Predictive value of comb-push ultrasound shear elastography for the differentiation of reactive and metastatic axillary lymph nodes: A preliminary investigation

Autoři: Adriana Gregory aff001;  Max Denis aff001;  Mahdi Bayat aff002;  Viksit Kumar aff002;  Bae Hyung Kim aff002;  Jeremy Webb aff001;  Rohit Nayak aff001;  Saba Adabi aff001;  Duane D. Meixner aff001;  Eric C. Polley aff003;  Robert T. Fazzio aff001;  Mostafa Fatemi aff002;  Azra Alizad aff001
Působiště autorů: Department of Radiology, Mayo Clinic College of Medicine, Rochester, Minnesota, United States of America aff001;  Department of Physiology and Biomedical Engineering, Mayo Clinic College of Medicine,Rochester, Minnesota, United States of America aff002;  Biomedical Statistics and Informatics, Mayo Clinic College of Medicine, Rochester, Minnesota, United States of America aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article



To evaluate the predictive performance of comb-push ultrasound shear elastography for the differentiation of reactive and metastatic axillary lymph nodes.


From June 2014 through September 2018, 114 female volunteers (mean age 58.1±13.3 years; range 28–88 years) with enlarged axillary lymph nodes identified by palpation or clinical imaging were prospectively enrolled in the study. Mean, standard deviation and maximum shear wave elastography parameters from 117 lymph nodes were obtained and compared to fine needle aspiration biopsy results. Mann-Whitney U test and ROC curve analysis were performed.


The axillary lymph nodes were classified as reactive or metastatic based on the fine needle aspiration outcomes. A statistically significant difference between reactive and metastatic axillary lymph nodes was observed based on comb-push ultrasound shear elastography (CUSE) results (p<0.0001) from mean and maximum elasticity values. Mean elasticity showed the best separation with a ROC analysis resulting in 90.5% sensitivity, 94.4% specificity, 0.97 area under the curve, 95% positive predictive value, and 89.5% negative predictive value with a 30.2-kPa threshold.


CUSE provided a quantifiable parameter that can be used for the assessment of enlarged axillary lymph nodes to differentiate between reactive and metastatic processes.

Klíčová slova:

Biopsy – Breast cancer – Cancer detection and diagnosis – Collagens – Lymph nodes – Magnetic resonance imaging – Metastasis – Ultrasound imaging


1. Alkuwari E, Auger M. Accuracy of fine‐needle aspiration cytology of axillary lymph nodes in breast cancer patients. Cancer Cytopathology. 2008;114(2):89–93. doi: 10.1002/cncr.23344 18286535

2. Koelliker SL, Chung MA, Mainiero MB, Steinhoff MM, Cady B. Axillary lymph nodes: US-guided fine-needle aspiration for initial staging of breast cancer—correlation with primary tumor size. Radiology. 2008;246(1):81–9. doi: 10.1148/radiol.2463061463 17991784

3. Lyman GH, Temin S, Edge SB, Newman LA, Turner RR, Weaver DL, et al. Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update. Journal of Clinical Oncology. 2014;32(13):1365–83. doi: 10.1200/JCO.2013.54.1177 24663048

4. Tanis PJ, Nieweg OE, Olmos RAV, Kroon BB. Anatomy and physiology of lymphatic drainage of the breast from the perspective of sentinel node biopsy1. Journal of the American College of Surgeons. 2001;192(3):399–409. doi: 10.1016/s1072-7515(00)00776-6 11245383

5. Bedi DG, Krishnamurthy R, Krishnamurthy S, Edeiken BS, Le-Petross H, Fornage BD, et al. Cortical Morphologic Features of Axillary Lymph Nodes as a Predictor of Metastasis in Breast Cancer: In Vitro Sonographic Study. American Journal of Roentgenology. 2008;191(3):646–52. doi: 10.2214/AJR.07.2460 18716089

6. Alvarez 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. American Journal of Roentgenology. 2006;186(5):1342–8. doi: 10.2214/AJR.05.0936 16632729

7. Fein DA, Fowble BL, Hanlon AL, Hooks MA, Hoffman JP, Sigurdson ER, et al. Identification of women with T1‐T2 breast cancer at low risk of positive axillary nodes. Journal of surgical oncology. 1997;65(1):34–9. doi: 10.1002/(sici)1096-9098(199705)65:1<34::aid-jso7>;2-p 9179265

8. McGee JM, Youmans R, Clingan F, Malnar K, Bellefeuille C, Berry B. The value of axillary dissection in T1a breast cancer. The American journal of surgery. 1996;172(5):501–5. doi: 10.1016/s0002-9610(96)00228-0 8942553

9. Carter CL, Allen C, Henson DE. Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer. 1989;63(1):181–7. doi: 10.1002/1097-0142(19890101)63:1<181::aid-cncr2820630129>;2-h 2910416

10. Harlow S, Krag D, Weaver D, Ashikaga T. Extra-axillary sentinel lymph nodes in breast cancer. Breast Cancer. 1999;6(2):159. doi: 10.1007/bf02966925 11091709

11. Carlson GW, Wood WC. Management of axillary lymph node metastasis in breast cancer: making progress. Jama. 2011;305(6):606–7. doi: 10.1001/jama.2011.131 21304087

12. Chen S, Lin X, Chen X, Zheng B. Noninvasive Evaluation of Benign and Malignant Superficial Lymph Nodes by Virtual Touch Tissue Quantification. Journal of Ultrasound in Medicine. 2016;35(3):571–5. doi: 10.7863/ultra.15.05053 26921088

13. Tourasse C, Dénier JF, Awada A, Gratadour A-C, Nessah-Bousquet K, Gay J. Elastography in the assessment of sentinel lymph nodes prior to dissection. European journal of radiology. 2012;81(11):3154–9. doi: 10.1016/j.ejrad.2012.04.031 22656671

14. Tan S, Miao LY, Cui LG, Sun PF, Qian LX. Value of Shear Wave Elastography Versus Contrast‐Enhanced Sonography for Differentiating Benign and Malignant Superficial Lymphadenopathy Unexplained by Conventional Sonography. Journal of Ultrasound in Medicine. 2017;36(1):189–99. doi: 10.7863/ultra.16.01014 27925679

15. Tamaki K, Tamaki N, Kamada Y, Uehara K, Miyashita M, Chan MS, et al. Non-invasive evaluation of axillary lymph node status in breast cancer patients using shear wave elastography. The Tohoku journal of experimental medicine. 2013;231(3):211–6. doi: 10.1620/tjem.231.211 24213140

16. Kilic F, Velidedeoglu M, Ozturk T, Kandemirli SG, Dikici AS, Er ME, et al. Ex vivo assessment of sentinel lymph nodes in breast cancer using shear wave elastography. Journal of Ultrasound in Medicine. 2016;35(2):271–7. doi: 10.7863/ultra.15.03039 26715659

17. Evans A, Rauchhaus P, Whelehan P, Thomson K, Purdie CA, Jordan LB, et al. Does shear wave ultrasound independently predict axillary lymph node metastasis in women with invasive breast cancer? Breast cancer research and treatment. 2014;143(1):153–7. doi: 10.1007/s10549-013-2747-z 24305976

18. Alam F, Islam MM, Shirin M, Shawkat S, Al Azad S, Karim E. Characterization of Axillary Lymph Nodes as Normal, Reactive and Benign Using Conventional Ultrasonography. Journal of Science Foundation. 2015;13(2):36–45.

19. Bazemore AW, Smucker DR. Lymphadenopathy and malignancy. American family physician. 2002;66(11):2103–10. 12484692

20. Rizwan A, Bulte C, Kalaichelvan A, Cheng M, Krishnamachary B, Bhujwalla ZM, et al. Metastatic breast cancer cells in lymph nodes increase nodal collagen density. Scientific reports. 2015;5:10002. doi: 10.1038/srep10002 25950608

21. Kwansa AL, De Vita R, Freeman JW. Tensile mechanical properties of collagen type I and its enzymatic crosslinks. Biophysical chemistry. 2016;214:1–10. doi: 10.1016/j.bpc.2016.04.001 27160969

22. Bercoff J, Tanter M, Fink M. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE transactions on ultrasonics, ferroelectrics, and frequency control. 2004;51(4):396–409. doi: 10.1109/tuffc.2004.1295425 15139541

23. Nightingale K, McAleavey S, Trahey G. Shear-wave generation using acoustic radiation force: in vivo and ex vivo results. Ultrasound in medicine & biology. 2003;29(12):1715–23.

24. Sarvazyan AP, Rudenko OV, Swanson SD, Fowlkes JB, Emelianov SY. Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. Ultrasound in medicine & biology. 1998;24(9):1419–35.

25. Song P, Zhao H, Manduca A, Urban MW, Greenleaf JF, Chen S. Comb-push ultrasound shear elastography (CUSE): a novel method for two-dimensional shear elasticity imaging of soft tissues. IEEE transactions on medical imaging. 2012;31(9):1821–32. doi: 10.1109/TMI.2012.2205586 22736690

26. Youk JH, Son EJ, Kim J-A, Gweon HM. Pre-operative evaluation of axillary lymph node status in patients with suspected breast cancer using shear wave elastography. Ultrasound in medicine & biology. 2017;43(8):1581–6.

27. Chen S, Lin X, Chen X, Zheng B. Noninvasive evaluation of benign and malignant superficial lymph nodes by virtual touch tissue quantification: a pilot study. Journal of Ultrasound in Medicine. 2016;35(3):571–5. doi: 10.7863/ultra.15.05053 26921088

28. Rautiainen S, Masarwah A, Sudah M, Sutela A, Pelkonen O, Joukainen S, et al. Axillary lymph node biopsy in newly diagnosed invasive breast cancer: comparative accuracy of fine-needle aspiration biopsy versus core-needle biopsy. Radiology. 2013;269(1):54–60. doi: 10.1148/radiol.13122637 23771915

29. Alkuwari E, Auger M. Accuracy of fine‐needle aspiration cytology of axillary lymph nodes in breast cancer patients: a study of 115 cases with cytologic‐histologic correlation. Cancer Cytopathology: Interdisciplinary International Journal of the American Cancer Society. 2008;114(2):89–93.

30. Ciatto S, Brancato B, Risso G, Ambrogetti D, Bulgaresi P, Maddau C, et al. Accuracy of fine needle aspiration cytology (FNAC) of axillary lymph nodes as a triage test in breast cancer staging. Breast cancer research and treatment. 2007;103(1):85–91. doi: 10.1007/s10549-006-9355-0 17033920

31. Rocha RD, Girardi AR, Pinto RR, Freitas VARd. Axillary ultrasound and fine-needle aspiration in preoperative staging of axillary lymph nodes in patients with invasive breast cancer. Radiologia brasileira. 2015;48(6):345–52. doi: 10.1590/0100-3984.2014.0121 26811550

32. Aristizabal S, Amador C, Qiang B, Kinnick RR, Nenadic IZ, Greenleaf JF, et al. Shear wave vibrometry evaluation in transverse isotropic tissue mimicking phantoms and skeletal muscle. Physics in Medicine & Biology. 2014;59(24):7735.

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