Skip to main content
SpringerLink
Log in

Hepatic neuroendocrine tumour: Apparent diffusion coefficient as a potential marker of prognosis associated with tumour grade and overall survival

  • Gastrointestinal
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To evaluate the correlation between grade of hepatic neuroendocrine tumours (NETs) according to the 2010 World Health Organization (WHO) classification and the apparent diffusion coefficient (ADC) and to assess whether ADC value can predict overall survival (OS) after diagnosis of hepatic NETs.

Methods

The study included 63 patients who underwent magnetic resonance (MR) imaging with diffusion-weighted images for the evaluation of hepatic NETs. The correlation between qualitative and quantitative MR imaging findings, including ADC values, and WHO classifications was assessed. The association between ADC value and OS was analyzed.

Results

The ADC values and WHO classification of hepatic NETs were moderately negatively correlated in a statistically significant manner (ρ = −0.57, p < 0.001). The OS rates were significantly different according to the ADC value (low ADC vs. high ADC, p = 0.006) as well as WHO classifications (G1+ G2 vs. G3, p = 0.038). However, multivariate analysis revealed that the only independent predictor for OS was a low ADC value (hazard ratio: 3.37, p = 0.010).

Conclusion

There was a significant correlation between the ADC value of hepatic NETs and the WHO tumour grade. Additionally, the ADC value of a hepatic NET might be more accurate than the current WHO tumour grade for predicting OS.

Key points

• ADC values of hepatic NET and WHO tumour grade were negatively correlated.

• Lower ADC values of hepatic NET were significantly correlated with worse OS.

• ADC value might be more accurate than WHO grade for predicting OS.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

Abbreviations

ADC:

Apparent diffusion coefficient

CI:

Confidence interval

DWI:

Diffusion-weighted image

HR:

Hazard ratio

MR:

Magnetic resonance

NET:

Neuroendocrine tumour

OS:

Overall survival

PACS:

Picture archiving and communication system

ROI:

Region-of-interest

ROC:

Receiver operating characteristic

WHO:

World Health Organization

References

  1. Klimstra DS, Modlin IR, Coppola D, Lloyd RV, Suster S (2010) The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems. Pancreas 39:707–712

    Article  PubMed  Google Scholar 

  2. Saxena A, Chua TC, Perera M, Chu F, Morris DL (2012) Surgical resection of hepatic metastases from neuroendocrine neoplasms: a systematic review. Surg Oncol 21:e131–e141

    Article  PubMed  Google Scholar 

  3. Cho CS, Labow DM, Tang L et al (2008) Histologic grade is correlated with outcome after resection of hepatic neuroendocrine neoplasms. Cancer 113:126–134

    Article  PubMed  Google Scholar 

  4. Saxena A, Chua TC, Sarkar A et al (2011) Progression and survival results after radical hepatic metastasectomy of indolent advanced neuroendocrine neoplasms (NENs) supports an aggressive surgical approach. Surgery 149:209–220

    Article  PubMed  Google Scholar 

  5. Anlauf M (2011) Neuroendocrine neoplasms of the gastroenteropancreatic system: pathology and classification. Horm Metab Res 43:825–831

    Article  CAS  PubMed  Google Scholar 

  6. Pasaoglu E, Dursun N, Ozyalvacli G, Hacihasanoglu E, Behzatoglu K, Calay O (2015) Comparison of World Health Organization 2000/2004 and World Health Organization 2010 classifications for gastrointestinal and pancreatic neuroendocrine tumors. Ann Diagn Pathol 19:81–87

    Article  PubMed  Google Scholar 

  7. Kloppel G (2011) Classification and pathology of gastroenteropancreatic neuroendocrine neoplasms. Endocr Relat Cancer 18(Suppl 1):S1–16

    Article  PubMed  Google Scholar 

  8. Padhani AR, Liu G, Koh DM et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kim M, Kang TW, Kim YK et al (2016) Pancreatic neuroendocrine tumour: Correlation of apparent diffusion coefficient or WHO classification with recurrence-free survival. Eur J Radiol 85:680–687

    Article  PubMed  Google Scholar 

  10. Jang KM, Kim SH, Lee SJ, Choi D (2014) The value of gadoxetic acid-enhanced and diffusion-weighted MRI for prediction of grading of pancreatic neuroendocrine tumors. Acta Radiol 55:140–148

    Article  PubMed  Google Scholar 

  11. Kim JH, Eun HW, Kim YJ, Han JK, Choi BI (2013) Staging accuracy of MR for pancreatic neuroendocrine tumor and imaging findings according to the tumor grade. Abdom Imaging 38:1106–1114

    Article  PubMed  Google Scholar 

  12. Kang TW, Kim SH, Jang KM et al (2015) Gastrointestinal stromal tumours: correlation of modified NIH risk stratification with diffusion-weighted MR imaging as an imaging biomarker. Eur J Radiol 84:33–40

    Article  PubMed  Google Scholar 

  13. Attenberger UI, Pilz LR, Morelli JN et al (2014) Multi-parametric MRI of rectal cancer - do quantitative functional MR measurements correlate with radiologic and pathologic tumor stages? Eur J Radiol 83:1036–1043

    Article  CAS  PubMed  Google Scholar 

  14. Akashi M, Nakahusa Y, Yakabe T et al (2014) Assessment of aggressiveness of rectal cancer using 3-T MRI: correlation between the apparent diffusion coefficient as a potential imaging biomarker and histologic prognostic factors. Acta Radiol 55:524–531

    Article  PubMed  Google Scholar 

  15. ZH L, CH H, Qian WX, Cao WH (2016) Preoperative diffusion-weighted imaging value of rectal cancer: preoperative T staging and correlations with histological T stage. Clin Imaging 40:563–568

    Article  Google Scholar 

  16. Shankar S, Kalra N, Bhatia A et al (2016) Role of Diffusion Weighted Imaging (DWI) for Hepatocellular Carcinoma (HCC) Detection and its Grading on 3T MRI: A Prospective Study. J Clin Exp Hepatol 6:303–310

    Article  PubMed  PubMed Central  Google Scholar 

  17. Wang LX, Liu K, Lin GW, Jiang T (2015) Primary hepatic neuroendocrine tumors: comparing CT and MRI features with pathology. Cancer Imaging 15:13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Besa C, Ward S, Cui Y, Jajamovich G, Kim M, Taouli B (2016) Neuroendocrine liver metastases: Value of apparent diffusion coefficient and enhancement ratios for characterization of histopathologic grade. J Magn Reson Imaging 44:1432–1441

    Article  PubMed  Google Scholar 

  19. Fenwick SW, Wyatt JI, Toogood GJ, Lodge JP (2004) Hepatic resection and transplantation for primary carcinoid tumors of the liver. Ann Surg 239:210–219

    Article  PubMed  PubMed Central  Google Scholar 

  20. Knox CD, Anderson CD, Lamps LW, Adkins RB, Pinson CW (2003) Long-term survival after resection for primary hepatic carcinoid tumor. Ann Surg Oncol 10:1171–1175

    Article  PubMed  Google Scholar 

  21. Kang TW, Rhim H, Lee J et al (2016) Magnetic resonance imaging with gadoxetic acid for local tumour progression after radiofrequency ablation in patients with hepatocellular carcinoma. Eur Radiol 26:3437–3446

    Article  PubMed  Google Scholar 

  22. Asbach P, Hein PA, Stemmer A et al (2008) Free-breathing echo-planar imaging based diffusion-weighted magnetic resonance imaging of the liver with prospective acquisition correction. J Comput Assist Tomogr 32:372–378

    Article  PubMed  Google Scholar 

  23. Haradome H, Grazioli L, Tsunoo M et al (2010) Can MR fluoroscopic triggering technique and slow rate injection provide appropriate arterial phase images with reducing artifacts on gadoxetic acid-DTPA (Gd-EOB-DTPA)-enhanced hepatic MR imaging? J Magn Reson Imaging 32:334–340

    Article  PubMed  Google Scholar 

  24. Tse JR, Naini BV, DS L, Raman SS (2016) Qualitative and Quantitative Gadoxetic Acid-enhanced MR Imaging Helps Subtype Hepatocellular Adenomas. Radiology 279:118–127

    Article  PubMed  Google Scholar 

  25. Ba-Ssalamah A, Antunes C, Feier D et al (2015) Morphologic and Molecular Features of Hepatocellular Adenoma with Gadoxetic Acid-enhanced MR Imaging. Radiology 277:104–113

    Article  PubMed  Google Scholar 

  26. Merkle EM, Zech CJ, Bartolozzi C et al (2016) Consensus report from the 7th International Forum for Liver Magnetic Resonance Imaging. Eur Radiol 26:674–682

    Article  PubMed  Google Scholar 

  27. Hood L, Friend SH (2011) Predictive, personalized, preventive, participatory (P4) cancer medicine. Nat Rev Clin Oncol 8:184–187

    Article  PubMed  Google Scholar 

  28. Rudin M (2007) Imaging readouts as biomarkers or surrogate parameters for the assessment of therapeutic interventions. Eur Radiol 17:2441–2457

    Article  PubMed  Google Scholar 

  29. Fairweather M, Swanson R, Wang J et al (2017) Management of Neuroendocrine Tumor Liver Metastases: Long-Term Outcomes and Prognostic Factors from a Large Prospective Database. Ann Surg Oncol 24:2319–2325

    Article  PubMed  Google Scholar 

  30. Ramage JK, Ahmed A, Ardill J et al (2012) Guidelines for the management of gastroenteropancreatic neuroendocrine (including carcinoid) tumours (NETs). Gut 61:6–32

    Article  CAS  PubMed  Google Scholar 

  31. Wang H, Cruz-Roa A, Basavanhally A et al (2014) Mitosis detection in breast cancer pathology images by combining handcrafted and convolutional neural network features. J Med Imaging (Bellingham) 1:034003

    Article  Google Scholar 

  32. Adesoye T, Daleo MA, Loeffler AG, Winslow ER, Weber SM, Cho CS (2015) Discordance of Histologic Grade Between Primary and Metastatic Neuroendocrine Carcinomas. Ann Surg Oncol 22(Suppl 3):S817–S821

    Article  PubMed  PubMed Central  Google Scholar 

  33. Janson ET, Holmberg L, Stridsberg M et al (1997) Carcinoid tumors: analysis of prognostic factors and survival in 301 patients from a referral center. Ann Oncol 8:685–690

    Article  CAS  PubMed  Google Scholar 

  34. Shen YH, Chen S, Zhang WT et al (2014) Clinical analysis of gastroenteropancreatic neuroendocrine tumor with liver metastasis, compared with primary hepatic neuroendocrine tumor. J Cancer Res Ther 10(Suppl):276–280

    PubMed  Google Scholar 

  35. Yang Z, Tang LH, Klimstra DS (2011) Effect of tumor heterogeneity on the assessment of Ki67 labeling index in well-differentiated neuroendocrine tumors metastatic to the liver: implications for prognostic stratification. Am J Surg Pathol 35:853–860

    Article  PubMed  Google Scholar 

Download references

Funding

The authors state that this work has not received any funding.

Author information

Authors and Affiliations

  1. Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Irwon-Dong, Gangnam-gu, Seoul, 135-710, Korea

    Ji Hye Min, Tae Wook Kang, Young Kon Kim & Seong Hyun Kim

  2. Department of Radiology, Chungnam National University Hospital, Chungnam National University College of Medicine, Daejeon, Republic of Korea

    Ji Hye Min, Kyung Sook Shin & Jeong Eun Lee

  3. Department of Pathology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea

    Sang Yun Ha

  4. Biostatics and Clinical Epidemiology Center, Samsung Medical Center, Seoul, Republic of Korea

    Insuk Sohn

Authors
  1. Ji Hye Min
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tae Wook Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Young Kon Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Seong Hyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kyung Sook Shin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jeong Eun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sang Yun Ha
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Insuk Sohn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tae Wook Kang.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Won Jae Lee.

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

One of the authors (Insuk Sohn) has significant statistical expertise.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• Retrospective

• Case-control

• Performed at one institution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Min, J.H., Kang, T.W., Kim, Y.K. et al. Hepatic neuroendocrine tumour: Apparent diffusion coefficient as a potential marker of prognosis associated with tumour grade and overall survival. Eur Radiol 28, 2561–2571 (2018). https://doi.org/10.1007/s00330-017-5248-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-017-5248-3

Keywords

Search

Navigation