Skip to main content
Top
Published in: European Radiology 4/2018

01-04-2018 | Hepatobiliary-Pancreas

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

Authors: Ankur Pandey, Pallavi Pandey, Mounes Aliyari Ghasabeh, Farnaz Najmi Varzaneh, Pegah Khoshpouri, Nannan Shao, Manijeh Zargham Pour, Daniel Fadaei Fouladi, Ralph H. Hruban, Anne Marie O’Broin-Lennon, Ihab R. Kamel

Published in: European Radiology | Issue 4/2018

Login to get access

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.
Literature
1.
go back to reference Halpert B, Gyorkey F (1959) Lesions observed in accessory spleens of 311 patients. Am J Clin Pathol 32(2):165–168CrossRefPubMed Halpert B, Gyorkey F (1959) Lesions observed in accessory spleens of 311 patients. Am J Clin Pathol 32(2):165–168CrossRefPubMed
2.
go back to reference Hwang HS, Lee SS, Kim SC, Seo DW, Kim J (2011) Intrapancreatic accessory spleen: clinicopathologic analysis of 12 cases. Pancreas 40(6):956–965CrossRefPubMed Hwang HS, Lee SS, Kim SC, Seo DW, Kim J (2011) Intrapancreatic accessory spleen: clinicopathologic analysis of 12 cases. Pancreas 40(6):956–965CrossRefPubMed
3.
go back to reference Halpert B, Alden ZA (1964) Accessory Spleens in or at the Tail of the Pancreas. A Survey of 2,700 Additional Necropsies. Arch Pathol 77:652–654PubMed Halpert B, Alden ZA (1964) Accessory Spleens in or at the Tail of the Pancreas. A Survey of 2,700 Additional Necropsies. Arch Pathol 77:652–654PubMed
5.
go back to reference 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):1471–1473CrossRefPubMed 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):1471–1473CrossRefPubMed
6.
go back to reference 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):400–405PubMed 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):400–405PubMed
7.
go back to reference 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):162–174CrossRefPubMedPubMedCentral 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):162–174CrossRefPubMedPubMedCentral
8.
go back to reference Kazanjian KK, Reber HA, Hines OJ (2006) Resection of pancreatic neuroendocrine tumors: results of 70 cases. Arch Surg 141(8):765–769 discussion 9-70CrossRefPubMed Kazanjian KK, Reber HA, Hines OJ (2006) Resection of pancreatic neuroendocrine tumors: results of 70 cases. Arch Surg 141(8):765–769 discussion 9-70CrossRefPubMed
9.
go back to reference 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–E2PubMedPubMedCentral 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–E2PubMedPubMedCentral
10.
go back to reference Meyer-Rochow GY, Gifford AJ, Samra JS, Sywak MS (2007) Intrapancreatic splenunculus. Am J Surg 194(1):75–76CrossRefPubMed Meyer-Rochow GY, Gifford AJ, Samra JS, Sywak MS (2007) Intrapancreatic splenunculus. Am J Surg 194(1):75–76CrossRefPubMed
11.
go back to reference 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):1338–1347CrossRefPubMed 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):1338–1347CrossRefPubMed
12.
go back to reference 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):1887–1897CrossRefPubMed 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):1887–1897CrossRefPubMed
13.
go back to reference 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):1273–1278CrossRefPubMed 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):1273–1278CrossRefPubMed
14.
go back to reference 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):494–495PubMed 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):494–495PubMed
15.
go back to reference 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):528–531PubMed 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):528–531PubMed
16.
go back to reference 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):481–483CrossRefPubMed 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):481–483CrossRefPubMed
17.
go back to reference Kartalis N, Lindholm TL, Aspelin P, Permert J, Albiin N (2009) Diffusion-weighted magnetic resonance imaging of pancreas tumours. Eur Radiol 19(8):1981–1990CrossRefPubMed Kartalis N, Lindholm TL, Aspelin P, Permert J, Albiin N (2009) Diffusion-weighted magnetic resonance imaging of pancreas tumours. Eur Radiol 19(8):1981–1990CrossRefPubMed
18.
go back to reference 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):928–936CrossRefPubMed 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):928–936CrossRefPubMed
19.
go back to reference 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):1748–1759CrossRefPubMed 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):1748–1759CrossRefPubMed
20.
go back to reference 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):1348–1358CrossRefPubMed 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):1348–1358CrossRefPubMed
21.
go back to reference Le Bihan D, Turner R, Douek P, Patronas N (1992) Diffusion MR imaging: clinical applications. AJR Am J Roentgenol 159(3):591–599CrossRefPubMed Le Bihan D, Turner R, Douek P, Patronas N (1992) Diffusion MR imaging: clinical applications. AJR Am J Roentgenol 159(3):591–599CrossRefPubMed
22.
go back to reference 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):46–51CrossRefPubMed 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):46–51CrossRefPubMed
23.
go back to reference 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):1521–1530CrossRefPubMed 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):1521–1530CrossRefPubMed
24.
go back to reference 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):159–167CrossRefPubMed 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):159–167CrossRefPubMed
25.
go back to reference 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):1157–1165CrossRefPubMed 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):1157–1165CrossRefPubMed
26.
go back to reference 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):e5910CrossRef 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):e5910CrossRef
27.
go back to reference 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):468–485CrossRefPubMedPubMedCentral 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):468–485CrossRefPubMedPubMedCentral
28.
go back to reference 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):1375–1381CrossRefPubMed 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):1375–1381CrossRefPubMed
29.
go back to reference 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):619–627CrossRefPubMed 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):619–627CrossRefPubMed
30.
go back to reference 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):671–676CrossRefPubMed 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):671–676CrossRefPubMed
31.
go back to reference 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):837–845CrossRefPubMed 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):837–845CrossRefPubMed
32.
go back to reference DV C. Guidelines, criteria, and rules of thumb for evaluating normed and standardized assessment instruments in psychology. . Psychol Assess 1994;6(4):284–290. 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.
go back to reference Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33(1):159–174CrossRefPubMed Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33(1):159–174CrossRefPubMed
34.
go back to reference 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):794–800CrossRefPubMed 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):794–800CrossRefPubMed
35.
go back to reference 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):459–465CrossRefPubMed 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):459–465CrossRefPubMed
36.
go back to reference 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):305–309CrossRefPubMed 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):305–309CrossRefPubMed
Metadata
Title
Accuracy of apparent diffusion coefficient in differentiating pancreatic neuroendocrine tumour from intrapancreatic accessory spleen
Authors
Ankur Pandey
Pallavi Pandey
Mounes Aliyari Ghasabeh
Farnaz Najmi Varzaneh
Pegah Khoshpouri
Nannan Shao
Manijeh Zargham Pour
Daniel Fadaei Fouladi
Ralph H. Hruban
Anne Marie O’Broin-Lennon
Ihab R. Kamel
Publication date
01-04-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 4/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-5122-3

Other articles of this Issue 4/2018

European Radiology 4/2018 Go to the issue