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Published in: Breast Cancer 1/2017

01-01-2017 | Original Article

Predictive and prognostic value of FDG-PET/CT imaging and different response evaluation criteria after primary systemic therapy of breast cancer

Authors: Tímea Tőkés, Kornélia Kajáry, Gyöngyvér Szentmártoni, Zsolt Lengyel, Tamás Györke, László Torgyík, Krisztián Somlai, Anna-Mária Tőkés, Janina Kulka, Magdolna Dank

Published in: Breast Cancer | Issue 1/2017

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Abstract

Objectives

(1) To predict pathological complete remission (pCR) and survival after primary systemic therapy (PST) in patients diagnosed with breast cancer by using two different PET/CT based scores: a simplified PERCIST-based PET/CT score (Method 1) and a combined PET/CT score supplemented with the morphological results of the RECIST system (Method 2) and (2) to assess the effect of different breast carcinoma subtypes on tumor response and its evaluation.

Methods

Eighty-eight patients were enrolled in the study who underwent PET/CT imaging before and after PST. PET/CTs were evaluated by changes in maximum Standardized Uptake Value (SUVmax) and tumor size. Method 1 and 2 were applied to predict pathological complete remission (pCR). Kaplan–Meier analyses for survival were performed. Classification into biological subtypes was performed based on the pre-therapeutic tumor characteristics.

Results

A total of 30/88 patients showed pCR (34.1 %). Comparing pCR/non-pCR patient groups, significant differences were detected by changes in SUVmax (p < 0.001) and tumor size (p < 0.001) regarding the primary breast lesions. To predict pCR, Method 2 had higher sensitivity (72.4 % vs. 44.8 %) and negative predictive value (57.9 % vs. 45.8 %) with lower false negativity rate (16 vs. 32) than Method 1. pCR rate was higher in Her2-positive and triple negative tumors. Despite the significant differences detected between the biological subtypes regarding changes in primary tumor SUVmax (p = 0.007) and size (p = 0.015), the subtypes only had significant impact on response evaluation with Method 2 and not with Method 1. In our study, neither clinical nor pathological CR were predictors of longer progression-free survival.

Conclusions

Our results suggest that combined PET/CT criteria are more predictive of pCR. The effect of biological subtypes is significant on pCR rate as well as on the changes in FDG-uptake and morphological tumor response. Response evaluation with combined criteria was also able to reflect the differences between the biological behavior of breast tumor subtypes.
Literature
2.
go back to reference Kaufmann M, Morrow M, von Minckwitz G, Harris JR. Locoregional treatment of primary breast cancer: consensus recommendations from an International Expert Panel. Cancer. 2010;116:1184–91.CrossRefPubMed Kaufmann M, Morrow M, von Minckwitz G, Harris JR. Locoregional treatment of primary breast cancer: consensus recommendations from an International Expert Panel. Cancer. 2010;116:1184–91.CrossRefPubMed
4.
go back to reference Avril N, Sassen S, Roylance R. Response to therapy in breast cancer. J Nucl Med. 2009;50(Suppl 1):55S–63S.CrossRefPubMed Avril N, Sassen S, Roylance R. Response to therapy in breast cancer. J Nucl Med. 2009;50(Suppl 1):55S–63S.CrossRefPubMed
5.
go back to reference Machiavelli MR, Romero AO, Perez JE, Lacava JA, Dominguez ME, Rodriguez R, et al. Prognostic significance of pathological response of primary tumor and metastatic axillary lymph nodes after neoadjuvant chemotherapy for locally advanced breast carcinoma. Cancer J Sci Am. 1998;4:125–31.PubMed Machiavelli MR, Romero AO, Perez JE, Lacava JA, Dominguez ME, Rodriguez R, et al. Prognostic significance of pathological response of primary tumor and metastatic axillary lymph nodes after neoadjuvant chemotherapy for locally advanced breast carcinoma. Cancer J Sci Am. 1998;4:125–31.PubMed
6.
go back to reference Wolmark N, Wang J, Mamounas E, Bryant J, Fisher B. Preoperative chemotherapy in patients with operable breast cancer: nine-year results from National Surgical Adjuvant Breast and Bowel Project B-18. J Natl Cancer Inst Monogr. 2001; 96–102. Wolmark N, Wang J, Mamounas E, Bryant J, Fisher B. Preoperative chemotherapy in patients with operable breast cancer: nine-year results from National Surgical Adjuvant Breast and Bowel Project B-18. J Natl Cancer Inst Monogr. 2001; 96–102.
7.
go back to reference Prowell TM, Pazdur R. Pathological complete response and accelerated drug approval in early breast cancer. N Engl J Med. 2012;366:2438–41.CrossRefPubMed Prowell TM, Pazdur R. Pathological complete response and accelerated drug approval in early breast cancer. N Engl J Med. 2012;366:2438–41.CrossRefPubMed
8.
go back to reference Tardivon AA, Ollivier L, El Khoury C, Thibault F. Monitoring therapeutic efficacy in breast carcinomas. Eur Radiol. 2006;16:2549–58.CrossRefPubMed Tardivon AA, Ollivier L, El Khoury C, Thibault F. Monitoring therapeutic efficacy in breast carcinomas. Eur Radiol. 2006;16:2549–58.CrossRefPubMed
9.
go back to reference Groheux D, Espie M, Giacchetti S, Hindie E. Performance of FDG PET/CT in the clinical management of breast cancer. Radiology. 2013;266:388–405.CrossRefPubMed Groheux D, Espie M, Giacchetti S, Hindie E. Performance of FDG PET/CT in the clinical management of breast cancer. Radiology. 2013;266:388–405.CrossRefPubMed
10.
go back to reference Groheux D, Giacchetti S, Delord M, Hindie E, Vercellino L, Cuvier C, et al. 18F-FDG PET/CT in staging patients with locally advanced or inflammatory breast cancer: comparison to conventional staging. J Nucl Med. 2013;54:5–11.CrossRefPubMed Groheux D, Giacchetti S, Delord M, Hindie E, Vercellino L, Cuvier C, et al. 18F-FDG PET/CT in staging patients with locally advanced or inflammatory breast cancer: comparison to conventional staging. J Nucl Med. 2013;54:5–11.CrossRefPubMed
11.
go back to reference Wang Y, Zhang C, Liu J, Huang G. Is 18F-FDG PET accurate to predict neoadjuvant therapy response in breast cancer? A meta-analysis. Breast Cancer Res Treat. 2012;131:357–69.CrossRefPubMed Wang Y, Zhang C, Liu J, Huang G. Is 18F-FDG PET accurate to predict neoadjuvant therapy response in breast cancer? A meta-analysis. Breast Cancer Res Treat. 2012;131:357–69.CrossRefPubMed
12.
go back to reference Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumors. J Nucl Med. 2009;50(Suppl 1):122S–50S.CrossRefPubMedPubMedCentral Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PERCIST: evolving considerations for PET response criteria in solid tumors. J Nucl Med. 2009;50(Suppl 1):122S–50S.CrossRefPubMedPubMedCentral
13.
go back to reference Tőkés T, Szentmártoni Gy, Torgyík L, Kulka J, Lengyel Zs, Györke T, et al. Complexity of the response evaluation during primary systemic therapy of breast cancer. J Clin Oncol ASCO Annual Meeting Abstracts 2014; 32(15_Suppl): e12010. Tőkés T, Szentmártoni Gy, Torgyík L, Kulka J, Lengyel Zs, Györke T, et al. Complexity of the response evaluation during primary systemic therapy of breast cancer. J Clin Oncol ASCO Annual Meeting Abstracts 2014; 32(15_Suppl): e12010.
14.
go back to reference Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.CrossRefPubMed Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.CrossRefPubMed
15.
go back to reference Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ, et al. Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol. 2011;22:1736–47.CrossRefPubMedPubMedCentral Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ, et al. Strategies for subtypes—dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol. 2011;22:1736–47.CrossRefPubMedPubMedCentral
16.
go back to reference Tokes T, Szentmartoni G, Torgyik L, Kajary K, Lengyel Z, Gyorke T, et al. Response evaluation after primary systemic therapy of Her2 positive breast cancer—an observational cross-sectional study. Croat Med J. 2015;56:128–38.CrossRefPubMedPubMedCentral Tokes T, Szentmartoni G, Torgyik L, Kajary K, Lengyel Z, Gyorke T, et al. Response evaluation after primary systemic therapy of Her2 positive breast cancer—an observational cross-sectional study. Croat Med J. 2015;56:128–38.CrossRefPubMedPubMedCentral
17.
go back to reference Lang I, Kahan Z, Pinter T, Dank M, Boer K, Pajkos G, et al. Pharmaceutical therapy of breast cancer. Magy Onkol. 2010;54:237–54.CrossRefPubMed Lang I, Kahan Z, Pinter T, Dank M, Boer K, Pajkos G, et al. Pharmaceutical therapy of breast cancer. Magy Onkol. 2010;54:237–54.CrossRefPubMed
19.
go back to reference Jones RL, Lakhani SR, Ring AE, Ashley S, Walsh G, Smith IE. Pathological complete response and residual DCIS following neoadjuvant chemotherapy for breast carcinoma. Br J Cancer. 2006;94:358–62.CrossRefPubMedPubMedCentral Jones RL, Lakhani SR, Ring AE, Ashley S, Walsh G, Smith IE. Pathological complete response and residual DCIS following neoadjuvant chemotherapy for breast carcinoma. Br J Cancer. 2006;94:358–62.CrossRefPubMedPubMedCentral
20.
go back to reference Allred DC, Harvey JM, Berardo M, Clark GM. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol. 1998;11:155–68.PubMed Allred DC, Harvey JM, Berardo M, Clark GM. Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol. 1998;11:155–68.PubMed
21.
go back to reference Wolff AC, Hammond ME, Schwartz JN, Hagerty KL, Allred DC, Cote RJ, et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. J Clin Oncol. 2007;25:118–45.CrossRefPubMed Wolff AC, Hammond ME, Schwartz JN, Hagerty KL, Allred DC, Cote RJ, et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. J Clin Oncol. 2007;25:118–45.CrossRefPubMed
22.
go back to reference Wolff AC, Hammond ME, Hicks DG, Dowsett M, McShane LM, Allison KH, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol. 2013;31:3997–4013.CrossRefPubMed Wolff AC, Hammond ME, Hicks DG, Dowsett M, McShane LM, Allison KH, et al. Recommendations for human epidermal growth factor receptor 2 testing in breast cancer: American Society of Clinical Oncology/College of American Pathologists clinical practice guideline update. J Clin Oncol. 2013;31:3997–4013.CrossRefPubMed
23.
go back to reference Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thurlimann 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;24:2206–23.CrossRefPubMedPubMedCentral Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thurlimann 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;24:2206–23.CrossRefPubMedPubMedCentral
24.
go back to reference Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17:1471–4.CrossRefPubMed Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17:1471–4.CrossRefPubMed
25.
go back to reference Shankar LK, Hoffman JM, Bacharach S, Graham MM, Karp J, Lammertsma AA, et al. Consensus recommendations for the use of 18F-FDG PET as an indicator of therapeutic response in patients in National Cancer Institute Trials. J Nucl Med. 2006;47:1059–66.PubMed Shankar LK, Hoffman JM, Bacharach S, Graham MM, Karp J, Lammertsma AA, et al. Consensus recommendations for the use of 18F-FDG PET as an indicator of therapeutic response in patients in National Cancer Institute Trials. J Nucl Med. 2006;47:1059–66.PubMed
26.
go back to reference Boellaard R, O’Doherty MJ, Weber WA, Mottaghy FM, Lonsdale MN, Stroobants SG, et al. FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37:181–200.CrossRefPubMed Boellaard R, O’Doherty MJ, Weber WA, Mottaghy FM, Lonsdale MN, Stroobants SG, et al. FDG PET and PET/CT: EANM procedure guidelines for tumour PET imaging: version 1.0. Eur J Nucl Med Mol Imaging. 2010;37:181–200.CrossRefPubMed
27.
go back to reference Mauri D, Pavlidis N, Ioannidis JP. Neoadjuvant versus adjuvant systemic treatment in breast cancer: a meta-analysis. J Natl Cancer Inst. 2005;97:188–94.CrossRefPubMed Mauri D, Pavlidis N, Ioannidis JP. Neoadjuvant versus adjuvant systemic treatment in breast cancer: a meta-analysis. J Natl Cancer Inst. 2005;97:188–94.CrossRefPubMed
28.
go back to reference Bonnefoi H, Litiere S, Piccart M, MacGrogan G, Fumoleau P, Brain E, et al. Pathological complete response after neoadjuvant chemotherapy is an independent predictive factor irrespective of simplified breast cancer intrinsic subtypes: a landmark and two-step approach analyses from the EORTC 10994/BIG 1-00 phase III trial. Ann Oncol. 2014;25:1128–36.CrossRefPubMedPubMedCentral Bonnefoi H, Litiere S, Piccart M, MacGrogan G, Fumoleau P, Brain E, et al. Pathological complete response after neoadjuvant chemotherapy is an independent predictive factor irrespective of simplified breast cancer intrinsic subtypes: a landmark and two-step approach analyses from the EORTC 10994/BIG 1-00 phase III trial. Ann Oncol. 2014;25:1128–36.CrossRefPubMedPubMedCentral
29.
go back to reference Groheux D, Giacchetti S, Espie M, Rubello D, Moretti JL, Hindie E. Early monitoring of response to neoadjuvant chemotherapy in breast cancer with 18F-FDG PET/CT: defining a clinical aim. Eur J Nucl Med Mol Imaging. 2011;38:419–25.CrossRefPubMed Groheux D, Giacchetti S, Espie M, Rubello D, Moretti JL, Hindie E. Early monitoring of response to neoadjuvant chemotherapy in breast cancer with 18F-FDG PET/CT: defining a clinical aim. Eur J Nucl Med Mol Imaging. 2011;38:419–25.CrossRefPubMed
30.
go back to reference Keam B, Im SA, Koh Y, Han SW, Oh DY, Cho N, et al. Predictive value of FDG PET/CT for pathologic axillary node involvement after neoadjuvant chemotherapy. Breast Cancer. 2013;20:167–73.CrossRefPubMed Keam B, Im SA, Koh Y, Han SW, Oh DY, Cho N, et al. Predictive value of FDG PET/CT for pathologic axillary node involvement after neoadjuvant chemotherapy. Breast Cancer. 2013;20:167–73.CrossRefPubMed
31.
go back to reference Straver ME, Aukema TS, Olmos RA, Rutgers EJ, Gilhuijs KG, Schot ME, et al. Feasibility of FDG PET/CT to monitor the response of axillary lymph node metastases to neoadjuvant chemotherapy in breast cancer patients. Eur J Nucl Med Mol Imaging. 2010;37:1069–76.CrossRefPubMedPubMedCentral Straver ME, Aukema TS, Olmos RA, Rutgers EJ, Gilhuijs KG, Schot ME, et al. Feasibility of FDG PET/CT to monitor the response of axillary lymph node metastases to neoadjuvant chemotherapy in breast cancer patients. Eur J Nucl Med Mol Imaging. 2010;37:1069–76.CrossRefPubMedPubMedCentral
32.
go back to reference Mghanga FP, Lan X, Bakari KH, Li C, Zhang Y. Fluorine-18 fluorodeoxyglucose positron emission tomography-computed tomography in monitoring the response of breast cancer to neoadjuvant chemotherapy: a meta-analysis. Clin Breast Cancer. 2013;13:271–9.CrossRefPubMed Mghanga FP, Lan X, Bakari KH, Li C, Zhang Y. Fluorine-18 fluorodeoxyglucose positron emission tomography-computed tomography in monitoring the response of breast cancer to neoadjuvant chemotherapy: a meta-analysis. Clin Breast Cancer. 2013;13:271–9.CrossRefPubMed
33.
go back to reference Groheux D, Hindie E, Giacchetti S, Delord M, Hamy AS, de Roquancourt A, et al. Triple-negative breast cancer: early assessment with 18F-FDG PET/CT during neoadjuvant chemotherapy identifies patients who are unlikely to achieve a pathologic complete response and are at a high risk of early relapse. J Nucl Med. 2012;53:249–54.CrossRefPubMed Groheux D, Hindie E, Giacchetti S, Delord M, Hamy AS, de Roquancourt A, et al. Triple-negative breast cancer: early assessment with 18F-FDG PET/CT during neoadjuvant chemotherapy identifies patients who are unlikely to achieve a pathologic complete response and are at a high risk of early relapse. J Nucl Med. 2012;53:249–54.CrossRefPubMed
34.
go back to reference Groheux D, Giacchetti S, Hatt M, Marty M, Vercellino L, de Roquancourt A, et al. HER2-overexpressing breast cancer: FDG uptake after two cycles of chemotherapy predicts the outcome of neoadjuvant treatment. Br J Cancer. 2013;109:1157–64.CrossRefPubMedPubMedCentral Groheux D, Giacchetti S, Hatt M, Marty M, Vercellino L, de Roquancourt A, et al. HER2-overexpressing breast cancer: FDG uptake after two cycles of chemotherapy predicts the outcome of neoadjuvant treatment. Br J Cancer. 2013;109:1157–64.CrossRefPubMedPubMedCentral
35.
go back to reference Humbert O, Cochet A, Riedinger JM, Berriolo-Riedinger A, Arnould L, Coudert B, et al. HER2-positive breast cancer: F-FDG PET for early prediction of response to trastuzumab plus taxane-based neoadjuvant chemotherapy. Eur J Nucl Med Mol Imaging. 2014;41:1525–33.CrossRefPubMed Humbert O, Cochet A, Riedinger JM, Berriolo-Riedinger A, Arnould L, Coudert B, et al. HER2-positive breast cancer: F-FDG PET for early prediction of response to trastuzumab plus taxane-based neoadjuvant chemotherapy. Eur J Nucl Med Mol Imaging. 2014;41:1525–33.CrossRefPubMed
36.
go back to reference Jung SY, Kim SK, Nam BH, Min SY, Lee SJ, Park C, et al. Prognostic Impact of [18F] FDG-PET in operable breast cancer treated with neoadjuvant chemotherapy. Ann Surg Oncol. 2010;17:247–53.CrossRefPubMed Jung SY, Kim SK, Nam BH, Min SY, Lee SJ, Park C, et al. Prognostic Impact of [18F] FDG-PET in operable breast cancer treated with neoadjuvant chemotherapy. Ann Surg Oncol. 2010;17:247–53.CrossRefPubMed
37.
go back to reference Berruti A, Amoroso V, Gallo F, Bertaglia V, Simoncini E, Pedersini R, et al. Pathologic complete response as a potential surrogate for the clinical outcome in patients with breast cancer after neoadjuvant therapy: a meta-regression of 29 randomized prospective studies. J Clin Oncol. 2014;32:3883–91.CrossRefPubMed Berruti A, Amoroso V, Gallo F, Bertaglia V, Simoncini E, Pedersini R, et al. Pathologic complete response as a potential surrogate for the clinical outcome in patients with breast cancer after neoadjuvant therapy: a meta-regression of 29 randomized prospective studies. J Clin Oncol. 2014;32:3883–91.CrossRefPubMed
38.
go back to reference Nakajo M, Kajiya Y, Kaneko T, Kaneko Y, Takasaki T, Tani A, et al. FDG PET/CT and diffusion-weighted imaging for breast cancer: prognostic value of maximum standardized uptake values and apparent diffusion coefficient values of the primary lesion. Eur J Nucl Med Mol Imaging. 2010;37:2011–20.CrossRefPubMed Nakajo M, Kajiya Y, Kaneko T, Kaneko Y, Takasaki T, Tani A, et al. FDG PET/CT and diffusion-weighted imaging for breast cancer: prognostic value of maximum standardized uptake values and apparent diffusion coefficient values of the primary lesion. Eur J Nucl Med Mol Imaging. 2010;37:2011–20.CrossRefPubMed
Metadata
Title
Predictive and prognostic value of FDG-PET/CT imaging and different response evaluation criteria after primary systemic therapy of breast cancer
Authors
Tímea Tőkés
Kornélia Kajáry
Gyöngyvér Szentmártoni
Zsolt Lengyel
Tamás Györke
László Torgyík
Krisztián Somlai
Anna-Mária Tőkés
Janina Kulka
Magdolna Dank
Publication date
01-01-2017
Publisher
Springer Japan
Published in
Breast Cancer / Issue 1/2017
Print ISSN: 1340-6868
Electronic ISSN: 1880-4233
DOI
https://doi.org/10.1007/s12282-016-0685-4

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