Skip to main content
Erschienen in: Abdominal Radiology 6/2019

12.03.2019 | Hepatobiliary

Liver metastases of neuroendocrine tumors: is it possible to diagnose different histologic subtypes depending on multiphasic CT features?

verfasst von: Basak Gulpinar, Elif Peker, Melahat Kul, Atilla Halil Elhan, Nuray Haliloglu

Erschienen in: Abdominal Radiology | Ausgabe 6/2019

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To assess and compare the multiphasic computed tomography (CT) features of neuroendocrine tumor (NET) liver metastases and to investigate the possibility to predict the histologic subtype of the primary tumor.

Materials and methods

Between January 2013 and December 2017 patients with biopsy proven NET with at least one liver metastasis who underwent multiphasic CT were enrolled in this study. All cases were acquired using a standardized multiphasic liver CT protocol, arterial, portal, and hepatic venous phases were obtained. Images were retrospectively analyzed in consensus by two abdominal radiologists blinded to clinical data and histologic subtype. The size, number, and location of lesions were noted. Enhancement patterns of each lesion on arterial, portal, and hepatic venous phases were assessed. For quantitative analysis, CT attenuation of tumors, liver parenchyma, and aorta were measured using a circular region of interest (ROI) on arterial, portal, and hepatic venous phases for reflecting the blood supply of the tumor. Tumor-to-aorta and tumor-to-liver ratio were calculated in all three phases. Differences between subtypes of NET liver metastases were studied using ROC analysis of clustered data.

Results

A total of 255 neuroendocrine tumor liver metastases divided into 101 (39.6%) pancreatic, 60 (23.5%) gastroenteric and 94 (36.8%) lung NET liver metastases were analyzed. Contrast enhancement of lesions was homogeneous in 78% of patients (n = 199), which was significantly more frequent in patients with pancreatic group than in those with gastroenteric origin (n = 90, 89.1% vs. n = 28, 46.7%; p < 0.001). Gastroenteric NET metastases frequently showed heterogeneous enhancement, which was significantly higher than in the other two groups (50% vs. 3% and 2%). With respect to the location of the primary tumor, the difference in enhancement patterns of the liver lesions was statistically significant (p < 0.001). Pancreatic NET metastases were mostly hyperdense on arterial images and isodense on portal and hepatic venous phase images (79.2%, n = 80). Gastroenteric NET metastases were mostly hyperdense on arterial phase images and hypodense on portal and hepatic venous phase images (n = 28, 46.7%). The most frequent pattern for lung NET metastases was hypoattenuation on all three phase images (n = 44, 46.8%). ROC analysis of clustered data revealed statistically significant differences between pancreatic NET liver metastases, gastroenteric NET liver metastases, and lung NET liver metastases in terms of tumor-to-aorta (T–A) ratio and tumor-to-liver (T–L) ratio (p < 0.001).

Conclusion

We observed statistically significant differences in multiphasic CT features (enhancement pattern, T–A ratio, and T–L ratio) between histologic subtypes of NET liver metastases. As the difference in histological subtypes of NET liver metastases results in a different prognosis and different management strategy, these CT features might help to identify the primary tumor when it is not known to ensure accurate tumor staging and to provide optimal treatment.
Literatur
1.
Zurück zum Zitat Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, Abdalla EK, Fleming JB, Vauthey JN, Rashid A, Evans DB. One hundred years after carcinoid: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26:3063–72CrossRefPubMed Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE, Abdalla EK, Fleming JB, Vauthey JN, Rashid A, Evans DB. One hundred years after carcinoid: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26:3063–72CrossRefPubMed
2.
Zurück zum Zitat Pavel M, Baudin E, Couvelard A, et al. ENETS Consensus Guidelines for the management of patients with liver and other distant metastases from neuroendocrine neoplasms of foregut, midgut, hindgut, and unknown primary. Neuroendocrinology. 2012;95:157–176CrossRefPubMed Pavel M, Baudin E, Couvelard A, et al. ENETS Consensus Guidelines for the management of patients with liver and other distant metastases from neuroendocrine neoplasms of foregut, midgut, hindgut, and unknown primary. Neuroendocrinology. 2012;95:157–176CrossRefPubMed
3.
Zurück zum Zitat S. Scigliano, R. Lebtahi, F. Maire, et al. Clinical and imaging follow-up after exhaustive liver resection of endocrine metastases: a 15-year monocentric experience. Endocr. Relat. Cancer, 2009: 977-99 S. Scigliano, R. Lebtahi, F. Maire, et al. Clinical and imaging follow-up after exhaustive liver resection of endocrine metastases: a 15-year monocentric experience. Endocr. Relat. Cancer, 2009: 977-99
4.
Zurück zum Zitat G. d’Assignies, P. Fina, O. Bruno, et al., High sensitivity of diffusion-weighted MR imaging for the detection of liver metastases from neuroendocrine tumors: comparison with T2-weighted and dynamic gadolinium-enhanced MR imaging, Radiology, 2013: 390–399. G. d’Assignies, P. Fina, O. Bruno, et al., High sensitivity of diffusion-weighted MR imaging for the detection of liver metastases from neuroendocrine tumors: comparison with T2-weighted and dynamic gadolinium-enhanced MR imaging, Radiology, 2013: 390–399.
5.
Zurück zum Zitat C. Dromain, T. de Baere, E. Baudin, et al., MR imaging of hepatic metastases caused by neuroendocrine tumors: comparing four techniques, AJR Am. J. Roentgenol. 2003; 180:121–128CrossRefPubMed C. Dromain, T. de Baere, E. Baudin, et al., MR imaging of hepatic metastases caused by neuroendocrine tumors: comparing four techniques, AJR Am. J. Roentgenol. 2003; 180:121–128CrossRefPubMed
6.
Zurück zum Zitat Alireza Mojtahedi et al. The value of 68Ga-DOTATATE PET/CT in diagnosis and management of neuroendocrine tumors compared to current FDA approved imaging modalities: a review of literature, Am J Nucl Med Mol Imaging 2014;4:426-434 Alireza Mojtahedi et al. The value of 68Ga-DOTATATE PET/CT in diagnosis and management of neuroendocrine tumors compared to current FDA approved imaging modalities: a review of literature, Am J Nucl Med Mol Imaging 2014;4:426-434
7.
Zurück zum Zitat C. Dromain, T. de Baere, J. Lumbroso, et al., Detection of liver metastases from endocrine tumors: a prospective comparison of somatostatin receptor scintigraphy computed tomography, and magnetic resonance imaging, J. Clin. Oncol. 2005; 23:70–78CrossRefPubMed C. Dromain, T. de Baere, J. Lumbroso, et al., Detection of liver metastases from endocrine tumors: a prospective comparison of somatostatin receptor scintigraphy computed tomography, and magnetic resonance imaging, J. Clin. Oncol. 2005; 23:70–78CrossRefPubMed
8.
Zurück zum Zitat A.G. Rockall, R.H. Reznek, Imaging of neuroendocrine tumours (CT/MR/US). Best practice & research, Clin. Endocrinol. Metab. 2007; 21:43–68. A.G. Rockall, R.H. Reznek, Imaging of neuroendocrine tumours (CT/MR/US). Best practice & research, Clin. Endocrinol. Metab. 2007; 21:43–68.
9.
Zurück zum Zitat E.K. Paulson, V.G. McDermott, M.T. Keogan, D.M. DeLong, M.G. Frederick, R.C. Nelson, Carcinoid metastases to the liver: role of triple-phase helical CT, Radiology 1998; 206: 143–150.CrossRefPubMed E.K. Paulson, V.G. McDermott, M.T. Keogan, D.M. DeLong, M.G. Frederick, R.C. Nelson, Carcinoid metastases to the liver: role of triple-phase helical CT, Radiology 1998; 206: 143–150.CrossRefPubMed
10.
Zurück zum Zitat W.D. Foley, T.A. Mallisee, M.D. Hohenwalter, C.R. Wilson, F.A. Quiroz, A.J. Taylor, Multiphase hepatic CT with a multirow detector CT scanner, AJR Am. J. Roentgenol. 2000; 175:679–685.CrossRefPubMed W.D. Foley, T.A. Mallisee, M.D. Hohenwalter, C.R. Wilson, F.A. Quiroz, A.J. Taylor, Multiphase hepatic CT with a multirow detector CT scanner, AJR Am. J. Roentgenol. 2000; 175:679–685.CrossRefPubMed
11.
Zurück zum Zitat I.M. Danet, R.C. Semelka, P. Leonardou, et al., Spectrum of MRI appearances of untreated metastases of the liver, AJR Am. J. Roentgenol. 2003; 181: 809–817.CrossRefPubMed I.M. Danet, R.C. Semelka, P. Leonardou, et al., Spectrum of MRI appearances of untreated metastases of the liver, AJR Am. J. Roentgenol. 2003; 181: 809–817.CrossRefPubMed
12.
Zurück zum Zitat P. Kunz, D. Lagunes, L. Anthony et al, Consensus Guidelines for the Management and Treatment of Neuroendocrine Tumors, Pancreas 2013; 42: 557-577 P. Kunz, D. Lagunes, L. Anthony et al, Consensus Guidelines for the Management and Treatment of Neuroendocrine Tumors, Pancreas 2013; 42: 557-577
13.
Zurück zum Zitat Obuchowski NA. Nonparametric analysis of clustered ROC curve data. Biometrics. 1997: 567-578 Obuchowski NA. Nonparametric analysis of clustered ROC curve data. Biometrics. 1997: 567-578
14.
Zurück zum Zitat Benevento A, Boni L, Frediani L. Result of liver resection as treatment for metastases from noncolorectal cancer. J Surg Oncol 2000; 74:24-29CrossRefPubMed Benevento A, Boni L, Frediani L. Result of liver resection as treatment for metastases from noncolorectal cancer. J Surg Oncol 2000; 74:24-29CrossRefPubMed
15.
Zurück zum Zitat Steinmuller T, Kianmanesh R, Falconi M et al. Consensus guidelines for the management of patients with liver metastases from digestive (neuro)-endocrine tumors: foregut, midgut, hindgut, and unknown primary. Neuroendocrinology 2008;87:47-62.CrossRefPubMed Steinmuller T, Kianmanesh R, Falconi M et al. Consensus guidelines for the management of patients with liver metastases from digestive (neuro)-endocrine tumors: foregut, midgut, hindgut, and unknown primary. Neuroendocrinology 2008;87:47-62.CrossRefPubMed
16.
Zurück zum Zitat Alagusundaramoorthy SS, Gedaly R. Role of surgery and transplantation in the treatment of hepatic metastases from neuroendocrine tumor. World J Gastroenterol 2014;20:14348-58.CrossRefPubMedPubMedCentral Alagusundaramoorthy SS, Gedaly R. Role of surgery and transplantation in the treatment of hepatic metastases from neuroendocrine tumor. World J Gastroenterol 2014;20:14348-58.CrossRefPubMedPubMedCentral
17.
Zurück zum Zitat Kennedy A, Bester L, Salem R, Sharma RA, Parks RW, Ruszniewski P; NET-Liver-Metastases Consensus Conference. Role of hepatic intra-arterial therapies in metastatic neuroendocrine tumours (NET): guidelines from the NET-Liver-Metastases Consensus Conference. HPB (Oxford) 2015;17:29-37. Kennedy A, Bester L, Salem R, Sharma RA, Parks RW, Ruszniewski P; NET-Liver-Metastases Consensus Conference. Role of hepatic intra-arterial therapies in metastatic neuroendocrine tumours (NET): guidelines from the NET-Liver-Metastases Consensus Conference. HPB (Oxford) 2015;17:29-37.
18.
Zurück zum Zitat Singh S, Asa SL, Dey C, et al. Diagnosis and management of gastrointestinal neuroendocrine tumors: An evidence-based Canadian consensus. Cancer Treat Rev. 2016;47:32–45.CrossRefPubMed Singh S, Asa SL, Dey C, et al. Diagnosis and management of gastrointestinal neuroendocrine tumors: An evidence-based Canadian consensus. Cancer Treat Rev. 2016;47:32–45.CrossRefPubMed
19.
Zurück zum Zitat Öberg K, Knigge U, Kwekkeboom D, et al. Neuroendocrine gastro-entero-pancreatic tumors: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2012;23 Öberg K, Knigge U, Kwekkeboom D, et al. Neuroendocrine gastro-entero-pancreatic tumors: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2012;23
20.
Zurück zum Zitat Sundin A, Vullierme MP, Kaltsas G, et al. ENETS Consensus Guidelines for the Standards of Care in Neuroendocrine Tumors: radiologic examinations. Neuroendocrinology. 2009;90:167–83.CrossRefPubMed Sundin A, Vullierme MP, Kaltsas G, et al. ENETS Consensus Guidelines for the Standards of Care in Neuroendocrine Tumors: radiologic examinations. Neuroendocrinology. 2009;90:167–83.CrossRefPubMed
21.
Zurück zum Zitat L. Catena, E. Bichisao, M. Milione, et al., Neuroendocrine tumors of unknown primary site: gold dust or misdiagnosed neoplasms, Tumori 2011;97 :564–567.CrossRefPubMed L. Catena, E. Bichisao, M. Milione, et al., Neuroendocrine tumors of unknown primary site: gold dust or misdiagnosed neoplasms, Tumori 2011;97 :564–567.CrossRefPubMed
22.
Zurück zum Zitat J.H. Oliver 3rd, R.L. Baron, M.P. Federle, B.C. Jones, R. Sheng, Hypervascular liver metastases: do unenhanced and hepatic arterial phase CT images affect tumor detection, Radiology, 1997;205:709–715.CrossRefPubMed J.H. Oliver 3rd, R.L. Baron, M.P. Federle, B.C. Jones, R. Sheng, Hypervascular liver metastases: do unenhanced and hepatic arterial phase CT images affect tumor detection, Radiology, 1997;205:709–715.CrossRefPubMed
23.
Zurück zum Zitat J.H. Oliver 3rd, R.L. Baron, M.P. Federle, H.E. Rockette Jr., Detecting hepatocellular carcinoma: value of unenhanced or arterial phase CT imaging or both used in conjunction with conventional portal venous phase contrast-enhanced CT imaging, AJR Am. J. Roentgenol. 1996;167:71–77.CrossRefPubMed J.H. Oliver 3rd, R.L. Baron, M.P. Federle, H.E. Rockette Jr., Detecting hepatocellular carcinoma: value of unenhanced or arterial phase CT imaging or both used in conjunction with conventional portal venous phase contrast-enhanced CT imaging, AJR Am. J. Roentgenol. 1996;167:71–77.CrossRefPubMed
24.
Zurück zum Zitat M. Ronot, F. Cuccioli, M. Dioguardi Burgioa, Neuroendocrine liver metastases: Vascular patterns on triple-phase MDCT are indicative of primary tumor location. European Journal of Radiology 2017; 89:156–162. M. Ronot, F. Cuccioli, M. Dioguardi Burgioa, Neuroendocrine liver metastases: Vascular patterns on triple-phase MDCT are indicative of primary tumor location. European Journal of Radiology 2017; 89:156–162.
25.
Zurück zum Zitat W. Wang, L.D. Chen, M.D. Lu, et al., Contrast-enhanced ultrasound features of histologically proven focal nodular hyperplasia: diagnostic performance compared with contrast-enhanced CT, Eur Radiol. 2013; 23 :2546–2554.CrossRefPubMed W. Wang, L.D. Chen, M.D. Lu, et al., Contrast-enhanced ultrasound features of histologically proven focal nodular hyperplasia: diagnostic performance compared with contrast-enhanced CT, Eur Radiol. 2013; 23 :2546–2554.CrossRefPubMed
26.
Zurück zum Zitat V. Roche, F. Pigneur, L. Tselikas, et al., Differentiation of focal nodular hyperplasia from hepatocellular adenomas with low-mecanical-index contrast-enhanced sonography (CEUS): effect of size on diagnostic confidence. Eur Radiol2015 Jan;25:186-95CrossRef V. Roche, F. Pigneur, L. Tselikas, et al., Differentiation of focal nodular hyperplasia from hepatocellular adenomas with low-mecanical-index contrast-enhanced sonography (CEUS): effect of size on diagnostic confidence. Eur Radiol2015 Jan;25:186-95CrossRef
27.
Zurück zum Zitat C. Rousseau, M. Ronot, E. Sibileau, et al., Central element in liver masses, helpful, or pitfall? Abdom Imaging. 2015 Aug;40:1904-25.CrossRefPubMed C. Rousseau, M. Ronot, E. Sibileau, et al., Central element in liver masses, helpful, or pitfall? Abdom Imaging. 2015 Aug;40:1904-25.CrossRefPubMed
28.
Zurück zum Zitat M.D. McInnes, R.M. Hibbert, J.R. Inacio, N. Schieda, Focal nodular hyperplasia and hepatocellular adenoma: accuracy of gadoxetic acid-enhanced MR imaging-a systematic review, Radiology. 2015 ;277:927CrossRefPubMed M.D. McInnes, R.M. Hibbert, J.R. Inacio, N. Schieda, Focal nodular hyperplasia and hepatocellular adenoma: accuracy of gadoxetic acid-enhanced MR imaging-a systematic review, Radiology. 2015 ;277:927CrossRefPubMed
29.
Zurück zum Zitat A. Roche, B.V. Girish, T. de Baere, et al., Prognostic factors for chemoembolization in liver metastases from endocrine tumors, Hepatogastroenterology,2004;51:1751–1756.PubMed A. Roche, B.V. Girish, T. de Baere, et al., Prognostic factors for chemoembolization in liver metastases from endocrine tumors, Hepatogastroenterology,2004;51:1751–1756.PubMed
30.
Zurück zum Zitat F. Marrache, M.P. Vullierme, C. Roy, et al., Arterial phase enhancement and body mass index are predictors of response to chemoembolisation for liver metastases of endocrine tumours, Br. J. Cancer 2007; 96: 49–55.CrossRefPubMed F. Marrache, M.P. Vullierme, C. Roy, et al., Arterial phase enhancement and body mass index are predictors of response to chemoembolisation for liver metastases of endocrine tumours, Br. J. Cancer 2007; 96: 49–55.CrossRefPubMed
31.
Zurück zum Zitat Aura D. Herrera Martínez, et al. Targeted Systemic Treatment of Neuroendocrine Tumors: Current Options and Future Perspectives, Drugs (2019) 79:21–42.CrossRefPubMed Aura D. Herrera Martínez, et al. Targeted Systemic Treatment of Neuroendocrine Tumors: Current Options and Future Perspectives, Drugs (2019) 79:21–42.CrossRefPubMed
32.
Zurück zum Zitat M. E. Pavel, et al. Efficacy of everolimus plus octreotide LAR in patients with advanced neuroendocrine tumor and carcinoid syndrome: final overall survival from the randomized, placebo-controlled phase 3 RADIANT-2 study Annals of Oncology 28: 1569–1575, 2017 M. E. Pavel, et al. Efficacy of everolimus plus octreotide LAR in patients with advanced neuroendocrine tumor and carcinoid syndrome: final overall survival from the randomized, placebo-controlled phase 3 RADIANT-2 study Annals of Oncology 28: 1569–1575, 2017
Metadaten
Titel
Liver metastases of neuroendocrine tumors: is it possible to diagnose different histologic subtypes depending on multiphasic CT features?
verfasst von
Basak Gulpinar
Elif Peker
Melahat Kul
Atilla Halil Elhan
Nuray Haliloglu
Publikationsdatum
12.03.2019
Verlag
Springer US
Erschienen in
Abdominal Radiology / Ausgabe 6/2019
Print ISSN: 2366-004X
Elektronische ISSN: 2366-0058
DOI
https://doi.org/10.1007/s00261-019-01963-y

Weitere Artikel der Ausgabe 6/2019

Abdominal Radiology 6/2019 Zur Ausgabe

Classics in Abdominal Radiology

The “kissing sign” of liver and spleen

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.