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Published in: European Journal of Nuclear Medicine and Molecular Imaging 10/2017

01-09-2017 | Original Article

[18]Fluorodeoxyglucose Positron Emission Tomography for the Textural Features of Cervical Cancer Associated with Lymph Node Metastasis and Histological Type

Authors: Wei-Chih Shen, Shang-Wen Chen, Ji-An Liang, Te-Chun Hsieh, Kuo-Yang Yen, Chia-Hung Kao

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 10/2017

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Abstract

Background

In this study, we investigated the correlation between the lymph node (LN) status or histological types and textural features of cervical cancers on 18F-fluorodeoxyglucose positron emission tomography/computed tomography.

Methods

We retrospectively reviewed the imaging records of 170 patients with International Federation of Gynecology and Obstetrics stage IB–IVA cervical cancer. Four groups of textural features were studied in addition to the maximum standardized uptake value (SUVmax), metabolic tumor volume, and total lesion glycolysis (TLG). Moreover, we studied the associations between the indices and clinical parameters, including the LN status, clinical stage, and histology. Receiver operating characteristic curves were constructed to evaluate the optimal predictive performance among the various textural indices. Quantitative differences were determined using the Mann–Whitney U test. Multivariate logistic regression analysis was performed to determine the independent factors, among all the variables, for predicting LN metastasis.

Results

Among all the significant indices related to pelvic LN metastasis, homogeneity derived from the gray-level co-occurrence matrix (GLCM) was the sole independent predictor. By combining SUVmax, the risk of pelvic LN metastasis can be scored accordingly. The TLGmean was the independent feature of positive para-aortic LNs. Quantitative differences between squamous and nonsquamous histology can be determined using short-zone emphasis (SZE) from the gray-level size zone matrix (GLSZM).

Conclusion

This study revealed that in patients with cervical cancer, pelvic or para-aortic LN metastases can be predicted by using textural feature of homogeneity from the GLCM and TLGmean, respectively. SZE from the GLSZM is the sole feature associated with quantitative differences between squamous and nonsquamous histology.
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Literature
1.
2.
go back to reference Asselin MC, O’Connor JP, Boellaard R, Thacker NA, Jackson A. Quantifying heterogeneity in human tumors using MRI and PET. Eur J Cancer. 2012;48:447–55.CrossRefPubMed Asselin MC, O’Connor JP, Boellaard R, Thacker NA, Jackson A. Quantifying heterogeneity in human tumors using MRI and PET. Eur J Cancer. 2012;48:447–55.CrossRefPubMed
3.
go back to reference Chicklore S, Goh V, Siddique M, Roy A, Marsden PK, Cook GJ. Quantifying tumor heterogeneity in 18 F-FDG PET/CT imaging by texture analysis. Eur J Nucl Med Mol Imaging. 2013;40:133–40.CrossRefPubMed Chicklore S, Goh V, Siddique M, Roy A, Marsden PK, Cook GJ. Quantifying tumor heterogeneity in 18 F-FDG PET/CT imaging by texture analysis. Eur J Nucl Med Mol Imaging. 2013;40:133–40.CrossRefPubMed
4.
go back to reference Tixier F, Le Rest CC, Hatt M, 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.CrossRefPubMedPubMedCentral Tixier F, Le Rest CC, Hatt M, 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.CrossRefPubMedPubMedCentral
5.
go back to reference Vaidya M, Creach KM, Frye J, Dehdashti F, Bradley JD, El Naqa I. Combined PET/CT image characteristics for radiotherapy tumor response in lung cancer. Radiother Oncol. 2012;102:239–45.CrossRefPubMed Vaidya M, Creach KM, Frye J, Dehdashti F, Bradley JD, El Naqa I. Combined PET/CT image characteristics for radiotherapy tumor response in lung cancer. Radiother Oncol. 2012;102:239–45.CrossRefPubMed
6.
go back to reference Cook GJR, Yip C, Siddique M, 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.CrossRefPubMed Cook GJR, Yip C, Siddique M, 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.CrossRefPubMed
7.
go back to reference Hatt M, Majdoub M, Vallieres 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;56:38–44.CrossRefPubMed Hatt M, Majdoub M, Vallieres 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;56:38–44.CrossRefPubMed
8.
go back to reference Ohri N, Duan F, Snyder BS, et al. Pretreatment 18FDG-PET textural features in locally advanced non-small cell lung cancer: secondary analysis of ACRIN 6668/RTOG 0235. J Nucl Med. 2016. Ohri N, Duan F, Snyder BS, et al. Pretreatment 18FDG-PET textural features in locally advanced non-small cell lung cancer: secondary analysis of ACRIN 6668/RTOG 0235. J Nucl Med. 2016.
9.
go back to reference Kidd EA, Grigsby PW. Intratumoral metabolic heterogeneity of cervical cancer. Clin Cancer Res. 2008;14:5236–524.CrossRefPubMed Kidd EA, Grigsby PW. Intratumoral metabolic heterogeneity of cervical cancer. Clin Cancer Res. 2008;14:5236–524.CrossRefPubMed
10.
go back to reference Yang F, Thomas MA, Dehdashti F, Grigsby PW. Temporal analysis of intratumoral metabolic heterogeneity characterized by textural features in cervical cancer. Eur J Nucl Med Mol Imaging. 2013;40:716–27.CrossRefPubMedPubMedCentral Yang F, Thomas MA, Dehdashti F, Grigsby PW. Temporal analysis of intratumoral metabolic heterogeneity characterized by textural features in cervical cancer. Eur J Nucl Med Mol Imaging. 2013;40:716–27.CrossRefPubMedPubMedCentral
11.
go back to reference Ho KC, Fang YH, Chung HW, et al. A preliminary investigation into textural features of intratumoral metabolic heterogeneity in FDG PET for overall survival prognosis in patients with bulky cervical cancer treated with definitive concurrent chemoradiotherapy. Am J Nucl Med Mol Imaging. 2016;6:166–75.PubMedPubMedCentral Ho KC, Fang YH, Chung HW, et al. A preliminary investigation into textural features of intratumoral metabolic heterogeneity in FDG PET for overall survival prognosis in patients with bulky cervical cancer treated with definitive concurrent chemoradiotherapy. Am J Nucl Med Mol Imaging. 2016;6:166–75.PubMedPubMedCentral
12.
go back to reference Cheng NM, Fang YH, Lee LY, et al. Zone-size nonuniformity of 18F-FDG PET regional textural features predicts survival in patients with oropharyngeal cancer. Eur J Nucl Med Mol Imaging. 2015;42:419–28.CrossRefPubMed Cheng NM, Fang YH, Lee LY, et al. Zone-size nonuniformity of 18F-FDG PET regional textural features predicts survival in patients with oropharyngeal cancer. Eur J Nucl Med Mol Imaging. 2015;42:419–28.CrossRefPubMed
13.
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;55:414–22.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;55:414–22.CrossRefPubMed
14.
go back to reference Stehman FB, Bundy BN, DiSaia PJ, Keys HM, Larson JE, Fowler WC. Carcinoma of the cervix treated with radiation therapy. I. A multi-variate analysis of prognostic variables in the gynecologic oncology group. Cancer. 1991;67:2776–85.CrossRefPubMed Stehman FB, Bundy BN, DiSaia PJ, Keys HM, Larson JE, Fowler WC. Carcinoma of the cervix treated with radiation therapy. I. A multi-variate analysis of prognostic variables in the gynecologic oncology group. Cancer. 1991;67:2776–85.CrossRefPubMed
15.
go back to reference Kidd EA, Siegel BA, Dehdashti F, et al. Lymph node staging by positron emission tomography in cervical cancer: relationship to prognosis. J Clin Oncol. 2010;28:2108–13.CrossRefPubMed Kidd EA, Siegel BA, Dehdashti F, et al. Lymph node staging by positron emission tomography in cervical cancer: relationship to prognosis. J Clin Oncol. 2010;28:2108–13.CrossRefPubMed
16.
go back to reference Yen TC, Ng KK, Ma SY, et al. Value of dual-phase 2-fluoro-2-deoxy-d-glucose positron emission tomography in cervical cancer. J Clin Oncol. 2003;21:3651–8.CrossRefPubMed Yen TC, Ng KK, Ma SY, et al. Value of dual-phase 2-fluoro-2-deoxy-d-glucose positron emission tomography in cervical cancer. J Clin Oncol. 2003;21:3651–8.CrossRefPubMed
17.
go back to reference Reinhardt MJ, Ehritt-Braun C, Vogelgesang, et al. Metastatic lymph nodes in patients with cervical cancer: detection with MR imaging and FDG PET. Radiology. 2001;218:776–82.CrossRefPubMed Reinhardt MJ, Ehritt-Braun C, Vogelgesang, et al. Metastatic lymph nodes in patients with cervical cancer: detection with MR imaging and FDG PET. Radiology. 2001;218:776–82.CrossRefPubMed
18.
go back to reference Chen SW, Hsieh TC, Yen KY, Liang JA, Kao CH. Pretreatment 18F-FDG PET/CT in whole body total lesion glycolysis to predict survival in patients with pharyngeal cancer treated with definitive radiotherapy. Clin Nucl Med. 2014;39:e296–300.CrossRefPubMed Chen SW, Hsieh TC, Yen KY, Liang JA, Kao CH. Pretreatment 18F-FDG PET/CT in whole body total lesion glycolysis to predict survival in patients with pharyngeal cancer treated with definitive radiotherapy. Clin Nucl Med. 2014;39:e296–300.CrossRefPubMed
19.
go back to reference Meyer F. Topographic distance and watershed lines. Signal Processing. 1994;38:113–25.CrossRef Meyer F. Topographic distance and watershed lines. Signal Processing. 1994;38:113–25.CrossRef
20.
go back to reference Haralick RM, Shanmugam K, Dinstein I. Textural features for image classification. IEEE Trans Syst Man Cybern. 1973;3:610–21.CrossRef Haralick RM, Shanmugam K, Dinstein I. Textural features for image classification. IEEE Trans Syst Man Cybern. 1973;3:610–21.CrossRef
21.
go back to reference Sun C, Wee WG. Neighboring gray level dependence matrix for texture classification. Comput Vis Graph Image Process. 1983;23:341–52.CrossRef Sun C, Wee WG. Neighboring gray level dependence matrix for texture classification. Comput Vis Graph Image Process. 1983;23:341–52.CrossRef
22.
go back to reference Loh H, Leu J, Luo R. The analysis of natural textures using run length features. IEEE Trans Ind Electron. 1988;35:323–8.CrossRef Loh H, Leu J, Luo R. The analysis of natural textures using run length features. IEEE Trans Ind Electron. 1988;35:323–8.CrossRef
23.
go back to reference Thibault G, Fertil B, Navarro C, et al. Texture indexes and gray level size zone matrix: application to cell nuclei classification. Pattern Recognit Inf Process. 2009;140–145. Thibault G, Fertil B, Navarro C, et al. Texture indexes and gray level size zone matrix: application to cell nuclei classification. Pattern Recognit Inf Process. 2009;140–145.
24.
go back to reference Brooks FJ, Grigsby PW. FDG uptake heterogeneity in FIGO IIb cervical carcinoma does not predict pelvic lymph node involvement. Radiat Oncol. 2013;23(8):294.CrossRef Brooks FJ, Grigsby PW. FDG uptake heterogeneity in FIGO IIb cervical carcinoma does not predict pelvic lymph node involvement. Radiat Oncol. 2013;23(8):294.CrossRef
25.
go back to reference van Velden FH, Kramer GM, Frings V, Nissen IA, Mulder ER, de Langen AJ, Hoekstra OS, Smit EF, Boellaard R. Repeatability of Radiomic Features in Non-Small-Cell Lung Cancer [(18)F]FDG-PET/CT Studies: Impact of Reconstruction and Delineation. Mol Imaging Biol. 2016;18:788–95.CrossRefPubMedPubMedCentral van Velden FH, Kramer GM, Frings V, Nissen IA, Mulder ER, de Langen AJ, Hoekstra OS, Smit EF, Boellaard R. Repeatability of Radiomic Features in Non-Small-Cell Lung Cancer [(18)F]FDG-PET/CT Studies: Impact of Reconstruction and Delineation. Mol Imaging Biol. 2016;18:788–95.CrossRefPubMedPubMedCentral
26.
go back to reference Leijenaar RT, Nalbantov G, Carvalho S, van Elmpt WJ, Troost EG, Boellaard R, Aerts HJ, Gillies RJ, Lambin P. The effect of SUV discretization in quantitative FDG-PET Radiomics: the need for standardized methodology in tumor texture analysis. Sci Rep. 2015;5:11075.CrossRefPubMedPubMedCentral Leijenaar RT, Nalbantov G, Carvalho S, van Elmpt WJ, Troost EG, Boellaard R, Aerts HJ, Gillies RJ, Lambin P. The effect of SUV discretization in quantitative FDG-PET Radiomics: the need for standardized methodology in tumor texture analysis. Sci Rep. 2015;5:11075.CrossRefPubMedPubMedCentral
27.
go back to reference Desseroit MC, Tixier F, Weber WA, Siegel BA, Cheze Le Rest C, Visvikis D, Hatt M. Reliability of PET/CT shape and heterogeneity features in functional and morphological components of Non-Small Cell Lung Cancer tumors: a repeatability analysis in a prospective multi-center cohort. J Nucl Med. 2016; doi:10.2967/jnumed.116.180919.PubMed Desseroit MC, Tixier F, Weber WA, Siegel BA, Cheze Le Rest C, Visvikis D, Hatt M. Reliability of PET/CT shape and heterogeneity features in functional and morphological components of Non-Small Cell Lung Cancer tumors: a repeatability analysis in a prospective multi-center cohort. J Nucl Med. 2016; doi:10.​2967/​jnumed.​116.​180919.PubMed
28.
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;53:693–700.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;53:693–700.CrossRefPubMedPubMedCentral
29.
go back to reference Leijenaar RT, Carvalho S, Velazquez ER, van Elmpt WJ, Parmar C, Hoekstra OS, Hoekstra CJ, Boellaard R, Dekker AL, Gillies RJ, Aerts HJ, Lambin P. Stability of FDG-PET Radiomics features: an integrated analysis of test-retest and inter-observer variability. Acta Oncol. 2013;52:1391–7.CrossRefPubMed Leijenaar RT, Carvalho S, Velazquez ER, van Elmpt WJ, Parmar C, Hoekstra OS, Hoekstra CJ, Boellaard R, Dekker AL, Gillies RJ, Aerts HJ, Lambin P. Stability of FDG-PET Radiomics features: an integrated analysis of test-retest and inter-observer variability. Acta Oncol. 2013;52:1391–7.CrossRefPubMed
30.
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;44:151–65.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;44:151–65.CrossRefPubMed
31.
go back to reference Contag SA, Gostout BS, Clayton AC, Dixon MH, McGovern RM, Calhoun ES. Comparison of gene expression in squamous cell carcinoma and adenocarcinoma of the uterine cervix. Gynecol Oncol. 2004;95:610–7.CrossRefPubMed Contag SA, Gostout BS, Clayton AC, Dixon MH, McGovern RM, Calhoun ES. Comparison of gene expression in squamous cell carcinoma and adenocarcinoma of the uterine cervix. Gynecol Oncol. 2004;95:610–7.CrossRefPubMed
32.
go back to reference Fujimoto T, Nishikawa A, Iwasaki M, Akutagawa N, Teramoto M, Kudo R. Gene expression profiling in two morphologically different uterine cervical carcinoma cell lines derived from a single donor using a human cancer cDNA array. Gynecol Oncol. 2004;93:446–53.CrossRefPubMed Fujimoto T, Nishikawa A, Iwasaki M, Akutagawa N, Teramoto M, Kudo R. Gene expression profiling in two morphologically different uterine cervical carcinoma cell lines derived from a single donor using a human cancer cDNA array. Gynecol Oncol. 2004;93:446–53.CrossRefPubMed
33.
go back to reference Hatt M, Lee J, Schmidtlein CR, El Naqa I, Caldwell C, De Bernardi E, et al. Classification and evaluation strategies of auto-segmentation approaches for PET: Report of AAPM Task Group No. 211. Med Phys. 2017 Jan 24; doi:10.1002/mp.12124. Hatt M, Lee J, Schmidtlein CR, El Naqa I, Caldwell C, De Bernardi E, et al. Classification and evaluation strategies of auto-segmentation approaches for PET: Report of AAPM Task Group No. 211. Med Phys. 2017 Jan 24; doi:10.​1002/​mp.​12124.
Metadata
Title
[18]Fluorodeoxyglucose Positron Emission Tomography for the Textural Features of Cervical Cancer Associated with Lymph Node Metastasis and Histological Type
Authors
Wei-Chih Shen
Shang-Wen Chen
Ji-An Liang
Te-Chun Hsieh
Kuo-Yang Yen
Chia-Hung Kao
Publication date
01-09-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 10/2017
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-017-3697-1

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