Sonography of Neck Lymph Nodes. Part I: Normal Lymph Nodes

Clinical Radiology (2003) 58: 351 358 doi:10.1016/s0009-9260(02)00584-6, available online at www.sciencedirect.com Review Sonography of Neck Lymph Nodes. Part I: Normal Lymph Nodes M. YING*, A.AHUJA *Department of Optometry and Radiography, The Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong SAR, People s Republic of China and Department of Diagnostic Radiology and Organ Imaging, Prince of Wales Hospital, Shatin, New Territories, Hong Kong SAR, People s Republic of China Received: 16 July 2002 Revised: 13 November 2002 Accepted: 20 November 2002 Grey scale and power Doppler sonography play an important role in assessment of cervical lymphadenopathy. However, before examination of pathological nodes, a clear understanding of the anatomy of cervical nodes, scanning technique and sonographic appearances of normal cervical nodes is essential. This article reviews these topics in order to provide a baseline for sonographic examination of cervical lymphadenopathy. Ying, M., Ahuja, A. (2003). Clinical Radiology 58: 351 358. q 2003 The Royal College of Radiologists. Published by Elsevier Science Ltd. All rights reserved. Key words: ultrasound, cervical lymph nodes, normal. INTRODUCTION Assessment of cervical lymph nodes is important for patients with head and neck carcinomas, and is useful in determining patient prognosis, and in selecting treatment [1 5]. High-resolution sonography has been commonly used to evaluate cervical lymphadenopathy and the role of greyscale sonography in the assessment of cervical lymph nodes is well established [4 8]. With the advent of power Doppler sonography (PDS), the distribution of intranodal vessels and perfusion of the cervical nodes can be evaluated, and the bloodflow velocity and vascular resistance of the intranodal vessels can also be measured [9 13]. Grey-scale ultrasound has a high sensitivity (97%), and a high specificity (93%) when used in conjunction with ultrasound-guided fine-needle aspiration cytology (FNAC) [2]. It has also been reported that ultrasound-guided FNAC is more accurate than the conventional or blinded FNAC in differentiating metastatic and non-metastatic cervical nodes, with fewer false-negative (1 and 8%, respectively) and false-positive (1 and 5%, respectively) findings [14]. Familiarity with lymphatics is essential for examination of Guarantors of study: Dr M. Ying and Dr A. Ahuja. Author for correspondence: Dr Anil Ahuja, Department of Diagnostic Radiology and Organ Imaging, Prince of Wales Hospital, Shatin, New Territories, Hong Kong SAR, People s Republic of China. Tel: þ852-2632-2290; Fax: þ852-2636-0012; E-mail: aniltahuja@cuhk.edu.hk the head and neck. For the beginner, ultrasound evaluation of neck nodes may be a daunting prospect because there are approximately 800 lymph nodes in the body and 300 of them are in the neck. The nodes vary in size from 3 to 25 mm, are embedded within the soft tissues of the neck either partly or completely surrounded by fat. However, most of the neck nodes are quite superficial in location and are readily identified by high-resolution ultrasound, and despite the complicated anatomy of the neck, the location, distribution and draining areas of these nodes is fairly constant. Therefore if the radiologist is familiar with the anatomy and the sonographic appearances of these nodes, assessing them is not as difficult as it first seems. NORMAL ANATOMY Cervical lymph nodes are solitary structures composed of lymphoid tissue and are distributed along the course of lymphatic vessels in the neck. Each is divided into two main regions, the cortex and the medulla. The cortex is composed of densely packed lymphocytes, which group together to form spherical lymphoid follicles. The intermediate area between the cortex and the medulla is known as the paracortex, and is a transitional area for lymphocyte migration [15 17]. The medulla of the lymph node is composed of medullary trabeculae, medullary cords, and medullary sinuses. The 0009-9260/03/$30.00/0 q 2003 The Royal College of Radiologists. Published by Elsevier Science Ltd. All rights reserved.

352 CLINICAL RADIOLOGY medullary trabeculae have a similar composition to the capsule, whereas the structural base for the medullary cords and medullary sinuses is the reticular tissue, which is composed of reticulum cells. As medullary trabeculae are composed of dense connective tissue, similar to the capsule, and have a wellestablished network branching from the capsule, they provide guidance for blood vessels and nerves to other regions of the lymph node. The medullary cords are arranged in a parallel pattern and contain numerous lymphoid cells, mainly plasma cells and small lymphocytes. The medullary sinuses are filled with lymph and are part of the sinus system of the lymph node [15 17]. Similar to the lymph nodes in other body regions, cervical lymph nodes are permeated by blood vessels. The main artery enters the lymph node at the hilus, where it branches into several smaller arteries and arterioles. In the cortex, arterioles further branch off into several sinuous capillaries and supply the lymphoid follicles, as well as the lymphocytes. Some of the arterioles reach the capsule via trabeculae of the lymph node and then anastomose with other branches [16 18]. The venous system consists of venules, small veins and a main vein, which have a similar route to the hilus as the arterial system. In the cortex, the venules converge to form small veins. In the medulla, the small veins further converge to form the main vein, which leaves the lymph node at the hilus [16 18]. CLASSIFICATION OF LYMPH NODES The cervical lymph nodes used to be classified into groups according to their location in the neck (Table 1). However, due to the complexity and difficulty of this classification, the American Joint Committee on Cancer (AJCC) classification is now commonly used, especially by surgeons and oncologists. The AJCC classification divided palpable cervical lymph nodes into seven levels, or groups, which are based on the extent and level of cervical nodal involvement by metastatic tumour (Fig. 1) [19 21]. Although the AJCC classification is now commonly used in identifying the location of lymph nodes, some important nodes, such as the parotid and retropharyngeal nodes, are not incorporated into this classification [21]. As the AJCC classification is not limited to ultrasound but is also used in computed tomography (CT) and magnetic resonance imaging (MRI), some of the lymph nodes included in this classification system may not be accessible by ultrasound, such as the prelaryngeal, paratracheal and upper mediastinal nodes. Another classification of lymph nodes, which is also based on the location of the lymph nodes was established by Hajek et al. [22] to simplify ultrasound examination of the neck. The lymph node regions are classified into eight regions according to the location in the neck (Fig. 2). One must note, that this classification is merely to simplify the sonographic examination of the neck. It is designed to ensure that a radiologist examines all areas in the neck in a systematic way in order not to miss a lesion. It does not reflect the staging of cancers which is based on the AJCC classification. Fig. 1 Schematic diagram of the neck showing the AJCC classification of cervical lymph nodes. Level I nodes are submental and submandibular nodes; level II nodes are upper internal jugular chain nodes; level III nodes are middle internal jugular chain nodes; level IV nodes are lower internal jugular chain nodes; level V nodes are spinal accessory chain nodes and transverse cervical chain nodes; level VI nodes are anterior cervical nodes; level VII nodes are upper mediastinal nodes. EQUIPMENT AND SCANNING TECHNIQUE A 7.5 MHz linear transducer is the basic requirement for ultrasound examination of the neck. Higher frequency Fig. 2 Schematic diagram of the neck showing the classification of the cervical lymph nodes to facilitate the evaluation of nodal distribution with ultrasound. 1 Submental, 2 submandibular, 3 parotid, 4 upper cervical (above the level of hyoid bone), 5 middle cervical (between the level of hyoid bone and cricoid cartilage), 6 lower cervical (below the level of cricoid cartilage), 7 supraclavicular fossa, 8 posterior triangle.

THE SONOGRAPHY OF NECK LYMPH NODES. PART I: NORMAL LYMPH NODES 353 Table 1 Classification of cervical lymph nodes according to their location in the neck Nodal groups Locations Number of nodes Drainage areas Efferent pathways Submental Submental triangle 1 to 8 Chin Submandibular nodes Middle part of lower lip Cheeks Anterior gingiva Floor of mouth Lower incisors Tip of the tongue Submandibular Submandibular triangle 3 to 6 Lateral chin Internal jugular chain nodes Upper lip Lower lip (except medial part) Cheeks Nose Anterior nasal cavity Gums Teeth except lower incisors Palate Medial part of the eyelids Floor of mouth Submandibular and sublingual salivary glands Parotid Extra-parotid: pre-auricular Extra-parotid: 3 to 4 Skin of the head and neck Internal jugular chain nodes Parotid glands Subcapsular: pre-auricular and within the tail of the parotid gland Intra-glandular: within the superficial lobe and the fascia between the superficial and deep lobes Subcapsular: pre-auricular, 1 to 2; parotid tail, 3 to 4 Intra-glandular: 3 to 4 Forehead and temporal region Middle and lateral part of the face Auricle External auditory canal Eustachian tube Posterior cheek Buccal mucous membrane Gums Internal jugular chain Along the course of the internal jugular vein and adjacent to the carotid sheath 15 to 40 Submandibular, parotid and retropharyngeal nodes subclavian vein, internal jugular vein Right side: right lymphatic duct, Tonsil Left side: thoracic duct, subclavian vein, internal jugular vein Pharynx Larynx Oesophagus Thyroid glands Supraclavicular chain (transverse cervical chain) Above the clavicle and along the course of the transverse cervical vessels 1 to 10 Internal jugular nodes Right side: right lymphatic duct, subclavian vein, internal jugular vein Posterior triangle nodes Left side: thoracic duct, subclavian vein, internal jugular vein Infraclavicular areas Skin of the anterolateral part of the neck (continued on next page)

354 CLINICAL RADIOLOGY Table 1 (continued) Nodal groups Locations Number of nodes Drainage areas Efferent pathways Posterior triangle chain (spinal accessory chain) Along the course of the spinal accessory nerve and in the posterior triangle of the neck 4 to 20 Parotid region Supraclavicular chain and internal jugular chain Occipital region Lateral part of the neck Shoulder Anterior cervical Pre-tracheal chain: along the course of the anterior jugular vein and anterior to the strap muscles Pre-laryngeal chain: midline in location and anterior to the cricothyroid membrane Para-tracheal chain: lateral to the trachea and posterior to the thyroid in the tracheoesophageal groove 7 to 20 Pre-tracheal chain: skin and muscles of the anterior neck Pre-laryngeal chain: mainly the larynx Para-tracheal chain: supraglottic and subglottic larynx, pyriform sinus, thyroid, trachea and esophagus Right side: thoracic duct, anterior mediastinal node Left side: lowest internal jugular chain node, highest intrathoracic node Occipital Apex of the posterior triangle, between the occipital bone, sternomastoid and trapezius 3 to 10 Occipital region Posterior triangle chain Mastoid Behind the ear and near the mastoid process 1 to 4 Parotid region Parotid nodes Parietal area of the vault Upper internal jugular chain nodes Auricle External auditory meatus Facial Subcutaneous tissues of the face 5 to 10 Eyelids Submandibular nodes Cheek Middle portion of face Sublingual Between the genioglossus muscles and along the anterior lingual vessels Uncertain Tongue Submental nodes Floor of the mouth Submandibular nodes Internal jugular chain nodes Retropharyngeal Retropharyngeal space 2 to 5 Nasopharynx Upper internal jugular chain nodes Oropharynx

THE SONOGRAPHY OF NECK LYMPH NODES. PART I: NORMAL LYMPH NODES 355 transducer, i.e. 10 MHz or above, allows better resolution for superficial structures but there is a trade-off with a lack of penetration. A 5 MHz convex transducer is sometimes useful for the assessment of deep lesions, whereas the use of a standoff gel block may allow better visualization of large or superficial mass. Colour Doppler applications are now standard on most ultrasound machines, and beginners may find it useful for identifying vascular structures. However, there will be less dependence once they are familiar with the sonographic anatomy. PDS is desirable for the assessment of vasculature in small structures, such as lymph nodes and thyroid. When using PDS, the Doppler setting should be optimized for detecting small vessels, i.e.: high sensitivity low wall filter pulsed repetition frequency (PRF) 700 Hz medium persistence the colour gain is first increased to a level which shows colour noise, and then decreased to the level where the noise just disappears. PDS may be difficult for lesions adjacent to major artery and in uncooperative patients. It is because evaluation of vascular pattern of the lymph nodes is difficult when there is flash artefact due to movement of the lesions. Deep nodes in obese patients necks are also difficult to be evaluated with PDS. In measuring the vascular resistance (resistive index, RI; pulsatility index, PI), the more prominent vessels are usually selected. Measurements are obtained from the average of three consecutive Doppler spectral waveforms in order to get a more accurate value. The smallest sample volume should be chosen. If blood flow velocity (peak systolic velocity, PSV and end diastolic velocity, EDV) is measured, angle correction should be made at an angle of 608 or less. An adjustable and mobile examination table is essential in ultrasound of the neck, which allows easy positioning so that the patient s neck is at the level of the ultrasound monitor and within the scanning range of the operators. The patient should be positioned supine with the neck hyper-extended. A pillow or triangular soft pad should be placed under the shoulders and lower neck for support. The examination is started with a transverse scan of the submental area. The transducer is then swept laterally to one side of the neck while the patient s head rotates towards the opposite side to allow free manipulation of the transducer. The submandibular region is examined with a transverse scan along the inferior border of the mandibular body. The transducer should be angled cranially as some of the submandibular nodes are located in the submandibular niche hidden by the mandibular body. The parotid nodes are assessed with longitudinal and transverse scans along the ramus of the mandible. The internal jugular chain nodes are examined in transverse scan with the transducer scans along the internal jugular vein and common carotid artery from the tail of parotid gland to the junction between internal jugular vein and the subclavian vein. The internal jugular chain nodes can be divided into three groups: upper cervical (above the level of hyoid bone), middle cervical (between the level of hyoid bone and cricoid cartilage) and lower cervical (below the level of cricoid cartilage). From the lower cervical region, the transducer is then swept laterally to the supraclavicular fossa and the supraclavicular nodes are assessed with transverse scan. The posterior triangle nodes are examined with transverse scans from the mastoid and along the imaginary line of the spinal accessory nerve, which is between the sternomastoid and the trapezius. The same scanning protocol is used on the opposite side of the neck so that the major nodal chains in the neck are covered. The monitor should be positioned for comfortable viewing when performing a FNAC biopsy. A monitor with a moveable arm is ideal. The patient s neck should be close enough to the operator so that both the hand holding the transducer and the hand holding the needle or biopsy gun are relaxed. SONOGRAPHIC APPEARANCES OF NORMAL CERVICAL NODES Number and Distribution Normal cervical lymph nodes are detectable with ultrasound in healthy people. At least five or six normal cervical nodes are identified routinely by sonography [8,23], and there is no significant racial [23] or sexual [24] difference in the average number of normal cervical lymph nodes. The number of cervical lymph nodes that can be detected by ultrasound decreases with advancing age [24]. Among the different regions of the neck, normal cervical lymph nodes are commonly found in submandibular (19 23%), parotid (15 16%), upper cervical (18 19%) regions and posterior triangle (35 37%) [23 25]. Therefore, patients with multiple lymph nodes in other regions should raise the suspicion of pathology. Size The size of normal cervical lymph nodes varies with the location in the various regions of the neck, age and sex. Lymph nodes in the upper neck, including submandibular and upper cervical nodes, tend to be larger than the lymph nodes in other regions [8,26 29]. This may be because inflammation in the Fig. 3 Grey scale sonogram showing an oval, hypoechoic normal cervical lymph node (arrows). Note the echogenic hilus (arrowheads) continuous with the adjacent fat.

356 CLINICAL RADIOLOGY Table 2 Performance of optimum short axis and optimum S:L ratio in different regions of the neck Regions Optimum short axis when combined with the optimum S:L ratio Sensitivity (%) Specificity (%) PPV (%) NPV (%) Accuracy (%) Submental 3 mm (0.5) 93 76 76 93 84 Submandibular 8 mm (0.7) 22 86 42 70 66 Parotid 5 mm (0.5) 67 98 89 91 91 Upper cervical 4 mm (0.4) 82 79 81 80 80 Middle cervical 3 mm (0.3) 78 91 95 63 82 Posterior triangle 3 mm (0.4) 76 89 92 69 81 S:L, short axis to long axis ratio. oral cavity predisposes to the development of reactive hyperplasia in the upper neck nodes. Normal cervical nodes in younger subjects (aged 20 39 years) tend to be smaller than those in older subjects (aged $40 years) [24]. This is explained by the increase in intranodal fatty infiltration with age [30]. Fatty infiltration also makes the lymph nodes, especially those that are small, difficult to differentiate from the surrounding soft tissue [24]. The upper limit of the maximal short axis axial diameter for normal cervical nodes is controversial with two values being considered: 5 and 8 mm. Hajek et al. [22] and Solbiati et al. [31] suggested that the normal upper limit of the maximal short axis axial diameter of the cervical lymph node is 5 mm. However, Bruneton et al. [29] and Ying et al. [8] reported that normal cervical lymph nodes have a maximal short axis axial diameter of 8 mm or less. A maximal short axis axial diameter of 8 mm is preferred as the normal upper limit as it gives a higher specificity than a maximal short axis axial diameter of 5 mm. However, one should note that a higher cut-off also results in a lowered sensitivity. Shape Shape has been suggested to be a useful criterion in distinguishing normal from malignant nodes. The shape of lymph nodes is usually assessed by the S:L ratio. A lymph node with an S:L ratio less than 0.5 is oval in shape, whereas an S:L ratio greater than or equal to 0.5 indicates round node [7,8,31, 32,33]. An oval node indicates normality (Fig. 3), whereas malignant nodes tend to be round [4,5,7,31,32,34]. However, the normal submandibular and parotid nodes are usually round, S:L $ 0.5 (95 and 59%, respectively) [8]. Although, 0.5 is commonly used as the cut-off value in differentiating normal and abnormal nodes [4,5,31,32], it has been reported that the optimum cut-off value of S:L ratio is different in different regions of the neck (Table 2) [35]. Also, when the optimum S:L ratio and maximum transverse diameter of the lymph nodes are combined, different optimum cut-off values of the maximum transverse diameter were found in different regions of the neck (Table 2) [35]. The shape of normal cervical nodes varies in various regions of the neck [8], but not with the age and sex [24]. Echogenic Hilus An echogenic hilus is a normal sonographic feature of most normal cervical lymph nodes (75 100%) [8], but is more commonly seen in larger nodes than in smaller nodes (Fig. 3). This is because limited branching and separation of walls of the lymphatic sinuses and blood vessels in smaller nodes do not provide enough interfaces to reflect the ultrasound waves to make the hilus echogenic [36]. About 90% of normal cervical lymph nodes with maximum transverse diameter greater than 5 mm showed an echogenic hilus [36]. The echogenic hilus was previously considered to be intranodal fatty tissue [30,34]. Solbiati et al. [31] subsequently noted that the echogenic hilus consisted of sinuses, small intranodal arteries and veins, and fatty tissue. Rubaltelli et al. [37] suggested that the echogenic pattern of the nodal hilus mainly corresponds to the presence of lymphatic sinuses, and Fig. 4 Power Doppler sonogram of a normal cervical lymph node showing central hilar vascularity (arrows). Fig. 5 Power Doppler sonogram showing a normal cervical node without any vascular signal (arrows), i.e. apparently avascular.

THE SONOGRAPHY OF NECK LYMPH NODES. PART I: NORMAL LYMPH NODES 357 fatty tissue makes the echogenic nodal hilus more obvious but is not essential for its visualization. This was further proven by Vassallo et al. [4,5] who reported that the echogenic hilus corresponds to the abundance of collecting sinuses, which provide acoustic interfaces to reflect a portion of the ultrasonic wave, making the hilus echogenic. On ultrasound, the nodal hilus is seen to be continuous with the surrounding fatty tissue [8,38]. In routine clinical practice, radiologists should be aware that the absence of the echogenic hilus on grey-scale sonography does not imply the absence of hilar vascularity on PDS [39]. There is no racial difference in the incidence of echogenic hilus within cervical lymph nodes [23]. The incidence of visualizing-echogenic hilus within cervical nodes increases significantly with advancing age, but does not vary significantly between men and women [24]. The age-related variation of the incidence of echogenic hilus is believed to be due to the increased fatty deposition in lymph nodes in elderly, which makes the nodal hilum more obvious [24,30,36]. Vascular Features Normal cervical lymph nodes may show hilar vascularity (Fig. 4) or appear avascular (Fig. 5), but none should show peripheral vascularity [25]. Among the different regions of the neck, the parotid and posterior triangle nodes tend to be apparently avascular (52 and 60%, respectively). This is probably due to the smaller size of the lymph nodes in these regions, which makes detection of intranodal vasculature difficult [25]. The degree of vascularity of submental and submandibular nodes is significantly higher than that of other regional nodes. Submental nodes have a higher RI and PI, in association with lower EDV, than other regional nodes, whereas there is no significant difference in PSV between lymph nodes in different regions [25]. The incidence of detected vascular signals and blood flow velocity (PSV and EDV) within normal cervical nodes increases with the size of the nodes, and about 90% of normal cervical nodes with a maximum transverse diameter greater than 5 mm showed hilar vascularity [36]. The increased blood flow velocity in bigger nodes is probably explained by the fact that the vessels are larger in bigger nodes allowing faster flow of blood [36], which can be readily detected. The RI and PI does not vary with the size of lymph nodes. The degree of vascularity of normal cervical nodes is not related to the age or gender [25], but the detection rate of vascular signals and vascular resistance are significantly higher in elderly. This is thought to be due to the higher stiffness of vessels in the elderly making the small vessels less compressible, and thus blood flow is easily detected [25]. Blood flow velocity, however, does not vary with age. Blood flow velocity and vascular resistance do not vary between men and women [25]. With the use of spectral Doppler, the blood flow velocity (PSV and EDV) and vascular resistance (RI and PI) of normal cervical nodes can be measured. However, its role in routine clinical practice is very limited. Ultrasound and ultrasound-guided FNAC are useful methods to differentiate metastatic from non-metastatic cervical nodes [2,14]. Ultrasound-guided FNAC can detect metastasis in cervical lymph nodes when clinical examination, ultrasound, CT and MRI are negative [40]. Therefore, it has been suggested that ultrasound-guided FNAC should be used for patients with or without palpable nodes, and patients with or without positive findings in clinical or radiological examinations [40 42]. 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