Skip to main content
Top
Published in: Annals of Surgical Oncology 7/2019

Open Access 01-07-2019 | Breast Cancer | Breast Oncology

Significance of Metabolic Tumor Volume at Baseline and Reduction of Mean Standardized Uptake Value in 18F-FDG-PET/CT Imaging for Predicting Pathological Complete Response in Breast Cancers Treated with Preoperative Chemotherapy

Authors: Tomoko Higuchi, MD, Yukie Fujimoto, MD, Hiromi Ozawa, MD, Ayako Bun, MD, Reiko Fukui, MD, Yoshimasa Miyagawa, MD, PhD, Michiko Imamura, MD, PhD, Kazuhiro Kitajima, MD, PhD, Koichiro Yamakado, MD, PhD, Yasuo Miyoshi, MD, PhD

Published in: Annals of Surgical Oncology | Issue 7/2019

Login to get access

Abstract

Background

The usefulness of 18F-fluorodeoxyglucose-positron emission tomography/computed tomography for evaluating the treatment efficacy of breast cancers is well-established; however, the predictive values of parameters such as metabolic tumor volume (MTV) and total lesion glycolysis (TLG) remain unknown.

Methods

This study examined 199 breast cancers treated with primary systemic chemotherapy (PSC) followed by operation, and determined the values of maximum standardized uptake value (SUVmax), peak SUV (SUVpeak), mean SUV (SUVmean), MTV, and TLG at baseline. Among these cases, data on early changes in these metabolic parameters in 70 breast cancers were also assessed.

Results

A pathological complete response (pCR) was achieved in 64 breast cancers. Breast cancers with low MTV at baseline had a significantly higher pCR rate than breast cancers with high MTV (47.9% vs. 23.4%; p = 0.0005). High reduction rates (∆) of SUVmax (p = 0.0001), SUVpeak (p = 0.0001), and SUVmean (p < 0.0001) resulted in an increased pCR compared with those for low ∆. The pCR rate was highest for the combination of low MTV and high ∆SUVmean (86.7%), and lowest for high MTV and low ∆SUVmean (15.4%); the remaining combinations were intermediate (58.6%; p < 0.0001). The combination of low MTV at baseline and high ∆SUVmean was a significant and independent predictor for pCR (odds ratio 28.63; 95% confidence interval 1.94–422.42; p = 0.0146) in multivariable analysis.

Conclusions

Low levels of MTV at baseline and a high reduction of SUVmean after PSC was significantly associated with pCR. These findings suggest the usefulness of these metabolic parameters for predicting the treatment efficacy of breast cancers.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mazouni C, Kau SW, Frye D, et al. Inclusion of taxanes, particularly weekly paclitaxel, in preoperative chemotherapy improves pathologic complete response rate in estrogen receptor-positive breast cancers. Ann Oncol. 2007; 18:874–880.CrossRefPubMed Mazouni C, Kau SW, Frye D, et al. Inclusion of taxanes, particularly weekly paclitaxel, in preoperative chemotherapy improves pathologic complete response rate in estrogen receptor-positive breast cancers. Ann Oncol. 2007; 18:874–880.CrossRefPubMed
2.
go back to reference Munkacsy G, Szasz MA, Menyhart O. Gene expression-based prognostic and predictive tools in breast cancer. Breast Cancer. 2015; 22:245–252.CrossRefPubMed Munkacsy G, Szasz MA, Menyhart O. Gene expression-based prognostic and predictive tools in breast cancer. Breast Cancer. 2015; 22:245–252.CrossRefPubMed
3.
4.
go back to reference Lin CY, Lin CL, Kao CH. Staging/restaging performance of F18-fluorodeoxyglucose positron emission tomography/magnetic resonance imaging in breast cancer: a review and meta-analysis. Eur J Radiol. 2018; 107:158–165.CrossRefPubMed Lin CY, Lin CL, Kao CH. Staging/restaging performance of F18-fluorodeoxyglucose positron emission tomography/magnetic resonance imaging in breast cancer: a review and meta-analysis. Eur J Radiol. 2018; 107:158–165.CrossRefPubMed
5.
go back to reference Kadoya T, Aogi K, Kiyoto S, Masumoto N, Sugawara Y, Okada M. Role of maximum standardized uptake value in fluorodeoxyglucose positron emission tomography/computed tomography predicts malignancy grade and prognosis of operable breast cancer: a multi-institute study. Breast Cancer Res Treat. 2013; 141:269–275.CrossRefPubMedPubMedCentral Kadoya T, Aogi K, Kiyoto S, Masumoto N, Sugawara Y, Okada M. Role of maximum standardized uptake value in fluorodeoxyglucose positron emission tomography/computed tomography predicts malignancy grade and prognosis of operable breast cancer: a multi-institute study. Breast Cancer Res Treat. 2013; 141:269–275.CrossRefPubMedPubMedCentral
6.
go back to reference Ahn SG, Park JT, Lee HM, et al. Standardized uptake value of 18F-fluorodeoxyglucose positron emission tomography for prediction of tumor recurrence in breast cancer beyond tumor burden. Breast Cancer Res. 2014; 16:502.CrossRefPubMedPubMedCentral Ahn SG, Park JT, Lee HM, et al. Standardized uptake value of 18F-fluorodeoxyglucose positron emission tomography for prediction of tumor recurrence in breast cancer beyond tumor burden. Breast Cancer Res. 2014; 16:502.CrossRefPubMedPubMedCentral
7.
go back to reference Chang JS, Lee J, Kim HJ, et al. (18)F-FDG/PET may help to identify a subgroup of patients with T1-T2 breast cancer and 1-3 positive lymph nodes who are at a high risk of recurrence after mastectomy. Cancer Res Treat. 2016; 48:508–517.CrossRefPubMed Chang JS, Lee J, Kim HJ, et al. (18)F-FDG/PET may help to identify a subgroup of patients with T1-T2 breast cancer and 1-3 positive lymph nodes who are at a high risk of recurrence after mastectomy. Cancer Res Treat. 2016; 48:508–517.CrossRefPubMed
8.
go back to reference Evangelista L, Cervino AR, Ghiotto C, et al. Could semiquantitative FDG analysis add information to the prognosis in patients with stage II/III breast cancer undergoing neoadjuvant treatment? Eur J Nucl Med Mol Imaging. 2015; 42:1648–1655.CrossRefPubMed Evangelista L, Cervino AR, Ghiotto C, et al. Could semiquantitative FDG analysis add information to the prognosis in patients with stage II/III breast cancer undergoing neoadjuvant treatment? Eur J Nucl Med Mol Imaging. 2015; 42:1648–1655.CrossRefPubMed
9.
go back to reference Higuchi T, Nishimukai A, Ozawa H, et al. Prognostic significance of preoperative 18F-FDG PET/CT for breast cancer subtypes. Breast 2016; 30:5–12.CrossRefPubMed Higuchi T, Nishimukai A, Ozawa H, et al. Prognostic significance of preoperative 18F-FDG PET/CT for breast cancer subtypes. Breast 2016; 30:5–12.CrossRefPubMed
10.
go back to reference Goulon D, Necib H, Henaff B, Rousseau C, Carlier T, Kraeber-Bodere F. Quantitative evaluation of therapeutic response by FDG-PET-CT in metastatic breast cancer. Front Med (Lausanne). 2016; 3:19. Goulon D, Necib H, Henaff B, Rousseau C, Carlier T, Kraeber-Bodere F. Quantitative evaluation of therapeutic response by FDG-PET-CT in metastatic breast cancer. Front Med (Lausanne). 2016; 3:19.
11.
go back to reference Andrade WP, Lima EN, Osório CA, et al. Can FDG-PET/CT predict early response to neoadjuvant chemotherapy in breast cancer? Eur J Surg Oncol. 2013; 39:1358–1363.CrossRefPubMed Andrade WP, Lima EN, Osório CA, et al. Can FDG-PET/CT predict early response to neoadjuvant chemotherapy in breast cancer? Eur J Surg Oncol. 2013; 39:1358–1363.CrossRefPubMed
12.
go back to reference Avril S, Muzic RF Jr, Plecha D, Traughber BJ, Vinayak S, Avril N. 18F-FDG PET/CT for monitoring of treatment response in breast cancer. J Nucl Med. 2016; 57:34S–39S.CrossRefPubMedPubMedCentral Avril S, Muzic RF Jr, Plecha D, Traughber BJ, Vinayak S, Avril N. 18F-FDG PET/CT for monitoring of treatment response in breast cancer. J Nucl Med. 2016; 57:34S–39S.CrossRefPubMedPubMedCentral
13.
go back to reference Groheux D, Mankoff D, Espie M, Hindie E. 18F-FDG PET/CT in the early prediction of pathological response in aggressive subtypes of breast cancer: review of the literature and recommendations for use in clinical trials. Eur J Nucl Med Mol Imaging. 2016; 43:983–993.CrossRefPubMed Groheux D, Mankoff D, Espie M, Hindie E. 18F-FDG PET/CT in the early prediction of pathological response in aggressive subtypes of breast cancer: review of the literature and recommendations for use in clinical trials. Eur J Nucl Med Mol Imaging. 2016; 43:983–993.CrossRefPubMed
14.
go back to reference Akimoto E, Kadoya T, Kajitani K, et al. Role of 18F-PET/CT in predicting prognosis of patients with breast cancer after neoadjuvant chemotherapy. Clin Breast Cancer. 2018; 18:45–52.CrossRefPubMed Akimoto E, Kadoya T, Kajitani K, et al. Role of 18F-PET/CT in predicting prognosis of patients with breast cancer after neoadjuvant chemotherapy. Clin Breast Cancer. 2018; 18:45–52.CrossRefPubMed
15.
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; 50:122S–150S.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; 50:122S–150S.CrossRefPubMedPubMedCentral
16.
go back to reference Soret M, Bacharach SL, Buvat I. Partial-volume effect in PET tumor imaging. J Nucl Med. 2007; 48:932–945.CrossRefPubMed Soret M, Bacharach SL, Buvat I. Partial-volume effect in PET tumor imaging. J Nucl Med. 2007; 48:932–945.CrossRefPubMed
17.
go back to reference Groheux D, Sanna A, Majdoub M, et al. Baseline tumor 18F-FDG uptake and modifications after 2 cycles of neoadjuvant chemotherapy are prognostic of outcome in ER+/HER2- breast cancer. J Nucl Med. 2015; 56:824–831.CrossRefPubMed Groheux D, Sanna A, Majdoub M, et al. Baseline tumor 18F-FDG uptake and modifications after 2 cycles of neoadjuvant chemotherapy are prognostic of outcome in ER+/HER2- breast cancer. J Nucl Med. 2015; 56:824–831.CrossRefPubMed
18.
go back to reference Lee HW, Lee HM, Choi SE, et al. The prognostic impact of early change in 18F-FDG PET SUV after neoadjuvant chemotherapy in patients with locally advanced breast cancer. J Nucl Med. 2016; 57:1183–1188.CrossRefPubMed Lee HW, Lee HM, Choi SE, et al. The prognostic impact of early change in 18F-FDG PET SUV after neoadjuvant chemotherapy in patients with locally advanced breast cancer. J Nucl Med. 2016; 57:1183–1188.CrossRefPubMed
19.
go back to reference The Japanese Breast Cancer Society. General rules for clinical and pathological recording of breast cancer, 18th ed. Tokyo: Kanehara Co., Ltd; 2018. The Japanese Breast Cancer Society. General rules for clinical and pathological recording of breast cancer, 18th ed. Tokyo: Kanehara Co., Ltd; 2018.
20.
go back to reference Kitajima K, Miyoshi Y, Yamano T, Odawara S, Higuchi T, Yamakado K. Prognostic value of FDG-PET and DWI in breast cancer. Ann Nucl Med. 2018; 32:44–53.CrossRefPubMed Kitajima K, Miyoshi Y, Yamano T, Odawara S, Higuchi T, Yamakado K. Prognostic value of FDG-PET and DWI in breast cancer. Ann Nucl Med. 2018; 32:44–53.CrossRefPubMed
21.
go back to reference Cheng L, Zhang J, Wang Y, et al. Textural features of 18F-FDG PET after two cycles of neoadjuvant chemotherapy can predict pCR in patients with locally advanced breast cancer. Ann Nucl Med. 2017; 31:544–552.CrossRefPubMed Cheng L, Zhang J, Wang Y, et al. Textural features of 18F-FDG PET after two cycles of neoadjuvant chemotherapy can predict pCR in patients with locally advanced breast cancer. Ann Nucl Med. 2017; 31:544–552.CrossRefPubMed
22.
go back to reference Jena A, Taneja S, Singh A, et al. Association of pharmacokinetic and metabolic parameters derived using simultaneous PET/MRI: initial findings and impact on response evaluation in breast cancer. Eur J Radiol. 2017; 92:30–36.CrossRefPubMed Jena A, Taneja S, Singh A, et al. Association of pharmacokinetic and metabolic parameters derived using simultaneous PET/MRI: initial findings and impact on response evaluation in breast cancer. Eur J Radiol. 2017; 92:30–36.CrossRefPubMed
23.
go back to reference Garcia-Vicente AM, Pérez-Beteta J, Pérez-García VM, Molina D, Jiménez-Londoño GA, et al. Metabolic tumor burden assessed by dual time point [18F]FDG PET/CT in locally advanced breast cancer: relation with tumor biology. Mol Imaging Biol. 2017; 19:636–644.CrossRefPubMed Garcia-Vicente AM, Pérez-Beteta J, Pérez-García VM, Molina D, Jiménez-Londoño GA, et al. Metabolic tumor burden assessed by dual time point [18F]FDG PET/CT in locally advanced breast cancer: relation with tumor biology. Mol Imaging Biol. 2017; 19:636–644.CrossRefPubMed
24.
go back to reference Jin S, Kim SB, Ahn JH, et al. 18 F-fluorodeoxyglucose uptake predicts pathological complete response after neoadjuvant chemotherapy for breast cancer: a retrospective cohort study. J Surg Oncol. 2013; 107:180–187.CrossRefPubMed Jin S, Kim SB, Ahn JH, et al. 18 F-fluorodeoxyglucose uptake predicts pathological complete response after neoadjuvant chemotherapy for breast cancer: a retrospective cohort study. J Surg Oncol. 2013; 107:180–187.CrossRefPubMed
25.
go back to reference Pahk K, Rhee S, Cho J, et al. The role of interim 18F-FDG PET/CT in predicting early response to neoadjuvant chemotherapy in breast cancer. Anticancer Res. 2014; 34:4447–4455.PubMed Pahk K, Rhee S, Cho J, et al. The role of interim 18F-FDG PET/CT in predicting early response to neoadjuvant chemotherapy in breast cancer. Anticancer Res. 2014; 34:4447–4455.PubMed
26.
go back to reference Groheux D, Majdoub M, Sanna A, et al. Early metabolic response to neoadjuvant treatment: FDG PET/CT criteria according to breast cancer subtype. Radiology. 2015; 277:358–371.CrossRefPubMed Groheux D, Majdoub M, Sanna A, et al. Early metabolic response to neoadjuvant treatment: FDG PET/CT criteria according to breast cancer subtype. Radiology. 2015; 277:358–371.CrossRefPubMed
27.
go back to reference Cho N, Im SA, Cheon GJ, et al. Integrated 18F-FDG PET/MRI in breast cancer: early prediction of response to neoadjuvant chemotherapy. Eur J Nucl Med Mol Imaging. 2018; 45:328–339.CrossRefPubMed Cho N, Im SA, Cheon GJ, et al. Integrated 18F-FDG PET/MRI in breast cancer: early prediction of response to neoadjuvant chemotherapy. Eur J Nucl Med Mol Imaging. 2018; 45:328–339.CrossRefPubMed
28.
go back to reference Groheux D, Biard L, Lehmann-Che J, et al. Tumor metabolism assessed by FDG-PET/CT and tumor proliferation assessed by genomic grade index to predict response to neoadjuvant chemotherapy in triple negative breast cancer. Eur J Nucl Med Mol Imaging. 2018; 45:1279–1288.CrossRefPubMed Groheux D, Biard L, Lehmann-Che J, et al. Tumor metabolism assessed by FDG-PET/CT and tumor proliferation assessed by genomic grade index to predict response to neoadjuvant chemotherapy in triple negative breast cancer. Eur J Nucl Med Mol Imaging. 2018; 45:1279–1288.CrossRefPubMed
29.
go back to reference de Cremoux P, Biard L, Poirot B, et al. 18FDG-PET/CT and molecular markers to predict response to neoadjuvant chemotherapy and outcome in HER2-negative advanced luminal breast cancers patients. Oncotarget. 2018; 9:16343–16353.CrossRefPubMedPubMedCentral de Cremoux P, Biard L, Poirot B, et al. 18FDG-PET/CT and molecular markers to predict response to neoadjuvant chemotherapy and outcome in HER2-negative advanced luminal breast cancers patients. Oncotarget. 2018; 9:16343–16353.CrossRefPubMedPubMedCentral
30.
go back to reference Humbert O, Riedinger JM, Charon-Barra C, et al. Identification of biomarkers including 18FDG-PET/CT for early prediction of response to neoadjuvant chemotherapy in triple-negative breast cancer. Clin Cancer Res. 2015; 21:5460–5468.CrossRefPubMed Humbert O, Riedinger JM, Charon-Barra C, et al. Identification of biomarkers including 18FDG-PET/CT for early prediction of response to neoadjuvant chemotherapy in triple-negative breast cancer. Clin Cancer Res. 2015; 21:5460–5468.CrossRefPubMed
31.
go back to reference Connolly RM, Leal JP, Goetz MP, et al. TBCRC 008: Early change in 18F-FDG uptake on PET predicts response to preoperative systemic therapy in human epidermal growth factor receptor 2–negative primary operable breast cancer. J Nucl Med. 2015; 56:31–37.CrossRefPubMed Connolly RM, Leal JP, Goetz MP, et al. TBCRC 008: Early change in 18F-FDG uptake on PET predicts response to preoperative systemic therapy in human epidermal growth factor receptor 2–negative primary operable breast cancer. J Nucl Med. 2015; 56:31–37.CrossRefPubMed
32.
go back to reference Kiyoto S, Sugawara Y, Hosokawa K, Nishimura R, Yamashita N, Ohsumi S, et al. Predictive ability of 18F-fluorodeoxyglucose positron emission tomography/computed tomography for pathological complete response and prognosis after neoadjuvant chemotherapy in triple-negative breast cancer patients. Asia Ocean J Nucl Med Biol. 2016; 4:3–11.PubMedPubMedCentral Kiyoto S, Sugawara Y, Hosokawa K, Nishimura R, Yamashita N, Ohsumi S, et al. Predictive ability of 18F-fluorodeoxyglucose positron emission tomography/computed tomography for pathological complete response and prognosis after neoadjuvant chemotherapy in triple-negative breast cancer patients. Asia Ocean J Nucl Med Biol. 2016; 4:3–11.PubMedPubMedCentral
33.
go back to reference Lemarignier C, Martineau A, Teixeira L, Vercellino L, Espié M, Merlet P, et al. Correlation between tumour characteristics, SUV measurements, metabolic tumour volume, TLG and textural features assessed with 18F-FDG PET in a large cohort of oestrogen receptor-positive breast cancer patients. Eur J Nucl Med Mol Imaging. 2017; 44:1145–1154.CrossRefPubMed Lemarignier C, Martineau A, Teixeira L, Vercellino L, Espié M, Merlet P, et al. Correlation between tumour characteristics, SUV measurements, metabolic tumour volume, TLG and textural features assessed with 18F-FDG PET in a large cohort of oestrogen receptor-positive breast cancer patients. Eur J Nucl Med Mol Imaging. 2017; 44:1145–1154.CrossRefPubMed
34.
go back to reference Im HJ, Kim YK, Kim YI, Lee JJ, Lee WW, Kim SE. Usefulness of combined metabolic-volumetric indices of (18)F-FDG PET/CT for the early prediction of neoadjuvant chemotherapy outcomes in breast cancer. Nucl Med Mol Imaging 2013; 47:36–43.CrossRefPubMed Im HJ, Kim YK, Kim YI, Lee JJ, Lee WW, Kim SE. Usefulness of combined metabolic-volumetric indices of (18)F-FDG PET/CT for the early prediction of neoadjuvant chemotherapy outcomes in breast cancer. Nucl Med Mol Imaging 2013; 47:36–43.CrossRefPubMed
35.
go back to reference Li H, Yao L, Jin P, Hu L, Li X, Guo T, Yang K. MRI and PET/CT for evaluation of the pathological response to neoadjuvant chemotherapy in breast cancer: a systematic review and meta-analysis. Breast. 2018; 40:106–115.CrossRefPubMed Li H, Yao L, Jin P, Hu L, Li X, Guo T, Yang K. MRI and PET/CT for evaluation of the pathological response to neoadjuvant chemotherapy in breast cancer: a systematic review and meta-analysis. Breast. 2018; 40:106–115.CrossRefPubMed
Metadata
Title
Significance of Metabolic Tumor Volume at Baseline and Reduction of Mean Standardized Uptake Value in 18F-FDG-PET/CT Imaging for Predicting Pathological Complete Response in Breast Cancers Treated with Preoperative Chemotherapy
Authors
Tomoko Higuchi, MD
Yukie Fujimoto, MD
Hiromi Ozawa, MD
Ayako Bun, MD
Reiko Fukui, MD
Yoshimasa Miyagawa, MD, PhD
Michiko Imamura, MD, PhD
Kazuhiro Kitajima, MD, PhD
Koichiro Yamakado, MD, PhD
Yasuo Miyoshi, MD, PhD
Publication date
01-07-2019
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 7/2019
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-019-07325-8

Other articles of this Issue 7/2019

Annals of Surgical Oncology 7/2019 Go to the issue