Surgical Oncology
Volume 14, Issue 4 , Pages 155-178 , December 2005

Intraductal papillary mucinous neoplasms of the pancreas: A surgical perspective

  • George H. Sakorafas

      Affiliations

    • Department of Surgery, 251 Hellenic Air Force Hospital, Arkadias 19-21, GR-115 26 Athens, Greece
    • Corresponding Author InformationCorresponding author. Tel.: +302107487318; fax: +302107487192.
  • ,
  • Michael G. Sarr

      Affiliations

    • Department of Surgery, Mayo Clinic, Rochester, MN, USA
  • ,
  • Cornelis J.H. van de Velde

      Affiliations

    • Department of Surgery, Leiden University Medical Center, Leiden, Netherlands
  • ,
  • George Peros

      Affiliations

    • 4th Department of Surgery, ATTIKON University Hospital, Athens University, Medical School, Greece

References 

  1. Horvath KD, Chabot JA. An aggressive resectional approach to cystic neoplasms of the pancreas. American Journal of Surgery. 1999;178:269–274
  2. Sakorafas GH, Sarr MG. Cystic neoplasms of the pancreas. In:  Bland KI,  Sarr MG editor. The practice of general surgery. Philadelphia, PA: W.B. Saunders Co; 2002;p. 771–776
  3. Ohhashi K, Murakami Y, Takekoshi T. Four cases of mucous secreting pancreatic cancer (abstr). Progress in Diagnstic Endoscopy. 1982;20:348–351
  4. Nakazawa S, Yamao K, Yamada M, et al. Study of the classification of mucin-producing cystic tumors of the pancreas. Japanese Journal of Gastroenterology. 1985;88:924–932
  5. Itai Y, Ohhashi K, Nagai H, et al. Ductectatic mucinous cystadenoma and cystadenocarcinoma of the pancreas. Radiology. 1986;161:697–700
  6. Morohoshi T, Kanda M, Asanuma K, et al. Intraductal papillary mucinous neoplasms of the pancreas. A clinicopathologic study of six patients. Cancer. 1989;64:1329–1335
  7. Yamada M, Kozuka S, Yamao K, et al. Mucin producing tumor of the pancreas. Cancer. 1991;68:159–168
  8. Bastid C, Bernard JP, Sarles H, et al. Mucinous ductal ectasia of the pancreas: a premalignant disease and a cause of obstructive pancreatitis. Pancreas. 1991;6:15–22
  9. Kawarada Y, Yano T, Yamamoto T, et al. Intraductal mucin-producing tumors of the pancreas. American Journal of Gastroenterology. 1992;87:634–638
  10. Yamaguchi K, Ogawa Y, Chijiwa K, et al. Mucin-hypersecreting tumors of the pancreas: assessing the grade of malignancy preoperatively. American Journal of Surgery. 1996;171:427–431
  11. Sugiyama M, Atomi Y, Hachiya J. Intraductal papillary tumors of the pancreas: evaluation with magnetic resonance cholangiopancreatography. American Journal of Gastroenterology. 1998;93:156–159
  12. Traverso LW, Peralta EA, Ryan JA, et al. Intraductal neoplasms of the pancreas. American Journal of Surgery. 1998;175:426–432
  13. Sohn TA, Yeo CJ, Cameron JL, et al. Intraductal papillary mucinous neoplasms of the pancreas: an increasingly recognized clinicopathologic entity. Annals of Surgery. 2001;234:313–322
  14. Salvia R, Fernandez-del Castillo C, Bassi C, et al. Main-duct intraductal papillary mucinous neoplasms of the pancreas. Annals of Surgery. 2004;239:678–687
  15. Loftus EV, Olivares-Pakzad BA, Batts KP, et al. Intraductal papillary-mucinous tumors of the pancreas: clinicopathologic features, outcome, and nomenclature. Members of the Pancreas Clinic, and Pancreatic Surgeons of the Mayo Clinic. Gastroenterology. 1996;110:1909–1918
  16. Kloppel G, Solcia E, Longnecker DS, et al. Histological typing of tumors of the exocrine pancreas. In: World Health Organization International Histological Classification of Tumors. 2nd ed. Berlin: Springer; 1996;p. 11–20
  17. Solcia E, Capella C, Kloppel G. Tumors of the exocrine pancreas. In:  Solcia E,  Capella C,  Kloppel G editor. Atlas of tumor pathology. Washington, DC: AFIP; 1997;p. 145–210
  18. Longnecker DS, Adler G, Hruban RH, Kloppel G. Intraductal papillary mucinous neoplasms of the pancreas. In: Hamilton SR, Aaltonen LA, editors. WHO Classification of Tumors of the Digestive System, 2000. p. 237–40.
  19. Sohn TA, Yeo CJ, Cameron JL, et al. Intraductal papillary mucinous neoplasms of the pancreas. An updated experience. Annals of Surgery. 2004;239:788–799
  20. Sugiyama M, Atomi Y. Intraductal papillary mucinous tumors of the pancreas: imaging studies and treatment strategies. Annals of Surgery. 1998;228:685–691
  21. Longnecker DS. Observations on the etiology and pathogenesis of intraductal papillary-mucinous neoplasms of the pancreas. Hepatogastroenterology. 1998;45:1973–1980
  22. D’ Angelica M, Brennan MF, Suriawinata AA, et al. Intraductal papillary mucinous neoplasms of the pancreas. Annals of Surgery. 2004;239:400–408
  23. Adsay NV, Longnecker DS, Klimstra DS. Pancreatic tumors with cystic dilatation of the ducts: intraductal papillary mucinous neoplasms and intraductal oncocytic papillary neoplasms. Seminars in Diagnostic Pathology. 2000;17:16–30
  24. Sarr MG, Murr M, Smyrk TC, et al. Primary cystic neoplasms of the pancreas: neoplastic disorders of emerging importance—current state-of-the-art and unanswered questions. Journal of Gastrointestinal Surgery. 2003;7:417–428
  25. Reddy RP, Smyrk TC, Zapiach M, Levy MJ, Pearson RK, Clain JE, et al. Pancreatic mucinous cystic neoplasm defined by ovarian stroma: demographics, clinical features and prevalence of cancer. Clinical Gastroenterology and Hepatology. 2004;2:1026–1031
  26. Sakorafas GH, Sarr MG. Pancreatic cancer after surgery for chronic pancreatitis. Digestive and Liver Diseases. 2003;35:482–485
  27. Sakorafas GH, Sarr MG. Primary cystic neoplasms of the pancreas. In: Yeo CJ, editor. Shackelford's surgery of the alimentary tract, 6th ed. W.B. Saunders, Philadelphia, PA, in press.
  28. Shima Y, Mori M, Takakura N, et al. Diagnosis and management of cystic pancreatic tumor with mucin production. British Journal of Surgery. 2000;87:1041–1047
  29. Cellier C, Cuillerier E, Palazzo L, et al. Intraductal papillary and mucinous tumors of the pancreas: accuracy of preoperative computed tomography, endoscopic retrograde pancreatography and endoscopic ultrasonography, and long-term outcome in a large surgical series. Gastrointestinal Endoscopy. 1998;47:42–49
  30. Siech M, Tripp K, Schmidt-Rohlfing B, et al. Intraductal papillary mucinous tumors of the pancreas. American Journal of Surgery. 1999;177:117–120
  31. Fukushima N, Mukai K, Kanai Y, et al. Intraductal papillary tumors and mucinous cystic tumors of the pancreas; clinicopathologic study of 38 cases. Human Pathology. 1997;28:1010–1017
  32. Hruban RH, Takaori K, Klimstra DS, et al. An illustrated consensus on the classification of pancreatic intraepithelial neoplasia and intraductal papillary mucinous neoplasms. American Journal of Surgical Pathology. 2004;28:977–987
  33. In:  Hamilton SR,  Aaltonen LA editor. World Health Organization Classification of Tumors. Tumors of the digestive system. Lyon: IARC Press; 2000;p. 234–240
  34. Adsay NV, Pierson C, Sarkar F, et al. Colloid (mucinous non-cystic) carcinoma of the pancreas. American Journal of Surgical Pathology. 2001;25:26–42
  35. Adsay NV, Merati K, Basturk O, et al. Pathologically and biologically distinct types of epithelium in intraductal papillary mucinous neoplasms. Delineation of an “Intestinal” pathway of carcinogenesis in the pancreas. American Journal of Surgical Pathology. 2004;28:839–848
  36. Adsay NV, Conlon KC, Zee SY, et al. Intraductal papillary-mucinous neoplasms of the pancreas: an analysis of in situ and invasive carcinomas in 28 patients. Cancer. 2002;94:62–77
  37. Yonezawa S, Horinouchi M, Osako M, et al. Gene expression of gastric type mucin (MUC5AC) in pancreatic tumors: its relationship with the biological behavior of the tumor. Pathology International. 1999;49:45–54
  38. Yonezawa S, Nakamura A, Horinouchi M, et al. The expression of several types of mucin is related to the biological behavior of pancreatic neoplasms. Journal of Hepatobiliary Pancreatic Surgery. 2002;9:328–341
  39. Adsay NV, Adair CF, Heffess CS, et al. Intraductal oncocytic papillary neoplasms of the pancreas. American Journal of Surgical Pathology. 1996;177:117–120
  40. Nakamura A, Horinouchi M, Goto M, et al. New classification of pancreatic intraductal papillary-mucinous tumor by mucin expression: its relationship with potential for malignancy. Journal of Pathology. 2002;197:201–210
  41. Luttges J, Feyerabend B, Buchelt T, et al. The mucin profile of noninvasive and invasive mucinous cystic neoplasms of the pancreas. American Journal of Surgical Pathology. 2002;26:466–471
  42. Luttges J, Zamboni G, Longnecker D, et al. The immunohistochemical mucin expression pattern distinguishes different types of intraductal papillary mucinous neoplasms of the pancreas and determines their relationship to mucinous noncystic carcinoma and ductal adenocarcinoma. American Journal of Surgical Pathology. 2001;25:942–948
  43. Irie H, Honda H, Aibe H, et al. MR cholangiopancreatographic differentiation of benign and malignant intraductal mucin-producing tumors of the pancreas. American Journal of Roentgenology. 2000;174:1403–1408
  44. 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. American Journal of Surgical Pathology. 2000;24:1372–1377
  45. Kobari M, Eguawa S, Shibuya K, et al. Intraductal papillary mucinous tumors of the pancreas comprise 2 clinical subtypes; differences in clinical characteristics and surgical management. Archives of Surgery. 1999;134:1131–1136
  46. Matsumoto T, Aramaki M, Yada K, et al. Optimal management of the branch duct type intraductal papillary mucinous neoplasms of the pancreas. Journal of Clinical Gastroenterology. 2003;36:261–265
  47. Yamaguchi K, Tanaka M. Intraductal papillary-mucinous tumor of the pancreas: a historical review of the nomenclature and recent controversy. Pancreas. 2001;23:12–19
  48. Yonezawa S, Taira M, Osako M, et al. MUC1 mucin expression in invasive areas of intraductal papillary mucinous tumors of the pancreas. Pathology International. 1998;48:319–322
  49. Hollingsworth MA, Strawhecker JM, Caffrey TC, et al. Expression of MUC1, MUC2, MUC3, and MUC4 mucin mRNAs in human pancreatic and intestinal tumor cell lines. International Journal of Cancer. 1994;57:198–203
  50. Makiguchi Y, Hinoda Y, Imai K. Effect of MUC1 mucin, an anti-adhesion molecule, on tumor cell growth. Japanese Journal of Cancer Research. 1996;87:505–511
  51. Satoh S, Hinoda Y, Hayashi T, et al. Enhancement of metastatic properties of pancreatic cancer cells by MUC1 gene encoding an anti-adhesion molecule. International Journal of Cancer. 2000;88:507–518
  52. Allen A, Hutton DA, Pearson JP. The MUC2 gene product: a human intestinal mucin. International Journal of Biochemistry & Cell Biology. 1998;30:797–801
  53. Ho JJ, Han SW, Pan PL, et al. Methylation status of promoters and expression of MUC2 and MUC5A mucins in pancreatic cancer cells. International Journal of Oncology. 2003;22:273–279
  54. Terris B, Dubois S, Buisine MP, et al. Mucin gene expression in intraductal papillary-mucinous pancreatic tumors and related lesions. Journal of Pathology. 2002;197:632–637
  55. Yonezawa S, Sueyoshi K, Nomoto M, et al. MUC2 gene expression is found in non-invasive tumors but not in invasive tumors of the pancreas and liver: its close relationship with prognosis of the patients. Human Pathology. 1997;28:344–352
  56. Adsay NV, Merati K, Andea A, et al. The dichotomy in the pre-invasive neoplasia to invasive carcinoma sequence in the pancreas: differential MUC1 and MUC2 expression supports the existence of two separate pathways of carcinogenesis. Modern Pathology. 2002;15:1087–1095
  57. Adsay NV, Merati K, Nassar H, et al. Pathogenesis of colloid (pure mucinous) carcinoma of exocrine organs: coupling of gel-forming mucin (MUC2) production with altered cell polarity and abnormal cell–stroma interaction may be the key factor in the morphogenesis and indolent behavior of colloid carcinoma in the breast and pancreas. American Journal of Surgical Pathology. 2003;27:571–578
  58. Z’graggen K, Rivera JA, Corris PA, et al. Prevalence of activating K-ras mutations in the evolutionary stages of neoplasia in intraductal papillary mucinous tumors of the pancreas. Annals of Surgery. 1997;226:491–498
  59. Islam HK, Fujioka Y, Tomidokoro T, et al. Immunohistochemical study of genetic alterations in intraductal and invasive ductal tumors of the pancreas. Hepatogastroenterology. 2001;48:879–883
  60. Sasaki S, Yamamoto H, Kaneto H, et al. Differential roles of alterations of p53, p16, and SMAD4 expression in the progression of intraductal papillary-mucinous tumors of the pancreas. Oncology Reports. 2003;10:21–25
  61. Biankin AV, Biankin SA, Kench JG, et al. Aberrant p16(INK4A) and DPC4Smad4 expression in intraductal papillary mucinous tumors of the pancreas is associated with invasive ductal adenocarcinoma. Gut. 2002;50:861–868
  62. Wada K. p16 and p53 gene alterations and accumulations in the malignant evolution of intraductal papillary-mucinous tumors of the pancreas. Journal of Hepatobiliary Pancreatic Surgery. 2002;9:76–85
  63. Tada M, Omata M, Ohto M. Ras gene mutations in intraductal papillary neoplasms of the pancreas. Cancer. 1991;67:634–637
  64. Moskaluk CA, Hruban RH, Kern SE. p16 and K-ras gene mutations in the intraductal precursors of human pancreatic adenocarcinoma. Cancer Research. 1997;57:2140–2143
  65. Sakorafas GH, Tsiotou AG, Tsiotos GG. Molecular biology of pancreatic cancer; oncogenes, tumour suppressor genes, growth factors, and their receptors from a clinical perspective. Cancer Treatment Reviews. 2000;26(1):29–52
  66. Sakorafas GH, Tsiotos GG. Molecular biology of pancreatic cancer: potential clinical implications. BioDrugs. 2001;15(7):439–452
  67. Fujii H, Inagaki M, Kasai K, et al. Genetic progression and heterogeneity in intraductal papillary mucinous-mucinous neoplasms of the pancreas. American Journal of Pathology. 1997;151:1447–1454
  68. Sessa F, Solcia E, Capella C, et al. Intraductal papillary-mucinous tumors represent a distinct group of pancreatic neoplasms: an investigation of tumor cell differentiation and K-ras, p53, and c-erbB-2 abnormalities in 26 patients. Virchows Archiv. 1994;425:357–367
  69. Kawahira H, Kobayashi S, Kaneko K, et al. p53 protein expression in intraductal papillary mucinous tumors (IPMT) of the pancreas as an indicator of tumor malignancy. Hepatogastroenterology. 2000;47:973–977
  70. Wada K, Takada T, Yasuda H, et al. Does “clonal progression” relate to the development of intraductal papillary mucinous tumors of the pancreas?. Journal of Gastrointestinal Surgery. 2004;8:289–296
  71. Bonhomme C, Duluc I, Martin E, et al. The Cdx2 homeobox gene has a tumor suppressor function in the distal colon in addition to a homeotic role during gut development. Gut. 2003;52:1465–1471
  72. Sato N, Rosty C, Jansen M, et al. STK11/LKB1 Peutz–Jeghers gene inactivation in intraductal papillary-mucinous neoplasms of the pancreas. American Journal of Pathology. 2001;159:2017–2022
  73. Iacobuzio-Donahue CA, Klinstra DS, et al. DPC-4 protein is expressed in virtually all human intraductal papillary mucinous neoplasms of the pancreas: comparison with conventional ductal carcinomas. American Journal of Pathology. 2000;157:755–761
  74. House GM, Guo M, Iacobuzio-Donajue C, et al. Molecular progression of promoter methylation in intraductal papillary mucinous neoplasms (IPMN) of the pancreas. Carcinogenesis. 2003;24:193–198
  75. Izawa T, Obara T, Tanno S, et al. Clonality and field cancerization in intraductal papillary-mucinous tumors of the pancreas. Cancer. 2001;92:1807–1817
  76. Kondo H, Sugano K, Fukayama N, et al. 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
  77. Sakorafas GH. Molecular biology of pancreatic cancer: how useful is it for the clinician?. Iatriki (GR). 2001;79:337–342
  78. Irie H, Yoshimitsu K, Aibe H, et al. Natural history of pancreatic intraductal papillary mucinous tumor of branch duct type. Journal of Computer Assisted Tomography. 2004;28:117–122
  79. Doi R, Fujimoto K, Wada M, et al. Surgical management of intraductal papillary mucinous tumor of the pancreas. Surgery. 2002;132:80–85
  80. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61:759–767
  81. Tsiotou AG, Krespis EN, Sakorafas GH, Krespi A. The genetic basis of colorectal cancer—clinical implications. European Journal of Surgical Oncology. 1995;21:96–100
  82. Wilentz RE, Hruban RH. Pathology of cancer of the pancreas. Surgical Oncology Clinics of North America. 1998;7:43–65
  83. Adsay NV. The “new kid on the block”: intraductal papillary mucinous neoplasms of the pancreas: current concepts and controversies. Surgery. 2003;133:459–463
  84. Kloppel G. Clinicopathologic view of intraductal papillary-mucinous tumor of the pancreas. Hepatogastroenterology. 1998;45:1981–1985
  85. Luttges J, Beyser K, Pust S, et al. Pancreatic mucinous non-cystic (colloid) carcinomas and intraductal papillary mucinous carcinomas are usually microsatellite stable. Modern Pathology. 2003;16:537–542
  86. Sarr MG, Sakorafas GH, Balsiger BM, Farley DR. The spectrum of cystic neoplasms of the pancreas. In:  Dervenis C,  Bassi C editor. Pancreatic tumors. Stuttgart: Georg Thieme Verlag; 2000;p. 297–303
  87. Sarr MG, Kendrick ML, Nagorney DM, et al. Cystic neoplasms of the pancreas. Surgical Clinics of North America. 2001;81:497–509
  88. Martin I, Hammond P, Scott J, et al. Cystic tumors of the pancreas. British Journal of Surgery. 1998;85:1484–1486
  89. Azar C, Van de Stadt J, Rickaert F, et al. Intraductal papillary mucinous tumors of the pancreas. Clinical and therapeutic issues in 32 patients. Gut. 1996;39:457–464
  90. Cellier C, Cuillerier E, Palazzo L, et al. Intraductal papillary and mucinous tumors of the pancreas: accuracy of preoperative computed tomography, endoscopic retrograde pancreatography, and long-term outcome in a large surgical series. Gastrointestinal Endoscopy. 1998;47:42–49
  91. Lim JH, Lee G, Oh YL. Radiologic spectrum of intraductal papillary mucinous tumors of the pancreas. Radiographics. 2001;21:323–340
  92. Albert J, Schilling D, Breer H, et al. Mucinous cystadenomas and intraductal papillary mucinous tumors of the pancreas in magnetic resonance cholangiopancreatography. Endoscopy. 2000;32:472–476
  93. Procacci C, Carbognin G, Buasiutti C, et al. Intraductal papillary mucinous tumors of the pancreas: spectrum of CT and MR findings with pathologic correlation. European Radiology. 2001;11:1939–1951
  94. Izuishi K, Nakagohri T, Konishi M, et al. Spatial assessment by magnetic resonance cholangiopancreatography for preoperative imaging in partial pancreatic head resection. American Journal of Surgery. 2001;182:188–191
  95. Megibow AJ, Lavelle MT, Rofsky NM. Cystic tumors of the pancreas. The radiologist. Surgical Clinics of North America. 2001;81:489–495
  96. Koito K, Namieno T, Ihimura T, et al. Mucin-producing pancreatic tumors: comparison of MR cholangiopancreatography with endoscopic retrograde cholangiopancreatography. Radiology. 1998;208:231–237
  97. Onaya H, Itai Y, Niitsu M, et al. Ductectatic mucinous cystic neoplasm of the pancreas: evaluation with MR cholangiopancreatography. American Journal of Roentgenology. 1998;171:171–177
  98. Fukukura Y, Fujiyoshi F, Sasaki M, et al. HASTE MR cholangiopancreatography in the evaluation of intraductal papillary mucinous tumors of the pancreas. Journal of Computer Assisted Tomography. 1999;23:301–305
  99. Sahani D, Prasad S, Saini S, Mueller P. Cystic pancreatic neoplasms evaluation by CT and magnetic resonance cholangiopancreatography. Gastrointestinal Endoscopic Clinics of North America. 2002;12:657–672
  100. Arakawa A, Yamashita Y, Namimoto T, et al. Intraductal papillary tumors of the pancreas. Histopathologic correlation of MR cholangiopancreatography findings. Acta Radiologica. 2000;41:343–347
  101. Fukukura Y, Fujiyoshi F, Hamada H, et al. Intraductal papillary mucinous tumors of the pancreas. Comparison of helical CT and MR imaging. Acta Radiologica. 2003;44:464–471
  102. Brugge WR, Lewandrowski K, Lee-Lewandrowski E, et al. Diagnosis of pancreatic cystic neoplasms: a report of the cooperative pancreatic cyst study. Gastroenterology. 2004;126:1330–1336
  103. Gress F, Gottlieb K, Cummings O, et al. Endoscopic ultrasound characteristics of mucinous cystic neoplasms of the pancreas. American Journal of Gastroenterology. 2000;95:961–965
  104. Ahmad NA, Kochman ML, Lewis JD, et al. Can EUS alone differentiate between malignant and benign cystic lesions of the pancreas?. American Journal of Gastroenterology. 2001;96:3295–3300
  105. Song MH, Lee SK, Kim MH, et al. EUS in the evaluation of pancreatic cystic lesions. Gastrointestinal Endoscopy. 2003;57:891–896
  106. Sedlack R, Affi A, Vasquez-Sequeiros E, et al. Utility of EUS in the evaluation of cystic pancreatic lesions. Gastrointestinal Endoscopy. 2002;56:543–547
  107. Bradwein SL, Farrell JJ, Centeno BA, et al. Detection and tumor staging of malignancy in cystic, intraductal, and solid tumors of the pancreas by EUS. Gastrointestinal Endoscopy. 2001;53:722–777
  108. Yamao K, Okubo K, Sawaka A, et al. Endoluminal ultrasonography in the diagnosis of pancreatic diseases. Abdominal Imaging. 2003;28(4):545–555
  109. Telford JJ, Carr-Locke DL. The role of ERCP and pancreatoscopy in cystic and intraductal tumors. Gastrointestinal Endoscopic Clinics of North America. 2002;12(4):747–757
  110. Vasquez-Sequeiros E, Wiersema MJ. Peroral pancreatoscopy and intraductal ultrasound for diagnosis of intraductal papillary mucinous tumors of the pancreas. American Journal of Gastroenterology. 2002;97(11):2915–2917
  111. Hara T, Yamaguchi T, Ishihara T, et al. Diagnosis and patient management of intraductal papillary mucinous tumor of the pancreas by using peroral pancreatoscopy and intraductal ultrasonography. Gastroenterology. 2002;122:34–43
  112. Fernandez-del Castillo C, Warshaw AL. Cystic tumors of the pancreas. Surgical Clinics of North America. 1995;75:1001–1016
  113. Freeny PC, Weinstein CJ, Taft DA, et al. Cystic neoplasms of the pancreas: new angiographic and ultrasonographic findings. American Journal of Roentgenology. 1978;131:795–802
  114. Scott J, Martin I, Redhead D, et al. Mucinous cystic neoplasms of the pancreas: imaging features and diagnostic difficulties. Clinical Radiology. 2000;53:187–192
  115. Lewandrowski KB, Southern JF, Pins MR, et al. Cyst fluid analysis in the differential diagnosis of pancreatic cysts: a comparison of pseudocysts, serous cystadenomas, mucinous cystic neoplasms, and mucinous cystadenocarcinomas. Annals of Surgery. 1993;217:41–47
  116. Hammel P, Levy P, Voitot H, et al. Preoperative cyst fluid analysis is useful for the differential diagnosis of cystic lesions of the pancreas. Gastroenterology. 1995;108:1230–1235
  117. Recine M, Kaw M, Evans DB, Krishanamurthy S. Fine-needle aspiration cytology of mucinous tumors of the pancreas. Cancer (Cancer Cytopathology). 2004;102:92–99
  118. Curry CA, Eng J, Horton KM, et al. CT of primary cystic pancreatic neoplasms: can CT be used for patient triage and treatment?. American Journal of Roentgenology. 2000;175:99–103
  119. Rhodes I, Humar A, Lum PA, et al. Computed tomographic and cytologic assessment of cystic pancreatic neoplasms: a difficult preoperative diagnosis. Canadian Association of Radiologists Journal. 1993;44:359–363
  120. Mallery JS, Centeno BA, Hahn PF, et al. Pancreatic tissue sampling guided by EUS, CT/US, and surgery: a comparison of sensitivity and specificity. Gastrointestinal Endoscopy. 2002;56:218–224
  121. Maire F, Couvelard A, Hammel P, et al. Intraductal papillary mucinous tumors of the pancreas: the preoperative value of cytologic and histopathologic diagnosis. Gastrointestinal Endoscopy. 2003;58:701–706
  122. Centeno BA, Warshaw AL, Mayo-Smith W, et al. Cytologic diagnosis of pancreatic cystic lesions. A prospective study of 28 percutaneous aspirates. Acta Cytologica. 1997;41:972–980
  123. Fischler DF, Toddy SM. Non-gynecologic cytology utilizing the ThinPrep Processor. Acta Cytologica. 1996;40:669–675
  124. Warshaw AL, Compton CC, Lewandrowski K, et al. Cystic tumors of the pancreas: new clinical, radiologic, and pathologic observations in 67 patients. Annals of Surgery. 1990;212:432–445
  125. Brugge WR, Lauwers G, Sahani D, et al. Cystic neoplasms of the pancreas. New England Journal of Medicine. 2004;351:1218–1226
  126. Uehara H, Nakaizumi A, Iishi H, et al. Cytologic examination of pancreatic juice for differential diagnosis of benign and malignant mucinous mucin-producing tumors of the pancreas. Cancer. 1994;74:826–833
  127. Lee LS, Saltzman JR, Bounds BC, et al. EUS-guided fine needle aspiration of pancreatic cysts: a retrospective analysis of complications and their predictors. Clinical Gastroenterology and Hepatology. 2005;3:231–236
  128. Barbe L, Ponsot P, Vilgrain V, et al. Tumeurs intra-canalaires papillaires mucineuses pancreatiques. Aspects cliniques et morphologiques chez 30 malades. Gastroenterology Clinics of Biology. 1997;21:278–286
  129. Aithal GP, Chen RY, Cunningham JT, et al. Accuracy of EUS for detection of intraductal papillary mucinous tumor of the pancreas. Gastrointestinal Endoscopy. 2002;56:701–707
  130. Thompson LDR, Becker RC, Przygodzki RM, et al. Mucinous cystic neoplasm (mucinous cystadenocarcinoma of low grade malignant potential) of the pancreas. American Journal of Surgical Pathology. 1999;23:1–16
  131. Zamboni G, Scarpa A, Bogina G, et al. Mucinous cystic tumors of the pancreas. American Journal of Surgical Pathology. 1999;23:410–422
  132. Chari ST, Raimondo M, Clain JE, et al. Is benign pancreatic intraductal papillary tumor (IPMT) truly benign?. Gastroenterology. 2000;18(Suppl. 1):A642
  133. Chari ST, Yadav D, Smyrk TC, et al. Study of recurrence after surgical resection of intraductal papillary mucinous neoplasm of the pancreas. Gastroenterology. 2002;123:1500–1507
  134. Sarr MG, Carpenter HA, Prabhakar LP, et al. Clinical and pathologic correlation of 84 mucinous cystic neoplasms of the pancreas—can one reliably differentiate benign from malignant (or premalignant) neoplasms?. Annals of Surgery. 2000;231:205–212
  135. Andea AA, Cheng J, Lauwers GY, et al. Assay in pancreatic intraepithelial neoplasia (PanIn) in pancreata involved by mucinous cystic neoplasm. Modern Pathology. 2002;15:282A
  136. Hruban RH, Adsay NV, Albores-Saavedra J, et al. Pancreatic intraepithelial neoplasia (PanIN): a new nomenclature and classification system for pancreatic duct lesions. American Journal of Surgical Pathology. 2001;25:579–586
  137. Soldini D, Gugger M, Burchkardt E, et al. Progressive genomic alterations in intraductal papillary mucinous tumors of the pancreas and morphologically similar lesions of the pancreatic ducts. Journal of Pathology. 2003;199:453–461
  138. Kogiri M, Tokuhara K, Itoh D, et al. Atypical hyperplasia of the pancreas associated with a stricture of the main pancreatic duct. Journal of Gastroenterology. 2003;38:295–297
  139. Takaori K. Dilemma in classification of possible precursors of pancreatic cancer involving the main pancreatic duct: PanIN or IPMN?. Journal of Gastroenterology. 2003;38:311–313
  140. Takaori K, Matsusue S, Fujikawa T, et al. Carcinoma in situ of the pancreas associated with localized fibrosis: a clue to early detection of neoplastic lesions arising from pancreatic ducts. Pancreas. 1998;17:102–105
  141. Seidel G, Zahurak M, Iacobuzio-Donahue CA, et al. Almost all infiltrating colloid carcinomas of the pancreas and periampullary region arise from in situ papillary neoplasms: a study of 39 cases. American Journal of Surgical Pathology. 2002;26:56–63
  142. Kimura W, Kuroda A, Makuuchi M. Problems in the diagnosis and treatment of a so-called mucin-producing tumor of the pancreas. Pancreas. 1998;16:363–369
  143. Kawai M, Uchiyama K, Tani M, et al. Clinicopathological features of malignant intraductal papillary mucinous tumors of the pancreas. Archives of Surgery. 2004;139:188–192
  144. Yamao K, Ohashi K, Nakamura T, et al. Evaluation of various imaging methods in the differential diagnosis of intraductal papillary mucinous tumor (IPMT) of the pancreas. Hepatogastroenterology. 2001;48:962–966
  145. Sugiyama M, Izumisato Y, Abe N, et al. Predictive factors for malignancy in intraductal papillary-mucinous tumors of the pancreas. British Journal of Surgery. 2003;90:1244–1249
  146. Obara T, Maguchi H, Saitoh Y, et al. Mucin-producing tumor of the pancreas: surgery or follow-up?. Nippon Shokakibyo Gakkai Zasshi. 1994;91:66–74
  147. Sugiyama M, Atomi Y, Kuroda A. Two types of mucin-producing cystic tumors of the pancreas: diagnosis and treatment. Surgery. 1997;122:617–625
  148. Kubo H, Chijiiwa Y, Akahoshi K, et al. Intraductal papillary-mucinous tumors of the pancreas: differential diagnosis between benign and malignant tumors by endoscopic ultrasonography. American Journal of Gastroenterology. 2001;96:1429–1434
  149. Karihara K, Nagai H, Kasahara K, et al. Biliopancreatic fistula associated with intraductal papillary-mucinous pancreatic cancer: institutional experience and review of the literature. Hepatogastroenterology. 2000;47:1164–1167
  150. Tibayan F, Vierra M, Mindelzun B, et al. Clinical presentation of mucin-secreting tumors of the pancreas. American Journal of Surgery. 2000;179:349–351
  151. Taouli B, Vilgrain V, Vullierme MP, et al. Intraductal papillary mucinous tumors of the pancreas: helical CT with histopathological correlation. Radiology. 2000;217:757–764
  152. Bernard P, Scoazec JY, Joubert M, et al. Intraductal papillary-mucinous tumors of the pancreas: predictive criteria of malignancy according to pathologic examination of 53 cases. Archives of Surgery. 2002;137:1274–1278
  153. Nagai E, Ueki T, Chijiwa K, et al. Intraductal papillary mucinous neoplasms of the pancreas associated with the so-called mucinous ductal ectasia: histochemical and immunohistochemical analysis. American Journal of Surgical Pathology. 1995;19:576–589
  154. Falconi M, Salvia R, Bassi C, et al. Clinicopathological features and treatment of intraductal papillary mucinous tumors of the pancreas. British Journal of Surgery. 2001;88:376–381
  155. Delcore R, Thomas JH, Forster J, et al. Characteristics of cystic neoplasms and results of aggressive surgical treatment. American Journal of Surgery. 1992;164:437–442
  156. Le Borgne J, de Calan L, Partensky C. Cystadenomas and cystadenocarcinomas of the pancreas. Annals of Surgery. 1999;230:152–161
  157. de Calan L, Levard H, Hennet H, et al. Pancreatic cystadenoma and cystadenocarcinoma: diagnostic value of preoperative morphological investigations. European Journal of Surgery. 1995;161:35–40
  158. Howard JM. Cystic neoplasms and true cysts of the pancreas. Surgical Clinics of North America. 1989;69:651–665
  159. Yeo CJ, Sarr MG. Cystic and pseudocystic diseases of the pancreas. Current Problems in Surgery. 1994;31:175–243
  160. Sheehan MK, Beck K, Pickleman J, Aranha GV. Spectrum of cystic neoplasms of the pancreas and their surgical management. Archives of Surgery. 2003;138:657–662
  161. Tajiri T, Tate G, Inagaki T, et al. Intraductal tubular neoplasms of the pancreas. Histogenesis and differentiation. Pancreas. 2005;30:115–121
  162. Paye F, Sauvanet A, Terris B, et al. Intraductal papillary mucinous tumors of the pancreas: pancreatic resections guided by preoperative morphological assessment and intraoperative frozen section examination. Surgery. 2000;127:536–544
  163. Obara T, Maguchi H, Saitoh Y, et al. Mucin-producing tumor of the pancreas. American Journal of Gastroenterology. 1993;88:564–569
  164. Wada K, Kozarek RA, Traverso LW. Outcomes following resection of invasive and noninvasive intraductal papillary mucinous neoplasms of the pancreas. American Journal of Surgery. 2005;189:632–637
  165. Adsay NV. Intraductal papillary mucinous neoplasms of the pancreas: pathology and molecular genetics. Journal of Gastrointestinal Surgery. 2002;6:656–659
  166. Kanazumi N, Nakao A, Kaneko T, et al. Surgical treatment of intraductal papillary-mucinous tumors of the pancreas. Hepatogastroenterology. 2001;48:967–971
  167. Maire F, Hammel P, Terris B, et al. Prognosis of malignant intraductal papillary mucinous tumors of the pancreas after surgical resection: comparison with pancreatic ductal adenocarcinoma. Gut. 2002;51:717–722
  168. Sugiura H, Kondo S, Islam HK, et al. Clinicopathological features and outcomes of intraductal papillary mucinous tumors of the pancreas. Hepatogastroenterology. 2002;49:263–267
  169. Yamano K, Ohashi K, Nakamura T, et al. Surgical treatment of intraductal papillary mucinous tumors of the pancreas. Hepatogastroenterology. 2000;47:1129–1134
  170. Raimondo M, Tachibana I, Urrutia R, et al. Invasive cancer and survival of intraductal papillary mucinous tumors of the pancreas. American Journal of Gastroenterology. 2002;97:2553–2558
  171. Fukushima N, Mukai K, Sakamoto M, et al. Invasive carcinoma derived from intraductal papillary-mucinous carcinoma of the pancreas: clinicopathologic and immunohistochemical study of eight cases. Virchows Archiv. 2001;439:6–13
  172. Sohn TA, Yeo CJ, Cameron JL, et al. Resected adenocarcinoma of the pancreas—616 patients: results, outcomes, and prognostic indicators. Journal of Gastrointestinal Surgery. 2000;4:567–579
  173. Cuillerier E, Cellier C, Palazzo L, et al. Outcome after surgical resection of intraductal papillary and mucinous tumors of the pancreas. American Journal of Gastroenterology. 2000;95:441–445
  174. Billings BJ, Christein JD, Harmsen WS, Harrington JR, Chari ST, Que FG, et al. Quality-of-life after total pancreatectomy. Is it really that bad on log-term follow-up?. Journal of Gastrointestinal Surgery. 2005;9:1059–1067
  175. Moriya T, Kimura W, Sakurai F, et al. Minute invasive ductal adenocarcinoma of the residual pancreas after distal pancreatectomy for intraductal papillary mucinous tumors. International Journal of Gastrointestinal Cancer. 2002;31:191–197
  176. Sho M, Nakajima Y, Nakahiro H, et al. Pattern of recurrence after resection for intraductal papillary mucinous tumors of the pancreas. World Journal of Surgery. 1998;22:874–878
  177. Kitagawa Y, Unger TA, Taylor S, et al. Mucus is a predictor of better prognosis and survival in patients with intraductal papillary mucinous tumor of the pancreas. Journal of Gastrointestinal Surgery. 2003;7:12–19

PII: S0960-7404(06)00003-X

doi: 10.1016/j.suronc.2006.01.002

Surgical Oncology
Volume 14, Issue 4 , Pages 155-178 , December 2005