Diagnostic Accuracy of Sonographic Criteria for Evaluation of Cervical Lymphadenopathy

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1 Diagnostic Accuracy of Sonographic Criteria for Evaluation of Cervical Lymphadenopathy Michael Ying, MPhil, Anil Ahuja, FRCR, Constantine Metreweli, FRCR Although ultrasonographic criteria for abnormal nodes are used routinely in the evaluation of cervical lymphadenopathy, the diagnostic accuracy of these criteria in different areas has not been documented. This study evaluated 977 normal cervical nodes from 80 normal subjects and 1419 abnormal cervical nodes from 277 patients with proven cervical lymphadenopathy. The diagnostic accuracy (sensitivity, specificity, positive predictive value, negative predictive value, and accuracy) of size, shape (short axis to long axis ratio), echogenic hilus, and nodal border for regional lymph nodes are evaluated and discussed. KEY WORDS: Lymph nodes, cervical; Lymphadenopathy; Ultrasonography, diagnostic criteria. ABBREVIATIONS UGFNAC, Ultrasonographically guided fine-needle aspiration cytology; S/L, short axis to long axis; CCA, Common carotid artery; IJV, Internal jugular vein; PPV, Positive predictive value; NPV, Negative predictive value; ROC, Receiver operating characteristic; CT, Computed tomography Received November 28, 1997, from the Department of Optometry and Radiography (M.Y.), Hong Kong Polytechnic University, Hung Hom, Kowloon; and the Department of Diagnostic Radiology and Organ Imaging (A.A., C.M.), Prince of Wales Hospital, Shatin, New Territories, Hong Kong. Revised manuscript accepted for publication March 16, Address correspondence and reprint requests to Michael Ying, Department of Optometry and Radiography, Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong. Sonographic criteria for distinguishing normal from abnormal lymph nodes have been described previously. These include size, shape, echogenic hilus, nodal border, and distribution. 1 4 However, the individual reliability of these criteria has not been assessed. Some of the previously described criteria for assessing cervical lymph nodes can specifically identify abnormal nodes (such as intranodal necrosis, matting, and surrounding soft tissue edema), whereas others are not specific for either normal or abnormal nodes (such as size, shape, echogenic hilus, and nodal border). Moreover, as reported earlier, 5 we found that the normal appearance of cervical lymph nodes is not the same in different regions of the neck. Thus, this study was undertaken to assess the accuracy of these nonspecific criteria in differentiating normal nodes from abnormal nodes in different regions of the neck by the American Institute of Ultrasound in Medicine J Ultrasound Med 17: , /98/$3.50

2 438 CERVICAL LYMPHADENOPATHY J Ultrasound Med 17: , 1998 MATERIALS AND METHODS Eighty healthy subjects (37 men, 43 women) with no history of malignancy, tuberculosis, chronic tonsillitis, glandular fever, or neck surgery were included in the study. All subjects were Cantonese Chinese, and none of them had any history of recent acute inflammation of the upper respiratory tract or ear, nose, or throat disease. The subjects ranged in age from 12 to 76 years (mean, 32.2 years). Scans were performed with a 5 to 10 MHz linear transducer on a General Electric LOGIQ 500 (General Electric, Milwaukee, WI) ultrasound system. The subjects lay supine on the examination couch with the shoulders supported by a pillow. The neck was hyperextended. As the shape of the lymph nodes depends on the scan plane, scans were obtained with the transducer placed transversely and longitudinally, and measurements were made in the plane that showed a maximum cross-sectional area of the node. In each subject, all cervical lymph nodes detected in the examination were included in the study. A review of the ultrasonograms of 277 patients (151 men, 126 women) with proven cervical lymphadenopathy also was conducted as a part of this study. The patients were classified into seven etiologic groups: 1. Pharyngeal, laryngeal, and esophageal carcinomas, 33 patients 2. Oral cavity carcinomas, 23 patients 3. Infraclavicular carcinomas, 16 patients 4. Papillary carcinoma of the thyroid, 55 patients 5. Nasopharyngeal carcinoma, 84 patients 6. Non-Hodgkin lymphoma, 19 patients 7. Tuberculous lymphadenitis, 47 patients None of these patients had had previous radiotherapy or chemotherapy. Their age range was 12 to 94 years (mean, 47.6 years). All the scans were performed on a commercially available ultrasound system (Aloka 650, Tokyo, Japan) with a linear 7.5 and a sector 10 MHz transducer with a built-in water bath. All the patients underwent UGFNAC on the largest node. In each patient, all other lymph nodes with a ultrasonographic appearance similar to that of the aspirated node were considered to have a similar pathologic result. Cervical lymph nodes were assessed for their size, shape, echogenic hilus, and sharpness of border. As the longitudinal diameter of the nodes was found to be an unreliable criterion in assessment of cervical nodes, 6 only the short axis of the nodes was evaluated. Six cut-off points of the short axis of nodes were evaluated for their accuracy: (1) 5 mm; (2) 6 mm; (3) 7 mm; (4) 8 mm; (5) 9 mm; and (6) 10 mm. These cut-off points of the short axis were selected because they were the sizes that were reported previously to be useful for distinguishing normal from abnormal cervical nodes. 2,3,7,8 In this study, a normal lymph node with a short axis greater than the selected cutoff point was considered a false-positive finding, whereas a short axis less than or equal to the selected cut-off point was considered a true-negative finding. Similarly, an abnormal lymph node with a short axis greater than the selected cut-off point was considered a true-positive result, whereas a short axis less than or equal to the selected cut-off point was considered a false-negative result. The shape of the cervical nodes was assessed by the S/L ratio. 4,9 An S/L ratio equal to or greater than 0.5 indicates a round node, whereas an S/L ratio less than 0.5 indicates an oval or elongated node. In this study, a normal lymph node with an S/L ratio equal to or greater than 0.5 was considered a false-positive finding, whereas an S/L ratio less than 0.5 was considered a true-negative finding. An abnormal lymph node with an S/L ratio equal to or greater than 0.5 was considered a true-positive result, whereas an S/L ratio less than 0.5 was considered a falsenegative result. The nodal hilus is identified as an intranodal echogenic structure continuous with the surrounding fat. 10 It should not be confused with coagulation necrosis, which may also be seen as echogenic area within the node. However, these echogenic foci are not continuous with surrounding fat. In the present study, a normal lymph node without an echogenic hilus was considered to be a false-positive finding, whereas a normal node with an echogenic hilus was considered a true-negative result. An abnormal lymph node without an echogenic hilus was considered a true-positive result, whereas an abnormal node with an echogenic hilus was considered a falsenegative finding. It has been reported that lymph nodes with a sharp border were considered to be abnormal, whereas those with an unsharp border tended to be normal. 7 In this study, a normal lymph node with a sharp border was considered a false-positive result, whereas a normal node with an unsharp border was considered a true-negative result. An abnormal lymph node with a sharp border was considered a true-positive finding, whereas an abnormal node with an unsharp border was considered a false-negative finding. The distribution of cervical lymph nodes was made into eight regions in the neck, similar to the

3 J Ultrasound Med 17: , 1998 YING ET AL 439 method described by Hajek and coworkers 2 : (1) submental, (2) submandibular, (3) parotid, (4) upper cervical: above the hyoid bone and along the CCA and the IJV, (5) middle cervical: between the hyoid bone and the cricoid cartilage and along the CCA and IJV, (6) lower cervical: below the cricoid cartilage and along the CCA and IJV, (7) supraclavicular fossa, and (8) posterior triangle (also known as accessory chain) (Fig. 1). The sensitivity, specificity, PPV, NPV, and accuracy were calculated. The ROC curves for the size of the lymph nodes in different regions of the neck were plotted. Graphs showing the relationship between the sensitivity and specificity for the shape, echogenic hilus, and nodal border of the lymph nodes in different regions of the neck also were plotted. RESULTS In the 80 normal subjects, 977 cervical lymph nodes were detected. In the 277 patients, 1419 lymph nodes were detected. The distribution of normal and abnormal lymph nodes is shown in Table 1. As the numbers of normal nodes in regions 6 and 7 were low, the calculated statistical parameters may not be reliable in these areas. Therefore, only lymph nodes in submental (region 1), submandibular (region 2), parotid (region 3), upper cervical (region 4), middle cervical (region 5), and posterior triangle (region 8) were evaluated. How well the different sonographic criteria perform in these regions is shown in Tables 2 through 7. In the parotid region, using 10 mm as the size cut-off, the PPV was invalid as no true-positive or false-positive findings were obtained. The sensitivity and specificity for size in different regional nodes were charted as ROC curves (Fig. 2). The curve that is highest and near the Y axis (which is nearest the top left-hand corner) shows the best sensitivity with a high specificity. In Figure 2, the curve for the parotid nodes is the one nearest the top left-hand corner when compared with other curves. The sensitivity and specificity for shape (S/L ratio), echogenic hilus, and nodal border in different regional nodes were plotted in Figures 3 to 5, respectively. The point that is nearest the top left-hand corner shows that the criterion for the corresponding regional nodes has a high sensitivity together with a high specificity. In Figure 3 (graph for the nodal shape), the point for the submental nodes and the point for the upper cervical nodes have a similar distance, both being nearest to the top left-hand corner. The submental nodes show a higher sensitivity (97.6%), whereas the upper cervical nodes have a higher specificity (98.3%). Figure 4 (graph for the echogenic hilus) shows that the point for the submandibular nodes is nearest to the top left-hand corner. In Figure 5 (graph for the nodal border), the point for the submental nodes is nearest to the top left-hand corner. DISCUSSION Different sonographic criteria have been established by which normal lymph nodes can be distinguished from abnormal nodes. 4,10 12 Unlike other criteria, size, shape, echogenic hilus, and sharpness of nodal border are not specific for either normal or abnormal nodes. Thus, it is essential for sonographers to be Figure 1 Schematic diagram of the neck shows the distribution of the cervical lymph nodes.

4 440 ACERVICAL LYMPHADENOPATHY J Ultrasound Med 17: , 1998 Table 1: Distribution of Normal and Abnormal Cervical Lymph Nodes Number of Lymph Nodes (Percentage) Region Nodes Normal Nodes Abnormal Nodes 1 Submental 45 (4.6%) 41 (2.9%) 2 Submandibular 237 (24.3%) 124 (8.7%) 3 Parotid 72 (7.4%) 22 (1.6%) 4 Upper cervical 230 (23.5%) 283 (19.9%) 5 Middle cervical 30 (3.1%) 75 (5.3%) 6 Lower cervical 2 (0.2%) 69 (4.9%) 7 Supraclavicular 7 (0.7%) 132 (9.3%) fossa 8 Posterior triangle 354 (36.2%) 673 (47.4%) Total familiar with the accuracy of these criteria in differentiating normal from abnormal nodes. The ROC curves for size in different regional nodes (Fig. 2) showed that the curve for the parotid nodes had the highest sensitivity together with a high specificity. It indicated that the short axis of lymph nodes was more accurate in assessment of the parotid nodes than in assessment of other regional nodes. In Figure 3, as the point for the submental nodes and the point for the upper cervical nodes had a similar distance to the top left-hand corner; thus we assumed that the nodal shape (S/L ratio) had a similar accuracy in differential diagnosis of the submental and upper cervical nodes and was more accurate when these nodes were examined. Similarly, nodal shape had a higher reliability when the echogenic hilus was used to assess the submandibular nodes (Fig. 4), whereas the nodal border was more accurate when the submental nodes were examined (Fig. 5). In assessing nodal size, we found that with increasing size, the sensitivity decreased whereas the specificity increased (Tables 2 through 7). The decreasing sensitivity was probably due to the fact that smaller positive nodes (abnormal nodes) were detected when increasing the cut-off point. However, the specificity increased because more large negative nodes (normal nodes) were detected. The result was consistent with that of previous reports in the literature. 6,11 Similar to these reports, 11 the accuracy did not constantly change with the cut-off point. The PPV and NPV are actually important indicators of the diagnostic usefulness of the criteria, since they show the probability of the criteria that give a correct diagnosis, whereas the sensitivity and specificity do not give this information. In order to make an objective evaluation of the nodal size, the cut-off point was selected when it obtained a highest accuracy. For the submental nodes (region 1), a short axis of 5 mm is the optimum size criterion for diagnosis as it shows the highest sensitivity (58%), specificity (100%), PPV (100%), NPV (73%), and accuracy (80%) among the cut-off points studied. The 100% for specificity and PPV was probably due to the fact that no false-positive nodes were found in this cut-off point (5 mm). Results showed that all normal submental nodes had a short axis of less than 5 mm, and any submental nodes with a short axis greater than 5 mm could indicate an abnormality (either inflammation or malignancy). The S/L ratio had an accuracy of about 84%, which makes it a better criterion than the size and the presence of an echogenic hilus for the diagnosis. The high NPV (97%) indicated that the S/L ratio was highly valuable in diagnosis of negative submental nodes, since only a few abnormal nodes show an S/L ratio less than 0.5 (one node in this study). Although the echogenic hilus was the least accurate criterion, it had about 77% accuracy, PPV, and NPV in the diagnosis of submental nodes overall. The nodal border is the most accurate among the criteria studied, as it has accuracy, PPV, and NPV of 85%. For the submandibular nodes (region 2), 9 mm is the most accurate size criterion (accuracy = 76%). The PPV and the NPV are 77% and 76%, respectively. This indicates that about 77% of nodes with a short axis greater than 9 mm were abnormal, and about Table 2: Performance of the for Submental Nodes (Region 1) Sensitivity Specificity PPV NPV Accuracy

5 J Ultrasound Med 17: , 1998 YING ET AL 441 Table 3: Performance of the for Submandibular Nodes (Region 2) Sensitivity Specificity PPV NPV Accuracy Table 4: Performance of the for Parotid Nodes (Region 3) Sensitivity Specificity PPV NPV Accuracy Table 5: Performance of the for Upper Cervical Nodes (Region 4) Sensitivity Specificity PPV NPV Accuracy Table 6: Performance of the for Middle Cervical Nodes (Region 5) Sensitivity Specificity PPV NPV Accuracy Table 7: Performance of the for Posterior Triangle Nodes (Region 8) Sensitivity Specificity PPV NPV Accuracy

6 442 ACERVICAL LYMPHADENOPATHY J Ultrasound Med 17: , 1998 Figure 2 ROC curves show the relationship between the sensitivity and the specificity of the size in different regional nodes (see also Tables 2 to 7). 76% of nodes with a short axis less than 9 mm were normal. The size criterion for submandibular nodes (9 mm) is higher than the size criterion of other regional nodes (5 to 7 mm). This probably is due to the large size of normal submandibular nodes, 5 and thus a higher size criterion is required to differentiate normal from abnormal nodes. Previous literature has also reported that the size criterion for submandibular nodes is higher than the size criterion for the cervical nodes in other areas. 1 The S/L ratio is not helpful for differentiating normal from abnormal nodes since the accuracy, PPV, and NPV are only about 30%. The specificity of the S/L ratio for submandibular nodes also is low (5%). The unsatisfactory result of the S/L ratio in submandibular nodes is due mainly to the fact that the majority of normal submandibular nodes have an S/L ratio greater than The echogenic hilus is the most accurate criterion, with an accuracy of 88%, PPV of 94%, and NPV of 86%. The high PPV indicated that submandibular nodes with absent echogenic hilus are highly suggestive of abnormality. The nodal border is the second most accurate criterion for the diagnosis. The accuracy, PPV, and NPV are 78%, 64%, and 89%, respectively. The relatively low PPV for the nodal border probably is due to the high prevalence of normal nodes with a sharp border (24%). For the parotid nodes (region 3), a short axis of 6 mm is the most accurate size criterion for the differentiation. It showed the highest sensitivity (73%), specificity (97%), PPV (89%), NPV (92%), and accuracy (91%) when compared with other size criteria studied. Similar to submandibular nodes, the S/L ratio is not accurate in differentiating normal parotid nodes from abnormal parotid nodes, since only 52% of lymph nodes were diagnosed correctly as normal or abnormal using this criterion. The low PPV (30%) probably is due to the high prevalence of normal parotid nodes with an S/L greater than 0.5 (57%). Although the S/L was not accurate for the diagnosis of parotid nodes, it was useful to predict negative nodes since about 89% of lymph nodes with an S/L less than 0.5 were normal nodes (NPV = 89%). The echogenic hilus is the second most accurate criterion for differentiating normal from abnormal parotid nodes (accuracy = 87%). The echogenic hilus is the criterion that shows the highest NPV (94%) among the criteria studied (i.e., it indicated that the presence of an echogenic hilus in parotid nodes is highly suggestive of normality). The nodal border is less accurate than the size and echogenic hilus but is more accurate than the S/L ratio. The low PPV of the nodal border (46%) occurs because of the high prevalence of normal nodes with a sharp border (29%). For the upper cervical nodes (region 4), a short axis of 7 mm is the most accurate size criterion (71%) when compared with other size criteria studied. Except for submandibular nodes, the selected size criterion for upper cervical nodes is higher than that for lymph nodes in other areas (5 to 6 mm). Som 1 also found a larger size criterion more accurate for submandibular and upper cervical nodes (both are 1.5 cm); however, the size criteria are different from those in the present study. The difference in the result may be due to the use of different imaging modalities. Som 1 used CT scanning, whereas ultrasonography was used in the present study. CT is reported to have a limited reliability in detecting lymph nodes less than 5 mm in diameter, 13,14 and, therefore, small nodes may be missed. However, ultrasonography can demonstrate lymph nodes as small as 2 mm in diameter. 3,15 The S/L ratio (82.3%) and the echogenic hilus (81.7%) had similar accuracies for the differentiation in the upper cervical region, which were higher than those of size (71%) and nodal border (69%). The high PPV of the S/L ratio indicated that an upper cervical node with an S/L ratio greater than 0.5 is highly suggestive of abnormality. However, the relatively low diagnostic accuracy of nodal border sharpness may be due to the high prevalence of sharp borders in normal upper cervical nodes (44%). For the middle cervical nodes (region 5), the most accurate size criterion for the diagnosis was 5 mm in the short axis, with an accuracy of 72%. The high PPV (98%) indicated that a 5 mm short axis was valuable in predicting a positive node. However, the low NPV (51%) showed that a cut-off point of 5 mm in the short axis was not accurate for predicting negative nodes, since only about half of the nodes with

7 J Ultrasound Med 17: , 1998 YING ET AL 443 Figure 3 Graph shows the relationship between the sensitivity and the specificity of the shape in different regional nodes (see also Tables 2 to 7). Figure 4 Graph shows the relationship between the sensitivity and the specificity of the echogenic hilus in different regional nodes (see also Tables 2 to 7). a short axis less than 5 mm were normal. The S/L ratio and the nodal border had a similar diagnostic accuracy (69% and 64%, respectively). The high PPV of the S/L ratio (98%) showed that an S/L ratio greater than 0.5 in middle cervical nodes was highly suggestive of abnormality. The low PPV and NPV of the nodal border in middle cervical nodes probably occurred because the majority of normal nodes had a sharp border (97%). The echogenic hilus is the most accurate criterion for differentiating normal from abnormal nodes in the middle cervical region (accuracy = 78%). The high PPV (91%) makes it a useful criterion in predicting abnormal nodes. In the middle cervical region, the NPV of the four criteria studied tends to be low (10% to 58%), which is not seen in other areas and indicates that none of the criteria studied can identify a normal middle cervical node accurately. For the posterior triangle nodes (region 8), the most accurate cut-off point of the short axis was 5 mm, with an accuracy of 79%. Lymph nodes greater than 5 mm are highly likely to be abnormal (PPV = 94%). However, the probability that lymph nodes with a short axis less than 5 mm were normal was 63% (NPV = 63%). The S/L ratio had a high PPV (99%), which showed that posterior triangle lymph nodes with an S/L ratio greater than 0.5 were highly suggestive of abnormality. The relatively low NPV (57%) probably was due to the high prevalence of abnormal nodes with an S/L ratio less than 0.5. The echogenic hilus is the most accurate diagnostic criterion in the posterior triangle region, with an accuracy of 88%, PPV of 89%, and NPV of 75%. The nodal border is the least accurate diagnostic criterion in the posterior triangle, with the lowest accuracy (62%), PPV (68%), and NPV (42%) when compared with other criteria. The inaccuracy probably is due to the high prevalence of unsharp borders in abnormal nodes (22%) and the high rate of sharp borders in normal nodes (69%). Normal posterior triangle nodes with sharp borders also were noted in our previous report. 5 CONCLUSION In the assessment of the cervical lymph nodes, the short axis is more accurate for the parotid nodes than for the lymph nodes in other regions. The nodal shape is more reliable in the differential diagnosis when the submental and upper cervical nodes are assessed. The echogenic hilus is more accurate when it is used to assess the submandibular nodes. The

8 444 ACERVICAL LYMPHADENOPATHY J Ultrasound Med 17: , 1998 accurate criterion is the nodal border (69%). A short axis of 7 mm is considered the most accurate size criterion (71%). Upper cervical nodes with an S/L ratio greater than 0.5 are highly suggestive of abnormality. For the middle cervical nodes, the most accurate criterion is the echogenic hilus (78%), and the least accurate criterion is the nodal border (64%). A short axis of 5 mm is the most accurate size criterion (72%). A short axis greater than 5 mm, an S/L ratio greater than 0.5, and absence of an echogenic hilus in middle cervical nodes are highly suggestive of abnormality. For the posterior triangle nodes, the most accurate criterion is the echogenic hilus (84%), whereas the least accurate criterion is the nodal border (62%). A short axis of 5 mm is considered the most accurate size criterion (79%). A short axis greater than 5 mm or an S/L ratio greater than 0.5 in the posterior triangle nodes is highly suggestive of abnormality. In conclusion, ultrasonography is an ideal initial examination for cervical lymphadenopathy if appropriate sonographic criteria are used. Figure 5 Graph shows the relationship between the sensitivity and the specificity of the nodal border in different regional nodes (see also Tables 2 to 7). nodal border is more accurate when the submental nodes are assessed. For the submental nodes, the nodal border is the most accurate criterion (85%), whereas the echogenic hilus is the least accurate criterion (77%). A short axis of 5 mm is the most accurate size criterion (80%). Submental nodes with a short axis greater than 5 mm should be considered abnormal. Submental nodes with an S/L ratio less than 0.5 are highly likely to be normal. For the submandibular nodes, the most accurate criterion is the echogenic hilus (88%); the least accurate criterion is the shape of lymph nodes (S/L) (30%). A short axis of 9 mm is the most accurate size criterion (76%). An absent hilus in the submandibular nodes is highly suggestive of abnormality. For the parotid nodes, the most accurate criterion is the size of lymph nodes (short axis) (91%), whereas the least accurate criterion is their shape (52%). A short axis of 6 mm is found to be the most accurate size criterion. Parotid nodes with a short axis less than 6 mm, with an echogenic hilus, or with an unsharp border are strongly suspected to be normal. For the upper cervical nodes, the most accurate criterion is the shape of lymph nodes (82%); the least REFERENCES 1. Som PM: Lymph nodes of the neck. Radiology 165:593, Hajek PC, Salomonowitz E, Turk R, et al: Lymph nodes of the neck: Evaluation with US. Radiology 158:739, Solbiati L, Cioffi V, Ballarati E: Ultrasonography of the neck. Radiol Clin North Am 30:941, Tohnosu N, Onoda S, Isono K: Ultrasonographic evaluation of cervical lymph node metastases in esophageal cancer with special reference to the relationship between the short to long axis ratio (S/L) and the cancer content. J Clin Ultrasound 17:101, Ying M, Ahuja A, Brook F, et al: Sonographic appearance and distribution of normal cervical lymph nodes in a Chinese population. J Ultrasound Med 15:431, van den Brekel MW, Stel HV, Castelijns JA, et al: Cervical lymph node metastasis: Assessment of radiologic criteria. Radiology 177:379, Shozushima M, Suzuki M, Nakasima T, et al: Ultrasound diagnosis of lymph node metastasis in head and neck cancer. Dentomaxillofac Radiol 19:165, Bruneton JN, Balu-Maestro C, Marcy PY, et al: Very high frequency (13 MHz) ultrasonographic examination of the normal neck: Detection of normal lymph nodes and thyroid nodules. J Ultrasound Med 13:87, Solbiati L, Arsizio B, Rizzatto G, et al: High-resolution sonography of cervical lymph nodes in head and neck cancer: Criteria for differentiation of reactive versus malignant nodes. Radiology 169(P):113, Sakai F, Kiyono K, Sone S, et al: Ultrasonic evaluation of cervical metastatic lymphadenopathy. J Ultrasound Med 7:305, 1988

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