Lymph Node Hilus. Gray Scale and Power Doppler Sonography of Cervical Nodes. Article

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1 Article Lymph Node Hilus Gray Scale and Power Doppler Sonography of Cervical Nodes Anil Ahuja, FRCR, Michael Ying, MPhil, Ann King, FRCR, Hok Yuen Yuen, FRCR Objective. To investigate the difference in the nodal hilus evaluated by gray scale and power Doppler sonography. Methods. One hundred ninety-two patients with proven cervical lymphadenopathy were included in the study (metastases, n = 118; tuberculosis, n = 56; and lymphoma, n = 18). Lymph nodes were evaluated by gray scale sonography for the echogenic hilus and power Doppler sonography for hilar vascularity. Results. Hilar vascularity was found even though the lymph node did not show an echogenic hilus on gray scale sonography (metastases, 59%; tuberculosis, 66%; and lymphoma, 91%). Conclusions. Sonologists should be aware that gray scale and Doppler sonography show different aspects of the hilus, and the absence of the hilus on gray scale sonography does not necessarily imply an associated absence of hilar vascularity. Key words: gray scale sonography; power Doppler sonography; hilus; cervical nodes. Abbreviations FNAC, fine-needle aspiration cytology; PDS, power Doppler sonography; PI, pulsatility index; RI, resistive index Received March 7, 2001, from the Department of Diagnostic Radiology and Organ Imaging, Prince of Wales Hospital, The Chinese University of Hong Kong, Shatin, Hong Kong. Dr Ying is now with the Department of Optometry and Radiography, The Hong Kong Polytechnic University, Kowloon, Hong Kong. Revision requested April 23, Revised manuscript accepted for publication May 22, Address correspondence and reprint requests to Anil Ahuja, FRCR, Department of Diagnostic Radiology and Organ Imaging, Prince of Wales Hospital, Shatin, New Territories, Hong Kong. The role of sonography in the evaluation of neck nodes is well established. Previously, sonography of lymph nodes involved only gray scale sonography, and evaluation of the nodal hilar architecture was an essential part of the examination. The absence of a hilus was usually considered an abnormality. 1,2 However, to our knowledge, the sonographic literature has not addressed whether the absence of an echogenic hilus on gray scale sonography implies the absence of hilar vasculature. With power Doppler sonography (PDS), it is now possible to evaluate intranodal vasculature. In our experience, often in abnormal nodes the echogenic hilar architecture is absent on gray scale imaging (Fig. 1), but the hilar vessels are clearly shown on PDS (Fig. 2). Because this has not been emphasized in the literature, often sonologists have presumed that the absence of the echogenic hilus on gray scale sonography also implies the absence of hilar vasculature. We were therefore interested in documenting the appearance of hilar vessels so that sonologists would be aware of the differences in nodal hilar evaluation by gray scale sonography and PDS by the American Institute of Ultrasound in Medicine J Ultrasound Med 20: , /01/$3.50

2 Lymph Node Hilus: Gray Scale and Power Doppler Sonography Figure 1. Gray scale longitudinal sonogram of a well-defined hypoechoic node with absence of an echogenic hilus. Materials and Methods A total of 192 nonconsecutive patients with enlarged abnormal nodes in the neck were included in this study. The patients had sonographic examinations because of the palpable neck nodes. None of the patients was studied twice. The discovery of nodes was the result of a systematic sonographic search in selected patients. These included 118 patients with metastatic neck nodes, 56 with tuberculous nodes, and 18 with lymphoma. There were 108 male and 84 female patients. The age range was 16 to 85 years. Figure 2. Power Doppler sonogram of the same node as in Figure 1 showing the presence of hilar vascularity. Lymph nodes were classified into 5 levels: level 1, submental and submandibular nodes; level 2, upper cervical chain nodes; level 3, middle cervical chain nodes; level 4, lower cervical chain nodes; and level 5, posterior triangle and supraclavicular nodes. The distribution of nodes provides clues in the differential diagnosis of cervical lymphadenopathy, because different pathologic nodes may have different distributions. 3,4 In each patient, first gray scale sonography was performed to evaluate the neck nodes. The gray scale features that help in identifying abnormal nodes include a round shape (short axis/long axis 0.5), the absence of an echogenic hilus, hypoechogenicity (compared with adjacent muscle), sharp margins, and the presence of intranodal necrosis. 3 The maximum transverse diameter of the nodes was also measured. In a patient with multiple nodes, PDS was performed on the largest node that showed the absence of an echogenic hilus and at least 2 other sonographic features of malignancy. Only nodes proved by fine-needle aspiration cytology (FNAC) were included in this study. All lymph nodes included in this study were palpable. All examinations were performed by the same sonologist (A.A.) using a 5- to 12-MHz transducer (HDI 5000; ATL Ultrasound, Bothell, WA). The vascular patterns and intranodal resistance were evaluated during realtime scanning. In all patients, PDS was performed using standardized parameters. 5 The power Doppler sonography settings were for high sensitivity with a low wall filter to allow detection of vessels with low blood flow. The pulse repetition frequency was 700 Hz, and medium persistence was used. The color gain was increased until background noise appeared and then reduced until the noise was suppressed, thus ensuring maximum sensitivity. 6,7 When consistent Doppler signals were obtained, the color map was used to guide placement of the pulsed Doppler gate, and tracings of the arterial signal were recorded using a sample volume of 1 mm. The vascular resistance was evaluated at random sites within 3 vessels that consistently showed 3 consecutive Doppler spectral waveforms. The mean resistive index (RI) and pulsatility index (PI) were estimated. 988 J Ultrasound Med 20: , 2001

3 Ahuja et al The vascular patterns of lymph nodes were classified into 3 main categories according to the location of the vascularity: (1) hilar, with flow signals branching radially from the hilus, regardless of whether the signals originated from the central region or from the periphery; (2) capsular (or peripheral), with flow signals along the periphery of the lymph nodes and branches perforating the periphery of the node and not arising from the hilar vessels; and (3) mixed, with the presence of hilar and capsular flow. Results A total of 26 metastatic nodes from infraclavicular primary tumors were included in this study. Most of the nodes (22 of 26) were present in the supraclavicular region of the neck (level 5). Eighteen nodes had maximum transverse diameters of 1 cm or greater. There were 33 nodes from head and neck squamous cell carcinomas. They were scattered in all regions of the neck. Fifteen (45%) of 33 were present in level 2, and 27 had maximum Metastatic nodes from papillary carcinoma (14) were equally distributed between levels 3 and 5, and 5 of the 14 nodes had maximum Metastatic nodes from nasopharyngeal carcinoma (45) were fairly equally distributed between levels 2 and 5, and 42 had maximum Of the 56 tuberculous nodes, 46 were present in level 5, and the remaining nodes were present in levels 1 and 2. Thirty-five nodes had maximum The lymphomatous nodes (18) were predominantly present in levels 2 and 5, and 16 had maximum transverse diameters of 1 cm or greater. Tables 1 and 2 summarize the appearance of the hilar architecture on gray scale sonography and PDS. Regardless of the presence or absence of an echogenic hilus, displaced hilar vascularity was common in tuberculous nodes (70% and 83%, respectively; Fig. 3). Table 3 summarizes the vascular resistance of nodes with and without an echogenic hilus. Table 4 shows the gray scale features of abnormal nodes. Table 5 shows the relationship between size and vascular patterns of different pathologic nodes. Table 1. Vascular Patterns of Different Pathologic Nodes With or Without an Echogenic Hilus Nodes Metastasis Tuberculosis Lymphoma With an echogenic hilus, n (%) Hilar 2 (20.0) 14 (70.0) 2 (28.6) Peripheral 0 (0.0) 0 (0.0) 0 (0.0) Mixed (hilar and peripheral) 8 (80.0) 6 (30.0) 5 (71.4) Avascular 0 (0.0) 0 (0.0) 0 (0.0) Without an echogenic hilus, n (%) Hilar 1 (0.9) 17 (47.2) 3 (27.3) Peripheral 39 (36.1) 5 (14.0) 0 (0.0) Mixed (hilar and peripheral) 63 (58.3) 7 (19.4) 7 (63.6) Avascular 5 (4.7) 7 (19.4) 1 (9.1) Discussion With the increasing use of high-resolution sonography in the head and neck, sonography combined with FNAC is often the initial modality of choice in evaluating enlarged neck nodes. Sonography of neck nodes in routine clinical practice consists of 2 parts, gray scale and Doppler sonography. Gray scale sonography is used to evaluate the size, shape, hilar architecture, intranodal necrosis, intranodal calcification, nodal border, nodal matting, and adjacent soft tissue edema. Doppler sonography is used to evaluate the presence and distribution of intranodal resistance and to estimate intranodal intravascular resistance. The following discussion will be limited to the echogenic hilus on gray scale sonography and the distribution of intranodal vascularity on PDS. The echogenic hilus seen on gray scale sonography of a node was previously thought to represent intranodal fat 8,9 within the lymph node. Table 2. Displacement of Hilar Vascularity in Different Pathologic Nodes Nodes Metastasis Tuberculosis Lymphoma With an echogenic hilus and with hilar vascularity present (including hilar only and mixed), n (%) Displaced hilar vessel 0 (0.0) 14 (70.0) 0 (0.0) Nondisplaced hilar vessel 10 (100.0) 6 (30.0) 7 (100.0) Without an echogenic hilus but with hilar vascularity present (including hilar only and mixed), n (%) Displaced hilar vessel 10 (15.6) 20 (83.3) 0 (0.0) Nondisplaced hilar vessel 54 (84.4) 4 (16.7) 10 (100.0) J Ultrasound Med 20: ,

4 Lymph Node Hilus: Gray Scale and Power Doppler Sonography Figure 3. Power Doppler sonogram of a hypoechoic node with displaced hilar vessels (arrows). Note the intranodal cystic necrosis (arrowheads). Table 3. Vascular Resistance in Different Pathologic Nodes Nodes Metastasis Tuberculosis Lymphoma With echogenic hilus RI PI Without echogenic hilus RI PI However, it is now generally accepted that the echogenic hilus is mainly the result of multiple fluid-filled sinuses, each of which acts as an acoustic interface, partially reflecting incident sound waves and imparting an echogenic structure. 1,10,11 The presence of an echogenic hilus within a node was considered a sign of benignity. 1,12 However, Evans et al 11 showed the presence of an echogenic hilus even in malignant nodes and suggested that its presence or absence cannot be taken as the sole deciding factor of whether a node is benign or malignant. On Doppler sonography, the patterns of vascular distribution within nodes have been described previously Normal nodes predominantly have hilar vascularity or are avascular. 16 The occurrence of vascularity in normal nodes increases with increasing size, and about 90% of normal nodes with maximum transverse diameters greater than 5 mm show hilar vascularity. 17 Reactive nodes tend to have prominent hilar vascularity 15,18 because of an increase in vessel diameter and blood flow. 14 In malignant nodes, 4 predominant abnormal vascular patterns have been described: avascular areas, displacement of vessels, increased peripheral vessels, and an aberrant course of hilar vessels. 19 The increase in peripheral nodal vascularity is due to the initial deposition of carcinoma cells in the marginal and medullary sinuses. The infiltrating tumor induces aberrant feeding vessels in the periphery of the tumor rests by tumor angiogenesis and sinusoid tumor vascularity within the tumor rests. In the later stages the capsule and perinodal tissues may be invaded. 13 As tumor infiltration of the node progresses, increased vascularity is seen in both the central and peripheral zones of the nodes. Power Doppler sonography is able to show this abnormal vascularity and to evaluate the distribution. Moreover, PDS in conjunction with spectral Doppler tracings can also estimate the intranodal vascular resistance, thus differentiating histologically proven benign and malignant nodes with a high degree of accuracy (83% 89% sensitivity and 76% 98% specificity). 13,14,20 In this study, 108 (91.5%) of 118 malignant nodes did not show the presence of the echogenic hilus on gray scale sonography. However, on PDS 63 (58.3%) of 108 nodes showed the presence of mixed (hilar and capsular) vascularity, 1 (0.9%) showed only hilar vascularity, 39 (36.1%) had peripheral vascularity, and 5 (4.7%) were avascular. In the tuberculous group, although 36 (64.3%) of 56 nodes did not show the echogenic hilus on gray scale sonography, 17 (47.2%) of 36 showed hilar vascularity; 7 (19.4%) showed mixed (hilar and capsular) vascularity; 7 (19.4%) were avascular; and 5 (14%) showed peripheral vascularity. In patients with lymphoma, 11 (61%) of 18 nodes showed no hilus on gray scale sonography, of which 7 (63.6%) of 11 had mixed vascularity (capsular and hilar); 3 (27.3%) had hilar vascularity; and 1 (11%) was avascular. In this study, displaced hilar vascularity was commonly found in tuberculous nodes, regardless of the presence or absence of an echogenic hilus (70% and 83%, respectively). This is probably due to the high incidence of intranodal cystic necrosis in tuberculous nodes (91%), which displaced the vascularity Therefore, displacement of hilar vessels is highly indicative of tuberculous lymphadenitis. 990 J Ultrasound Med 20: , 2001

5 Ahuja et al In metastasis and tuberculosis, higher RIs (0.81 and 0.72, respectively) and PIs (1.99 and 1.38, respectively) were noted in lymph nodes without an echogenic hilus compared with lymph nodes with an echogenic hilus. However, a lower RI (0.71) and PI (1.3) were found in lymphomatous nodes without an echogenic hilus. In clinical practice, diagnosis is made by excision biopsy or radial neck dissection if the results of FNAC are not conclusive. In this study, the diagnosis of all patients was made on the basis of FNAC. In FNAC, the sampling was obtained from both the lymph node cortex and hilus. Conclusion The sonologist must be aware that although the same node is evaluated with the same transducer, gray scale and Doppler sonography show different aspects of the hilus, and the absence of the hilus on gray scale sonography does not necessarily imply an associated absence of hilar vascularity. The absence of the echogenic hilus on gray scale sonography is due to tumor infiltration of the sinuses with distortion of the internal architecture, which no longer has multiple reflective surfaces. The hilar vessels may still remain patent (although displaced by tumor infiltration) and can be detected on Doppler sonography. References 1. Rubaltelli L, Proto E, Salmaso R, et al. Sonography of abnormal lymph nodes in vitro: correlation of sonographic and histologic findings. AJR Am J Roentgenol 1990; 155: Solbiati L, Rizzatto G, Bellotti E, et al. High-resolution sonography of cervical lymph nodes in head and neck cancer: criteria for differentiation of reactive versus malignant nodes. Radiology 1988; 169(P): 113. Abstract. 3. Ahuja A, Ying M, King W, et al. A practical approach to ultrasound of cervical lymph nodes. J Laryngol Otol 1997; 111: Ying M, Ahuja A, Brook F, et al. Sonographic appearance and distribution of normal cervical lymph nodes in a Chinese population. J Ultrasound Med 1996; 15: Table 4. Gray Scale Features of Different Pathologic Nodes Feature Metastasis Tuberculosis Lymphoma Shape, n (%) (85.6) 38 (67.8) 16 (88.9) < (14.4) 18 (32.2) 2 (11.1) Echogenic hilus, n (%) Absent 108 (91.5) 36 (64.3) 11 (61.1) Present 10 (8.5) 20 (35.7) 7 (38.9) Nodal margins, n (%) Sharp 93 (78.8) 24 (42.8) 16 (88.9) Not sharp 25 (21.2) 32 (57.2) 2 (11.1) Echogenicity, n (%) Hypoechoic 107 (90.7) 56 (100.0) 18 (100.0) Hyperechoic 11 (9.3) 0 (0.0) 0 (0.0) Intranodal necrosis, n (%) Present 25 (21.2) 51 (91.1) 1 (5.6) Absent 93 (78.8) 5 (8.9) 17 (94.4) Soft tissue edema, n (%) 1 (0.8) 20 (35.7) 0 (0.0) Matting, n (%) 0 (0.0) 26 (46.4) 0 (0.0) Table 5. Vascular Patterns in Different Pathologic Nodes of Different Sizes Hilar, Capsular, Mixed, Absent, Size, cm n (%) n (%) n (%) n (%) Metastasis <1 0 (0.0) 11 (42.3) 14 (53.9) 1 (3.8) (2.9) 21 (30.4) 43 (62.3) 3 (4.4) >2 1 (4.3) 7 (30.4) 14 (60.9) 1 (4.4) Tuberculosis <1 14 (66.7) 0 (0.0) 4 (19.0) 3 (14.3) (45.2) 5 (16.1) 8 (25.8) 4 (12.9) >2 0 (0.0) 0 (0.0) 1 (25.0) 3 (75.0) Lymphoma <1 1 (50.0) 0 (0.0) 1 (50.0) 0 (0.0) (27.3) 0 (0.0) 7 (63.6) 1 (9.1) >2 1 (20.0) 0 (0.0) 4 (80.0) 0 (0.0) 5. Ahuja AT, Ho SS, Leung SF, et al. Metastatic adenopathy from nasopharyngeal carcinoma: successful response to radiation therapy assessed by color duplex sonography. AJNR Am J Neuroradiol 1999; 20: Cosgrove DO, Kedar RP, Bamber JC, et al. Breast diseases: color Doppler US in differential diagnosis. Radiology 1993; 189: McNicholas MM, Mercer PM, Miller JC, et al. Color Doppler sonography in the evaluation of palpable breast masses. AJR Am J Roentgenol 1993; 161: Sakai F, Kiyono K, Sone S, et al. Ultrasonic evaluation of cervical metastatic lymphadenopathy. J Ultrasound Med 1988; 7: J Ultrasound Med 20: ,

6 Lymph Node Hilus: Gray Scale and Power Doppler Sonography 9. Marchal G, Oyen R, Verschakelen J, et al. Sonographic appearance of normal lymph nodes. J Ultrasound Med 1985; 4: Vassallo P, Wernecke K, Roos N, et al. Differentiation of benign from malignant superficial lymphadenopathy: the role of high-resolution US. Radiology 1992; 183: Evans RM, Ahuja A, Metreweli C. The linear echogenic hilus in cervical lymphadenopathy a sign of benignity or malignancy? Clin Radiol 1993; 47: Sutton RT, Reading CC, Charboneau JW, et al. USguided biopsy of neck masses in postoperative management of patients with thyroid cancer. Radiology 1988; 168: Ariji Y, Kimura Y, Hayashi N, et al. Power Doppler sonography of cervical lymph nodes in patients with head and neck cancer. AJNR Am J Neuroradiol 1998; 19: Wu CH, Chang YL, Hsu WC, et al. Usefulness of Doppler spectral analysis and power Doppler sonography in the differentiation of cervical lymphadenopathies. AJR Am J Roentgenol 1998; 171: Ahuja A, Ying M, Yuen YH, et al. Power Doppler sonography to differentiate tuberculous cervical lymphadenopathy from nasopharyngeal carcinoma. AJNR Am J Neuroradiol 2001; 22: Ying M, Ahuja AT, Evans R, et al. Cervical lymphadenopathy: sonographic differentiation between tuberculous nodes and nodal metastases from nonhead and neck carcinomas. J Clin Ultrasound 1998; 26: Ahuja A, Ying M, Evans R, et al. The application of ultrasound criteria for malignancy in differentiating tuberculous cervical adenitis from metastatic nasopharyngeal carcinoma. Clin Radiol 1995; 50: Wu CH, Shih JC, Chang YL, et al. Two-dimensional and three-dimensional power Doppler sonographic classification of vascular patterns in cervical lymphadenopathies. J Ultrasound Med 1998; 17: Giovagnorio F, Caiazzo R, Avitto A. Evaluation of vascular patterns of cervical lymph nodes with power Doppler sonography. J Clin Ultrasound 1997; 25: Ying M, Ahuja A, Brook F, et al. Power Doppler sonography of normal cervical lymph nodes. J Ultrasound Med 2000; 19: Ying M, Ahuja A, Brook F, et al. Vascularity and gray scale sonographic features of normal cervical lymph nodes: variations with nodal size. Clin Radiol 2001; 56: Na DG, Lim HK, Byun HS, et al. Differential diagnosis of cervical lymphadenopathy: usefulness of color Doppler sonography. AJR Am J Roentgenol 1997; 168: Castenholz A. Architecture of the lymph node with regard to its function. In: Grundmann E, Vollmer E (eds). Reaction Patterns of the Lymph Node. Part 1. Cell Types and Functions. New York, NY: Springer- Verlag; 1990: J Ultrasound Med 20: , 2001