Skip to main content
Top
Published in: European Journal of Nuclear Medicine and Molecular Imaging 2/2018

01-02-2018 | Original Article

Texture analysis of high-resolution dedicated breast 18 F-FDG PET images correlates with immunohistochemical factors and subtype of breast cancer

Authors: Alexis Moscoso, Álvaro Ruibal, Inés Domínguez-Prado, Anxo Fernández-Ferreiro, Míchel Herranz, Luis Albaina, Sonia Argibay, Jesús Silva-Rodríguez, Juan Pardo-Montero, Pablo Aguiar

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 2/2018

Login to get access

Abstract

Purpose

This study aims to determine whether PET textural features measured with a new dedicated breast PET scanner reflect biological characteristics of breast tumors.

Methods

One hundred and thirty-nine breast tumors from 127 consecutive patients were included in this analysis. All of them underwent a 18F-FDG PET scan before treatment. Well-known PET quantitative parameters such as SUV m a x , SUV m e a n , metabolically active tumor volume (MATV) and total lesion glycolysis (TLG) were extracted. Together with these parameters, local, regional, and global heterogeneity descriptors, which included five textural features (TF), were computed. Immunohistochemical classification of breast cancer considered five subtypes: luminal A like (LA), luminal B like/HER2 − (LB −), luminal B like/HER2+ (LB+), HER2-positive-non-luminal (HER2pnl), and triple negative (TN). Associations between PET features and tumor characteristics were assessed using non-parametric hypothesis tests.

Results

Along with well-established associations, new correlations were found. HER2-positive tumors had significantly higher uptake (p < 0.001, AUCs > 0.70) and presented different global and regional heterogeneity (p = 0.002, p = 0.016, respectively, AUCs < 0.70). Nine out of ten analyzed features were significantly associated with immunohistochemical subtype. Uptake was lower for LA tumors (p < 0.001) with AUCs ranging from 0.71 to 0.88 for each subgroup comparison. Heterogeneity metrics were significantly associated when comparing LA and LB − (p < 0.01), being regional heterogeneity metrics more discriminative than any other parameter (AUC = 0.80 compared to AUC = 0.71 for SUV). LB+ and HER2pnl tumors also showed more regional heterogeneity than LA tumors (AUCs = 0.79 and 0.84, respectively). After comparison with whole-body PET studies, we observed an overall improvement in the classification ability of both non-heterogeneity metrics and textural features.

Conclusions

PET parameters extracted from high-resolution dedicated breast PET images showed new and stronger correlations with immunohistochemical factors and immunohistochemical subtype of breast cancer compared to whole-body PET.
Appendix
Available only for authorised users
Literature
1.
3.
go back to reference Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thrlimann B, et al. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol 2013;24(9):2206–23.CrossRefPubMedPubMedCentral Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thrlimann B, et al. Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol 2013;24(9):2206–23.CrossRefPubMedPubMedCentral
4.
go back to reference Haralick RM, Shanmugam K, Dinstein I. Textural features for image classification. IEEE Trans Syst Man Cybern 1973;SMC-3:610–21.CrossRef Haralick RM, Shanmugam K, Dinstein I. Textural features for image classification. IEEE Trans Syst Man Cybern 1973;SMC-3:610–21.CrossRef
5.
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
6.
go back to reference Alic L, Niessen WJ, Veenland JF. Quantification of heterogeneity as a biomarker in tumor imaging: a systematic review. PLoS ONE 2014;9:1–1.CrossRef Alic L, Niessen WJ, Veenland JF. Quantification of heterogeneity as a biomarker in tumor imaging: a systematic review. PLoS ONE 2014;9:1–1.CrossRef
7.
go back to reference Chicklore S, Goh V, Siddique M, Roy A, Marsden PK, Cook GJR. Quantifying tumour heterogeneity in 18F-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 GJR. Quantifying tumour heterogeneity in 18F-FDG PET/CT imaging by texture analysis. Eur J Nucl Med Mol Imaging 2013;40:133–40.CrossRefPubMed
8.
go back to reference Tixier F, Le Rest CC, Hatt M, Albarghach N, Pradier O, 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;52:369378.CrossRef Tixier F, Le Rest CC, Hatt M, Albarghach N, Pradier O, 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;52:369378.CrossRef
9.
go back to reference Lovinfosse P, Janvary ZL, Coucke P, Jodogne S, Bernard C, Hatt M, et al. FDG PET/CT texture analysis for predicting the outcome of lung cancer treated by stereotactic body radiation therapy. Eur J Nucl Med Mol Imaging 2016;43:1453–60.CrossRefPubMed Lovinfosse P, Janvary ZL, Coucke P, Jodogne S, Bernard C, Hatt M, et al. FDG PET/CT texture analysis for predicting the outcome of lung cancer treated by stereotactic body radiation therapy. Eur J Nucl Med Mol Imaging 2016;43:1453–60.CrossRefPubMed
10.
go back to reference Cook GJ, Yip C, Siddique M, Goh V, Chicklore S, 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;54:1926. Cook GJ, Yip C, Siddique M, Goh V, Chicklore S, 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;54:1926.
11.
go back to reference Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. Engl J Med 2012;366:883892.CrossRef Gerlinger M, Rowan AJ, Horswell S, Larkin J, Endesfelder D, Gronroos E, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. Engl J Med 2012;366:883892.CrossRef
12.
go back to reference Zardavas D, Irrthum A, Swanton C, Piccart M. Clinical management of breast cancer heterogeneity. Nat Rev Clin Oncol. 2015;12(7):381–94.CrossRefPubMed Zardavas D, Irrthum A, Swanton C, Piccart M. Clinical management of breast cancer heterogeneity. Nat Rev Clin Oncol. 2015;12(7):381–94.CrossRefPubMed
13.
go back to reference Bastien RR, Rodrguez-Lescure Á, Ebbert MT, Prat A, Munárriz B, Rowe L, et al. PAM50 breast cancer subtyping by RT-qPCR and concordance with standard clinical molecular markers. BMC Med Genomics. 2012;5:44.CrossRefPubMedPubMedCentral Bastien RR, Rodrguez-Lescure Á, Ebbert MT, Prat A, Munárriz B, Rowe L, et al. PAM50 breast cancer subtyping by RT-qPCR and concordance with standard clinical molecular markers. BMC Med Genomics. 2012;5:44.CrossRefPubMedPubMedCentral
14.
go back to reference Son SH, Kim D-H, Hong CM, Kim C-Y, Jeong SY, Lee S-W, et al. Prognostic implication of intratumoral metabolic heterogeneity in invasive ductal carcinoma of the breast. BMC Cancer 2014;14:585.CrossRefPubMedPubMedCentral Son SH, Kim D-H, Hong CM, Kim C-Y, Jeong SY, Lee S-W, et al. Prognostic implication of intratumoral metabolic heterogeneity in invasive ductal carcinoma of the breast. BMC Cancer 2014;14:585.CrossRefPubMedPubMedCentral
15.
go back to reference Soussan M, Orlhac F, Boubaya M, Zelek L, Ziol M, Vronique E, et al. Relationship between tumor heterogeneity measured on FDG-PET/CT and pathological prognostic factors in invasive breast cancer. PLoS One 2014;9(4):e94017.CrossRefPubMedPubMedCentral Soussan M, Orlhac F, Boubaya M, Zelek L, Ziol M, Vronique E, et al. Relationship between tumor heterogeneity measured on FDG-PET/CT and pathological prognostic factors in invasive breast cancer. PLoS One 2014;9(4):e94017.CrossRefPubMedPubMedCentral
16.
go back to reference Groheux D, Majdoub M, Tixier F, Le Rest CC, Martineau A, Merlet P, et al. Do clinical, histological or immunohistochemical primary tumour characteristics translate into different (18)F-FDG PET/CT volumetric and heterogeneity features in stage II/III breast cancer? Eur J Nucl Med Mol Imaging 2015;42 (11):1682–91.CrossRefPubMedPubMedCentral Groheux D, Majdoub M, Tixier F, Le Rest CC, Martineau A, Merlet P, et al. Do clinical, histological or immunohistochemical primary tumour characteristics translate into different (18)F-FDG PET/CT volumetric and heterogeneity features in stage II/III breast cancer? Eur J Nucl Med Mol Imaging 2015;42 (11):1682–91.CrossRefPubMedPubMedCentral
17.
18.
go back to reference Moliner L, González AJ, Soriano A, Sánchez F, Correcher C, Orero A, et al. Design and evaluation of the MAMMI dedicated breast PET. Med Phys 2012;39:5393–5404.CrossRefPubMed Moliner L, González AJ, Soriano A, Sánchez F, Correcher C, Orero A, et al. Design and evaluation of the MAMMI dedicated breast PET. Med Phys 2012;39:5393–5404.CrossRefPubMed
19.
go back to reference García Hernández T, Vicedo González A, Ferrer Rebolleda J, Sánchez Jurado R, Roselló Ferrando J, Brualla González L, et al. Performance evaluation of a high-resolution dedicated breast PET scanner. Med Phys 2016;43:2261–72.CrossRefPubMed García Hernández T, Vicedo González A, Ferrer Rebolleda J, Sánchez Jurado R, Roselló Ferrando J, Brualla González L, et al. Performance evaluation of a high-resolution dedicated breast PET scanner. Med Phys 2016;43:2261–72.CrossRefPubMed
20.
go back to reference Koolen BB, Vidal-Sicart S, Benlloch Baviera JM, Valdés Olmos R A. Evaluating heterogeneity of primary tumor (18)F-FDG uptake in breast cancer with a dedicated breast PET (MAMMI): a feasibility study based on correlation with PET/CT. Nucl Med Commun 2014;35(5):446–52.CrossRefPubMed Koolen BB, Vidal-Sicart S, Benlloch Baviera JM, Valdés Olmos R A. Evaluating heterogeneity of primary tumor (18)F-FDG uptake in breast cancer with a dedicated breast PET (MAMMI): a feasibility study based on correlation with PET/CT. Nucl Med Commun 2014;35(5):446–52.CrossRefPubMed
21.
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. Minsk, Belarus; 2009. p. 140–145. 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. Minsk, Belarus; 2009. p. 140–145.
22.
go back to reference Van Velden FHP, Cheebsumon P, Yaqub M, 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.CrossRefPubMedPubMedCentral Van Velden FHP, Cheebsumon P, Yaqub M, 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.CrossRefPubMedPubMedCentral
23.
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. J Nucl Med 2012; 53:693–700.CrossRefPubMedPubMedCentral 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. J Nucl Med 2012; 53:693–700.CrossRefPubMedPubMedCentral
24.
go back to reference Hatt M, Tixier F, Cheze Le Rest C, Pradier O, Visvikis D. Robustness of intratumour 18F-FDG PET uptake heterogeneity quantification for therapy response prediction in oesophageal carcinoma. Eur J Nucl Med Mol Imaging 2013;40:1662–71.CrossRefPubMed Hatt M, Tixier F, Cheze Le Rest C, Pradier O, Visvikis D. Robustness of intratumour 18F-FDG PET uptake heterogeneity quantification for therapy response prediction in oesophageal carcinoma. Eur J Nucl Med Mol Imaging 2013;40:1662–71.CrossRefPubMed
25.
go back to reference Hatt M, Majdoub M, Vallières 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 multicancer site patient cohort. J Nucl Med 2015;56:38–44.CrossRefPubMed Hatt M, Majdoub M, Vallières 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 multicancer site patient cohort. J Nucl Med 2015;56:38–44.CrossRefPubMed
26.
go back to reference Yan J, Chu-Shern JL, Loi HY, Khor LK, Sinha AK, Quek ST. Impact of image reconstruction settings on texture features in 18F-FDG PET. J Nucl Med. 2015;56:1667–73. Yan J, Chu-Shern JL, Loi HY, Khor LK, Sinha AK, Quek ST. Impact of image reconstruction settings on texture features in 18F-FDG PET. J Nucl Med. 2015;56:1667–73.
27.
go back to reference Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B Methodol 1995;57(1):289–300. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B Methodol 1995;57(1):289–300.
28.
go back to reference Aerts HJ, Velazquez ER, Leijenaar RT, Parmar C, Grossmann P, Carvalho S, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 2014;5:4006.PubMedPubMedCentral Aerts HJ, Velazquez ER, Leijenaar RT, Parmar C, Grossmann P, Carvalho S, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 2014;5:4006.PubMedPubMedCentral
29.
go back to reference Brooks FJ, Grigsby PW. The effect of small tumor volumes on studies of intratumoral heterogeneity of tracer uptake. J Nucl Med 2014 Jan;55(1):37–42.CrossRefPubMed Brooks FJ, Grigsby PW. The effect of small tumor volumes on studies of intratumoral heterogeneity of tracer uptake. J Nucl Med 2014 Jan;55(1):37–42.CrossRefPubMed
30.
go back to reference Jadvar H, Alavi A. Gambhir SS, 18F-FDG uptake in lung, breast, and colon cancers: molecular biology correlates and disease characterization. J Nucl Med 2009;50(11):1820–7.CrossRefPubMedPubMedCentral Jadvar H, Alavi A. Gambhir SS, 18F-FDG uptake in lung, breast, and colon cancers: molecular biology correlates and disease characterization. J Nucl Med 2009;50(11):1820–7.CrossRefPubMedPubMedCentral
31.
go back to reference Osborne JR, Port E, Gonen M, Doane A, Yeung H. Gerald W, others. 18F-FDG PET of locally invasive breast cancer and association of estrogen receptor status with standardized uptake value: microarray and immunohistochemical analysis. J Nucl Med 2010;51(4):543–50.CrossRefPubMedPubMedCentral Osborne JR, Port E, Gonen M, Doane A, Yeung H. Gerald W, others. 18F-FDG PET of locally invasive breast cancer and association of estrogen receptor status with standardized uptake value: microarray and immunohistochemical analysis. J Nucl Med 2010;51(4):543–50.CrossRefPubMedPubMedCentral
32.
go back to reference Koolen BB, Vrancken Peeters MJ, Wesseling J, Lips EH, Vogel WV, Aukema TS. Association of primary tumour FDG uptake with clinical, histopathological and molecular characteristics in breast cancer patients scheduled for neoadjuvant chemotherapy. Eur J Nucl Med Mol Imaging. 2012;39(12):1830–8.CrossRefPubMed Koolen BB, Vrancken Peeters MJ, Wesseling J, Lips EH, Vogel WV, Aukema TS. Association of primary tumour FDG uptake with clinical, histopathological and molecular characteristics in breast cancer patients scheduled for neoadjuvant chemotherapy. Eur J Nucl Med Mol Imaging. 2012;39(12):1830–8.CrossRefPubMed
33.
go back to reference Lee SS, Bae SK, Park YS, Park JS, Kim TH, Yoon HK. Correlation of molecular subtypes of invasive ductal carcinoma of breast with glucose metabolism in FDG PET/CT: Based on the Recommendations of the St. Gallen Consensus Meeting 2013. Nucl Med Mol Imaging 2017;51(1):79–85.CrossRefPubMed Lee SS, Bae SK, Park YS, Park JS, Kim TH, Yoon HK. Correlation of molecular subtypes of invasive ductal carcinoma of breast with glucose metabolism in FDG PET/CT: Based on the Recommendations of the St. Gallen Consensus Meeting 2013. Nucl Med Mol Imaging 2017;51(1):79–85.CrossRefPubMed
34.
go back to reference Cheang MC, Chia SK, Voduc D, Gao D, Leung S, Snider J, et al. Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst 2009;101(10):736– 50.CrossRefPubMedPubMedCentral Cheang MC, Chia SK, Voduc D, Gao D, Leung S, Snider J, et al. Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst 2009;101(10):736– 50.CrossRefPubMedPubMedCentral
35.
go back to reference Dowsett M, Nielsen TO, A’Hern R, Bartlett J, Coombes RC, Cuzick J, et al. Assessment of Ki67 in breast cancer: recommendations from the International Ki67 in Breast Cancer working group. J Natl Cancer Inst 2011;103(22):1656–64.CrossRefPubMedPubMedCentral Dowsett M, Nielsen TO, A’Hern R, Bartlett J, Coombes RC, Cuzick J, et al. Assessment of Ki67 in breast cancer: recommendations from the International Ki67 in Breast Cancer working group. J Natl Cancer Inst 2011;103(22):1656–64.CrossRefPubMedPubMedCentral
Metadata
Title
Texture analysis of high-resolution dedicated breast 18 F-FDG PET images correlates with immunohistochemical factors and subtype of breast cancer
Authors
Alexis Moscoso
Álvaro Ruibal
Inés Domínguez-Prado
Anxo Fernández-Ferreiro
Míchel Herranz
Luis Albaina
Sonia Argibay
Jesús Silva-Rodríguez
Juan Pardo-Montero
Pablo Aguiar
Publication date
01-02-2018
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 2/2018
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-017-3830-1

Other articles of this Issue 2/2018

European Journal of Nuclear Medicine and Molecular Imaging 2/2018 Go to the issue