Staging the axilla in women with breast cancer: the utility of preoperative ultrasound-guided needle biopsy

Nehmat Houssami, Robin M Turner, Nehmat Houssami, Robin M Turner

Abstract

Preoperative staging of the axilla in women with invasive breast cancer using ultrasound-guided needle biopsy (UNB) identifies approximately 50% of patients with axillary nodal metastases prior to surgical intervention. Although moderately sensitive, it is a highly specific staging strategy that is rarely falsely-positive, hence a positive UNB allows patients to be triaged to axillary lymph-node dissection (ALND) avoiding potentially unnecessary sentinel node biopsy (SNB). In this review, we extend our previous work through an updated literature search, focusing on studies that report data on UNB utility. Based on data for 10,934 breast cancer patients, sourced from 35 studies, a positive UNB allowed triage of 1,745 cases (simple proportion 16%) to axillary surgical treatment: the utility of UNB was a median 19.8% [interquartile range (IQR) 11.6%-26.7%] across these studies. We also modelled data from a subgroup of studies, and estimated that amongst patients with metastases to axillary nodes, the odds ratio (OR) for high nodal disease burden for a positive UNB versus a negative UNB was 4.38 [95% confidence interval (95% CI): 3.13, 6.13], P<0.001. From this model, the estimated proportion with high nodal disease burden was 58.9% (95% CI: 50.2%, 67.0%) for a positive UNB, whereas the estimated proportion with high nodal disease burden was 24.6% (95% CI: 17.7%, 33.2%) if UNB was negative. Overall, axillary UNB has good clinical utility and a positive UNB can effectively triage to ALND. However, the evolving landscape of axillary surgical treatment means that UNB will have relatively less utility where surgeons have modified their practice to omission of ALND for minimal nodal metastatic disease.

Keywords: Breast cancer; axillary staging; node metastases; test utility; ultrasound-guided needle biopsy (UNB).

Conflict of interest statement

No potential conflicts of interest are disclosed.

Figures

Figure 1
Figure 1
Bubble plot shows study-specific UNB utility (proportion of subjects triaged to axillary surgery based on UNB result) in relation to underlying prevalence of node metastases.
Figure 2
Figure 2
Estimated OR for high nodal disease burden in patients with a positive UNB vs. those with a negative UNB amongst patients with axillary node metastases. Study-specific and pooled estimates shown in plot; pooled OR=4.38 (95% CI: 3.13, 6.13); a positive UNB refers to positive ultrasound/positive needle biopsy, a negative UNB refers to positive ultrasound/negative needle biopsy amongst patients subsequently shown to have nodal metastases on SNB and/or ALND; high nodal disease burden refers to >3 nodes (relative to 1-3 nodes) however the study from Garcia-Fernandez 2011 used ≥2 nodes to classify higher node disease burden. UNB, ultrasound-guided needle biopsy; SNB, sentinel node biopsy; OR, odds ratio; ALND, axillary lymph-node dissection.

References

    1. Kell MR, Burke JP, Barry M, Morrow M. Outcome of axillary staging in early breast cancer: a meta-analysis. Breast Cancer Res Treat 2010;120:441-447
    1. Wang Z, Wu LC, Chen JQ. Sentinel lymph node biopsy compared with axillary lymph node dissection in early breast cancer: a meta-analysis. Breast Cancer Res Treat 2011;129:675-689
    1. Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW, Blumencranz PW, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 2011;305:569-575
    1. Bossuyt PM, Reitsma JB, Linnet K, Moons KG. Beyond diagnostic accuracy: the clinical utility of diagnostic tests. Clin Chem 2012;58:1636-1643
    1. 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;254:243-251
    1. Diepstraten SC, Sever AR, Buckens CF, Veldhuis WB, van Dalen T, van den Bosch MA, et al. 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;21:51-59
    1. Verbanck J, Vandewiele I, De Winter H, Tytgat J, Van Aelst F, Tanghe W.Value of axillary ultrasonography and sonographically guided puncture of axillary nodes: a prospective study in 144 consecutive patients. J Clin Ultrasound 1997;25:53-56
    1. Bonnema J, van Geel AN, van Ooijen B, Mali SP, Tjiam SL, Henzen-Logmans SC, et al. Ultrasound-guided aspiration biopsy for detection of nonpalpable axillary node metastases in breast cancer patients: new diagnostic method. World J Surg 1997;21:270-274
    1. Holwitt DM, Swatske ME, Gillanders WE, Monsees BS, Gao F, Aft RL, et al. 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;196:477-482
    1. Popli MB, Sahoo M, Mehrotra N, Choudhury M, Kumar A, Pathania OP, et al. Preoperative ultrasound-guided fine-needle aspiration cytology for axillary staging in breast carcinoma. Australas Radiol 2006;50:122-126
    1. Davis JT, Brill YM, Simmons S, Sachleben BC, Cibull ML, McGrath P, et al. Ultrasound-guided fine-needle aspiration of clinically negative lymph nodes versus sentinel node mapping in patients at high risk for axillary metastasis. Ann Surg Oncol 2006;13:1545-1552
    1. Deurloo EE, Tanis PJ, Gilhuijs KG, Muller SH, Kröger R, Peterse JL, et al. Reduction in the number of sentinel lymph node procedures by preoperative ultrasonography of the axilla in breast cancer. Eur J Cancer 2003;39:1068-1073
    1. Abe H, Schmidt RA, Kulkarni K, Sennett CA, Mueller JS, Newstead GM. Axillary lymph nodes suspicious for breast cancer metastasis: sampling with US-guided 14-gauge core-needle biopsy--clinical experience in 100 patients. Radiology 2009;250:41-49
    1. Sapino A, Cassoni P, Zanon E, Fraire F, Croce S, Coluccia C, et al. Ultrasonographically-guided fine-needle aspiration of axillary lymph nodes: role in breast cancer management. Br J Cancer 2003;88:702-706
    1. Brancato B, Zappa M, Bricolo D, Catarzi S, Risso G, Bonardi R, et al. Role of ultrasound-guided fine needle cytology of axillary lymph nodes in breast carcinoma staging. Radiol Med 2004;108:345-355
    1. Britton PD, Goud A, Godward S, Barter S, Freeman A, Gaskarth M, et al. Use of ultrasound-guided axillary node core biopsy in staging of early breast cancer. Eur Radiol 2009;19:561-569
    1. Podkrajsek M, Music MM, Kadivec M, Zgajnar J, Besic N, Pogacnik A, et al. Role of ultrasound in the preoperative staging of patients with breast cancer. Eur Radiol 2005;15:1044-1050
    1. Bedrosian I, Bedi D, Kuerer HM, Fornage BD, Harker L, Ross MI, et al. Impact of clinicopathological factors on sensitivity of axillary ultrasonography in the detection of axillary nodal metastases in patients with breast cancer. Ann Surg Oncol 2003;10:1025-1030
    1. Cowher MS, Erb KM, Poller W, Julian TB. Correlation of the use of axillary ultrasound and lymph node needle biopsy with surgical lymph node pathology in patients with invasive breast cancer. Am J Surg 2008;196:756-759
    1. Damera A, Evans AJ, Cornford EJ, Wilson AR, Burrell HC, James JJ, et al. Diagnosis of axillary nodal metastases by ultrasound-guided core biopsy in primary operable breast cancer. Br J Cancer 2003;89:1310-1313
    1. van Rijk MC, Deurloo EE, Nieweg OE, Gilhuijs KG, Peterse JL, Rutgers EJ, et al. Ultrasonography and fine-needle aspiration cytology can spare breast cancer patients unnecessary sentinel lymph node biopsy. Ann Surg Oncol 2006;13:31-35
    1. Boughey JC, Middleton LP, Harker L, Garrett B, Fornage B, Hunt KK, et al. Utility of ultrasound and fine-needle aspiration biopsy of the axilla in the assessment of invasive lobular carcinoma of the breast. Am J Surg 2007;194:450-455
    1. Genta F, Zanon E, Camanni M, Deltetto F, Drogo M, Gallo R, et al. 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;31:1155-1163
    1. 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;246:81-89
    1. Altomare V, Guerriero G, Carino R, Battista C, Primavera A, Altomare A, et al. Axillary lymph node echo-guided fine-needle aspiration cytology enables breast cancer patients to avoid a sentinel lymph node biopsy. Preliminary experience and a review of the literature. Surg Today 2007;37:735-739
    1. Jain A, Haisfield-Wolfe ME, Lange J, Ahuja N, Khouri N, Tsangaris T, et al. The role of ultrasound-guided fine-needle aspiration of axillary nodes in the staging of breast cancer. Ann Surg Oncol 2008;15:462-471
    1. Gilissen F, Oostenbroek R, Storm R, Westenend P, Plaisier P.Prevention of futile sentinel node procedures in breast cancer: ultrasonography of the axilla and fine-needle aspiration cytology are obligatory. Eur J Surg Oncol 2008;34:497-500
    1. Luparia A, Campanino P, Cotti R, Lucarelli D, Durando M, Mariscotti G, et al. Role of axillary ultrasound in the preoperative diagnosis of lymph node metastases in patients affected by breast carcinoma. Radiol Med 2010;115:225-237
    1. Duchesne N, Jaffey J, Florack P, Duchesne S.Redefining ultrasound appearance criteria of positive axillary lymph nodes. Can Assoc Radiol J 2005;56:289-296
    1. 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;269:54-60
    1. Garcia-Ortega MJ, Benito MA, Vahamonde EF, Torres PR, Velasco AB, Paredes MM. Pretreatment axillary ultrasonography and core biopsy in patients with suspected breast cancer: diagnostic accuracy and impact on management. Eur J Radiol 2011;79:64-72
    1. Hackney L, Williams S, Bajwa S, Morley-Davies AJ, Kirby RM, Britton I. Influence of tumor histology on preoperative staging accuracy of breast metastases to the axilla. Breast J 2013;19:49-55
    1. de Kanter AY, van Eijck CH, van Geel AN, Kruijt RH, Henzen SC, Paul MA, et al. Multicentre study of ultrasonographically guided axillary node biopsy in patients with breast cancer. Br J Surg 1999;86:1459-1462
    1. Kuenen-Boumeester V, Menke-Pluymers M, de Kanter AY, Obdeijn IM, Urich D, Van Der Kwast TH. Ultrasound-guided fine needle aspiration cytology of axillary lymph nodes in breast cancer patients. A preoperative staging procedure. Eur J Cancer 2003;39:170-174
    1. 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 Res Treat 2007;103:85-91
    1. Sahoo S, Sanders MA, Roland L, Pile N, Chagpar AB. A strategic approach to the evaluation of axillary lymph nodes in breast cancer patients: analysis of 168 patients at a single institution. Am J Surg 2007;194:524-526
    1. Tahir M, Osman KA, Shabbir J, Rogers C, Suarez R, Reynolds T, et al. Preoperative axillary staging in breast cancer-saving time and resources. Breast J 2008;14:369-371
    1. Hinson JL, McGrath P, Moore A, Davis JT, Brill YM, Samoilova E, et al. The critical role of axillary ultrasound and aspiration biopsy in the management of breast cancer patients with clinically negative axilla. Ann Surg Oncol 2008;15:250-255
    1. 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;97:680-683
    1. Lee MC, Eatrides J, Chau A, Han G, Kiluk JV, Khakpour N, et al. Consequences of axillary ultrasound in patients with T2 or greater invasive breast cancers. Ann Surg Oncol 2011;18:72-77
    1. Chang MC, Crystal P, Colgan TJ. The evolving role of axillary lymph node fine-needle aspiration in the management of carcinoma of the breast. Cancer Cytopathol 2011;119:328-334
    1. García Fernández A, Fraile M, Giménez N, Reñe A, Torras M, Canales L, et al. 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
    1. 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;22:30-35
    1. Solon JG, Power C, Al-Azawi D, Duke D, Hill AD. Ultrasound-guided core biopsy: an effective method of detecting axillary nodal metastases. J Am Coll Surg 2012;214:12-17
    1. Rattay T, Muttalib M, Khalifa E, Duncan A, Parker SJ. Clinical utility of routine pre-operative axillary ultrasound and fine needle aspiration cytology in patient selection for sentinel lymph node biopsy. Breast 2012;21:210-214
    1. Leenders MW, Broeders M, Croese C, Richir MC, Go HL, Langenhorst BL, et al. Ultrasound and fine needle aspiration cytology of axillary lymph nodes in breast cancer. To do or not to do? Breast 2012;21:578-583
    1. Caretta-Weyer H, Sisney GA, Beckman C, Burnside ES, Salkowsi LR, Strigel RM, et al. Impact of axillary ultrasound and core needle biopsy on the utility of intraoperative frozen section analysis and treatment decision making in women with invasive breast cancer. Am J Surg 2012;204:308-314
    1. van Wely BJ, de Wilt JH, Schout PJ, Kooistra B, Wauters CA, Venderinck D, 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;140:113-118
    1. Cools-Lartigue J, Sinclair A, Trabulsi N, Meguerditchian A, Mesurolle B, Fuhrer R, et al. Preoperative axillary ultrasound and fine-needle aspiration biopsy in the diagnosis of axillary metastases in patients with breast cancer: predictors of accuracy and future implications. Ann Surg Oncol 2013;20:819-827
    1. Amonkar SJ, Oates E, McLean L, Nicholson S. Pre-operative staging of the axilla in primary breast cancer. Byredefining the abnormal appearing node can we reduce investigations without affecting overall treatment? Breast 2013;22:1114-1118
    1. Topal U, Punar S, Tasdelen I, Adim SB. Role of ultrasound-guided core needle biopsy of axillary lymph nodes in the initial staging of breast carcinoma. Eur J Radiol 2005;56:382-385
    1. Joh JE, Han G, Kiluk JV, Laronga C, Khakpour N, Lee MC. Indications for axillary ultrasound use in breast cancer patients. Clin Breast Cancer 2012;12:433-437
    1. Giuliano AE, McCall L, Beitsch P, Whitworth PW, Blumencranz P, Leitch AM, 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 432-3
    1. Dengel LT, Van Zee KJ, King TA, Stempel M, Cody HS, El-Tamer M, et al. Axillary dissection can be avoided in the majority of clinically node-negative patients undergoing breast-conserving therapy. Ann Surg Oncol 2014;21:22-27
    1. Britton P, Moyle P, Benson JR, Goud A, Sinnatamby R, Barter S, et al. Ultrasound of the axilla: where to look for the sentinel lymph node. Clin Radiol 2010;65:373-376
    1. Sever A, Jones S, Cox K, Weeks J, Mills P, Jones P.Preoperative localization of sentinel lymph nodes using intradermal microbubbles and contrast-enhanced ultrasonography in patients with breast cancer. Br J Surg 2009;96:1295-1299
    1. Sever AR, Mills P, Jones SE, Cox K, Weeks J, Fish D, et al. Preoperative sentinel node identification with ultrasound using microbubbles in patients with breast cancer. AJR Am J Roentgenol 2011;196:251-256
    1. 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;21:678-681

Source: PubMed

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