma. Nat Genet 1994;8:27-32.
26. Schutte M, Hruban RH, Geradts J, Maynard R, Hilgers W, Rabindran SK, Moskaluk CA, Hahn SA, Schwarte-Waldhoff I, Schmiegel W, Baylin SB, Kern SE, Herman JG: Abrogation of the rb/p16 tumor-suppressive pathway in virtually all pancreatic carcinomas. Cancer Res 1997;57:3126-3130.
27. Wilentz RE, Geradts J, Maynard R, Offerhaus GJ, Kang M, Goggins M, Yeo CJ, Kern SE, Hruban RH: Inactivation of the p16 (ink4a) tumor suppressor gene in pancreatic duct lesions: loss of intranuclear expression. Cancer Res 1998;58:4740-4744.
28. Meeker AK, De Marzo AM: Recent advances in telomere biology: implications for human cancer. Curr Opin Oncol 2004;16:32-38.
29. van Heek NT, Meeker AK, Kern SE, Yeo CJ, Lillemoe KD, Cameron JL, Offerhaus GJ, Hicks JL, Wilentz RE, Goggins MG, De Marzo AM, Hruban RH, Maitra A: Telomere shortening is nearly universal in pancreatic intraepithelial neoplasia. Am J Pathol 2002;161:1541-1547.
30. Callen E, Surralles J: Telomere dysfunction in genome instability syndromes. Mutat Res 2004;567:85-104.
31. Rodier F, Kim SH, Nijjar T, Yaswen P, Campisi J: Cancer and aging: the importance of telomeres in genome maintenance. Int J Biochem Cell Biol 2005;37:977-990.
32. Luttges J, Galehdari H, Brocker V, Schwarte-Waldhoff I, Henne-Bruns D, Kloppel G, Schmiegel W, Hahn SA: Allelic loss is often the first hit in the biallelic inactivation of the p53 and dpc4 genes during pancreatic carcinogenesis. Am J Pathol 2001;158:1677-1683.
33. Goggins M, Hruban RH, Kern SE: Brca2 is inactivated late in the development of pancreatic intraepithelial neoplasia: evidence and implications. Am J Pathol 2000;156:1767-1771.
34. Wilentz RE, Iacobuzio-Donahue CA, Argani P, McCarthy DM, Parsons JL, Yeo CJ, Kern SE, Hruban RH: Loss of expression of dpc4 in pancreatic intraepithelial neoplasia: evidence that dpc4 inactivation occurs late in neoplastic progression. Cancer Res 2000;60:2002-2006.
35. Sato N, Goggins M: The role of epigenetic alterations in pancreatic cancer. J Hepatobiliary Pancreat Surg 2006;13:286-295.
36. Rosty C, Geradts J, Sato N, Wilentz RE, Roberts H, Sohn T, Cameron JL, Yeo CJ, Hruban RH, Goggins M: P16 inactivation in pancreatic intraepithelial neoplasias (panins) arising in patients with chronic pancreatitis. Am J Surg Pathol 2003;27:1495-1501.
37. Fukushima N, Sato N, Ueki T, Rosty C, Walter KM, Wilentz RE, Yeo CJ, Hruban RH, Goggins M: Aberrant methylation of preproenkephalin and p16 genes in pancreatic intraepithelial neoplasia and pancreatic ductal adenocarcinoma. Am J Pathol 2002;160:1573-1581.
38. Thayer SP, di Magliano MP, Heiser PW, Nielsen CM, Roberts DJ, Lauwers GY, Qi YP, Gysin S, Fernandez-del Castillo C, Yajnik V, Antoniu B, McMahon M, Warshaw AL, Hebrok M: Hedgehog is an early and late mediator of pancreatic cancer tumorigenesis. Nature 2003;425:851-856.
39. Miyamoto Y, Maitra A, Ghosh B, Zechner U, Argani P, Iacobuzio-Donahue CA, Sriuranpong V, Iso T, Meszoely IM, Wolfe MS, Hruban RH, Ball DW, Schmid RM, Leach SD: Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell 2003;3:565-576.
40. Friess H, Guo XZ, Nan BC, Kleeff O, Büchler MW: Growth factors and cytokines in pancreatic carcinogenesis. Ann N Y Acad Sci 1999;880:110-121.
41. Day JD, Digiuseppe JA, Yeo C, Lai-Goldman M, Anderson SM, Goodman SN, Kern SE, Hruban RH: Immunohistochemical evaluation of her-2/neu expression in pancreatic adenocarcinoma and pancreatic intraepithelial neoplasms. Hum Pathol 1996;27:119-124.
42. Ueda S, Ogata S, Tsuda H, Kawarabayashi N, Kimura M, Sugiura Y, Tamai S, Matsubara O, Hatsuse K, Mochizuki H: The correlation between cytoplasmic overexpression of epidermal growth factor receptor and tumor aggressiveness: poor prognosis in patients with pancreatic ductal adenocarcinoma. Pancreas 2004;29:e1-e8.
43. Argani P, Iacobuzio-Donahue C, Ryu B, Rosty C, Goggins M, Wilentz RE, Murugesan SR, Leach SD, Jaffee E, Yeo CJ, Cameron JL, Kern SE, Hruban RH: Mesothelin is overexpressed in the vast majority of ductal adenocarcinomas of the pancreas: identification of a new pancreatic cancer marker by serial analysis of gene expression (SAGE). Clin Cancer Res 2001;7:3862-3868.
44. Corso CD, Stubbs DD, Lee SH, Goggins M, Hruban RH, Hunt WD: Real-time detection of mesothelin in pancreatic cancer cell line supernatant using an acoustic wave immunosensor. Cancer Detect Prev 2006;30:180-187.
45. Mamot C, Drummond DC, Noble CO, Kallab V, Guo Z, Hong K, Kirpotin DB, Park JW: Epidermal growth factor receptor-targeted immunoliposomes significantly enhance the efficacy of multiple anticancer drugs in vivo. Cancer Res 2005;65:11631-11638.
46. Salvia R, Festa L, Butturini G, Tonsi A, Sartori N, Biasutti C, Capelli P, Pederzoli P: Pancreatic cystic tumors. Minerva Chir 2004;59:185-207.
47. Wilentz RE, Albores-Saavedra J, Hruban RH: Mucinous cystic neoplasms of the pancreas. Semin Diagn Pathol 2000;17:31-42.
48. Zamboni G, Scarpa A, Bogina G, Iacono C, Bassi C, Talamini G, Sessa F, Capella C, Solcia E, Rickaert F, Mariuzzi GM, Kloppel G: Mucinous cystic tumors of the pancreas: clinicopathological features, prognosis, and relationship to other mucinous cystic tumors. Am J Surg Pathol 1999;23:410-422.
49. Klimstra DS: Cystic, mucin-producing neoplasms of the pancreas: the distinguishing features of mucinous cystic neoplasms and intraductal papillary mucinous neoplasms. Semin Diagn Pathol 2005;22:318-329.
50. Wilentz RE, Albores-Saavedra J, Zahurak M, Talamini MA, Yeo CJ, Cameron JL, Hruban RH: Pathologic examination accurately predicts prognosis in mucinous cystic neoplasms of the pancreas. Am J Surg Pathol 1999;23:1320-1327.
51. Jimenez RE, Warshaw AL, Z'Graggen K, Hartwig W, Taylor DZ, Compton CC, Fernandez-del Castillo C: Sequential accumulation of k-ras mutations and p53 overexpression in the progression of pancreatic mucinous cystic neoplasms to malignancy. Ann Surg 1999;230:501-509; discussion 509-511.
52. Iacobuzio-Donahue CA, Wilentz RE, Argani P, Yeo CJ, Cameron JL, Kern SE, Hruban RH: Dpc4 protein in mucinous cystic neoplasms of the pancreas: frequent loss of expression in invasive carcinomas suggests a role in genetic progression. Am J Surg Pathol 2000;24:1544-1548.
53. Fukushima N, Sato N, Prasad N, Leach SD, Hruban RH, Goggins M: Characterization of gene expression in mucinous cystic neoplasms of the pancreas using oligonucleotide microarrays. Oncogene 2004;23:9042-9051.
54. Schmitz-Winnenthal FH, Z'Graggen K, Volk C, Schmied BM, Büchler MW: Intraductal papillary mucinous tumors of the pancreas. Curr Gastroenterol Rep 2003;5:133-140.
55. Tanaka M, Kobayashi K, Mizumoto K, Yamaguchi K: Clinical aspects of intraductal papillary mucinous neoplasm of the pancreas. J Gastroenterol 2005;40:669-675.
56. Sohn TA, Yeo CJ, Cameron JL, Hruban RH, Fukushima N, Campbell KA, Lillemoe KD: Intraductal papillary mucinous neoplasms of the pancreas: an updated experience. Ann Surg 2004;239:788-797; discussion 797-789.
57. Furukawa T, Kloppel G, Volkan Adsay N, Albores-Saavedra J, Fukushima N, Horii A, Hruban RH, Kato Y, Klimstra DS, Longnecker DS, Luttges J, Offerhaus GJ, Shimizu M, Sunamura M, Suriawinata A, Takaori K, Yonezawa S: Classification of types of intraductal papillary-mucinous neoplasm of the pancreas: a consensus study. Virchows Arch 2005;447:794-799.
58. Kobari M, Egawa S, Shibuya K, Shimamura H, Sunamura M, Takeda K, Matsuno S, Furukawa T: Intraductal papillary mucinous tumors of the pancreas comprise 2 clinical subtypes: differences in clinical characteristics and surgical management. Arch Surg 1999;134:1131-1136.
59. Sugiyama M, Izumisato Y, Abe N, Masaki T, Mori T, Atomi Y: Predictive factors for malignancy in intraductal papillary-mucinous tumours of the pancreas. Br J Surg 2003;90:1244-1249.
60. Kitagawa Y, Unger TA, Taylor S, Kozarek RA, Traverso LW: Mucus is a predictor of better prognosis and survival in patients with intraductal papillary mucinous tumor of the pancreas. J Gastrointest Surg 2003;7:12-18; discussion 18-19.
61. Terris B, Ponsot P, Paye F, Hammel P, Sauvanet A, Molas G, Bernades P, Belghiti J, Ruszniewski P, Flejou JF: 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.
62. Nishihara K, Fukuda T, Tsuneyoshi M, Kominami T, Maeda S, Saku M: Intraductal papillary neoplasm of the pancreas. Cancer 1993;72:689-696.
63. Adsay NV, Merati K, Basturk O, Iacobuzio-Donahue C, Levi E, Cheng JD, Sarkar FH, Hruban RH, Klimstra DS: Pathologically and biologically distinct types of epithelium in intraductal papillary mucinous neoplasms: delineation of an 'intestinal' pathway of carcinogenesis in the pancreas. Am J Surg Pathol 2004;28:839-848.
64. Adsay NV, Merati K, Andea A, Sarkar F, Hruban RH, Wilentz RE, Goggins M, Iacobuzio-Donahue C, Longnecker DS, Klimstra DS: The dichotomy in the preinvasive neoplasia to invasive carcinoma sequence in the pancreas: differential expression of MUC1 and MUC2 supports the existence of two separate pathways of carcinogenesis. Mod Pathol 2002;15:1087-1095.
65. Moriya T, Kimura W, Semba S, Sakurai F, Hirai I, Ma J, Fuse A, Maeda K, Yamakawa M: Biological similarities and differences between pancreatic intraepithelial neoplasias and intraductal papillary mucinous neoplasms. Int J Gastrointest Cancer 2005;35:111-119
66. Yonezawa S, Nakamura A, Horinouchi M, Sato E: The expression of several types of mucin is related to the biological behavior of pancreatic neoplasms. J Hepatobiliary Pancreat Surg 2002;9:328-341.
67. Adsay NV, Pierson C, Sarkar F, Abrams J, Weaver D, Conlon KC, Brennan MF, Klimstra DS: Colloid (mucinous noncystic) carcinoma of the pancreas. Am J Surg Pathol 2001;25:26-42.
68. Seidel G, Zahurak M, Iacobuzio-Donahue C, Sohn TA, Adsay NV, Yeo CJ, Lillemoe KD, Cameron JL, Hruban RH, Wilentz RE: Almost all infiltrating colloid carcinomas of the pancreas and periampullary region arise from in situ papillary neoplasms: a study of 39 cases. Am J Surg Pathol 2002;26:56-63.
69. Yoshizawa K, Nagai H, Sakurai S, Hironaka M, Morinaga S, Saitoh K, Fukayama M: Clonality and k-ras mutation analyses of epithelia in intraductal papillary mucinous tumor and mucinous cystic tumor of the pancreas. Virchows Arch 2002;441:437-443.
70. Kondo H, Sugano K, Fukayama N, Hosokawa K, Ohkura H, Ohtsu A, Mukai K, Yoshida S: Detection of k-ras gene mutations at codon 12 in the pancreatic juice of patients with intraductal papillary mucinous tumors of the pancreas. Cancer 1997;79:900-905.
71. Iacobuzio-Donahue CA, Klimstra DS, Adsay NV, Wilentz RE, Argani P, Sohn TA, Yeo CJ, Cameron JL, Kern SE, Hruban RH: Dpc-4 protein is expressed in virtually all human intraductal papillary mucinous neoplasms of the pancreas: comparison with conventional ductal adenocarcinomas. Am J Pathol 2000;157:755-761.
72. Sahin F, Maitra A, Argani P, Sato N, Maehara N, Montgomery E, Goggins M, Hruban RH, Su GH: Loss of stk11/lkb1 expression in pancreatic and biliary neoplasms. Mod Pathol 2003;16:686-691.
73. Schonleben F, Qiu W, Ciau NT, Ho DJ, Li X, Allendorf JD, Remotti HE, Su GH: Pik3ca mutations in intraductal papillary mucinous neoplasm/carcinoma of the pancreas. Clin Cancer Res 2006;12:3851-3855.
74. Samuels Y, Wang Z, Bardelli A, Silliman N, Ptak J, Szabo S, Yan H, Gazdar A, Powell SM, Riggins GJ, Willson JK, Markowitz S, Kinzler KW, Vogelstein B, Velculescu VE: High frequency of mutations of the pik3ca gene in human cancers. Science 2004;304:554.
75. Maitra A, Kern SE, Hruban RH: Molecular pathogenesis of pancreatic cancer. Best Pract Res Clin Gastroenterol 2006;20:211-226.
76. Winter JM, Cameron JL, Lillemoe KD, Campbell KA, Chang D, Riall TS, Coleman J, Sauter PK, Canto M, Hruban RH, Schulick RD, Choti MA, Yeo CJ: Periampullary and pancreatic incidentaloma: a single institution's experience with an increasingly common diagnosis. Ann Surg 2006;243:673-680; discussion 680-673.
77. Spinelli KS, Fromwiller TE, Daniel RA, Kiely JM, Nakeeb A, Komorowski RA, Wilson SD, Pitt HA: Cystic pancreatic neoplasms: observe or operate. Ann Surg 2004;239:651-657; discussion 657-659.
78. Fernandez-del Castillo C, Targarona J, Thayer SP, Rattner DW, Brugge WR, Warshaw AL: Incidental pancreatic cysts: clinicopathologic characteristics and comparison with symptomatic patients. Arch Surg 2003;138:427-433; discussion 433-434.
79. Balcom IV IJ, Fernandez-del Castillo C, Warshaw AL: Cystic lesions in the pancreas: when to watch, when to resect. Curr Gastroenterol Rep 2000;2:152-158.
80. Tanaka M, Chari S, Adsay V, Fernandez-del Castillo C, Falconi M, Shimizu M, Yamaguchi K, Yamao K, Matsuno S; International Association of Pancreatology: International consensus guidelines for management of intraductal papillary mucinous neoplasms and mucinous cystic neoplasms of the pancreas. Pancreatology 2006;6:17-32.
81. Levy MJ, Clain JE: Evaluation and management of cystic pancreatic tumors: emphasis on the role of EUS FNA. Clin Gastroenterol Hepatol 2004;2:639-653.
82. Eloubeidi MA, Jhala D, Chhieng DC, Chen VK, Eltoum I, Vickers S, Mel Wilcox C, Jhala N: Yield of endoscopic ultrasound-guided fine-needle aspiration biopsy in patients with suspected pancreatic carcinoma. Cancer 2003;99:285-292.
83. Brugge WR, Lewandrowski K, Lee-Lewandrowski E, Centeno BA, Szydlo T, Regan S, del Castillo CF, Warshaw AL: Diagnosis of pancreatic cystic neoplasms: a report of the cooperative pancreatic cyst study. Gastroenterology 2004;126:1330-1336.
84. Sperti C, Pasquali C, Di Prima F, Rugge M, Petrin P, Costantino V, Canton A, Pedrazzoli S: Percutaneous CT-guided fine-needle aspiration cytology in the differential diagnosis of pancreatic lesions. Ital J Gastroenterol 1994;26:126-131.
85. Jhala NC, Jhala DN, Chhieng DC, Eloubeidi MA, Eltoum IA: Endoscopic ultrasound-guided fine-needle aspiration: a cytopathologist's perspective. Am J Clin Pathol 2003;120:351-367.
86. Sperti C, Pasquali C, Pedrazzoli S, Guolo P, Liessi G: Expression of mucin-like carcinoma-associated antigen in the cyst fluid differentiates mucinous from nonmucinous pancreatic cysts. Am J Gastroenterol 1997;92:672-675.
87. Ryu JK, Woo SM, Hwang JH, Jeong JB, Yoon YB, Park IA, Han JK, Kim YT: Cyst fluid analysis for the differential diagnosis of pancreatic cysts. Diagn Cytopathol 2004;31:100-105.
88. Hammel PR, Forgue-Lafitte ME, Levy P, Voitot H, Vilgrain V, Flejou JF, Molas G, Gespach C, Ruszniewski P, Bernades P, Bara J: Detection of gastric mucins (m1 antigens) in cyst fluid for the diagnosis of cystic lesions of the pancreas. Int J Cancer 1997;74:286-290.
89. Pelaez-Luna M, Chari ST: Cyst fluid analysis to diagnose pancreatic cystic lesions: an as yet unfulfilled promise. Gastroenterology 2006;130:1007-1009; discussion 1009.
90. Petersen GM, Hruban RH: Familial pancreatic cancer: where are we in 2003? J Natl Cancer Inst 2003;95:180-181.
91. Klein AP, Hruban RH, Brune KA, Petersen GM, Goggins M: Familial pancreatic cancer. Cancer J 2001;7:266-273.
92. Habbe N, Langer P, Sina-Frey M, Bartsch DK: Familial pancreatic cancer syndromes. Endocrinol Metab Clin North Am 2006;35:417-430, xi.
93. Petersen GM, de Andrade M, Goggins M, Hruban RH, Bondy M, Korczak JF, Gallinger S, Lynch HT, Syngal S, Rabe KG, Seminara D, Klein AP: Pancreatic cancer genetic epidemiology consortium. Cancer Epidemiol Biomarkers Prev 2006;15:704-710.
94. Klein AP, Beaty TH, Bailey-Wilson JE, Brune KA, Hruban RH, Petersen GM: Evidence for a major gene influencing risk of pancreatic cancer. Genet Epidemiol 2002;23:133-149.
95. Tersmette AC, Petersen GM, Offerhaus GJ, Falatko FC, Brune KA, Goggins M, Rozenblum E, Wilentz RE, Yeo CJ, Cameron JL, Kern SE, Hruban RH: Increased risk of incident pancreatic cancer among first-degree relatives of patients with familial pancreatic cancer. Clin Cancer Res 2001;7:738-744.
96. Klein AP, Brune KA, Petersen GM, Goggins M, Tersmette AC, Offerhaus GJ, Griffin C, Cameron JL, Yeo CJ, Kern S, Hruban RH: Prospective risk of pancreatic cancer in familial pancreatic cancer kindreds. Cancer Res 2004;64:2634-2638.
97. Rulyak SJ, Kimmey MB, Veenstra DL, Brentnall TA: Cost-effectiveness of pancreatic cancer screening in familial pancreatic cancer kindreds. Gastrointest Endosc 2003;57:23-29.
98. Choi MG, Kim SW, Han SS, Jang JY, Park YH: High incidence of extrapancreatic neoplasms in patients with intraductal papillary mucinous neoplasms. Arch Surg 2006;141:51-56; discussion 56.
99. Hruban RH, Canto MI, Griffin C, Kern SE, Klein AP, Laheru D, Yeo CJ: Treatment of familial pancreatic cancer and its precursors. Curr Treat Options Gastroenterol 2005;8:365-375.
100. Brune K, Abe T, Canto M, O'Malley L, Klein AP, Maitra A, Volkan Adsay N, Fishman EK, Cameron JL, Yeo CJ, Kern SE, Goggins M, Hruban RH: 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.