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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2003.12.017 on October 13, 2003

Annals of Surgical Oncology 10:1025-1030 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Impact of Clinicopathological Factors on Sensitivity of Axillary Ultrasonography in the Detection of Axillary Nodal Metastases in Patients With Breast Cancer

Isabelle Bedrosian, MD, Deepak Bedi, MD, Henry M. Kuerer, MD, PhD, Bruno D. Fornage, MD, Lori Harker, PA-C, Merrick I. Ross, MD, Frederick C. Ames, MD, Savitri Krishnamurthy, MD, Beth S. Edeiken-Monroe, MD, Funda Meric, MD, Barry W. Feig, MD, Jeri Akins, MPAS, PA-C, S. Eva Singletary, MD, Nadeem Q. Mirza, MD, MPH and Kelly K. Hunt, MD

From the Departments of Surgical Oncology (IB, HMK, LH, MIR, FCA, FM, BWF, JA, SES, NQM, KKH), Radiology (DB, BDF, BSE), and Pathology (SK), The University of Texas M. D. Anderson Cancer Center, Houston, Texas.

Correspondence: Address correspondence and reprint requests to: Kelly K. Hunt, MD, Associate Professor and Chief, Surgical Breast Section, Department of Surgical Oncology, Box 444, M. D. Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030; Fax: 713-792-4689; E-mail: khunt{at}mdanderson.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Ultrasonography and fine-needle aspiration (FNA) are used to evaluate the breast and regional nodes in breast cancer patients. We sought to identify factors influencing the sensitivity of ultrasonography for detection of nodal metastasis.

Methods: Patients with a clinically negative axilla who underwent axillary ultrasonography and sentinel lymph node biopsy were included.

Results: Of 208 patients, axillary ultrasonography was negative in 180 (86%) and suspicious or indeterminate in 28 (14%). FNA was performed in 22 patients whose findings were indeterminate or suspicious, and 3 were positive for malignancy. Final pathological examinations revealed positive nodes in 53 patients: 39 (22%) of 180 with negative ultrasonographic findings and 14 (50%) of 28 with indeterminate or suspicious ultrasonographic findings (P = .001). Excisional biopsy was more common for patients with indeterminate or suspicious findings on preoperative ultrasonography (P = .038). There were no significant differences in tumor size, histological features, size of nodal metastasis, or number of positive nodes between patients whose ultrasonography findings were negative and those whose findings were indeterminate or suspicious.

Conclusions: Ultrasonographically suggested nodal metastasis is associated with the finding of nodal disease on final pathological examination. No significant clinicopathologic criteria were found to impact sensitivity of ultrasonography; however, excisional biopsy for diagnosis may be a confounding variable in subsequent axillary ultrasonography.

Key Words: Axillary lymph nodes • Breast cancer • Metastasis • Ultrasonography


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Axillary ultrasonography is increasingly being used to improve the staging of breast cancer patients who have negative axillary lymph nodes on physical examination.1,2 This approach has a number of advantages. First, node-positive patients identified with ultrasonography can be referred for axillary dissection, without the need for sentinel lymph node (SLN) staging.2 Second, some series have indicated a risk of severe systemic reactions to the Lymphazurin blue dye used in SLN mapping.3,4 Although this risk is quite small, avoiding the use of SLN mapping in patients known to have axillary metastases will minimize exposure to this hazard. Most significantly, patients identified preoperatively as harboring nodal disease may be considered for enrollment in neoadjuvant chemotherapy protocols.1,5

The sensitivity of ultrasonography in the detection of nodal metastasis in breast cancer ranges from 50% to 87%, depending on the specific criteria used to define suspicious nodes on sonography.6–8 Studies showing a higher sensitivity generally also show a lower specificity (approximately 50%).7 High-resolution and Doppler ultrasonography have been reported to be both more sensitive and more specific than standard ultrasonography in the detection of axillary metastases, with sensitivities ranging from 70% to 84% and specificity of 98%.9,10 The addition of ultrasonography-guided fine-needle aspiration (FNA) biopsy has also been reported to increase the sensitivity of preoperative nodal staging to approximately 80% and the specificity to 100%.7

Although ultrasound technology and the criteria for determination of nodal metastasis are becoming refined, less is known about how various clinical and histological criteria may influence the diagnostic utility of preoperative ultrasonography of the axilla. We sought to identify clinical and histopathological factors affecting the sensitivity of ultrasonography in the detection of nodal metastasis in patients without palpable axillary adenopathy.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patient Population and Clinicopathological Features
Using our lymphatic mapping database, we identified and reviewed the records of patients with clinically negative axillary nodes who underwent preoperative axillary ultrasonography followed by SLN biopsy at our institution between February 1994 and May 2000. Patients who had received preoperative chemotherapy were excluded from the review. Approval for the study was obtained from the M. D. Anderson Cancer Center Institutional Review Board.

The following clinicopathological features were examined: method of diagnosis of breast cancer (FNA, core, or excisional biopsy), tumor size, histological characteristics, number of positive nodes, and size of nodal metastasis (<=5 mm or >5 mm).

Examination of the Axilla
Clinical and ultrasonographic examinations of the ipsilateral axilla were performed when patients presented to The M. D. Anderson Cancer Center. Axillary ultrasonography was performed by a radiologist with use of 7.5–12-mHz transducers. The ultrasonographic examination was considered positive for metastasis if one of the following criteria was satisfied: (1) eccentric cortical enlargement or lobulation, with displacement of fatty hilum, (2) hypoechoic echotexture, or (3) round or ovoid nodes.11 Ultrasound-guided FNA was performed for pathological confirmation if findings on ultrasonography were judged suspicious for malignancy. When findings on ultrasonography were judged indeterminate, FNA was performed at the radiologist’s discretion.

Pathological Evaluation of the Axilla
All patients underwent SLN dissection as part of their surgical procedure. SLNs were identified in 195 of the 205 patients (95%). SLNs were processed by sectioning the node along the short axis at 2–3-mm intervals. Sections were then submitted entirely in cassettes, and three deeper levels were cut from each block. Immunohistochemistry was used to confirm suspicious cells identified on serial sectioning. Patients with positive SLNs were offered level I and II axillary dissection. Level III nodes were removed only if they appeared clinically involved at the time of surgery. Non-SLNs were evaluated by means of standard pathological techniques; serial sectioning and immunohistochemical analysis were not performed. For statistical analysis, the size of the metastatic focus in the lymph node was calculated as the maximum diameter of the largest single deposit.

Statistical Methods
The SPSS 10.1 software package (SPSS Inc., Chicago, IL) was used for statistical analysis. Descriptive statistics were used to assess the frequency distribution among the study population. Differences in the distribution of characteristics between groups were determined with the Pearson {chi}2 test or Fisher’s exact test. P values of less than or equal to .05 were considered to be statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient and Tumor Characteristics
Of the 513 patients prospectively enrolled in our SLN biopsy database between February 1994 and May 2000, 301 had undergone preoperative ultrasonography of the axilla. Ninety-three patients were excluded from the current study because they had received neoadjuvant chemotherapy, leaving 208 patients for this analysis. Patient and tumor characteristics are listed in Table 1. The majority of patients presented with T1 tumors. The tumors in almost half of the patients were diagnosed by core needle biopsy, and the majority of the patients underwent breast surgery within 1 month of their preoperative ultrasonographic evaluation. The overall incidence of pathologically confirmed nodal disease in the cohort was 25% (Table 1). From patients who underwent completion axillary dissection (n = 134), the average number of lymph nodes recovered was 19.


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  		TABLE 1. Patient and tumor characteristics (n = 208)
 
Findings on Axillary Ultrasonography and FNA
Axillary ultrasonographic findings were reported as negative for 180 patients, suspicious for malignancy for 6, and indeterminate for 22 (Fig. 1). Twenty-two of the 28 patients with suspicious or indeterminate axillary lymph nodes on ultrasonography underwent FNA. The six patients not evaluated with FNA had indeterminate axillary ultrasonographic findings. In three patients, the FNA demonstrated the presence of malignant cells; in the remaining 19 patients, the FNA findings were negative for malignancy.



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  		FIG. 1. Findings on ipsilateral axillary ultrasonography (US) and fine-needle aspiration (FNA) in 208 patients with breast cancer for whom physical examination of the axilla was negative.

 
Concordance Between Findings of Axillary Ultrasonography and FNA and Findings on Final Pathological Evaluation of the Axilla
Fifty-three patients (25%) had positive axillary lymph nodes on final histological examination of the axilla. Of these 53 patients, three had metastasis diagnosed before surgery by means of ultrasonography-guided FNA biopsy. In the remaining 50 patients, findings on ultrasonography and FNA and findings on final pathological evaluation of the axilla were discordant. Among these 50 patients, the nodes of 11 had an indeterminate or suspicious sonographic appearance on preoperative axillary ultrasonography. Nine of these patients underwent FNA, and findings on FNA were negative for malignancy in all nine cases. Patients with indeterminate or suspicious findings on axillary ultrasonography were more likely to have nodal metastasis at final pathological assessment, regardless of findings on FNA, than were patients who had benign axillary ultrasonography findings (50% [14 of 28] vs. 22% [39 of 180]; P = .001) (Table 2). The sensitivity and specificity of ultrasonography with selective FNA biopsy were 25% and 100%, respectively (Table 3).


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  		TABLE 2. Concordance between axillary ultrasound findings and pathologic nodal status
 

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  		TABLE 3. Concordance between axillary ultrasound with FNA and pathologic nodal status
 
Correlation Between Clinicopathological Factors and Suspicious or Indeterminate Findings of Axillary Ultrasonography
We examined the cohort of 53 node-positive patients to determine whether certain clinical or pathological parameters affected the sensitivity of ultrasonography in the detection of nodal metastasis. Clinical criteria included tumor size and method of diagnostic biopsy. Pathological factors assessed were histological tumor type and surrogate markers of axillary tumor burden: number of positive nodes and size of largest nodal metastatic deposit. Of these clinical and pathological determinants, only initial excisional breast biopsy for diagnosis was a significant determinant of ultrasonographic detection of metastatic disease in the axilla (P = .038; Table 4).


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  		TABLE 4. Impact of clinical and pathologic factors on the sensitivity of preoperative axillary US in the detection of nodal metastases
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Preoperative image-guided staging of the axillary nodal basin is increasingly being performed in clinically node-negative breast cancer patients. Accurate imaging of the axilla is important for pretreatment staging of patients enrolled in neoadjuvant protocols.1,5 In addition, preoperative imaging may be applied more generally to patients with early-stage operable breast cancer to identify those with node-positive disease who can subsequently undergo a single operative intervention, without the need for sentinel node biopsy. Intraoperative assessment of SLNs with frozen-section or touch-preparation examination has not been consistently reliable, and 5% to 50% of patients still require a second operative procedure to complete axillary nodal clearance.12–17 Image-guided preoperative identification of nodal metastases without the additional step of SLN biopsy may save operative time and increase cost-effectiveness.

Many studies have documented clinical examination to be unreliable for staging the axilla in breast cancer patients.18–19 Therefore, multiple imaging modalities have been evaluated as alternatives to clinical examination of the axilla.20–21 In the detection of nodal metastases, positron emission tomography, computed tomography, magnetic resonance imaging, 99mTc sestamibi imaging, and immunoscintigraphy all have accuracy equal to or less than that of high-resolution ultrasonography of the axilla.20–21 The relative ease of cytological evaluation of suspicious-appearing nodes with ultrasonography-guided FNA provides an additional advantage to this modality. Ultrasonography has therefore become the primary imaging technique for determining the status of the regional nodal basins in patients with breast cancer.

The accuracy of preoperative ultrasonographic diagnosis of nodal metastasis has improved with the development of high-frequency ultrasonography technology, the addition of FNA techniques, and better definition of the ultrasonographic criteria for diagnosis of malignancy.11,22 Recent series involving the use of high-resolution ultrasonography with or without FNA have shown sensitivity ranging from 50% to 92%, specificity ranging from 90% to 100%, and accuracy ranging from 76% to 92%.7,8,10,23,24 A number of investigators have evaluated preoperative axillary ultrasonography as a management tool. Bonnema et al.7 found that ultrasonography combined with cytological evaluation identified metastatic disease in the axilla in 26% of the patients studied. Similarly, in a multicenter trial of 185 patients without clinically palpable adenopathy, de Kanter and colleagues2 found that 17% of patients had nodal metastasis diagnosed preoperatively by means of combined ultrasonography and FNA and therefore avoided the extra procedure of SLN biopsy for staging.

Despite the increasing use of preoperative ultrasonography for axillary staging, there are few data regarding the clinical and pathological criteria that influence the sensitivity of ultrasonography for the diagnosis of axillary nodal metastasis. In their multicenter study, de Kanter et al.2 found that ultrasonography plus FNA was more sensitive in the detection of metastasis in patients with larger (>=T2) tumors and in patients who had multiple positive nodes on final pathological evaluation. Similarly, Krishnamurthy et al.25 recently demonstrated that ultrasonography-guided FNA was 100% sensitive in detection of metastasis in the axilla if more than three nodes were involved with disease, and it was 93% sensitive for detection of tumor metastasis greater than 5 mm in size. In our study, these parameters did not appear to influence findings on ultrasonography and FNA, but patients who had obvious nodal metastasis on the basis of ultrasonography had already been excluded from the study population. In the current study, an excisional biopsy for diagnosis of breast cancer did appear to be a confounding variable in subsequent ultrasonographic evaluation of the axilla.

The differences between these studies may be related to sample size and specific cohort selection criteria. In our study, in order to minimize the potential confounding effect of neoadjuvant therapy,25 patients with FNA-proven metastasis referred for preoperative chemotherapy were not included in the analysis. This selection bias, however, may account for the disparity between the findings of our study and of those previously reported and precludes an accurate assessment of the true sensitivity of ultrasonography. In addition, the overall number of nodes visualized in the axilla has been shown to be an important factor determining the likelihood of detection of axillary nodal metastases. Although the number of visualized nodes was not available for this review, the failure to technically assess the axilla may also account for discrepancies noted between our study and others.

Our data confirm the high rate of false-negative results previously reported for ultrasonography-guided FNA,2,8 particularly when few nodes are involved or only micrometastatic disease is present. In our series, the sensitivity of ultrasonography-guided FNA was 25%, and the specificity was 100%. Our findings are in agreement with those of two previous studies, in which the reported sensitivities of ultrasonography-guided FNA were 18%8 and 36%,2 but our findings conflict with those of another previous study that showed a sensitivity of 80%.7 The reason for this discrepancy is not clear and does not appear to be related to differences in cohorts, incidence of nodal disease, or techniques for FNA. Technical limitations and sampling error remain significant problems, making it difficult to accurately diagnose small-volume axillary nodal metastasis.

In addition, for the current study, we examined only patients who had undergone SLN biopsy because they were believed to be node-negative on the basis of the initial screening. It was our goal to determine how many of these patients whose ultrasonographic findings were indeterminate proved to have metastasis. In our series, two of three ultrasonography-negative patients with nodal disease had metastatic foci smaller than 5 mm.

In summary, the combination of ultrasonography and FNA of the axillary lymph nodes is a useful approach for staging of the axilla. Despite negative findings on FNA, nodes that were suspicious or indeterminate on preoperative axillary ultrasonography were more likely to contain metastases on the final pathological evaluation than were nodes with a benign appearance on ultrasonography. Excisional biopsy before axillary ultrasonography may be a confounding variable for accurate ultrasonography staging. Tumor size, histological features, and nodal tumor burden did not appear to influence the sensitivity of ultrasonography in the detection of metastasis. Further study is required to better assess additional factors that may alter nodal architecture responsible for ultrasonographic findings indicative of metastasis.


   FOOTNOTES
 
Suspicion of axillary nodal metastasis due to ultrasonographic findings in breast cancer patients is associated with pathologically positive nodes, despite negative ultrasonography-guided FNA findings. Tumor size and extent of nodal metastasis did not affect the sensitivity of ultrasonography for detection of nodal disease.

Received for publication December 19, 2002. Accepted for publication July 11, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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