Sonographic Appearance and Distribution of Normal Cervical Lymph Nodes in a Chinese Population

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1 Sonographic Appearance and Distribution of Normal Cervical Lymph Nodes in a Chinese Population Michael Ying, POOR, Anil Ahuja, FRCR, Fiona Brook, DCR, RDMS~ Brian Brown, PhD, Constantine Metreweli, FRCR In 100 normal subjects who had a sonographic examination of the neck, 1211 lymph nodes were detected. In all the subjects, at least five lymph nodes were seen. The distribution, number, echogenicity, shape, presence or absence of echogenic hilus, and the sharpness of nodal borders of normal cervical lymph nodes were deter- mined. The usefulness of these sonographic features in understanding the normal distribution and characteristics of the nodes in the Chinese population is discussed. The relationship between the shape and size of lymph node also was assessed. KEY WORDS: Sonography; Lymph nodes, cervical; Neck, lymph nodes. H igh-resolution sonographic examination plays an important role in assessment of cervical lymph nodes. A 7.5 MHz transducer allows detection of lymph node as small as 2 mm in diameter) Normal cervical lymph nodes usually are small, and therefore high-resolution sonography is required for their evaluation. Previous investigations have usually studied pathologic ABBREVIATIONS CCA, Common carotid artery; IJV, Internal jugular vein; 5/ L, Short axis to long <~xis ; CT, Computed tomography nodes,2-l and few studies have examined normal cervical lymph nodes,5,6 and these were predominantly in Caucasians. To our knowledge, the distribution of the normal lymph nodes in the neck in the Chinese population has not been described previously. A clear understanding of the distribution and sonographic appearances of normal cervical lymph nodes is necessary in differentiating normal nodes from pathologic nodes. This study was carried out to determine these characteristics of normal nodes in different regions of the neck. SUBJECTS AND METHODS Received October 23, 1995, from the Departments of Optometry and Radiography (M.Y., F.B., B.B.), The Hong Kong Polytechnic University, Hung Horn, Hong Kong and the Department of Diagnostic Radiology ilnd Organ lmaging (A.A., C.M.,) Prince of Wales Hospital, Shatin, New Territories, Hong Kong. Revised manuscript accepted for publication February 29, Address correspondence and reprint requests to Anil T. Ahu~1, FRCR, Department of Diagnostic R.1diology and Organ lmaging Prince of Wales Hospital, Shatin NT, Hong Kong. One hundred healthy subjects with no history of neck surgery, head and neck malignancy, tuberculosis, lymphoma, chronic tonsillitis, or glandular fever were included in the study. Examination of the 25 subjects with a recent history of acute inflammatory upper respiratory tract or ear, nose, or throat disease were deferred for 2 weeks after they became asymptomatic. All the subjects (44 men and 56 women) were Cantonese Chinese. The age range for the sub by the American Institute of Ultrasound in Medicine J Ultrasound Med 15: , / 96/ $3.50

2 432 NORMAL CERVICAL LYMPH NODES IN CHINESE POPULATION jects was 14 to 76 years (mean# 33.3 years). All the scans were performed with a General Electric LOGIQ 500 ultrasound system (General Electric, Milwaukee, Wl) in conjunction with a real-time linear multifrequency (5 to 10 MHz) transducer. The subjects lay supine on the couch with the shoulders supported by a pillow. The neck was hyperextended. Since the shape of the nodes depends on the scan plane, scans were obtained with the transducer placed transversely and longitudinally until the plane showed the maximum cross sectional area of the lymph.node, similar to the method described by Tohnosu and coworkers.7 Eight regions in the neck were delineated as described by Hajek and colleaguesb: I, submental; 2, submandibular; 3, parotid; 4, upper cervical, above the hyoid bone and along the CCA and IJV (Fig. 1); 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; 8, posterior triangle (also known as accessory chain) (Fig. 2). Except the submental nodes, which are located in the midline, all the lymph nodes were divided into left and right sides. The lymph nodes were assessed for their shape, echogenicity, echogenic hilus, distribution, and nodal border. Shape of the lymph nodes was determined by the S/L ratio. An S/L ratio less than 0.5 indicates a long or oval node (Fig. 3), whereas 0.5 or greater indicates a rounded node. Echogenicity of the lymph nodes was compared with that of the sur- j Ultrasound Med 15: , 1996 rounding fatty tissue and classified as being hyp~ choic (Fig. 4), isoechoic, or hyperechoic. The major vascular hilus appears as a hyperechoic linear structure (Figs. 4,5) within a lymph node and is continuous with the surrounding connective tissue (Fig. 4).4,9 The nodal border was assessed for its sharpness, determined by the boundary between the lymph node and the surrounding tissue; this border normally is sharp and well defined. RESULTS In the 100 subjects, 1211lymph nodes were detected. The number of lymph nodes in any one subject is ranged from five to 24. All subjects had bilateral lymph nodes. The smallest node detected in this study measured 3 mm x 2 mm and the largest node measured 38 mmx 11 mm. When the subjects were classified into five different age groups (< 20 years, 21 to 30 years, 31 to 40 years, 41 to 50 years, > 50 years), no significant difference was found in mean number of nodes between different age groups. TI1ere were 579 nodes in the 44 male subjects and 632 nodes in the 56 female subjects. TI1e mean number of lymph nodes in male subjects (13.2 nodes) is higher than that in female subjects (11.3 nodes). In the middle cervical portion, nodes were twice as often seen on the right (66%) than on the left (34%). In the rest of the neck, no significant difference was noted in the distribution of nodes between the two sides. Figure 1 Transverse scan of a normal left cervical chain lymph node (black arrows) closely related to the CCA (ar rowlwnds) and under the sternomastoid muscle (Wilif( (black arrows) under the sternomastoid muscle (whif( nnmvs) but away from the CCA (arrow/leads). Note the difference in arrows). location of this node compared to the cervical node in Figure 1. Figure 2 Transverse scan of a left posterior triangle lymph node

3 JUltrasound Med 15: , 1996 YING ET AL 433 Assessment of cervical lymph nodes usually concentrates on the pathologic nodes; however, knowledge of the normal distribution and appearance of cervical lymph nodes is essential in diagnosis. Clinical examination of cervical lymph node is inaccurate, especially for abnormal deep or small nodes,8,10 or for normal nodes. CT has limited reliability in detecting lymph nodes less than 5 mm diameter.l1,12 Furthermore, nodal shape determination by CT may be unreliable because some of the cervical lymph nodes are oriented with their long axis parallel to the longitudinal axis of the body, and CT demonstrates these lymph nodes only in the transverse plane, in which they appear round.s,t2-l4 High-resolution sonography, on the other hand, can detect lymph nodes as small as 2 mm in diameter, 1,15 and nodes can be assessed in more than one plane. In this study, all subjects had at least five lymph nodes detected by sonography. This is substantially different from a previous study, in which normal nodes were seen only in 67.6% of subjects.6 Normal lymph nodes are located in all regions of the neck,16-t9 and often not all of them can be visualized sonographically. The normal lymph nodes that were commonly detected in our study were the sub mandibular (region 2), 23.6%; upper cervical (region 4), 23.7%; and posterior triangle (region 8), 37.5%. Under clinical conditions, any different distribution of the lymph nodes could, by itself, raise the suspicion of cervical lymphadenopathy. Multiple lymph node involvement is common in lymphoma and metastasis.b,t8,20 Therefore, solitariness of lymph nodes may be useful in diagnosis. Most of the normal lymph nodes found in submental Figure 4 Transverse scan of the submandibular area shows an oval, hypoechoic lymph node with normal hilus (smallwlritc arrows) continuous with adjacent fat (arrowheads). Also identified is the ramus of the mandible (large white arrows). Figure 5 Longitudinal scan of the jugulodigastric node (sentinel or Kuttner node) with a normal hilus and a long elliptical shape. Figure 3 Coronal scan of the submental area shows an oval lymph node (white arrows). Also seen are the mylohyoid (curved black arrows) and paired geniohyoid (stmiglrt black arrows) muscles. The distribution of the normal cervical lymph nodes is shown in Figure 6. The number, shape, echogenic hilus, border sharpness, short axis, and long axis of the lymph nodes in different regions of the neck are shown in Table 1. DISCUSSION

4 NORMAL CERVICAL LYMPH NODES IN CHINESE POPULATION (region 1), parotid (region 3), middle cervical (region 5), lower cervical (region 6), and supraclavicular (region 7) regions are solitary. The lymph nodes detected in the submandibular and upper cervical regions can be either solitary (53.7% and 53.6%, respectively) or paired (42.1 % and 43.3%, respectively). In contrast, multiple lymph nodes are commonly found in the posterior triangle (77.4%). On the basis of these findings, multiple lymph nodes found in submental, parotid, middle cervical, lower cervical, and supraclavicular regions should also raise the suspicion of lymphadenopathy. Similarly, three or more lymph nodes found in submandibular and upper cervical regions may indicate pathologic lymph nodes. However, since multiple lymph nodes are common in the posterior triangle, multiplicity of lymph nodes alone is not useful for the diagnosis in this region, and other features need to be elicited. The echogenicity of normal lymph nodes varies between hypoechoic and isoechoic in comparison to the surrounding fatty tissue. In the eight regions studied, the majority of lymph nodes (> 90%) are hypoechoic, whereas the remaining ones were isa. echoic. This is similar to the findings of Sakai and coworkers,4 who also found most of the nodes to be hypoechoic. In this study, 95% of nodes had a transverse diameter of 8 mm or less, similar to results in the normal Caucasian population.6 However, when we evaluated size based on the long axis of the node, the majority of nodes in the cervical chain, supraclavicular fossa, and posterior triangle were larger than 8 mm. This is also similar to the results in previous reports in Caucasians, which showed that cer- Figure 6 Histogram showing the distribution of nonnal cervical lymph nodes. -l.l.t- 0.2' '.(. 23.7'.0 ~7. 5~ - Numb r of lymph nodl's JUltrasound Med 15: , 1996 vical nodes except submental and submaxillary groups usually demonstrate a larger longitudinal diameter and a shorter transverse diameter. Nodes greater than 8 mm in transverse diameter are generally considered to be metastatic.2 However, size alone is not a useful indicator of benignity or malignancy; rather, it is the increasing size of a node that is more useful in detecting malignancy.2t Shape has been stated to be a useful criterion in differentiating normal or reactive nodes from malignant nodes. An oval node indicates normal or reactive nodes, whereas malignant nodes tend to be round./ In the eight regions of the neck, all normal lymph nodes were oval with the exception of the submandibular and parotid nodes. About 95% of submandibular nodes and 60% of parotid nodes appeared round. Nodal shape thus would seem to have little value in differentiating between normality and malignancy for lymph nodes in these areas. The echogenic hilus is considered to be a normal sonographic feature of the lymph nodes.23 In this study, most of the lymph nodes (75% to 100%) possessed an echogenic hilus. However, as there were only two nodes in the lower cervical region and eight nodes in the supraclavicular fossa, further evaluation of these areas will be required for more accurate assessment. About 98% of submandibular nodes have an echogenic hilus. This might be a useful sonographic sign to indicate normality of these particular nodes. In this study, 49% of nodes had a sharp border whereas 51 % demonstrated unsharp borders. Nodes with unsharp borders were seen predominantly in the submental (86%), submandibular (779: ), parotid (74%), and upper cervical (55'A ) areas, whereas nodes in the middle cervical (97%) and lower cervical (100%) regions, supraclavicular fossa (100%), and posterior triangle (70%) were sharply outlined. However, since the number of nodes in lower cervical region (two nodes) and supraclavicular fossa (eight nodes) are too small, the result may not truly indicate the status of nodes in these areas. The high frequency of unsharp borders of submental, submandibular, and parotid nodes may be due to poor transducer contact, as these nodes are under the ramus of the mandible, and may also be related to the deposition of fat within the nodes.24 Thus, nodes with sharp borders are seen predominantly in lower neck and posterior triangle, whereas unsharp nodes are common in the upper neck. When we compared the relationship between S/ L ratio and lymph node size, we found that with increasing short axis of the node the S/ L ratio also increased, whereas with increasing long axis of the

5 J Ultrasound Med 15: , 1996 YING ETAL 435 Table 1: Ultrasonographic Features of the Normal Lymph Nodes in Different Regions of the Neck Features of Nodes 2 3 Regions of the Neck Number 1 node 73.7% 53.7% 71.9% 2 nodes 23.7% 42.1% 21.9% 0::3 nodes 2.6% 4.2% 6.2% Shape S/L < % 4.9% 40.7% S/L0:: % 95.1% 59.3% Echogenic hilus Present 80.0% 97.9% 86.0% Absent 20.0% 2.1% 14.0% Nodal border Sharp 14.0% 23.1% 25.6% Unsharp 86.0% 76.9% 74.4% Short axis <5mm 92.0% 27.3% 95.3% 5-Smm 8.0% 55.9% 4.7% >8mm 0.0% 16.8% 0.0% Long axis <5mm 10.0% 3.9% 20.9% 5-Smm 60.0% 36.7% 53.5% >8mm 30.0% 59.4% 25.6% % 97.3% 100.0% 85.7% 22.6% 43.3% 2.7% 0.0% 14.3% 36.4% 3.1% 0.0% 0.0% 0.0% 41.0% 95.1% 97.4% 100.0% 75.0% 98.2% 4.9% 2.6% 0.0% 25.0% 1.8% 82.9% 78.9% 100.0% 75.0% 80.8% 17.1% 21.1 % 0.0% 25.0% 19.2% 44.6% 97.4% 100.0% 100.0% 70.5% 55.4% 2.6% 0.0% 0.0% 29.5% 48.8% 97.4% 100.0% 87.5% 91.9% 47.0% 0.0% 0.0% 12.5% 6.8% 4.2% 2.6% 0.0% 0.0% 1.3% 0.0% 2.6% 0.0% 0.0% 0.2% 1.0% 13.2% 0.0% 62.5% 6.4% 99.0% 84.2% 100.0% 37.5% 93.4% node the S/L ratio decreased. Although the S/L ratio increased when the short axis increased, the correlation coefficient (r) that indicated this relationship was not strong enough to apply to most of the nodes (r = 0.62), an exception was the submental nodes.25 Similarly, when the S/L ratio decreased with increasing the long axis, the correlation coefficient (r) was also not applicable (r = 0.57). In determining normality of nodes, various size criteria have been used. Hajek and colleaguesb and Solbiati and coworkers15 suggested 5 mm transverse diameter as a upper limit of normal cervical nodes, whereas Bruneton and coworkers6 suggested 8 mm as the upper limit. Others have combined shape and size to identify normal or abnormal nodes. Sugama and Kitamural noted that metastatic nodes usually were round with a transverse diameter of 1 cm, whereas Tohnosu and associates? suggested that nodes with a S/L ratio greater than 0.5 (i.e., round,) and a long axis greater than 1 cm were metastatic. We combined size and shape and used 5 mm, 8 mm, and 1 cm as cut-off point (in short and long axes). When we plotted a graph of shape against size (short axis), we found that with 5 mm as cut-off point, 56% fulfilled both criteria for normality; with 8 mm as cutoff point, 68% fulfilled both criteria; and with 1 cm as cut-off point, 70% fulfilled both criteria for normality. When we combined the shape and long axis, we found that with 5 mm as cut-off point, only 0.4% fulfilled both criteria, with 8 mm only 6.6% fulfilled both criteria, and with 1 cm only 16.6% had both parameters normal. Results showed that the present size criteria combined with the S/L ratio to indicate normality of nodes were valid only for the short axis and were not suitable for the long axis because only few lymph nodes satisfied both conditions of normality. Therefore, nodal size (short axis) greater than 10 mm combined with an 5/L ratio greater than 0.5 may be useful to identify pathologic nodes. Similar findings also have been reported by Sugama and coworkers,l who.showed that lymph nodes with a transverse diameter of 10 mm and an S/ L ratio greater than 0.5 were likely to be metastatic. CONCLUSION This study establishes criteria for normal cervical lymph nodes in the adult Chinese population. Normal nodes are found in all the subjects, particu larly in the submandibular area, upper cervical chain, and the posterior triangle. The majority of the nodes are hypoechoic, with a maximum transverse diameter less than 8 mm. The majority of nodes in

6 436 NORMAL CERVICAL LYMPH NODES IN CHINESE POPULATION J Ultrasound Med 15: , 1996 the submandibular area and parotid region are round, but in all other regions of the neck they are oval, and most demonstrate an echo genic hilus. Nodes in the lower neck and posterior triangle have sharp borders, whereas those in the upper neck have unsharp borders. The S/L ratio is unreliable in the submandibular area and parotid region, as these nodes normally have an 5/L ratio greater than 0.5. The present established size criteria (5 mm, 8 mm, 10 mm) when combined with an S/ L ratio, are more useful when measurements are made in the maximum transverse diameter rather than the length of the node. REFERENCES 1. Sugama Y, Kitamura S: Ultrasonographic evaluation of neck nnd suprad avicular lymph nodes metastasized from lung cancer. Intern Med 31: 160, Bruneton JN, Roux P, Caramella E, et al: Ear, nose, and throat cancer: Ultrasound diagnosis of metastasis to cervical lymph nodes. Radiology 152:771, Gerrits CJH, van Overhagen H, van Lom K, et al: Ultrasound examination of pathological cervical lymph nodes in patients with non-hodgkin's lymphoma and Hodgkin's disease. Br J Haematol88:626, Sakai F, Kiyono K, Sone S, et al: Ultrasonic evaluation of cervical metastatic lymphadenopathy- J Ultrasound Med 7:305, Marchal G, Oyen R, Verschakelen J, et al: Sonographic appearance of normal lymph nodes. J Ultrasound Med 4:417, Bruneton JN, &tu-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, Tohnosu N, Onoda 5, 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 (5 / L) and the cancer content. J Clin Ultrasound 17:101, Hajek PC, Salomonowitz E, Turk R, et at: Lymph nodes of the neck: Evaluation with US. Radiology 158:739, Evans RM, Ahuja A, Metreweli C: The linear echogenic hilus in cervical lymphadenopathy-a sign of benignity or malignancy. Clin Radiol47:262, Sako K, Pradier RN, Marchetta FC, et al: Fallibility of palpation in the diagnosis of metastases to cervical nodes. Surg Gynecol Obstet 118:989, lshii JI, Amagasa T, Tachibana T, et a): US and CT evaluation of cervical lymph node metastasis from oral cancer. J Craniomaxillofac Surg 19:123, Mancuso AA, Maceri D, Rice D, et al~ CT of cervical lymph node cancer. AJR 136:381, van den Brekel MWM, Stel HV, Castelijns JA, et al: Cervical lymph node metastasis: Assessment of radiologic criteria. Radiology 177:379, Vassallo P, Edel G, Roos N, et al: In-vitro high resolution ultrasonography of benign and malignant lymph nodes: A sonographic pathology correlation. Invest Radiol 28:698, Solbiati L, Cioffi V, Ballarati E: Ultrasonography of the neck. Radio) Clin North Am 30:941, Som PM; Lymph nodes of the neck. Radiology 165:593, Lindberg R: Distribution of cervical lymph node metas tases from squamous cell carcinoma of the upper respi ratory and digestive tracts. Cancer 29:1446, Swartz JD, Yussen PS, Popky GL: Imaging of the neck: Nodal disease. Crit Rev Diagn Imaging 31 :413, DuBrul EL: Sicher's oral anatomy. London, CV, Mosby Company, 1980, p Bruneton JN, Normand F, Balu Maestro C, et al: Lymphomatous superficial lymph nodes: US detection. Radiology 165:233, Vassallo P, Wemecke K, Roos N, et at: Differentiation of benign from malignant superficial lymphadenopathy: The role of high-resolution US. Radiology 183:215, 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 169:113, Rubaltelli L, Proto E, Salmaso R, et al: Sonography of abnormal lymph nodes in vitro: Correlation of sonographic and histologic findings. AjR 155: 1241, Shozushima M, Suzuki M, Nakasima T, et al: Ultrasound diagnosis of lymph node metastasis in head and neck cancer. Dento Maxillofac Radiol19:165, Portney LG, Watkins MP: Foundations of Clinical Research: Application to Practice. Norwalk, CT, Appleton & Lange, 1993, p 442