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1
Department of Radiology and Cancer Biology, Nagasaki University School of
Dentistry, 1-7-1 Sakamoto, Nagasaki 852-8588, Japan.
2
Department of General Education, School of Health Sciences, Kyushu University,
Fukuoka 812-0054, Japan.
Received August 14, 2000;
accepted after revision September 25, 2000.
Address correspondence to T. Nakamura.
Abstract
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MATERIALS AND METHODS. We analyzed 209 cervical nodes (102 metastatic and 107 nonmetastatic) from 62 patients with head and neck cancer. These nodes were topographically correlated by node between images and surgical specimens, and accordingly between sonography and CT.
RESULTS. The area under the receiver operating characteristic curve (Az value) for the overall impressions of metastatic or nonmetastatic nodes was significantly greater for sonography (power Doppler sonography plus gray-scale sonography, 0.97 ± 0.005; gray-scale sonography, 0.95 ± 0.004) than for CT (0.87 ± 0.018). Receiver operating characteristic curve analysis also showed that the greater ability of sonography to depict the internal architecture of the nodes (Az value, 0.96 ± 0.006) compared with CT (Az value, 0.81 ± 0.027) significantly contributed to the better performance of sonography compared with CT in diagnosing metastatic nodes in the neck. On the other hand, size criterion (the short-axis diameter) was equally predictive in sonography and CT. The greater contributions of internal architectures relative to the size criterion of the node in the sonographic assessment for metastatic nodes were further evidenced by the findings that sonography provided higher sensitivity and specificity than CT did, whereas the cutoff points for the short-axis diameter in both tests were equivalent.
CONCLUSION. Sonography performed significantly better than CT in depicting cervical metastatic nodes. Sonography could be a useful adjunct to CT in surveying cervical metastatic nodes.
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Sonographic evaluation of enlarged nodes is also based on assessment of the internal architecture of the node as well as size determination of the node, and abnormalities in the node may be reflected by increased parenchymal echogenicity or loss of hilar echogenicity in malignant disease of the node [5,6,7]. In addition, the recent development of Doppler sonography technology has shed light on the diagnostic significance of changes in nodal blood flow in differentiating metastatic from nonmetastatic nodes [8,9,10]. These studies have shown that, albeit some controversies, the assessment of nodal blood flow patterns had some impact on improving the performance of sonography in depicting metastatic nodes in the neck [6].
Therefore, in this study, we compared the performance of gray-scale sonography, power Doppler sonography, and CT in staging metastatic nodes in the necks of patients with head and neck squamous cell carcinoma. Our focus was on the diagnostic performance of two imaging criteria—namely, the size and internal architecture of the node—on sonography and CT.
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Sonographic Imaging
Gray-scale and power Doppler sonography were performed using a unit (Logiq
700; General Electric Yokogawa Medical Systems, Tokyo, Japan) equipped with a
wide-bandwidth transducer (range, 6-13 MHz). Gray-scale sonography was
performed at 10 MHz; power Doppler sonography was performed at 8 MHz. Standard
Doppler settings were chosen for optimal detection of the signals from the
lymph node vessels, which had low-velocity flow. Common settings of pulse
repetition frequency (500 Hz) and wall filter (75 or 62 Hz) were used.
Representative images from each lymph node were obtained using gray-scale and
power Doppler sonography so that the maximal axial section of the nodes
appeared on sonographic images.
The following sonographic criteria were used in this study: short axial diameter of the node measured with a calliper on sonograms; the presence or absence of hilar echoes; and the presence or absence of hilar blood flow. Previous reports have shown that an increase in short axial diameter but not the long axial diameter is an efficient indicator for metastatic nodes [5, 6]. A preferential increase in short-axis diameter results in a round or oval node, so these features are suggestive of metastatic nodes. The hilum is identified as a highly echogenic structure in the central part of the node. Metastatic tumor cells frequently invade this part of the node and, in that case, the echogenicity of the hilum may be lost. Multivariate feature analysis showed that the presence or absence of hilar echoes, an increase in the short-axis diameter, and the presence of normal hilar flow were the sonographic features that were predictive of nonmetastatic (presence of hilar echoes and hilar flow) and metastatic (increases in short-axis diameter) lymph nodes [8].
Helical CT
Patients were scanned using a CT imaging system (HiSpeed Advantage SG;
General Electric Medical Systems, Milwaukee, WI). The scanning orientation was
parallel to the Frankfurt horizontal line. Scanning was performed with a
collimation of 3 mm, a pitch of 1:1, a matrix of 512 x 512, a display
field of view of 23 cm, 120 kVp, and 200 mA. CT examination was carried out
after an IV bolus injection of approximately 100 mL (2 mL/kg of body weight)
of iopamidol (Iopamiron 300; Schering, Berlin, Germany) at a rate of 1.0
mL/sec. We started scanning 80 sec after the start of contrast medium
injection. CT for examination of metastatic nodes in the neck was usually
completed in 50-60 sec after the start of scanning. The scanning period
(80-140 sec after the start of contrast medium injection) was confirmed to be
the time when the lymph node showed plateaulike staining kinetics and provided
appropriate contrast against the neighboring muscles. We preferred this rate
of contrast medium injection (1.0 mL/sec) instead of faster rates (e.g., 2.0
mL/sec) because the slower injection rate provided prolonged plateaulike
periods for lymph nodes without any significant loss of enhancement efficiency
during the following scanning period. We obtained reformatted axial images of
3 mm in thickness from these data.
We used two CT criteria, both of which were deemed to be important indicators for differentiating benign from metastatic nodes in the preceding studies [1, 2]: short- and long-axis diameters of the node measured with a caliper on CT images and the presence or absence of abnormal staining patterns of the node, such as rim enhancement and irregularly increased staining of the node.
Receiver Operating Characteristic (ROC) Curve Analysis
We performed ROC curve analyses on overall impression of whether the node
was metastatic or nonmetastatic, the presence or absence of an internal
architecture suggestive of a metastatic or nonmetastatic node, and the size of
the node on either sonographic or CT images. We used a total of 621 images
(207 images each for gray-scale sonography, power Doppler sonography, and CT)
of the metastatic and nonmetastatic lymph nodes. Sonographic and CT images
were documented on print paper using a color digital printer (Pictrography;
Fujifilm, Tokyo, Japan) and were presented to four radiologists who were
experienced in both sonography and CT in the head and neck region, had not
previously seen these cases, and were not aware of any patient information.
Before ROC curve analyses, the quality of printed images regarding noise of
images, special resolution, and motion artifacts was assessed by two of the
authors as excellent, good, fair, or poor. All 621 images were categorized as
excellent, good, or fair.
In advance, one of the authors measured the size of the nodes used in this study: the short-axis diameter of the node for sonography and the short- and long-axis diameters of the node for CT. Then the four observers were first asked to score the presence or absence of hilar echoes on gray-scale sonographic images using a 5-point rating scale (1 = definitely present, 2 = probably present, 3 = unclear if the finding is present or not, 4 = probably not present, 5 = definitely not present). Next, they were asked to score the presence or absence of abnormal staining patterns of the node on CT images using a similar rating scale (1 = definitely not present, 2 = probably not present, 3 = unclear if the finding is present or not, 4 = probably present, 5 = definitely present). Then, at least 2 weeks after the second assessment, the observers were again asked to score the presence or absence of normal hilar blood flow or normal hilar echogenicity in the nodes on gray-scale plus power Doppler sonographic images. There may be an undefined but important imaging feature or features that could affect the observers' decision about differentiation between benign and malignant nodes. To estimate the relative importance of the imaging criteria tested in the present study, we also assessed the overall impression of the observers of the nodal images concerning benignancy and malignancy. Therefore, again at least 2 weeks after the third assessment, the overall impressions of these observers of the gray-scale images, gray-scale plus power Doppler sonographic images, and CT images were also scored using a 5-point rating scale (1 = definitely not metastatic, 2 = probably not metastatic, 3 = indeterminate, 4 = probably metastatic, 5 = definitely metastatic). We also assessed the performance of the size criterion for predicting the presence or absence of metastasis in the node. This test was based on an ordinal scale of increasing points for either the short- or long-axis diameter of lymph nodes. A rank of 1 represented nodes with a short- or long-axis diameter of 4 mm or less, and an increase of 1 mm in short- or long-axis diameter increased the rank by 1. Thus, for example, if a node was 10 mm in its short-axis diameter, then it would be assigned a rank of 7.
For each imaging technique, a binormal ROC curve was fitted to each observer's rating data using software (ROCKIT; Metz CE, Chicago, IL) [11]. The diagnostic performance of each imaging technique was determined by calculating the area under each observer-specific ROC curve (Az value) [12]. Two-way analysis of variance test showed that significant differences in rating data were noted among different imaging techniques but not among the four observers. Therefore, averaged ROC curves representing the performance of the four observers as a group were calculated for comparing the imaging technique. Az values were expressed as means ± standard errors, and the significance of the difference in the Az value between the imaging techniques was tested by the paired t test for each observer. ROC curves were also calculated and fitted for size determination represented by the ordinal scale of increasing points described earlier. The significance was tested by the Student's t test for data obtained from assessment based on node size. We tested the significance of the differences in Az values between the imaging techniques for a total of 207 nodes in the neck and for each node population categorized into three levels in the neck.
Calculation of Sensitivity and Specificity for Each Imaging
Technique
We calculated the sensitivity (the number of nodes with positive findings
at imaging and at histology divided by the number of nodes with positive
findings at histology) and specificity (the number of nodes with negative
findings at imaging and at histology divided by the number of nodes with
negative findings at histology). The accuracy was calculated using the
following formula: the number of nodes with positive findings at imaging and
at histology plus the number of nodes with negative findings at imaging and at
histology divided by the total number of nodes.
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These findings suggest that, compared with CT, sonography has a greater potential in depicting nodes metastatic from squamous cell carcinomas in the head and neck region. To substantiate this hypothesis, we assessed the ability of sonography and CT to detect metastatic nodes by conducting ROC curve analyses on enlarged nodes that were topographically correlated by node between sonograms and CT images. ROC curves for the overall impression revealed that gray-scale sonography yielded significantly better performance than CT (Az value for CT, 0.87 ± 0.018; Az value for gray-scale sonography, 0.95 ± 0.004; p = 0.017) (Fig. 4). Gray-scale plus power Doppler sonography performed as well as gray-scale sonography, with Az values at a similar level for these two techniques (0.97 ± 0.005; p = 0.095). These findings may indicate that blood flow signals as depicted by Doppler sonography did not significantly contribute to the diagnostic performance of sonography in depicting metastatic nodes.
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We next conducted ROC curve analyses on data obtained by either size determination alone or by assessment of internal architecture alone for each of the three imaging techniques. ROC curve analysis for sonography showed that Az values calculated for the assessment using internal architectural patterns (0.92 ± 0.005 for gray-scale sonography; 0.96 ± 0.006 for gray-scale plus power Doppler sonography) were significantly greater than those for assessment using short-axis diameter (0.87 ± 0.024) (p = 0.004 vs. gray-scale sonography; p < 0.001 vs. gray-scale plus power Doppler sonography) (Fig. 5). In contrast, ROC analysis for CT showed that Az values calculated for the assessment using internal architecture (abnormal staining of the node) (0.81 ± 0.027) did not differ significantly from those for the assessment using short-axis diameter (0.86 ± 0.026; p = 0.15) (Fig. 6). Furthermore, Az values for the assessment using the internal architecture of the node with gray-scale sonography (0.92 ± 0.005) were greater than those obtained with CT (0.81 ± 0.027; p = 0.020). Gray-scale plus power Doppler sonography was associated with a further increase in Az value in the assessment of internal architecture (0.96 ± 0.006, p = 0.007 vs. gray-scale sonography). ROC curve analyses of CT images indicated that size determination using the short-axis diameter of the node was associated with an Az value (0.86 ± 0.026) proximate to that of the overall impression (0.87 ± 0.018) (Fig. 2C). The Az value obtained on CT images by size determination using long-axis diameter (0.73 ± 0.034), on the other hand, was significantly smaller than that obtained by size determination using short-axis diameter (0.86 ± 0.026; p < 0.005) (Fig. 6). The Az values for size determination by the short-axis diameter of the node were at similar levels in sonographic (0.87 ± 0.024) and CT (0.86 ± 0.026) evaluation.
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Consistent with the findings of ROC analysis for assessment using the internal architecture of the node, combined assessment on gray-scale plus power Doppler sonography displayed the greatest sensitivity and specificity among the three different imaging techniques (sensitivity, 0.68, 0.69. and 0.74 for CT, gray-scale sonography, and gray-scale plus power Doppler sonography, respectively; specificity, 0.82, 0.90, and 0.96 for CT, gray-scale sonography, and gray-scale plus power Doppler sonography, respectively). The compromise cutoff points of the short axial diameter criterion for metastatic nodes that were associated with the best accuracy (0.79 for sonography and 0.80 for CT) were 9 and 10 mm for sonography and CT, respectively, supporting the notion that the size criterion was equally effective for sonography and CT.
Then we asked whether the observed superiority in the performance of sonography in depicting metastatic nodes is dependent on levels in the neck. To address this question, we compared Az values at each level of the neck calculated from the averaged ROC curves fitted for the overall impression of the four observers. At all three levels in the neck, gray-scale plus power Doppler sonography yielded significantly greater Az values (0.94 ± 0.007, 0.96 ± 0.010, and 0.97 ± 0.008, for levels I, II, and III plus IV, respectively) than those obtained on CT (0.89 ± 0.012, 0.92 ± 0.015, and 0.86 ± 0.003, for levels I, II, and III plus IV, respectively; p = 0.046, 0.040, and 0.042, for levels I, II, and III plus IV, respectively). Gray-scale sonography, on the other hand, yielded significantly greater Az values than did CT at levels I (0.94 ± 0.008, p = 0.016) and III plus IV (0.95 ± 0.007, p = 0.022), but not at level II (0.95 ± 0.009, p = 0.171). This was, at least in part, because of a significantly elevated Az value for CT at level II of the neck, compared with those at the other levels in the neck (paired t test, p = 0.0006). At all three levels in the neck, no significant difference was found in Az values between gray-scale and power Doppler sonography.
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Sonographic evaluation was found to be adequate for differentiating metastatic nodes from nonmetastatic nodes in patients with head and neck cancer [1, 5,6,7,8,9,10]. Multivariate feature analysis showed that of the sonographic criteria advocated for metastatic or nonmetastatic nodes, the presence or absence of hilar echogenicity, an increase in short-axis diameter, and the presence of normal hilar blood flow were the only sonographic features that were predictive of metastatic (increases in short-axis length) or reactive (the presence of normal hilar blood flow, hilar echoes, or both) nodes [6]. ROC curve analyses in our study showed that the performance of gray-scale plus power Doppler sonography using internal architecture assessment was significantly greater than that of gray-scale sonography using internal architecture assessment (Fig. 2B). However, the overall performance of gray-scale and gray-scale plus power Doppler sonography was not significantly different (Fig. 2A). Taken together with the findings from multivariate analysis [6], which showed the only three sonographic features (short-axis diameter, the presence or absence of hilar echoes, and the presence or absence of hilar blood flow) contributing significantly to the diagnostic performance of sonography for detecting metastatic and reactive cervical nodes, the present findings suggest that as yet an undefined factor or factors may contribute, albeit not significantly, to the diagnostic performance of gray-scale sonography for depicting metastatic nodes on the basis of overall impression assessment.
Diagnosis of metastatic nodes using CT also depends on size determination and assessment of changes in the internal architecture. In this context, Curtin et al. [4] studied the effect of size criteria and internal architectural changes of the node on diagnostic accuracy for metastatic nodes, and these researchers showed that the addition of information on internal architecture of the node resulted in a substantial improvement of the diagnostic performance of CT using long-axis length (maximum axial diameter). We found that CT did not perform well when the long-axis diameter criterion alone was used (Fig. 2C); however, when the short-axis diameter was used as a size criterion, even the size criterion alone, CT performed as well as, if not better than, when the internal architecture alone was used (Fig. 2C). The performance of CT using short-axis diameter assessment approximated that of CT using overall impression. Therefore, these findings suggest that the contribution of size determination to the diagnostic performance was relatively greater in CT than in sonography.
Different anatomic levels in the neck may affect the performance of diagnostic imaging for metastatic lymph nodes. Several studies of CT and sonography have confirmed that enlarged nodes at different levels require different size criteria for predicting whether nodes are metastatic [4, 7]. Therefore, we also assessed the performance of sonography and CT for detection of metastatic nodes in each of the three levels in the neck. As stated, at all levels in the neck, gray-scale plus power Doppler sonography performed best among the three imaging techniques. Our findings also indicated that the performance of sonography was not significantly different among the different levels in the neck. Again, gray-scale sonography as assessed by overall impression performed as well as gray-scale plus power Doppler sonography at all levels in the neck. It is interesting to note that level II was the only level in the neck in which CT performed as well as gray-scale sonography. At the other levels in the neck, gray-scale sonography performed better than CT. This finding could also be explained by the finding that nodes at level II were largest among the nodes at all three levels on CT images; the average short-axis lengths of nodes at levels I, II, and III plus IV, respectively, were 7 (reactive) and 11 mm (metastatic), 7 (reactive) and 13 mm (metastatic), and 6 (reactive) and 10 mm (metastatic). The long-axis lengths of reactive and metastatic nodes were also greatest for nodes at level II. Another study of sonography [7] also showed that metastatic nodes at level II were larger than those at the other levels of the neck. Thus, greater sizes of nodes at level II may facilitate precise interpretation of the internal architecture of metastatic nodes at this anatomic level using CT.
The lack of a requirement for radiation and the low cost may be major advantages of sonographic examination. In addition, our findings clearly indicated that sonography performed better than CT for detecting metastatic nodes in patients with head and neck squamous cell carcinoma. Nevertheless, the fact that sonographic examination takes more time than CT may greatly diminish the value of sonography; in general, CT for the whole neck is usually completed 2-3 min after the start of contrast medium injection, whereas sonographic examination of the bilateral neck requires at least 30 min. In addition, CT examination is necessary for the detection of deep cervical nodes such as those in the retropharyngeal space. Therefore, CT should be the first choice for a survey of metastatic nodes in the neck, and it may be reasonable to perform sonographic examination for detailed study of suspected nodes in the neck after CT surveillance.
Acknowledgments
We acknowledge Yoshiharu Higashida for his suggestions. We are also
grateful to Charles E. Metz for the use of his ROCKIT program.
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