Skip to main content

Lymph Node Staging with US (and FNA)

  • Chapter
  • First Online:
Lobar Approach to Breast Ultrasound

Abstract

Preoperative knowledge of regional lymph node status (N staging) is essential before planning a treatment for breast cancer. US is able to detect metastases smaller than 5 mm and to guide sampling, including for the internal mammary chain, without risk.

There is new evidence that in the absence of metastatic disease on US examination and US-guided fine-needle aspiration cytology (FNAC), axillary sentinel lymph node (surgical) biopsy (SLNB) and even axillary lymph node dissection (ALND) would be unnecessary because both are rarely positive for heavy metastatic burden, and therefore treatment options will not change.

Promoting this way of workup for patients with breast cancer would be beneficial for the patients, as compared to other imaging techniques and surgical procedures, in terms of irradiation, time to diagnosis, and treatment. Last but not least, the cheap US-guided FNAC is cost-effective, both for developing countries having restricted access to high-level technologies, such as MRI, PET/CT, and SLNB, and in First World countries which are faced with a permanent increase in health expenditure.

This chapter offers a current review of the methods for nodal staging assessment in breast cancer patients and underlines new frontiers for evaluation of small superficial lymph nodes with ultrasound such as the “avascularity” of a micrometastasis in the nodal cortex. The impact of intramammary nodes and internal (parasternal) mammary nodes are particularly discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Institutional subscriptions

Abbreviations

ALND:

Axillary lymph node (surgical) dissection

AUS:

Axillary ultrasound

FNA:

Fine-Needle Aspiration

LN:

Lymph node

SN:

Sentinel node

NPV:

Negative predictive value

PPV:

Positive predictive value

SLNB:

Sentinel lymph node (surgical) biopsy

US:

Ultrasound

US-FNAB:

US-guided fine-needle aspiration biopsy (with core biopsy needle)

US-FNAC:

US-guided fine-needle aspiration cytology

References

  1. Nemoto T, Natarajan N, Bedwani R, Vana J, Murphy GP. Breast cancer in the medial half. Results of 1978 National Survey of the American College of Surgeons. Cancer. 1983;51(8):1333–8.

    Article  PubMed  CAS  Google Scholar 

  2. Saez RA, McGuire WL, Clark GM. Prognostic factors in breast cancer. Semin Surg Oncol. 1989;5(2):102–10. Review

    Article  PubMed  CAS  Google Scholar 

  3. Colzani E, Liljegren A, Johansson AL, Adolfsson J, Hellborg H, Hall PF, Czene K. Prognosis of patients with breast cancer: causes of death and effects of time since diagnosis, age, and tumor characteristics. J Clin Oncol. 2011;29:4014–21.

    Article  PubMed  Google Scholar 

  4. de Boer M, van Dijck JA, Bult P, Borm GF, Tjan-Heijnen VC. Breast cancer prognosis and occult lymph node metastases, isolated tumor cells, and micrometastases. J Natl Cancer Inst. 2010;102:410–25.

    Article  PubMed  Google Scholar 

  5. Fisher B, Bauer M, Wickerham DL, Redmond CK, Fisher ER, Cruz AB, Foster R, Gardner B, Lerner H, Margolese R, et al. Relation of number of positive axillary nodes to the prognosis of patients with primary breast cancer. An NSABP update. Cancer. 1983;52(9):1551–7.

    Article  PubMed  CAS  Google Scholar 

  6. Allemani C, Weir HK, Carreira H, Harewood R, Spika D, Wang XS et al.; CONCORD Working Group. Global surveillance of cancer survival 1995–2009: analysis of individual data for 25,676,887 patients from 279 population-based registries in 67 countries (CONCORD-2). Lancet. 2015;385(9972):977–1010.

    Google Scholar 

  7. Saadatmand S, Bretveld R, Siesling S. Tilanus-Linthorst. Influence of tumour stage at breast cancer detection on survival in modern times: population based study in 173,797 patients. BMJ. 2015;351:h4901.

    Google Scholar 

  8. Ojeda-Fournier H, Nguyen JQ. Ultrasound evaluation of regional breast lymph node. Semin Roentgenol. 2011;46(1):51–9.

    Article  PubMed  Google Scholar 

  9. Baruah BP, Goyal A, Young P, Douglas-Jones AG, Mansel RE. Axillary node staging by ultrasonography and fine-needle aspiration cytology in patients with breast cancer. Br J Surg. 2010;97(5):680–3.

    Article  PubMed  CAS  Google Scholar 

  10. Deurloo EE, Tanis PJ, Gilhuijs KG, Muller SH, Kröger R, Peterse JL, Rutgers EJ, Valdés Olmos R, Schultze Kool LJ. Reduction in the number of sentinel lymph node procedures by preoperative ultrasonography of the axilla in breast cancer. Eur J Cancer. 2003;39:1068–73.

    Article  PubMed  CAS  Google Scholar 

  11. Diaz-Ruiz MJ, Arnau A, Montesinos J, Miguel A, Culell P, Solernou L, Tortajada L, Vergara C, Yanguas C, Salvador-Tarrasón R. Diagnostic accuracy and impact on management of ultrasonography-guided fine-needle aspiration to detect axillary metastasis in breast cancer patients: a prospective study. Breast Care (Basel). 2016;11(1):34–9.

    Article  PubMed  Google Scholar 

  12. Huber D, Duc C, Schneider N, Fournier D. Ultrasound-guided fine needle aspiration cytology in staging clinically node-negative invasive breast cancer. Gynecol Surg. 2012;9:185.

    Article  Google Scholar 

  13. Francissen CMTP, Dings PJM, van Dalen T, Strobbe LJA, van Laarhoven HWM, de Wilt JHW. Axillary recurrence after a tumor-positive sentinel lymph node biopsy without axillary treatment: a review of the literature. Ann Surg Oncol. 2012;19(13):4140–9.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, McCall LM, Morrow M. Axillary dissection vs. no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011;305:569–75.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Maaskant-Braat AJ, van de Poll-Franse LV, Voogd AC, Coebergh JW, Roumen RM, Nolthenius-Puylaert MC, Nieuwenhuijzen GA. Sentinel node micrometastases in breast cancer do not affect prognosis: a population-based study. Breast Cancer Res Treat. 2011;127(1):195–203.

    Article  PubMed  Google Scholar 

  16. Tallet A, Lambaudie E, Cohen M, Minsat M, Bannier M, Resbeut M, Houvenaeghel G. Locoregional treatment of early breast cancer with isolated tumor cells or micrometastases on sentinel lymph node biopsy. World J Clin Oncol. 2016;7(2):243–52.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Blum A, Schlagenhauff B, Stroebel W, Breuninger H, Rassner G, Garbe C. Ultrasound examination of regional lymph nodes significantly improves early detection of locoregional metastases during the follow-up of patients with cutaneous disease: result of a prospective study of 1288 patients. Cancer. 2000;88(11):2534–9.

    Article  PubMed  CAS  Google Scholar 

  18. Tregnaghi A, De Candia A, Calderone M, Cellini L, Rossi CR, Talenti E, Blandamura S, Borsato S, Muzzio PC, Rubaltelli L. Ultrasonographic evaluation of superficial lymph node metastases in melanoma. Eur J Radiol. 1996;24(3):216–21.

    Article  Google Scholar 

  19. Voit C, Mayer T, Kron M, Schoengen A, Sterry W, Weber L, Proebstle TM. Efficacy of ultrasound B-scan compared with physical examination in follow-up of melanoma patients. Cancer. 2001;91(12):2409–16.

    Article  PubMed  CAS  Google Scholar 

  20. Mandava A, Ravuri PR, Konathan R. High-resolution ultrasound imaging of cutaneous lesions. Indian J Radiol Imaging. 2013;23(3):269–77.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Dudea SM, Lenghel M, Botar-Jid C, Vasilescu D, Duma M. Ultrasonography of superficial lymph nodes: benign vs. malignant. Med Ultrason. 2012;14(4):294–306.

    PubMed  Google Scholar 

  22. Kristo B, Krišto B, Buljan M. The lymph node roundness index in the evaluation of lymph nodes of the neck. Coll Antropol. 2015;39(1):165–9.

    PubMed  CAS  Google Scholar 

  23. Hillen F, Griffioen AW. Tumour vascularization: sprouting angiogenesis and beyond. Cancer Metastasis Rev. 2007;26(3–4):489–502. Review

    Article  PubMed  PubMed Central  Google Scholar 

  24. Chiorean L, Barr RG, Braden B, Jenssen C, Cui XW, Hocke M, Schuler A, Dietrich CF. Transcutaneous ultrasound: elastographic lymph node evaluation. current clinical applications and literature review. Ultrasound Med Biol. 2016;42(1):16–30.

    Article  PubMed  Google Scholar 

  25. Kilic F, Velidedeoglu M, Ozturk T, Kandemirli SG, Dikici AS, Er ME, Aydogan F, Kantarci F, Yilmaz MH. Ex vivo assessment of sentinel lymph nodes in breast cancer using shear wave elastography. J Ultrasound Med. 2016;35(2):271–7.

    Article  PubMed  Google Scholar 

  26. Wojcinski S, Dupont J, Schmidt W, Cassel M, Hillemanns P. Real-time ultrasound elastography in 180 axillary lymph nodes: elasticity distribution in healthy lymph nodes and prediction of breast cancer metastases. BMC Med Imaging. 2012;12:35.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Gkretsi V, Stylianou A, Papageorgis P, Polydorou C. Stylianopoulos T. Remodeling components of the tumor microenvironment to enhance cancer therapy. Front Oncol. 2015;5:214.

    Google Scholar 

  28. Ran S, Volk L, Hall K, Flister MJ. Lymphangiogenesis and lymphatic metastasis in breast cancer. Pathophysiology. 2010;17(4):229–51.

    Article  PubMed  Google Scholar 

  29. Suami H, Pan WR, Mann GB, Taylor GI. The lymphatic anatomy of the breast and its implications for sentinel lymph node biopsy: a human cadaver study. Ann Surg Oncol. 2008;15(3):863–71.

    Article  PubMed  Google Scholar 

  30. Manca G, Volterrani D, Mazzarri S, Duce V, Svirydenka A, Giuliano A, Mariani G. Sentinel lymph node mapping in breast cancer: a critical reappraisal of the internal mammary chain issue. Q J Nucl Med Mol Imaging. 2014;58(2):114–26.

    PubMed  CAS  Google Scholar 

  31. Tanis PJ, Nieweg OE, Valdés Olmos RA, Peterse JL, Rutgers EJ, Hoefnagel CA, Kroon BB. Impact of non-axillary sentinel node biopsy on staging and treatment of breast cancer patients. Br J Cancer. 2002;87(7):705–10.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Liu Y. Role of FDG PET-CT in evaluation of locoregional nodal disease for initial staging of breast cancer. World J Clin Oncol. 2014;5(5):982–9.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Robertson IJ, Hand F, Kell MR. FDG-PET/CT in the staging of local/regional metastases in breast cancer. Breast. 2011;20(6):491–4.

    Article  PubMed  Google Scholar 

  34. Hong J, Choy E, Soni N, Carmalt H, Gillett D, Spillane AJ. Extra-axillary sentinel node biopsy in the management of early breast cancer. Eur J Surg Oncol. 2005;31(9):942–8.

    Article  PubMed  CAS  Google Scholar 

  35. Baltzer PA, Dietzel M, Burmeister HP, Zoubi R, Gajda M, Camara O, Kaiser WA. Application of MR mammography beyond local staging: is there a potential to accurately assess axillary lymph nodes? Evaluation of an extended protocol in an initial prospective study. AJR Am J Roentgenol. 2011;196(5):W641–7.

    Article  PubMed  Google Scholar 

  36. Tran A, Pio BS, Khatibi B, Czernin J, Phelps ME, Silverman DH. 18F-FDG PET for staging breast cancer in patients with inner-quadrant versus outer-quadrant tumors: comparison with long-term clinical outcome. J Nucl Med. 2005;46(9):1455–9.

    PubMed  Google Scholar 

  37. Krause A, Dunkelmann S, Makovitzky J, Küchenmeister I, Schümichen C, Reimer T, Friese K, Gerber B. Detection of atypical site of "sentinel lymph nodes" by lymph drainage scintigraphy in patients with breast carcinoma. Zentralbl Gynakol. 2000;122(10):514–8.

    Article  PubMed  CAS  Google Scholar 

  38. Altinyollar H, Dingil G, Berberoglu U. Detection of infraclavicular lymph node metastases using ultrasonography in breast cancer. J Surg Oncol. 2005;92(4):299–303.

    Article  PubMed  Google Scholar 

  39. van Rijk MC, Tanis PJ, Nieweg OE, Olmos RA, Rutgers EJ, Hoefnagel CA, Kroon BB. Clinical implications of sentinel nodes outside the axilla and internal mammary chain in patients with breast cancer. J Surg Oncol. 2006;94(4):281–6.

    Article  PubMed  Google Scholar 

  40. Stachs A, Göde K, Hartmann S, Stengel B, Nierling U, Dieterich M, Reimer T, Gerber B. Accuracy of axillary ultrasound in preoperative nodal staging of breast cancer—size of metastases as limiting factor. Spring. 2013;2:350.

    Article  Google Scholar 

  41. Khout H, Richardson C, Toghyan H, Fasih T. The role of combined assessment in preoperative axillary staging. Ochsner J. 2013;13(4):489–94.

    PubMed  PubMed Central  Google Scholar 

  42. Gipponi M, Fregatti P, Garlaschi A, Murelli F, Margarino C, Depaoli F, Baccini P, Gallo M, Friedman D. Axillary ultrasound and fine-needle aspiration cytology in the preoperative staging of axillary node metastasis in breast cancer patients. Breast. 2016;30:146–50.

    Article  PubMed  Google Scholar 

  43. Feng Y, Huang R, He Y, Lu A, Fan Z, Fan T, Qi M, Wang X, Cao W, Wang X, Xie Y, Wang T, Li J, Ouyang T. Efficacy of physical examination, ultrasound, and ultrasound combined with fine-needle aspiration for axilla staging of primary breast cancer. Breast Cancer Res Treat. 2015;149(3):761–5.

    Article  PubMed  Google Scholar 

  44. Pamilo M, Soiva M, Lavast EM. Real-time ultrasound, axillary mammography, and clinical examination in the detection of axillary lymph node metastases in breast cancer patients. J Ultrasound Med. 1989;8(3):115–20.

    Article  PubMed  CAS  Google Scholar 

  45. Usmani S, Ahmed N, Al Saleh N, abu Huda F, Amanguno HG, Amir T, al Kandari F. The clinical utility of combining pre-operative axillary ultrasonography and fine needle aspiration cytology with radionuclide guided sentinel lymph node biopsy in breast cancer patients with palpable axillary lymph nodes. Eur J Radiol. 2015;84(12):2515–20.

    Article  PubMed  Google Scholar 

  46. Specht MC, Fey JV, Borgen PI, Cody HS 3rd. Is the clinically positive axilla in breast cancer really a contraindication to sentinel lymph node biopsy? J Am Coll Surg. 2005;200(1):10–4.

    Article  PubMed  Google Scholar 

  47. Dialani V, James DF, Slanetz PJ. A practical approach to imaging the axilla. Insights Imaging. 2015;6(2):217–29.

    Article  PubMed  CAS  Google Scholar 

  48. Ecanow JS, Abe H, Newstead GM, Ecanow DB, Jeske JM. Axillary staging of breast cancer: what the radiologist should know. Radiographics. 2013;33(6):1589–612.

    Article  PubMed  Google Scholar 

  49. Wu PQ, Liu CL, Liu ZY, Ye WT, Liang CH. Value of mamography, CT and DCE-MRI in detecting axillary lymph node metastasis of breast cancer. Nan Fang Yi Ke Da Xue Xue Bao. 2016;36(4):493–9.

    PubMed  Google Scholar 

  50. Walsh R, Kornguth PJ, Soo MS, Bentley R, DeLong DM. Axillary lymph nodes: mammographic, pathologic, and clinical correlation. AJR Am J Roentgenol. 1997;168(1):33–8.

    Article  PubMed  CAS  Google Scholar 

  51. Lee CH, Giurescu ME, Philpotts LE, Horvath LJ, Tocino I. Clinical importance of unilaterally enlarging lymph nodes on otherwise normal mammograms. Radiology. 1997;203(2):329–34.

    Article  PubMed  CAS  Google Scholar 

  52. Valente SA, Levine GM, Silverstein MJ, Rayhanabad JA, Weng-Grumley JG, Ji L, Holmes DR, Sposto R, Sener SF. Accuracy of predicting axillary lymph node positivity by physical examination, mammography, ultrasonography, and magnetic resonance imaging. Ann Surg Oncol. 2012;19(6):1825–30.

    Article  PubMed  Google Scholar 

  53. Shetty MK, Carpenter WS. Sonographic evaluation of isolated abnormal axillary lymph nodes identified on mammograms. J Ultrasound Med. 2004;23:63–71.

    Article  PubMed  Google Scholar 

  54. Murray ME, Given-Wilson RM. The clinical importance of axillary lymphadenopathy detected on screening mammography. Clin Radiol. 1997;52(6):458–61.

    Article  PubMed  CAS  Google Scholar 

  55. March DE, Wechsler RJ, Kurtz AB, Rosenberg AL, Needleman L. CT-pathologic correlation of axillary lymph nodes in breast carcinoma. J Comput Assist Tomogr. 1991;15:440–4.

    Article  PubMed  CAS  Google Scholar 

  56. Uematsu T, Sano M, Homma K. In vitro high-resolution helical CT of small axillary lymph nodes in patients with breast cancer: correlation of CT and histology. AJR Am J Roentgenol. 2001;176(4):1069–74.

    Article  PubMed  CAS  Google Scholar 

  57. Chudgar A, Clark A, Mankoff D. Applications of PET/CT in breast cancer, NCCN guidelines and beyond. J Nucl Med. 2016;57:1304.

    Google Scholar 

  58. Peare R, Staff RT, Heys SD. The use of FDG-PET in assessing axillary lymph node status in breast cancer: a systematic review and meta-analysis of the literature. Breast Cancer Res Treat. 2010;123:281–90.

    Article  PubMed  Google Scholar 

  59. Riegger C, Koeninger A, Hartung V, Otterbach F, Kimmig R, Forsting M, Bockisch A, Antoch G, Heusner TA. Comparison of the diagnostic value of FDG-PET/CT and axillary ultrasound for the detection of lymph node metastases in breast cancer patients. Acta Radiol. 2012;53(10):1092–8.

    Article  PubMed  Google Scholar 

  60. Fujii T, Yajima R, Tatsuki H, Oosone K, Kuwano H. Implication of 18F-fluorodeoxyglucose uptake of affected axillary lymph nodes in cases with breast cancer. Anticancer Res. 2016;36(1):393–7.

    PubMed  CAS  Google Scholar 

  61. Ahmed M, Purushotham AD, Douek M. Novel techniques for sentinel lymph node biopsy in breast cancer: a systematic review. Lancet Oncol. 2014;15(8):e351–62.

    Article  PubMed  Google Scholar 

  62. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220:391–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Kell MR, Burke JP, Barry M, Morrow M. Outcome of axillary staging in early breast cancer: a meta-analysis. Breast Cancer Res Treat. 2010;120:441–7.

    Article  PubMed  Google Scholar 

  64. Straver ME, Meijnen P, van Tienhoven G, van de Velde CJ, Mansel RE, Bogaerts J, Demonty G, Duez N, Cataliotti L, Klinkenbijl J, Westenberg HA, van der Mijle H, Hurkmans C, Rutgers EJ. Role of axillary clearance after a tumor-positive sentinel node in the administration of adjuvant therapy in early breast cancer. J Clin Oncol. 2010;28(5):731–7.

    Article  PubMed  Google Scholar 

  65. Veronesi U, Viale G, Paganelli G, Zurrida S, Luini A, Galimberti V, Veronesi P, Intra M, Maisonneuve P, Zucca F, Gatti G, Mazzarol G, De Cicco C, Vezzoli D. Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg. 2010;251:595–600.

    Article  PubMed  Google Scholar 

  66. Zavagno G, De Salvo G L, Scalco G. et al.; GIVOM Trialists. A randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the SENTINELLA/GIVOM trial. Ann Surg. 2008;247:207–13.

    Article  PubMed  Google Scholar 

  67. Maguire A, Brogi E. Sentinel lymph nodes for breast carcinoma: a paradigm shift. Arch Pathol Lab Med. 2016;140(8):791–8.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Husted Madsen A, Haugaard K, Soerensen J, Bokmand S, Friis E, Holtveg H, Peter Garne J, Horby J, Christiansen P. Arm morbidity following sentinel lymph node biopsy or axillary lymph node dissection: a study from the Danish Breast Cancer Cooperative Group. Breast. 2008;17(2):138–47. Epub 2007 Oct 24

    Article  PubMed  Google Scholar 

  69. Kuijs VJL, Moossdorff M, Schipper RJ, Beets-Tan RGH, Heuts EM, Keymeulen KBMI, Smidt ML, Lobbes MBI. The role of MRI in axillary lymph node imaging in breast cancer patients: a systematic review. Insights Imaging. 2015;6:203–15.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Rahman RL, Crawford SL, Siwawa P. Management of axilla in breast cancer: the saga continues. Breast. 2015;24(4):343–53.

    Article  Google Scholar 

  71. Yoshimura G, Sakurai T, Oura S, Suzuma T, Tamaki T, Umemura T, Kokawa Y, Yang Q. Evaluation of axillary lymph node status in breast cancer with MRI. Breast Cancer. 1999;6:249–58.

    Article  PubMed  CAS  Google Scholar 

  72. Kvistad KA, Rydland J, Smethurst HB, Lundgren S, Fjosne HE, Haraldseth O. Axillary lymph node metastases in breast cancer: preoperative detection with dynamic contrast-enhanced MRI. Eur Radiol. 2000;10:1464–71.

    Article  PubMed  CAS  Google Scholar 

  73. García Fernández A, Fraile M, Giménez N, Reñe A, Torras M, Canales L, Torres J, Barco I, González S, Veloso E, González C, Cirera L, Pessarrodona A. Use of axillary ultrasound, ultrasound-fine needle aspiration biopsy and magnetic resonance imaging in the preoperative triage of breast cancer patients considered for sentinel node biopsy. Ultrasound Med Biol. 2011;37:16–22.

    Article  PubMed  Google Scholar 

  74. Harnan SE, Cooper KL, Meng Y, Ward SE, Fitzgerald P, Papaioannou D, Ingram C, Lorenz E, Wilkinson ID, Wyld L. Magnetic resonance for assessment of axillary lymph node status in early breast cancer: a systematic review and meta-analysis. Eur J Surg Oncol. 2011;37(11):928–36.

    Article  PubMed  CAS  Google Scholar 

  75. Chung J, Youk JH, Kim JA, Gweon HM, Kim EK, Ryu YH, Son EJ. Role of diffusion-weighted MRI: predicting axillary lymph node metastases in breast cancer. Acta Radiol. 2014;55(8):909–16.

    Article  PubMed  Google Scholar 

  76. Yun SJ, Sohn YM, Seo M. Differentiation of benign and metastatic axillary lymph nodes in breast cancer: additive value of MRI computer-aided evaluation. Clin Radiol. 2016;71(4):403.e1–7.

    Article  CAS  Google Scholar 

  77. Arslan G, Altintoprak KM, Yirgin IK, Atasoy MM, Celik L. Diagnostic accuracy of metastatic axillary lymph nodes in breast MRI. Spring. 2016;5(1):735.

    Article  Google Scholar 

  78. Estourgie SH, Nieweg OE, Olmos RA, Rutgers EJ, Kroon BB. Lymphatic drainage patterns from the breast. Ann Surg. 2004;239(2):232–7.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Freedman GM, Fowble BL, Nicolaou N, Sigurdson ER, Torosian MH, Boraas MC, Hoffman JP. Should internal mammary lymph nodes in breast cancer be a target for the radiation oncologist? Int J Radiat Oncol Biol Phys. 2000;46(4):805–14. Review.

    Article  PubMed  CAS  Google Scholar 

  80. Veronesi U, Cascinelli N, Bufalino R, Morabito A, Greco M, Galluzzo D, Delle Donne V, De Lellis R, Piotti P, Sacchini V, et al. Risk of internal mammary lymph node metastases and its relevance on prognosis of breast cancer patients. Ann Surg. 1983;198:681–4.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Huang O, Wang L, Shen K, Lin H, Hu Z, Liu G, Wu J, Lu J, Shao Z, Han Q, Shen Z. Breast cancer subpopulation with high risk of internal mammary lymph nodes metastasis: analysis of 2,269 Chinese breast cancer patients treated with extended radical mastectomy. Breast Cancer Res Treat. 2008;107:379–87.

    Article  PubMed  Google Scholar 

  82. Ragaz J, Olivotto IA, Spinelli JJ, Phillips N, Jackson SM, Wilson KS, Knowling MA, Coppin CM, Weir L, Gelmon K, Le N, Durand R, Coldman AJ, Manji M. Locoregional radiation therapy in patients with high-risk breast cancer receiving adjuvant chemotherapy: 20-year results of the British Columbia randomized trial. J Natl Cancer Inst. 2005;97:116–26.

    Article  PubMed  Google Scholar 

  83. Colleoni M, Zahrieh D, Gelber RD, Holmberg SB, Mattsson JE, Rudenstam CM, Lindtner J, Erzen D, Snyder R, Collins J, Fey MF, Thürlimann B, Crivellari D, Murray E, Mendiola C, Pagani O, Castiglione-Gertsch M, Coates AS, Price K, Goldhirsch A. Site of primary tumor has a prognostic role in operable breast cancer: the international breast cancer study group experience. J Clin Oncol. 2005;23:1390–400.

    Article  PubMed  Google Scholar 

  84. Cody HS, Urban JA. Internal mammary node status: a major prognosticator in axillary node-negative breast cancer. Ann Surg Oncol. 1995;2:32–7.

    Article  PubMed  Google Scholar 

  85. Noguchi M, Koyasaki N, Ohta N, Kitagawa H, Earashi M, Thomas M, Miyazaki I, Mizukami Y. Internal mammary nodal status is a more reliable prognostic factor than DNA ploidy and c-erb B-2 expression in patients with breast cancer. Arch Surg. 1993;128:242–6.

    Article  PubMed  CAS  Google Scholar 

  86. Jochelson MS, Lebron L, Jacobs SS, Zheng J, Moskowitz CS, Powell SN, Sacchini V, Ulaner GA, Morris EA, Dershaw DD. Detection of internal mammary adenopathy in patients with breast cancer by PET/CT and MRI. AJR Am J Roentgenol. 2015;205(4):899–904.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Qiu PF, Liu YB, Wang YS. Internal mammary sentinel lymph node biopsy: abandon or persist? Onco Targets Ther. 2016;9:3879–82.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Scatarige JC, Boxen I, Smathers RL. Internal mammary lymphadenopathy: imaging of a vital lymphatic pathway in breast cancer. Radiographics. 1990;10(5):857–70. Review

    Article  PubMed  CAS  Google Scholar 

  89. Glass EC, Essner R, Giuliano AE. Sentinel node localization in breast cancer. Semin Nucl Med. 1999;29:57–68.

    Article  PubMed  CAS  Google Scholar 

  90. van der Ent FW, Kengen RA, Pol HA, Povel JA, Stroeken HJ, Hoofwijk AG. Halsted Revisited: Internal Mammary Sentinel Lymph Node Biopsy in Breast. Ann Surg. 2001 Jul;234(1):79–84.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Chen RC, Lin NU, Golshan M, Harris JR, Bellon JR. Internal mammary nodes in breast cancer: diagnosis and implications for patient management—a systematic review. J Clin Oncol. 2008;26(30):4981–9.

    Article  PubMed  Google Scholar 

  92. Zhang YJ, Oh JL, Whitman GJ, Iyengar P, Yu TK, Tereffe W, Woodward WA, Perkins G, Buchholz TA, Strom EA. Clinically apparent internal mammary nodal metastasis in patients with advanced breast cancer: incidence and local control. Int J Radiat Oncol Biol Phys. 2010;77:1113–9.

    Article  PubMed  Google Scholar 

  93. Wang CL, Eissa MJ, Rogers JV, Aravkin AY, Porter BA, Beatty JD. (18)F-FDG PET/CT-positive internal mammary lymph nodes: pathologic correlation by ultrasound-guided fine-needle aspiration and assessment of associated risk factors. AJR Am J Roentgenol. 2013;200(5):1138–44.

    Article  PubMed  Google Scholar 

  94. Kinoshita T, Odagiri K, Andoh K, Doiuchi T, Sugimura K, Shiotani S, Asaga T. Evaluation of small internal mammary lymph node metastases in breast cancer by MRI. Radiat Med. 1999;17:189–93.

    PubMed  CAS  Google Scholar 

  95. Cheon H, Kim HJ, Lee SW, Kim DH, Lee CH, Cho SH, Shin KM, Lee SM, Kim GC, Kim WH. Internal mammary node adenopathy on breast MRI and PET/CT for initial staging in patients with operable breast cancer: prevalence and associated factors. Breast Cancer Res Treat. 2016;160(3):523–30.

    Article  PubMed  CAS  Google Scholar 

  96. Dogan BE, Dryden MJ, Wei W, Fornage BD, Buchholz TA, Smith B, Hunt K, Krishnamurthy S, Yang WT. Sonography and sonographically guided needle biopsy of internal mammary nodes in staging of patients with breast cancer. AJR Am J Roentgenol. 2015;205(4):905–11.

    Article  PubMed  Google Scholar 

  97. Farrús B, Vidal-Sicart S, Velasco M, Zanón G, Fernández PL, Muñoz M, Santamaría G, Albanell J, Biete A. Incidence of internal mammary node metastases after a sentinel lymph node technique in breast cancer and its implication in the radiotherapy plan. Int J Radiat Oncol Biol Phys. 2004;60(3):715–21.

    Article  PubMed  Google Scholar 

  98. Gui GP, Behranwala KA, Abdullah N, Seet J, Osin P, Nerurkar A, Lakhani SR. The inframammary fold: contents, clinical significance and implications for immediate breast reconstruction. Br J Plast Surg. 2004;57(2):146–9.

    Article  PubMed  CAS  Google Scholar 

  99. Troupis T, Michalinos A, Skandalakis P. Intramammary lymph nodes: a question seeking for an answer or an answer seeking for a question? Breast. 2012;21(5):615–20.

    Article  PubMed  CAS  Google Scholar 

  100. Nassar A, Cohen C, Cotsonis G, Carlson G. Significance of intramammary lymph nodes in the staging of breast cancer: correlation with tumor characteristics and outcome. Breast J. 2008;14(2):147–52.

    Article  PubMed  Google Scholar 

  101. Abdullgaffar B, Gopal P, Abdulrahim M, Ghazi E, Mohamed E. The significance of intramammary lymph nodes in breast cancer: a systematic review and meta-analysis. Int J Surg Pathol. 2012;20(6):555–63.

    Article  PubMed  Google Scholar 

  102. Rampaul RS, Dale OT, Mitchell M, Blamey RW, Macmillan RD, Robertson JF, Ellis IO. Incidence of intramammary nodes in completion mastectomy specimens after axillary node sampling: implications for breast conserving surgery. Breast. 2008;17(2):195–8.

    Article  PubMed  CAS  Google Scholar 

  103. Günhan-Bilgen I, Memiş A, Ustün EE. Metastatic intramammary lymph nodes: mammographic and ultrasonographic features. Eur J Radiol. 2001;40(1):24–9.

    Article  PubMed  Google Scholar 

  104. Shen J, Hunt KK, Mirza NQ, Krishnamurthy S, Singletary SE, Kuerer HM, Meric-Bernstam F, Feig B, Ross MI, Ames FC, Babiera GV. Intramammary lymph node metastases are an independent predictor of poor outcome in patients with breast carcinoma. Cancer. 2004;101(6):1330–7.

    Article  PubMed  Google Scholar 

  105. Svane G, Franzén S. Radiologic appearance of nonpalpable intramammary lymph nodes. Acta Radiol. 1993;34:577–80.

    Article  PubMed  CAS  Google Scholar 

  106. Gordon PB, Gilks B. Sonographic appearance of normal intramammary lymph nodes. J Ultrasound Med. 1988;7(10):545–8.

    Article  PubMed  CAS  Google Scholar 

  107. Stomper PC, Leibowich S, Meyer JE. The prevalence and distribution of well circumscribed nodules on screening mammography: analysis of 1500 mammograms. Breast Dis. 1991;4:197–203.

    Google Scholar 

  108. Kim SJ, Ko EY, Shin JH, Kang SS, Mun SH, Han BK, Cho EY. Application of sonographic BI-RADS to synchronous breast nodules detected in patients with breast cancer. AJR Am J Roentgenol. 2008;191(3):653–8.

    Article  PubMed  Google Scholar 

  109. Edeiken-Monroe BS, Monroe DP, Monroe BJ, Arnljot K, Giaccomazza M, Sneige N, Fornage BD. Metastases to intramammary lymph nodes in patients with breast cancer: sonographic findings. J Clin Ultrasound. 2008;36:279–85.

    Article  PubMed  Google Scholar 

  110. Nogareda Z, Álvarez A, Perlaza P, Caparrós FX, Alonso I, Paredes P, Vidal-Sicart S. Presence of intramammary lymph nodes in the preoperative lymphoscintigraphy to locate the sentinel lymph node. Clinical significance. Rev Esp Med Nucl Imagen Mol. 2015;34(2):83–8.

    PubMed  CAS  Google Scholar 

  111. Mahajan A, et al. Diagnosis of a malignant intramammary node retrospectively aided by mastectomy specimen MRI-Is the search worth it? A case report and review of current literature. Korean J Radiol. 2013;14(4):576–80.

    Article  PubMed  PubMed Central  Google Scholar 

  112. Kembhavi SA, Choudhary H, Deodhar K, Thakur MH. Reactive intramammary lymph node mimicking recurrence on MRI study in a patient with prior breast conservation therapy. J Cancer Res Ther. 2013;9(1):111–3.

    Article  PubMed  Google Scholar 

  113. Vijan SS, Hamilton S, Chen B, Reynolds C, Boughey JC, Degnim AC. Intramammary lymph nodes: patterns of discovery and clinical significance. Surgery. 2009;145:495–9.

    Article  PubMed  Google Scholar 

  114. Aksoy Ozcan U, Tezcanli E, Yildirim Y, Garipagaoglu M. The great mimicker: zona zoster at the mastectomy site causing contralateral intramammary lymph node enlargement. Case Rep Oncol Med. 2012;2012:468576.

    PubMed  PubMed Central  Google Scholar 

  115. Houvenaeghel G, Tallet A, Jalaguier-Coudray A, Cohen M, Bannier M, Jauffret-Fara C, Lambaudie E. Is breast conservative surgery a reasonable option in multifocal or multicentric tumors? World J Clin Oncol. 2016;7(2):234–42.

    Article  PubMed  PubMed Central  Google Scholar 

  116. Lynch SP, Lei X, Hsu L, Meric-Bernstam F, Buchholz TA, Zhang H, Hortobágyi GN, Gonzalez-Angulo AM, Valero V. Breast cancer multifocality and multicentricity and locoregional recurrence. Oncologist. 2013;18(11):1167–73.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Bruneton JN, Caramella E, Héry M, Aubanel D, Manzino JJ, Picard JL. Axillary lymph node metastases in breast cancer: preoperative detection with US. Radiology. 1986;158(2):325–6.

    Article  PubMed  CAS  Google Scholar 

  118. Mustonen P, Farin P, Kosunen O. Ultrasonographic detection of metastatic axillary lymph nodes in breast cancer. Ann Chir Gynaecol. 1990;79(1):15–8.

    PubMed  CAS  Google Scholar 

  119. Ciatto S, Brancato B, Risso G, Ambrogetti D, Bulgaresi P, Maddau C, Turco P, Houssami N. Accuracy of fine needle aspiration cytology (FNAC) of axillary lymph nodes as a triage test in breast cancer staging. Breast Cancer Res Treat. 2007;103(1):85–91.

    Article  PubMed  Google Scholar 

  120. Krishnamurthy S, Sneige N, Bedi DG, Edieken BS, Fornage BD, Kuerer HM, Singletary SE, Hunt KK. Role of ultrasound-guided fine-needle aspiration of indeterminate and suspicious axillary lymph nodes in the initial staging of breast carcinoma. Cancer. 2002;95(5):982–8.

    Article  PubMed  Google Scholar 

  121. Alvarez S, Añorbe E, Alcorta P, et al. Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. AJR Am J Roentgenol. 2006;186:1342–8.

    Article  PubMed  Google Scholar 

  122. Choi 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(2):119–22.

    Article  PubMed  Google Scholar 

  123. Dihge L, Grabau DA, Rasmussen RW, Bendahl PO, Rydén L. The accuracy of preoperative axillary nodal staging in primary breast cancer by ultrasound is modified by nodal metastatic load and tumor biology. Acta Oncol. 2016;55(8):976–82.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Fornage BD. Local and regional staging of invasive breast cancer with sonography: 25 years of practice at MD Anderson Cancer Center. Oncologist. 2014;19(1):5–15.

    Article  PubMed  Google Scholar 

  125. Fournier D, Huber D, Duc C, Laswad T, Moreau J, Villemain AM, Schneider N. The role of ultrasonography guided-fine-needle-aspiration in axillary lymph node staging of breast cancer. Case series of 108 patients. ECR 2012/C-2585. Vienna. March 1–5 2012.

    Google Scholar 

  126. Houssami N, Ciatto S, Turner RM, Cody HS 3rd, Macaskill P. Preoperative ultrasound-guided needle biopsy of axillary nodes in invasive breast cancer: meta-analysis of its accuracy and utility in staging the axilla. Ann Surg. 2011;254(2):243–51.

    Article  PubMed  Google Scholar 

  127. Mainiero MB, Cinelli CM, Koelliker SL, Graves TA, Chung MA. Axillary ultrasound and fine-needle aspiration in the preoperative evaluation of the breast cancer patient: an algorithm based on tumor size and lymph node appearance. AJR Am J Roentgenol. 2010;195(5):1261–7.

    Article  PubMed  Google Scholar 

  128. Bedi DG, Krishnamurthy R, Krishnamurthy S, Edeiken BS, Le-Petross H, Fornage BD, Bassett RL Jr, Hunt KK. Cortical morphologic features of axillary lymph nodes as a predictor of metastasis in breast cancer: in vitro sonographic study. AJR Am J Roentgenol. 2008;191(3):646–52.

    Article  PubMed  Google Scholar 

  129. Duchesne N, Jaffey J, Florack P, Duchesne S. Redefining ultrasound appearance criteria of positive axillary lymph nodes. Can Assoc Radiol J. 2005;56(5):289–96.

    PubMed  Google Scholar 

  130. Britton PD, Goud A, Godward S, Barter S, Freeman A, Gaskarth M, Rajan P, Sinnatamby R, Slattery J, Provenzano E, O’Donovan M, Pinder S, Benson JR, Forouhi P, Wishart GC. Use of ultrasound-guided axillary node core biopsy in staging of early breast cancer. Eur Radiol. 2009;19(3):561–9.

    Article  PubMed  CAS  Google Scholar 

  131. Cho N, Moon WK, Han W, Park IA, Cho J, Noh DY. Preoperative sonographic classification of axillary lymph nodes in patients with breast cancer: node-to-node correlation with surgical histology and sentinel node biopsy results. AJR Am J Roentgenol. 2009;193(6):1731–7.

    Article  PubMed  Google Scholar 

  132. Fournier D. Ultrasound assessment of sentinel lymph node on breast cancer. Contribution of Aixplorer and its harmonic imaging. Swiss Congress of Radiology. Luzern. 30. Mai – 1. Juni 2013.

    Google Scholar 

  133. Kubota K, Ogawa Y, Nishigawa T, Yoshida S. Tissue harmonic imaging ultrasound of the axillary lymph nodes: evaluation of response to neoadjuvant chemotherapy in breast cancer patients. Oncol Rep. 2003;10(6):1911–4.

    PubMed  Google Scholar 

  134. Shapiro RS, Wagreich J, Parsons RB, Stancato-Pasik A, Yeh HC, Lao R. Tissue harmonic imaging sonography: evaluation of image quality compared with conventional sonography. AJR Am J Roentgenol. 1998;171(5):1203–6.

    Article  PubMed  CAS  Google Scholar 

  135. Dellaportas D, Koureas A, Contis J, Lykoudis PM, Vraka I, Psychogios D, Kondi-Pafiti A, Voros DK. Contrast-enhanced color Doppler ultrasonography for preoperative evaluation of sentinel lymph node in breast cancer patients. Breast Care (Basel). 2015;10(5):331–5.

    Article  Google Scholar 

  136. Sarvazyan A, Hall TJ, Urban MW, Fatemi M, Aglyamov SR, Garra BS. An overview of elastography—an emerging branch of medical imaging. Curr Med Imaging Rev. 2011;7(4):255–82.

    Article  PubMed  PubMed Central  Google Scholar 

  137. Cosgrove DO, Berg WA, Doré CJ, Skyba DM, Henry JP, Gay J, Cohen-Bacrie C, BE1 Study Group. Shear wave elastography for breast masses is highly reproducible. Eur Radiol. 2012;22(5):1023–32.

    Article  PubMed  Google Scholar 

  138. Liu B, Zheng Y, Huang G, Lin M, Shan Q, Lu Y, Tian W, Xie X. Breast lesions: quantitative diagnosis using ultrasound shear wave elastography—a systematic review and meta-analysis. Ultrasound Med Biol. 2016;42(4):835–47.

    Article  PubMed  Google Scholar 

  139. Thomas A, Kümmel S, Fritzsche F, Warm M, Ebert B, Hamm B, Fischer T. Real-time sonoelastography performed in addition to B-mode ultrasound and mammography: improved differentiation of breast lesions? Acad Radiol. 2006;13(12):1496–504.

    Article  PubMed  Google Scholar 

  140. Shah AR, Glazebrook KN, Boughey JC, Hoskin TL, Shah SS, Bergquist JR, Dupont SC, Hieken TJ. Does BMI affect the accuracy of preoperative axillary ultrasound in breast cancer patients? Ann Surg Oncol. 2014;21(10):3278–83.

    Article  PubMed  Google Scholar 

  141. 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.

    Article  PubMed  Google Scholar 

  142. Gooch J, King TA, Eaton A, Dengel L, Stempel M, Corben AD, Morrow M. The extent of extracapsular extension may influence the need for axillary lymph node dissection in patients with T1-T2 breast cancer. Ann Surg Oncol. 2014;21(9):2897–903.

    Article  PubMed  PubMed Central  Google Scholar 

  143. Giuliano AE, McCall L, Beitsch P, et al. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial. Ann Surg. 2010;252:426–32. discussion 32–3

    Google Scholar 

  144. Rutgers EJ, Donker M, Straver ME, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer patients: final analysis of the EORTC AMAROS trial (10981/ 22023). J Clin Oncol. 2013;31(Suppl; abstract):LBA1001.

    Article  Google Scholar 

  145. Katz A, Niemierko A, Gage I, Evans S, Shaffer M, Smith FP, Taghian A, Magnant C. Factors associated with involvement of four or more axillary nodes for sentinel lymph node-positive patients. Int J Radiat Oncol Biol Phys. 2006;65(1):40–4.

    Article  PubMed  Google Scholar 

  146. Beriwal S, Soran A, Kocer B, Wilson JW, Ahrendt GM, Johnson R. Factors that predict the burden of axillary disease in breast cancer patients with a positive sentinel node. Am J Clin Oncol. 2008;31(1):34–8.

    Article  PubMed  Google Scholar 

  147. Sauer T, Kåresen R. The value of preoperative ultrasound guided fine-needle aspiration cytology of radiologically suspicious axillary lymph nodes in breast cancer. Cytojournal. 2014;11:26.

    Article  PubMed  PubMed Central  Google Scholar 

  148. Tahir M, Osman KA, Shabbir J, Rogers C, Suarez R, Reynolds T, Bucknall T. Preoperative axillary staging in breast cancer-saving time and resource. Breast J. 2008;14(4):369–71.

    Article  PubMed  Google Scholar 

  149. Kramer GM, Leenders MW, Schijf LJ, Go HL, van der Ploeg T, van den Tol MP, Schreurs WH. Is ultrasound-guided fine-needle aspiration cytology of adequate value in detecting breast cancer patients with three or more positive axillary lymph nodes? Breast Cancer Res Treat. 2016;156(2):271.

    Article  PubMed  CAS  Google Scholar 

  150. Neal CH, Daly CP, Nees AV, Helvie MA. Can preoperative axillary US help exclude N2 and N3 metastatic breast cancer? Radiology. 2010;257(2):335–41.

    Article  PubMed  Google Scholar 

  151. Schiettecatte A, Bourgain C, Breucq C, Buls N, De Wilde V, de Mey J. Initial axillary staging of breast cancer using ultrasound-guided fine needle aspiration: a liquid-based cytology study. Cytopathology. 2011;22(1):30–5.

    Article  PubMed  CAS  Google Scholar 

  152. van Wely BJ, de Wilt JH, Schout PJ, et al. Ultrasound-guided fine-needle aspiration of suspicious nodes in breast cancer patients; selecting patients with extensive nodal involvement. Breast Cancer Res Treat. 2013;140:113–8.

    Article  PubMed  CAS  Google Scholar 

  153. Rocha RD, Girardi AR, Pinto RR, de Freitas VA. Axillary ultrasound and fine-needle aspiration in preoperative staging of axillary lymph nodes in patients with invasive breast cancer. Radiol Bras. 2015;48(6):345–52.

    Article  PubMed  PubMed Central  Google Scholar 

  154. Tucker NS, Cyr AE, Ademuyiwa FO, Tabchy A, George K, Sharma PK, Jin LX, Sanati S, Aft R, Gao F, Margenthaler JA, Gillanders WE. Axillary ultrasound accurately excludes clinically significant lymph node disease in patients with early stage breast cancer. Ann Surg. 2016;264(6):1098–102.

    Article  PubMed  Google Scholar 

  155. Fernández B, Paish EC, Green AR, Lee AH, Macmillan RD, Ellis IO, Rakha EA. Lymph-node metastases in invasive lobular carcinoma are different from those in ductal carcinoma of the breast. J Clin Pathol. 2011;64(11):995–1000.

    Article  PubMed  Google Scholar 

  156. Brouckaert O, Laenen A, Smeets A, Christiaens MR, Vergote I, Wildiers H, Moerman P, Floris G, Neven P; MBC Leuven. Prognostic implications of lobular breast cancer histology: new insights from a single hospital cross-sectional study and SEER data. Breast. 2014;23(4):371–7.

    Google Scholar 

  157. Boerner S, Sneige N. Specimen adequacy and false-negative diagnosis rate in fine-needle aspirates of palpable breast masses. Cancer. 1998;84(6):344–8.

    Article  PubMed  CAS  Google Scholar 

  158. Ganott MA, Zuley ML, Abrams GS, Lu AH, Kelly AE, Sumkin JH, Chivukula M, Carter G, Austin RM, Bandos AI. Ultrasound guided core biopsy versus fine needle aspiration for evaluation of axillary lymphadenopathy in patients with breast cancer. ISRN Oncol. 2014;2014:703160.

    PubMed  PubMed Central  Google Scholar 

  159. Holwitt DM, Swatske ME, Gillanders WE, Monsees BS, Gao F, Aft RL, Eberlein TJ, Margenthaler JA. Scientific Presentation Award: the combination of axillary ultrasound and ultrasound-guided biopsy is an accurate predictor of axillary stage in clinically node-negative breast cancer patients. Am J Surg. 2008;196(4):477–82.

    Article  PubMed  PubMed Central  Google Scholar 

  160. Diepstraten SC, Sever AR, Buckens CF, Veldhuis WB, van Dalen T, van den Bosch MA, Mali WP, Verkooijen HM. Value of preoperative ultrasound-guided axillary lymph node biopsy for preventing completion axillary lymph node dissection in breast cancer: a systematic review and meta-analysis. Ann Surg Oncol. 2014;21(1):51–9.

    Article  PubMed  Google Scholar 

  161. Mendoza P, Lacambra M, Tan PH, Tse GM. Fine needle aspiration cytology of the breast: the nonmalignant categories. Patholog Res Int. 2011;2011:547580.

    PubMed  PubMed Central  Google Scholar 

  162. Scopa CD, Koukouras D, Androulakis J, Bonikos D. Sources of diagnostic discrepancies in fine-needle aspiration of the breast. Diagn Cytopathol. 1991;7(5):546–8.

    Article  PubMed  CAS  Google Scholar 

  163. Britton PD, Provenzano E, Barter S, Gaskarth M, Goud A, Moyle P, Sinnatamby R, Wallis M, Benson JR, Forouhi P, Wishart GC. Ultrasound guided percutaneous axillary lymph node core biopsy: how often is the sentinel lymph node being biopsied? Breast. 2009;18(1):13–6.

    Article  PubMed  CAS  Google Scholar 

  164. Karnon J, Peters J, Platt J, Chilcott J, McGoogan E, Brewer N. Liquid-based cytology in cervical screening: an updated rapid and systematic review and economic analysis. Health Technol Assess 2004;8(20).

    Google Scholar 

  165. Mayor S. NHS cervical screening programme to introduce liquid based cytology. BMJ. 2003;327(7421):948.

    Article  PubMed  PubMed Central  Google Scholar 

  166. Saqi A. The state of cell blocks and ancillary testing: past, present, and future. Arch Pathol Lab Med. 2016;140(12):1318–22.

    Article  PubMed  Google Scholar 

  167. Tripathy K, Misra A, Ghosh JK. Efficacy of liquid-based cytology versus conventional smears in FNA samples. J Cytol. 2015;32(1):17–20. https://doi.org/10.4103/0970-9371.155225.

    Article  PubMed  PubMed Central  Google Scholar 

  168. Fournier D, Joris F, Pauzé JL, Gaudin G, Vogel J. Avantages pratiques du transport en milieu liquide lors de ponction à l’aiguille fine des lésions du sein : à propos de750 ponctions dont 210 cancers. 21es journées Nationales de la Société Française de Sénologie et de Pathologie Mammaire, 20–22 oct 1999.

    Google Scholar 

  169. Joris F, Pauzé JL, Fournier D, Gaudin G, Vogel J. Cytologie des lésions du sein par ponction à l’aiguille : comparaison des potentialités du transport en milieu liquide et de l’analyse en couche mince par rapport à la méthode traditionnelle d’étalement sur lames. Erster Gemeinsamer Senologie Kongress der Deutschen-Österreichischen-Schweizer Gesellschaft für Senologie. Lugano. 5.-8 Juli 2000.

    Google Scholar 

  170. Jing X, Wey E, Michael CW. Diagnostic value of fine needle aspirates processed by ThinPrep® for the assessment of axillary lymph node status in patients with invasive carcinoma of the breast. Cytopathology. 2013;24:372–6.

    Article  PubMed  CAS  Google Scholar 

  171. Britton P, Moyle P, Benson JR, Goud A, Sinnatamby R, Barter S, Gaskarth M, Provenzano E, Wallis M. Ultrasound of the axilla: where to look for the sentinel lymph node. Clin Radiol. 2010;65(5):373–6.

    Article  PubMed  CAS  Google Scholar 

  172. Cox K, Sever A, Jones S, Weeks J, Mills P, Devalia H, Fish D, Jones P. Validation of a technique using microbubbles and contrast enhanced ultrasound (CEUS) to biopsy sentinel lymph nodes (SLN) in pre-operative breast cancer patients with a normal grey-scale axillary ultrasound. Eur J Surg Oncol. 2013;39(7):760–5.

    Article  PubMed  CAS  Google Scholar 

  173. Cui XW, Jenssen C, Saftoiu A, et al. New ultrasound techniques for lymph node evaluation. World J Gastroenterol. 2013;19:4850–60.

    Article  PubMed  PubMed Central  Google Scholar 

  174. Sever AR, Mills P, Weeks J, Jones SE, Fish D, Jones PA, Mali W. Preoperative needle biopsy of sentinel lymph nodes using intradermal microbubbles and contrast-enhanced ultrasound in patients with breast cancer. AJR Am J Roentgenol. 2012;199(2):465–70.

    Article  PubMed  Google Scholar 

  175. Ouyang Q, Chen L, Zhao H, et al. Detecting metastasis of lymph nodes and predicting aggressiveness in patients with breast carcinomas. J Ultrasound Med. 2010;29:343–52.

    Article  PubMed  Google Scholar 

  176. Yang WT, Metreweli C, Lam PK, Chang J. Benign and malignant breast masses and axillary nodes: evaluation with echo-enhanced color power Doppler US. Radiology. 2001;220:795–802.

    Article  PubMed  CAS  Google Scholar 

  177. Genta F, Zanon E, Camanni M, Deltetto F, Drogo M, Gallo R, Gilardi C. Cost/accuracy ratio analysis in breast cancer patients undergoing ultrasound-guided fine-needle aspiration cytology, sentinel node biopsy, and frozen section of node. World J Surg. 2007;31(6):1155–63.

    Article  PubMed  Google Scholar 

  178. Glynn RW, Williams L, Dixon JM. A further survey of surgical management of the axilla in UK breast cancer patients. Ann R Coll Surg Engl. 2010;92(6):506–11.

    Article  PubMed  PubMed Central  Google Scholar 

  179. Fillion MM, Glass KE, Hayek J, Wehr A, Phillips G, Terando A, Agnese DM. Healthcare costs reduced after incorporating the results of the American College of Surgeons Oncology Group Z0011 trial into clinical practice. Breast J. 2016;30.

    Google Scholar 

  180. Camp MS, Greenup RA, Taghian A, Coopey SB, Specht M, Gadd M, Hughes K, Smith BL. Application of ACOSOG Z0011 criteria reduces perioperative costs. Ann Surg Oncol. 2013;20(3):836–4.

    Article  PubMed  Google Scholar 

  181. McMasters KM, Wong SL, Tuttle TM, Carlson DJ, Brown CM, Dirk Noyes R, Glaser RL, Vennekotter DJ, Turk PS, Tate PS, Sardi A, Edwards MJ. Preoperative lymphoscintigraphy for breast cancer. Ann Surg. 2000;231(5):724–31.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  182. Gnant M, Harbeck N, Thomssen C. St. Gallen 2011: summary of the consensus discussion. Breast Care (Basel). 2011;6(2):136–41.

    Article  Google Scholar 

  183. Dengel LT, Van Zee KJ, King TA, Stempel M, Cody HS, El-Tamer M, Gemignani ML, Sclafani LM, Sacchini VS, Heerdt AS, Plitas G, Junqueira M, Capko D, Patil S, Morrow M. Axillary dissection can be avoided in the majority of clinically node-negative patients undergoing breast-conserving therapy. Ann Surg Oncol. 2014;21(1):22–7.

    Article  PubMed  Google Scholar 

  184. Giuliano AE, Ballman K, McCall L, Beitsch P, Whitworth PW, Blumencranz P, Leitch AM, Saha S, Morrow M, Hunt KK. Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: long-term follow-up from the American College of Surgeons Oncology Group (Alliance) ACOSOG Z0011 randomized trial. Ann Surg. 2016;264(3):413–20.

    Article  PubMed  Google Scholar 

  185. Joyce DP, Lowery AJ, McGrath-Soo LB, Downey E, Kelly L, O’Donoghue GT, Barry M, Hill AD. Management of the axilla: has Z0011 had an impact? Ir J Med Sci. 2016;185(1):145–9.

    Article  PubMed  CAS  Google Scholar 

  186. Gentilini O, Veronesi U. Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: Sentinel node vs Observation after axillary UltraSouND). Breast. 2012;21(5):678–81.

    Article  PubMed  Google Scholar 

  187. Reimer T, Hartmann S, Stachs A, et al. Local treatment of the axilla in early breast cancer: concepts from the National Surgical Adjuvant Breast and Bowel Project B-04 to the planned Intergroup Sentinel Mamma trial. Breast Care (Basel). 2014;9:87–95.

    Article  Google Scholar 

  188. Humphrey KL, Saksena MA, Freer PE, Smith BL, Rafferty EA. To do or not to do: axillary nodal evaluation after ACOSOG Z0011 trial. Radiographics. 2014;34(7):1807–16.

    Article  PubMed  Google Scholar 

  189. Reyna C, Kiluk JV, Frelick A, Khakpour N, Laronga C, Lee MC. Impact of axillary ultrasound (AUS) on axillary dissection in breast conserving surgery (BCS). J Surg Oncol. 2015;111(7):813–8.

    Article  PubMed  Google Scholar 

  190. Cox K, Weeks J, Mills P, Chalmers R, Devalia H, Fish D, Sever A. Contrast-enhanced ultrasound biopsy of sentinel lymph nodes in patients with breast cancer: implications for axillary metastases and conservation. Ann Surg Oncol. 2016;23(1):58–64.

    Article  PubMed  Google Scholar 

  191. Moorman AM, Bourez RL, Heijmans HJ, Kouwenhoven EA. Axillary ultrasonography in breast cancer patients helps in identifying patients preoperatively with limited disease of the axilla. Ann Surg Oncol. 2014;21(9):2904–10.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dominique Fournier M.D. .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Fournier, D. (2018). Lymph Node Staging with US (and FNA). In: Amy, D. (eds) Lobar Approach to Breast Ultrasound. Springer, Cham. https://doi.org/10.1007/978-3-319-61681-0_10

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-61681-0_10

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-61680-3

  • Online ISBN: 978-3-319-61681-0

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics