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In Vitro High-Resolution Helical CT of Small Axillary Lymph Nodes in Patients with Breast Cancer

Correlation of CT and Histology

¹ Department of Radiology, Niigata Cancer Center Hospital, 2-15-3, Niigatashi, Kawagishicho, Niigata 951-8566, Japan.
² Department of Surgery, Niigata Cancer Center Hospital, Niigata 951-8566, Japan.
³ Department of Pathology, Niigata Cancer Center Hospital, Niigata 951-8566, Japan.

Received June 20, 2000; accepted after revision September 15, 2000.

 
Address correspondence to T. Uematsu.

Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
OBJECTIVE. This study seeks to determine whether high-resolution in vitro helical CT can show the internal structure of small axillary nodes and to establish the CT characteristics of benign versus metastatic axillary nodes in patients with breast cancer.

SUBJECTS AND METHODS. We obtained in vitro helical CT images of 212 nodes excised from 19 patients with breast cancer. The longest mean size was 5.9 mm, and the range was 0.5 to 26.5 mm. The hilar and cortical characteristics, the size, and the ratio of the longest axis to the shortest axis were evaluated. CT findings were correlated with histologic findings.

RESULTS. Pathologic assessment of excised nodes with a central low-density hilum visualized on CT showed arteries, veins, lymphatic sinuses, and fatty tissue. A peripheral high-density cortex on CT contained mostly lymphatic tissue. Abnormal (eccentric, irregular) cortices were observed in malignant nodes (p<0.0001). Marked differences were observed among the proportions of benign and malignant nodes when the ratio of the longest axis to the shortest axis was less than 2 and an abnormal cortex was observed. CT could also detect extracapsular lymph node extension.

CONCLUSION. In vitro high-resolution helical CT can detect the internal structure of small nodes. Morphologic changes detected on helical CT help distinguish benign from malignant nodes.

Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Axillary lymph node status is one of the most important prognostic factors in breast cancer and is of particular value in choosing adjuvant therapy [1,2,3,4,5]. Important prognostic information is gained from histopathologic examination of axillary nodes dissected by surgeons, and axillary lymph node dissection is part of the standard treatment of breast cancer [3]. Axillary lymph node dissection also assures regional tumor control and improves survival [4,5]. However, axillary lymph node dissection has exposed many patients without nodal involvement to the unnecessary morbidity associated with the procedure [3, 6]. Therefore, if a noninvasive diagnostic modality could provide accurate preoperative axillary lymph node status, axillary lymph node dissection could be avoided in patients without nodal involvement. Physical examination has been the most common method used to determine the involvement of axillary lymph nodes; however, the predictive value is limited [1]. Multiple imaging modalities that have been used to assess axillary lymph nodes include mammography [7, 8], sonography [9, 10], CT [11, 12], lymphography [13], nuclear scintigraphy [14, 15], MR imaging [16], and positron emission tomography [17]. In all cases, to be of value for clinical decision making, the accuracy of any imaging modality must closely approach that of histopathology.

Conventional CT is not an accurate predictor of axillary metastases because of its low negative predictive value, and nodal size alone has been shown to be an unreliable criterion for differentiation of benign from malignant nodes [11]. However, helical CT has a number of important potential advantages compared with conventional CT, including improved lesion detection, improved lesion densitometry, optimization of enhancement with IV contrast material, and improved multiplanar and three-dimensional (3D) reconstructions [18].

This prospective in vitro study of helical CT in small axillary lymph nodes in patients with breast cancer has been performed to determine whether high-resolution and 3D helical CT images can show the internal structure of the axillary nodes and to establish the CT characteristics of benign versus metastatic axillary nodes.

Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
We obtained in vitro helical CT images of 212 nodes excised from 19 patients (age range, 32-78 years; mean age, 49.7 years) with breast cancer. The clinical N stages in our series were N0 (n=18) and N1 (n=1). Thirteen patients had T1 lesions and six had T2 lesions. The pathologic type was ductal carcinoma in 18 patients and mucinous carcinoma in one. The 212 fresh axillary lymph nodes were numbered separately after dissection (levels I and II nodes) by the same surgeon and placed in a partitioned case filled with saline (Fig. 1). The identified nodes were immediately transferred to the radiology department. The nodes were wrapped in commercially available plastic wrap and were placed in a small acrylic bead bath (Fig. 2A,2B). The acrylic bead bath consisted of a 24 x 16 x 14.5 cm commercially available expanded rigid polystyrene plastic box filled with a large number of acrylic beads and conformed to in vivo conditions while CT was performed. The numbered nodes were returned to the case and sent to the pathology department.

View larger version (145K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. —Photograph shows partitioned case filled with saline. Lymph nodes are put into case and numbered.

View larger version (102K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —Acrylic beads and small acrylic bead bath. Photograph shows commercially available acrylic beads about 4 mm in diameter.

View larger version (58K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —Acrylic beads and small acrylic bead bath. Drawing shows small bath of acrylic beads (white) with lymph nodes (black) inserted.

Helical CT was performed with a ProSpeed SA Libra scanner (General Electric Yokogawa Medical Systems, Tokyo, Japan) using the following technical parameters: image matrix, 512 x 512; field of view, 13-26 cm; 120 kVp; 250 mA; X-ray beam thickness, 3 mm; table speed, 3 mm/0.8 sec; pitch, 1:1. Images were reconstructed using a soft-reconstruction kernel at 1.5-mm intervals. The ranges of the appropriate window level and width settings were 400 and 40 H, respectively.

All helical CT images of the nodes were assessed prospectively by the same radiologist without knowledge of the histopathologic findings.

The three morphologic features evaluated on CT were central low-density hilum, peripheral high-density cortex, and lymph node shape. The hilum was assessed, and the nodes were separated into two hilar classes: presence and absence. The peripheral cortex was assessed, and the nodes were separated into four cortical classes: normal, concentric, eccentric, and irregular (Fig. 3). Normal cortex was defined as a high-density C-shaped rim measuring less than 2 mm around a central low-density hilum. Concentric cortex was defined as a high-density rim measuring greater than 2 mm when the low-density hilum (when present) lay in the center of the node. Eccentric cortex was defined as a high-density rim measuring greater than 2 mm when the low-density hilum (when present) did not lie in the center of the node but was placed to one side in any plane. Irregular cortex occurred when the shape of the low-density hilum (when present) no longer conformed to the overall shape of the lymph node, and the hilum was indented or flattened. If the nodal hilum—the reference structure—was absent, cortical width could not be assessed.

View larger version (5K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —Drawing shows cortical rim morphology on high-resolution helical CT. From top to bottom: normal cortex (<2 mm), concentric cortex (2 mm), eccentric cortex, and irregular cortex.

Lymph node shape was assessed by measuring the longest and shortest diameters on the 3D helical CT image and by calculating their ratio. Extracapsular invasion was determined on CT images when there was increased density and stranding of perinodal fat.

After the CT study, each lymph node was sectioned in the largest plane, divided into two blocks, and stained with H and E. At histopathologic examination, the presence of metastasis, extracapsular invasion, and other morphologic characteristics of the cortex and medulla were coded. Histopathologic findings were correlated with the CT findings.

The sensitivity and specificity of different criteria were calculated. The significance of the differences between the results obtained for the three groups was assessed using the unpaired t test.

Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Number of Positive Nodes
The mean number of nodes examined from 19 patients was 11 (range, 5-25 nodes). Of the 212 lymph nodes examined, 42 nodes from eight patients contained metastasis. The number of metastatic nodes in the positive levels I and II axillary dissections ranged from one to 18 (mean, 5 nodes). Three of 42 metastatic nodes contained micrometastasis.

Nodal Hilum
Pathologic assessment of excised nodes with a central low-density hilum seen on CT showed arteries, veins, lymphatic sinuses, and fatty tissue. Of 170 benign lymph nodes, 29% showed a hilum present and 71% showed no hilum. Of 42 malignant nodes, 24% showed a hilum present and 76% showed no hilum. The difference in the distribution of benign and malignant nodes in the hilar classes was not significant (p=0.52) (Table 1).

Nodal Cortex
A peripheral high-density cortex on CT contained mostly lymphatic tissue. In 72% of all nodes, the hilum was absent. Therefore, we could not classify 153 nodes according to their cortex. Of the remaining 59 nodes, 49 were benign and 10 malignant.

In the benign nodes, 94% exhibited a normal cortex (Fig. 4A,4B). None of the benign nodes showed an irregular cortex (Fig. 5). Of the malignant nodes, 90% exhibited an abnormal cortex; however, none of the malignant nodes showed a concentric cortex (Fig. 6). Of the five nodes with an eccentric cortex, four were malignant (Fig. 7A,7B) and the remaining one was benign. The difference in the distribution of benign and malignant nodes in the cortex classes was statistically significant (p<0.0001) (Table 1).

View larger version (63K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —Normal benign lymph node from breast of 40-year-old woman. In vitro high-resolution helical CT scan shows high-density C-shaped rim around central low-density hilum.

View larger version (90K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —Normal benign lymph node from breast of 40-year-old woman. Histologic section shows C-shaped lymphoid tissue and central fatty tissue. (H and E, x 1)

View larger version (45K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5. —Malignant lymph node with irregular cortical rim from breast of 46-year-old woman. In vitro high-resolution helical CT scan shows irregular high-density cortex.

View larger version (46K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6. —Benign lymph node with wide concentric cortical rim from breast of 78-year-old woman. In vitro high-resolution helical CT scan shows concentric cortical widening.

View larger version (71K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7A. —Malignant lymph node with eccentric cortical rim thickening from breast of 48-year-old woman. In vitro high-resolution helical CT scan shows focal cortical widening.

View larger version (106K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7B. —Malignant lymph node with eccentric cortical rim thickening from breast of 48-year-old woman. Histologic section shows eccentric peripheral metastatic lesion (arrow). (H and E, x 1)

Node Size
The mean of the longest diameters was 5.9 mm; the range was 0.5-26.5 mm. Table 2 shows the number and percentage of malignant lymph nodes in relation to the longest axis and shortest axis diameters. The shortest diameter may prove to be the more accurate diameter to use in predicting tumor-positive nodes. However, positive and negative nodes had a large range of overlap in size. Table 3 shows the sensitivity and specificity for several cutoff points of these size criteria per lymph node. As illustrated in Tables 2 and 3, the size criterion cannot accurately predict benign or malignant status of the node.

Node Shape
Table 4 shows the number and percentage of malignant nodes in relation to the longest-shortest axis ratio. All 10 lymph nodes with a longest-shortest axis ratio smaller than 1.5 were metastatic. Table 5 shows the sensitivity and specificity for two cutoff points of the longest-shortest axis ratio criteria per lymph node. As illustrated in Tables 4 and 5, a longest-shortest axis ratio smaller than 2 proved to be a more valid criterion for predicting malignant involvement than longest-shortest axis ratios smaller than 1.5.

Of the 170 benign nodes, 165 (97%) showed a longest-shortest axis ratio greater than 2, and five (3%) showed a longest-shortest axis ratio less than or equal to 2. Of the 42 malignant nodes, 17 (40%) showed a longest-shortest axis ratio greater than 2, and 25 malignant nodes (60%) exhibited a longest-shortest axis ratio equal to or less than 2. The differences in distribution of malignant and benign nodes in the two longest-shortest axis ratio classes were significant (p < 0.0001) (Table 1).

Of the 17 malignant nodes with a longest-shortest axis ratio greater than 2, six (35%) had an irregular abnormal cortex. The cortex of the remaining 11 malignant nodes (65%) could not be characterized because the hilum was not visualized.

Extracapsular Invasion
Extracapsular extension of tumors from nodes was suggested on CT images in 18 nodes, and all were positive for extracapsular invasion at histopathology.

Micrometastasis
Three of the 42 metastatic nodes were micrometastases. The one micrometastatic node with a longest-shortest axis ratio equal to or less than 2 was true-positive on CT findings. The other micrometastatic node with an irregular cortex was true-positive on CT findings. The remaining one micrometastatic node without malignant findings on CT was false-negative.

Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
CT of the axilla is more informative than physical examination [11]. CT can accurately detect the level of axilla involvement when lymph nodes are enlarged and can be used to evaluate extracapsular node extension [11]. However, conventional CT is not an accurate predictor of axillary metastases because of its low negative predictive value and because node size alone has been shown to be an unreliable criterion for differentiation of benign from malignant nodes [11]. Morphologic changes help distinguish benign from malignant nodes [9].

Recent advances in high-resolution helical CT have resulted in improved depiction of axillary lymph nodes. In our study, the histologic basis of nodal texture at CT has been fully evaluated. Pathologic assessment of excised nodes with a central low-density hilum seen on CT showed arteries, veins, lymphatic sinuses, and fatty tissue. A peripheral high-density cortex on CT contained mostly lymphatic tissue. In our study, high-resolution helical CT was able to show internal structures of nodes.

The assessment of nodes with a hilum showed concomitant abnormal cortex in only 6% of benign nodes but in 90% of malignant nodes. In addition, none of the benign nodes showed an irregular cortex, and none of the malignant nodes showed a concentric cortex. A previous high-resolution sonography study reported that a concentric cortex was seen in only 21-23% of malignant nodes [9]. Therefore, a concentric cortex is seen more frequently in benign than in malignant nodes. However, a concentric cortex does not rule out suspicions of malignancy. The differences in the distribution of benign and malignant nodes in the cortex classes were significant (p < 0.0001). Furthermore, six malignant nodes with normal shape (longest-shortest axis ratio > 2) had an irregular cortex. Thus, the presence of a hilum accompanied by abnormal cortex should be regarded as probably malignant.

In the absence of a hilum, we could not classify the cortex, which further reflects the reciprocity of these two structures. The percentage of the absence of the hilum in benign nodes was as high as in malignant nodes. The difference in the distribution of benign and malignant nodes in the hilar classes was not significant (p = 0.52).

Three-dimensional imaging reformats continuous data collection into a series of images that closely resemble the original structure [19]. For the evaluation of node size, 3D imaging reformations can show the longest diameter of a node and allow free rotation of the plane with the longest diameter to assess the shortest diameter. The present findings showed no significant differences between benign and malignant nodes in terms of the longest diameter and the shortest diameter, but there were marked differences in terms of the longest-shortest axis ratio. Our findings suggest that nodes with a longest-shortest axis ratio equal to or less than 2 are regarded as highly likely to be malignant. The tendency of benign nodes to show a longest-shortest axis ratio greater than 2 and malignant nodes to show a longest-shortest axis ratio equal to or less than 2 has been reported previously [9].

In our study, extracapsular invasion was suggested on CT in 18 nodes, and all were positive for extranodal tumor at histopathology. A previous study reported that extracapsular invasion was suggested on CT in three cases because of the increased density and perinodal stranding of axillary fat [11]. Furthermore, in the our study, CT allowed detection of the micrometastasis in two of three nodes. However, the number of micrometastatic nodes in our study was too small to discuss the ability of CT to detect micrometastasis.

Results from our study are not significantly different from the results of Vassallo et al. [9], who examined criteria based on high-resolution sonography findings in superficial lymph nodes. In some results, in vivo high-resolution sonography seems superior to ex vivo high-resolution helical CT because the same longest-shortest axis ratio equal to or less than 2 had higher sensitivity (85%) on the high-resolution sonography study than the sensitivity (60%) in our study, and hilar visualization was better (67%) with high-resolution sonography than with high-resolution helical CT (28%). Vassallo et al. also reported the absence of the hilum more frequently in malignant than in benign nodes, making the absence of the hilum a strong criterion for malignancy. However, in our study, the hilum of the node was present in equal frequency in benign and malignant nodes. The reasons for these differences between our study and the high-resolution sonography study are unknown, but perhaps they were caused by the smaller size of nodes in our study; we examined 18 women with breast cancer and clinically negative lymph node findings and only one with clinically positive node findings. However, Vassallo et al. examined 78 patients with clinically suspected lymphadenopathy, not including breast cancer.

A potential advantage of helical CT over high-resolution sonography is the visualization of lymph nodes regardless of depth. High-resolution sonography is essentially of value only for visualization of superficial lesions and cannot recognize deeper nodes [9], and the effectiveness of sonography depends on the investigator's skill. CT offers an objective noninvasive method for direct visualization of the axilla.

The results of this preliminary in vitro study support an in vivo evaluation of axillary staging using high-resolution helical CT. Therefore, the technical parameters of in vivo high-resolution helical CT for axillary staging can be set to match the parameters used in our study.

The hilum was absent in 72% of all small nodes in our in vitro study so these nodes could not be classified according to their cortical morphology. Therefore, nodal shape (longest-shortest axis ratio) may be important, and cortical morphology can complement nodal shape in predicting malignancy in vivo.

In conclusion, pathologic assessment of excised nodes with a central low-density hilum seen on CT showed arteries, veins, lymphatic sinuses, and fatty tissue. A peripheral high-density cortex on CT contained mostly lymphatic tissue. Abnormal (eccentric, irregular) cortices were seen in malignant nodes (p < 0.0001). Marked differences were observed among the proportions of benign and malignant nodes when the longest-shortest axis ratio was less than 2 and an abnormal cortex was observed. CT was also able to detect extracapsular lymph node extension. High-resolution helical CT in vitro can detect the internal structure of small nodes. Morphologic changes that are detectable on high-resolution helical CT help distinguish benign from malignant nodes in vitro.

References

Top Abstract Introduction Subjects and Methods Results Discussion References

 

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