HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2463061463v1 246/1/81    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Koelliker, S. L. Articles by Cady, B. Search for Related Content PubMed PubMed Citation Articles by Koelliker, S. L. Articles by Cady, B.

Axillary Lymph Nodes: US-guided Fine-Needle Aspiration for Initial Staging of Breast Cancer—Correlation with Primary Tumor Size¹

¹ From the Department of Radiology, Women and Infants Hospital/Rhode Island Hospital, Brown Medical School, 593 Eddy St, Providence, RI 02903 (S.L.K., M.B.M.); Department of Surgery, Rhode Island Hospital, Brown Medical School, Providence, RI (M.A.C., B.C.); and Department of Pathology, Women and Infants Hospital, Brown Medical School, Providence, RI (M.M.S.). From the 2004 RSNA Annual Meeting. Received August 22, 2006; revision requested October 27; revision received December 14; accepted January 16, 2007; final version accepted April 9. Address correspondence to S.L.K. (e-mail: skoelliker{at}lifespan.org).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATION FOR PATIENT CARE... References

 
Purpose: To retrospectively assess the sensitivity and specificity of ultrasonographic (US)-guided fine-needle aspiration (FNA) of axillary lymph nodes for preoperative staging of breast cancer across a range of primary tumor sizes, by using histologic findings as a reference standard.

Materials and Methods: Institutional review board approval was obtained for this HIPAA-compliant study; informed consent was waived. US-guided FNA results in 74 patients with breast cancer (75 axillae) were compared with final pathologic results. Lymph nodes were classified as benign, indeterminate, or suspicious on the basis of US characteristics at retrospective review. US-guided FNA in the most suspicious node at US, or the largest node if all appeared benign, was performed. Final pathologic results (sentinel lymph node biopsy [SNB] or axillary lymph node dissection [ALND]) were compared with US and preoperative US-guided FNA results. Results were assessed according to tumor size. Sensitivity, specificity, and positive predictive value of US and US-guided FNA were calculated.

Results: Primary tumor sizes were 0.3–12 cm (mean, 3 cm). Patient age range was 31–81 years (mean age, 51 years). Sensitivity of US-guided FNA for predicting positive results at ALND or SNB was 71%–75%. Specificity was 100%. Sensitivity of US-guided FNA increased with primary tumor size.

Conclusion: US-guided FNA of axillary lymph nodes in patients with newly diagnosed breast cancer had a sensitivity that increased with increasing size of the primary tumor.

© RSNA, 2007

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATION FOR PATIENT CARE... References

 
Axillary lymph node staging remains the most important prognostic indicator of outcome in patients with breast cancer (1–3). Axillary lymph node dissection (ALND) remains the reference standard because it is the most conclusive method of evaluating the axilla, but it is associated with substantially increased morbidity (4). Sentinel node biopsy (SNB) offers an assessment technique in which only one or a few lymph nodes are removed to stage the axilla (5). When there is a negative finding at SNB, the axilla is usually presumed to be free of disease (6,7). However, when there is a positive finding, the patient most often undergoes full ALND to assess the number of lymph nodes involved to enable more complete staging and local control of disease. In many centers, SNB has replaced ALND for surgical evaluation of the axilla, with ALND reserved as a second procedure in patients with positive findings at SNB (5).

Ultrasonographic (US) evaluation of the axilla with US-guided fine-needle aspiration (FNA) has been shown to offer a means of nonsurgical staging of the axilla (8–14). Axillary lymph nodes are depicted at US, and the most suspicious lymph node is identified. FNA is guided by using US to sample the most suspicious area. The specimen is evaluated with cytologic examination. The procedure has almost no morbidity, is quick, and is minimally painful.

The addition of US-guided FNA to the evaluation of the axilla offers the benefit of nonsurgical detection of axillary metastases, and US-guided FNA is typically faster to perform, is more easily tolerated, and allows more rapid cytologic interpretation than a surgical procedure. When the US-guided FNA finding is negative, the patient undergoes SNB for further evaluation. However, when the US-guided FNA finding is positive, SNB can be omitted and the patient can undergo ALND (1–7), which minimizes the number of surgeries. In addition to its use in preoperative staging, US-guided FNA can be used to nonsurgically stage the axilla before neoadjuvant chemotherapy.

Despite the potential advantages of US-guided FNA, the procedure has not been widely adopted for initial axillary staging of breast cancer. Most previous studies have included either patients with abnormal lymph nodes at US (8,9) or only those with locally advanced breast cancer (10) and have revealed that US-guided FNA is a useful preoperative tool in these patients. Some authors (11) suggest that the procedure may be able to replace SNB as the initial staging procedure in larger tumors only, while others (12) suggest that US-guided FNA of axillary lymph nodes should be included in the preoperative staging of all primary breast cancers. Therefore, the indications for US-guided FNA of the axilla have not been clearly established. We previously demonstrated a high sensitivity and specificity of US-guided FNA in staging the axilla in patients with locally advanced breast cancer (tumors > 3 cm) (10). Thus, the objective of our current study was to retrospectively assess the sensitivity and specificity of US-guided FNA for preoperative staging of breast cancer across a range of primary tumor sizes, by using histologic findings as a reference standard.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATION FOR PATIENT CARE... References

 
Patients
Our study was a retrospective review of medical records of patients with breast cancer from the Women and Infants Hospital between January 1998 and April 30, 2003. The institutional review board approved the study. Informed consent from patients for participation was waived in this retrospective study. Health Insurance Portability and Accountability Act compliance was maintained. A total of 88 women (89 axillae), from among 607 patients with newly diagnosed breast cancer at the institution, were referred for US-guided FNA during the study period. One patient with bilateral breast cancer underwent bilateral US-guided FNA; for the purpose of data analysis, the two axillae were treated as independent observations. One patient was excluded because there was a delay of 18 months after US-guided FNA before ALND, at which point she had clinical progression of disease in the axilla. Thirteen additional patients were excluded because there were no final pathologic findings (at ALND or SNB) available. Therefore, a total of 74 women who underwent 75 US-guided FNAs comprised the group.

Between January 1998 and May 2001, there were 26 patients (27 axillae) with primary breast cancers greater than 3 cm in size whose results have been previously reported (10) and who were included in the current study. After May 2001, the criteria for US-guided FNA were expanded to include women with tumors smaller than 3 cm who were candidates to undergo SNB. Excluded from our study were women who did not undergo either SNB or ALND or who had a substantial delay between US-guided FNA and surgical staging. Patients with negative axillae at clinical examination and those with positive axillae at clinical examination were included in the study, but sufficient medical records were not available to detail the number of positive axillae at clinical examination in the patient population.

Surgical records and pathologic databases were reviewed by one author (S.L.K.) to determine the final pathologic stage based on either SNB or ALND findings. Data regarding patient age, primary tumor size, tumor histologic findings, and US-guided FNA cytologic results were obtained. Primary tumor size was obtained at histologic examination. The size criterion for T1 was 2 cm or smaller; for T2, larger than 2 cm and smaller than or equal to 5 cm; for T3, larger than 5 cm; and for T4, inflammatory carcinoma determined by using positive results at skin biopsy.

Image Review
For each patient, US images recorded at biopsy were retrospectively reviewed. One author (S.L.K., with 8 years of experience in breast imaging at the time of image review), a radiologist who was unaware of cytologic and pathologic results, retrospectively reviewed the images of the axillary lymph nodes and recorded the characteristics of the cortex and hilum of each visible lymph node (Table 1). Of the 75 US-guided FNAs performed, images from eight patients were not available for retrospective review. Therefore, there were 67 axillae in which the axillary lymph nodes were characterized with regard to the overall degree of suspicion for malignancy. A subjective overall assessment of benign, indeterminate, or malignant was made on the basis of a combination of characteristics (Table 1). Lymph nodes with a completely replaced or eccentric hilum were characterized as suspicious, those with discordant cortical and hilar features (eg, a central benign-appearing hilum but a thick or lobulated suspicious cortex) were considered indeterminate, and those with a thin cortex and central hilum were considered benign (Figs 1–3). Thin versus thick cortex was subjectively determined. A cortex with focal or asymmetric thickening was considered lobulated. A hypoechoic cortex was defined as one that was more hypoechoic than subcutaneous fat.

View larger version (143K): [in this window] [in a new window] [Download PPT slide]   Figure 1a: Sagittal US images of benign axillary lymph nodes. All were negative at US, US-guided FNA, and ALND or SNB. (a) Image of axillary lymph node (arrow) shows oval shape, thin cortex, and central fatty hilum. (b) Image of axillary lymph node demonstrates US-guided FNA, with tip of needle (arrow) in cortex.

View larger version (145K): [in this window] [in a new window] [Download PPT slide]   Figure 1b: Sagittal US images of benign axillary lymph nodes. All were negative at US, US-guided FNA, and ALND or SNB. (a) Image of axillary lymph node (arrow) shows oval shape, thin cortex, and central fatty hilum. (b) Image of axillary lymph node demonstrates US-guided FNA, with tip of needle (arrow) in cortex.

View larger version (143K): [in this window] [in a new window] [Download PPT slide]   Figure 2: Transverse US image of indeterminate axillary lymph node shows central fatty hilum (white arrow) and uniform, although slightly thickened, cortex (black arrows). Both cytologic findings at US-guided FNA and histologic findings at SNB were positive.

View larger version (146K): [in this window] [in a new window] [Download PPT slide]   Figure 3a: Transverse US images of malignant axillary lymph nodes, with positive findings at US, US-guided FNA, and ALDN or SNB. (a) Image shows eccentric fatty hilum (white arrow) and partially thickened cortex (black arrows). (b) Image shows lymph node with irregular shape and central, but deformed, fatty hilum (white arrows), with focally lobulated cortex (black arrows). (c) Image shows round lymph node (arrow) with fatty hilum completely replaced by tumor. (d) Image shows US-guided FNA technique, with tip of needle (arrow) in suspicious portion of cortex.

View larger version (134K): [in this window] [in a new window] [Download PPT slide]   Figure 3b: Transverse US images of malignant axillary lymph nodes, with positive findings at US, US-guided FNA, and ALDN or SNB. (a) Image shows eccentric fatty hilum (white arrow) and partially thickened cortex (black arrows). (b) Image shows lymph node with irregular shape and central, but deformed, fatty hilum (white arrows), with focally lobulated cortex (black arrows). (c) Image shows round lymph node (arrow) with fatty hilum completely replaced by tumor. (d) Image shows US-guided FNA technique, with tip of needle (arrow) in suspicious portion of cortex.

View larger version (164K): [in this window] [in a new window] [Download PPT slide]   Figure 3c: Transverse US images of malignant axillary lymph nodes, with positive findings at US, US-guided FNA, and ALDN or SNB. (a) Image shows eccentric fatty hilum (white arrow) and partially thickened cortex (black arrows). (b) Image shows lymph node with irregular shape and central, but deformed, fatty hilum (white arrows), with focally lobulated cortex (black arrows). (c) Image shows round lymph node (arrow) with fatty hilum completely replaced by tumor. (d) Image shows US-guided FNA technique, with tip of needle (arrow) in suspicious portion of cortex.

View larger version (166K): [in this window] [in a new window] [Download PPT slide]   Figure 3d: Transverse US images of malignant axillary lymph nodes, with positive findings at US, US-guided FNA, and ALDN or SNB. (a) Image shows eccentric fatty hilum (white arrow) and partially thickened cortex (black arrows). (b) Image shows lymph node with irregular shape and central, but deformed, fatty hilum (white arrows), with focally lobulated cortex (black arrows). (c) Image shows round lymph node (arrow) with fatty hilum completely replaced by tumor. (d) Image shows US-guided FNA technique, with tip of needle (arrow) in suspicious portion of cortex.

The most suspicious lymph node at US—that with the most replaced hilum—in the ipsilateral axilla was selected for aspiration by the same radiologist performing the procedure. In cases in which more than one node had a completely replaced hilum, the largest node was selected. If the lymph nodes appeared normal, the largest node was selected. Written informed consent was obtained for each procedure. No immediate postprocedural complications were recognized by the radiologists. All patients were seen by their referring surgeons within 1 week to obtain results; there were no reported complications.

US-guided FNA of lymph nodes was performed with a 22-gauge needle attached to a 10-mL syringe, with suction applied by using numerous short excursions in and out of the area being sampled. For suspicious lymph nodes, the needle was directed into multiple areas of the cortex. In patients with indeterminate nodes, the needle was directed into the thickest or focally thickened area of cortex. In patients with lymph nodes that appeared normal, the needle was directed into the immediate subcapsular cortex (the area first involved by metastatic tumor) in multiple areas throughout the node. Three samples were obtained from each node. The aspirate was placed in a solution (CytoLyt Solution; Cytyc, Boxborough, Mass) and sent to the cytology laboratory for processing. The sample was concentrated by using centrifugation (600g for 10 minutes). The supernatant was removed, and the pellet was resuspended in PreservCyt Solution (Cytyc). After sitting for 15 minutes, the sample was run on a ThinPrep 2000 Processor (Cytyc). The resulting slide was stained with Papanicolaou stain, covered with a coverslip, and evaluated by a pathologist (M.M.S.) with expertise in cytology and breast pathology. All specimens were processed after biopsy; in no cases were preliminary reports regarding specimen adequacy given by the pathologist during the biopsy procedure. Specimens were interpreted as follows: insufficient, no cellular material other than blood; negative, only normal cellular components present or a specific benign diagnosis; suspicious, atypical cells suspicious for malignancy; or malignant, definite malignant cells present (15).

Reference Standard
Lymph nodes obtained at SNB and ALND were examined by using standard hematoxylin-eosin–stained sections. For nodes obtained at SNB, five slides were obtained by sectioning at 200-µm intervals and were examined by using standard hematoxylin-eosin staining by the pathologist.

Statistical Analysis
Final surgical histopathologic findings at either ALND or SNB were used as the reference standard (positive vs negative finding for the presence of metastatic axillary nodal disease). Sensitivity, specificity, positive predictive value, and accuracy were calculated for US-guided FNA pathologic findings. Confidence intervals were calculated for sensitivities and specificities based on a 95% confidence level (16). Positive predictive values for radiologist-assessed pre–US-guided FNA US features and for overall assessment were calculated. Suspicious cytologic results were calculated as both positive and negative to yield a range of sensitivities, depending on how the procedure may be applied in practice. Insufficient cytologic results were considered negative. Radiologist assessment of US images with indeterminate results was considered positive, because in practice such lymph nodes would likely be considered for US-guided FNA; it is not recommended that in clinical practice one treat such a patient as having a positive axilla without cytologic or histologic confirmation. Results are presented for the entire sample and according to primary tumor size.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATION FOR PATIENT CARE... References

 
Women ranged in age from 31 to 81 years (mean age, 51 years). Mean primary breast cancer tumor size was 3 cm (range, 0.3–12 cm). There were 58 (77%) invasive ductal tumors, eight (11%) invasive lobular tumors, six (8%) mixed invasive lobular and ductal tumors, one (1%) tubular tumor, one (1%) extensive ductal carcinoma in situ tumor, and one (1%) inflammatory and mixed tumor.

Final Pathologic Findings
Of the 75 axillae included in the study, 51 (68%) were positive for metastatic carcinoma at SNB or ALND (Fig 4) (17). Lymph nodes were more likely to be positive for metastatic disease at surgical staging with increasing size of the primary tumor. US and US-guided FNA findings were more often positive as the primary tumor size increased (Table 2). Sensitivity of US-guided FNA increased with tumor size (Table 3). The prevalence of patients with positive axillae in our study (68%) was greater than the prevalence in the general population of patients (33.8%) with breast cancer at our institution during the same time frame (Table 4). Although patients with all sizes of tumors were referred for US-guided FNA, a greater percentage of patients with larger tumors (stage, higher than T1) were referred for US-guided FNA (Table 4).

View larger version (9K): [in this window] [in a new window] [Download PPT slide]   Figure 4: Flowchart shows results of US-guided FNA (USFNA) in patients with breast cancer.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATION FOR PATIENT CARE... References

 
Our results confirm that the larger the primary tumor, the more likely the patient is to benefit from US-guided FNA. US-guided FNA is more sensitive for detecting lymph node metastasis in patients with larger primary tumors because lymph node metastases tend to be larger in these cases. Six (50%) of 12 of our false-negative findings at US-guided FNA involved lymph nodes with small (<5 mm) metastatic foci, four of which were micrometastatic (<2 mm) foci. Sensitivity declined with smaller tumor size, although the specificity (100%) was excellent. We believe that because US-guided FNA is such a quick and easily tolerated procedure, a sensitivity of 56% in T1 lesions (<2 cm) is acceptable because half the patients with a positive axilla in this group would not have to undergo SNB; however, our study population had a prevalence of axillary disease of 50%, which was substantially higher than the prevalence in the general population of patients with T1 lesions at our institution during the study period (23.1%) (Table 4). Further evaluation with larger numbers of T1 lesions that would permit analysis of the subgroups of tumors in this category is needed to further investigate the benefits of US-guided FNA in this diverse population.

While lymph nodes that appeared abnormal at US were more likely to be positive at US-guided FNA, our results suggest a benefit to performing US-guided FNA in lymph nodes that appear normal at US, particularly in patients with a high likelihood of having nodal disease. Criteria used to distinguish benign from malignant lymph nodes include cortical thickness, contour, and echogenicity and the appearance of the hilum (18–22). The most predictive features of lymph node tumor involvement in our study were hypoechoic cortex, eccentric hilum, and completely replaced hilum. We found nodal size to be of limited value as a distinguishing feature. For axillary lymph nodes that appeared normal at US, it remains unclear which lymph node should be sampled. While we chose the largest node in this setting, the lymph node closest to the breast may most likely be the sentinel node (12) and may more appropriate for biopsy when nodes appear normal; our study was performed prior to the publication of those results. Sensitivity of US-guided FNA in lymph nodes that appear normal at US could be potentially even higher than we have reported if the lymph node closest to the breast is sampled.

By performing US-guided FNA in lymph nodes that were normal at US, we increased our rate of preoperative detection of axillary lymph node metastases by three cases (13.0% of benign-appearing axillae at US). The subjective nature of assessment of the US appearance of lymph nodes may further support the use of US-guided FNA in both normal- and abnormal-appearing axillae. This may prove more important with patients with larger tumors, who are more likely to have positive axillae. It may be less fruitful to perform US-guided FNA in an axilla that was normal at US when the chance of axillary nodal involvement is small, such as in patients with primary tumors of T1 size.

US-guided FNA is a well-tolerated, minimally invasive procedure. In staging the axilla of a patient with known carcinoma, a cytologic result positive for metastastic adenocarcinoma is sufficient to replace SNB and to proceed to ALND or neoadjuvant chemotherapy. While core biopsy of axillary lymph nodes (23,24) is an alternative to US-guided FNA, we demonstrated success with FNA, with only one (1%) patient of 75 with an insufficient sample. This may vary by institution on the basis of availability of experienced cytopathologists, as well as on the basis of specimen preparation technique. The ThinPrep cytologic preparation used has been shown to be superior to conventional preparations in nongynecologic cytologic evaluations, showing better overall quality and fewer insufficient samples (15). Because the specimens are collected directly into a fixative solution, the quality of the cell sample does not depend on the skill of the clinicians making the smears. Better preservation of cells in ThinPrep slides allows more definitive diagnosis of cases that are borderline between suspicious and malignant in conventional preparation slides. We believe that this technique, as well as the experienced cytopathologists at our institution, may account for our lower insufficiency rate than that obtained by others. While core biopsy is preferred for the evaluation of the primary tumor because of the histologic information (invasive vs in situ carcinoma) obtained, a positive cytologic result from a lymph node is indicative of metastatic tumor, and histologic evaluation is not necessary for diagnosis.

Our study was limited by the potential variability among the surgeons in their assessment of which patients to refer for US-guided FNA. Patients with large tumors and high-risk features comprise the majority of our population. Initially, the study included patients who were candidates for neoadjuvant chemotherapy on the basis of large primary tumor size. The study was later expanded to include patients with all tumor sizes, which accounts for the much smaller number of these patients referred. Only one group of surgeons at the institution was involved with the study, which accounts for the smaller number of patients enrolled from among all patients with tumors during the study period. There were no standard criteria used to guide patient selection for the procedure. There may be features of the primary tumor other than size, such as nuclear grade, receptor status, and lymphovascular invasion, that we did not evaluate in this study and may be taken into consideration when determining which patients would most benefit from US-guided FNA. A prospective study of all patients with breast cancer who are candidates for SNB or neoadjuvant chemotherapy is needed to further define the best role for US-guided FNA in the initial staging of the axilla.

In conclusion, US-guided FNA is useful in the initial axillary staging of breast cancer; the sensitivity of the technique increases with increasing tumor size.

	ADVANCES IN KNOWLEDGE

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATION FOR PATIENT CARE... References

 

• US fine-needle aspiration of axillary lymph nodes has a specificity of 100% (95% confidence interval: 89%, 100%).
  
• The sensitivity of US fine-needle aspiration increases with increasing tumor size, ranging from 56% for T1 tumors to 100% for T4 tumors.
  

	IMPLICATION FOR PATIENT CARE

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATION FOR PATIENT CARE... References

 

• US evaluation of the axilla coupled with fine-needle aspiration may offer nonsurgical staging of the axilla in patients with breast cancer.
  

	FOOTNOTES

 

Abbreviations: ALND = axillary lymph node dissection • FNA = fine-needle aspiration • SNB = sentinel lymph node biopsy

Author contributions: Guarantor of integrity of entire study, S.L.K.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, S.L.K., M.A.C., M.B.M.; clinical studies, S.L.K., M.A.C., M.M.S.; statistical analysis, S.L.K.; and manuscript editing, all authors

Authors stated no financial relationship to disclose.

	References

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION ADVANCES IN KNOWLEDGE IMPLICATION FOR PATIENT CARE... References

 

1. Merkel DE, Osborne CK. Prognostic factors in breast cancer. Hematol Oncol Clin North Am 1989;3(4):641–652.[Medline]
2. Tubiana-Hulin M, Le Doussal V, Hacene K, Rouesse J, Brunet M. Sequential identification of factors predicting distant relapse in breast cancer patients treated by conservative surgery. Cancer 1993;72(4):1261–1271.[CrossRef][Medline]
3. Hacene K, Le Doussal V, Rouesse J, Brunet M. Predicting distant metastases in operable breast cancer patients. Cancer 1990;66(9):2034–2043.[CrossRef][Medline]
4. Keshtgar MR, Baum M. Axillary dissection over the years: where to from here? World J Surg 2001;25(6):761–766.[CrossRef][Medline]
5. Grube BJ, Giuliano AE. The current role of sentinel node biopsy in the treatment of breast cancer. Adv Surg 2004;38:121–166.[Medline]
6. Jeruss JS, Winchester DJ, Sener SF, et al. Axillary recurrence after sentinel node biopsy. Ann Surg Oncol 2005;12(1):34–40.[Abstract/Free Full Text]
7. Smidt ML, Janssen CM, Kuster DM, Bruggink ED, Strobbe LJ. Axillary recurrence after a negative sentinel node biopsy for breast cancer: incidence and clinical significance. Ann Surg Oncol 2005;12(1):29–33.[Abstract/Free Full Text]
8. Krishnamurthy S, Sneige N, Bedi DG, 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.[CrossRef][Medline]
9. Sapino A, Cassoni P, Zanon F, et al. Ultrasonographically-guided fine-needle aspiration of axillary lymph nodes: role in breast cancer management. Br J Cancer 2003;88(5):702–706.[CrossRef][Medline]
10. Oruwari JU, Chung MA, Koelliker S, Steinhoff MM, Cady B. Axillary staging using ultrasound-guided fine needle aspiration biopsy in locally advanced breast cancer. Am J Surg 2002;184(4):307–309.[CrossRef][Medline]
11. de Kanter AY, van Eijck CH, van Geel AN, et al. Multicentre study of ultrasonographically guided axillary node biopsy in patients with breast cancer. Br J Surg 1999;86(11):1459–1462.[CrossRef][Medline]
12. 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(2):170–174.[CrossRef][Medline]
13. Bonnema J, van Geel AN, van Ooijen B, 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(3):270–274.[CrossRef][Medline]
14. 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(2):53–56.[CrossRef][Medline]
15. Leung CS, Chiu B, Bell V. Comparison of ThinPrep and conventional preparations: nongynecologic cytologic evaluation. Diagn Cytopathol 1997;16(4):368–371.[CrossRef][Medline]
16. Clopper CJ, Pearson ES. The use of confidence or fiducial limits illustrated in the case of the binomial. Biometrika 1934;26:404–413.[Free Full Text]
17. Bossuyt PM, Reitsma JB, Bruns DE, et al. Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD initiative. Radiology 2003;226(1):24–28.[Abstract/Free Full Text]
18. Tresserra F, Feu J, Grases PJ, Navarro B. Ultrasonographic detection of normal lymph nodes in patients with breast cancer. Br J Radiol 1999;72(860):827–828.[Medline]
19. Deurloo EE, Tanis PJ, Gilhuijs KG, 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(8):1068–1073.[CrossRef][Medline]
20. Lernevall A. Imaging of axillary lymph nodes. Acta Oncol 2000;39(3):277–281.[CrossRef][Medline]
21. Sato K, Tamaki K, Tsuda H, et al. Utility of axillary ultrasound examination to select breast cancer patients suited for optimal sentinel node biopsy. Am J Surg 2004;187(6):679–683.[CrossRef][Medline]
22. Bedrosian I, Bedi D, Kuerer HM, 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(9):1025–1030.[Abstract/Free Full Text]
23. Abdsaleh S, Azavedo E, Lindgren PG. Ultrasound-guided large needle core biopsy of the axilla. Acta Radiol 2004;45(2):193–196.[CrossRef][Medline]
24. Damera A, Evans AJ, Cornford EJ, et al. Diagnosis of axillary nodal metastases by ultrasound-guided core biopsy in primary operable breast cancer. Br J Cancer 2003;89(7):1310–1313.[CrossRef][Medline]

This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2463061463v1 246/1/81    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Koelliker, S. L. Articles by Cady, B. Search for Related Content PubMed PubMed Citation Articles by Koelliker, S. L. Articles by Cady, B.