Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 1/2015

01-01-2015 | Review Article

Diagnostic accuracy and impact on management of 18F-FDG PET and PET/CT in colorectal liver metastasis: a meta-analysis and systematic review

Authors: Anna Margherita Maffione, Egesta Lopci, Christina Bluemel, Francesco Giammarile, Ken Herrmann, Domenico Rubello

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 1/2015

Login to get access

Abstract

Purpose

The first aim of the review (aim 1) was to obtain the diagnostic performance values of 18F-FDG PET for the detection and staging of liver metastases in patients with colorectal cancer (CRC), the second aim (aim 2) was to compare PET and conventional imaging modalities, and the third aim (aim 3) was to evaluate the impact of PET on patient management. The incidence of extrahepatic disease (EHD) detected by PET is also reviewed.

Methods

A comprehensive search was performed on PubMed/MEDLINE for studies evaluating PET and PET/CT in CRC patients with liver metastases up to June 2014. For inclusion PET had to have been performed prior to surgery, there had to be at least 18 patients in the study, and the reported data had to allow calculation of 2 × 2 contingency tables (for aim 1). A total of 18 studies were eligible for at least one of the three intended subanalyses including a total of 1,059 patients. Pooled sensitivity, specificity and accuracy and the corresponding 95 % confidence intervals were derived from the contingency tables on a patient basis (patient-based analysis, PBA) and a lesion basis (lesion-based analysis, LBA) for eight studies.

Results

Pooled sensitivity and specificity of PET on PBA were both 93 %. Corresponding values for LBA were 60 % and 79 %, respectively. Areas under the summary ROC were 0.97 for PBA and 0.67 for LBA. Regarding aim 2, PET had a slightly lower sensitivity than MRI and CT on PBA (93 %, 100 % and 98 %, respectively) and LBA (66 %, 89 % and 79 %, respectively) but appeared to be more specific than MRI and CT (86 %, 81 % and 67 %, respectively). PET findings resulted in changes in the management of a mean of 24 % of patients. The mean incidence of PET-based EHD was 32 %.

Conclusion

This meta-analysis suggests that FDG PET/CT is highly accurate for the detection of liver metastases on a patient basis but less accurate on a lesion basis. Compared to MRI, PET is less sensitive but more specific and affects the management of about one-quarter of patients.
Literature
2.
go back to reference Kew MC. Sleisenger and Fordtran’s gastrointestinal and liver disease: pathophysiology/diagnosis/management. In: Feldman M, Friedman LS, Sleisenger MH, Scharschmidt BF, editors. Hepatic tumors and cysts. 7th ed. Philadelphia: Saunders; 2002. Kew MC. Sleisenger and Fordtran’s gastrointestinal and liver disease: pathophysiology/diagnosis/management. In: Feldman M, Friedman LS, Sleisenger MH, Scharschmidt BF, editors. Hepatic tumors and cysts. 7th ed. Philadelphia: Saunders; 2002.
3.
go back to reference Van Cutsem E, Nordlinger B, Adam R, Köhne CH, Pozzo C, Poston G, et al.; European Colorectal Metastases Treatment Group. Towards a pan-European consensus on the treatment of patients with colorectal liver metastases. Eur J Cancer. 2006;42(14):2212–21.PubMedCrossRef Van Cutsem E, Nordlinger B, Adam R, Köhne CH, Pozzo C, Poston G, et al.; European Colorectal Metastases Treatment Group. Towards a pan-European consensus on the treatment of patients with colorectal liver metastases. Eur J Cancer. 2006;42(14):2212–21.PubMedCrossRef
4.
go back to reference National Comprehensive Cancer Network. Clinical practice guidelines in oncology. Colon cancer version 1.2015. Fort Washington, PA: National Comprehensive Cancer Network. COL-B, page 2 National Comprehensive Cancer Network. Clinical practice guidelines in oncology. Colon cancer version 1.2015. Fort Washington, PA: National Comprehensive Cancer Network. COL-B, page 2
5.
go back to reference Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, et al. Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg. 2002;235(6):759–66.PubMedCentralPubMedCrossRef Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, et al. Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg. 2002;235(6):759–66.PubMedCentralPubMedCrossRef
6.
go back to reference Floriani I, Torri V, Rulli E, Garavaglia D, Compagnoni A, Salvolini L, et al. Performance of imaging modalities in diagnosis of liver metastases from colorectal cancer: a systematic review and meta-analysis. J Magn Reson Imaging. 2010;31(1):19–31.PubMedCrossRef Floriani I, Torri V, Rulli E, Garavaglia D, Compagnoni A, Salvolini L, et al. Performance of imaging modalities in diagnosis of liver metastases from colorectal cancer: a systematic review and meta-analysis. J Magn Reson Imaging. 2010;31(1):19–31.PubMedCrossRef
7.
go back to reference Kekelidze M, D’Errico L, Pansini M, Tyndall A, Hohmann J. Colorectal cancer: current imaging methods and future perspectives for the diagnosis, staging and therapeutic response evaluation. World J Gastroenterol. 2013;19(46):8502–14.PubMedCentralPubMedCrossRef Kekelidze M, D’Errico L, Pansini M, Tyndall A, Hohmann J. Colorectal cancer: current imaging methods and future perspectives for the diagnosis, staging and therapeutic response evaluation. World J Gastroenterol. 2013;19(46):8502–14.PubMedCentralPubMedCrossRef
8.
go back to reference Fletcher JW, Djulbegovic B, Soares HP, Siegel BA, Lowe VJ, Lyman GH, et al. Recommendations on the use of 18F-FDG PET in oncology. J Nucl Med. 2008;49(3):480–508.PubMedCrossRef Fletcher JW, Djulbegovic B, Soares HP, Siegel BA, Lowe VJ, Lyman GH, et al. Recommendations on the use of 18F-FDG PET in oncology. J Nucl Med. 2008;49(3):480–508.PubMedCrossRef
9.
go back to reference Ruers TJ, Wiering B, van der Sijp JR, Roumen RM, de Jong KP, Comans EF, et al. Improved selection of patients for hepatic surgery of colorectal liver metastases with (18)F-FDG PET: a randomized study. J Nucl Med. 2009;50(7):1036–41.PubMedCrossRef Ruers TJ, Wiering B, van der Sijp JR, Roumen RM, de Jong KP, Comans EF, et al. Improved selection of patients for hepatic surgery of colorectal liver metastases with (18)F-FDG PET: a randomized study. J Nucl Med. 2009;50(7):1036–41.PubMedCrossRef
10.
go back to reference Moulton CA, Gu CS, Law CH, Tandan VR, Hart R, Quan D, et al. Effect of PET before liver resection on surgical management for colorectal adenocarcinoma metastases: a randomized clinical trial. JAMA. 2014;311(18):1863–9.PubMedCrossRef Moulton CA, Gu CS, Law CH, Tandan VR, Hart R, Quan D, et al. Effect of PET before liver resection on surgical management for colorectal adenocarcinoma metastases: a randomized clinical trial. JAMA. 2014;311(18):1863–9.PubMedCrossRef
11.
go back to reference Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36.PubMedCrossRef Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155(8):529–36.PubMedCrossRef
12.
13.
go back to reference Coenegrachts K, De Geeter F, ter Beek L, Walgraeve N, Bipat S, Stoker J, et al. Comparison of MRI (including SS SE-EPI and SPIO-enhanced MRI) and FDG-PET/CT for the detection of colorectal liver metastases. Eur Radiol. 2009;19(2):370–9.PubMedCrossRef Coenegrachts K, De Geeter F, ter Beek L, Walgraeve N, Bipat S, Stoker J, et al. Comparison of MRI (including SS SE-EPI and SPIO-enhanced MRI) and FDG-PET/CT for the detection of colorectal liver metastases. Eur Radiol. 2009;19(2):370–9.PubMedCrossRef
14.
go back to reference Huguet EL, Old S, Praseedom RK, Balan KK, Gibbs P, Jamieson NV. F18-FDG-PET evaluation of patients for resection of colorectal liver metastases. Hepatogastroenterology. 2007;54(78):1667–71.PubMed Huguet EL, Old S, Praseedom RK, Balan KK, Gibbs P, Jamieson NV. F18-FDG-PET evaluation of patients for resection of colorectal liver metastases. Hepatogastroenterology. 2007;54(78):1667–71.PubMed
15.
go back to reference Rappeport ED, Loft A, Berthelsen AK, von der Recke P, Larsen PN, Mogensen AM, et al. Contrast-enhanced FDG-PET/CT vs SPIO-enhanced MRI vs. FDG-PET vs. CT in patients with liver metastases from colorectal cancer: a prospective study with intraoperative confirmation. Acta Radiol. 2007;48(4):369–78.PubMedCrossRef Rappeport ED, Loft A, Berthelsen AK, von der Recke P, Larsen PN, Mogensen AM, et al. Contrast-enhanced FDG-PET/CT vs SPIO-enhanced MRI vs. FDG-PET vs. CT in patients with liver metastases from colorectal cancer: a prospective study with intraoperative confirmation. Acta Radiol. 2007;48(4):369–78.PubMedCrossRef
16.
go back to reference Bacigalupo L, Aufort S, Eberlé MC, Assenat E, Ychou M, Gallix B. Assessment of liver metastases from colorectal adenocarcinoma following chemotherapy: SPIO-MRI versus FDG-PET/CT. Radiol Med. 2010;115(7):1087–100.PubMedCrossRef Bacigalupo L, Aufort S, Eberlé MC, Assenat E, Ychou M, Gallix B. Assessment of liver metastases from colorectal adenocarcinoma following chemotherapy: SPIO-MRI versus FDG-PET/CT. Radiol Med. 2010;115(7):1087–100.PubMedCrossRef
17.
go back to reference Akiyoshi T, Oya M, Fujimoto Y, Kuroyanagi H, Ueno M, Yamaguchi T, et al. Comparison of preoperative whole-body positron emission tomography with MDCT in patients with primary colorectal cancer. Colorectal Dis. 2009;11(5):464–9.PubMedCrossRef Akiyoshi T, Oya M, Fujimoto Y, Kuroyanagi H, Ueno M, Yamaguchi T, et al. Comparison of preoperative whole-body positron emission tomography with MDCT in patients with primary colorectal cancer. Colorectal Dis. 2009;11(5):464–9.PubMedCrossRef
18.
go back to reference Chua SC, Groves AM, Kayani I, Menezes L, Gacinovic S, Du Y, et al. The impact of 18F-FDG PET/CT in patients with liver metastases. Eur J Nucl Med Mol Imaging. 2007;34(12):1906–14.PubMedCrossRef Chua SC, Groves AM, Kayani I, Menezes L, Gacinovic S, Du Y, et al. The impact of 18F-FDG PET/CT in patients with liver metastases. Eur J Nucl Med Mol Imaging. 2007;34(12):1906–14.PubMedCrossRef
19.
go back to reference Ramos E, Valls C, Martinez L, Lladó L, Torras J, Ruiz S, et al. Preoperative staging of patients with liver metastases of colorectal carcinoma. Does PET/CT really add something to multidetector CT? Ann Surg Oncol. 2011;18(9):2654–61.PubMedCrossRef Ramos E, Valls C, Martinez L, Lladó L, Torras J, Ruiz S, et al. Preoperative staging of patients with liver metastases of colorectal carcinoma. Does PET/CT really add something to multidetector CT? Ann Surg Oncol. 2011;18(9):2654–61.PubMedCrossRef
20.
go back to reference Selzner M, Hany TF, Wildbrett P, McCormack L, Kadry Z, Clavien PA. Does the novel PET/CT imaging modality impact on the treatment of patients with metastatic colorectal cancer of the liver? Ann Surg. 2004;240(6):1027–34.PubMedCentralPubMedCrossRef Selzner M, Hany TF, Wildbrett P, McCormack L, Kadry Z, Clavien PA. Does the novel PET/CT imaging modality impact on the treatment of patients with metastatic colorectal cancer of the liver? Ann Surg. 2004;240(6):1027–34.PubMedCentralPubMedCrossRef
21.
go back to reference Briggs RH, Chowdhury FU, Lodge JP, Scarsbrook AF. Clinical impact of FDG PET-CT in patients with potentially operable metastatic colorectal cancer. Clin Radiol. 2011;66(12):1167–74.PubMedCrossRef Briggs RH, Chowdhury FU, Lodge JP, Scarsbrook AF. Clinical impact of FDG PET-CT in patients with potentially operable metastatic colorectal cancer. Clin Radiol. 2011;66(12):1167–74.PubMedCrossRef
22.
go back to reference Joyce DL, Wahl RL, Patel PV, Schulick RD, Gearhart SL, Choti MA. Preoperative positron emission tomography to evaluate potentially resectable hepatic colorectal metastases. Arch Surg. 2006;141(12):1220–6.PubMedCrossRef Joyce DL, Wahl RL, Patel PV, Schulick RD, Gearhart SL, Choti MA. Preoperative positron emission tomography to evaluate potentially resectable hepatic colorectal metastases. Arch Surg. 2006;141(12):1220–6.PubMedCrossRef
23.
go back to reference Sørensen M, Mortensen FV, Høyer M, Vilstrup H, Keiding S; Liver Tumour Board at Aarhus University Hospital. FDG-PET improves management of patients with colorectal liver metastases allocated for local treatment: a consecutive prospective study. Scand J Surg. 2007;96(3):209–13.PubMed Sørensen M, Mortensen FV, Høyer M, Vilstrup H, Keiding S; Liver Tumour Board at Aarhus University Hospital. FDG-PET improves management of patients with colorectal liver metastases allocated for local treatment: a consecutive prospective study. Scand J Surg. 2007;96(3):209–13.PubMed
24.
go back to reference Engledow AH, Skipworth JR, Pakzad F, Imber C, Ell PJ, Groves AM. The role of 18FDG PET/CT in the management of colorectal liver metastases. HPB (Oxford). 2012;14(1):20–5.CrossRef Engledow AH, Skipworth JR, Pakzad F, Imber C, Ell PJ, Groves AM. The role of 18FDG PET/CT in the management of colorectal liver metastases. HPB (Oxford). 2012;14(1):20–5.CrossRef
25.
go back to reference Bonanni L, De’liguori Carino N, Deshpande R, Ammori BJ, Sherlock DJ, Valle JW, et al. A comparison of diagnostic imaging modalities for colorectal liver metastases. Eur J Surg Oncol. 2014;40(5):545–50.PubMedCrossRef Bonanni L, De’liguori Carino N, Deshpande R, Ammori BJ, Sherlock DJ, Valle JW, et al. A comparison of diagnostic imaging modalities for colorectal liver metastases. Eur J Surg Oncol. 2014;40(5):545–50.PubMedCrossRef
26.
go back to reference Lake ES, Wadhwani S, Subar D, Kauser A, Harris C, Chang D, et al. The influence of FDG PET-CT on the detection of extrahepatic disease in patients being considered for resection of colorectal liver metastasis. Ann R Coll Surg Engl. 2014;96(3):211–5.PubMedCrossRef Lake ES, Wadhwani S, Subar D, Kauser A, Harris C, Chang D, et al. The influence of FDG PET-CT on the detection of extrahepatic disease in patients being considered for resection of colorectal liver metastasis. Ann R Coll Surg Engl. 2014;96(3):211–5.PubMedCrossRef
27.
go back to reference Cantwell CP, Setty BN, Holalkere N, Sahani DV, Fischman AJ, Blake MA. Liver lesion detection and characterization in patients with colorectal cancer: a comparison of low radiation dose non-enhanced PET/CT, contrast-enhanced PET/CT, and liver MRI. J Comput Assist Tomogr. 2008;32(5):738–44.PubMedCrossRef Cantwell CP, Setty BN, Holalkere N, Sahani DV, Fischman AJ, Blake MA. Liver lesion detection and characterization in patients with colorectal cancer: a comparison of low radiation dose non-enhanced PET/CT, contrast-enhanced PET/CT, and liver MRI. J Comput Assist Tomogr. 2008;32(5):738–44.PubMedCrossRef
28.
go back to reference Carnaghi C, Tronconi MC, Rimassa L, Tondulli L, Zuradelli M, Rodari M, et al. Utility of 18F-FDG PET and contrast-enhanced CT scan in the assessment of residual liver metastasis from colorectal cancer following adjuvant chemotherapy. Nucl Med Rev Cent East Eur. 2007;10(1):12–5.PubMed Carnaghi C, Tronconi MC, Rimassa L, Tondulli L, Zuradelli M, Rodari M, et al. Utility of 18F-FDG PET and contrast-enhanced CT scan in the assessment of residual liver metastasis from colorectal cancer following adjuvant chemotherapy. Nucl Med Rev Cent East Eur. 2007;10(1):12–5.PubMed
29.
go back to reference Rojas Llimpe FL, Di Fabio F, Ercolani G, Giampalma E, Cappelli A, Serra C, et al. Imaging in resectable colorectal liver metastasis patients with or without preoperative chemotherapy: results of the PROMETEO-01 study. Br J Cancer. 2014;111(4):667–73.PubMedCrossRef Rojas Llimpe FL, Di Fabio F, Ercolani G, Giampalma E, Cappelli A, Serra C, et al. Imaging in resectable colorectal liver metastasis patients with or without preoperative chemotherapy: results of the PROMETEO-01 study. Br J Cancer. 2014;111(4):667–73.PubMedCrossRef
30.
go back to reference Seo HJ, Kim MJ, Lee JD, Chung WS, Kim YE. Gadoxetate disodium-enhanced magnetic resonance imaging versus contrast-enhanced 18F-fluorodeoxyglucose positron emission tomography/computed tomography for the detection of colorectal liver metastases. Invest Radiol. 2011;46(9):548–55.PubMedCrossRef Seo HJ, Kim MJ, Lee JD, Chung WS, Kim YE. Gadoxetate disodium-enhanced magnetic resonance imaging versus contrast-enhanced 18F-fluorodeoxyglucose positron emission tomography/computed tomography for the detection of colorectal liver metastases. Invest Radiol. 2011;46(9):548–55.PubMedCrossRef
31.
go back to reference Niekel MC, Bipat S, Stoker J. Diagnostic imaging of colorectal liver metastases with CT, MR imaging, FDG PET, and/or FDG PET/CT: a meta-analysis of prospective studies including patients who have not previously undergone treatment. Radiology. 2010;257(3):674–84.PubMedCrossRef Niekel MC, Bipat S, Stoker J. Diagnostic imaging of colorectal liver metastases with CT, MR imaging, FDG PET, and/or FDG PET/CT: a meta-analysis of prospective studies including patients who have not previously undergone treatment. Radiology. 2010;257(3):674–84.PubMedCrossRef
32.
go back to reference van Kessel CS, Buckens CF, van den Bosch MA, van Leeuwen MS, van Hillegersberg R, Verkooijen HM. Preoperative imaging of colorectal liver metastases after neoadjuvant chemotherapy: a meta-analysis. Ann Surg Oncol. 2012;19(9):2805–13.PubMedCentralPubMedCrossRef van Kessel CS, Buckens CF, van den Bosch MA, van Leeuwen MS, van Hillegersberg R, Verkooijen HM. Preoperative imaging of colorectal liver metastases after neoadjuvant chemotherapy: a meta-analysis. Ann Surg Oncol. 2012;19(9):2805–13.PubMedCentralPubMedCrossRef
33.
go back to reference Huebner RH, Park KC, Shepherd JE, Schwimmer J, Czernin J, Phelps ME, et al. A meta-analysis of the literature for whole-body FDG PET detection of recurrent colorectal cancer. J Nucl Med. 2000;41(7):1177–89.PubMed Huebner RH, Park KC, Shepherd JE, Schwimmer J, Czernin J, Phelps ME, et al. A meta-analysis of the literature for whole-body FDG PET detection of recurrent colorectal cancer. J Nucl Med. 2000;41(7):1177–89.PubMed
34.
go back to reference Wiering B, Krabbe PF, Jager GJ, Oyen WJ, Ruers TJ. The impact of fluor-18-deoxyglucose-positron emission tomography in the management of colorectal liver metastases. Cancer. 2005;104(12):2658–70.PubMedCrossRef Wiering B, Krabbe PF, Jager GJ, Oyen WJ, Ruers TJ. The impact of fluor-18-deoxyglucose-positron emission tomography in the management of colorectal liver metastases. Cancer. 2005;104(12):2658–70.PubMedCrossRef
35.
go back to reference Petersen RK, Hess S, Alavi A, Høilund-Carlsen PF. Clinical impact of FDG-PET/CT on colorectal cancer staging and treatment strategy. Am J Nucl Med Mol Imaging. 2014;4(5):471–82.PubMedCentralPubMed Petersen RK, Hess S, Alavi A, Høilund-Carlsen PF. Clinical impact of FDG-PET/CT on colorectal cancer staging and treatment strategy. Am J Nucl Med Mol Imaging. 2014;4(5):471–82.PubMedCentralPubMed
36.
go back to reference Yang Y, Czernin J. Contribution of imaging to cancer care costs. J Nucl Med. 2011;52 Suppl 2:86S–92S.PubMedCrossRef Yang Y, Czernin J. Contribution of imaging to cancer care costs. J Nucl Med. 2011;52 Suppl 2:86S–92S.PubMedCrossRef
37.
go back to reference Siepe B, Hoilund-Carlsen PF, Gerke O, Weber WA, Motschall E, Vach W. The move from accuracy studies to randomized trials in PET: current status and future directions. J Nucl Med. 2014;55(8):1228–34.PubMedCrossRef Siepe B, Hoilund-Carlsen PF, Gerke O, Weber WA, Motschall E, Vach W. The move from accuracy studies to randomized trials in PET: current status and future directions. J Nucl Med. 2014;55(8):1228–34.PubMedCrossRef
Metadata
Title
Diagnostic accuracy and impact on management of 18F-FDG PET and PET/CT in colorectal liver metastasis: a meta-analysis and systematic review
Authors
Anna Margherita Maffione
Egesta Lopci
Christina Bluemel
Francesco Giammarile
Ken Herrmann
Domenico Rubello
Publication date
01-01-2015
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 1/2015
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-014-2930-4

Other articles of this Issue 1/2015

European Journal of Nuclear Medicine and Molecular Imaging 1/2015 Go to the issue