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Published in: European Radiology 1/2018

Open Access 01-01-2018 | Oncology

Development and validation of a prognostic model incorporating texture analysis derived from standardised segmentation of PET in patients with oesophageal cancer

Authors: Kieran G Foley, Robert K. Hills, Beatrice Berthon, Christopher Marshall, Craig Parkinson, Wyn G. Lewis, Tom D. L. Crosby, Emiliano Spezi, Stuart Ashley Roberts

Published in: European Radiology | Issue 1/2018

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Abstract

Objectives

This retrospective cohort study developed a prognostic model incorporating PET texture analysis in patients with oesophageal cancer (OC). Internal validation of the model was performed.

Methods

Consecutive OC patients (n = 403) were chronologically separated into development (n = 302, September 2010-September 2014, median age = 67.0, males = 227, adenocarcinomas = 237) and validation cohorts (n = 101, September 2014-July 2015, median age = 69.0, males = 78, adenocarcinomas = 79). Texture metrics were obtained using a machine-learning algorithm for automatic PET segmentation. A Cox regression model including age, radiological stage, treatment and 16 texture metrics was developed. Patients were stratified into quartiles according to a prognostic score derived from the model. A p-value < 0.05 was considered statistically significant. Primary outcome was overall survival (OS).

Results

Six variables were significantly and independently associated with OS: age [HR =1.02 (95% CI 1.01-1.04), p < 0.001], radiological stage [1.49 (1.20-1.84), p < 0.001], treatment [0.34 (0.24–0.47), p < 0.001], log(TLG) [5.74 (1.44–22.83), p = 0.013], log(Histogram Energy) [0.27 (0.10–0.74), p = 0.011] and Histogram Kurtosis [1.22 (1.04–1.44), p = 0.017]. The prognostic score demonstrated significant differences in OS between quartiles in both the development (X2 143.14, df 3, p < 0.001) and validation cohorts (X2 20.621, df 3, p < 0.001).

Conclusions

This prognostic model can risk stratify patients and demonstrates the additional benefit of PET texture analysis in OC staging.

Key points

PET texture analysis adds prognostic value to oesophageal cancer staging.
Texture metrics are independently and significantly associated with overall survival.
A prognostic model including texture analysis can help risk stratify patients.
Appendix
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Literature
1.
go back to reference Aerts HJ, Velazquez ER, Leijenaar RT et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006PubMedPubMedCentral Aerts HJ, Velazquez ER, Leijenaar RT et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006PubMedPubMedCentral
2.
go back to reference Lambin P, Rios-Velazquez E, Leijenaar R et al (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446CrossRefPubMedPubMedCentral Lambin P, Rios-Velazquez E, Leijenaar R et al (2012) Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer 48:441–446CrossRefPubMedPubMedCentral
3.
go back to reference Gillies RJ, Kinahan PE, Hricak H (2016) Radiomics: images are more than pictures, they are data. Radiology 278:563–577CrossRefPubMed Gillies RJ, Kinahan PE, Hricak H (2016) Radiomics: images are more than pictures, they are data. Radiology 278:563–577CrossRefPubMed
4.
go back to reference Gerlinger M, Rowan AJ, Horswell S et al (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366:883–892CrossRefPubMedPubMedCentral Gerlinger M, Rowan AJ, Horswell S et al (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366:883–892CrossRefPubMedPubMedCentral
5.
go back to reference Orlhac F, Soussan M, Maisonobe JA, Garcia CA, Vanderlinden B, Buvat I (2014) 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 55:414–422CrossRefPubMed Orlhac F, Soussan M, Maisonobe JA, Garcia CA, Vanderlinden B, Buvat I (2014) 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 55:414–422CrossRefPubMed
6.
go back to reference Hatt M, Majdoub M, Vallieres M et al (2015) 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 56:38–44CrossRefPubMed Hatt M, Majdoub M, Vallieres M et al (2015) 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 56:38–44CrossRefPubMed
7.
go back to reference van Rossum PS, Fried DV, Zhang L et al (2016) The incremental value of subjective and quantitative assessment of 18F-FDG PET for the prediction of pathologic complete response to preoperative chemoradiotherapy in esophageal cancer. J Nucl Med 57:691–700CrossRefPubMed van Rossum PS, Fried DV, Zhang L et al (2016) The incremental value of subjective and quantitative assessment of 18F-FDG PET for the prediction of pathologic complete response to preoperative chemoradiotherapy in esophageal cancer. J Nucl Med 57:691–700CrossRefPubMed
8.
go back to reference Sobin LH, Gospodarowicz MK, Wittekind CH (2009) UICC TNM Classification of Malignant Tumours, 7th edn. Wiley, New York Sobin LH, Gospodarowicz MK, Wittekind CH (2009) UICC TNM Classification of Malignant Tumours, 7th edn. Wiley, New York
9.
go back to reference Berthon B, Marshall C, Evans M, Spezi E (2016) ATLAAS: an automatic decision tree-based learning algorithm for advanced image segmentation in positron emission tomography. Phys Med Biol 61:4855–4869CrossRefPubMed Berthon B, Marshall C, Evans M, Spezi E (2016) ATLAAS: an automatic decision tree-based learning algorithm for advanced image segmentation in positron emission tomography. Phys Med Biol 61:4855–4869CrossRefPubMed
10.
go back to reference Deasy JO, Blanco AI, Clark VH (2003) CERR: a computational environment for radiotherapy research. Med Phys 30:979–985CrossRefPubMed Deasy JO, Blanco AI, Clark VH (2003) CERR: a computational environment for radiotherapy research. Med Phys 30:979–985CrossRefPubMed
11.
go back to reference Leijenaar RT, Nalbantov G, Carvalho S et al (2015) The effect of SUV discretization in quantitative FDG-PET radiomics: the need for standardized methodology in tumor texture analysis. Sci Rep 5:11075CrossRefPubMedPubMedCentral Leijenaar RT, Nalbantov G, Carvalho S et al (2015) The effect of SUV discretization in quantitative FDG-PET radiomics: the need for standardized methodology in tumor texture analysis. Sci Rep 5:11075CrossRefPubMedPubMedCentral
12.
go back to reference Wahl RL, Jacene H, Kasamon Y, Lodge MA (2009) From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumours. J Nucl Med 50:1–50CrossRef Wahl RL, Jacene H, Kasamon Y, Lodge MA (2009) From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumours. J Nucl Med 50:1–50CrossRef
13.
go back to reference Haralick RM, Shanmugam K, Dinstein I (1973) Textural features for image classification. IEEE Trans Syst, Man Cybern 3:610–621 Haralick RM, Shanmugam K, Dinstein I (1973) Textural features for image classification. IEEE Trans Syst, Man Cybern 3:610–621
14.
go back to reference Amadasun M, King R (1989) Textural features corresponding to textural properties. IEEE Trans Syst, Man Cybern 19:1264–1273CrossRef Amadasun M, King R (1989) Textural features corresponding to textural properties. IEEE Trans Syst, Man Cybern 19:1264–1273CrossRef
15.
go back to reference Thibault G, Fertil B, Navarro C et al. (2009) Texture indexes and gray level size zone matrix application to cell nuclei classification. Pattern Recognit Inf Process:140–145 Thibault G, Fertil B, Navarro C et al. (2009) Texture indexes and gray level size zone matrix application to cell nuclei classification. Pattern Recognit Inf Process:140–145
16.
go back to reference Tixier F, Le Rest CC, Hatt M et al (2011) Intratumor heterogeneity characterized by textural features on baseline 18F-FDG PET images predicts response to concomitant radiochemotherapy in esophageal cancer. J Nucl Med 52:369–378CrossRefPubMedPubMedCentral Tixier F, Le Rest CC, Hatt M et al (2011) Intratumor heterogeneity characterized by textural features on baseline 18F-FDG PET images predicts response to concomitant radiochemotherapy in esophageal cancer. J Nucl Med 52:369–378CrossRefPubMedPubMedCentral
17.
go back to reference Yip C, Landau D, Kozarski R et al (2014) Primary esophageal cancer: heterogeneity as potential prognostic biomarker in patients treated with definitive chemotherapy and radiation therapy. Radiology 270:141–148CrossRefPubMed Yip C, Landau D, Kozarski R et al (2014) Primary esophageal cancer: heterogeneity as potential prognostic biomarker in patients treated with definitive chemotherapy and radiation therapy. Radiology 270:141–148CrossRefPubMed
18.
go back to reference Hatt M, Tixier F, Cheze Le Rest C, Pradier O, Visvikis D (2013) Robustness of intratumour 18F-FDG PET uptake heterogeneity quantification for therapy response prediction in oesophageal carcinoma. Eur J Nucl Med Mol Imaging 40:1662–1671CrossRefPubMed Hatt M, Tixier F, Cheze Le Rest C, Pradier O, Visvikis D (2013) Robustness of intratumour 18F-FDG PET uptake heterogeneity quantification for therapy response prediction in oesophageal carcinoma. Eur J Nucl Med Mol Imaging 40:1662–1671CrossRefPubMed
19.
go back to reference Wu W, Parmar C, Grossmann P et al (2016) Exploratory study to identify radiomics classifiers for lung cancer histology. Front Oncol 6:71PubMedPubMedCentral Wu W, Parmar C, Grossmann P et al (2016) Exploratory study to identify radiomics classifiers for lung cancer histology. Front Oncol 6:71PubMedPubMedCentral
20.
go back to reference Peduzzi P, Concato J, Kemper E, Holford TR, Feinstein AR (1996) A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol 49:1373–1379CrossRefPubMed Peduzzi P, Concato J, Kemper E, Holford TR, Feinstein AR (1996) A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol 49:1373–1379CrossRefPubMed
21.
go back to reference Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRef Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723CrossRef
22.
go back to reference Moons KG, Kengne AP, Woodward M et al (2012) Risk prediction models: I. Development, internal validation, and assessing the incremental value of a new (bio)marker. Heart 98:683–690CrossRefPubMed Moons KG, Kengne AP, Woodward M et al (2012) Risk prediction models: I. Development, internal validation, and assessing the incremental value of a new (bio)marker. Heart 98:683–690CrossRefPubMed
23.
go back to reference Moons KG, Royston P, Vergouwe Y, Grobbee DE, Altman DG (2009) Prognosis and prognostic research: what, why, and how? BMJ 338:b375CrossRefPubMed Moons KG, Royston P, Vergouwe Y, Grobbee DE, Altman DG (2009) Prognosis and prognostic research: what, why, and how? BMJ 338:b375CrossRefPubMed
24.
go back to reference Blazeby JM, Farndon JR, Donovan J, Alderson D (2000) A prospective longitudinal study examining the quality of life of patients with esophageal carcinoma. Cancer 88:1781–1787CrossRefPubMed Blazeby JM, Farndon JR, Donovan J, Alderson D (2000) A prospective longitudinal study examining the quality of life of patients with esophageal carcinoma. Cancer 88:1781–1787CrossRefPubMed
25.
go back to reference Orlhac F, Theze B, Soussan M, Boisgard R, Buvat I (2016) Multiscale texture analysis: from 18F-FDG PET images to histologic images. J Nucl Med 57:1823–1828CrossRefPubMed Orlhac F, Theze B, Soussan M, Boisgard R, Buvat I (2016) Multiscale texture analysis: from 18F-FDG PET images to histologic images. J Nucl Med 57:1823–1828CrossRefPubMed
26.
go back to reference Yip C, Davnall F, Kozarski R et al (2015) Assessment of changes in tumor heterogeneity following neoadjuvant chemotherapy in primary esophageal cancer. Dis Esophagus 28:172–179CrossRefPubMed Yip C, Davnall F, Kozarski R et al (2015) Assessment of changes in tumor heterogeneity following neoadjuvant chemotherapy in primary esophageal cancer. Dis Esophagus 28:172–179CrossRefPubMed
27.
go back to reference Ganeshan B, Skogen K, Pressney I, Coutroubis D, Miles K (2012) Tumour heterogeneity in oesophageal cancer assessed by CT texture analysis: preliminary evidence of an association with tumour metabolism, stage, and survival. Clin Radiol 67:157–164CrossRefPubMed Ganeshan B, Skogen K, Pressney I, Coutroubis D, Miles K (2012) Tumour heterogeneity in oesophageal cancer assessed by CT texture analysis: preliminary evidence of an association with tumour metabolism, stage, and survival. Clin Radiol 67:157–164CrossRefPubMed
28.
go back to reference Galavis PE, Hollensen C, Jallow N, Paliwal B, Jeraj R (2010) Variability of textural features in FDG PET images due to different acquisition modes and reconstruction parameters. Acta Oncol 49:1012–1016CrossRefPubMedPubMedCentral Galavis PE, Hollensen C, Jallow N, Paliwal B, Jeraj R (2010) Variability of textural features in FDG PET images due to different acquisition modes and reconstruction parameters. Acta Oncol 49:1012–1016CrossRefPubMedPubMedCentral
29.
go back to reference Doumou G, Siddique M, Tsoumpas C, Goh V, Cook GJ (2015) The precision of textural analysis in (18)F-FDG-PET scans of oesophageal cancer. Eur Radiol 25:2805–2812CrossRefPubMed Doumou G, Siddique M, Tsoumpas C, Goh V, Cook GJ (2015) The precision of textural analysis in (18)F-FDG-PET scans of oesophageal cancer. Eur Radiol 25:2805–2812CrossRefPubMed
30.
go back to reference Cook GJR, Siddique M, Taylor BP, Yip C, Chicklore S, Goh V (2014) Radiomics in PET: principles and applications. Clin Transl Imaging 2:269–276CrossRef Cook GJR, Siddique M, Taylor BP, Yip C, Chicklore S, Goh V (2014) Radiomics in PET: principles and applications. Clin Transl Imaging 2:269–276CrossRef
31.
go back to reference Lambin P, Zindler J, Vanneste B et al (2015) Modern clinical research: How rapid learning health care and cohort multiple randomised clinical trials complement traditional evidence based medicine. Acta Oncol 54:1289–1300CrossRefPubMed Lambin P, Zindler J, Vanneste B et al (2015) Modern clinical research: How rapid learning health care and cohort multiple randomised clinical trials complement traditional evidence based medicine. Acta Oncol 54:1289–1300CrossRefPubMed
32.
go back to reference Karran A, Blake P, Chan D et al (2014) Propensity score analysis of oesophageal cancer treatment with surgery or definitive chemoradiotherapy. Br J Surg 101:502–510CrossRefPubMed Karran A, Blake P, Chan D et al (2014) Propensity score analysis of oesophageal cancer treatment with surgery or definitive chemoradiotherapy. Br J Surg 101:502–510CrossRefPubMed
Metadata
Title
Development and validation of a prognostic model incorporating texture analysis derived from standardised segmentation of PET in patients with oesophageal cancer
Authors
Kieran G Foley
Robert K. Hills
Beatrice Berthon
Christopher Marshall
Craig Parkinson
Wyn G. Lewis
Tom D. L. Crosby
Emiliano Spezi
Stuart Ashley Roberts
Publication date
01-01-2018
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 1/2018
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-017-4973-y

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