Skip to main content
Log in

Quantitative analysis of enhanced CT in differentiating well-differentiated pancreatic neuroendocrine tumors and poorly differentiated neuroendocrine carcinomas

  • Hepatobiliary-Pancreas
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objective

To identify quantitative CT features for distinguishing well-differentiated pancreatic neuroendocrine tumors (PNETs) from poorly differentiated pancreatic neuroendocrine carcinomas (PNECs).

Materials and methods

Seventeen patients with PNECs and 131 patients with PNETs confirmed by biopsy or surgery were retrospectively included. General demographic (sex, age) and CT quantitative parameters (arterial/portal absolute enhancement, arterial/portal relative enhancement ratio, arterial/portal enhancement ratio) were collected. Univariate and multivariate logistic regression analyses were performed to confirm independent variables for differentiating PNECs from PNETs. Receiver operating characteristic (ROC) curves for each quantitative parameter were generated to determine their diagnostic ability.

Results

PNECs had a much lower mean arterial/portal absolute enhancement value (19.5 ± 11.0 vs. 78.8 ± 47.2; 28.1 ± 15.8 vs. 77.0 ± 39.4), arterial/portal relative enhancement ratio (0.57 ± 0.36 vs. 2.03 ± 1.31; 0.80 ± 0.52 vs. 1.99 ± 1.13), and arterial/portal enhancement ratio (0.62 ± 0.27 vs. 1.22 ± 0.49; 0.74 ± 0.19 vs. 1.21 ± 0.36) than PNETs (all p < 0.001). After multivariable analysis, arterial absolute enhancement (odds ratio [OR]: 0.96, 95% confidence interval [CI]: 0.93, 0.99) and portal absolute enhancement (OR: 0.96, 95% CI: 0.92, 0.99) were independent factors for differentiating PNECs from PNETs. For each quantitative parameter, arterial lesion enhancement yielded the highest diagnostic performance, with an area under the curve (AUC) of 0.922 (95% CI: 0.867–0.960), followed by portal absolute enhancement.

Conclusions

Arterial/portal absolute enhancements were independent predictors with good diagnostic accuracy for differentiating between PNETs and PNECs. Quantitative parameters of enhanced CT can distinguish PNECs from PNETs.

Key Points

• PNECs were hypovascular and had a much lower enhanced CT attenuation in both arterial and portal phases than well-differentiated PNETs.

• Quantitative parameters derived from enhanced CT can be used to distinguish PNECs from PNETs.

• Arterial absolute enhancement and portal absolute enhancement were independent predictive factors for differentiating between PNETs and PNECs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AUC:

Area under the curve

CI:

Confidence interval

G1:

Grade 1

G2:

Grade 2

G3:

Grade 3

HPF:

High-power fields

HU:

Hounsfield unit

ICC:

Intraclass correlation coefficient

NENs:

Neuroendocrine neoplasms

OR:

Odds ratio

PanNENs:

Pancreatic neuroendocrine neoplasms

PNECs:

Pancreatic neuroendocrine carcinomas

PNETs:

Pancreatic neuroendocrine tumors

ROC:

Receiver operating characteristic

ROI:

Region of interest

References

  1. Ma ZY, Gong YF, Zhuang HK et al (2020) Pancreatic neuroendocrine tumors: a review of serum biomarkers, staging, and management. World J Gastroenterol 26:2305–2322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Cives M, Strosberg JR (2018) Gastroenteropancreatic neuroendocrine tumors. CA Cancer J Clin 68:471–487

    Article  PubMed  Google Scholar 

  3. Choe J, Kim KW, Kim HJ et al (2019) What is new in the 2017 World Health Organization classification and 8th American Joint Committee on Cancer Staging System for pancreatic neuroendocrine neoplasms? Korean J Radiol 20:5–17

    Article  PubMed  Google Scholar 

  4. Bosman F, Carneiro F, Hruban RH, Theise ND (2010) World Health Organization classification of tumours of the digestive system. IARC Press, Lyon, France, pp 13–14

    Google Scholar 

  5. Perren A, Couvelard A, Scoazec JY et al (2017) ENETS consensus guidelines for the standards of care in neuroendocrine tumors: pathology: diagnosis and prognostic stratification. Neuroendocrinology 105:196–200

    Article  CAS  PubMed  Google Scholar 

  6. Lloyd RV, Osamura RY, Kloppel G, Rosai J (2017) WHO classification of tumours of endocrine organs. WHO/ IARC Classification of Tumours. 4th ed. Vol 10. IARC Press, Lyon, France

    Google Scholar 

  7. Kim JY, Hong SM, Ro JY (2017) Recent updates on grading and classification of neuroendocrine tumors. Ann Diagn Pathol 29:11–16

    Article  PubMed  Google Scholar 

  8. Luo G, Javed A, Strosberg JR et al (2017) Modified staging classification for pancreatic neuroendocrine tumors on the basis of the American Joint Committee on Cancer and European Neuroendocrine Tumor Society Systems. J Clin Oncol 35:274–280

    Article  PubMed  Google Scholar 

  9. Guilmette JM, Nosé V (2019) Neoplasms of the neuroendocrine pancreas: an update in the classification, definition, and molecular genetic advances. Adv Anat Pathol 26:13–30

    Article  CAS  PubMed  Google Scholar 

  10. Yang B, Chen HY, Zhang XY, Pan Y, Lu YF, Yu RS (2020) The prognostic value of multidetector CT features in predicting overall survival outcomes in patients with pancreatic neuroendocrine tumors. Eur J Radiol 124:108847

    Article  PubMed  Google Scholar 

  11. Kim JH, Eun HW, Kim YJ, Lee JM, Han JK, Choi BI (2016) Pancreatic neuroendocrine tumour (PNET): staging accuracy of MDCT and its diagnostic performance for the differentiation of PNET with uncommon CT findings from pancreatic adenocarcinoma. Eur Radiol 26:1338–1347

    Article  PubMed  Google Scholar 

  12. Kim DW, Kim HJ, Kim KW et al (2015) Neuroendocrine neoplasms of the pancreas at dynamic enhanced CT: comparison between grade 3 neuroendocrine carcinoma and grade 1/2 neuroendocrine tumour. Eur Radiol 25:1375–1383

    Article  PubMed  Google Scholar 

  13. Karmazanovsky G, Belousova E, Schima W, Glotov A, Kalinin D, Kriger A (2019) Nonhypervascular pancreatic neuroendocrine tumors: spectrum of MDCT imaging findings and differentiation from pancreatic ductal adenocarcinoma. Eur J Radiol 110:66–73

    Article  PubMed  Google Scholar 

  14. Park HJ, Kim HJ, Kim KW et al (2020) Comparison between neuroendocrine carcinomas and well-differentiated neuroendocrine tumors of the pancreas using dynamic enhanced CT. Eur Radiol 30:4772–4782

    Article  PubMed  Google Scholar 

  15. Nagayama Y, Inoue T, Kato Y et al (2021) Relative enhancement ratio of portal venous phase to unenhanced CT in the diagnosis of lipid-poor adrenal adenomas. Radiology 301:360–368

    Article  PubMed  Google Scholar 

  16. Kim DW, Kim HJ, Kim KW et al (2016) Prognostic value of CT findings to predict survival outcomes in patients with pancreatic neuroendocrine neoplasms: a single institutional study of 161 patients. Eur Radiol 26:1320–1329

    Article  PubMed  Google Scholar 

  17. Chen H-Y, Deng X-Y, Pan Y et al (2021) Pancreatic serous cystic neoplasms and mucinous cystic neoplasms: differential diagnosis by combining imaging features and enhanced CT texture analysis. Front Oncol 11:745001

    Article  PubMed  PubMed Central  Google Scholar 

  18. Fang JM, Shi J (2019) A clinicopathologic and molecular update of pancreatic neuroendocrine neoplasms with a focus on the new World Health Organization classification. Arch Pathol Lab Med 143:1317–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lam AK, Ishida H (2021) Pancreatic neuroendocrine neoplasms: clinicopathological features and pathological staging. Histol Histopathol 36:367–382

    CAS  PubMed  Google Scholar 

  20. Chen H-Y, Zhang X-Y, Deng X-Y et al (2020) Grade 3 pancreatic neuroendocrine tumors on MDCT: establishing a diagnostic model and comparing survival against pancreatic ductal adenocarcinoma. AJR Am J Roentgenol 215:1–8

  21. Bian Y, Jiang H, Ma C et al (2020) CT-based radiomics score for distinguishing between grade 1 and grade 2 nonfunctioning pancreatic neuroendocrine tumors. AJR Am J Roentgenol 215:852–863

  22. Azoulay A, Cros J, Vullierme MP et al (2020) Morphological imaging and CT histogram analysis to differentiate pancreatic neuroendocrine tumor grade 3 from neuroendocrine carcinoma. Diagn Interv Imaging 101:821–830

    Article  CAS  PubMed  Google Scholar 

  23. Xue Y, Reid MD, Pehlivanoglu B et al (2020) Morphologic variants of pancreatic neuroendocrine tumors: clinicopathologic analysis and prognostic stratification. Endocr Pathol 31:239–253

    Article  CAS  PubMed  Google Scholar 

  24. Singhi AD, Klimstra DS (2018) Well-differentiated pancreatic neuroendocrine tumours (PanNETs) and poorly differentiated pancreatic neuroendocrine carcinomas (PanNECs): concepts, issues and a practical diagnostic approach to high-grade (G3) cases. Histopathology 72:168–177

    Article  PubMed  Google Scholar 

  25. Ro C, Chai W, Yu VE, Yu R (2013) Pancreatic neuroendocrine tumors: biology, diagnosis,and treatment. Chin J Cancer 32:312–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Liang W, Yang P, Huang R et al (2019) A combined nomogram model to preoperatively predict histologic grade in pancreatic neuroendocrine tumors. Clin Cancer Res 25:584–594

    Article  PubMed  Google Scholar 

  27. Loi S, Mori M, Benedetti G et al (2020) Robustness of CT radiomic features against image discretization and interpolation in characterizing pancreatic neuroendocrine neoplasms. Phys Med 76:125–133

    Article  PubMed  Google Scholar 

Download references

Funding

This study was supported by funding from the National Natural Science Foundation of China (82072032), Major Medical and Health Science and Technology Projects in Zhejiang Province (WKJ-ZJ-2002), and Key R&D Projects in Zhejiang Province (2019C03058).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ri-Sheng Yu or Guo-Liang Shao.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Guo-Liang Shao.

Conflict of interest

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.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• observational

• multicenter study

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, HY., Pan, Y., Chen, JY. et al. Quantitative analysis of enhanced CT in differentiating well-differentiated pancreatic neuroendocrine tumors and poorly differentiated neuroendocrine carcinomas. Eur Radiol 32, 8317–8325 (2022). https://doi.org/10.1007/s00330-022-08891-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-022-08891-4

Keywords

Navigation