European Radiology

, Volume 25, Issue 5, pp 1329–1338 | Cite as

Implications of Imaging Criteria for the Management and Treatment of Intraductal Papillary Mucinous Neoplasms – Benign versus Malignant Findings

  • Thula Cannon Walter
  • Ingo G. Steffen
  • Lars H. Stelter
  • Martin H. Maurer
  • Marcus Bahra
  • Wladimir Faber
  • Fritz Klein
  • Hendrik Bläker
  • Bernd Hamm
  • Timm Denecke
  • Christian Grieser
Gastrointestinal

Abstract

Objectives

Evaluation of computed tomography (CT) and magnetic resonance imaging (MRI) for differentiation of pancreatic intraductal papillary mucinous neoplasm (IPMN) subtypes based on objective imaging criteria.

Methods

Fifty-eight patients with 60 histologically confirmed IPMNs were included in this retrospective study. Eighty-three imaging studies (CT,n = 42; MRI,n = 41) were analysed by three independent blinded observers (O1–O3), using established imaging criteria to assess likelihood of malignancy (−5, very likely benign; 5, very likely malignant) and histological subtype (i.e., low-grade (LGD), moderate-grade (MGD), high-grade dysplasia (HGD), early invasive carcinoma (IPMC), solid carcinoma (CA) arising from IPMN).

Results

Forty-one benign (LGD IPMN,n = 20; MGD IPMN,n = 21) and 19 malignant (HGD IPMN,n = 3; IPMC,n = 6; solid CA,n = 10) IPMNs located in the main duct (n = 6), branch duct (n = 37), or both (n = 17) were evaluated. Overall accuracy of differentiation between benign and malignant IPMNs was 86/92 % (CT/MRI). Exclusion of overtly malignant cases (solid CA) resulted in overall accuracy of 83/90 % (CT/MRI). The presence of mural nodules and ductal lesion size ≥30 mm were significant indicators of malignancy (p = 0.02 and p < 0.001, respectively).

Conclusions

Invasive IPMN can be identified with high confidence and sensitivity using CT and MRI. The diagnostic problem that remains is the accurate radiological differentiation of premalignant and non-invasive subtypes.

Key Points

CT and MRI can differentiate benign from malignant forms of IPMN.

Identifying (pre)malignant histological IPMN subtypes by CT and MRI is difficult.

Overall, diagnostic performance with MRI was slightly (not significantly) superior to CT.

Keywords

IPMN CT MRI Pancreatic cancer Intraductal papillary mucinous neoplasm 

Notes

Acknowledgments

The scientific guarantor of this publication is Dr. med. Christian Grieser. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. One of the authors (I. Steffen,) has significant statistical expertise. Institutional Review Board approval was obtained. Written informed consent was waived by the Institutional Review Board. Methodology: retrospective, diagnostic or prognostic study, performed at one institution.

References

  1. 1.
    Girometti R, Intini S, Brondani G et al (2011) Incidental pancreatic cysts on 3D turbo spin echo magnetic resonance cholangiopancreatography: prevalence and relation with clinical and imaging features. Abdom Imaging 36:196–205CrossRefPubMedGoogle Scholar
  2. 2.
    Longnecker D, Adler G, Hruban R et al (2000) Intraductal papillary-mucinous neoplasms of the pancreas. WHO classification of tumors of the digestive system. IARC, Lyon, pp 237–240Google Scholar
  3. 3.
    Castillo CF (2005) Intraductal papillary mucinous neoplasms of the pancreas: a plea for prospective differentiation between main-duct and side-branch tumors. Ann Surg Oncol 12:98–99CrossRefPubMedGoogle Scholar
  4. 4.
    Fernandez-del Castillo C, Targarona J, Thayer SP, Rattner DW, Brugge WR, Warshaw AL (2003) Incidental pancreatic cysts: clinicopathologic characteristics and comparison with symptomatic patients. Arch Surg 138:427–433, discussion 433–434CrossRefPubMedGoogle Scholar
  5. 5.
    Garcea G, Dennison AR (2011) Branch-type intraductal papillary mucinous neoplasms: an update. Pancreatology 11:336–342CrossRefPubMedGoogle Scholar
  6. 6.
    Sawai Y, Yamao K, Bhatia V et al (2010) Development of pancreatic cancers during long-term follow-up of side-branch intraductal papillary mucinous neoplasms. Endoscopy 42:1077–1084CrossRefPubMedGoogle Scholar
  7. 7.
    Uehara H, Ishikawa O, Katayama K et al (2011) Size of mural nodule as an indicator of surgery for branch duct intraductal papillary mucinous neoplasm of the pancreas during follow-up. J Gastroenterol 46:657–663CrossRefPubMedGoogle Scholar
  8. 8.
    Waters JA, Schmidt CM (2008) Intraductal papillary mucinous neoplasm—when to resect? Adv Surg 42:87–108CrossRefPubMedGoogle Scholar
  9. 9.
    Shi C, Hruban RH (2012) Intraductal papillary mucinous neoplasm. Hum Pathol 43:1–16CrossRefPubMedGoogle Scholar
  10. 10.
    Ogawa H, Itoh S, Ikeda M, Suzuki K, Naganawa S (2008) Intraductal papillary mucinous neoplasm of the pancreas: assessment of the likelihood of invasiveness with multisection CT. Radiology 248:876–886CrossRefPubMedGoogle Scholar
  11. 11.
    Schnelldorfer T, Sarr MG, Nagorney DM et al (2008) Experience with 208 resections for intraductal papillary mucinous neoplasm of the pancreas. Arch Surg 143:639–646, discussion 646CrossRefPubMedGoogle Scholar
  12. 12.
    Tanaka M, Chari S, Adsay V et al (2006) International consensus guidelines for management of intraductal papillary mucinous neoplasms and mucinous cystic neoplasms of the pancreas. Pancreatology 6:17–32CrossRefPubMedGoogle Scholar
  13. 13.
    Tanaka M, Fernandez-del Castillo C, Adsay V et al (2012) International consensus guidelines 2012 for the management of IPMN and MCN of the pancreas. Pancreatology 12:183–197CrossRefPubMedGoogle Scholar
  14. 14.
    Waters JA, Schmidt CM, Pinchot JW et al (2008) CT vs MRCP: optimal classification of IPMN type and extent. J Gastrointest Surg 12:101–109CrossRefPubMedGoogle Scholar
  15. 15.
    Zhang J, Wang PJ, Yuan XD (2010) Correlation between CT patterns and pathological classification of intraductal papillary mucinous neoplasm. Eur J Radiol 73:96–101CrossRefPubMedGoogle Scholar
  16. 16.
    Fritz S, Klauss M, Bergmann F et al (2012) Small (Sendai negative) branch-duct IPMNs: not harmless. Ann Surg 256:313–320CrossRefPubMedGoogle Scholar
  17. 17.
    Hardacre JM, McGee MF, Stellato TA, Schulak JA (2007) An aggressive surgical approach is warranted in the management of cystic pancreatic neoplasms. Am J Surg 193:374–378, discussion 378–379CrossRefPubMedGoogle Scholar
  18. 18.
    Kawakubo K, Tada M, Isayama H et al (2013) Risk for mortality from causes other than pancreatic cancer in patients with intraductal papillary mucinous neoplasm of the pancreas. Pancreas 42:687–691CrossRefPubMedGoogle Scholar
  19. 19.
    Okabayashi T, Shima Y, Kosaki T et al (2013) Invasive carcinoma derived from branch duct-type IPMN may be a more aggressive neoplasm than that derived from main duct-type IPMN. Oncol Lett 5:1819–1825PubMedCentralPubMedGoogle Scholar
  20. 20.
    Distler M, Kersting S, Niedergethmann M et al (2013) Pathohistological subtype predicts survival in patients with intraductal papillary mucinous neoplasm (IPMN) of the pancreas. Ann Surg 258:324–330CrossRefPubMedGoogle Scholar
  21. 21.
    Alexander BM, Fernandez-Del Castillo C, Ryan DP et al (2011) Intraductal papillary mucinous adenocarcinoma of the pancreas: clinical outcomes, prognostic factors, and the role of adjuvant therapy. Gastrointest Cancer Res 4:116–121PubMedCentralPubMedGoogle Scholar
  22. 22.
    Koh YX, Chok AY, Zheng HL, Tan CS, Goh BK (2014) Systematic review and meta-analysis comparing the surgical outcomes of invasive intraductal papillary mucinous neoplasms and conventional pancreatic ductal adenocarcinoma. Ann Surg Oncol 21:2782–2800CrossRefPubMedGoogle Scholar
  23. 23.
    Bennett BM (1972) On comparisons of sensitivity, specificity and predictive value of a number of diagnostic procedures. Biometrics 28:793–800CrossRefPubMedGoogle Scholar
  24. 24.
    Arlix A, Bournet B, Otal P et al (2012) Long-term clinical and imaging follow–up of nonoperated branch duct form of intraductal papillary mucinous neoplasms of the pancreas. Pancreas 41:295–301CrossRefPubMedGoogle Scholar
  25. 25.
    Chiu SS, Lim JH, Lee WJ et al (2006) Intraductal papillary mucinous tumour of the pancreas: differentiation of malignancy and benignancy by CT. Clin Radiol 61:776–783CrossRefPubMedGoogle Scholar
  26. 26.
    Fujino Y, Matsumoto I, Ueda T, Toyama H, Kuroda Y (2007) Proposed new score predicting malignancy of intraductal papillary mucinous neoplasms of the pancreas. Am J Surg 194:304–307CrossRefPubMedGoogle Scholar
  27. 27.
    Lafemina J, Katabi N, Klimstra D et al (2013) Malignant progression in IPMN: a cohort analysis of patients initially selected for resection or observation. Ann Surg Oncol 20:440–447CrossRefPubMedGoogle Scholar
  28. 28.
    Okabayashi T, Nishimori I, Nishioka A et al (2008) Long-term effects of multimodal treatment for patients with resectable carcinoma of the pancreas. Oncol Rep 20:651–656PubMedGoogle Scholar
  29. 29.
    White R, D'Angelica M, Katabi N et al (2007) Fate of the remnant pancreas after resection of noninvasive intraductal papillary mucinous neoplasm. J Am Coll Surg 204:987–993, discussion 993–985CrossRefPubMedGoogle Scholar
  30. 30.
    Hwang DW, Jang JY, Lim CS et al (2011) 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 26:740–746CrossRefPubMedCentralPubMedGoogle Scholar
  31. 31.
    Jang JY, Kim SW, Lee SE et al (2008) Treatment guidelines for branch duct type intraductal papillary mucinous neoplasms of the pancreas: when can we operate or observe? Ann Surg Oncol 15:199–205CrossRefPubMedGoogle Scholar
  32. 32.
    Salvia R, Fernandez-del Castillo C, Bassi C et al (2004) Main-duct intraductal papillary mucinous neoplasms of the pancreas: clinical predictors of malignancy and long-term survival following resection. Ann Surg 239:678–685, discussion 685–677CrossRefPubMedCentralPubMedGoogle Scholar
  33. 33.
    Yang AD, Melstrom LG, Bentrem DJ et al (2007) Outcomes after pancreatectomy for intraductal papillary mucinous neoplasms of the pancreas: an institutional experience. Surgery 142:529–534, discussion 534–527CrossRefPubMedGoogle Scholar
  34. 34.
    Werner J, Fritz S, Buchler MW (2012) Intraductal papillary mucinous neoplasms of the pancreas–a surgical disease. Nat Rev Gastroenterol Hepatol 9:253–259CrossRefPubMedGoogle Scholar
  35. 35.
    Kang MJ, Jang JY, Kim SJ et al (2011) Cyst growth rate predicts malignancy in patients with branch duct intraductal papillary mucinous neoplasms. Clin Gastroenterol Hepatol 9:87–93CrossRefPubMedGoogle Scholar
  36. 36.
    Crippa S, Salvia R, Warshaw AL et al (2008) Mucinous cystic neoplasm of the pancreas is not an aggressive entity: lessons from 163 resected patients. Ann Surg 247:571–579CrossRefPubMedCentralPubMedGoogle Scholar
  37. 37.
    Crippa S, Partelli S, Falconi M (2010) Extent of surgical resections for intraductal papillary mucinous neoplasms. World J Gastrointest Surg 2:347–351CrossRefPubMedCentralPubMedGoogle Scholar
  38. 38.
    Nagai K, Doi R, Ito T et al (2009) Single-institution validation of the international consensus guidelines for treatment of branch duct intraductal papillary mucinous neoplasms of the pancreas. J Hepato-Biliary-Pancreat Surg 16:353–358CrossRefGoogle Scholar
  39. 39.
    Sugiyama M, Atomi Y (1998) Intraductal papillary mucinous tumors of the pancreas: imaging studies and treatment strategies. Ann Surg 228:685–691CrossRefPubMedCentralPubMedGoogle Scholar
  40. 40.
    Sugiyama M, Atomi Y, Hachiya J (1998) Intraductal papillary tumors of the pancreas: evaluation with magnetic resonance cholangiopancreatography. Am J Gastroenterol 93:156–159CrossRefPubMedGoogle Scholar
  41. 41.
    Vullierme MP, Giraud-Cohen M, Hammel P et al (2007) Malignant intraductal papillary mucinous neoplasm of the pancreas: in situ versus invasive carcinoma surgical resectability. Radiology 245:483–490CrossRefPubMedGoogle Scholar
  42. 42.
    Choi BS, Kim TK, Kim AY et al (2003) Differential diagnosis of benign and malignant intraductal papillary mucinous tumors of the pancreas: MR cholangiopancreatography and MR angiography. Korean J Radiol 4:157–162CrossRefPubMedCentralPubMedGoogle Scholar
  43. 43.
    Traverso LW, Moriya T, Hashimoto Y (2012) Intraductal papillary mucinous neoplasms of the pancreas: making a disposition using the natural history. Curr Gastroenterol Rep 14:106–111CrossRefPubMedGoogle Scholar
  44. 44.
    Fatima Z, Ichikawa T, Motosugi U et al (2011) Magnetic resonance diffusion-weighted imaging in the characterization of pancreatic mucinous cystic lesions. Clin Radiol 66:108–111CrossRefPubMedGoogle Scholar
  45. 45.
    Kang TW, Kim SH, Park HJ et al (2013) Differentiating xanthogranulomatous cholecystitis from wall-thickening type of gallbladder cancer: added value of diffusion-weighted MRI. Clin Radiol 68:992–1001CrossRefPubMedGoogle Scholar
  46. 46.
    Sandrasegaran K, Akisik FM, Patel AA et al (2011) Diffusion-weighted imaging in characterization of cystic pancreatic lesions. Clin Radiol 66:808–814CrossRefPubMedGoogle Scholar
  47. 47.
    Kang KM, Lee JM, Shin CI et al (2013) Added value of diffusion-weighted imaging to MR cholangiopancreatography with unenhanced mr imaging for predicting malignancy or invasiveness of intraductal papillary mucinous neoplasm of the pancreas. J Magn Reson Imaging 38:555–563CrossRefPubMedGoogle Scholar
  48. 48.
    Ohira G, Kimura K, Ymada N et al (2013) MUC1 and HER2 might be associated with invasive phenotype of intraductal papillary mucinous neoplasm (IPMN). Hepatogastroenterology 60(125):1067–72. doi:  10.5754/hge121268
  49. 49.
    Wu J, Matthaei H, Maitra A et al (2011) Recurrent GNAS mutations define an unexpected pathway for pancreatic cyst development. Sci Transl Med 3:92ra66CrossRefPubMedCentralPubMedGoogle Scholar
  50. 50.
    Pitman MB, Centeno BA, Daglilar ES, Brugge WR, Mino-Kenudson M (2013) Cytological criteria of high-grade epithelial atypia in the cyst fluid of pancreatic intraductal papillary mucinous neoplasms. Cancer Cytopathol. doi: 10.1002/cncy.21344 Google Scholar
  51. 51.
    Pitman MB, Centeno BA, Genevay M, Fonseca R, Mino-Kenudson M (2013) Grading epithelial atypia in endoscopic ultrasound-guided fine-needle aspiration of intraductal papillary mucinous neoplasms: An international interobserver concordance study. Cancer Cytopathol. doi: 10.1002/cncy.21334 Google Scholar
  52. 52.
    Kamphues C, Al-Abadi H, Durr A et al (2013) DNA index as a strong prognostic factor in patients with adenocarcinoma of the pancreatic head: results of a 5-year prospective study. Pancreas 42:807–812CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2014

Authors and Affiliations

  • Thula Cannon Walter
    • 1
  • Ingo G. Steffen
    • 1
  • Lars H. Stelter
    • 1
  • Martin H. Maurer
    • 4
  • Marcus Bahra
    • 2
  • Wladimir Faber
    • 2
  • Fritz Klein
    • 2
  • Hendrik Bläker
    • 3
  • Bernd Hamm
    • 1
  • Timm Denecke
    • 1
  • Christian Grieser
    • 1
  1. 1.Klinik für Radiologie, Campus Virchow-KlinikumCharité – Universitätsmedizin BerlinBerlinGermany
  2. 2.Klinik für Allgemein-, Viszeral- und Transplantationschirurgie Campus Virchow-KlinikumCharité – Universitätsmedizin BerlinBerlinGermany
  3. 3.Institut für Pathologie, Campus Charité MitteCharité – Universitätsmedizin BerlinBerlinGermany
  4. 4.Universitätsinstitut für Radiologe, InselspitalUniversitätsklinik BernBernSchweiz

Personalised recommendations