Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 11/2013

01-10-2013 | Original Article

Robustness of intratumour 18F-FDG PET uptake heterogeneity quantification for therapy response prediction in oesophageal carcinoma

Authors: Mathieu Hatt, Florent Tixier, Catherine Cheze Le Rest, Olivier Pradier, Dimitris Visvikis

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 11/2013

Login to get access

Abstract

Purpose

Intratumour uptake heterogeneity in PET quantified in terms of textural features for response to therapy has been investigated in several studies, including assessment of their robustness for reconstruction and physiological reproducibility. However, there has been no thorough assessment of the potential impact of preprocessing steps on the resulting quantification and its predictive value. The goal of this work was to assess the robustness of PET heterogeneity in textural features for delineation of functional volumes and partial volume correction (PVC).

Methods

This retrospective analysis included 50 patients with oesophageal cancer. PVC of each PET image was performed. Tumour volumes were determined using fixed and adaptive thresholding, and the fuzzy locally adaptive Bayesian algorithm, and heterogeneity was quantified using local and regional textural features. Differences in the absolute values of the image-derived parameters considered were assessed using Bland-Altman analysis. The impact on their predictive value for the identification of patient nonresponders was assessed by comparing areas under the receiver operating characteristic curves.

Results

Heterogeneity parameters were more dependent on delineation than on PVC. The parameters most sensitive to delineation and PVC were regional ones (intensity variability and size zone variability), whereas local parameters such as entropy and homogeneity were the most robust. Despite the large differences in absolute values obtained from different delineation methods or after PVC, these differences did not necessarily translate into a significant impact on their predictive value.

Conclusion

Parameters such as entropy, homogeneity, dissimilarity (for local heterogeneity characterization) and zone percentage (for regional characterization) should be preferred. This selection is based on a demonstrated high differentiation power in terms of predicting response, as well as a significant robustness with respect to the delineation method used and the partial volume effects.
Literature
1.
go back to reference Krause BJ, Schwarzenbock S, Souvatzoglou M. FDG PET and PET/CT. Recent Results Cancer Res. 2013;187:351–69.PubMedCrossRef Krause BJ, Schwarzenbock S, Souvatzoglou M. FDG PET and PET/CT. Recent Results Cancer Res. 2013;187:351–69.PubMedCrossRef
2.
go back to reference Jarritt PH, Carson KJ, Hounsell AR, Visvikis D. The role of PET/CT scanning in radiotherapy planning. Br J Radiol. 2006;79(Spec No 1):S27–35.PubMedCrossRef Jarritt PH, Carson KJ, Hounsell AR, Visvikis D. The role of PET/CT scanning in radiotherapy planning. Br J Radiol. 2006;79(Spec No 1):S27–35.PubMedCrossRef
3.
go back to reference Herrmann K, Benz MR, Krause BJ, Pomykala KL, Buck AK, Czernin J. (18)F-FDG-PET/CT in evaluating response to therapy in solid tumors: where we are and where we can go. Q J Nucl Med Mol Imaging. 2011;55:620–32.PubMed Herrmann K, Benz MR, Krause BJ, Pomykala KL, Buck AK, Czernin J. (18)F-FDG-PET/CT in evaluating response to therapy in solid tumors: where we are and where we can go. Q J Nucl Med Mol Imaging. 2011;55:620–32.PubMed
4.
go back to reference Liao S, Penney BC, Wroblewski K, Zhang H, Simon CA, Kampalath R, et al. Prognostic value of metabolic tumor burden on 18F-FDG PET in nonsurgical patients with non-small cell lung cancer. Eur J Nucl Med Mol Imaging. 2012;39:27–38.PubMedCrossRef Liao S, Penney BC, Wroblewski K, Zhang H, Simon CA, Kampalath R, et al. Prognostic value of metabolic tumor burden on 18F-FDG PET in nonsurgical patients with non-small cell lung cancer. Eur J Nucl Med Mol Imaging. 2012;39:27–38.PubMedCrossRef
5.
go back to reference Hatt M, Visvikis D, Pradier O, Cheze-le Rest C. Baseline (18)F-FDG PET image-derived parameters for therapy response prediction in oesophageal cancer. Eur J Nucl Med Mol Imaging. 2011;38:1595–606.PubMedCrossRef Hatt M, Visvikis D, Pradier O, Cheze-le Rest C. Baseline (18)F-FDG PET image-derived parameters for therapy response prediction in oesophageal cancer. Eur J Nucl Med Mol Imaging. 2011;38:1595–606.PubMedCrossRef
6.
go back to reference Deron P, Mertens K, Goethals I, Rottey S, Duprez F, De Neve W, et al. Metabolic tumour volume. Prognostic value in locally advanced squamous cell carcinoma of the head and neck. Nuklearmedizin. 2011;50:141–6.PubMedCrossRef Deron P, Mertens K, Goethals I, Rottey S, Duprez F, De Neve W, et al. Metabolic tumour volume. Prognostic value in locally advanced squamous cell carcinoma of the head and neck. Nuklearmedizin. 2011;50:141–6.PubMedCrossRef
7.
go back to reference Melton GB, Lavely WC, Jacene HA, Schulick RD, Choti MA, Wahl RL, et al. Efficacy of preoperative combined 18-fluorodeoxyglucose positron emission tomography and computed tomography for assessing primary rectal cancer response to neoadjuvant therapy. J Gastrointest Surg. 2007;11:961–9. discussion 969.PubMedCrossRef Melton GB, Lavely WC, Jacene HA, Schulick RD, Choti MA, Wahl RL, et al. Efficacy of preoperative combined 18-fluorodeoxyglucose positron emission tomography and computed tomography for assessing primary rectal cancer response to neoadjuvant therapy. J Gastrointest Surg. 2007;11:961–9. discussion 969.PubMedCrossRef
8.
go back to reference Hatt M, Groheux D, Martineau A, Espie M, Hindie E, Giacchetti S, et al. Comparison between 18F-FDG PET image-derived indices for early prediction of response to neoadjuvant chemotherapy in breast cancer. J Nucl Med. 2013;54:341–9.PubMedCrossRef Hatt M, Groheux D, Martineau A, Espie M, Hindie E, Giacchetti S, et al. Comparison between 18F-FDG PET image-derived indices for early prediction of response to neoadjuvant chemotherapy in breast cancer. J Nucl Med. 2013;54:341–9.PubMedCrossRef
9.
go back to reference Lee HY, Hyun SH, Lee KS, Kim BT, Kim J, Shim YM, et al. Volume-based parameter of 18F-FDG PET/CT in malignant pleural mesothelioma: prediction of therapeutic response and prognostic implications. Ann Surg Oncol. 2010;17:2787–94.PubMedCrossRef Lee HY, Hyun SH, Lee KS, Kim BT, Kim J, Shim YM, et al. Volume-based parameter of 18F-FDG PET/CT in malignant pleural mesothelioma: prediction of therapeutic response and prognostic implications. Ann Surg Oncol. 2010;17:2787–94.PubMedCrossRef
10.
go back to reference Cazaentre T, Morschhauser F, Vermandel M, Betrouni N, Prangere T, Steinling M, et al. Pre-therapy 18F-FDG PET quantitative parameters help in predicting the response to radioimmunotherapy in non-Hodgkin lymphoma. Eur J Nucl Med Mol Imaging. 2010;37:494–504.PubMedCrossRef Cazaentre T, Morschhauser F, Vermandel M, Betrouni N, Prangere T, Steinling M, et al. Pre-therapy 18F-FDG PET quantitative parameters help in predicting the response to radioimmunotherapy in non-Hodgkin lymphoma. Eur J Nucl Med Mol Imaging. 2010;37:494–504.PubMedCrossRef
11.
go back to reference Basu S, Kwee TC, Gatenby R, Saboury B, Torigian DA, Alavi A. Evolving role of molecular imaging with PET in detecting and characterizing heterogeneity of cancer tissue at the primary and metastatic sites, a plausible explanation for failed attempts to cure malignant disorders. Eur J Nucl Med Mol Imaging. 2011;38:987–91.PubMedCrossRef Basu S, Kwee TC, Gatenby R, Saboury B, Torigian DA, Alavi A. Evolving role of molecular imaging with PET in detecting and characterizing heterogeneity of cancer tissue at the primary and metastatic sites, a plausible explanation for failed attempts to cure malignant disorders. Eur J Nucl Med Mol Imaging. 2011;38:987–91.PubMedCrossRef
12.
go back to reference Visvikis D, Hatt M, Tixier F, Cheze Le Rest C. The age of reason for FDG PET image-derived indices. Eur J Nucl Med Mol Imaging. 2012;39:1670–2.PubMedCrossRef Visvikis D, Hatt M, Tixier F, Cheze Le Rest C. The age of reason for FDG PET image-derived indices. Eur J Nucl Med Mol Imaging. 2012;39:1670–2.PubMedCrossRef
13.
go back to reference Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout R G, Granton P, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48:441–6. Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout R G, Granton P, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48:441–6.
14.
go back to reference Chicklore S, Goh V, Siddique M, Roy A, Marsden PK, Cook GJ. Quantifying tumour heterogeneity in 18F-FDG PET/CT imaging by texture analysis. Eur J Nucl Med Mol Imaging. 2013;40:133–40.PubMedCrossRef Chicklore S, Goh V, Siddique M, Roy A, Marsden PK, Cook GJ. Quantifying tumour heterogeneity in 18F-FDG PET/CT imaging by texture analysis. Eur J Nucl Med Mol Imaging. 2013;40:133–40.PubMedCrossRef
15.
go back to reference Davnall F, Yip CS, Ljungqvist G, Selmi M, Ng F, Sanghera B, et al. Assessment of tumor heterogeneity: an emerging imaging tool for clinical practice? Insights Imaging. 2012;3:573–89.PubMedCrossRef Davnall F, Yip CS, Ljungqvist G, Selmi M, Ng F, Sanghera B, et al. Assessment of tumor heterogeneity: an emerging imaging tool for clinical practice? Insights Imaging. 2012;3:573–89.PubMedCrossRef
16.
go back to reference Cook GJ, Yip C, Siddique M, Goh V, Chicklore S, Roy A, et al. Are pretreatment 18F-FDG PET tumor textural features in non-small cell lung cancer associated with response and survival after chemoradiotherapy? J Nucl Med. 2013;54:19–26.PubMedCrossRef Cook GJ, Yip C, Siddique M, Goh V, Chicklore S, Roy A, et al. Are pretreatment 18F-FDG PET tumor textural features in non-small cell lung cancer associated with response and survival after chemoradiotherapy? J Nucl Med. 2013;54:19–26.PubMedCrossRef
17.
go back to reference O’Sullivan F, Wolsztynski E, O’Sullivan J, Richards T, Conrad E, Eary J. A statistical modeling approach to the analysis of spatial patterns of FDG-PET uptake in human sarcoma. IEEE Trans Med Imaging. 2011;30:2059–71.PubMedCrossRef O’Sullivan F, Wolsztynski E, O’Sullivan J, Richards T, Conrad E, Eary J. A statistical modeling approach to the analysis of spatial patterns of FDG-PET uptake in human sarcoma. IEEE Trans Med Imaging. 2011;30:2059–71.PubMedCrossRef
18.
go back to reference Tixier F, Le Rest CC, Hatt M, Albarghach N, Pradier O, Metges JP, 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;52:369–78.PubMedCrossRef Tixier F, Le Rest CC, Hatt M, Albarghach N, Pradier O, Metges JP, 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;52:369–78.PubMedCrossRef
19.
go back to reference Tan S, Kligerman S, Chen W, Lu M, Kim G, Feigenberg S, et al. Spatial-temporal [(18)F]FDG-PET features for predicting pathologic response of esophageal cancer to neoadjuvant chemoradiation therapy. Int J Radiat Oncol Biol Phys. 2013;85:1375–82.PubMedCrossRef Tan S, Kligerman S, Chen W, Lu M, Kim G, Feigenberg S, et al. Spatial-temporal [(18)F]FDG-PET features for predicting pathologic response of esophageal cancer to neoadjuvant chemoradiation therapy. Int J Radiat Oncol Biol Phys. 2013;85:1375–82.PubMedCrossRef
20.
go back to reference El Naqa I, Grigsby P, Apte A, Kidd E, Donnelly E, Khullar D, et al. Exploring feature-based approaches in PET images for predicting cancer treatment outcomes. Pattern Recognit. 2009;42:1162–71.PubMedCrossRef El Naqa I, Grigsby P, Apte A, Kidd E, Donnelly E, Khullar D, et al. Exploring feature-based approaches in PET images for predicting cancer treatment outcomes. Pattern Recognit. 2009;42:1162–71.PubMedCrossRef
21.
go back to reference Miller TR, Pinkus E, Dehdashti F, Grigsby PW. Improved prognostic value of 18F-FDG PET using a simple visual analysis of tumor characteristics in patients with cervical cancer. J Nucl Med. 2003;44:192–7.PubMed Miller TR, Pinkus E, Dehdashti F, Grigsby PW. Improved prognostic value of 18F-FDG PET using a simple visual analysis of tumor characteristics in patients with cervical cancer. J Nucl Med. 2003;44:192–7.PubMed
22.
go back to reference van Velden FH, Cheebsumon P, Yaqub M, Smit EF, Hoekstra OS, Lammertsma AA, et al. Evaluation of a cumulative SUV-volume histogram method for parameterizing heterogeneous intratumoural FDG uptake in non-small cell lung cancer PET studies. Eur J Nucl Med Mol Imaging. 2011;38:1636–47.PubMedCrossRef van Velden FH, Cheebsumon P, Yaqub M, Smit EF, Hoekstra OS, Lammertsma AA, et al. Evaluation of a cumulative SUV-volume histogram method for parameterizing heterogeneous intratumoural FDG uptake in non-small cell lung cancer PET studies. Eur J Nucl Med Mol Imaging. 2011;38:1636–47.PubMedCrossRef
23.
go back to reference Galavis PE, Hollensen C, Jallow N, Paliwal B, Jeraj R. Variability of textural features in FDG PET images due to different acquisition modes and reconstruction parameters. Acta Oncol. 2010;49:1012–6.PubMedCrossRef Galavis PE, Hollensen C, Jallow N, Paliwal B, Jeraj R. Variability of textural features in FDG PET images due to different acquisition modes and reconstruction parameters. Acta Oncol. 2010;49:1012–6.PubMedCrossRef
24.
go back to reference Tixier F, Hatt M, Cheze Le Rest C, Le Pogam A, Corcos L, Visvikis D. Reproducibility of tumor uptake heterogeneity characterization through textural feature analysis in 18F-FDG PET imaging. J Nucl Med. 2012;53:693–700.PubMedCrossRef Tixier F, Hatt M, Cheze Le Rest C, Le Pogam A, Corcos L, Visvikis D. Reproducibility of tumor uptake heterogeneity characterization through textural feature analysis in 18F-FDG PET imaging. J Nucl Med. 2012;53:693–700.PubMedCrossRef
25.
go back to reference Visvikis D, Turzo A, Gouret A, Damine P, Lamare F, Bizais Y, et al. Characterisation of SUV accuracy in FDG PET using 3-D RAMLA and the Philips Allegro PET scanner. J Nucl Med. 2004;45:103. Visvikis D, Turzo A, Gouret A, Damine P, Lamare F, Bizais Y, et al. Characterisation of SUV accuracy in FDG PET using 3-D RAMLA and the Philips Allegro PET scanner. J Nucl Med. 2004;45:103.
26.
go back to reference Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst. 2000;92:205–16.PubMedCrossRef Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst. 2000;92:205–16.PubMedCrossRef
27.
go back to reference Erdi YE, Mawlawi O, Larson SM, Imbriaco M, Yeung H, Finn R, et al. Segmentation of lung lesion volume by adaptive positron emission tomography image thresholding. Cancer. 1997;80:2505–9.PubMedCrossRef Erdi YE, Mawlawi O, Larson SM, Imbriaco M, Yeung H, Finn R, et al. Segmentation of lung lesion volume by adaptive positron emission tomography image thresholding. Cancer. 1997;80:2505–9.PubMedCrossRef
28.
go back to reference Nestle U, Kremp S, Schaefer-Schuler A, Sebastian-Welsch C, Hellwig D, Rube C, et al. Comparison of different methods for delineation of 18F-FDG PET-positive tissue for target volume definition in radiotherapy of patients with non-small cell lung cancer. J Nucl Med. 2005;46:1342–8.PubMed Nestle U, Kremp S, Schaefer-Schuler A, Sebastian-Welsch C, Hellwig D, Rube C, et al. Comparison of different methods for delineation of 18F-FDG PET-positive tissue for target volume definition in radiotherapy of patients with non-small cell lung cancer. J Nucl Med. 2005;46:1342–8.PubMed
29.
go back to reference Hatt M, Cheze le Rest C, Turzo A, Roux C, Visvikis D. A fuzzy locally adaptive Bayesian segmentation approach for volume determination in PET. IEEE Trans Med Imaging. 2009;28:881–93.PubMedCrossRef Hatt M, Cheze le Rest C, Turzo A, Roux C, Visvikis D. A fuzzy locally adaptive Bayesian segmentation approach for volume determination in PET. IEEE Trans Med Imaging. 2009;28:881–93.PubMedCrossRef
30.
go back to reference Hatt M, Cheze Le Rest C, Albarghach N, Pradier O, Visvikis D. PET functional volume delineation: a robustness and repeatability study. Eur J Nucl Med Mol Imaging. 2011;38:663–72.PubMedCrossRef Hatt M, Cheze Le Rest C, Albarghach N, Pradier O, Visvikis D. PET functional volume delineation: a robustness and repeatability study. Eur J Nucl Med Mol Imaging. 2011;38:663–72.PubMedCrossRef
31.
go back to reference Hatt M, Cheze-Le Rest C, Aboagye EO, Kenny LM, Rosso L, Turkheimer FE, et al. Reproducibility of 18F-FDG and 3′-deoxy-3′-18F-fluorothymidine PET tumor volume measurements. J Nucl Med. 2010;51:1368–76.PubMedCrossRef Hatt M, Cheze-Le Rest C, Aboagye EO, Kenny LM, Rosso L, Turkheimer FE, et al. Reproducibility of 18F-FDG and 3′-deoxy-3′-18F-fluorothymidine PET tumor volume measurements. J Nucl Med. 2010;51:1368–76.PubMedCrossRef
32.
go back to reference Hatt M, Cheze le Rest C, Descourt P, Dekker A, De Ruysscher D, Oellers M, et al. Accurate automatic delineation of heterogeneous functional volumes in positron emission tomography for oncology applications. Int J Radiat Oncol Biol Phys. 2010;77:301–8.PubMedCrossRef Hatt M, Cheze le Rest C, Descourt P, Dekker A, De Ruysscher D, Oellers M, et al. Accurate automatic delineation of heterogeneous functional volumes in positron emission tomography for oncology applications. Int J Radiat Oncol Biol Phys. 2010;77:301–8.PubMedCrossRef
33.
go back to reference Boussion N, Cheze Le Rest C, Hatt M, Visvikis D. Incorporation of wavelet-based denoising in iterative deconvolution for partial volume correction in whole-body PET imaging. Eur J Nucl Med Mol Imaging. 2009;36:1064–75.PubMedCrossRef Boussion N, Cheze Le Rest C, Hatt M, Visvikis D. Incorporation of wavelet-based denoising in iterative deconvolution for partial volume correction in whole-body PET imaging. Eur J Nucl Med Mol Imaging. 2009;36:1064–75.PubMedCrossRef
34.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44:837–45.PubMedCrossRef DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44:837–45.PubMedCrossRef
Metadata
Title
Robustness of intratumour 18F-FDG PET uptake heterogeneity quantification for therapy response prediction in oesophageal carcinoma
Authors
Mathieu Hatt
Florent Tixier
Catherine Cheze Le Rest
Olivier Pradier
Dimitris Visvikis
Publication date
01-10-2013
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 11/2013
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-013-2486-8

Other articles of this Issue 11/2013

European Journal of Nuclear Medicine and Molecular Imaging 11/2013 Go to the issue