Skip to main content
Top
Published in: Breast Cancer Research 6/2014

Open Access 01-12-2014 | Research article

Standardized uptake value of 18F-fluorodeoxyglucose positron emission tomography for prediction of tumor recurrence in breast cancer beyond tumor burden

Authors: Sung Gwe Ahn, Jong Tae Park, Hak Min Lee, Hak Woo Lee, Tae Joo Jeon, Kyunghwa Han, Seung Ah Lee, Seung Myung Dong, Young Hoon Ryu, Eun Ju Son, Joon Jeong

Published in: Breast Cancer Research | Issue 6/2014

Login to get access

Abstract

Introduction

18F-fluorodeoxyglucose positron emission tomography (FDG-PET) can reveal the metabolic activity of malignant tumors. Recent advances gained from molecular studies suggest that tumor biology can be a good predictor of prognosis in breast cancer. We compared the ability of maximum standardized uptake values (SUVmax) derived by FDG-PET with tumor burden in predicting tumor recurrence for patients with breast cancer.

Methods

496 patients with breast cancer who underwent preoperative FDG-PET between April 2004 and May 2009 were retrospectively identified. SUVmax was obtained by FDG-PET, and the cutoff point was defined using a time-dependent receiver operating characteristic curve for recurrence-free survival (RFS). The primary endpoint was RFS.

Results

In multivariate analysis for RFS, SUVmax carried independent prognostic significance (hazard ratio, 2.39; 95% confidence interval, 1.20 to 4.76; P = 0.012). When the patients were classified into four groups according to the combined factors of tumor size (≤2 cm versus >2 cm) and SUVmax (<4 versus ≥4), RFS differed significantly (P < 0.001). Similarly, SUVmax had prognostic value in combination with nodal status (negative versus positive) or stage (I versus II and III) (P < 0.001 and P = 0.001, respectively). In hormone receptor–positive disease, SUVmax remained a significant prognostic factor for RFS based on multivariate analysis.

Conclusions

Our results highlight the prognostic value of FDG-PET in prediction of tumor relapse for patients with breast cancer. Particularly in patients with hormone receptor–positive disease, the tumor metabolic information provided by FDG-PET is more significantly correlated with prognosis than tumor burden.
Appendix
Available only for authorised users
Literature
1.
go back to reference Demicheli R, Abbattista A, Miceli R, Valagussa P, Bonadonna G: Time distribution of the recurrence risk for breast cancer patients undergoing mastectomy: further support about the concept of tumor dormancy. Breast Cancer Res Treat. 1996, 41: 177-185. 10.1007/BF01807163.CrossRefPubMed Demicheli R, Abbattista A, Miceli R, Valagussa P, Bonadonna G: Time distribution of the recurrence risk for breast cancer patients undergoing mastectomy: further support about the concept of tumor dormancy. Breast Cancer Res Treat. 1996, 41: 177-185. 10.1007/BF01807163.CrossRefPubMed
2.
go back to reference Carter CL, Allen C, Henson DE: Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer. 1989, 63: 181-187. 10.1002/1097-0142(19890101)63:1<181::AID-CNCR2820630129>3.0.CO;2-H.CrossRefPubMed Carter CL, Allen C, Henson DE: Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer. 1989, 63: 181-187. 10.1002/1097-0142(19890101)63:1<181::AID-CNCR2820630129>3.0.CO;2-H.CrossRefPubMed
3.
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 O, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D: Molecular portraits of human breast tumours. Nature. 2000, 406: 747-752. 10.1038/35021093.CrossRefPubMed Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lønning PE, Børresen-Dale AL, Brown PO, Botstein D: Molecular portraits of human breast tumours. Nature. 2000, 406: 747-752. 10.1038/35021093.CrossRefPubMed
4.
go back to reference Park YH, Lee SJ, Cho EY, Choi YL, Lee JE, Nam SJ, Yang JH, Shin JH, Ko EY, Han BK, Ahn JS, Im YH: Clinical relevance of TNM staging system according to breast cancer subtypes. Ann Oncol. 2011, 22: 1554-1560. 10.1093/annonc/mdq617.CrossRefPubMed Park YH, Lee SJ, Cho EY, Choi YL, Lee JE, Nam SJ, Yang JH, Shin JH, Ko EY, Han BK, Ahn JS, Im YH: Clinical relevance of TNM staging system according to breast cancer subtypes. Ann Oncol. 2011, 22: 1554-1560. 10.1093/annonc/mdq617.CrossRefPubMed
5.
go back to reference Hernandez-Aya LF, Chavez-MacGregor M, Lei X, Meric-Bernstam F, Buchholz TA, Hsu L, Sahin AA, Do KA, Valero V, Hortobagyi GN, Gonzalez-Angulo AM: Nodal status and clinical outcomes in a large cohort of patients with triple-negative breast cancer. J Clin Oncol. 2011, 29: 2628-2634. 10.1200/JCO.2010.32.1877.CrossRefPubMedPubMedCentral Hernandez-Aya LF, Chavez-MacGregor M, Lei X, Meric-Bernstam F, Buchholz TA, Hsu L, Sahin AA, Do KA, Valero V, Hortobagyi GN, Gonzalez-Angulo AM: Nodal status and clinical outcomes in a large cohort of patients with triple-negative breast cancer. J Clin Oncol. 2011, 29: 2628-2634. 10.1200/JCO.2010.32.1877.CrossRefPubMedPubMedCentral
6.
go back to reference Seo S, Hatano E, Higashi T, Hara T, Tada M, Tamaki N, Iwaisako K, Ikai I, Uemoto S: Fluorine-18 fluorodeoxyglucose positron emission tomography predicts tumor differentiation, P-glycoprotein expression, and outcome after resection in hepatocellular carcinoma. Clin Cancer Res. 2007, 13: 427-433. 10.1158/1078-0432.CCR-06-1357.CrossRefPubMed Seo S, Hatano E, Higashi T, Hara T, Tada M, Tamaki N, Iwaisako K, Ikai I, Uemoto S: Fluorine-18 fluorodeoxyglucose positron emission tomography predicts tumor differentiation, P-glycoprotein expression, and outcome after resection in hepatocellular carcinoma. Clin Cancer Res. 2007, 13: 427-433. 10.1158/1078-0432.CCR-06-1357.CrossRefPubMed
7.
go back to reference Cerfolio RJ, Bryant AS, Ohja B, Bartolucci AA: The maximum standardized uptake values on positron emission tomography of a non-small cell lung cancer predict stage, recurrence, and survival. J Thorac Cardiovasc Surg. 2005, 130: 151-159. 10.1016/j.jtcvs.2004.11.007.CrossRefPubMed Cerfolio RJ, Bryant AS, Ohja B, Bartolucci AA: The maximum standardized uptake values on positron emission tomography of a non-small cell lung cancer predict stage, recurrence, and survival. J Thorac Cardiovasc Surg. 2005, 130: 151-159. 10.1016/j.jtcvs.2004.11.007.CrossRefPubMed
8.
go back to reference Ueda S, Kondoh N, Tsuda H, Yamamoto S, Asakawa H, Fukatsu K, Kobayashi T, Yamamoto J, Tamura K, Ishida J, Abe Y, Yamamoto M, Mochizuki H: Expression of centromere protein F (CENP-F) associated with higher FDG uptake on PET/CT, detected by cDNA microarray, predicts high-risk patients with primary breast cancer. BMC Cancer. 2008, 8: 384-10.1186/1471-2407-8-384.CrossRefPubMedPubMedCentral Ueda S, Kondoh N, Tsuda H, Yamamoto S, Asakawa H, Fukatsu K, Kobayashi T, Yamamoto J, Tamura K, Ishida J, Abe Y, Yamamoto M, Mochizuki H: Expression of centromere protein F (CENP-F) associated with higher FDG uptake on PET/CT, detected by cDNA microarray, predicts high-risk patients with primary breast cancer. BMC Cancer. 2008, 8: 384-10.1186/1471-2407-8-384.CrossRefPubMedPubMedCentral
9.
go back to reference Palaskas N, Larson SM, Schultz N, Komisopoulou E, Wong J, Rohle D, Campos C, Yannuzzi N, Osborne JR, Linkov I, Kastenhuber ER, Taschereau R, Plaisier SB, Tran C, Heguy A, Wu H, Sander C, Phelps ME, Brennan C, Port E, Huse JT, Graeber TG, Mellinghoff IK: 18F-fluorodeoxy-glucose positron emission tomography marks MYC-overexpressing human basal-like breast cancers. Cancer Res. 2011, 71: 5164-5174. 10.1158/0008-5472.CAN-10-4633.CrossRefPubMedPubMedCentral Palaskas N, Larson SM, Schultz N, Komisopoulou E, Wong J, Rohle D, Campos C, Yannuzzi N, Osborne JR, Linkov I, Kastenhuber ER, Taschereau R, Plaisier SB, Tran C, Heguy A, Wu H, Sander C, Phelps ME, Brennan C, Port E, Huse JT, Graeber TG, Mellinghoff IK: 18F-fluorodeoxy-glucose positron emission tomography marks MYC-overexpressing human basal-like breast cancers. Cancer Res. 2011, 71: 5164-5174. 10.1158/0008-5472.CAN-10-4633.CrossRefPubMedPubMedCentral
10.
go back to reference Basu S, Chen W, Tchou J, Mavi A, Cermik T, Czerniecki B, Schnall M, Alavi A: Comparison of triple-negative and estrogen receptor-positive/progesterone receptor-positive/HER2-negative breast carcinoma using quantitative fluorine-18 fluorodeoxyglucose/positron emission tomography imaging parameters: a potentially useful method for disease characterization. Cancer. 2008, 112: 995-1000. 10.1002/cncr.23226.CrossRefPubMed Basu S, Chen W, Tchou J, Mavi A, Cermik T, Czerniecki B, Schnall M, Alavi A: Comparison of triple-negative and estrogen receptor-positive/progesterone receptor-positive/HER2-negative breast carcinoma using quantitative fluorine-18 fluorodeoxyglucose/positron emission tomography imaging parameters: a potentially useful method for disease characterization. Cancer. 2008, 112: 995-1000. 10.1002/cncr.23226.CrossRefPubMed
11.
go back to reference Shimoda W, Hayashi M, Murakami K, Oyama T, Sunagawa M: The relationship between FDG uptake in PET scans and biological behavior in breast cancer. Breast Cancer. 2007, 14: 260-268. 10.2325/jbcs.14.260.CrossRefPubMed Shimoda W, Hayashi M, Murakami K, Oyama T, Sunagawa M: The relationship between FDG uptake in PET scans and biological behavior in breast cancer. Breast Cancer. 2007, 14: 260-268. 10.2325/jbcs.14.260.CrossRefPubMed
12.
go back to reference Mavi A, Cermik TF, Urhan M, Puskulcu H, Basu S, Yu JQ, Zhuang H, Czerniecki B, Alavi A: The effects of estrogen, progesterone, and C-erbB-2 receptor states on 18F-FDG uptake of primary breast cancer lesions. J Nucl Med. 2007, 48: 1266-1272. 10.2967/jnumed.106.037440.CrossRefPubMed Mavi A, Cermik TF, Urhan M, Puskulcu H, Basu S, Yu JQ, Zhuang H, Czerniecki B, Alavi A: The effects of estrogen, progesterone, and C-erbB-2 receptor states on 18F-FDG uptake of primary breast cancer lesions. J Nucl Med. 2007, 48: 1266-1272. 10.2967/jnumed.106.037440.CrossRefPubMed
13.
go back to reference Moeder CB, Giltnane JM, Harigopal M, Molinaro A, Robinson A, Gelmon K, Huntsman D, Camp RL, Rimm DL: Quantitative justification of the change from 10% to 30% for human epidermal growth factor receptor 2 scoring in the American Society of Clinical Oncology/College of American Pathologists guidelines: tumor heterogeneity in breast cancer and its implications for tissue microarray–based assessment of outcome. J Clin Oncol. 2007, 25: 5418-5425. 10.1200/JCO.2007.12.8033.CrossRefPubMed Moeder CB, Giltnane JM, Harigopal M, Molinaro A, Robinson A, Gelmon K, Huntsman D, Camp RL, Rimm DL: Quantitative justification of the change from 10% to 30% for human epidermal growth factor receptor 2 scoring in the American Society of Clinical Oncology/College of American Pathologists guidelines: tumor heterogeneity in breast cancer and its implications for tissue microarray–based assessment of outcome. J Clin Oncol. 2007, 25: 5418-5425. 10.1200/JCO.2007.12.8033.CrossRefPubMed
14.
go back to reference American Joint Committee on Cancer (AJCC): AJCC Cancer Staging Manual. 7th edition. Edited by Edge S, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. New York: Springer; 2010. American Joint Committee on Cancer (AJCC): AJCC Cancer Staging Manual. 7th edition. Edited by Edge S, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. New York: Springer; 2010.
15.
go back to reference Harrell FE, Lee KL, Mark DB: Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996, 15: 361-387. 10.1002/(SICI)1097-0258(19960229)15:4<361::AID-SIM168>3.0.CO;2-4.CrossRefPubMed Harrell FE, Lee KL, Mark DB: Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med. 1996, 15: 361-387. 10.1002/(SICI)1097-0258(19960229)15:4<361::AID-SIM168>3.0.CO;2-4.CrossRefPubMed
16.
go back to reference Han W, Kang SY, Korean Breast Cancer Society: Relationship between age at diagnosis and outcome of premenopausal breast cancer: age less than 35 years is a reasonable cut-off for defining young age-onset breast cancer. Breast Cancer Res Treat. 2010, 119: 193-200. 10.1007/s10549-009-0388-z.CrossRefPubMed Han W, Kang SY, Korean Breast Cancer Society: Relationship between age at diagnosis and outcome of premenopausal breast cancer: age less than 35 years is a reasonable cut-off for defining young age-onset breast cancer. Breast Cancer Res Treat. 2010, 119: 193-200. 10.1007/s10549-009-0388-z.CrossRefPubMed
18.
go back to reference De Cicco C, Gilardi L, Botteri E, Fracassi SL, Di Dia GA, Botta F, Prisco G, Lombardo D, Rotmensz N, Veronesi U, Paganelli G: Is [18F] fluorodeoxyglucose uptake by the primary tumor a prognostic factor in breast cancer?. Breast. 2013, 22: 39-43. 10.1016/j.breast.2012.05.009.CrossRefPubMed De Cicco C, Gilardi L, Botteri E, Fracassi SL, Di Dia GA, Botta F, Prisco G, Lombardo D, Rotmensz N, Veronesi U, Paganelli G: Is [18F] fluorodeoxyglucose uptake by the primary tumor a prognostic factor in breast cancer?. Breast. 2013, 22: 39-43. 10.1016/j.breast.2012.05.009.CrossRefPubMed
19.
go back to reference Inoue T, Yutani K, Taguchi T, Tamaki Y, Shiba E, Noguchi S: Preoperative evaluation of prognosis in breast cancer patients by [18F]2-deoxy-2-fluoro-d-glucose-positron emission tomography. J Cancer Res Clin Oncol. 2004, 130: 273-278. 10.1007/s00432-003-0536-5.CrossRefPubMed Inoue T, Yutani K, Taguchi T, Tamaki Y, Shiba E, Noguchi S: Preoperative evaluation of prognosis in breast cancer patients by [18F]2-deoxy-2-fluoro-d-glucose-positron emission tomography. J Cancer Res Clin Oncol. 2004, 130: 273-278. 10.1007/s00432-003-0536-5.CrossRefPubMed
20.
go back to reference Ueda S, Tsuda H, Asakawa H, Shigekawa T, Fukatsu K, Kondo N, Yamamoto M, Hama Y, Tamura K, Ishida J, Abe Y, Mochizuki H: Clinicopathological and prognostic relevance of uptake level using 18F-fluorodeoxyglucose positron emission tomography/computed tomography fusion imaging (18F-FDG PET/CT) in primary breast cancer. Jpn J Clin Oncol. 2008, 38: 250-258. 10.1093/jjco/hyn019.CrossRefPubMed Ueda S, Tsuda H, Asakawa H, Shigekawa T, Fukatsu K, Kondo N, Yamamoto M, Hama Y, Tamura K, Ishida J, Abe Y, Mochizuki H: Clinicopathological and prognostic relevance of uptake level using 18F-fluorodeoxyglucose positron emission tomography/computed tomography fusion imaging (18F-FDG PET/CT) in primary breast cancer. Jpn J Clin Oncol. 2008, 38: 250-258. 10.1093/jjco/hyn019.CrossRefPubMed
21.
go back to reference Vander Heiden MG, Cantley LC, Thompson CB: Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009, 324: 1029-1033. 10.1126/science.1160809.CrossRefPubMedPubMedCentral Vander Heiden MG, Cantley LC, Thompson CB: Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009, 324: 1029-1033. 10.1126/science.1160809.CrossRefPubMedPubMedCentral
22.
go back to reference Schieber MS, Chandel NS: ROS links glucose metabolism to breast cancer stem cell and EMT phenotype. Cancer Cell. 2013, 23: 265-267. 10.1016/j.ccr.2013.02.021.CrossRefPubMed Schieber MS, Chandel NS: ROS links glucose metabolism to breast cancer stem cell and EMT phenotype. Cancer Cell. 2013, 23: 265-267. 10.1016/j.ccr.2013.02.021.CrossRefPubMed
23.
go back to reference Levine AJ, Puzio-Kuter AM: The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science. 2010, 330: 1340-1344. 10.1126/science.1193494.CrossRefPubMed Levine AJ, Puzio-Kuter AM: The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science. 2010, 330: 1340-1344. 10.1126/science.1193494.CrossRefPubMed
25.
go back to reference Wirapati P, Sotiriou C, Kunkel S, Farmer P, Pradervand S, Haibe-Kains B, Desmedt C, Ignatiadis M, Sengstag T, Schütz F, Goldstein DR, Piccart M, Delorenzi M: Meta-analysis of gene expression profiles in breast cancer: toward a unified understanding of breast cancer subtyping and prognosis signatures. Breast Cancer Res. 2008, 10: R65-10.1186/bcr2124.CrossRefPubMedPubMedCentral Wirapati P, Sotiriou C, Kunkel S, Farmer P, Pradervand S, Haibe-Kains B, Desmedt C, Ignatiadis M, Sengstag T, Schütz F, Goldstein DR, Piccart M, Delorenzi M: Meta-analysis of gene expression profiles in breast cancer: toward a unified understanding of breast cancer subtyping and prognosis signatures. Breast Cancer Res. 2008, 10: R65-10.1186/bcr2124.CrossRefPubMedPubMedCentral
26.
go back to reference Yau C, Sninsky J, Kwok S, Wang A, Degnim A, Ingle JN, Gillett C, Tutt A, Waldman F, Moore D, Esserman L, Benz CC: An optimized five-gene multi-platform predictor of hormone receptor negative and triple negative breast cancer metastatic risk. Breast Cancer Res. 2013, 15: R103-10.1186/bcr3567.CrossRefPubMedPubMedCentral Yau C, Sninsky J, Kwok S, Wang A, Degnim A, Ingle JN, Gillett C, Tutt A, Waldman F, Moore D, Esserman L, Benz CC: An optimized five-gene multi-platform predictor of hormone receptor negative and triple negative breast cancer metastatic risk. Breast Cancer Res. 2013, 15: R103-10.1186/bcr3567.CrossRefPubMedPubMedCentral
27.
go back to reference Koo HR, Park JS, Kang KW, Cho N, Chang JM, Bae MS, Kim WH, Lee SH, Kim MY, Kim JY, Seo M, Moon WK: 18F-FDG uptake in breast cancer correlates with immunohistochemically defined subtypes. Eur Radiol. 2014, 24: 610-618. 10.1007/s00330-013-3037-1.CrossRefPubMed Koo HR, Park JS, Kang KW, Cho N, Chang JM, Bae MS, Kim WH, Lee SH, Kim MY, Kim JY, Seo M, Moon WK: 18F-FDG uptake in breast cancer correlates with immunohistochemically defined subtypes. Eur Radiol. 2014, 24: 610-618. 10.1007/s00330-013-3037-1.CrossRefPubMed
Metadata
Title
Standardized uptake value of 18F-fluorodeoxyglucose positron emission tomography for prediction of tumor recurrence in breast cancer beyond tumor burden
Authors
Sung Gwe Ahn
Jong Tae Park
Hak Min Lee
Hak Woo Lee
Tae Joo Jeon
Kyunghwa Han
Seung Ah Lee
Seung Myung Dong
Young Hoon Ryu
Eun Ju Son
Joon Jeong
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 6/2014
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/s13058-014-0502-y

Other articles of this Issue 6/2014

Breast Cancer Research 6/2014 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine