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Published in: EJNMMI Research 1/2019

Open Access 01-12-2019 | Positron Emission Tomography | Original research

Optimal respiratory-gated [18F]FDG PET/CT significantly impacts the quantification of metabolic parameters and their correlation with overall survival in patients with pancreatic ductal adenocarcinoma

Authors: Esther M. M. Smeets, Dominique S. Withaar, Willem Grootjans, John J. Hermans, Kees van Laarhoven, Lioe-Fee de Geus-Oei, Martin Gotthardt, Erik H. J. G. Aarntzen

Published in: EJNMMI Research | Issue 1/2019

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Abstract

Purpose

Metabolic parameters are increasingly being used to characterize tumors. Motion artifacts due to patient respiration introduce uncertainties in quantification of metabolic parameters during positron emission tomography (PET) image acquisition. The present study investigates the impact of amplitude-based optimal respiratory gating (ORG) on quantification of PET-derived image features in patients with pancreatic ductal adenocarcinoma (PDAC), in correlation with overall survival (OS).

Methods

Sixty-nine patients with histologically proven primary PDAC underwent 2′-deoxy-2′-[18F]fluoroglucose ([18F]FDG) PET/CT imaging during diagnostic work-up. Standard image acquisition and reconstruction was performed in accordance with the EANM guidelines and ORG images were reconstructed with a duty cycle of 35%. PET-derived image features, including standard parameters, first- and second-order texture features, were calculated from the standard and corresponding ORG images, and correlation with OS was assessed.

Results

ORG significantly impacts the quantification of nearly all features; values of single-voxel parameters (e.g., SUVmax) showed a wider range, volume-based parameters (e.g., SUVmean) were reduced, and texture features were significantly changed. After correction for motion artifacts using ORG, some features that describe intra-tumoral heterogeneity were more strongly correlated to OS.

Conclusions

Correction for respiratory motion artifacts using ORG impacts the quantification of metabolic parameters in PDAC lesions. The correlation of metabolic parameters with OS was significantly affected, in particular parameters that describe intra-tumor heterogeneity. Therefore, interpretation of single-voxel or average metabolic parameters in relation to clinical outcome should be done cautiously. Furthermore, ORG is a valuable tool to improve quantification of intra-tumoral heterogeneity in PDAC.
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Literature
1.
go back to reference Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. N Engl J Med. 2014;371(22):2140–1.PubMed Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. N Engl J Med. 2014;371(22):2140–1.PubMed
2.
go back to reference Conroy T, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364(19):1817–25.CrossRef Conroy T, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364(19):1817–25.CrossRef
3.
go back to reference Von Hoff DD, et al. Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J Clin Oncol. 2011;29(34):4548–54.CrossRef Von Hoff DD, et al. Gemcitabine plus nab-paclitaxel is an active regimen in patients with advanced pancreatic cancer: a phase I/II trial. J Clin Oncol. 2011;29(34):4548–54.CrossRef
4.
go back to reference Gresham GK, et al. Chemotherapy regimens for advanced pancreatic cancer: a systematic review and network meta-analysis. BMC Cancer. 2014;14:471.CrossRef Gresham GK, et al. Chemotherapy regimens for advanced pancreatic cancer: a systematic review and network meta-analysis. BMC Cancer. 2014;14:471.CrossRef
5.
go back to reference Walentowicz-Sadlecka M, et al. The preoperative maximum standardized uptake value measured by 18F-FDG PET/CT as an independent prognostic factor of overall survival in endometrial cancer patients. Biomed Res Int. 2014;2014:234813.CrossRef Walentowicz-Sadlecka M, et al. The preoperative maximum standardized uptake value measured by 18F-FDG PET/CT as an independent prognostic factor of overall survival in endometrial cancer patients. Biomed Res Int. 2014;2014:234813.CrossRef
6.
go back to reference Ulger S, et al. High FDG uptake predicts poorer survival in locally advanced nonsmall cell lung cancer patients undergoing curative radiotherapy, independently of tumor size. J Cancer Res Clin Oncol. 2014;140(3):495–502.CrossRef Ulger S, et al. High FDG uptake predicts poorer survival in locally advanced nonsmall cell lung cancer patients undergoing curative radiotherapy, independently of tumor size. J Cancer Res Clin Oncol. 2014;140(3):495–502.CrossRef
7.
go back to reference Tong AN, et al. Prognostic value of FDG uptake in primary inoperable non-small cell lung cancer. Med Oncol. 2014;31(1):780.CrossRef Tong AN, et al. Prognostic value of FDG uptake in primary inoperable non-small cell lung cancer. Med Oncol. 2014;31(1):780.CrossRef
8.
go back to reference Eary JF, et al. Sarcoma mid-therapy [F-18]fluorodeoxyglucose positron emission tomography (FDG PET) and patient outcome. J Bone Joint Surg Am. 2014;96(2):152–8.CrossRef Eary JF, et al. Sarcoma mid-therapy [F-18]fluorodeoxyglucose positron emission tomography (FDG PET) and patient outcome. J Bone Joint Surg Am. 2014;96(2):152–8.CrossRef
9.
go back to reference Ulaner GA, et al. Prognostic value of quantitative fluorodeoxyglucose measurements in newly diagnosed metastatic breast cancer. Cancer Med. 2013;2(5):725–33.PubMedPubMedCentral Ulaner GA, et al. Prognostic value of quantitative fluorodeoxyglucose measurements in newly diagnosed metastatic breast cancer. Cancer Med. 2013;2(5):725–33.PubMedPubMedCentral
10.
go back to reference Sperti C, et al. 18-Fluorodeoxyglucose positron emission tomography in predicting survival of patients with pancreatic carcinoma. J Gastrointest Surg. 2003;7:953–60.CrossRef Sperti C, et al. 18-Fluorodeoxyglucose positron emission tomography in predicting survival of patients with pancreatic carcinoma. J Gastrointest Surg. 2003;7:953–60.CrossRef
11.
go back to reference Chen BB, et al. Multiparametric PET/MR imaging biomarkers are associated with overall survival in patients with pancreatic cancer. Eur J Nucl Med Mol Imaging. 2018;45(7):1205–17.CrossRef Chen BB, et al. Multiparametric PET/MR imaging biomarkers are associated with overall survival in patients with pancreatic cancer. Eur J Nucl Med Mol Imaging. 2018;45(7):1205–17.CrossRef
12.
go back to reference Epelbaum R, et al. Tumor aggressiveness and patient outcome in cancer of the pancreas assessed by dynamic 18F-FDG PET/CT. J Nucl Med. 2013;54(1):12–8.CrossRef Epelbaum R, et al. Tumor aggressiveness and patient outcome in cancer of the pancreas assessed by dynamic 18F-FDG PET/CT. J Nucl Med. 2013;54(1):12–8.CrossRef
13.
go back to reference Heinrich S, et al. Neoadjuvant chemotherapy generates a significant tumor response in resectable pancreatic cancer without increasing morbidity: results of a prospective phase II trial. Ann Surg. 2008;248(6):1014–22.CrossRef Heinrich S, et al. Neoadjuvant chemotherapy generates a significant tumor response in resectable pancreatic cancer without increasing morbidity: results of a prospective phase II trial. Ann Surg. 2008;248(6):1014–22.CrossRef
15.
go back to reference Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature. 2013;501(7467):346–54.CrossRef Junttila MR, de Sauvage FJ. Influence of tumour micro-environment heterogeneity on therapeutic response. Nature. 2013;501(7467):346–54.CrossRef
16.
go back to reference Callahan J, et al. Motion effects on SUV and lesion volume in 3D and 4D PET scanning. Australas Phys Eng Sci Med. 2011;34(4):489–95.CrossRef Callahan J, et al. Motion effects on SUV and lesion volume in 3D and 4D PET scanning. Australas Phys Eng Sci Med. 2011;34(4):489–95.CrossRef
17.
go back to reference Chang G, et al. Implementation of an automated respiratory amplitude gating technique for PET/CT: clinical evaluation. J Nucl Med. 2010;51(1):16–24.CrossRef Chang G, et al. Implementation of an automated respiratory amplitude gating technique for PET/CT: clinical evaluation. J Nucl Med. 2010;51(1):16–24.CrossRef
18.
go back to reference Grootjans W, et al. Amplitude-based optimal respiratory gating in positron emission tomography in patients with primary lung cancer. Eur Radiol. 2014;24(12):3242–50.CrossRef Grootjans W, et al. Amplitude-based optimal respiratory gating in positron emission tomography in patients with primary lung cancer. Eur Radiol. 2014;24(12):3242–50.CrossRef
19.
go back to reference Halbrook CJ, Lyssiotis CA. Employing metabolism to improve the diagnosis and treatment of pancreatic cancer. Cancer Cell. 2017;31(1):5–19.CrossRef Halbrook CJ, Lyssiotis CA. Employing metabolism to improve the diagnosis and treatment of pancreatic cancer. Cancer Cell. 2017;31(1):5–19.CrossRef
20.
go back to reference Kawada K, et al. Relationship between 18F-fluorodeoxyglucose accumulation and KRAS/BRAF mutations in colorectal cancer. Clin Cancer Res. 2012;18(6):1696–703.CrossRef Kawada K, et al. Relationship between 18F-fluorodeoxyglucose accumulation and KRAS/BRAF mutations in colorectal cancer. Clin Cancer Res. 2012;18(6):1696–703.CrossRef
21.
go back to reference Priolo C, et al. AKT1 and MYC induce distinctive metabolic fingerprints in human prostate cancer. Cancer Res. 2014;74(24):7198–204.CrossRef Priolo C, et al. AKT1 and MYC induce distinctive metabolic fingerprints in human prostate cancer. Cancer Res. 2014;74(24):7198–204.CrossRef
22.
go back to reference Waddell N, et al. Whole genomes redefine the mutational landscape of pancreatic cancer. Nature. 2015;518(7540):495–501.CrossRef Waddell N, et al. Whole genomes redefine the mutational landscape of pancreatic cancer. Nature. 2015;518(7540):495–501.CrossRef
23.
go back to reference Sahin IH, Iacobuzio-Donahue CA, O'Reilly EM. Molecular signature of pancreatic adenocarcinoma: an insight from genotype to phenotype and challenges for targeted therapy. Expert Opin Ther Targets. 2016;20(3):341–59.CrossRef Sahin IH, Iacobuzio-Donahue CA, O'Reilly EM. Molecular signature of pancreatic adenocarcinoma: an insight from genotype to phenotype and challenges for targeted therapy. Expert Opin Ther Targets. 2016;20(3):341–59.CrossRef
24.
go back to reference Bailey P, et al. Genomic analyses identify molecular subtypes of pancreatic cancer. Nature. 2016;531(7592):47–52.CrossRef Bailey P, et al. Genomic analyses identify molecular subtypes of pancreatic cancer. Nature. 2016;531(7592):47–52.CrossRef
25.
go back to reference O'Connor JP, et al. Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res. 2015;21(2):249–57.CrossRef O'Connor JP, et al. Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res. 2015;21(2):249–57.CrossRef
26.
go back to reference Boellaard R, et al. FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37(1):181–200.CrossRef Boellaard R, et al. FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37(1):181–200.CrossRef
27.
go back to reference van Griethuysen JJM, et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77(21):e104–7.CrossRef van Griethuysen JJM, et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77(21):e104–7.CrossRef
28.
go back to reference Pedregosa F, et al. Scikit-learn: machine learning in python. J Mach Learn Res. 2011;12:2825–30. Pedregosa F, et al. Scikit-learn: machine learning in python. J Mach Learn Res. 2011;12:2825–30.
29.
go back to reference Topkan E, et al. Predictive value of metabolic 18FDG-PET response on outcomes in patients with locally advanced pancreatic carcinoma treated with definitive concurrent chemoradiotherapy. BMC Gastroenterol. 2011;11:123.CrossRef Topkan E, et al. Predictive value of metabolic 18FDG-PET response on outcomes in patients with locally advanced pancreatic carcinoma treated with definitive concurrent chemoradiotherapy. BMC Gastroenterol. 2011;11:123.CrossRef
30.
go back to reference Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.CrossRef Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646–74.CrossRef
31.
go back to reference Tixier F, et al. Intratumor heterogeneity characterized by textural features on baseline 18F-FDG PET images predicts response to concomitant radiochemotherapy in esophageal cancer. J Nucl Med. 2011;52(3):369–78.CrossRef Tixier F, et al. Intratumor heterogeneity characterized by textural features on baseline 18F-FDG PET images predicts response to concomitant radiochemotherapy in esophageal cancer. J Nucl Med. 2011;52(3):369–78.CrossRef
32.
go back to reference Soussan M, et al. Relationship between tumor heterogeneity measured on FDG-PET/CT and pathological prognostic factors in invasive breast cancer. PLoS One. 2014;9(4):e94017.CrossRef Soussan M, et al. Relationship between tumor heterogeneity measured on FDG-PET/CT and pathological prognostic factors in invasive breast cancer. PLoS One. 2014;9(4):e94017.CrossRef
33.
go back to reference Hatt M, et al. 18F-FDG PET uptake characterization through texture analysis: investigating the complementary nature of heterogeneity and functional tumor volume in a multi-cancer site patient cohort. J Nucl Med. 2015;56(1):38–44.CrossRef Hatt M, et al. 18F-FDG PET uptake characterization through texture analysis: investigating the complementary nature of heterogeneity and functional tumor volume in a multi-cancer site patient cohort. J Nucl Med. 2015;56(1):38–44.CrossRef
34.
go back to reference Grootjans W, et al. The impact of optimal respiratory gating and image noise on evaluation of intratumor heterogeneity on 18F-FDG PET imaging of lung cancer. J Nucl Med. 2016;57(11):1692–8.CrossRef Grootjans W, et al. The impact of optimal respiratory gating and image noise on evaluation of intratumor heterogeneity on 18F-FDG PET imaging of lung cancer. J Nucl Med. 2016;57(11):1692–8.CrossRef
35.
go back to reference Leijenaar RT, et al. The effect of SUV discretization in quantitative FDG-PET Radiomics: the need for standardized methodology in tumor texture analysis. Sci Rep. 2015;5:11075.CrossRef Leijenaar RT, et al. The effect of SUV discretization in quantitative FDG-PET Radiomics: the need for standardized methodology in tumor texture analysis. Sci Rep. 2015;5:11075.CrossRef
36.
go back to reference Galavis PE, et al. Variability of textural features in FDG PET images due to different acquisition modes and reconstruction parameters. Acta Oncol. 2010;49(7):1012–6.CrossRef Galavis PE, et al. Variability of textural features in FDG PET images due to different acquisition modes and reconstruction parameters. Acta Oncol. 2010;49(7):1012–6.CrossRef
37.
go back to reference Orlhac F, et al. Tumor texture analysis in 18F-FDG PET: relationships between texture parameters, histogram indices, standardized uptake values, metabolic volumes, and total lesion glycolysis. J Nucl Med. 2014;55(3):414–22.CrossRef Orlhac F, et al. Tumor texture analysis in 18F-FDG PET: relationships between texture parameters, histogram indices, standardized uptake values, metabolic volumes, and total lesion glycolysis. J Nucl Med. 2014;55(3):414–22.CrossRef
38.
go back to reference Boellaard R, et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging. 2015;42(2):328–54.CrossRef Boellaard R, et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging. 2015;42(2):328–54.CrossRef
39.
go back to reference Aerts HJ, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.CrossRef Aerts HJ, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.CrossRef
40.
go back to reference Coroller TP, et al. CT-based radiomic signature predicts distant metastasis in lung adenocarcinoma. Radiother Oncol. 2015;114(3):345–50.CrossRef Coroller TP, et al. CT-based radiomic signature predicts distant metastasis in lung adenocarcinoma. Radiother Oncol. 2015;114(3):345–50.CrossRef
Metadata
Title
Optimal respiratory-gated [18F]FDG PET/CT significantly impacts the quantification of metabolic parameters and their correlation with overall survival in patients with pancreatic ductal adenocarcinoma
Authors
Esther M. M. Smeets
Dominique S. Withaar
Willem Grootjans
John J. Hermans
Kees van Laarhoven
Lioe-Fee de Geus-Oei
Martin Gotthardt
Erik H. J. G. Aarntzen
Publication date
01-12-2019
Publisher
Springer Berlin Heidelberg
Published in
EJNMMI Research / Issue 1/2019
Electronic ISSN: 2191-219X
DOI
https://doi.org/10.1186/s13550-019-0492-y

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