Skip to main content
Top
Published in: World Journal of Surgical Oncology 1/2019

Open Access 01-12-2019 | Ultrasound | Research

Shortcomings of ultrasound-guided fine needle aspiration in the axillary management of women with breast cancer

Authors: Michel Attieh, Faek Jamali, Ghina Berjawi, Mothana Saadeldine, Fouad Boulos

Published in: World Journal of Surgical Oncology | Issue 1/2019

Login to get access

Abstract

Background

Ultrasound, along with ultrasound-guided fine needle aspiration, is currently used for the axillary evaluation of breast cancer patients in order to identify candidates for axillary lymph node dissection. The aim of this study is to evaluate the accuracy of this tool in correctly identifying patients who may or may not benefit from axillary clearance in light of the ACOSOG Z0011 trial recommendations.

Methods

One hundred one patients (65 with positive US-FNA with corresponding axillary lymph node dissection (ALND), and 36 with negative US-FNA with corresponding ALND/sentinel lymph node biopsy) were studied for the number of involved axillary lymph nodes, tumor clinicopathologic features, and axillary radiologic findings.

Results

From the positive US-FNA group, 43% of patients had two or fewer positive lymph nodes upon ALND pathologic examination. In the US-FNA negative group, the negative predictive value for detecting axillary disease was 72.7%. With both groups combined, the sensitivity, specificity, PPV, and NPV of US-FNA for selecting patients based on axillary disease burden were 86%, 51.7%, 57%, and 83.3%, respectively.

Conclusion

Based on Z0011 guidelines, US-FNA is not a reliable tool in triaging patients in need for ALND and leads to overtreatment of 43% patients when positive, while depriving a small but significant percentage of patients from necessary therapy, when negative.
Literature
1.
go back to reference Halsted W. The results of operations for the cure of cancer of the breast performed at the Johns Hopkins Hospital from June 1889 to January 1894. Johns Hopkins Hosp Bull. 1895;4:297. Halsted W. The results of operations for the cure of cancer of the breast performed at the Johns Hopkins Hospital from June 1889 to January 1894. Johns Hopkins Hosp Bull. 1895;4:297.
2.
go back to reference Habal N, Giuliano AE, Morton DL. The use of sentinel lymphadenectomy to identify candidates for postoperative adjuvant therapy of melanoma and breast cancer. Semin Oncol. 2001;28:41–52.CrossRef Habal N, Giuliano AE, Morton DL. The use of sentinel lymphadenectomy to identify candidates for postoperative adjuvant therapy of melanoma and breast cancer. Semin Oncol. 2001;28:41–52.CrossRef
3.
go back to reference Giuliano A, McCall L, Beitsch P, Whitworth P, Morrow M, Blumencranz P, et al. ACOSOG Z0011: a randomized trial of axillary node dissection in women with clinical T1-2 N0 M0 breast cancer who have a positive sentinel node. J Clin Oncol. 2010;28(18_suppl):CRA506-CRACRA.CrossRef Giuliano A, McCall L, Beitsch P, Whitworth P, Morrow M, Blumencranz P, et al. ACOSOG Z0011: a randomized trial of axillary node dissection in women with clinical T1-2 N0 M0 breast cancer who have a positive sentinel node. J Clin Oncol. 2010;28(18_suppl):CRA506-CRACRA.CrossRef
4.
go back to reference Van Wely B, De Wilt J, Schout P, Kooistra B, Wauters C, 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(1):113–8.CrossRef Van Wely B, De Wilt J, Schout P, Kooistra B, Wauters C, 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(1):113–8.CrossRef
5.
go back to reference 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.CrossRef 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.CrossRef
6.
go back to reference Gradishar WJ, Anderson BO, Balassanian R, Blair SL, Burstein HJ, Cyr A, et al. NCCN guidelines insights: breast cancer, version 1.2017. J Natl Compr Cancer Netw. 2017;15(4):433–51.CrossRef Gradishar WJ, Anderson BO, Balassanian R, Blair SL, Burstein HJ, Cyr A, et al. NCCN guidelines insights: breast cancer, version 1.2017. J Natl Compr Cancer Netw. 2017;15(4):433–51.CrossRef
7.
go back to reference Harnett A, Smallwood J, Titshall V, Champion A. Diagnosis and treatment of early breast cancer, including locally advanced disease—summary of NICE guidance. Bmj. 2009;338:b438.CrossRef Harnett A, Smallwood J, Titshall V, Champion A. Diagnosis and treatment of early breast cancer, including locally advanced disease—summary of NICE guidance. Bmj. 2009;338:b438.CrossRef
8.
go back to reference Cools-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(1):46–54.CrossRef Cools-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(1):46–54.CrossRef
9.
go back to reference 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(3):819–27.CrossRef 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(3):819–27.CrossRef
10.
go back to reference Elmore LC, Appleton CM, Zhou G, Margenthaler JA. Axillary ultrasound in patients with clinically node-negative breast cancer: which features are predictive of disease? J Surg Res. 2013;184(1):234–40.CrossRef Elmore LC, Appleton CM, Zhou G, Margenthaler JA. Axillary ultrasound in patients with clinically node-negative breast cancer: which features are predictive of disease? J Surg Res. 2013;184(1):234–40.CrossRef
11.
go back to reference Nath J, Sami N, Massey J, Donnelly J, Corder A. Selection for axillary clearance in breast cancer (ultrasound negative, sentinel node positive patients have low rates of further metastases). Eur J Surg Oncol. 2013;39(5):450–4.CrossRef Nath J, Sami N, Massey J, Donnelly J, Corder A. Selection for axillary clearance in breast cancer (ultrasound negative, sentinel node positive patients have low rates of further metastases). Eur J Surg Oncol. 2013;39(5):450–4.CrossRef
12.
go back to reference Hu X, Zhou X, Yang H, Wei W, Jiang Y, Liu J. Axillary ultrasound and fine needle aspiration biopsy in the preoperative diagnosis of axillary metastases in early-stage breast cancer. Oncol Lett. 2018;15(6):8477–83.PubMedPubMedCentral Hu X, Zhou X, Yang H, Wei W, Jiang Y, Liu J. Axillary ultrasound and fine needle aspiration biopsy in the preoperative diagnosis of axillary metastases in early-stage breast cancer. Oncol Lett. 2018;15(6):8477–83.PubMedPubMedCentral
13.
go back to reference Ameri B, Kanesa-Thasan R, Abu-Khalaf MM, Berger AC, Eisenberg T, Lazar MA, et al. Negative predictive value of ipsilateral axillary ultrasound in the pre-operative assessment of invasive breast cancer. J Clin Oncol. 2017:e12080–0.CrossRef Ameri B, Kanesa-Thasan R, Abu-Khalaf MM, Berger AC, Eisenberg T, Lazar MA, et al. Negative predictive value of ipsilateral axillary ultrasound in the pre-operative assessment of invasive breast cancer. J Clin Oncol. 2017:e12080–0.CrossRef
14.
go back to reference Leenders M, Broeders M, Croese C, Richir M, Go H, Langenhorst B, et al. Ultrasound and fine needle aspiration cytology of axillary lymph nodes in breast cancer. To do or not to do? Breast. 2012;21(4):578–83.CrossRef Leenders M, Broeders M, Croese C, Richir M, Go H, Langenhorst B, et al. Ultrasound and fine needle aspiration cytology of axillary lymph nodes in breast cancer. To do or not to do? Breast. 2012;21(4):578–83.CrossRef
15.
go back to reference Rattay T, Muttalib M, Khalifa E, Duncan A, Parker S. Clinical utility of routine pre-operative axillary ultrasound and fine needle aspiration cytology in patient selection for sentinel lymph node biopsy. Breast. 2012;21(2):210–4.CrossRef Rattay T, Muttalib M, Khalifa E, Duncan A, Parker S. Clinical utility of routine pre-operative axillary ultrasound and fine needle aspiration cytology in patient selection for sentinel lymph node biopsy. Breast. 2012;21(2):210–4.CrossRef
16.
go back to reference 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(12):1545–52.CrossRef 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(12):1545–52.CrossRef
17.
go back to reference 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(1):31–5.CrossRef 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(1):31–5.CrossRef
18.
go back to reference Yi M, Kuerer HM, Mittendorf EA, Hwang RF, Caudle AS, Bedrosian I, et al. Impact of the American College of Surgeons Oncology Group Z0011 criteria applied to a contemporary patient population. J Am Coll Surg. 2013;216(1):105–13.CrossRef Yi M, Kuerer HM, Mittendorf EA, Hwang RF, Caudle AS, Bedrosian I, et al. Impact of the American College of Surgeons Oncology Group Z0011 criteria applied to a contemporary patient population. J Am Coll Surg. 2013;216(1):105–13.CrossRef
19.
go back to reference Van Wely B, De Wilt J, Francissen C, Teerenstra S, Strobbe L. Meta-analysis of ultrasound-guided biopsy of suspicious axillary lymph nodes in the selection of patients with extensive axillary tumour burden in breast cancer. Br J Surg. 2015;102(3):159–68.CrossRef Van Wely B, De Wilt J, Francissen C, Teerenstra S, Strobbe L. Meta-analysis of ultrasound-guided biopsy of suspicious axillary lymph nodes in the selection of patients with extensive axillary tumour burden in breast cancer. Br J Surg. 2015;102(3):159–68.CrossRef
20.
go back to reference Stachs A, Göde K, Hartmann S, Stengel B, Nierling U, Dieterich M, et al. Accuracy of axillary ultrasound in preoperative nodal staging of breast cancer-size of metastases as limiting factor. SpringerPlus. 2013;2(1):350.CrossRef Stachs A, Göde K, Hartmann S, Stengel B, Nierling U, Dieterich M, et al. Accuracy of axillary ultrasound in preoperative nodal staging of breast cancer-size of metastases as limiting factor. SpringerPlus. 2013;2(1):350.CrossRef
21.
go back to reference Fournier K, Schiller A, Perry RR, Laronga C. Micrometastasis in the sentinel lymph node of breast cancer does not mandate completion axillary dissection. Ann Surg. 2004;239(6):859.CrossRef Fournier K, Schiller A, Perry RR, Laronga C. Micrometastasis in the sentinel lymph node of breast cancer does not mandate completion axillary dissection. Ann Surg. 2004;239(6):859.CrossRef
22.
go back to reference Lloyd P, Theophilidou E, Newcombe RG, Pugh L, Goyal A. Axillary tumour burden in women with a fine-needle aspiration/core biopsy-proven positive node on ultrasonography compared to women with a positive sentinel node. Br J Surg. 2017;104(13):1811–5.CrossRef Lloyd P, Theophilidou E, Newcombe RG, Pugh L, Goyal A. Axillary tumour burden in women with a fine-needle aspiration/core biopsy-proven positive node on ultrasonography compared to women with a positive sentinel node. Br J Surg. 2017;104(13):1811–5.CrossRef
23.
go back to reference Puri S, Sharma N, Newcombe RG, Kaushik M, Al-Attar M, Pascaline S, et al. Axillary tumour burden in women with one abnormal node on ultrasound compared to women with multiple abnormal nodes. Clin Radiol. 2018;73(4):391–5.CrossRef Puri S, Sharma N, Newcombe RG, Kaushik M, Al-Attar M, Pascaline S, et al. Axillary tumour burden in women with one abnormal node on ultrasound compared to women with multiple abnormal nodes. Clin Radiol. 2018;73(4):391–5.CrossRef
24.
go back to reference 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. J Clin Oncol. 2014;32(13):1365–83.CrossRef 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. J Clin Oncol. 2014;32(13):1365–83.CrossRef
25.
go back to reference 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(2):462–71.CrossRef 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(2):462–71.CrossRef
26.
go back to reference Cedolini C, Bertozzi S, Seriau L, Londero AP, Concina S, Cattin F, et al. Eight-year experience with the intraoperative frozen section examination of sentinel lymph node biopsy for breast cancer in a North-Italian university center. Int J Clin Exp Pathol. 2014;7(1):364.PubMed Cedolini C, Bertozzi S, Seriau L, Londero AP, Concina S, Cattin F, et al. Eight-year experience with the intraoperative frozen section examination of sentinel lymph node biopsy for breast cancer in a North-Italian university center. Int J Clin Exp Pathol. 2014;7(1):364.PubMed
27.
go back to reference 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(3):426.PubMedPubMedCentral 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(3):426.PubMedPubMedCentral
28.
go back to reference Gutierrez J, Dunn D, Bretzke M, Johnson E, O’Leary J, Stoller D, et al. Pathologic evaluation of axillary dissection specimens following unexpected identification of tumor within sentinel lymph nodes. Arch Pathol Lab Med. 2011;135(1):131–4.PubMed Gutierrez J, Dunn D, Bretzke M, Johnson E, O’Leary J, Stoller D, et al. Pathologic evaluation of axillary dissection specimens following unexpected identification of tumor within sentinel lymph nodes. Arch Pathol Lab Med. 2011;135(1):131–4.PubMed
29.
go back to reference Giuliano AE, Morrow M, Duggal S, Julian TB. Should ACOSOG Z0011 change practice with respect to axillary lymph node dissection for a positive sentinel lymph node biopsy in breast cancer? Clin Exp Metastasis. 2012;29(7):687–92.CrossRef Giuliano AE, Morrow M, Duggal S, Julian TB. Should ACOSOG Z0011 change practice with respect to axillary lymph node dissection for a positive sentinel lymph node biopsy in breast cancer? Clin Exp Metastasis. 2012;29(7):687–92.CrossRef
30.
go back to reference Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJH, Mansel RE, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15(12):1303–10.CrossRef Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJH, Mansel RE, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15(12):1303–10.CrossRef
31.
go back to reference Soares EWS, Nagai HM, Bredt LC, da Cunha AD, Andrade RJ, Soares GVS. Morbidity after conventional dissection of axillary lymph nodes in breast cancer patients. World J Surg Oncol. 2014;12(1):67.CrossRef Soares EWS, Nagai HM, Bredt LC, da Cunha AD, Andrade RJ, Soares GVS. Morbidity after conventional dissection of axillary lymph nodes in breast cancer patients. World J Surg Oncol. 2014;12(1):67.CrossRef
32.
go back to reference Purushotham AD, Upponi S, Klevesath MB, Bobrow L, Millar K, Myles JP, et al. Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol. 2005;23(19):4312–21.CrossRef Purushotham AD, Upponi S, Klevesath MB, Bobrow L, Millar K, Myles JP, et al. Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol. 2005;23(19):4312–21.CrossRef
Metadata
Title
Shortcomings of ultrasound-guided fine needle aspiration in the axillary management of women with breast cancer
Authors
Michel Attieh
Faek Jamali
Ghina Berjawi
Mothana Saadeldine
Fouad Boulos
Publication date
01-12-2019
Publisher
BioMed Central
Published in
World Journal of Surgical Oncology / Issue 1/2019
Electronic ISSN: 1477-7819
DOI
https://doi.org/10.1186/s12957-019-1753-y

Other articles of this Issue 1/2019

World Journal of Surgical Oncology 1/2019 Go to the issue