Skip to main content
Top
Published in: European Radiology 4/2015

01-04-2015 | Breast

Tumour 18 F-FDG Uptake on preoperative PET/CT may predict axillary lymph node metastasis in ER-positive/HER2-negative and HER2-positive breast cancer subtypes

Authors: Jin You Kim, Suck Hong Lee, Suk Kim, Taewoo Kang, Young Tae Bae

Published in: European Radiology | Issue 4/2015

Login to get access

Abstract

Objectives

To evaluate the association between tumour FDG uptake on preoperative PET/CT and axillary lymph node metastasis (ALNM) according to breast cancer subtype.

Methods

The records of 671 patients with invasive breast cancer who underwent 18 F-FDG PET/CT and surgery were reviewed. Using immunohistochemistry, tumours were divided into three subtypes: oestrogen receptor (ER)-positive/human epidermal growth factor receptor 2 (HER2)-negative, HER2-positive, and triple-negative. Tumour FDG uptake, expressed as maximum standardized uptake value (SUVmax), and clinicopathological variables were analysed.

Results

ALNM was present in 187 of 461 ER-positive/HER2-negative, 54 of 97 HER2-positive, and 38 of 113 triple-negative tumours. On multivariate analysis, high tumour SUVmax (≥4.25) (P < 0.001), large tumour size (>2 cm) (P = 0.003) and presence of lymphovascular invasion (P < 0.001) were independent variables associated with ALNM. On subset analyses, tumour SUVmax maintained independent significance for predicting ALNM in ER-positive/HER2-negative (adjusted odds ratio: 3.277, P < 0.001) and HER2-positive tumours (adjusted odds ratio: 14.637, P = 0.004). No association was found for triple-negative tumours (P = 0.161).

Conclusions

Tumour SUVmax may be an independent prognostic factor for ALNM in patients with invasive breast cancer, especially in ER-positive/HER2-negative and HER2-positive subtypes, but not in those with triple-negative subtype.

Key points

• Tumour SUVmax could be an imaging biomarker for predicting ALNM
• Tumour SUVmax predicting ALNM is effective in ER-positive/HER2-negative and HER2-positive subtypes
• Tumour SUVmax predicting ALNM is inaccurate in triple-negative subtypes
• Accurate prognostic prediction based on molecular subtype may facilitate individualized management
Literature
1.
go back to reference Weiss RB, Woolf SH, Demakos E et al (2003) Natural history of more than 20 years of node-positive primary breast carcinoma treated with cyclophosphamide, methotrexate, and fluorouracil-based adjuvant chemotherapy: a study by the cancer and leukemia group B. J Clin Oncol 21:1825–1835CrossRefPubMed Weiss RB, Woolf SH, Demakos E et al (2003) Natural history of more than 20 years of node-positive primary breast carcinoma treated with cyclophosphamide, methotrexate, and fluorouracil-based adjuvant chemotherapy: a study by the cancer and leukemia group B. J Clin Oncol 21:1825–1835CrossRefPubMed
2.
go back to reference Arriagada R, Le MG, Dunant A, Tubiana M, Contesso G (2006) Twenty‐five years of follow‐up in patients with operable breast carcinoma. Cancer 106:743–750CrossRefPubMed Arriagada R, Le MG, Dunant A, Tubiana M, Contesso G (2006) Twenty‐five years of follow‐up in patients with operable breast carcinoma. Cancer 106:743–750CrossRefPubMed
3.
go back to reference Colleoni M, Rotmensz N, Maisonneuve P et al (2007) Prognostic role of the extent of peritumoral vascular invasion in operable breast cancer. Ann Oncol 18:1632–1640CrossRefPubMed Colleoni M, Rotmensz N, Maisonneuve P et al (2007) Prognostic role of the extent of peritumoral vascular invasion in operable breast cancer. Ann Oncol 18:1632–1640CrossRefPubMed
4.
go back to reference Viale G, Zurrida S, Maiorano E et al (2005) Predicting the status of axillary sentinel lymph nodes in 4351 patients with invasive breast carcinoma treated in a single institution. Cancer 103:492–500CrossRefPubMed Viale G, Zurrida S, Maiorano E et al (2005) Predicting the status of axillary sentinel lymph nodes in 4351 patients with invasive breast carcinoma treated in a single institution. Cancer 103:492–500CrossRefPubMed
5.
go back to reference Yoshihara E, Smeets A, Laenen A et al (2013) Predictors of axillary lymph node metastases in early breast cancer and their applicability in clinical practice. Breast 22:357–361CrossRefPubMed Yoshihara E, Smeets A, Laenen A et al (2013) Predictors of axillary lymph node metastases in early breast cancer and their applicability in clinical practice. Breast 22:357–361CrossRefPubMed
6.
go back to reference Carey LA, Perou CM, Livasy CA et al (2006) Race, breast cancer subtypes, and survival in the carolina breast cancer study. JAMA 295:2492–2502CrossRefPubMed Carey LA, Perou CM, Livasy CA et al (2006) Race, breast cancer subtypes, and survival in the carolina breast cancer study. JAMA 295:2492–2502CrossRefPubMed
7.
go back to reference Van’t Veer LJ, Dai H, De Vijver V et al (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:530–536CrossRef Van’t Veer LJ, Dai H, De Vijver V et al (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:530–536CrossRef
8.
go back to reference Nguyen PL, Taghian AG, Katz MS et al (2008) Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol 26:2373–2378CrossRefPubMed Nguyen PL, Taghian AG, Katz MS et al (2008) Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol 26:2373–2378CrossRefPubMed
9.
go back to reference Desmedt C, Haibe-Kains B, Wirapati P et al (2008) Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes. Clin Cancer Res 14:5158–5165CrossRefPubMed Desmedt C, Haibe-Kains B, Wirapati P et al (2008) Biological processes associated with breast cancer clinical outcome depend on the molecular subtypes. Clin Cancer Res 14:5158–5165CrossRefPubMed
10.
go back to reference Sánchez-Muñoz A, García-Tapiador AM, Martínez-Ortega E et al (2008) Tumour molecular subtyping according to hormone receptors and HER2 status defines different pathological complete response to neoadjuvant chemotherapy in patients with locally advanced breast cancer. Clin Transl Oncol 10:646–653CrossRefPubMed Sánchez-Muñoz A, García-Tapiador AM, Martínez-Ortega E et al (2008) Tumour molecular subtyping according to hormone receptors and HER2 status defines different pathological complete response to neoadjuvant chemotherapy in patients with locally advanced breast cancer. Clin Transl Oncol 10:646–653CrossRefPubMed
11.
go back to reference de Ronde JJ, Hannemann J, Halfwerk H et al (2010) Concordance of clinical and molecular breast cancer subtyping in the context of preoperative chemotherapy response. Breast Cancer Res Treat 119:119–126CrossRefPubMed de Ronde JJ, Hannemann J, Halfwerk H et al (2010) Concordance of clinical and molecular breast cancer subtyping in the context of preoperative chemotherapy response. Breast Cancer Res Treat 119:119–126CrossRefPubMed
12.
go back to reference Fuster D, Duch J, Paredes P et al (2008) Preoperative staging of large primary breast cancer with [18 F] fluorodeoxyglucose positron emission tomography/computed tomography compared with conventional imaging procedures. J Clin Oncol 26:4746–4751CrossRefPubMed Fuster D, Duch J, Paredes P et al (2008) Preoperative staging of large primary breast cancer with [18 F] fluorodeoxyglucose positron emission tomography/computed tomography compared with conventional imaging procedures. J Clin Oncol 26:4746–4751CrossRefPubMed
13.
go back to reference Eubank WB, Mankoff D, Bhattacharya M et al (2004) Impact of FDG PET on defining the extent of disease and on the treatment of patients with recurrent or metastatic breast cancer. AJR Am J Roentgenol 183:479–486CrossRefPubMed Eubank WB, Mankoff D, Bhattacharya M et al (2004) Impact of FDG PET on defining the extent of disease and on the treatment of patients with recurrent or metastatic breast cancer. AJR Am J Roentgenol 183:479–486CrossRefPubMed
14.
go back to reference Hatt M, Groheux D, Martineau A et al (2013) Comparison between 18 F-FDG PET image-derived indices for early prediction of response to neoadjuvant chemotherapy in breast cancer. J Nucl Med 54:341–349CrossRefPubMed Hatt M, Groheux D, Martineau A et al (2013) Comparison between 18 F-FDG PET image-derived indices for early prediction of response to neoadjuvant chemotherapy in breast cancer. J Nucl Med 54:341–349CrossRefPubMed
15.
go back to reference Song B, Hong CM, Lee HJ et al (2011) Prognostic value of primary tumor uptake on F-18 FDG PET/CT in patients with invasive ductal breast cancer. Nucl Med Mol Imaging 45:117–124CrossRefPubMedCentralPubMed Song B, Hong CM, Lee HJ et al (2011) Prognostic value of primary tumor uptake on F-18 FDG PET/CT in patients with invasive ductal breast cancer. Nucl Med Mol Imaging 45:117–124CrossRefPubMedCentralPubMed
16.
go back to reference Ueda S, Tsuda H, Asakawa H et al (2008) Clinicopathological and prognostic relevance of uptake level using 18 F-fluorodeoxyglucose positron emission tomography/computed tomography fusion imaging (18 F-FDG PET/CT) in primary breast cancer. Jpn J Clin Oncol 38:250–258CrossRefPubMed Ueda S, Tsuda H, Asakawa H et al (2008) Clinicopathological and prognostic relevance of uptake level using 18 F-fluorodeoxyglucose positron emission tomography/computed tomography fusion imaging (18 F-FDG PET/CT) in primary breast cancer. Jpn J Clin Oncol 38:250–258CrossRefPubMed
17.
go back to reference Koo HR, Park JS, Kang KW et al (2014) 18 F-FDG uptake in breast cancer correlates with immunohistochemically defined subtypes. Eur Radiol 24:610–618CrossRefPubMed Koo HR, Park JS, Kang KW et al (2014) 18 F-FDG uptake in breast cancer correlates with immunohistochemically defined subtypes. Eur Radiol 24:610–618CrossRefPubMed
18.
go back to reference Greene FL (2002) AJCC cancer staging manual. Springer Greene FL (2002) AJCC cancer staging manual. Springer
19.
go back to reference Elston C, Ellis I (1991) Pathological prognostic factors in breast cancer. I. the value of histological grade in breast cancer: experience from a large study with long‐term follow‐up. Histopathology 19:403–410CrossRefPubMed Elston C, Ellis I (1991) Pathological prognostic factors in breast cancer. I. the value of histological grade in breast cancer: experience from a large study with long‐term follow‐up. Histopathology 19:403–410CrossRefPubMed
20.
go back to reference Allred DC, Harvey JM, Berardo M, Clark GM (1998) Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 11:155–168PubMed Allred DC, Harvey JM, Berardo M, Clark GM (1998) Prognostic and predictive factors in breast cancer by immunohistochemical analysis. Mod Pathol 11:155–168PubMed
21.
go back to reference Moeder CB, Giltnane JM, Harigopal M et al (2007) 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 25:5418–5425CrossRefPubMed Moeder CB, Giltnane JM, Harigopal M et al (2007) 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 25:5418–5425CrossRefPubMed
22.
go back to reference Yamashita H, Toyama T, Nishio M et al (2006) p53 protein accumulation predicts resistance to endocrine therapy and decreased post-relapse survival in metastatic breast cancer. Breast Cancer Res 8:R48CrossRefPubMedCentralPubMed Yamashita H, Toyama T, Nishio M et al (2006) p53 protein accumulation predicts resistance to endocrine therapy and decreased post-relapse survival in metastatic breast cancer. Breast Cancer Res 8:R48CrossRefPubMedCentralPubMed
23.
go back to reference Cheang MC, Chia SK, Voduc D et al (2009) Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst 101:736–750CrossRefPubMedCentralPubMed Cheang MC, Chia SK, Voduc D et al (2009) Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst 101:736–750CrossRefPubMedCentralPubMed
24.
go back to reference Bader AA, Tio J, Petru E et al (2002) T1 breast cancer: identification of patients at low risk of axillary lymph node metastases. Breast Cancer Res Treat 76:11–17CrossRefPubMed Bader AA, Tio J, Petru E et al (2002) T1 breast cancer: identification of patients at low risk of axillary lymph node metastases. Breast Cancer Res Treat 76:11–17CrossRefPubMed
25.
go back to reference Ridriguez-Pinilla SM, Sarrio D, Honrado E et al (2006) Prognostic significance of basal-like phenotype and fascin expression in node-negative invasive breast cancers. Clin Cancer Res 12:1533–1539CrossRef Ridriguez-Pinilla SM, Sarrio D, Honrado E et al (2006) Prognostic significance of basal-like phenotype and fascin expression in node-negative invasive breast cancers. Clin Cancer Res 12:1533–1539CrossRef
26.
go back to reference Krag DN, Anderson SJ, Julian TB et al (2007) Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncol 8:881–888CrossRefPubMed Krag DN, Anderson SJ, Julian TB et al (2007) Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncol 8:881–888CrossRefPubMed
27.
go back to reference McMasters KM, Tuttle TM, Carlson DJ et al (2000) Sentinel lymph node biopsy for breast cancer: a suitable alternative to routine axillary dissection in multi-institutional practice when optimal technique is used. J Clin Oncol 18:2560–2566PubMed McMasters KM, Tuttle TM, Carlson DJ et al (2000) Sentinel lymph node biopsy for breast cancer: a suitable alternative to routine axillary dissection in multi-institutional practice when optimal technique is used. J Clin Oncol 18:2560–2566PubMed
28.
go back to reference Wilke LG, McCall LM, Posther KE et al (2006) Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann Surg Oncol 13:491–500CrossRefPubMed Wilke LG, McCall LM, Posther KE et al (2006) Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann Surg Oncol 13:491–500CrossRefPubMed
29.
go back to reference Valente SA, Levine GM, Silverstein MJ et al (2012) Accuracy of predicting axillary lymph node positivity by physical examination, mammography, ultrasonography, and magnetic resonance imaging. Ann Surg Oncol 19:1825–1830CrossRefPubMed Valente SA, Levine GM, Silverstein MJ et al (2012) Accuracy of predicting axillary lymph node positivity by physical examination, mammography, ultrasonography, and magnetic resonance imaging. Ann Surg Oncol 19:1825–1830CrossRefPubMed
30.
go back to reference Kim J, Lee J, Chang E et al (2009) Selective sentinel node plus additional non-sentinel node biopsy based on an FDG-PET/CT scan in early breast cancer patients: single institutional experience. World J Surg 33:943–949CrossRefPubMed Kim J, Lee J, Chang E et al (2009) Selective sentinel node plus additional non-sentinel node biopsy based on an FDG-PET/CT scan in early breast cancer patients: single institutional experience. World J Surg 33:943–949CrossRefPubMed
31.
go back to reference Veronesi U, De Cicco C, Galimberti VE et al (2007) A comparative study on the value of FDG-PET and sentinel node biopsy to identify occult axillary metastasis. Ann Oncol 18:473–478CrossRefPubMed Veronesi U, De Cicco C, Galimberti VE et al (2007) A comparative study on the value of FDG-PET and sentinel node biopsy to identify occult axillary metastasis. Ann Oncol 18:473–478CrossRefPubMed
32.
go back to reference Gil-Rendo A, Zornoza G, Garcia-Velloso MJ et al (2006) Fluorodeoxyglucose positron emission tomography with sentinel lymph node biopsy for evaluation of axillary involvement in breast cancer. Br J Surg 93:707–712CrossRefPubMed Gil-Rendo A, Zornoza G, Garcia-Velloso MJ et al (2006) Fluorodeoxyglucose positron emission tomography with sentinel lymph node biopsy for evaluation of axillary involvement in breast cancer. Br J Surg 93:707–712CrossRefPubMed
33.
go back to reference Fletcher JW, Djulbegovic B, Soares HP et al (2008) Recommendations on the use of 18 F-FDG PET in oncology. J Nucl Med 49:480–508CrossRefPubMed Fletcher JW, Djulbegovic B, Soares HP et al (2008) Recommendations on the use of 18 F-FDG PET in oncology. J Nucl Med 49:480–508CrossRefPubMed
34.
go back to reference Groves AM, Shastry M, Rodriguez-Justo M et al (2011) 18 F-FDG PET and biomarkers for tumour angiogenesis in early breast cancer. Eur J Nucl Med Mol Imaging 38:46–52CrossRefPubMed Groves AM, Shastry M, Rodriguez-Justo M et al (2011) 18 F-FDG PET and biomarkers for tumour angiogenesis in early breast cancer. Eur J Nucl Med Mol Imaging 38:46–52CrossRefPubMed
35.
go back to reference Song BI, Lee SW, Jeong SY et al (2012) 18 F-FDG uptake by metastatic axillary lymph nodes on pretreatment PET/CT as a prognostic factor for recurrence in patients with invasive ductal breast cancer. J Nucl Med 53:1337–1344CrossRefPubMed Song BI, Lee SW, Jeong SY et al (2012) 18 F-FDG uptake by metastatic axillary lymph nodes on pretreatment PET/CT as a prognostic factor for recurrence in patients with invasive ductal breast cancer. J Nucl Med 53:1337–1344CrossRefPubMed
36.
go back to reference Carey LA, Dees EC, Sawyer L et al (2007) The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res 13:2329–2334 Carey LA, Dees EC, Sawyer L et al (2007) The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res 13:2329–2334
37.
go back to reference Dent R, Trudeau M, Pritchard KI et al (2007) Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 13:4429–4434CrossRefPubMed Dent R, Trudeau M, Pritchard KI et al (2007) Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 13:4429–4434CrossRefPubMed
38.
go back to reference Voduc KD, Cheang MC, Tyldesley S, Gelmon K, Nielsen TO, Kennecke H (2010) Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol 28:1684–1691CrossRefPubMed Voduc KD, Cheang MC, Tyldesley S, Gelmon K, Nielsen TO, Kennecke H (2010) Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol 28:1684–1691CrossRefPubMed
39.
go back to reference Vicente AMG, Castrejón ÁS, Martín AL et al (2013) Molecular subtypes of breast cancer: metabolic correlation with 18 F-FDG PET/CT. Eur J Nucl Med Mol Imaging 40:1304–1311CrossRef Vicente AMG, Castrejón ÁS, Martín AL et al (2013) Molecular subtypes of breast cancer: metabolic correlation with 18 F-FDG PET/CT. Eur J Nucl Med Mol Imaging 40:1304–1311CrossRef
40.
go back to reference Hugh J, Hanson J, Cheang MC et al (2009) Breast cancer subtypes and response to docetaxel in node-positive breast cancer: use of an immunohistochemical definition in the BCIRG 001 trial. J Clin Oncol 27:1168–1176CrossRefPubMedCentralPubMed Hugh J, Hanson J, Cheang MC et al (2009) Breast cancer subtypes and response to docetaxel in node-positive breast cancer: use of an immunohistochemical definition in the BCIRG 001 trial. J Clin Oncol 27:1168–1176CrossRefPubMedCentralPubMed
41.
go back to reference Jatoi I, Hilsenbeck SG, Clark GM, Osborne CK (1999) Significance of axillary lymph node metastasis in primary breast cancer. J Clin Oncol 17:2334–2340PubMed Jatoi I, Hilsenbeck SG, Clark GM, Osborne CK (1999) Significance of axillary lymph node metastasis in primary breast cancer. J Clin Oncol 17:2334–2340PubMed
Metadata
Title
Tumour 18 F-FDG Uptake on preoperative PET/CT may predict axillary lymph node metastasis in ER-positive/HER2-negative and HER2-positive breast cancer subtypes
Authors
Jin You Kim
Suck Hong Lee
Suk Kim
Taewoo Kang
Young Tae Bae
Publication date
01-04-2015
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 4/2015
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-014-3452-y

Other articles of this Issue 4/2015

European Radiology 4/2015 Go to the issue