Clinical Radiology (2003) 58: 351–358 doi:10.1016/S0009-9260(02)00584-6, available online at www.sciencedirect.

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Review Sonography of Neck Lymph Nodes. Part I: Normal Lymph Nodes
M . Y I N G * , A . A H U JA † *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: þ 8522632-2290; Fax: þ 852-2636-0012; E-mail: aniltahuja@cuhk.edu.hk 0009-9260/03/$30.00/0

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

q 2003 The Royal College of Radiologists. Published by Elsevier Science Ltd. All rights reserved.

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

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

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

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

Fig. Hajek et al. 32. Although.34]. small intranodal arteries and veins. [29] and Ying et al. The shape of lymph nodes is usually assessed by the S:L ratio.4) 93 22 67 82 78 76 76 86 98 79 91 89 76 42 89 81 95 92 93 70 91 80 63 69 84 66 91 80 82 81 oral cavity predisposes to the development of reactive hyperplasia in the upper neck nodes. but not with the age and sex [24]. different optimum cut-off values of the maximum transverse diameter were found in different regions of the neck (Table 2) [35]. respectively) [8]. 4 – Power Doppler sonogram of a normal cervical lymph node showing central hilar vascularity (arrows). Bruneton et al.7) (0. Optimum short axis when combined with the optimum S:L ratio Sensitivity (%) Specificity (%) PPV (%) NPV (%) Accuracy (%) 3 mm 8 mm 5 mm 4 mm 3 mm 3 mm (0. The shape of normal cervical nodes varies in various regions of the neck [8].5.31. when the optimum S:L ratio and maximum transverse diameter of the lymph nodes are combined. Fig. The echogenic hilus was previously considered to be intranodal fatty tissue [30. especially those that are small. However. and fatty tissue.5) (0. 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]. However.5) (0. Echogenic Hilus An echogenic hilus is a normal sonographic feature of most normal cervical lymph nodes (75– 100%) [8]. 0. An oval node indicates normality (Fig. difficult to differentiate from the surrounding soft tissue [24]. 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]. i. Solbiati et al.32.32]. A lymph node with an S:L ratio less than 0. 3).5 is commonly used as the cut-off value in differentiating normal and abnormal nodes [4.34]. [31] subsequently noted that the echogenic hilus consisted of sinuses. [37] suggested that the echogenic pattern of the nodal hilus mainly corresponds to the presence of lymphatic sinuses. and Shape Shape has been suggested to be a useful criterion in distinguishing normal from malignant nodes. [31] suggested that the normal upper limit of the maximal short axis axial diameter of the cervical lymph node is 5 mm. whereas an S:L ratio greater than or equal to 0.33]. About 90% of normal cervical lymph nodes with maximum transverse diameter greater than 5 mm showed an echogenic hilus [36].3) (0.31. S:L $ 0. 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]. whereas malignant nodes tend to be round [4.e. [22] and Solbiati et al.8. Also. the normal submandibular and parotid nodes are usually round.5. apparently avascular. short axis to long axis ratio.5 (95 and 59%.5 indicates round node [7. Rubaltelli et al.31. Fatty infiltration also makes the lymph nodes. 5 – Power Doppler sonogram showing a normal cervical node without any vascular signal (arrows).5 is oval in shape. However. [8] reported that normal cervical lymph nodes have a maximal short axis axial diameter of 8 mm or less.356 CLINICAL RADIOLOGY Table 2 – Performance of optimum short axis and optimum S:L ratio in different regions of the neck Regions Submental Submandibular Parotid Upper cervical Middle cervical Posterior triangle S:L.7.4) (0. 3). . 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. but is more commonly seen in larger nodes than in smaller nodes (Fig. 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. one should note that a higher cut-off also results in a lowered sensitivity.

5] who reported that the echogenic hilus corresponds to the abundance of collecting sinuses. does not vary with age. Roos N. however. Therefore. but none should show peripheral vascularity [25]. Brook F. but does not vary significantly between men and women [24]. This is probably due to the smaller size of the lymph nodes in these regions. There is no racial difference in the incidence of echogenic hilus within cervical lymph nodes [23]. Lameris JS. it is difficult to collect adequate tissue volume from small lymph nodes (less than 4 mm in maximal short axis axial diameter) and from post-radiation nodes. [4. Ying M. Differential diagnosis of lymph node lesions: a semiquantitative approach with colour Doppler ultrasound. Wernecke K. the parotid and posterior triangle nodes tend to be apparently avascular (52 and 60%. which makes detection of intranodal vasculature difficult [25]. whereas there is no significant difference in PSV between lymph nodes in different regions [25]. 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