The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience

metin, yavuz; Orhan Metin, Nurgul; TAŞÇI, Filiz; Kul, Sibel; KADIOĞLU, MAKSUDE ESRA; Gözükara, Melih Gaffar

doi:10.55730/1300-0144.5419

The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience

Filiz TAŞÇI, (Recep Tayyip Erdoğan Üniversitesi, Tıp Fakültesi, Radyoloji Anabilim Dalı, Rize, Türkiye)

Yavuz METİN, (Ankara Üniversitesi, Tıp Fakültesi, Radyoloji Anabilim Dalı, Ankara, Türkiye)

Nurgül ORHAN METİN, (Beytepe Murat Erdi Eker Devlet Hastanesi, Radyoloji Bölümü, Ankara, Türkiye)

Maksude Esra KADIOĞLU, (Trabzon Kanuni Eğitim ve Araştırma Hastanesi, Radyoloji Bölümü, Trabzon, Türkiye)

Melih Gaffar GÖZÜKARA, (Amasya Merkez Toplum Sağlığı Merkezi, Halk Sağlığı Müdürlüğü, Amasya, Türkiye)

Sibel KUL (Karadeniz Teknik Üniversitesi, Tıp Fakültesi, Radyoloji Anabilim Dalı, Trabzon, Türkiye)

Turkish Journal of Medical Sciences

1 0

Yıl: 2022 Cilt: 52 Sayı: 4 Sayfa Aralığı: 1160 - 1168 Metin Dili: İngilizce DOI: 10.55730/1300-0144.5419 İndeks Tarihi: 26-12-2022

The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience

Öz:

Background/aim: Assessing the validity and clinical utility of axillary ultrasonography (AUS)-guided fine needle aspiration biopsy (FNAB) in detection of nodal metastasis during preoperative axillary investigation in comparison to the histopathologic diagnosis in early-stage breast cancer. Materials and methods: A total of 279 operated primary breast cancer patients (age: 55.3 ± 12.8, ranged 17–90 years) were included. Data on AUS findings at the time of initial diagnosis (first look AUS), second-look AUS findings performed by the breast radiologist during breast biopsy procedure and the AUS-guided FNAB findings were evaluated with respect to the final histopathology report obtained through axillary surgery via sentinel lymph node biopsy (SLNB) and/or axillary lymph node dissection (ALND). The diagnostic performance of each method in detecting metastatic ALNs were compared in terms of sensitivity, specificity, accuracy, positive predictive value (PPV), and negative predictive value (NPV). Results: The sensitivity, specificity, and accuracy of the first look AUS in detecting nodal metastasis were 64.56%, 86.78%, and 74.19% while the PPV and NPV were 86.44% and 65.22%, respectively. The sensitivity, specificity, and accuracy of the second-look AUS were 70.25%, 87.60%, and 77.78%, while PPV and NPV were 88.10% and 69.28%, respectively. The sensitivity, specificity, and accuracy of the second-look AUS guided FNAB were 89.19%, 73.33%, and 87.30%, while the PPV and NPV were 96.12% and 47.83%, respectively. The consideration of second-look AUS and finding of nodal metastasis in FNAB was associated with significantly higher likelihood of ALND (55.4% vs. 44.6%, p < 0.001) and lower likelihood of SLNB (34.7% vs. 65.3%, p < 0.001) compared to consideration of nonmetastatic ALN status. In 23 (22.3%) patients with positive findings on AUS-guided FNAB, SLNB was applied; 21 had positive results after surgical dissection, indicating that nearly 20% of patients had unnecessary SLNB. Conclusion: US-guided FNAB of suspicious ALNs is a simple, minimally invasive, and highly effective method for preoperative axillary staging in patients with invasive breast cancer avoiding the more invasive method SLNB and it enables the surgeon to proceed directly to ALND in positive cases.

Anahtar Kelime: Axillary ultrasonography axillary dissection breast cancer fine needle aspiration biopsy sentinel lymph node biopsy

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık

1. Ecanow JS, Abe H, Newstead GM, Ecanow DB, Jeske JM. Axillary staging of breast cancer: what the radiologist should know. Radiographics 2013; 33 (6): 1589-1612. doi: 10.1148/ rg.336125060
2. 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. Radiologia Brasileria 2015; 48 (6): 345-352. doi: 10.1590/0100- 3984.2014.0121
3. Samphao S, Eremin JM, El-Sheemy M, Eremin O. Management of the axilla in women with breast cancer: current clinical practice and a new selective targeted approach. Annals of Surgical Oncology 2008; 15 (5): 1282-1296. doi: 10.1245/ s10434-008-9863-8
4. 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 (2): 210-214. doi: 10.1016/j. breast.2011.09.014
5. 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): 81–89. doi.org/10.1148/ radiol.2463061463
6. 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. American Journal of Roentgenology 2010; 195 (5): 1261–1267. doi: 10.2214/AJR.10.4414
7. Lyman GH, Giuliano AE, Somerfield MR, Benson AB, Bodurka DC et al. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. Journal of Clinical Oncology 2005; 23 (30): 7703–7720. doi: 10.1200/JCO.2005.08.001
8. Shah R, Rosso K, Nathanson SD. Pathogenesis, prevention, diagnosis and treatment of breast cancer. World Journal of Clinical Oncology 2014; 5 (3): 283-298. doi: 10.5306/wjco. v5.i3.283
9. Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP et al. Technical outcomes of sentinel-lymphnode resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncology 2007; 8 (10): 881–888. doi: 10.1016/S1470-2045(07)70278-4
10. Fayyaz MB, Niazi IK. Diagnostic accuracy of US-FNAC of axillary lymph nodes in patients with primary breast cancer using sentinel lymph node biopsy as standard reference. Journal of Ayub Medical College Abbottabad 2019; 31 (2): 242- 247.
11. Gurleyik G, Gurleyik E, Aktekin A, Aker F. Preoperative assessment of the axilla by surgeon performed ultrasound and cytology in patients with breast cancer. Journal of Clinical Medicine Research 2015; 7 (6): 440-445. doi: 10.14740/ jocmr2114w
12. 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. Annals of Surgical Oncology 2014; 21 (9): 2904-2910. doi: 10.1245/s10434-014-3674-x
13. Cardoso-Coelho LP, Borges RS, Alencar AP, Cardoso-Campos- Verdes LM, da Silva-Sampaio JP et al. Comparative study between ultrasound-guided fine needle aspiration cytology of axillary lymph nodes and sentinel lymph node histopathology in early-stage breast cancer. Oncology Letters 2017; 13 (5): 3299-3302. doi: 10.3892/ol.2017.5817
14. Boland MR, Prichard RS, Daskalova I, Lowery AJ, Evoy D et al. Axillary nodal burden in primary breast cancer patients with positive pre-operative ultrasound guided fine needle aspiration cytology: Management in the era of ACOSOG Z011. European Journal of Surgical Oncology 2015; 41 (4): 559-565. doi: 10.1016/j.ejso.2015.01.011
15. Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. Journal of the American Medical Association 2011; 305 (6): 569–575. doi: 10.1001/jama.2011.90
16. Marino MA, Avendano D, Zapata P, Riedl CC, Pinker K. Lymph Node Imaging in Patients with Primary Breast Cancer: Concurrent Diagnostic Tools. Oncologist 2020; 25 (2): 231- 242. doi: 10.1634/theoncologist.2019-0427
17. Akıncı M, Bulut SP, Erözgen F, Gürbüzel M, Gülşen G et al. Predictive value of fine needle aspiration biopsy of axillary lymph nodes in preoperative breast cancer staging. Ulus Cerrahi Dergisi 2016; 32 (3):191-196. doi: 10.5152/UCD.2015.2913
18. Fung AD, Collins JA, Campassi C, Ioffe OB, Staats PN. Performance characteristics of ultrasound-guided fine-needle aspiration of axillary lymph nodes for metastatic breast cancer employing rapid onsite evaluation of adequacy: analysis of 136 cases and review of the literature. Cancer Cytopathology 2014; 122 (4): 282-291. doi: 10.1002/cncy.21384
19. Black D. Axillary Ultrasound: For All, for None, to Diagnose Positive Nodes, or to Support Avoiding Sentinel Lymph Node Biopsy Altogether. Annals of Surgical Oncology 2017 ; 24 (1): 64-69. doi: 10.1245/s10434-016-5499-2
20. Leenders MW, Broeders M, Croese C, Richir MC, Go HLS 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): 578–583. doi: 10.1016/j.breast.2012.05.008
21. Khout H, Richardson C, Toghyan H, Fasih T. The role of combined assessment in preoperative axillary staging. Ochsner Journal 2013; 13 (4): 489-494.
22. Stachs A, Gode K, Hartmann S, Stengel B, Nierling U et al. Accuracy of axillary ultrasound in preoperative nodal staging of breast cancer – size of metastases as limiting factor. Springerplus 2013; 29 (2): 350. doi: 10.1186/2193-1801-2-350
23. Oz A, Demirkazik FB, Akpinar MG, Soygur I, Baykal A et al. Efficiency of ultrasound and ultrasound- guided fine needle aspiration cytology in preoperative assessment of axillary lymph node metastases in breast cancer. Journal of Breast Cancer 2012; 15 (2): 211-217. doi: 10.4048/jbc.2012.15.2.211
24. Hieken TJ, Trull BC, Boughey JC, Jones KN, Reynolds CA et al. Preoperative axillary imaging with percutaneous lymph node biopsy is valuable in the contemporary management of patients with breast cancer. Surgery 2013; 154 (4): 831-838. doi: 10.1016/j.surg.2013.07.017
25. Mills P, Sever A, Weeks J, Fish D, Jones S et al. Axillary ultrasound assessment in primary breast cancer: an audit of 653 cases. Breast Journal 2010; 16 (5): 460–463. doi: 10.1111/j.1524-4741.2010.00952.x
26. 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): 1807–1816. doi: 10.1148/rg.347130141
27. Rao R, Euhus D, Mayo HG, Balch C. Axillary node interventions in breast cancer: a systematic review. Journal of the American Medical Association 2013; 310 (13): 1385-94. doi: 10.1001/ jama.2013.277804
28. Diepstraten SC, Sever AR, Buckens CF, Veldhuis WB, van Dalen T 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. Annals of Surgical Oncology 2014; 21 (1): 51-59. doi: 10.1245/s10434-013-3229-6
29. Kuenen-Boumeester V, Menke-Pluymers M, de Kanter AY, Obdeijn IM, Urich D et al. Ultrasound-guided fine needle aspiration cytology of axillary lymph nodes in breast cancer patients. A preoperative staging procedure. European Journal of Cancer 2003; 39 (2): 170-174. doi: 10.1016/s0959- 8049(02)00501-4
30. Krishnamurthy S, Sneige N, Bedi DG, Edieken BS, Fornage BD et al. 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- 988. doi: 10.1002/cncr.10786
31. Manzoor MU, Bashir U, Irshad A, Yousaf I, Din NU et al. Role of Ultrasound and Ultrasound-Guided Fine-Needle Aspiration Cytology for Axillary Lymph Node Evaluation in Breast Cancer Patients: Correlation with Primary Tumor Size and Positive Lymph Node Number. Breast Care 2012; 7 (2): 403–406. doi: 10.1159/000343581
32. Alvarez S, Añorbe E, Alcorta P, López F, Alonso I et al. Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. American Journal of Roentgenology 2006; 186 (5): 1342–1348. doi: 10.2214/ AJR.05.0936
33. Abe H, Schmidt RA, Kulkarni K, Sennett CA, Mueller JS et al. 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 (1): 41–49. doi: 10.1148/radiol.2493071483
34. Lee B, Lim AK, Krell J, Satchithananda K, Coombes RC et al. The efficacy of axillary ultrasound in the detection of nodal metastasis in breast cancer. American Journal of Roentgenology 2013; 200 (3): 314-320. doi: 10.2214/AJR.12.9032
35. Houssami N, Turner RM. Staging the axilla in women with breast cancer: the utility of preoperative ultrasound-guided needle biopsy. Cancer Biology and Medicine 2014; 11 (2): 69- 77. doi: 10.7497/j.issn.2095-3941.2014.02.001
36. Mainiero MB. Regional lymph node staging in breast cancer: the increasing role of imaging and ultrasound-guided axillary lymph node fine needle aspiration. Radiologic Clinics of North America 2010; 48 (5): 989-997. doi: 10.1016/j.rcl.2010.06.010
37. Feng Y, Huang R, He Y, Lu A, Fan Z et al. Efficacy of physical examination, ultrasound, and ultrasound combined with fine- needle aspiration for axilla staging of primary breast cancer. Breast Cancer Research and Treatment 2015; 149 (3): 761–765. doi: 10.1007/s10549-015-3280-z
38. Houssami N, Ciatto S, Turner RM, Cody HS, Macaskill P. Preoperative ultrasoundguided needle biopsy of axillary nodes in invasive breast cancer: meta-analysis of its accuracy and utility in staging the axilla. Annals of Surgery 2011; 254 (2): 243-251. doi: 10.1097/SLA.0b013e31821f1564
39. Cools-Lartigue J, Meterissian S. Accuracy of axillary ultrasound in the diagnosis of nodal metastasis in invasive breast cancer: a review. World Journal of Surgery 2012; 36 (1): 46-54. doi:10.1007/s00268-011-1319-9
40. Fant JS, Grant MD, Knox SM, Livingston SA, Ridl K et al. Preliminary outcome analysis in patients with breast cancer and a positive sentinel lymph node who declined axillary dissection. Annals of Surgical Oncology 2003; 10 (2): 126-130. doi: 10.1245/aso.2003.04.022
41. Guenther JM, Hansen NM, Di Fronzo LA, Giuliano AE, Collins JC et al. Axillary dissection is not required for all patients with breast cancer and positive sentinel nodes. Archives of Surgery 2003; 138 (1): 52-56. doi: 10.1001/archsurg.138.1.52
42. Jeruss JS, Winchester DJ, Sener SF, Brinkmann EM, Bilimoria MM et al. Axillary recurrence after sentinel node biopsy. Annals of Surgical Oncology 2005; 12 (1): 34-40. doi: 10.1245/ ASO.2005.04.020
43. Naik AM, Fey J, Gemignani M, Heerdt A, Montgomery L et al. The risk of axillary relapse after sentinel lymph node biopsy for breast cancer is comparable with that of axillary lymph node dissection: a follow-up study of 4008 procedures. Annals of Surgery 2004; 240 (3): 462-468. doi: 10.1097/01. sla.0000137130.23530.19
44. Hwang RF, Gonzalez-Angulo AM, Yi M, Buchholz TA, Meric- Bernstam F et al. Low locoregional failure rates in selected breast cancer patients with tumor-positive sentinel lymph nodes who do not undergo completion axillary dissection. Cancer 2007; 110 (4): 723-730. doi: 10.1002/cncr.22847
45. Pyo JS, Jung J, Lee SG, Kim NY, Kang DW. Diagnostic Accuracy of Fine-Needle Aspiration Cytology and Core-Needle Biopsy in the Assessment of the Axillary Lymph Nodes in Breast Cancer-A Meta-Analysis. Diagnostics (Basel) 2020; 10 (9): 717-729. doi: 10.3390/diagnostics10090717
46. Attieh M, Jamali F, Berjawi G, Saadeldine M, Boulos F. Shortcomings of ultrasound-guided fine needle aspiration in the axillary management of women with breast cancer. World Journal of Surgical Oncology 2019; 17 (1): 208-214. doi: 10.1186/s12957-019-1753-y
47. Davis JT, Brill YM, Simmons S, Sachleben BC, Cibull ML et al. Ultrasound-guided fine-needle aspiration of clinically negative lymph nodes versus sentinel node mapping in patients at high risk for axillary metastasis. Annals of Surgical Oncology 2006; 13 (12): 1545–1552. doi: 10.1245/s10434-006-9095-8
48. Van Rijk MC, Deurloo EE, Nieweg OE, Gilhuijs KG, Peterse JL et al. Ultrasonography and fine-needle aspiration cytology can spare breast cancer patients unnecessary sentinel lymph node biopsy. Annals of Surgical Oncology 2006; 13 (1): 31-35. doi:10.1245/ASO.2005.01.024

APA	TAŞÇI F, metin y, Orhan Metin N, KADIOĞLU M, Gözükara M, Kul S (2022). The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. , 1160 - 1168. 10.55730/1300-0144.5419
Chicago	TAŞÇI Filiz,metin yavuz,Orhan Metin Nurgul,KADIOĞLU MAKSUDE ESRA,Gözükara Melih Gaffar,Kul Sibel The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. (2022): 1160 - 1168. 10.55730/1300-0144.5419
MLA	TAŞÇI Filiz,metin yavuz,Orhan Metin Nurgul,KADIOĞLU MAKSUDE ESRA,Gözükara Melih Gaffar,Kul Sibel The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. , 2022, ss.1160 - 1168. 10.55730/1300-0144.5419
AMA	TAŞÇI F,metin y,Orhan Metin N,KADIOĞLU M,Gözükara M,Kul S The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. . 2022; 1160 - 1168. 10.55730/1300-0144.5419
Vancouver	TAŞÇI F,metin y,Orhan Metin N,KADIOĞLU M,Gözükara M,Kul S The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. . 2022; 1160 - 1168. 10.55730/1300-0144.5419
IEEE	TAŞÇI F,metin y,Orhan Metin N,KADIOĞLU M,Gözükara M,Kul S "The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience." , ss.1160 - 1168, 2022. 10.55730/1300-0144.5419
ISNAD	TAŞÇI, Filiz vd. "The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience". (2022), 1160-1168. https://doi.org/10.55730/1300-0144.5419

APA	TAŞÇI F, metin y, Orhan Metin N, KADIOĞLU M, Gözükara M, Kul S (2022). The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. Turkish Journal of Medical Sciences, 52(4), 1160 - 1168. 10.55730/1300-0144.5419
Chicago	TAŞÇI Filiz,metin yavuz,Orhan Metin Nurgul,KADIOĞLU MAKSUDE ESRA,Gözükara Melih Gaffar,Kul Sibel The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. Turkish Journal of Medical Sciences 52, no.4 (2022): 1160 - 1168. 10.55730/1300-0144.5419
MLA	TAŞÇI Filiz,metin yavuz,Orhan Metin Nurgul,KADIOĞLU MAKSUDE ESRA,Gözükara Melih Gaffar,Kul Sibel The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. Turkish Journal of Medical Sciences, vol.52, no.4, 2022, ss.1160 - 1168. 10.55730/1300-0144.5419
AMA	TAŞÇI F,metin y,Orhan Metin N,KADIOĞLU M,Gözükara M,Kul S The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. Turkish Journal of Medical Sciences. 2022; 52(4): 1160 - 1168. 10.55730/1300-0144.5419
Vancouver	TAŞÇI F,metin y,Orhan Metin N,KADIOĞLU M,Gözükara M,Kul S The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience. Turkish Journal of Medical Sciences. 2022; 52(4): 1160 - 1168. 10.55730/1300-0144.5419
IEEE	TAŞÇI F,metin y,Orhan Metin N,KADIOĞLU M,Gözükara M,Kul S "The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience." Turkish Journal of Medical Sciences, 52, ss.1160 - 1168, 2022. 10.55730/1300-0144.5419
ISNAD	TAŞÇI, Filiz vd. "The validity and clinical utility of axillary ultrasonography-guided fine needle aspiration biopsy in detection of nodal metastasis in early-stage breast cancer patients: a retrospective single-center experience". Turkish Journal of Medical Sciences 52/4 (2022), 1160-1168. https://doi.org/10.55730/1300-0144.5419