Skip to main content
SpringerLink
Log in

Accuracy of apparent diffusion coefficient in differentiating pancreatic neuroendocrine tumour from intrapancreatic accessory spleen

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

Abstract

Objectives

To evaluate and compare the accuracy of absolute apparent diffusion coefficient (ADC) and normalised ADC (lesion-to-spleen ADC ratio) in differentiating pancreatic neuroendocrine tumour (NET) from intrapancreatic accessory spleen (IPAS).

Methods

Study included 62 patients with the diagnosis of pancreatic NET (n=51) or IPAS (n=11). Two independent reviewers measured ADC on all lesions and spleen. Receiver operating characteristics (ROC) analysis to differentiate NET from IPAS was performed and compared for absolute and normalised ADC. Inter-reader reliability for the two methods was assessed.

Results

Pancreatic NET had significantly higher absolute ADC (1.431x10-3 vs 0.967x10-3 mm2/s; P<0.0001) and normalised ADC (1.59 vs 1.09; P<0.0001) compared to IPAS. An ADC value of ≥1.206x10-3 mm2/s was 70.6% sensitive and 90.9% specific for the diagnosis of NET vs. IPAS. Lesion to spleen ADC ratio of ≥1.25 was 80.4% sensitive, and 81.8% specific while ratio of ≥1.29 was 74.5% sensitive and 100% specific in the differentiation. The area under the curve (AUCs) for two methods were similar (88.2% vs. 88.8%; P=0.899). Both methods demonstrated excellent inter-reader reliability with ICCs for absolute ADC and ADC ratio being 0.957 and 0.927, respectively.

Conclusion

Both absolute and normalised ADC allow clinically relevant differentiation of pancreatic NET and IPAS.

Key points

• Imaging overlaps between IPASs and pancreatic-NETs lead to unnecessary procedures including pancreatectomy.

• Uniquely low ADC of spleen allows differentiating IPASs from pancreatic NETs.

• Both absolute-ADC and normalised-ADC (lesion-to-spleen ADC-ratio) demonstrate high accuracy in differentiating IPASs from NETs.

• Both methods demonstrate excellent inter-reader reliability.

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

Similar content being viewed by others

Abbreviations

ADC:

apparent diffusion coefficient

AUC:

area under the curve

CE:

contrast enhanced

CI:

confidence interval

DWI:

diffusion-weighted imaging

EUS-FNA:

endoscopic ultrasound guided fine needle aspiration

ICC:

intra-class correlation coefficient

IPAS:

intrapancreatic accessory spleen

MRI:

magnetic resonance imaging

NET:

neuroendocrine tumour

PanNET:

pancreatic neuroendocrine tumour

ROC:

receiver operating characteristics

ROI:

region of interest

SD:

standard deviation

SPECT:

single-photon emission computed tomography

References

  1. Halpert B, Gyorkey F (1959) Lesions observed in accessory spleens of 311 patients. Am J Clin Pathol 32(2):165–168

    Article  CAS  PubMed  Google Scholar 

  2. Hwang HS, Lee SS, Kim SC, Seo DW, Kim J (2011) Intrapancreatic accessory spleen: clinicopathologic analysis of 12 cases. Pancreas 40(6):956–965

    Article  PubMed  Google Scholar 

  3. Halpert B, Alden ZA (1964) Accessory Spleens in or at the Tail of the Pancreas. A Survey of 2,700 Additional Necropsies. Arch Pathol 77:652–654

    CAS  PubMed  Google Scholar 

  4. Spencer LA, Spizarny DL, Williams TR (2010) Imaging features of intrapancreatic accessory spleen. Br J Radiol 83(992):668–673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Uchiyama S, Chijiiwa K, Hiyoshi M, Ohuchida J, Imamura N, Nagano M et al (2008) Intrapancreatic accessory spleen mimicking endocrine tumor of the pancreas: case report and review of the literature. J Gastrointest Surg 12(8):1471–1473

    Article  PubMed  Google Scholar 

  6. Arkadopoulos N, Athanasopoulos P, Stafyla V, Karakatsanis A, Koutoulidis V, Theodosopoulos T et al (2009) Intrapancreatic accessory spleen issues: diagnostic and therapeutic challenges. JOP 10(4):400–405

    PubMed  Google Scholar 

  7. Kim SH, Lee JM, Han JK, Lee JY, Kim KW, Cho KC et al (2008) Intrapancreatic accessory spleen: findings on MR Imaging, CT, US and scintigraphy, and the pathologic analysis. Korean J Radiol 9(2):162–174

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kazanjian KK, Reber HA, Hines OJ (2006) Resection of pancreatic neuroendocrine tumors: results of 70 cases. Arch Surg 141(8):765–769 discussion 9-70

    Article  PubMed  Google Scholar 

  9. Toure L, Bedard J, Sawan B, Mosimann F (2010) Case note: intrapancreatic accessory spleen mimicking a pancreatic endocrine tumour. Can J Surg 53(1):E1–E2

    PubMed  PubMed Central  Google Scholar 

  10. Meyer-Rochow GY, Gifford AJ, Samra JS, Sywak MS (2007) Intrapancreatic splenunculus. Am J Surg 194(1):75–76

    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(5):1338–1347

    Article  PubMed  Google Scholar 

  12. Kim SH, Lee JM, Han JK, Lee JY, Kang WJ, Jang JY et al (2006) MDCT and superparamagnetic iron oxide (SPIO)-enhanced MR findings of intrapancreatic accessory spleen in seven patients. Eur Radiol 16(9):1887–1897

    Article  PubMed  Google Scholar 

  13. Heredia V, Altun E, Bilaj F, Ramalho M, Hyslop BW, Semelka RC (2008) Gadolinium- and superparamagnetic-iron-oxide-enhanced MR findings of intrapancreatic accessory spleen in five patients. Magn Reson Imaging 26(9):1273–1278

    Article  CAS  PubMed  Google Scholar 

  14. Ota T, Tei M, Yoshioka A, Mizuno M, Watanabe S, Seki M et al (1997) Intrapancreatic accessory spleen diagnosed by technetium-99m heat-damaged red blood cell SPECT. J Nucl Med 38(3):494–495

    CAS  PubMed  Google Scholar 

  15. Anaye A, Mathieu A, Closset J, Bali MA, Metens T, Matos C (2009) Successful preoperative localization of a small pancreatic insulinoma by diffusion-weighted MRI. JOP 10(5):528–531

    PubMed  Google Scholar 

  16. Matsuki M, Inada Y, Nakai G, Tatsugami F, Tanikake M, Narabayashi I et al (2007) Diffusion-weighed MR imaging of pancreatic carcinoma. Abdom Imaging 32(4):481–483

    Article  CAS  PubMed  Google Scholar 

  17. Kartalis N, Lindholm TL, Aspelin P, Permert J, Albiin N (2009) Diffusion-weighted magnetic resonance imaging of pancreas tumours. Eur Radiol 19(8):1981–1990

    Article  PubMed  Google Scholar 

  18. Lee SS, Byun JH, Park BJ, Park SH, Kim N, Park B et al (2008) Quantitative analysis of diffusion-weighted magnetic resonance imaging of the pancreas: usefulness in characterizing solid pancreatic masses. J Magn Reson Imaging 28(4):928–936

    Article  PubMed  Google Scholar 

  19. Lotfalizadeh E, Ronot M, Wagner M, Cros J, Couvelard A, Vullierme MP et al (2017) Prediction of pancreatic neuroendocrine tumour grade with MR imaging features: added value of diffusion-weighted imaging. Eur Radiol 27(4):1748–1759

    Article  PubMed  Google Scholar 

  20. Park HS, Kim SY, Hong SM, Park SH, Lee SS, Byun JH et al (2016) Hypervascular solid-appearing serous cystic neoplasms of the pancreas: Differential diagnosis with neuroendocrine tumours. Eur Radiol 26(5):1348–1358

    Article  PubMed  Google Scholar 

  21. Le Bihan D, Turner R, Douek P, Patronas N (1992) Diffusion MR imaging: clinical applications. AJR Am J Roentgenol 159(3):591–599

    Article  PubMed  Google Scholar 

  22. Corona-Villalobos CP, Pan L, Halappa VG, Bonekamp S, Lorenz CH, Eng J et al (2013) Agreement and reproducibility of apparent diffusion coefficient measurements of dual-b-value and multi-b-value diffusion-weighted magnetic resonance imaging at 1.5 Tesla in phantom and in soft tissues of the abdomen. J Comput Assist Tomogr 37(1):46–51

    Article  PubMed  Google Scholar 

  23. Yoshikawa T, Kawamitsu H, Mitchell DG, Ohno Y, Ku Y, Seo Y et al (2006) ADC measurement of abdominal organs and lesions using parallel imaging technique. AJR Am J Roentgenol 187(6):1521–1530

    Article  PubMed  Google Scholar 

  24. Jang KM, Kim SH, Lee SJ, Park MJ, Lee MH, Choi D (2013) Differentiation of an intrapancreatic accessory spleen from a small (<3-cm) solid pancreatic tumor: value of diffusion-weighted MR imaging. Radiology 266(1):159–167

    Article  PubMed  Google Scholar 

  25. Kang BK, Kim JH, Byun JH, Lee SS, Kim HJ, Kim SY et al (2014) Diffusion-weighted MRI: usefulness for differentiating intrapancreatic accessory spleen and small hypervascular neuroendocrine tumor of the pancreas. Acta Radiol 55(10):1157–1165

    Article  PubMed  Google Scholar 

  26. Zhu J, Zhang J, Gao JY, Li JN, Yang DW, Chen M et al (2017) Apparent diffusion coefficient normalization of normal liver: Will it improve the reproducibility of diffusion-weighted imaging at different MR scanners as a new biomarker? Medicine (Baltimore) 96(3):e5910

    Article  Google Scholar 

  27. Grech-Sollars M, Hales PW, Miyazaki K, Raschke F, Rodriguez D, Wilson M et al (2015) Multi-centre reproducibility of diffusion MRI parameters for clinical sequences in the brain. NMR Biomed 28(4):468–485

    Article  PubMed  PubMed Central  Google Scholar 

  28. Ye XH, Gao JY, Yang ZH, Liu Y (2014) Apparent diffusion coefficient reproducibility of the pancreas measured at different MR scanners using diffusion-weighted imaging. J Magn Reson Imaging 40(6):1375–1381

    Article  PubMed  Google Scholar 

  29. Barral M, Sebbag-Sfez D, Hoeffel C, Chaput U, Dohan A, Eveno C et al (2013) Characterization of focal pancreatic lesions using normalized apparent diffusion coefficient at 1.5-Tesla: preliminary experience. Diagn Interv Imaging 94(6):619–627

    Article  CAS  PubMed  Google Scholar 

  30. Do RK, Chandarana H, Felker E, Hajdu CH, Babb JS, Kim D et al (2010) Diagnosis of liver fibrosis and cirrhosis with diffusion-weighted imaging: value of normalized apparent diffusion coefficient using the spleen as reference organ. AJR Am J Roentgenol 195(3):671–676

    Article  PubMed  Google Scholar 

  31. DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44(3):837–845

    Article  CAS  PubMed  Google Scholar 

  32. DV C. Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. . Psychol Assess 1994;6(4):284–290.

  33. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33(1):159–174

    Article  CAS  PubMed  Google Scholar 

  34. Gimi B, Cederberg K, Derinkuyu B, Gargan L, Koral KM, Bowers DC et al (2012) Utility of apparent diffusion coefficient ratios in distinguishing common pediatric cerebellar tumors. Acad Radiol 19(7):794–800

    Article  PubMed  Google Scholar 

  35. Braithwaite AC, Dale BM, Boll DT, Merkle EM (2009) Short- and midterm reproducibility of apparent diffusion coefficient measurements at 3.0-T diffusion-weighted imaging of the abdomen. Radiology 250(2):459–465

    Article  PubMed  Google Scholar 

  36. Papanikolaou N, Gourtsoyianni S, Yarmenitis S, Maris T, Gourtsoyiannis N (2010) Comparison between two-point and four-point methods for quantification of apparent diffusion coefficient of normal liver parenchyma and focal lesions. Value of normalization with spleen. Eur J Radiol 73(2):305–309

    Article  PubMed  Google Scholar 

Download references

Funding

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

Author information

Authors and Affiliations

  1. Russell H. Morgan Department of Radiology and Radiological Sciences, Johns Hopkins University School of Medicine, 600 N Wolfe St, Room 143, Baltimore, MD, 21287, USA

    Ankur Pandey, Pallavi Pandey, Mounes Aliyari Ghasabeh, Farnaz Najmi Varzaneh, Pegah Khoshpouri, Nannan Shao, Manijeh Zargham Pour, Daniel Fadaei Fouladi & Ihab R. Kamel

  2. Department of Pathology, Johns Hopkins Medical Institutions, 1550 Orleans Street, Baltimore, MD, 21231, USA

    Ralph H. Hruban

  3. Division of Gastroenterology and Hepatology, Johns Hopkins Medical Institutions, Baltimore, MD, USA

    Anne Marie O’Broin-Lennon

Authors
  1. Ankur Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pallavi Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mounes Aliyari Ghasabeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Farnaz Najmi Varzaneh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pegah Khoshpouri
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nannan Shao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Manijeh Zargham Pour
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Daniel Fadaei Fouladi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ralph H. Hruban
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Anne Marie O’Broin-Lennon
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ihab R. Kamel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ihab R. Kamel.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Ihab R Kamel.

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

• diagnostic study

• 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

Pandey, A., Pandey, P., Ghasabeh, M.A. et al. Accuracy of apparent diffusion coefficient in differentiating pancreatic neuroendocrine tumour from intrapancreatic accessory spleen. Eur Radiol 28, 1560–1567 (2018). https://doi.org/10.1007/s00330-017-5122-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-017-5122-3

Keywords

Search

Navigation