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Published in: EJNMMI Research 1/2018

Open Access 01-12-2018 | Original research

Radiomics of the primary tumour as a tool to improve 18F-FDG-PET sensitivity in detecting nodal metastases in endometrial cancer

Authors: Elisabetta De Bernardi, Alessandro Buda, Luca Guerra, Debora Vicini, Federica Elisei, Claudio Landoni, Robert Fruscio, Cristina Messa, Cinzia Crivellaro

Published in: EJNMMI Research | Issue 1/2018

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Abstract

Background

A radiomic approach was applied in 18F-FDG PET endometrial cancer, to investigate if imaging features computed on the primary tumour could improve sensitivity in nodal metastases detection. One hundred fifteen women with histologically proven endometrial cancer who underwent preoperative 18F-FDG PET/CT were retrospectively considered. SUV, MTV, TLG, geometrical shape, histograms and texture features were computed inside tumour contours. On a first group of 86 patients (DB1), univariate association with LN metastases was computed by Mann-Whitney test and a neural network multivariate model was developed. Univariate and multivariate models were assessed with leave one out on 20 training sessions and on a second group of 29 patients (DB2). A unified framework combining LN metastases visual detection results and radiomic analysis was also assessed.

Results

Sensitivity and specificity of LN visual detection were 50% and 99% on DB1 and 33% and 95% on DB2, respectively. A unique heterogeneity feature computed on the primary tumour (the zone percentage of the grey level size zone matrix, GLSZM ZP) was able to predict LN metastases better than any other feature or multivariate model (sensitivity and specificity of 75% and 81% on DB1 and of 89% and 80% on DB2). Tumours with LN metastases are in fact generally characterized by a lower GLSZM ZP value, i.e. by the co-presence of high-uptake and low-uptake areas. The combination of visual detection and GLSZM ZP values in a unified framework obtained sensitivity and specificity of 94% and 67% on DB1 and of 89% and 75% on DB2, respectively.

Conclusions

The computation of imaging features on the primary tumour increases nodal staging detection sensitivity in 18F-FDG PET and can be considered for a better patient stratification for treatment selection. Results need a confirmation on larger cohort studies.
Literature
1.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.CrossRefPubMed Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.CrossRefPubMed
2.
go back to reference Bollineni VR, Ytre-Hauge S, Bollineni-Balabay O, Salvesen HB, Haldorsen IS. High diagnostic value of 18F-FDG PET/CT in endometrial cancer: systematic review and meta-analysis of the literature. J Nucl Med. 2016;57(6):879–85.CrossRefPubMed Bollineni VR, Ytre-Hauge S, Bollineni-Balabay O, Salvesen HB, Haldorsen IS. High diagnostic value of 18F-FDG PET/CT in endometrial cancer: systematic review and meta-analysis of the literature. J Nucl Med. 2016;57(6):879–85.CrossRefPubMed
3.
go back to reference Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, et al. Cancer statistics, 2005. CA Cancer J Clin. 2005;55(1):10–30.CrossRefPubMed Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, et al. Cancer statistics, 2005. CA Cancer J Clin. 2005;55(1):10–30.CrossRefPubMed
4.
go back to reference Frederick PJ, Straughn JM Jr. The role of comprehensive surgical staging in patients with endometrial cancer. Cancer Control. 2009;16(1):23–9.CrossRefPubMed Frederick PJ, Straughn JM Jr. The role of comprehensive surgical staging in patients with endometrial cancer. Cancer Control. 2009;16(1):23–9.CrossRefPubMed
5.
go back to reference Lewin SN, Herzog TJ, Barrena Medel NI, Deutsch I, Burke WM, Sun X, et al. Comparative performance of the 2009 international federation of gynecology and obstetrics’ staging system for uterine corpus cancer. Obstet Gynecol. 2010;116(5):1141–9.CrossRefPubMed Lewin SN, Herzog TJ, Barrena Medel NI, Deutsch I, Burke WM, Sun X, et al. Comparative performance of the 2009 international federation of gynecology and obstetrics’ staging system for uterine corpus cancer. Obstet Gynecol. 2010;116(5):1141–9.CrossRefPubMed
6.
go back to reference Benedetti Panici P, Basile S, Maneschi F, Alberto Lissoni A, Signorelli M, Scambia G, et al. Systematic pelvic lymphadenectomy vs. no lymphadenectomy in early-stage endometrial carcinoma: randomized clinical trial. J Natl Cancer Inst. 2008;100(23):1707–16.CrossRefPubMed Benedetti Panici P, Basile S, Maneschi F, Alberto Lissoni A, Signorelli M, Scambia G, et al. Systematic pelvic lymphadenectomy vs. no lymphadenectomy in early-stage endometrial carcinoma: randomized clinical trial. J Natl Cancer Inst. 2008;100(23):1707–16.CrossRefPubMed
7.
go back to reference Chan JK, Cheung MK, Huh WK, Osann K, Husain A, Teng NN, et al. Therapeutic role of lymph node resection in endometrioid corpus cancer: a study of 12,333 patients. Cancer. 2006;107(8):1823–30.CrossRefPubMed Chan JK, Cheung MK, Huh WK, Osann K, Husain A, Teng NN, et al. Therapeutic role of lymph node resection in endometrioid corpus cancer: a study of 12,333 patients. Cancer. 2006;107(8):1823–30.CrossRefPubMed
8.
go back to reference Chan JK, Kapp DS. Role of complete lymphadenectomy in endometrioid uterine cancer. Lancet Oncol. 2007;8(9):831–41.CrossRefPubMed Chan JK, Kapp DS. Role of complete lymphadenectomy in endometrioid uterine cancer. Lancet Oncol. 2007;8(9):831–41.CrossRefPubMed
9.
go back to reference Seracchioli R, Solfrini S, Mabrouk M, Facchini C, Di Donato N, Manuzzi L, et al. Controversies in surgical staging of endometrial cancer. Obstet Gynecol Int. 2010;2010:181963.CrossRefPubMedPubMedCentral Seracchioli R, Solfrini S, Mabrouk M, Facchini C, Di Donato N, Manuzzi L, et al. Controversies in surgical staging of endometrial cancer. Obstet Gynecol Int. 2010;2010:181963.CrossRefPubMedPubMedCentral
10.
go back to reference Kitchener H, Swart AM, Qian Q, Amos C, Parmar MK. Efficacy of systematic pelvic lymphadenectomy in endometrial cancer (MRC ASTEC trial): a randomised study. Lancet. 2009;373(9658):125–36.CrossRefPubMed Kitchener H, Swart AM, Qian Q, Amos C, Parmar MK. Efficacy of systematic pelvic lymphadenectomy in endometrial cancer (MRC ASTEC trial): a randomised study. Lancet. 2009;373(9658):125–36.CrossRefPubMed
11.
go back to reference Cragun JM, Havrilesky LJ, Calingaert B, Synan I, Secord AA, Soper JT, et al. Retrospective analysis of selective lymphadenectomy in apparent early-stage endometrial cancer. J Clin Oncol. 2005;23(16):3668–75.CrossRefPubMed Cragun JM, Havrilesky LJ, Calingaert B, Synan I, Secord AA, Soper JT, et al. Retrospective analysis of selective lymphadenectomy in apparent early-stage endometrial cancer. J Clin Oncol. 2005;23(16):3668–75.CrossRefPubMed
12.
go back to reference Crivellaro C, Baratto L, Dolci C, De Ponti E, Magni S, Elisei F, et al. Sentinel node biopsy in endometrial cancer: an update. Clin Transl Imaging. 2018;6(2):91–100. Crivellaro C, Baratto L, Dolci C, De Ponti E, Magni S, Elisei F, et al. Sentinel node biopsy in endometrial cancer: an update. Clin Transl Imaging. 2018;6(2):91–100.
13.
go back to reference Atri M, Zhang Z, Dehdashti F, Lee SI, Marques H, Ali S, et al. Utility of PET/CT to evaluate retroperitoneal lymph node metastasis in high-risk endometrial cancer: results of ACRIN 6671/GOG 0233 trial. Radiology. 2017;283(2):450–9.CrossRefPubMedPubMedCentral Atri M, Zhang Z, Dehdashti F, Lee SI, Marques H, Ali S, et al. Utility of PET/CT to evaluate retroperitoneal lymph node metastasis in high-risk endometrial cancer: results of ACRIN 6671/GOG 0233 trial. Radiology. 2017;283(2):450–9.CrossRefPubMedPubMedCentral
14.
go back to reference Signorelli M, Guerra L, Buda A, Picchio M, Mangili G, Dell'Anna T, et al. Role of the integrated FDG PET/CT in the surgical management of patients with high risk clinical early stage endometrial cancer: detection of pelvic nodal metastases. Gynecol Oncol. 2009;115(2):231–5.CrossRefPubMed Signorelli M, Guerra L, Buda A, Picchio M, Mangili G, Dell'Anna T, et al. Role of the integrated FDG PET/CT in the surgical management of patients with high risk clinical early stage endometrial cancer: detection of pelvic nodal metastases. Gynecol Oncol. 2009;115(2):231–5.CrossRefPubMed
15.
go back to reference Signorelli M, Crivellaro C, Buda A, Guerra L, Fruscio R, Elisei F, et al. Staging of high-risk endometrial cancer with PET/CT and sentinel lymph node mapping. Clin Nucl Med. 2015;40(10):780–5.CrossRefPubMed Signorelli M, Crivellaro C, Buda A, Guerra L, Fruscio R, Elisei F, et al. Staging of high-risk endometrial cancer with PET/CT and sentinel lymph node mapping. Clin Nucl Med. 2015;40(10):780–5.CrossRefPubMed
16.
go back to reference Tixier F, Vriens D, Cheze-Le Rest C, Hatt M, Disselhorst JA, Oyen WJ, et al. Comparison of tumor uptake heterogeneity characterization between static and parametric 18F-FDG PET images in non-small cell lung cancer. J Nucl Med. 2016;57(7):1033–9.CrossRefPubMed Tixier F, Vriens D, Cheze-Le Rest C, Hatt M, Disselhorst JA, Oyen WJ, et al. Comparison of tumor uptake heterogeneity characterization between static and parametric 18F-FDG PET images in non-small cell lung cancer. J Nucl Med. 2016;57(7):1033–9.CrossRefPubMed
17.
go back to reference Hatt M, Majdoub M, Vallieres M, Tixier F, Le Rest CC, Groheux D, 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.CrossRefPubMed Hatt M, Majdoub M, Vallieres M, Tixier F, Le Rest CC, Groheux D, 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.CrossRefPubMed
18.
go back to reference Hatt M, Tixier F, Pierce L, Kinahan PE, Le Rest CC, Visvikis D. Characterization of PET/CT images using texture analysis: the past, the present... Any future? Eur J Nucl Med Mol Imaging. 2017;44(1):151–65.CrossRefPubMed Hatt M, Tixier F, Pierce L, Kinahan PE, Le Rest CC, Visvikis D. Characterization of PET/CT images using texture analysis: the past, the present... Any future? Eur J Nucl Med Mol Imaging. 2017;44(1):151–65.CrossRefPubMed
19.
go back to reference Hatt M, Tixier F, Cheze Le Rest C, Pradier O, Visvikis D. Robustness of intratumour (1)(8)F-FDG PET uptake heterogeneity quantification for therapy response prediction in oesophageal carcinoma. Eur J Nucl Med Mol Imaging. 2013;40(11):1662–71.CrossRefPubMed Hatt M, Tixier F, Cheze Le Rest C, Pradier O, Visvikis D. Robustness of intratumour (1)(8)F-FDG PET uptake heterogeneity quantification for therapy response prediction in oesophageal carcinoma. Eur J Nucl Med Mol Imaging. 2013;40(11):1662–71.CrossRefPubMed
20.
go back to reference Orlhac F, Soussan M, Chouahnia K, Martinod E, Buvat I. 18F-FDG PET-derived textural indices reflect tissue-specific uptake pattern in non-small cell lung Cancer. PLoS One. 2015;10(12):e0145063.CrossRefPubMedPubMedCentral Orlhac F, Soussan M, Chouahnia K, Martinod E, Buvat I. 18F-FDG PET-derived textural indices reflect tissue-specific uptake pattern in non-small cell lung Cancer. PLoS One. 2015;10(12):e0145063.CrossRefPubMedPubMedCentral
21.
go back to reference Shen WC, Chen SW, Liang JA, Hsieh TC, Yen KY, Kao CH. [18]Fluorodeoxyglucose positron emission tomography for the textural features of cervical cancer associated with lymph node metastasis and histological type. Eur J Nucl Med Mol Imaging. 2017;44(10):1721–31.CrossRefPubMed Shen WC, Chen SW, Liang JA, Hsieh TC, Yen KY, Kao CH. [18]Fluorodeoxyglucose positron emission tomography for the textural features of cervical cancer associated with lymph node metastasis and histological type. Eur J Nucl Med Mol Imaging. 2017;44(10):1721–31.CrossRefPubMed
22.
go back to reference Boellaard R, Delgado-Bolton R, Oyen WJ, Giammarile F, Tatsch K, Eschner W, 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.CrossRefPubMed Boellaard R, Delgado-Bolton R, Oyen WJ, Giammarile F, Tatsch K, Eschner W, 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.CrossRefPubMed
23.
go back to reference Crivellaro C, Signorelli M, Guerra L, De Ponti E, Pirovano C, Fruscio R, et al. Tailoring systematic lymphadenectomy in high-risk clinical early stage endometrial cancer: the role of 18F-FDG PET/CT. Gynecol Oncol. 2013;130(2):306–11.CrossRefPubMed Crivellaro C, Signorelli M, Guerra L, De Ponti E, Pirovano C, Fruscio R, et al. Tailoring systematic lymphadenectomy in high-risk clinical early stage endometrial cancer: the role of 18F-FDG PET/CT. Gynecol Oncol. 2013;130(2):306–11.CrossRefPubMed
24.
go back to reference Fang YH, Lin CY, Shih MJ, Wang HM, Ho TY, Liao CT, et al. Development and evaluation of an open-source software package “CGITA” for quantifying tumor heterogeneity with molecular images. Biomed Res Int. 2014;2014:248505.PubMedPubMedCentral Fang YH, Lin CY, Shih MJ, Wang HM, Ho TY, Liao CT, et al. Development and evaluation of an open-source software package “CGITA” for quantifying tumor heterogeneity with molecular images. Biomed Res Int. 2014;2014:248505.PubMedPubMedCentral
25.
go back to reference Orlhac F, Soussan M, Maisonobe JA, Garcia CA, Vanderlinden B, Buvat I. 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.CrossRefPubMed Orlhac F, Soussan M, Maisonobe JA, Garcia CA, Vanderlinden B, Buvat I. 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.CrossRefPubMed
26.
go back to reference Tesar L, Shimizu A, Smutek D, Kobatake H, Nawano S. Medical image analysis of 3D CT images based on extension of Haralick texture features. Comput Med Imaging Graph. 2008;32(6):513–20.CrossRefPubMed Tesar L, Shimizu A, Smutek D, Kobatake H, Nawano S. Medical image analysis of 3D CT images based on extension of Haralick texture features. Comput Med Imaging Graph. 2008;32(6):513–20.CrossRefPubMed
27.
go back to reference Haralick RM, Shanmugam K. Textural features for image classification. IEEE Transactions on systems, man, and cybernetics. 1973;3(6):610–21.CrossRef Haralick RM, Shanmugam K. Textural features for image classification. IEEE Transactions on systems, man, and cybernetics. 1973;3(6):610–21.CrossRef
28.
go back to reference Kurani AS, Xu DH, Furst J, Raicu DS. Co–occurrence matrices for volumetric data. In: The 7th IASTED International Conference on Computer Graphics and Imaging – CGIM 2004, Kauai, Hawaii, US; 2004. Kurani AS, Xu DH, Furst J, Raicu DS. Co–occurrence matrices for volumetric data. In: The 7th IASTED International Conference on Computer Graphics and Imaging – CGIM 2004, Kauai, Hawaii, US; 2004.
29.
30.
go back to reference Thibault G, Fertil B, Navarro C, Pereira S, Cau P, Levy N, et al. Texture indexes and gray level size zone matrix. Application to cell nuclei classification. In: 10th international conference on pattern recognition and information processing, PRIP 2009. Minsk; 2009. p. 140–5. Thibault G, Fertil B, Navarro C, Pereira S, Cau P, Levy N, et al. Texture indexes and gray level size zone matrix. Application to cell nuclei classification. In: 10th international conference on pattern recognition and information processing, PRIP 2009. Minsk; 2009. p. 140–5.
31.
go back to reference Amadasun M, King R. Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern. 1989;19:1264–74.CrossRef Amadasun M, King R. Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern. 1989;19:1264–74.CrossRef
32.
go back to reference He D, Wang L. Texture features based on texture spectrum. Journal Pattern Recognition. 1991;24(5):391–9.CrossRef He D, Wang L. Texture features based on texture spectrum. Journal Pattern Recognition. 1991;24(5):391–9.CrossRef
33.
go back to reference Horng MH, Sun YN, Lin XZ. Texture feature coding method for classification of liver sonography. Comput Med Imaging Graph 2002;26:33–42. Horng MH, Sun YN, Lin XZ. Texture feature coding method for classification of liver sonography. Comput Med Imaging Graph 2002;26:33–42.
34.
go back to reference Sun C, Wee W. Neighboring gray level dependence matrix for texture classification. Computer Vision, Graphics, and Image Processing. 1983;23:341–52.CrossRef Sun C, Wee W. Neighboring gray level dependence matrix for texture classification. Computer Vision, Graphics, and Image Processing. 1983;23:341–52.CrossRef
35.
go back to reference Tixier F, Hatt M, Le Rest CC, Le Pogam A, Corcos L, Visvikis D. Reproducibility of tumor uptake heterogeneity characterization through textural feature analysis in 18F-FDG PET. J Nucl Med. 2012;53(5):693–700.CrossRefPubMedPubMedCentral Tixier F, Hatt M, Le Rest CC, Le Pogam A, Corcos L, Visvikis D. Reproducibility of tumor uptake heterogeneity characterization through textural feature analysis in 18F-FDG PET. J Nucl Med. 2012;53(5):693–700.CrossRefPubMedPubMedCentral
36.
go back to reference Nakamura K, Hongo A, Kodama J, Hiramatsu Y. The measurement of SUVmax of the primary tumor is predictive of prognosis for patients with endometrial cancer. Gynecol Oncol. 2011;123(1):82–7.CrossRefPubMed Nakamura K, Hongo A, Kodama J, Hiramatsu Y. The measurement of SUVmax of the primary tumor is predictive of prognosis for patients with endometrial cancer. Gynecol Oncol. 2011;123(1):82–7.CrossRefPubMed
37.
go back to reference Nakamura K, Kodama J, Okumura Y, Hongo A, Kanazawa S, Hiramatsu Y. The SUVmax of 18F-FDG PET correlates with histological grade in endometrial cancer. Int J Gynecol Cancer. 2010;20(1):110–5.CrossRefPubMed Nakamura K, Kodama J, Okumura Y, Hongo A, Kanazawa S, Hiramatsu Y. The SUVmax of 18F-FDG PET correlates with histological grade in endometrial cancer. Int J Gynecol Cancer. 2010;20(1):110–5.CrossRefPubMed
38.
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(3):369–78.CrossRefPubMedPubMedCentral 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(3):369–78.CrossRefPubMedPubMedCentral
39.
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. 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.
40.
go back to reference Ayhan A, Celik H, Dursun P. Lymphatic mapping and sentinel node biopsy in gynecological cancers: a critical review of the literature. World J Surg Oncol. 2008;6:53.CrossRefPubMedPubMedCentral Ayhan A, Celik H, Dursun P. Lymphatic mapping and sentinel node biopsy in gynecological cancers: a critical review of the literature. World J Surg Oncol. 2008;6:53.CrossRefPubMedPubMedCentral
Metadata
Title
Radiomics of the primary tumour as a tool to improve 18F-FDG-PET sensitivity in detecting nodal metastases in endometrial cancer
Authors
Elisabetta De Bernardi
Alessandro Buda
Luca Guerra
Debora Vicini
Federica Elisei
Claudio Landoni
Robert Fruscio
Cristina Messa
Cinzia Crivellaro
Publication date
01-12-2018
Publisher
Springer Berlin Heidelberg
Published in
EJNMMI Research / Issue 1/2018
Electronic ISSN: 2191-219X
DOI
https://doi.org/10.1186/s13550-018-0441-1

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