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Published in: European Journal of Nuclear Medicine and Molecular Imaging 5/2020

01-05-2020 | Breast Cancer | Original Article

Biological correlates of tumor perfusion and its heterogeneity in newly diagnosed breast cancer using dynamic first-pass 18F-FDG PET/CT

Authors: Neree Payan, Benoit Presles, François Brunotte, Charles Coutant, Isabelle Desmoulins, Jean-Marc Vrigneaud, Alexandre Cochet

Published in: European Journal of Nuclear Medicine and Molecular Imaging | Issue 5/2020

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Abstract

Purpose

The aim of this prospective study is to analyze the global tumor blood flow (BF) and its heterogeneity in newly diagnosed breast cancer (BC) according to tumor biological characteristics and molecular subtypes. These perfusion parameters were compared to those classically derived from metabolic studies to investigate links between perfusion and metabolism.

Methods

Two hundred seventeen newly diagnosed BC patients underwent a 18F-FDG PET/CT exam before any treatment. A 2-min dynamic acquisition, centered on the chest, was performed immediately after intravenous injection of 3 MBq/kg of 18F-FDG, followed by a two-step static acquisition 90 min later. Tumor BF was calculated (in ml/min/g) using a single compartment kinetic model. In addition to standard PET parameters, texture features (TF) describing the heterogeneity of tumor perfusion and metabolism were extracted. Patients were divided into three groups: Luminal (HR+/HER2-), HER2 (HER2+), and TN (HR-/HER2-). Global and TF parameters of BF and metabolism were compared in different groups of patients according to tumor biological characteristics.

Results

Tumors with lymph node involvement showed a higher perfusion, whereas no significant differences in SUV_max or SUV_mean were reported. TN tumors had a higher metabolic activity than HER2 and luminal tumors but no significant differences in global BF values were noted. HER2 tumors exhibited a larger tumor heterogeneity of both perfusion and metabolism compared to luminal and TN tumors. Heterogeneity of perfusion appeared well correlated to that of metabolism.

Conclusions

The study of breast cancer perfusion shows a higher BF in large tumors and in tumors with lymph node involvement, not paralleled by similar modifications in tumor global metabolism. In addition, the observed correlation between the perfusion heterogeneity and the metabolism heterogeneity suggests that tumor perfusion and consequently the process of tumor angiogenesis might be involved in the metabolism heterogeneity previously shown in BC.
Literature
1.
go back to reference Ahlgren J, Risberg B, Villman K, Bergh J. Angiogenesis in invasive breast carcinoma—a prospective study of tumour heterogeneity. Eur J Cancer 2002;38(1):64–69.PubMedCrossRef Ahlgren J, Risberg B, Villman K, Bergh J. Angiogenesis in invasive breast carcinoma—a prospective study of tumour heterogeneity. Eur J Cancer 2002;38(1):64–69.PubMedCrossRef
2.
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(10):e110,300.CrossRef Alic L, Niessen WJ, Veenland JF. Quantification of heterogeneity as a biomarker in tumor imaging: a systematic review. PLoS One 2014;9(10):e110,300.CrossRef
3.
go back to reference Amadasun M, King R. Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern 1989;19(5):1264–1274.CrossRef Amadasun M, King R. Textural features corresponding to textural properties. IEEE Trans Syst Man Cybern 1989;19(5):1264–1274.CrossRef
4.
go back to reference Amin MB, Edge SB, Greene FL, Byrd DR, Brookland RK, Washington MK, Gershenwald JE, Compton CC, Hess KR, Sullivan DC, Milburn Jessup J, Brierley JD, Gaspar LE, Schilsky RL, Balch CM, Winchester DP, Asare EA, Madera M, Gress DM, Meyer LR. 2018. AJCC Cancer Staging Manual. Springer. Amin MB, Edge SB, Greene FL, Byrd DR, Brookland RK, Washington MK, Gershenwald JE, Compton CC, Hess KR, Sullivan DC, Milburn Jessup J, Brierley JD, Gaspar LE, Schilsky RL, Balch CM, Winchester DP, Asare EA, Madera M, Gress DM, Meyer LR. 2018. AJCC Cancer Staging Manual. Springer.
5.
go back to reference Arnes JB, Stefansson IM, Straume O, Baak JP, Lønning PE, Foulkes WD, Akslen LA. Vascular proliferation is a prognostic factor in breast cancer. Breast Cancer Res Treat 2012;133(2):501–510.PubMedCrossRef Arnes JB, Stefansson IM, Straume O, Baak JP, Lønning PE, Foulkes WD, Akslen LA. Vascular proliferation is a prognostic factor in breast cancer. Breast Cancer Res Treat 2012;133(2):501–510.PubMedCrossRef
6.
go back to reference Bhargava R, Striebel J, Beriwal S, Flickinger JC, Onisko A, Ahrendt G, Dabbs DJ. Prevalence, morphologic features and proliferation indices of breast carcinoma molecular classes using immunohistochemical surrogate markers. Int J Clin Exp Pathol 2009;2(5):444.PubMedPubMedCentral Bhargava R, Striebel J, Beriwal S, Flickinger JC, Onisko A, Ahrendt G, Dabbs DJ. Prevalence, morphologic features and proliferation indices of breast carcinoma molecular classes using immunohistochemical surrogate markers. Int J Clin Exp Pathol 2009;2(5):444.PubMedPubMedCentral
7.
go back to reference Chao TC, Luo YF, Chen SC, Chen MF. Color Doppler ultrasound in breast carcinomas: relationship with hormone receptors, DNA ploidy, s-phase fraction, and histopathology. Ultrasound Med Biol 2001;27(3):351–355.PubMedCrossRef Chao TC, Luo YF, Chen SC, Chen MF. Color Doppler ultrasound in breast carcinomas: relationship with hormone receptors, DNA ploidy, s-phase fraction, and histopathology. Ultrasound Med Biol 2001;27(3):351–355.PubMedCrossRef
8.
go back to reference Choi WWL, Lewis MM, Lawson D, Yin-Goen Q, Birdsong GG, Cotsonis GA, Cohen C, Young AN. Angiogenic and lymphangiogenic microvessel density in breast carcinoma: correlation with clinicopathologic parameters and VEGF-family gene expression. Mod Pathol 2005;18(1):143–152.PubMedCrossRef Choi WWL, Lewis MM, Lawson D, Yin-Goen Q, Birdsong GG, Cotsonis GA, Cohen C, Young AN. Angiogenic and lymphangiogenic microvessel density in breast carcinoma: correlation with clinicopathologic parameters and VEGF-family gene expression. Mod Pathol 2005;18(1):143–152.PubMedCrossRef
9.
go back to reference Cochet A, Dygai-Cochet I, Riedinger JM, Humbert O, Berriolo-Riedinger A, Toubeau M, Guiu S, Coutant C, Coudert B, Fumoleau P, Brunotte F. 18F-FDG PET/CT provides powerful prognostic stratification in the primary staging of large breast cancer when compared with conventional explorations. Eur J Nucl Med Mol Imaging 2013;41(3):428–437.PubMedCrossRef Cochet A, Dygai-Cochet I, Riedinger JM, Humbert O, Berriolo-Riedinger A, Toubeau M, Guiu S, Coutant C, Coudert B, Fumoleau P, Brunotte F. 18F-FDG PET/CT provides powerful prognostic stratification in the primary staging of large breast cancer when compared with conventional explorations. Eur J Nucl Med Mol Imaging 2013;41(3):428–437.PubMedCrossRef
10.
go back to reference Cochet A, Pigeonnat S, Khoury B, Vrigneaud JM, Touzery C, Berriolo-Riedinger A, Dygai-Cochet I, Toubeau M, Humbert O, Coudert B, Fumoleau P, Arnould L, Brunotte F. Evaluation of breast tumor blood flow with dynamic first-pass 18F-FDG PET/CT: comparison with angiogenesis markers and prognostic factors. J Nucl Med 2012;53(4):512–520.PubMedCrossRef Cochet A, Pigeonnat S, Khoury B, Vrigneaud JM, Touzery C, Berriolo-Riedinger A, Dygai-Cochet I, Toubeau M, Humbert O, Coudert B, Fumoleau P, Arnould L, Brunotte F. Evaluation of breast tumor blood flow with dynamic first-pass 18F-FDG PET/CT: comparison with angiogenesis markers and prognostic factors. J Nucl Med 2012;53(4):512–520.PubMedCrossRef
11.
go back to reference Coradini D, Pellizzaro C, Veneroni S, Ventura L, Daidone MG. Infiltrating ductal and lobular breast carcinomas are characterised by different interrelationships among markers related to angiogenesis and hormone dependence. Br J Cancer 2002;87(10):1105–1111.PubMedPubMedCentralCrossRef Coradini D, Pellizzaro C, Veneroni S, Ventura L, Daidone MG. Infiltrating ductal and lobular breast carcinomas are characterised by different interrelationships among markers related to angiogenesis and hormone dependence. Br J Cancer 2002;87(10):1105–1111.PubMedPubMedCentralCrossRef
12.
go back to reference Coudert B, Pierga JY, Mouret-Reynier MA, Kerrou K, Ferrero JM, Petit T, Kerbrat P, Dupré PF, Bachelot T, Gabelle P, Giard S, Coeffic D, Bougnoux P, Prevost JB, Paintaud G, Thibault G, Hernandez J, Coudert M, Arnould L, Berriolo-Riedinger A. Use of [18F]-FDG PET to predict response to neoadjuvant trastuzumab and docetaxel in patients with HER2-positive breast cancer, and addition of bevacizumab to neoadjuvant trastuzumab and docetaxel in [18F]-FDG PET-predicted non-responders (AVATAXHER): an open-label, randomised phase 2 trial. Lancet Oncol 2014;15(13):1493–1502.PubMedCrossRef Coudert B, Pierga JY, Mouret-Reynier MA, Kerrou K, Ferrero JM, Petit T, Kerbrat P, Dupré PF, Bachelot T, Gabelle P, Giard S, Coeffic D, Bougnoux P, Prevost JB, Paintaud G, Thibault G, Hernandez J, Coudert M, Arnould L, Berriolo-Riedinger A. Use of [18F]-FDG PET to predict response to neoadjuvant trastuzumab and docetaxel in patients with HER2-positive breast cancer, and addition of bevacizumab to neoadjuvant trastuzumab and docetaxel in [18F]-FDG PET-predicted non-responders (AVATAXHER): an open-label, randomised phase 2 trial. Lancet Oncol 2014;15(13):1493–1502.PubMedCrossRef
13.
go back to reference Dunnwald LK, Gralow JR, Ellis GK, Livingston RB, Linden HM, Specht JM, Doot RK, Lawton TJ, Barlow WE, Kurland BF, Schubert EK, Mankoff DA. Tumor metabolism and blood flow changes by positron emission tomography: relation to survival in patients treated with neoadjuvant chemotherapy for locally advanced breast cancer. J Clin Oncol 2008;26(27):4449–4457.PubMedPubMedCentralCrossRef Dunnwald LK, Gralow JR, Ellis GK, Livingston RB, Linden HM, Specht JM, Doot RK, Lawton TJ, Barlow WE, Kurland BF, Schubert EK, Mankoff DA. Tumor metabolism and blood flow changes by positron emission tomography: relation to survival in patients treated with neoadjuvant chemotherapy for locally advanced breast cancer. J Clin Oncol 2008;26(27):4449–4457.PubMedPubMedCentralCrossRef
14.
15.
go back to reference Groheux D, Giacchetti S, Moretti JL, Porcher R, Espié M, Lehmann-Che J, de Roquancourt A, Hamy AS, Cuvier C, Vercellino L, Hindié E. Correlation of high 18F-FDG uptake to clinical, pathological and biological prognostic factors in breast cancer. Eur J Nucl Med Mol Imaging 2011;38(3):426– 435.PubMedCrossRef Groheux D, Giacchetti S, Moretti JL, Porcher R, Espié M, Lehmann-Che J, de Roquancourt A, Hamy AS, Cuvier C, Vercellino L, Hindié E. Correlation of high 18F-FDG uptake to clinical, pathological and biological prognostic factors in breast cancer. Eur J Nucl Med Mol Imaging 2011;38(3):426– 435.PubMedCrossRef
16.
go back to reference Groheux D, Majdoub M, Tixier F, Le Rest CC, Martineau A, Merlet P, Espié M, de Roquancourt A, Hindié E, Hatt M, Visvikis D. 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):1682–1691.PubMedPubMedCentralCrossRef Groheux D, Majdoub M, Tixier F, Le Rest CC, Martineau A, Merlet P, Espié M, de Roquancourt A, Hindié E, Hatt M, Visvikis D. 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):1682–1691.PubMedPubMedCentralCrossRef
17.
go back to reference Hatt M, Majdoub M, Vallières M, Tixier F, Le Rest CC, Groheux D, Hindié E, Martineau A, Pradier O, Hustinx R, Perdrisot R, Guillevin R, El Naqa I, Visvikis D. 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.PubMedCrossRef Hatt M, Majdoub M, Vallières M, Tixier F, Le Rest CC, Groheux D, Hindié E, Martineau A, Pradier O, Hustinx R, Perdrisot R, Guillevin R, El Naqa I, Visvikis D. 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.PubMedCrossRef
18.
go back to reference Hatt M, Tixier F, Le Rest CC, 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(11):1662–1671.PubMedCrossRef Hatt M, Tixier F, Le Rest CC, 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(11):1662–1671.PubMedCrossRef
19.
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): 151–165.PubMedCrossRef 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): 151–165.PubMedCrossRef
20.
go back to reference Humbert O, Lasserre M, Bertaut A, Fumoleau P, Coutant C, Brunotte F, Cochet A. Breast cancer blood flow and metabolism on dual-acquisition 18F-FDG PET: correlation with tumor phenotype and neoadjuvant chemotherapy response. J Nucl Med 2018;59(7):1035–1041.PubMedCrossRef Humbert O, Lasserre M, Bertaut A, Fumoleau P, Coutant C, Brunotte F, Cochet A. Breast cancer blood flow and metabolism on dual-acquisition 18F-FDG PET: correlation with tumor phenotype and neoadjuvant chemotherapy response. J Nucl Med 2018;59(7):1035–1041.PubMedCrossRef
21.
go back to reference Humbert O, Lasserre M, Bertaut A, Fumoleau P, Coutant C, Brunotte F, Cochet A. 2018. Breast Cancer Blood Flow and Metabolism on Dual-Acquisition 18F-FDG PET: Correlation with Tumor Phenotype and Neoadjuvant Chemotherapy Response, Vol. 59. Humbert O, Lasserre M, Bertaut A, Fumoleau P, Coutant C, Brunotte F, Cochet A. 2018. Breast Cancer Blood Flow and Metabolism on Dual-Acquisition 18F-FDG PET: Correlation with Tumor Phenotype and Neoadjuvant Chemotherapy Response, Vol. 59.
22.
go back to reference Humbert O, Riedinger JM, Vrigneaud JM, Kanoun S, Dygai-Cochet I, Berriolo-Riedinger A, Toubeau M, Depardon E, Lassere M, Tisserand S, Fumoleau P, Brunotte F, Cochet A. 18F-FDG PET-derived tumor blood flow changes after 1 cycle of neoadjuvant chemotherapy predicts outcome in triple-negative breast cancer. J Nucl Med 2016;57(11):1707–1712.PubMedCrossRef Humbert O, Riedinger JM, Vrigneaud JM, Kanoun S, Dygai-Cochet I, Berriolo-Riedinger A, Toubeau M, Depardon E, Lassere M, Tisserand S, Fumoleau P, Brunotte F, Cochet A. 18F-FDG PET-derived tumor blood flow changes after 1 cycle of neoadjuvant chemotherapy predicts outcome in triple-negative breast cancer. J Nucl Med 2016;57(11):1707–1712.PubMedCrossRef
23.
go back to reference Konecny GE, Meng YG, Untch M, Wang HJ, Bauerfeind I, Epstein M, Stieber P, Vernes JM, Gutierrez J, Hong K, Beryt M, Hepp H, Slamon DJ, Pegram MD. Association between HER-2/neu and vascular endothelial growth factor expression predicts clinical outcome in primary breast cancer patients. Clin Cancer Res 2004;10(5):1706–1716.PubMedCrossRef Konecny GE, Meng YG, Untch M, Wang HJ, Bauerfeind I, Epstein M, Stieber P, Vernes JM, Gutierrez J, Hong K, Beryt M, Hepp H, Slamon DJ, Pegram MD. Association between HER-2/neu and vascular endothelial growth factor expression predicts clinical outcome in primary breast cancer patients. Clin Cancer Res 2004;10(5):1706–1716.PubMedCrossRef
24.
go back to reference Kraby MR, Opdahl S, Russnes HG, Bofin AM. 2019. Microvessel density in breast cancer: the impact of field area on prognostic informativeness. J Clin Pathol. Kraby MR, Opdahl S, Russnes HG, Bofin AM. 2019. Microvessel density in breast cancer: the impact of field area on prognostic informativeness. J Clin Pathol.
25.
go back to reference Kumar R, Yarmand-Bagheri R. The role of HER2 in angiogenesis. Semin Oncol 2001;28(5 Suppl 16):27–32.PubMedCrossRef Kumar R, Yarmand-Bagheri R. The role of HER2 in angiogenesis. Semin Oncol 2001;28(5 Suppl 16):27–32.PubMedCrossRef
26.
go back to reference Laking G, Price P. Radionuclide imaging of perfusion and hypoxia. Eur J Nucl Med Mol Imaging 2010;37 (S1):20–29.CrossRef Laking G, Price P. Radionuclide imaging of perfusion and hypoxia. Eur J Nucl Med Mol Imaging 2010;37 (S1):20–29.CrossRef
27.
go back to reference Lee AH, Dublin EA, Bobrow LG, Poulsom R. Invasive lobular and invasive ductal carcinoma of the breast show distinct patterns of vascular endothelial growth factor expression and angiogenesis. J Pathol 1998;185(4): 394–401.PubMedCrossRef Lee AH, Dublin EA, Bobrow LG, Poulsom R. Invasive lobular and invasive ductal carcinoma of the breast show distinct patterns of vascular endothelial growth factor expression and angiogenesis. J Pathol 1998;185(4): 394–401.PubMedCrossRef
28.
go back to reference Leijenaar RTH, Nalbantov G, Carvalho S, van Elmpt WJC, Troost EGC, Boellaard R, Aerts HJWL, 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(11):075. Leijenaar RTH, Nalbantov G, Carvalho S, van Elmpt WJC, Troost EGC, Boellaard R, Aerts HJWL, 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(11):075.
29.
go back to reference Lemarignier C, Martineau A, Teixeira L, Vercellino L, Espié M, Merlet P, Groheux D. Correlation between tumour characteristics, SUV measurements, metabolic tumour volume, TLG and textural features assessed with F-FDG PET in a large cohort of oestrogen receptor-positive breast cancer patients. Eur J Nucl Med Mol Imaging 2017;44(7):1145–1154.PubMedCrossRef Lemarignier C, Martineau A, Teixeira L, Vercellino L, Espié M, Merlet P, Groheux D. Correlation between tumour characteristics, SUV measurements, metabolic tumour volume, TLG and textural features assessed with F-FDG PET in a large cohort of oestrogen receptor-positive breast cancer patients. Eur J Nucl Med Mol Imaging 2017;44(7):1145–1154.PubMedCrossRef
30.
go back to reference Mankoff DA, Dunnwald LK, Gralow JR, Ellis GK, Charlop A, Lawton TJ, Schubert EK, Tseng J, Livingston RB. Blood flow and metabolism in locally advanced breast cancer: relationship to response to therapy. J Nucl Med 2002;43(4):500–509.PubMed Mankoff DA, Dunnwald LK, Gralow JR, Ellis GK, Charlop A, Lawton TJ, Schubert EK, Tseng J, Livingston RB. Blood flow and metabolism in locally advanced breast cancer: relationship to response to therapy. J Nucl Med 2002;43(4):500–509.PubMed
31.
go back to reference Mankoff DA, Dunnwald LK, Partridge SC, Specht JM. Blood flow-metabolism mismatch: good for the tumor, bad for the patient. Clin Cancer Res 2009;15(17):5294–5296.PubMedPubMedCentralCrossRef Mankoff DA, Dunnwald LK, Partridge SC, Specht JM. Blood flow-metabolism mismatch: good for the tumor, bad for the patient. Clin Cancer Res 2009;15(17):5294–5296.PubMedPubMedCentralCrossRef
32.
go back to reference Mérida I, Ávila-Flores A. Tumor metabolism: new opportunities for cancer therapy. Clin Transl Oncol 2006;8(10):711–716.PubMedCrossRef Mérida I, Ávila-Flores A. Tumor metabolism: new opportunities for cancer therapy. Clin Transl Oncol 2006;8(10):711–716.PubMedCrossRef
33.
go back to reference Moscoso A, Ruibal Á, Domínguez-Prado I, Fernández-Ferreiro A, Herranz M, Albaina L, Argibay S, Silva-Rodríguez J, Pardo-Montero J, Aguiar P. Texture analysis of high-resolution dedicated breast F-FDG PET images correlates with immunohistochemical factors and subtype of breast cancer. Eur J Nucl Med Mol Imaging 2018;45(2):196–206.PubMedCrossRef Moscoso A, Ruibal Á, Domínguez-Prado I, Fernández-Ferreiro A, Herranz M, Albaina L, Argibay S, Silva-Rodríguez J, Pardo-Montero J, Aguiar P. Texture analysis of high-resolution dedicated breast F-FDG PET images correlates with immunohistochemical factors and subtype of breast cancer. Eur J Nucl Med Mol Imaging 2018;45(2):196–206.PubMedCrossRef
34.
go back to reference Mullani NA, Gould KL. First-pass measurements of regional blood flow with external detectors. J Nucl Med 1983;24(7):577–581.PubMed Mullani NA, Gould KL. First-pass measurements of regional blood flow with external detectors. J Nucl Med 1983;24(7):577–581.PubMed
35.
go back to reference Mullani NA, Herbst RS, O’Neil RG, Gould KL, Barron BJ, Abbruzzese JL. Tumor blood flow measured by PET dynamic imaging of first-pass 18F-FDG uptake: a comparison with 15o-labeled water-measured blood flow. J Nucl Med 2008;49(4):517–523.PubMedCrossRef Mullani NA, Herbst RS, O’Neil RG, Gould KL, Barron BJ, Abbruzzese JL. Tumor blood flow measured by PET dynamic imaging of first-pass 18F-FDG uptake: a comparison with 15o-labeled water-measured blood flow. J Nucl Med 2008;49(4):517–523.PubMedCrossRef
36.
go back to reference Neufeld G, Kessler O. Pro-angiogenic cytokines and their role in tumor angiogenesis. Cancer Metastasis Rev 2006;25(3):373–385.PubMedCrossRef Neufeld G, Kessler O. Pro-angiogenic cytokines and their role in tumor angiogenesis. Cancer Metastasis Rev 2006;25(3):373–385.PubMedCrossRef
37.
go back to reference Orlhac F, Nioche C, Soussan M, Buvat I. Understanding changes in tumor texture indices in PET: a comparison between visual assessment and index values in simulated and patient data. J Nucl Med 2017;58(3):387–392.PubMedCrossRef Orlhac F, Nioche C, Soussan M, Buvat I. Understanding changes in tumor texture indices in PET: a comparison between visual assessment and index values in simulated and patient data. J Nucl Med 2017;58(3):387–392.PubMedCrossRef
38.
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):e0145,063.CrossRef 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):e0145,063.CrossRef
39.
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):414–422.PubMedCrossRef 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):414–422.PubMedCrossRef
40.
go back to reference Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge Ø, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D. Molecular portraits of human breast tumours. Nature 2000; 406(6797):747–752. Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge Ø, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D. Molecular portraits of human breast tumours. Nature 2000; 406(6797):747–752.
42.
go back to reference Schaefer A, Kremp S, Hellwig D, Rübe C, Kirsch CM, Nestle U. A contrast-oriented algorithm for FDG-PET-based delineation of tumour volumes for the radiotherapy of lung cancer: derivation from phantom measurements and validation in patient data. Eur J Nucl Med Mol Imaging 2008;35(11):1989–1999.PubMedCrossRef Schaefer A, Kremp S, Hellwig D, Rübe C, Kirsch CM, Nestle U. A contrast-oriented algorithm for FDG-PET-based delineation of tumour volumes for the radiotherapy of lung cancer: derivation from phantom measurements and validation in patient data. Eur J Nucl Med Mol Imaging 2008;35(11):1989–1999.PubMedCrossRef
43.
go back to reference Seroul P, Sarrut D. 2008. VV: A viewer for the evaluation of 4D image registration. MIDAS Journal (Medical Image Computing and Computer-Assisted Intervention MICCAI’2008, Workshop - Systems and Architectures for Computer Assisted Interventions), 1–8. http://vv.creatis.insa-lyon.fr/. Seroul P, Sarrut D. 2008. VV: A viewer for the evaluation of 4D image registration. MIDAS Journal (Medical Image Computing and Computer-Assisted Intervention MICCAI’2008, Workshop - Systems and Architectures for Computer Assisted Interventions), 1–8. http://​vv.​creatis.​insa-lyon.​fr/​.
45.
go back to reference Son SH, Kim DH, Hong CM, Kim CY, Jeong SY, Lee SW, Lee J, Ahn BC. Prognostic implication of intratumoral metabolic heterogeneity in invasive ductal carcinoma of the breast. BMC Cancer 2014;14: 585.PubMedPubMedCentralCrossRef Son SH, Kim DH, Hong CM, Kim CY, Jeong SY, Lee SW, Lee J, Ahn BC. Prognostic implication of intratumoral metabolic heterogeneity in invasive ductal carcinoma of the breast. BMC Cancer 2014;14: 585.PubMedPubMedCentralCrossRef
46.
go back to reference Soussan M, Orlhac F, Boubaya M, Zelek L, Ziol M, Eder V, Buvat I. Relationship between tumor heterogeneity measured on FDG-PET/CT and pathological prognostic factors in invasive breast cancer. PLoS One 2014;9(4):e94,017.CrossRef Soussan M, Orlhac F, Boubaya M, Zelek L, Ziol M, Eder V, Buvat I. Relationship between tumor heterogeneity measured on FDG-PET/CT and pathological prognostic factors in invasive breast cancer. PLoS One 2014;9(4):e94,017.CrossRef
47.
go back to reference Specht JM, Kurland BF, Montgomery SK, Dunnwald LK, Doot RK, Gralow JR, Ellis GK, Linden HM, Livingston RB, Allison KH, Schubert EK, Mankoff DA. Tumor metabolism and blood flow as assessed by positron emission tomography varies by tumor subtype in locally advanced breast cancer. Clin Cancer Res 2010;16(10):2803–2810.PubMedPubMedCentralCrossRef Specht JM, Kurland BF, Montgomery SK, Dunnwald LK, Doot RK, Gralow JR, Ellis GK, Linden HM, Livingston RB, Allison KH, Schubert EK, Mankoff DA. Tumor metabolism and blood flow as assessed by positron emission tomography varies by tumor subtype in locally advanced breast cancer. Clin Cancer Res 2010;16(10):2803–2810.PubMedPubMedCentralCrossRef
48.
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.PubMedCrossRef 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.PubMedCrossRef
49.
go back to reference Walker MD, Asselin MC, Julyan PJ, Feldmann M, Talbot PS, Jones T, Matthews JC. Bias in iterative reconstruction of low-statistics PET data: benefits of a resolution model. Phys Med Biol 2011;56(4): 931–949.PubMedCrossRef Walker MD, Asselin MC, Julyan PJ, Feldmann M, Talbot PS, Jones T, Matthews JC. Bias in iterative reconstruction of low-statistics PET data: benefits of a resolution model. Phys Med Biol 2011;56(4): 931–949.PubMedCrossRef
50.
go back to reference Yan J, Chu-Shern JL, Loi HY, Khor LK, Sinha AK, Quek ST, Tham IWK, Townsend D. Impact of image reconstruction settings on texture features in 18F-FDG PET. J Nucl Med 2015;56(11):1667–1673.PubMedCrossRef Yan J, Chu-Shern JL, Loi HY, Khor LK, Sinha AK, Quek ST, Tham IWK, Townsend D. Impact of image reconstruction settings on texture features in 18F-FDG PET. J Nucl Med 2015;56(11):1667–1673.PubMedCrossRef
51.
go back to reference Yang W, Klos K, Yang Y, Smith TL, Shi D, Yu D. ErbB2 overexpression correlates with increased expression of vascular endothelial growth factors A, C, and D in human breast carcinoma. Cancer 2002;94 (11):2855–61.PubMedCrossRef Yang W, Klos K, Yang Y, Smith TL, Shi D, Yu D. ErbB2 overexpression correlates with increased expression of vascular endothelial growth factors A, C, and D in human breast carcinoma. Cancer 2002;94 (11):2855–61.PubMedCrossRef
52.
go back to reference Yoo TS, Ackerman MJ, Lorensen WE, Schroeder W, Chalana V, Aylward S, Metaxas D, Whitaker R. Engineering and algorithm design for an image processing API: a technical report on ITK - the insight toolkit. In: Westwood J, editor. Proceedings of medicine meets virtual reality. Amsterdam: IOS Press; 2002. P. 586–592. Yoo TS, Ackerman MJ, Lorensen WE, Schroeder W, Chalana V, Aylward S, Metaxas D, Whitaker R. Engineering and algorithm design for an image processing API: a technical report on ITK - the insight toolkit. In: Westwood J, editor. Proceedings of medicine meets virtual reality. Amsterdam: IOS Press; 2002. P. 586–592.
53.
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):381–394.PubMedCrossRef Zardavas D, Irrthum A, Swanton C, Piccart M. Clinical management of breast cancer heterogeneity. Nat Rev Clin Oncol 2015;12(7):381–394.PubMedCrossRef
Metadata
Title
Biological correlates of tumor perfusion and its heterogeneity in newly diagnosed breast cancer using dynamic first-pass 18F-FDG PET/CT
Authors
Neree Payan
Benoit Presles
François Brunotte
Charles Coutant
Isabelle Desmoulins
Jean-Marc Vrigneaud
Alexandre Cochet
Publication date
01-05-2020
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nuclear Medicine and Molecular Imaging / Issue 5/2020
Print ISSN: 1619-7070
Electronic ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-019-04422-4

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