Volume 39, Issue 10 pp. 2059-2070

Original Research

Predicting Axillary Lymph Node Metastasis in Patients With Breast Invasive Ductal Carcinoma With Negative Axillary Ultrasound Results Using Conventional Ultrasound and Contrast-Enhanced Ultrasound

An-Qi Zhu MD

Department of Medical Ultrasound, Shanghai Tenth People's Hospital, Ultrasound Research and Education Institute, Tongji University Cancer Center, Shanghai Engineering Research Center of Ultrasound Diagnosis and Treatment, Tongji University School of Medicine, Shanghai, China

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

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Xiao-Long Li MD,

Xiao-Long Li MD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

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Li-Wei An PhD,

Li-Wei An PhD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

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Le-Hang Guo MD,

Le-Hang Guo MD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

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Hui-Jun Fu MD,

Hui-Jun Fu MD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Department of Pathology, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

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Li-Ping Sun MD, PhD,

Li-Ping Sun MD, PhD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

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Hui-Xiong Xu MD, PhD,

Corresponding Author

Hui-Xiong Xu MD, PhD

[email protected]

orcid.org/0000-0002-8699-854X

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

Address correspondence to Hui-Xiong Xu, MD, PhD, Department of Medical Ultrasound, Shanghai Tenth People's Hospital, Ultrasound Research and Education Institute, Tongji University Cancer Center, Shanghai Engineering Research Center of Ultrasound Diagnosis and Treatment, Tongji University School of Medicine, 301 Yanchang Middle Rd, 200072 Shanghai, China. E-mail: [email protected]Search for more papers by this author

An-Qi Zhu MD,

An-Qi Zhu MD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

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Xiao-Long Li MD,

Xiao-Long Li MD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

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Li-Wei An PhD,

Li-Wei An PhD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

Search for more papers by this author

Le-Hang Guo MD,

Le-Hang Guo MD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

Search for more papers by this author

Hui-Jun Fu MD,

Hui-Jun Fu MD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Department of Pathology, Shanghai Tenth People's Hospital, Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

Search for more papers by this author

Li-Ping Sun MD, PhD,

Li-Ping Sun MD, PhD

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

Search for more papers by this author

Hui-Xiong Xu MD, PhD,

Corresponding Author

Hui-Xiong Xu MD, PhD

[email protected]

orcid.org/0000-0002-8699-854X

Thyroid Institute Tongji University School of Medicine, Shanghai, China

Shanghai Center for Thyroid Diseases, Shanghai, China

First published: 05 May 2020

https://doi.org/10.1002/jum.15314

Citations: 15

This work was supported in part by the National Natural Science Foundation of China (grants 81927801 and 81725008), Fundamental Research Funds for the Central Universities (grant 22120190213), Shanghai Municipal Health Commission (grants 2019LJ21 and SHSLCZDZK03502), and Science and Technology Commission of Shanghai Municipality (grants 19441903200 and 19DZ2251100). Drs Zhu and Li contributed equally to this work

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Abstract

Objectives

The purpose of this study was to establish a scoring system for predicting axillary lymph node metastasis (ALNM) in patients with breast invasive ductal carcinoma with negative axillary ultrasound (US) results.

Methods

In this retrospective study, 156 breast invasive ductal carcinoma lesions from 156 women were retrospectively enrolled. The features of conventional US and contrast-enhanced ultrasound (CEUS) qualitative enhancement patterns and quantitative enhancement parameters were analyzed. Subsequently, a scoring system was created by a multivariate logistic regression analysis.

Results

The results found that 60 patients (38%) showed ALNM. A scoring system was defined as risk score = 1.75 × (if lesion size ≥20 mm) + 1.93 × (if uncircumscribed margin shown on conventional US) + 1.77 × (if coarse or twisting penetrating vessels shown on CEUS). When the risk scores were less than 1.75, 1.75 to 1.93, 1.94 to 3.70, and 3.70 or higher, the risk rates of ALNM were 0% (0 of 9), 10.7% (5 of 46), 29.2% (14 of 48) and 77.4% (41 of 53), respectively. In comparison with conventional US alone, the scoring system using the combination of conventional US and CEUS showed better discrimination ability in terms of the area under the curve (0.830 versus 0.777; P = .037).

Conclusions

A scoring system based on conventional US and CEUS may improve the prediction of ALNM.

References

1Sridharan A, Eisenbrey JR, Dave JK, Forsberg F. Quantitative nonlinear contrast-enhanced ultrasound of the breast. AJR Am J Roentgenol 2016; 207: 274–281.
10.2214/AJR.16.16315
PubMed Web of Science® Google Scholar
2Dieci MV, Orvieto E, Dominici M, Conte P, Guarneri V. Rare breast cancer subtypes: histological, molecular, and clinical peculiarities. Oncologist 2014; 19: 805–813.
10.1634/theoncologist.2014-0108
PubMed Web of Science® Google Scholar
3Esen G, Gurses B, Yilmaz MH, et al. Gray scale and power Doppler US in the preoperative evaluation of axillary metastases in breast cancer patients with no palpable lymph nodes. Eur Radiol 2005; 15: 1215–1223.
10.1007/s00330-004-2605-9
PubMed Web of Science® Google Scholar
4Duraker N, Caynak ZC. Axillary lymph node status and prognosis in multifocal and multicentric breast carcinoma. Breast J 2014; 20: 61–68.
10.1111/tbj.12205
CAS PubMed Web of Science® Google Scholar
5Burkett BJ, Hanemann CW. A review of supplemental screening ultrasound for breast cancer: certain populations of women with dense breast tissue may benefit. Acad Radiol 2016; 23: 1604–1609.
10.1016/j.acra.2016.05.017
PubMed Web of Science® Google Scholar
6Guo Q, Dong Z, Zhang L, et al. Ultrasound features of breast cancer for predicting axillary lymph node metastasis. J Ultrasound Med 2018; 37: 1353–1354.
10.1002/jum.14469
Web of Science® Google Scholar
7Yu X, Hao X, Wan J, Wang Y, Yu L, Liu B. Correlation between ultrasound appearance of small breast cancer and axillary lymph node metastasis. Ultrasound Med Biol 2018; 44: 342–349.
10.1016/j.ultrasmedbio.2017.09.020
PubMed Web of Science® Google Scholar
8Yilmaz R, Demir AA, Kaplan A, et al. Magnetic resonance imaging features of idiopathic granulomatous mastitis: is there any contribution of diffusion-weighted imaging in the differential diagnosis? Radiol Med 2016; 121: 857–866.
10.1007/s11547-016-0666-x
PubMed Web of Science® Google Scholar
9Claudon M, Dietrich CF, Choi BI, et al. Guidelines and good clinical practice recommendations for contrast enhanced ultrasound (CEUS) in the liver—update 2012: a WFUMB-EFSUMB initiative in cooperation with representatives of AFSUMB, AIUM, ASUM, FLAUS and ICUS. Ultrasound Med Biol 2013; 39: 187–210.
10.1016/j.ultrasmedbio.2012.09.002
PubMed Web of Science® Google Scholar
10Moon WK, Im JG, Noh DY, Han MC. Nonpalpable breast lesions: evaluation with power Doppler US and a microbubble contrast agent—initial experience. Radiology 2000; 217: 240–246.
10.1148/radiology.217.1.r00oc03240
CAS PubMed Web of Science® Google Scholar
11Wan CF, Du J, Fang H, Li FH, Zhu JS, Liu Q. Enhancement patterns and parameters of breast cancers at contrast-enhanced US: correlation with prognostic factors. Radiology 2012; 262: 450–459.
10.1148/radiol.11110789
PubMed Web of Science® Google Scholar
12Wang Z, Zhou Q, Liu J, et al. Tumor size of breast invasive ductal cancer measured with contrast-enhanced ultrasound predicts regional lymph node metastasis and N stage. Int J Clin Exp Pathol 2014; 7: 6985–6991.
PubMed Web of Science® Google Scholar
13Zhao H, Xu R, Ouyang Q, Chen L, Dong B, Huihua Y. Contrast-enhanced ultrasound is helpful in the differentiation of malignant and benign breast lesions. Eur J Radiol 2010; 73: 288–293.
10.1016/j.ejrad.2009.05.043
PubMed Web of Science® Google Scholar
14Ji CL, Li XL, He YP, Li DD, Gu XG, Xu HX. Quantitative parameters of contrast-enhanced ultrasound in breast invasive ductal carcinoma: the correlation with pathological prognostic factors. Clin Hemorheol Microcirc 2017; 66: 333–345.
10.3233/CH-170251
PubMed Web of Science® Google Scholar
15Sidhu PS, Cantisani V, Dietrich CF, et al. The EFSUMB guidelines and recommendations for the clinical practice of contrast-enhanced ultrasound (CEUS) in non-hepatic applications: update 2017 (long version). Ultraschall Med 2018; 39: e2–e44.
10.1055/a-0586-1107
PubMed Web of Science® Google Scholar
16 American College of Radiology. Breast Imaging Reporting and Data System. Reston, VA: American College of Radiology; 2013.
Google Scholar
17Kim WH, Kim HJ, Lee SM, et al. Preoperative axillary nodal staging with ultrasound and magnetic resonance imaging: predictive values of quantitative and semantic features. Br J Radiol 2018; 91:20180507.
10.1259/bjr.20180507
PubMed Web of Science® Google Scholar
18 American College of Radiology. Breast Imaging Reporting and Data System (BI-RADS). 4th ed. Reston, VA: American College of Radiology; 2003.
Google Scholar
19Li XL, Xu HX, Li DD, et al. A risk model based on ultrasound, ultrasound elastography, and histologic parameters for predicting axillary lymph node metastasis in breast invasive ductal carcinoma. Sci Rep 2017; 7: 3029.
10.1038/s41598-017-03582-3
PubMed Web of Science® Google Scholar
20DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 1988; 44: 837–845.
10.2307/2531595
CAS PubMed Web of Science® Google Scholar
21Cools-Lartigue J, Meterissian S. Accuracy of axillary ultrasound in the diagnosis of nodal metastasis in invasive breast cancer: a review. World J Surg 2012; 36: 46–54.
10.1007/s00268-011-1319-9
PubMed Web of Science® Google Scholar
22Alvarez S, Añorbe E, Alcorta P, López F, Alonso I, Cortés J. Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. AJR Am J Roentgenol 2006; 186: 1342–1348.
10.2214/AJR.05.0936
PubMed Web of Science® Google Scholar
23Choi YJ, Ko EY, Han BK, Shin JH, Kang SS, Hahn SY. High-resolution ultrasonographic features of axillary lymph node metastasis in patients with breast cancer. Breast 2009; 18: 119–122.
10.1016/j.breast.2009.02.004
PubMed Web of Science® Google Scholar
24Hong AS, Rosen EL, Soo MS, Baker JA. BI-RADS for sonography: positive and negative predictive values of sonographic features. AJR Am J Roentgenol 2005; 184: 1260–1265.
10.2214/ajr.184.4.01841260
PubMed Web of Science® Google Scholar
25Li Z, Ren M, Tian J, et al. The differences in ultrasound and clinicopathological features between basal-like and normal-like subtypes of triple negative breast cancer. PLoS One 2015; 10:e0114820.
10.1371/journal.pone.0114820
PubMed Web of Science® Google Scholar
26Malladi S, Macalinao DG, Jin X, et al. Metastatic latency and immune evasion through autocrine inhibition of WNT. Cell 2016; 165: 45–60.
10.1016/j.cell.2016.02.025
CAS PubMed Web of Science® Google Scholar
27Cao XL, Bao W, Zhu SG, et al. Contrast-enhanced ultrasound characteristics of breast cancer: correlation with prognostic factors. Ultrasound Med Biol 2014; 40: 11–17.
10.1016/j.ultrasmedbio.2013.08.014
PubMed Web of Science® Google Scholar
28Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med 1995; 1: 27–31.
10.1038/nm0195-27
CAS PubMed Web of Science® Google Scholar
29Weidner N, Folkman J, Pozza F, et al. Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. J Natl Cancer Inst 1992; 84: 1875–1887.
10.1093/jnci/84.24.1875
CAS PubMed Web of Science® Google Scholar

Citing Literature

Volume39, Issue10

October 2020

Pages 2059-2070

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Contrast-Enhanced Ultrasound

Predicting Axillary Lymph Node Metastasis in Patients With Breast Invasive Ductal Carcinoma With Negative Axillary Ultrasound Results Using Conventional Ultrasound and Contrast-Enhanced Ultrasound

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Predicting Axillary Lymph Node Metastasis in Patients With Breast Invasive Ductal Carcinoma With Negative Axillary Ultrasound Results Using Conventional Ultrasound and Contrast-Enhanced Ultrasound

Abstract

Objectives

Methods

Results

Conclusions

References

Citing Literature

References

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