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Differentiation of pancreatic neuroendocrine tumors from pancreas renal cell carcinoma metastases on CT using qualitative and quantitative features

  • Pancreas
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Abstract

Purpose

To assess qualitative and quantitative imaging features on enhanced CT that may differentiate pancreatic neuroendocrine tumors (PNETs) from pancreatic renal cell carcinoma (RCC) metastases.

Methods

This IRB-approved multi-center retrospective case–control study compared 43 resected PNETs and 28 resected RCC metastases with pre-operative enhanced CT identified consecutively between 2003 and 2017. Two blinded radiologists (R1/R2) independently assessed tumor location, attenuation (relative to pancreas), composition (solid/cystic/mixed), homogeneity (homogeneous/heterogeneous), calcification, multiplicity, and for main pancreatic duct (MPD) dilation. Tumors were segmented for quantitative texture analysis. Data were analyzed with Chi square, logistic regression, and receiver operating characteristic (ROC). Inter-observer agreement was assessed (Cohen’s kappa).

Results

There was no difference in age, gender, location, attenuation, or composition (P > 0.05) between groups. PNETs were larger than RCC metastases (37 ± 23 mm vs. 26 ± 21 mm, P = 0.038), more frequently solitary (P < 0.001), subjectively more heterogeneous (P = 0.033/0.144, R1/R2), and associated with calcification (P = 0.002/0.004) and MPD dilation (P = 0.025/0.006). Agreement for subjective features was moderate-to-almost perfect (K = 0.4879–0.9481). Quantitative texture analysis showed higher entropy in PNETs (6.32 ± 0.49 versus 5.96 ± 0.53; P = 0.004) with no difference in other features studied (P > 0.05). Entropy had ROC area under the curve for diagnosis of PNET of 0.77 ± 0.06, with optimal sensitivity/specificity of 71.4/79.1%.

Conclusions

Compared to pancreatic RCC metastases, PNETs are larger, more frequently solitary, contain calcification, show MPD dilation, and are subjectively and quantitatively more heterogeneous tumors.

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Abbreviations

CECT:

Contrast-enhanced CT

DICOM:

Digital imaging and communications in medicine

EUS:

Endoscopic ultrasound

FNA:

Fine needle aspiration

JMRI:

Journal of Magnetic Resonance Imaging

MPD:

Main pancreatic duct

PNET:

Pancreatic neuroendocrine tumor

RCC:

Renal cell carcinoma

ROI:

Region of interest

References

  1. Masetti M, Zanini N, Martuzzi F, et al. (2010) Analysis of prognostic factors in metastatic tumors of the pancreas: a single-center experience and review of the literature. Pancreas 39:135-143

    Article  CAS  PubMed  Google Scholar 

  2. Brufau BP, Cerqueda CS, Villalba LB, et al. (2013) Metastatic renal cell carcinoma: radiologic findings and assessment of response to targeted antiangiogenic therapy by using multidetector CT. Radiographics 33:1691-1716

    Article  PubMed  Google Scholar 

  3. Adsay NV, Andea A, Basturk O, et al. (2004) Secondary tumors of the pancreas: an analysis of a surgical and autopsy database and review of the literature. Virchows Arch 444:527-535

    Article  PubMed  Google Scholar 

  4. Sheth S, Hruban RK, Fishman EK (2002) Helical CT of islet cell tumors of the pancreas: typical and atypical manifestations. AJR Am J Roentgenol 179:725-730

    Article  PubMed  Google Scholar 

  5. Taouli B, Ghouadni M, Correas JM, et al. (2003) Spectrum of abdominal imaging findings in von Hippel-Lindau disease. AJR Am J Roentgenol 181:1049-1054

    Article  PubMed  Google Scholar 

  6. Chrom P, Stec R, Bodnar L, Szczylik C (2018) Prognostic Significance of Pancreatic Metastases from Renal Cell Carcinoma in Patients Treated with Tyrosine Kinase Inhibitors. Anticancer Res 38:359-365

    CAS  PubMed  Google Scholar 

  7. Kassabian A, Stein J, Jabbour N, et al. (2000) Renal cell carcinoma metastatic to the pancreas: a single-institution series and review of the literature. Urology 56:211-215

    Article  CAS  PubMed  Google Scholar 

  8. Sellner F, Tykalsky N, De Santis M, Pont J, Klimpfinger M (2006) Solitary and multiple isolated metastases of clear cell renal carcinoma to the pancreas: an indication for pancreatic surgery. Ann Surg Oncol 13:75-85

    Article  PubMed  Google Scholar 

  9. Kazanjian KK, Reber HA, Hines OJ (2006) Resection of pancreatic neuroendocrine tumors: results of 70 cases. Arch Surg 141:765-769; discussion 769-770

  10. Lee LC, Grant CS, Salomao DR, et al. (2012) Small, nonfunctioning, asymptomatic pancreatic neuroendocrine tumors (PNETs): role for nonoperative management. Surgery 152:965-974

    Article  PubMed  Google Scholar 

  11. Rosenberg AM, Friedmann P, Del Rivero J, Libutti SK, Laird AM (2016) Resection versus expectant management of small incidentally discovered nonfunctional pancreatic neuroendocrine tumors. Surgery 159:302-309

    Article  PubMed  Google Scholar 

  12. Raymond E, Dahan L, Raoul JL, et al. (2011) Sunitinib malate for the treatment of pancreatic neuroendocrine tumors. N Engl J Med 364:501-513

    Article  CAS  PubMed  Google Scholar 

  13. Dutcher JP (2013) Recent developments in the treatment of renal cell carcinoma. Ther Adv Urol 5:338-353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Sperti C, Moletta L, Patane G (2014) Metastatic tumors to the pancreas: the role of surgery. World J Gastrointest Oncol 6:381-392

    Article  PubMed  PubMed Central  Google Scholar 

  15. Bernstein J, Ustun B, Alomari A, et al. (2013) Performance of endoscopic ultrasound-guided fine needle aspiration in diagnosing pancreatic neuroendocrine tumors. Cytojournal 10:10

    Article  PubMed  PubMed Central  Google Scholar 

  16. Ardengh JC, Lopes CV, Kemp R, et al. (2013) Accuracy of endoscopic ultrasound-guided fine-needle aspiration in the suspicion of pancreatic metastases. BMC Gastroenterol 13:63

    Article  PubMed  PubMed Central  Google Scholar 

  17. Pannala R, Hallberg-Wallace KM, Smith AL, et al. (2016) Endoscopic ultrasound-guided fine needle aspiration cytology of metastatic renal cell carcinoma to the pancreas: A multi-center experience. Cytojournal 13:24

    Article  PubMed  PubMed Central  Google Scholar 

  18. Hodgdon T, McInnes MD, Schieda N, et al. (2015) Can Quantitative CT Texture Analysis be Used to Differentiate Fat-poor Renal Angiomyolipoma from Renal Cell Carcinoma on Unenhanced CT Images? Radiology 276:787-796

    Article  PubMed  Google Scholar 

  19. Eilaghi A, Baig S, Zhang Y, et al. (2017) CT texture features are associated with overall survival in pancreatic ductal adenocarcinoma - a quantitative analysis. BMC Med Imaging 17:38

    Article  PubMed  PubMed Central  Google Scholar 

  20. Smith AD, Gray MR, del Campo SM, et al. (2015) Predicting Overall Survival in Patients With Metastatic Melanoma on Antiangiogenic Therapy and RECIST Stable Disease on Initial Posttherapy Images Using CT Texture Analysis. AJR Am J Roentgenol 205:W283-293

    Article  PubMed  Google Scholar 

  21. Schieda N, Thornhill RE, Al-Subhi M, et al. (2015) Diagnosis of Sarcomatoid Renal Cell Carcinoma With CT: Evaluation by Qualitative Imaging Features and Texture Analysis. AJR Am J Roentgenol 204:1013-1023

    Article  PubMed  Google Scholar 

  22. Schieda N, Lim RS, Krishna S, et al. (2018) Diagnostic Accuracy of Unenhanced CT Analysis to Differentiate Low-Grade From High-Grade Chromophobe Renal Cell Carcinoma. AJR Am J Roentgenol 210:1079-1087

    Article  PubMed  Google Scholar 

  23. Canellas R, Burk KS, Parakh A, Sahani DV (2018) Prediction of Pancreatic Neuroendocrine Tumor Grade Based on CT Features and Texture Analysis. AJR Am J Roentgenol 210:341-346

    Article  PubMed  Google Scholar 

  24. Ronkainen H, Soini Y, Vaarala MH, Kauppila S, Hirvikoski P (2010) Evaluation of neuroendocrine markers in renal cell carcinoma. Diagn Pathol 5:28

    Article  PubMed  PubMed Central  Google Scholar 

  25. Tacha D, Qi W, Zhou D, Bremer R, Cheng L (2013) PAX8 mouse monoclonal antibody [BC12] recognizes a restricted epitope and is highly sensitive in renal cell and ovarian cancers but does not cross-react with b cells and tumors of pancreatic origin. Appl Immunohistochem Mol Morphol 21:59-63

    CAS  PubMed  Google Scholar 

  26. Zhang GM, Sun H, Shi B, Jin ZY, Xue HD (2017) Quantitative CT texture analysis for evaluating histologic grade of urothelial carcinoma. Abdom Radiol (NY) 42:561-568

    Article  Google Scholar 

  27. Mammen S, Krishna S, Quon M, et al. (2018) Diagnostic Accuracy of Qualitative and Quantitative Computed Tomography Analysis for Diagnosis of Pathological Grade and Stage in Upper Tract Urothelial Cell Carcinoma. J Comput Assist Tomogr 42:204-210

    PubMed  Google Scholar 

  28. Rasband W (1997-2016) ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA. https://imagej.nih.gov/ij/. Accessed September 1, 2018.

  29. Kang TW, Kim SH, Lee J, et al. (2015) Differentiation between pancreatic metastases from renal cell carcinoma and hypervascular neuroendocrine tumour: Use of relative percentage washout value and its clinical implication. Eur J Radiol 84:2089-2096

    Article  PubMed  Google Scholar 

  30. Choi TW, Kim JH, Yu MH, Park SJ, Han JK (2018) Pancreatic neuroendocrine tumor: prediction of the tumor grade using CT findings and computerized texture analysis. Acta Radiol 59:383-392

    Article  CAS  PubMed  Google Scholar 

  31. Lyu HL, Cao JX, Wang HY et al (2018) Differentiation between pancreatic metastases from clear cell renal cell carcinoma and pancreatic neuroendocrine tumor using double-echo chemical shift imaging. Abdom Radiol (NY). https://doi.org/10.1007/s00261-018-1539-7

  32. Moosavi B, Shabana WM, El-Khodary M, et al. (2016) Intracellular lipid in clear cell renal cell carcinoma tumor thrombus and metastases detected by chemical shift (in and opposed phase) MRI: radiologic-pathologic correlation. Acta Radiol 57:241-248

    Article  PubMed  Google Scholar 

  33. Carrim ZI, Murchison JT (2003) The prevalence of simple renal and hepatic cysts detected by spiral computed tomography. Clin Radiol 58:626-629

    Article  CAS  PubMed  Google Scholar 

  34. Fidler JL, Fletcher JG, Reading CC, et al. (2003) Preoperative detection of pancreatic insulinomas on multiphasic helical CT. AJR Am J Roentgenol 181:775-780

    Article  CAS  PubMed  Google Scholar 

  35. Eelkema EA, Stephens DH, Ward EM, Sheedy PF 2nd (1984) CT features of nonfunctioning islet cell carcinoma. AJR Am J Roentgenol 143:943-948

    Article  CAS  PubMed  Google Scholar 

  36. Kawamoto S, Shi C, Hruban RH, et al. (2011) Small serotonin-producing neuroendocrine tumor of the pancreas associated with pancreatic duct obstruction. AJR Am J Roentgenol 197:W482-488

    Article  PubMed  Google Scholar 

  37. Hofman MS, Lau WF, Hicks RJ (2015) Somatostatin receptor imaging with 68 Ga DOTATATE PET/CT: clinical utility, normal patterns, pearls, and pitfalls in interpretation. Radiographics 35:500-516

    Article  PubMed  Google Scholar 

  38. Freudenberg LS, Gauler T, Gorges R, et al. (2008) Somatostatin receptor scintigraphy in advanced renal cell carcinoma. Results of a phase II-trial of somatostatine analogue therapy in patients with advanced RCC. Nuklearmedizin 47:127-131

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

All authors have no grants, disclosures, or other assistance to acknowledge.

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Authors and Affiliations

  1. Department of Diagnostic Imaging, Juravinski Hospital and Cancer Centre, Hamilton Health Sciences, McMaster University, 711 Concession Street, Hamilton, ON, L8V 1C3, Canada

    Christian B. van der Pol, Stefanie Lee, Scott Tsai & Natasha Larocque

  2. Department of Diagnostic Imaging, The Ottawa Hospital- Civic Campus, 1053 Carling Avenue, Ottawa, ON, K1Y 4E9, Canada

    Abdullah Alayed & Nicola Schieda

  3. Department of Pathology and Molecular Medicine, Juravinski Hospital and Cancer Centre, Hamilton Health Sciences, McMaster University, 711 Concession Street, Rm F1-103, Hamilton, ON, L8V 1C3, Canada

    Phillip Williams

Authors
  1. Christian B. van der Pol
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  2. Stefanie Lee
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  5. Abdullah Alayed
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Correspondence to Christian B. van der Pol.

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Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

This retrospective image review study was approved by the institution review boards with a waiver of informed consent for retrospective image analysis.

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van der Pol, C.B., Lee, S., Tsai, S. et al. Differentiation of pancreatic neuroendocrine tumors from pancreas renal cell carcinoma metastases on CT using qualitative and quantitative features. Abdom Radiol 44, 992–999 (2019). https://doi.org/10.1007/s00261-018-01889-x

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