Skip to main content

Imaging Features for Predicting High-Grade Dysplasia or Malignancy in Branch Duct Type Intraductal Papillary Mucinous Neoplasm of the Pancreas: A Systematic Review and Meta-Analysis

Abstract

Background

The consensus guidelines for branch-duct intraductal papillary mucinous neoplasm (BD-IPMN) of the pancreas are mostly based on imaging features. This study aimed to determine imaging features and their diagnostic accuracy for predicting high-grade dysplasia (HGD)/malignancy in BD-IPMN, including mixed type.

Methods

The PubMed, Embase, and Cochrane databases were searched, and data were extracted from relevant studies. As the main diagnostic accuracy index, diagnostic odds ratios (DORs) of imaging features for diagnosing HGD/malignancy in BD-IPMNs were pooled using the random-effects model. A bivariate random-effects approach was used to construct summary receiver operating characteristic curves for sensitivity and specificity estimation.

Results

The pooled DOR was the highest for the enhanced solid component/mural nodule (MN) (DOR, 12.21; 95 % confidence interval [CI], 6.14–24.27), followed by a main pancreatic duct (MPD) diameter of 10 mm or greater (DOR, 7.93; 95 % CI, 3.02–20.83), solid component (DOR, 4.85; 95 % CI, 2.49–9.42), lymphadenopathy (DOR, 4.84; 95 % CI, 1.11–21.06), MN (DOR, 4.48; 95 % CI, 3.15–6.39), an MPD diameter of 5 mm or greater (DOR, 3.69; 95 % CI, 2.62–5.19), abrupt change in MPD caliber with distal pancreatic atrophy (DOR, 2.65; 95 % CI, 1.66–4.24), thickened/enhancing walls (DOR, 2.38; 95 % CI, 1.57–3.60), and cyst size of 3 cm or larger (DOR, 1.98; 95 % CI, 1.48–2.64). The largest area under the curve (0.89 and 0.95, respectively) and high specificity (0.95 and 0.98, respectively) also were found for enhanced solid component/MN and an MPD diameter of 10 mm or greater, albeit with low sensitivity (0.38 and 0.14, respectively).

Conclusions

The aforementioned imaging features could aid in predicting HGD/malignancy of BD-IPMN. Furthermore, enhanced solid component/MN and an MPD diameter of 10 mm or greater were the most important predictors of HGD/malignancy in BD-IPMN and should be considered as indications for surgery.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. 1.

    de Jong K, Nio CY, Hermans JJ, et al. High prevalence of pancreatic cysts detected by screening magnetic resonance imaging examinations. Clin Gastroenterol Hepatol. 2010;8:806–11.

    PubMed  Article  PubMed Central  Google Scholar 

  2. 2.

    Tanaka M, Fernández-Del Castillo C, Kamisawa T, et al. Revisions of international consensus Fukuoka guidelines for the management of IPMN of the pancreas. Pancreatology. 2017;17:738–53.

    PubMed  Article  PubMed Central  Google Scholar 

  3. 3.

    Vege SS, Ziring B, Jain R, Moayyedi P. Clinical Guidelines Committee; American Gastroenterology Association. American Gastroenterological Association institute guideline on the diagnosis and management of asymptomatic neoplastic pancreatic cysts. Gastroenterology. 2015;148:819–22.

    PubMed  Article  PubMed Central  Google Scholar 

  4. 4.

    European Study Group on Cystic Tumours of the Pancreas. European evidence-based guidelines on pancreatic cystic neoplasms. Gut. 2018;67:789–804.

  5. 5.

    Tanaka M, Chari S, Adsay V, et al. International consensus guidelines for management of intraductal papillary mucinous neoplasms and mucinous cystic neoplasms of the pancreas. Pancreatology. 2006;6:17–32.

    PubMed  Article  PubMed Central  Google Scholar 

  6. 6.

    Tanaka M, Fernández-del Castillo C, Adsay V, et al. International consensus guidelines 2012 for the management of IPMN and MCN of the pancreas. Pancreatology. 2012;12:183–97.

    PubMed  Article  PubMed Central  Google Scholar 

  7. 7.

    Kim KW, Park SH, Pyo J, et al. Imaging features to distinguish malignant and benign branch-duct type intraductal papillary mucinous neoplasms of the pancreas: a meta-analysis. Ann Surg. 2014;259:72–81.

    PubMed  Article  PubMed Central  Google Scholar 

  8. 8.

    Sultana A, Jackson R, Tim G, et al. What is the best way to identify malignant transformation within pancreatic IPMN: a systematic review and meta-analyses. Clin Transl Gastroenterol. 2015;6:e130.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Kwon W, Han Y, Byun Y, et al. Predictive features of malignancy in branch duct type intraductal papillary mucinous neoplasm of the pancreas: a meta-analysis. Cancers Basel. 2020;12:2618.

    CAS  PubMed Central  Article  Google Scholar 

  10. 10.

    Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009;6:e1000100.

    PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155:529–36.

    PubMed  Article  PubMed Central  Google Scholar 

  12. 12.

    Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PM. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol. 2003;56:1129–35.

    PubMed  Article  PubMed Central  Google Scholar 

  13. 13.

    Reitsma JB, Glas AS, Rutjes AW, Scholten RJ, Bossuyt PM, Zwinderman AH. Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol. 2005;58:982–90.

    PubMed  Article  PubMed Central  Google Scholar 

  14. 14.

    Carbognin G, Zamboni G, Pinali L, et al. Branch duct IPMTs: value of cross-sectional imaging in the assessment of biological behavior and follow-up. Abdom Imaging. 2006;31:320–5.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  15. 15.

    Zhang J, Wang PJ, Yuan XD. Correlation between CT patterns and pathological classification of intraductal papillary mucinous neoplasm. Eur J Radiol. 2010;73:96–101.

    PubMed  Article  PubMed Central  Google Scholar 

  16. 16.

    Tan L, Zhao YE, Wang DB, et al. Imaging features of intraductal papillarymucinous neoplasms of the pancreas in multi-detector row computed tomography. World J Gastroenterol. 2009;15:4037–43.

    PubMed  PubMed Central  Article  Google Scholar 

  17. 17.

    Ogawa H, Itoh S, Ikeda M, Suzuki K, Naganawa S. Intraductal papillary mucinous neoplasm of the pancreas: assessment of the likelihood of invasiveness with multisection CT. Radiology. 2008;248:876–86.

    PubMed  Article  PubMed Central  Google Scholar 

  18. 18.

    Woo SM, Ryu JK, Lee SH, Yoon WJ, Kim YT, Yoon YB. Branch duct intraductal papillary mucinous neoplasms in a retrospective series of 190 patients. Br J Surg. 2009;96:405–11.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  19. 19.

    Hirono S, Tani M, Kawai M, et al. Treatment strategy for intraductal papillary mucinous neoplasm of the pancreas based on malignant predictive factors. Arch Surg. 2009;144:345–9.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. 20.

    Tang RS, Weinberg B, Dawson DW, et al. Evaluation of the guidelines for management of pancreatic branch-duct intraductal papillary mucinous neoplasm. Clin Gastroenterol Hepatol. 2008;6:815–9.

    PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    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;40:364–70.

    PubMed  Article  PubMed Central  Google Scholar 

  22. 22.

    Jang JY, Park T, Lee S, et al. Validation of international consensus guidelines for the resection of branch duct-type intraductal papillary mucinous neoplasms. Br J Surg. 2014;101:686–92.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  23. 23.

    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;202:214–9.

    PubMed  Article  PubMed Central  Google Scholar 

  24. 24.

    Arikawa S, Uchida M, Uozumi J, et al. Utility of multidetector row CT in diagnosing branch duct IPMNs of the pancreas compared with MR cholangiopancreatography and endoscopic ultrasonography. Kurume Med J. 2011;57:91–100.

    PubMed  Article  PubMed Central  Google Scholar 

  25. 25.

    Aso T, Ohtsuka T, Matsunaga T, et al. “High-risk stigmata” of the 2012 International Consensus Guidelines correlate with the malignant grade of branch duct intraductal papillary mucinous neoplasms of the pancreas. Pancreas. 2014;43:1239–43.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. 26.

    Attiyeh MA, Fernández-Del Castillo C, Al Efishat M, et al. Development and validation of a multi-institutional preoperative nomogram for predicting grade of dysplasia in intraductal papillary mucinous neoplasms (IPMNs) of the pancreas. Ann Surg. 2018;267:157–63.

    PubMed  Article  PubMed Central  Google Scholar 

  27. 27.

    Chakraborty J, Midya A, Gazit L, et al. CT radiomics to predict high-risk intraductal papillary mucinous neoplasms of the pancreas. Med Phys. 2018;45:5019–29.

    PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Chiu SS, Lim JH, Lee WJ, et al. Intraductal papillary mucinous tumour of the pancreas: differentiation of malignancy and benignancy by CT. Clin Radiol. 2006;61:776–83.

    PubMed  Article  PubMed Central  Google Scholar 

  29. 29.

    Correa-Gallego C, Do R, Lafemina J, et al. Predicting dysplasia and invasive carcinoma in intraductal papillary mucinous neoplasms of the pancreas: development of a preoperative nomogram. Ann Surg Oncol. 2013;20:4348–55.

    PubMed  Article  PubMed Central  Google Scholar 

  30. 30.

    Dortch JD, Stauffer JA, Asbun HJ. Pancreatic resection for side-branch intraductal papillary mucinous neoplasm (SB-IPMN): a contemporary single-institution experience. J Gastrointest Surg. 2015;19:1603–9.

    PubMed  Article  PubMed Central  Google Scholar 

  31. 31.

    Fritz S, Klauss M, Bergmann F, et al. Pancreatic main-duct involvement in branch-duct IPMNs: an underestimated risk. Ann Surg. 2014;260:848–55.

    PubMed  Article  PubMed Central  Google Scholar 

  32. 32.

    Goh BK, Thng CH, Tan DM, et al. Evaluation of the Sendai and 2012 International Consensus Guidelines based on cross-sectional imaging findings performed for the initial triage of mucinous cystic lesions of the pancreas: a single-institution experience with 114 surgically treated patients. Am J Surg. 2014;208:202–9.

    PubMed  Article  PubMed Central  Google Scholar 

  33. 33.

    Hirono S, Tani M, Kawai M, et al. The carcinoembryonic antigen level in pancreatic juice and mural nodule size are predictors of malignancy for branch duct type intraductal papillary mucinous neoplasms of the pancreas. Ann Surg. 2012;255:517–22.

    PubMed  Article  PubMed Central  Google Scholar 

  34. 34.

    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;26:740–6.

    PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

    Jang JY, Kim SW, Lee SE, et al. Treatment guidelines for branch duct type intraductal papillary mucinous neoplasms of the pancreas: when can we operate or observe? Ann Surg Oncol. 2008;15:199–205.

    PubMed  Article  PubMed Central  Google Scholar 

  36. 36.

    Kawaguchi Y, Yasuda K, Cho E, Uno K, Tanaka K, Nakajima M. Differential diagnosis of intraductal papillary-mucinous tumor of the pancreas by endoscopic ultrasonography and intraductal ultrasonography. Dig Endosc. 2004;16:101–6.

    Article  Google Scholar 

  37. 37.

    Kim TH, Song TJ, Hwang JH, et al. Predictors of malignancy in pure branch duct type intraductal papillary mucinous neoplasm of the pancreas: a nationwide multicenter study. Pancreatology. 2015;15:405–10.

    PubMed  Article  PubMed Central  Google Scholar 

  38. 38.

    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. Am J Gastroenterol. 2001;96:1429–34.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  39. 39.

    Liu Y, Lin X, Upadhyaya M, Song Q, Chen K. Intraductal papillary mucinous neoplasms of the pancreas: correlation of helical CT features with pathologic findings. Eur J Radiol. 2010;76:222–7.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  40. 40.

    Mimura T, Masuda A, Matsumoto I, et al. Predictors of malignant intraductal papillary mucinous neoplasm of the pancreas. J Clin Gastroenterol. 2010;44:e224–9.

    PubMed  Article  PubMed Central  Google Scholar 

  41. 41.

    Nagai K, Doi R, Ito T, et al. Single-institution validation of the International Consensus Guidelines for treatment of branch duct intraductal papillary mucinous neoplasms of the pancreas. J Hepatobiliary Pancreat Surg. 2009;16:353–8.

    PubMed  Article  PubMed Central  Google Scholar 

  42. 42.

    Nguyen AH, Toste PA, Farrell JJ, et al. Current recommendations for surveillance and surgery of intraductal papillary mucinous neoplasms may overlook some patients with cancer. J Gastrointest Surg. 2015;19:258–65.

    PubMed  Article  PubMed Central  Google Scholar 

  43. 43.

    Ohtsuka T, Kono H, Nagayoshi Y, et al. An increase in the number of predictive factors augments the likelihood of malignancy in branch duct intraductal papillary mucinous neoplasm of the pancreas. Surgery. 2012;151:76–83.

    PubMed  Article  PubMed Central  Google Scholar 

  44. 44.

    Pelaez-Luna M, Chari ST, Smyrk TC, et al. Do consensus indications for resection in branch duct intraductal papillary mucinous neoplasm predict malignancy? A study of 147 patients. Am J Gastroenterol. 2007;102:1759–64.

    PubMed  Article  PubMed Central  Google Scholar 

  45. 45.

    Ridtitid W, DeWitt JM, Schmidt CM, et al. Management of branch-duct intraductal papillary mucinous neoplasms: a large single-center study to assess predictors of malignancy and long-term outcomes. Gastrointest Endosc. 2016;84:436–45.

    PubMed  Article  PubMed Central  Google Scholar 

  46. 46.

    Robles EP, Maire F, Cros J, et al. Accuracy of 2012 International Consensus Guidelines for the prediction of malignancy of branch-duct intraductal papillary mucinous neoplasms of the pancreas. United Eur Gastroenterol J. 2016;4:580–6.

    Article  Google Scholar 

  47. 47.

    Rodriguez JR, Salvia R, Crippa S, et al. Branch-duct intraductal papillary mucinous neoplasms: observations in 145 patients who underwent resection. Gastroenterology. 2007;133:72–9 (quiz 309–10).

    PubMed  Article  PubMed Central  Google Scholar 

  48. 48.

    Sahora K, Mino-Kenudson M, Brugge W, et al. Branch duct intraductal papillary mucinous neoplasms: does cyst size change the tip of the scale? A critical analysis of the revised International Consensus Guidelines in a large single-institutional series. Ann Surg. 2013;258:466–75.

    PubMed  Article  PubMed Central  Google Scholar 

  49. 49.

    Saito M, Ishihara T, Tada M, et al. Use of F-18 fluorodeoxyglucose positron emission tomography with dual-phase imaging to identify intraductal papillary mucinous neoplasm. Clin Gastroenterol Hepatol. 2013;11:181–6.

    PubMed  Article  PubMed Central  Google Scholar 

  50. 50.

    Salla C, Karvouni E, Nikas I, et al. Imaging and cytopathological criteria indicating malignancy in mucin-producing pancreatic neoplasms: a series of 68 histopathologically confirmed cases. Pancreas. 2018;47:1283–9.

    PubMed  Article  PubMed Central  Google Scholar 

  51. 51.

    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;56:1086–90.

    PubMed  Article  PubMed Central  Google Scholar 

  52. 52.

    Schmidt CM, White PB, Waters JA, et al. Intraductal papillary mucinous neoplasms: predictors of malignant and invasive pathology. Ann Surg. 2007;246:644–51 (discussion 651–4).

    PubMed  Article  PubMed Central  Google Scholar 

  53. 53.

    Seo N, Byun JH, Kim JH, et al. Validation of the 2012 International Consensus Guidelines using computed tomography and magnetic resonance imaging: branch duct and main duct intraductal papillary mucinous neoplasms of the pancreas. Ann Surg. 2016;263:557–64.

    PubMed  Article  PubMed Central  Google Scholar 

  54. 54.

    Serikawa M, Sasaki T, Fujimoto Y, Kuwahara K, Chayama K. Management of intraductal papillary-mucinous neoplasm of the pancreas: treatment strategy based on morphologic classification. J Clin Gastroenterol. 2006;40:856–62.

    PubMed  Article  PubMed Central  Google Scholar 

  55. 55.

    Strauss A, Birdsey M, Fritz S, et al. Intraductal papillary mucinous neoplasms of the pancreas: radiological predictors of malignant transformation and the introduction of bile duct dilation to current guidelines. Br J Radiol. 2016;89:20150853.

    PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    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;90:1244–9.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  57. 57.

    Takeshita K, Kutomi K, Takada K, et al. Differential diagnosis of benign or malignant intraductal papillary mucinous neoplasm of the pancreas by multidetector row helical computed tomography: evaluation of predictive factors by logistic regression analysis. J Comput Assist Tomogr. 2008;32:191–7.

    PubMed  Article  PubMed Central  Google Scholar 

  58. 58.

    Uribarri-González L, Pérez-Cuadrado-Robles E, López-López S, et al. Development of a new risk score for invasive cancer in branch-duct intraductal papillary mucinous neoplasms according to morphological characterization by EUS. Endosc Ultrasound. 2020;9:193–9.

    PubMed  PubMed Central  Google Scholar 

  59. 59.

    Wakabayashi T, Kawaura Y, Morimoto H, et al. Clinical management of intra-ductal papillary mucinous tumors of the pancreas based on imaging findings. Pancreas. 2001;22:370–7.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  60. 60.

    Watanabe Y, Nishihara K, Niina Y, et al. Validity of the management strategy for intraductal papillary mucinous neoplasm advocated by the International Consensus Guidelines 2012: a retrospective review. Surg Today. 2016;46:1045–52.

    PubMed  Article  PubMed Central  Google Scholar 

  61. 61.

    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 high-volume centers. Pancreas. 2013;42:883–8.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  62. 62.

    Marchegiani G, Andrianello S, Borin A, et al. Systematic review, meta-analysis, and a high-volume center experience supporting the new role of mural nodules proposed by the updated 2017 International Guidelines on IPMN of the pancreas. Surgery. 2018;163:1272–9.

    PubMed  Article  PubMed Central  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding authors

Correspondence to Lin Cong MD or Yupei Zhao MD.

Ethics declarations

Disclosure

There are no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zhao, W., Liu, S., Cong, L. et al. Imaging Features for Predicting High-Grade Dysplasia or Malignancy in Branch Duct Type Intraductal Papillary Mucinous Neoplasm of the Pancreas: A Systematic Review and Meta-Analysis. Ann Surg Oncol (2021). https://doi.org/10.1245/s10434-021-10662-2

Download citation