Skip to main content
Top
Published in: Molecular Imaging and Biology 4/2020

Open Access 01-08-2020 | Lymphoma | Research Article

Optimizing Workflows for Fast and Reliable Metabolic Tumor Volume Measurements in Diffuse Large B Cell Lymphoma

Authors: Coreline N. Burggraaff, Fareen Rahman, Isabelle Kaßner, Simone Pieplenbosch, Sally F. Barrington, Yvonne W.S. Jauw, Gerben J.C. Zwezerijnen, Stefan Müller, Otto S. Hoekstra, Josée M. Zijlstra, Henrica C.W. De Vet, Ronald Boellaard, On behalf of the PETRA Consortium

Published in: Molecular Imaging and Biology | Issue 4/2020

Login to get access

Abstract

Purpose

This pilot study aimed to determine interobserver reliability and ease of use of three workflows for measuring metabolic tumor volume (MTV) and total lesion glycolysis (TLG) in diffuse large B cell lymphoma (DLBCL).

Procedures

Twelve baseline [18F]FDG PET/CT scans from DLBCL patients with wide variation in number and size of involved organs and lymph nodes were selected from the international PETRA consortium database. Three observers analyzed scans using three workflows. Workflow A: user-defined selection of individual lesions followed by four automated segmentations (41%SUVmax, A50%SUVpeak, SUV≥2.5, SUV≥4.0). For each lesion, observers indicated their “preferred segmentation.” Individually selected lesions were summed to yield total MTV and TLG. Workflow B: fully automated preselection of [18F]FDG-avid structures (SUV≥4.0 and volume≥3ml), followed by removing non-tumor regions with single mouse clicks. Workflow C: preselected volumes based on Workflow B modified by manually adding lesions or removing physiological uptake, subsequently checked by experienced nuclear medicine physicians. Workflow C was performed 3 months later to avoid recall bias from the initial Workflow B analysis. Interobserver reliability was expressed as intraclass correlation coefficients (ICC).

Results

Highest interobserver reliability in Workflow A was found for SUV≥2.5 and SUV≥4.0 methods (ICCs for MTV 0.96 and 0.94, respectively). SUV≥4.0 and A50%Peak were most and SUV≥2.5 was the least preferred segmentation method. Workflow B had an excellent interobserver reliability (ICC = 1.00) for MTV and TLG. Workflow C reduced the ICC for MTV and TLG to 0.92 and 0.97, respectively. Mean workflow analysis time per scan was 29, 7, and 22 min for A, B, and C, respectively.

Conclusions

Improved interobserver reliability and ease of use occurred using fully automated preselection (using SUV≥4.0 and volume≥3ml, Workflow B) compared with individual lesion selection by observers (Workflow A). Subsequent manual modification was necessary for some patients but reduced interobserver reliability which may need to be balanced against potential improvement on prognostic accuracy.
Appendix
Available only for authorised users
Literature
1.
go back to reference Pfreundschuh M, Ho AD, Cavallin-Stahl E et al (2008) Prognostic significance of maximum tumour (bulk) diameter in young patients with good-prognosis diffuse large-B-cell lymphoma treated with CHOP-like chemotherapy with or without rituximab: an exploratory analysis of the MabThera International Trial Group (MInT) study. Lancet Oncol 9:435–444 Pfreundschuh M, Ho AD, Cavallin-Stahl E et al (2008) Prognostic significance of maximum tumour (bulk) diameter in young patients with good-prognosis diffuse large-B-cell lymphoma treated with CHOP-like chemotherapy with or without rituximab: an exploratory analysis of the MabThera International Trial Group (MInT) study. Lancet Oncol 9:435–444
2.
go back to reference Barrington SF, Mikhaeel NG, Kostakoglu L et al (2014) Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol 32:3048–3058CrossRef Barrington SF, Mikhaeel NG, Kostakoglu L et al (2014) Role of imaging in the staging and response assessment of lymphoma: consensus of the International Conference on Malignant Lymphomas Imaging Working Group. J Clin Oncol 32:3048–3058CrossRef
3.
go back to reference Cheebsumon P, Boellaard R, de Ruysscher D et al (2012) Assessment of tumour size in PET/CT lung cancer studies: PET- and CT-based methods compared to pathology. EJNMMI Res 2:56CrossRef Cheebsumon P, Boellaard R, de Ruysscher D et al (2012) Assessment of tumour size in PET/CT lung cancer studies: PET- and CT-based methods compared to pathology. EJNMMI Res 2:56CrossRef
4.
go back to reference Frings V, de Langen AJ, Smit EF et al (2010) Repeatability of metabolically active volume measurements with 18F-FDG and 18F-FLT PET in non-small cell lung cancer. J Nucl Med 51:1870–1877CrossRef Frings V, de Langen AJ, Smit EF et al (2010) Repeatability of metabolically active volume measurements with 18F-FDG and 18F-FLT PET in non-small cell lung cancer. J Nucl Med 51:1870–1877CrossRef
5.
go back to reference Wang XY, Zhao YF, Liu Y, Yang YK, Zhu Z, Wu N (2017) Comparison of different automated lesion delineation methods for metabolic tumor volume of 18F-FDG PET/CT in patients with stage I lung adenocarcinoma. Medicine (Baltimore) 96(51):e9365CrossRef Wang XY, Zhao YF, Liu Y, Yang YK, Zhu Z, Wu N (2017) Comparison of different automated lesion delineation methods for metabolic tumor volume of 18F-FDG PET/CT in patients with stage I lung adenocarcinoma. Medicine (Baltimore) 96(51):e9365CrossRef
6.
go back to reference Cottereau AS, Lanic H, Mareschal S et al (2016) Molecular profile and FDG-PET/CT total metabolic tumor volume improve risk classification at diagnosis for patients with diffuse large B-cell lymphoma. Clin Cancer Res 22:3801–3809CrossRef Cottereau AS, Lanic H, Mareschal S et al (2016) Molecular profile and FDG-PET/CT total metabolic tumor volume improve risk classification at diagnosis for patients with diffuse large B-cell lymphoma. Clin Cancer Res 22:3801–3809CrossRef
7.
go back to reference Mikhaeel NG, Smith D, Dunn JT et al (2016) Combination of baseline metabolic tumour volume and early response on PET/CT improves progression-free survival prediction in DLBCL. Eur J Nucl Med Mol Imaging 43:1209–1219 Mikhaeel NG, Smith D, Dunn JT et al (2016) Combination of baseline metabolic tumour volume and early response on PET/CT improves progression-free survival prediction in DLBCL. Eur J Nucl Med Mol Imaging 43:1209–1219
8.
go back to reference Sasanelli M, Meignan M, Haioun C et al (2014) Pretherapy metabolic tumour volume is an independent predictor of outcome in patients with diffuse large B-cell lymphoma. Eur J Nucl Med Mol Imaging 41:2017–2022CrossRef Sasanelli M, Meignan M, Haioun C et al (2014) Pretherapy metabolic tumour volume is an independent predictor of outcome in patients with diffuse large B-cell lymphoma. Eur J Nucl Med Mol Imaging 41:2017–2022CrossRef
9.
go back to reference Song MK, Chung JS, Shin HJ et al (2012) Clinical significance of metabolic tumor volume by PET/CT in stages II and III of diffuse large B cell lymphoma without extranodal site involvement. Ann Hematol 91:697–703 Song MK, Chung JS, Shin HJ et al (2012) Clinical significance of metabolic tumor volume by PET/CT in stages II and III of diffuse large B cell lymphoma without extranodal site involvement. Ann Hematol 91:697–703
10.
go back to reference Ilyas H, Mikhaeel NG, Dunn JT et al (2018) Defining the optimal method for measuring baseline metabolic tumour volume in diffuse large B cell lymphoma. Eur J Nucl Med Mol Imaging 45:1142–1154 Ilyas H, Mikhaeel NG, Dunn JT et al (2018) Defining the optimal method for measuring baseline metabolic tumour volume in diffuse large B cell lymphoma. Eur J Nucl Med Mol Imaging 45:1142–1154
11.
go back to reference Kurtz DM, Green MR, Bratman SV et al (2015) Noninvasive monitoring of diffuse large B-cell lymphoma by immunoglobulin high-throughput sequencing. Blood 125:3679–3687 Kurtz DM, Green MR, Bratman SV et al (2015) Noninvasive monitoring of diffuse large B-cell lymphoma by immunoglobulin high-throughput sequencing. Blood 125:3679–3687
12.
go back to reference Meignan M, Sasanelli M, Casasnovas RO et al (2014) Metabolic tumour volumes measured at staging in lymphoma: methodological evaluation on phantom experiments and patients. Eur J Nucl Med Mol Imaging 41:1113–1122 Meignan M, Sasanelli M, Casasnovas RO et al (2014) Metabolic tumour volumes measured at staging in lymphoma: methodological evaluation on phantom experiments and patients. Eur J Nucl Med Mol Imaging 41:1113–1122
13.
go back to reference Kostakoglu L, Chauvie S (2018) Metabolic tumor volume metrics in lymphoma. Semin Nucl Med 48:50–66CrossRef Kostakoglu L, Chauvie S (2018) Metabolic tumor volume metrics in lymphoma. Semin Nucl Med 48:50–66CrossRef
14.
go back to reference Cottereau AS, Hapdey S, Chartier L et al (2017) Baseline total metabolic tumor volume measured with fixed or different adaptive thresholding methods equally predicts outcome in peripheral T cell lymphoma. J Nucl Med 58:276–281 Cottereau AS, Hapdey S, Chartier L et al (2017) Baseline total metabolic tumor volume measured with fixed or different adaptive thresholding methods equally predicts outcome in peripheral T cell lymphoma. J Nucl Med 58:276–281
15.
go back to reference Kanoun S, Tal I, Berriolo-Riedinger A et al (2015) Influence of software tool and methodological aspects of total metabolic tumor volume calculation on baseline [18F]FDG PET to predict survival in Hodgkin lymphoma. PLoS One 10:e0140830CrossRef Kanoun S, Tal I, Berriolo-Riedinger A et al (2015) Influence of software tool and methodological aspects of total metabolic tumor volume calculation on baseline [18F]FDG PET to predict survival in Hodgkin lymphoma. PLoS One 10:e0140830CrossRef
16.
go back to reference Boellaard R (2018) Quantitative oncology molecular analysis suite: ACCURATE [abstract]. J Nucl Med 59(suppl.1):1753 Boellaard R (2018) Quantitative oncology molecular analysis suite: ACCURATE [abstract]. J Nucl Med 59(suppl.1):1753
17.
go back to reference Frings V, van Velden FH, Velasquez LM et al (2014) Repeatability of metabolically active tumor volume measurements with FDG PET/CT in advanced gastrointestinal malignancies: a multicenter study. Radiology. 273:539–548 Frings V, van Velden FH, Velasquez LM et al (2014) Repeatability of metabolically active tumor volume measurements with FDG PET/CT in advanced gastrointestinal malignancies: a multicenter study. Radiology. 273:539–548
18.
go back to reference Schaefer A, Vermandel M, Baillet C et al (2016) Impact of consensus contours from multiple PET segmentation methods on the accuracy of functional volume delineation. Eur J Nucl Med Mol Imaging 43:911–924 Schaefer A, Vermandel M, Baillet C et al (2016) Impact of consensus contours from multiple PET segmentation methods on the accuracy of functional volume delineation. Eur J Nucl Med Mol Imaging 43:911–924
19.
go back to reference McGraw KO, Wong SP (1996) Forming inferences about some intraclass correlation coefficients. Psychol Methods 1:30–46CrossRef McGraw KO, Wong SP (1996) Forming inferences about some intraclass correlation coefficients. Psychol Methods 1:30–46CrossRef
20.
go back to reference Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163CrossRef Koo TK, Li MY (2016) A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 15:155–163CrossRef
21.
go back to reference Portney LG, Watkins MP (2009) Intraclass correlation coefficient (ICC). In: Foundations of clinical research: applications to practice. Pearson Prentice Hall, Upper Saddle River, New Jersey, pp 588–598 Portney LG, Watkins MP (2009) Intraclass correlation coefficient (ICC). In: Foundations of clinical research: applications to practice. Pearson Prentice Hall, Upper Saddle River, New Jersey, pp 588–598
22.
go back to reference Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1:307–310CrossRef Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1:307–310CrossRef
24.
go back to reference Ceriani L, Milan L, Johnson PWM et al (2019) Baseline PET features to predict prognosis in primary mediastinal B cell lymphoma: a comparative analysis of different methods for measuring baseline metabolic tumour volume. Eur J Nucl Med Mol Imaging 46:1334–1344CrossRef Ceriani L, Milan L, Johnson PWM et al (2019) Baseline PET features to predict prognosis in primary mediastinal B cell lymphoma: a comparative analysis of different methods for measuring baseline metabolic tumour volume. Eur J Nucl Med Mol Imaging 46:1334–1344CrossRef
25.
go back to reference Barrington SF, Meignan MA (2019) Time to prepare for risk adaptation in lymphoma by standardising measurement of metabolic tumour burden. J Nucl Med 60:1096–1102CrossRef Barrington SF, Meignan MA (2019) Time to prepare for risk adaptation in lymphoma by standardising measurement of metabolic tumour burden. J Nucl Med 60:1096–1102CrossRef
26.
go back to reference Parvez A, Tau N, Hussey D, Maganti M, Metser U (2018) (18)F-FDG PET/CT metabolic tumor parameters and radiomics features in aggressive non-Hodgkin’s lymphoma as predictors of treatment outcome and survival. Ann Nucl Med 32:410–416CrossRef Parvez A, Tau N, Hussey D, Maganti M, Metser U (2018) (18)F-FDG PET/CT metabolic tumor parameters and radiomics features in aggressive non-Hodgkin’s lymphoma as predictors of treatment outcome and survival. Ann Nucl Med 32:410–416CrossRef
Metadata
Title
Optimizing Workflows for Fast and Reliable Metabolic Tumor Volume Measurements in Diffuse Large B Cell Lymphoma
Authors
Coreline N. Burggraaff
Fareen Rahman
Isabelle Kaßner
Simone Pieplenbosch
Sally F. Barrington
Yvonne W.S. Jauw
Gerben J.C. Zwezerijnen
Stefan Müller
Otto S. Hoekstra
Josée M. Zijlstra
Henrica C.W. De Vet
Ronald Boellaard
On behalf of the PETRA Consortium
Publication date
01-08-2020
Publisher
Springer International Publishing
Published in
Molecular Imaging and Biology / Issue 4/2020
Print ISSN: 1536-1632
Electronic ISSN: 1860-2002
DOI
https://doi.org/10.1007/s11307-020-01474-z

Other articles of this Issue 4/2020

Molecular Imaging and Biology 4/2020 Go to the issue