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Radiotherapy and Oncology 85 (2007) 146–155

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Educational review

Anatomical bases for the radiological delineation of lymph node


areas. Major collecting trunks, head and neck
Benoı̂t Lengeléa, Marc Hamoirb, Pierre Scallietc,*, Vincent Grégoirec
a
Department of Experimental Morphology, bDepartment of Oto-rhino-laryngology and Head and Neck Surgery, and cDepartment of Radiation
Oncology, Université Catholique de Louvain, Brussels, Belgium

Abstract
Cancer spreads locally through direct infiltration into soft tissues or at distance by invading vascular structures,
then migrating through the lymphatic or blood flow. Although cancer cells carried in the blood can end in virtually
any corner of the body, lymphatic migration is usually stepwise, through successive nodal stops, which can
temporarily delay further progression. In radiotherapy, irradiation of lymphatic paths relevant to the localisation of
the primary has been common practice for decades. Similarly, excision of cancer is often completed by lymphatic
dissection.
Both in radiotherapy and in surgery, advanced knowledge of the lymphatic pathways relevant to any tumor location is
an important information for treatment preparation and execution. This first part describes the major collecting trunks
of the lymphatic system and then the lymphatics of the head and neck providing anatomical bases for the radiological
delineation of lymph node areas in the cervical region, it adds to the existing nomenclature of six nodal levels (I-VI),
three new areas listed as parotid, buccal and external jugular levels.
c 2007 Elsevier Ireland Ltd. All rights reserved. Radiotherapy and Oncology 85 (2007) 146–155.

Keywords: Anatomy; Lymphatics; Head and neck cancer; Radiotherapy; CTV; Cancer

Cancer spreads locally through direct infiltration into soft • Halsted (1895): Breast cancer is a disease that progresses
tissues, or at distance by invading vascular structures, then in a centrifugal and contiguous fashion. Thus improved
migrating through the lymphatic or blood flow. Although local control should decrease the frequency of metasta-
cancer cells carried in the blood can end in virtually any cor- ses and death from cancer [11].
ner of the body, lymphatic migration is usually stepwise, Halsted recommended radical mastectomy for ‘‘the
through successive nodal stops, which can temporarily delay cure of cancer of the breast’’. It was progressively
further progression. In radiotherapy, irradiation of lympha- replaced by more conservative surgery, associated with
tic paths relevant to the localisation of the primary has been radiotherapy, called in to sterilise invisible foci of tumour.
common practice for decades. The rationale was based on • B. Fisher (1980): Breast cancer is a systemic disease
the conventional chronological sequence: (1) primary tu- involving a complex spectrum of host-tumour interac-
mour – (2) invaded lymph nodes – (3) distant metastases tions; (. . .) variations in effective local regional treat-
(blood born), and the derived belief that a loco-regional can- ment are unlikely to affect survival substantially. Only
cer could be cured before further spreading if the primary systemic treatment is [5].
along with its drainage nodes were irradiated ‘‘en bloc’’. A more composite picture is accepted today, where
This paradigm has been largely challenged. The core cancer can spread through lymphatic, or through blood
issue was to determine whether cancer is a systemic vessels or both. To the question: are invaded lymph
disease from the onset, in which case emphasis should nodes simply a marker of systemic disease? The answer
be put upfront on systemic treatment, or if it remains is sometimes yes, sometimes not.
local for some times before metastasising, in which • S. Hellman (1994): Breast cancer is a heterogeneous dis-
case emphasis should be put on cancer screening and ease – a spectrum ranging from a disease that remains
active treatment of the early loco-regional disease. To local throughout its course to a disease which is systemic
say that the debate has been hot is a euphemism. when first detectable. Thus there could be situations
Breast cancer epitomises this controversy. Three eras where metastases would develop as a consequence of
can be isolated: residual inadequately treated loco-regional disease [14].


0167-8140/$ - see front matter c 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.radonc.2007.02.009
B. Lengelé et al. / Radiotherapy and Oncology 85 (2007) 146–155 147

The recent publication in The Lancet of the Early Breast mental foramina, lateral edges of the sternum and the
Cancer Trialist Cooperative Group overview of recent ran- two bony edges of the pubic symphysis are indeed suscepti-
domised trials strongly supports this last opinion. Loco- ble to draining in both sides of the body. This, of course,
regional radiotherapy after breast surgery always offers should be appreciated in view of the clinical situation, nota-
a survival advantage, though in proportions varying with bly nodal invasion on one side can redirect the lymphatic
the primary stage [4]. flow in the opposite side.
In this respect, detailed anatomical knowledge of the dy-
What applies to breast cancer presumably also applies to namic lymphatic network associated with each area of the
the other major cancer (lung, prostate, colo-rectal, head body is essential to define all the sites in which the presence
and neck), and a precise knowledge of both the anatomical of metastatic nodes should be investigated in tumour
location and the invasion probability of nodal areas draining assessment and staging, but also to delineate on a rational
a primary tumour is fundamental. morphological basis the optimal target volumes to be trea-
This paper is the first of a series of three, intending to ted by conformal radiotherapy [15].
summarize state-of-the-art knowledge regarding the lym-
phatic network in the human body. It makes use of modern
imaging to illustrate this knowledge, in a useful way for the
radiation oncologist and the dosimetrist faced with the General anatomy of the lymphatic system
arduous task to ‘‘contour’’ lymphatic CTVs on reference
The lymphatic system is constituted of numerous fine
anatomical (CT and/or MR) cross-sections.
vessels, which traverse several groups of nodes and trans-
This paper does however not discuss the appropriateness
port the lymph into the venous system. The capillaries of
of lymphatic irradiation, as it depends on tumour type,
origin have closed extremities which are disseminated with-
stage and location, i.e. a score of information impossible
in the connective tissues beyond the epithelial lining and
to capture in a single paper. That aspect of the question
which through several interconnecting anastomoses form
was dealt with in the recent publication of Gregoire, Scalli-
primary networks which drain the lymphatic fluid into the
et and Ang [7].
first collecting ducts. Passing through the successive groups
Part I deals with the major collecting trunks and the head
of lymph nodes, these ducts again divide into capillaries and
and neck region. It adds to the existing nomenclature of the
then finally give rise to the larger collecting vessels which
six nodal areas three new regions: the parotid area, the buc-
are usually two in number: the thoracic duct and right lym-
cal level and the external jugular level. These levels are rel-
phatic duct, which join the left and right brachiocephalic
evant to facial skin, scalp, orbital, eyelids and nasal
veins, respectively [1].
vestibule tumours, whereas the conventional areas num-
The lymphatic vessels have very thin endothelial walls,
bered I to VI refer to cancer of the upper aerodigestive tract.
are filled with a clear colourless fluid, and are usually not
visible in living tissue so that various staining or radio-opa-
que substances have to be injected before their distribution
and general pathways can be studied. In the small intestine
The lymphatic system however, they have a milk-white appearance during the
The anatomical study of the lymphatic system shows that immediate postprandial period, which explains their original
it consists of two superficial and deep networks of lymph ves- name of ‘lacteal veins’. They possess numerous valves
sels, which converge within each part of the body into deep which result in a characteristic moniliform appearance
lymph node areas. Located in the lateral regions of the neck, and are present in all tissues of the human body except
the root of the limbs, the central part of the chest and along for avascular structures such as the epidermis, the cornea
the large arteries and veins of the abdomen and pelvis, these and the cartilage. They are also absent in the brain, spinal
lymph nodes areas share the common characteristics of being cord, and bone marrow.
filled with fat, centred on large blood vessels, and well cir- According to their location, the lymphatic vessels branch
cumscribed by specific muscular bellies and fasciae. In most into two networks located, respectively, above and below
cases, the anatomical landmarks used to delineate these vol- the deep fasciae [29]. The superficial lymph vessels drain
umes on sequential radiological sections are quite similar to the skin and the subcutaneous tissue and tend to run along-
those used by surgeons during dissection procedures side the superficial veins, though some may be indepen-
[12,19,28]. However, the lymphatic drainage of each organ dently situated. Vessels of the deep subfascial network
involves several functional pathways including the main col- similarly course alongside the arteries and veins. They are
lecting chains, but also alternative routes which are not al- connected to the nodes, and unite to form deep main lym-
ways considered in current surgical practice. Taking this phatic channels which are usually located at the outer sur-
functional plasticity of the lymphatic system into account, face of the large veins. In rare cases, however, some of
the radiological delineation of the target volumes may thus them may pass behind the venous blood vessels. Such an
exactly match their surgical boundaries in the case of specific arrangement, which was already emphasised by Poirier
tumour locations, but in other malignancies it should extend two centuries ago, appears to be of major clinical impor-
beyond these narrow limits to include the entire potential tance not only for surgical dissection of the lymphatic
volume of their multidirectional lymphatic spread. chains, but also for the radiological delineation of the main
Bilaterality is another complex notion to appreciate. lymph node areas which are invariably located on the super-
Typically, structures lying in the space between the two ficial aspect of the large deep veins [18].
148 Delineation of head and neck lymph node areas

A relative separation exists between the lymph vessels of During its course, tributaries from the intercostal and pos-
the epi- and subfascial plexuses. Nevertheless, anastomoses terior mediastinal nodes flow into the thoracic duct. At its ori-
occur between both networks which as a rule lead the gin in the cisterna chyli, it drains both lumbar trunks that
superficial channels to drain into the deeper channels collect lymph from the lower limbs, the pelvis and the poster-
[24]. On the other hand, a large number of connecting chan- ior abdominal walls, together with large intestinal trunks
nels unite neighbouring ducts so that most of the lymphatic originating from all parts of the intra-abdominal digestive sys-
areas of the body communicate freely with the adjacent re- tem [18]. In the neck, the thoracic duct is joined by the left
gions. Major drainage pathways are thus constituted from jugular trunk from the left side of the head and neck, the left
the proximal capillary networks originating in the peripheral subclavian trunk from the left upper limb, and the left bron-
organs through collecting ducts which penetrate the lymph chomediastinal trunk which usually collects the ascending
nodes and finally rejoin the main ducts. Some of these path- lymph from the left chest viscera together with the parietal
ways cross the midline, while others directly reach the tho- lymphatic channel from the parasternal nodes [30].
racic duct without traversing any node [22]. From one
region, several distinct pedicles also extend that reach The right lymphatic duct
the same distal destination but take different routes with Described by Poirier and Charpy as the great lymphatic
various intermediate nodal relays. When considering these vein, the right lymphatic duct (Fig. 1) is formed by the un-
anatomical aspects, for each organ or topographical area ion of the right jugular, subclavian and bronchomediastinal
it is possible to define a preferential pathway of lymphatic trunks which collect the lymph from the right half of the
drainage, which is also the principal means of lymphatic head and neck, the right upper limb, the right side of the
spread for neoplastic or inflammatory cells in pathological thorax and right lung, and part of the convex surface of
situations [28]. On this main axis, the first targeted lymph the liver, respectively [18]. The duct measures about 1 cm
node is called the ‘sentinel node’. Nevertheless, the large in length and runs along the medial side of the scalenus
number of alternative connecting channels, combined with anterior, displays a large number of variations in the conflu-
the plasticity of the lymph vessels which have a marked ence pattern of its tributaries and finally enters the venous
capacity for regeneration after obstruction or damage, pro- system at Pirogoff’s angle, located at the junction of the
vide the lymphatic system with a dynamic functional struc- right subclavian and internal jugular veins [29].
ture in which all the areas described below have a constant
anatomical location, but display variable circulating rela-
tionships and a relative independence from the neighbour-
ing regions [10].
Lymphatics of the head and neck
Following the general arrangement of the lymphatic sys-
tem in the various parts of the body, the lymph nodes of the
head and neck area (Fig. 2) consist of superficial and deep
Major collecting ducts groups of nodes which form a transverse collar along the
The thoracic duct cervicocephalic junction and then a vertical chain which lies
The thoracic duct (Fig. 1) drains the lymph from the subdi- under the sternocleidomastoid muscle, along the large ves-
aphragmatic part of the body and from the left chest, left sels of the neck and the last cranial nerves, from the base of
upper limb and left part of the head and neck, back into the the skull downwards to the supraclavicular area. All these
blood circulation. Originating from the cisterna chyli located nodes are connected by numerous small vessels within the
in front of the first and second lumbar vertebrae, it enters the loose adipose tissue between the superficial, pretracheal
thorax through the aortic hiatus of the diaphragm and then and prevertebral laminae of the cervical fascia. These ves-
follows the anterior aspect of the vertebral column to reach sels give rise to a complex subcutaneous and subfascial lym-
the posterior mediastinum [26]. Usually not visible on com- phatic network, and, with the interposed node groups,
puted tomography (CT) or magnetic resonance (MR) images, constitute major and accessory chains which following a
it occupies a narrow space between the azygos vein on its specific pattern drain all the visceral and cutaneous parts
right, the hemi-azygos vein on its left, the thoracic vertebrae of the face and neck regions. In each area there is an ipsilat-
located posteriorly, and the aorta and oesophagus on its ante- eral drainage pathway into the main jugular or accessory
rior surface (Fig. 1). At the level of the fourth thoracic verte- chains. However, some median skin areas and organs lo-
bra the duct then inclines to the left, running along the cated posteriorly in the facial region have bilateral path-
posterior aspect of the aortic arch and then along the left side ways of lymphatic drainage with significant clinical
of the oesophagus behind the origin of the subclavian artery. implications in the treatment of head and neck cancers.
Reaching the lower part of the neck through the left side of
the thoracic inlet, it finally arches laterally near the trans- Lymph node groups of the pericervical circle
verse process of the seventh cervical vertebra, crosses over The pericervical circle (Fig. 2) is divided into five nodal
the prescalenic portion of the subclavian artery and finally groups which are named according to their specific location.
ends by opening into the area between the left internal jugu- They can be distinguished according to where they are situ-
lar and subclavian veins. At this point, a valvular bicuspid sys- ated, i.e. their position from posterior to anterior: the
tem prevents the blood from being sent back into the occipital, mastoid, parotid, submandibular and submental
terminal part of the duct, but sometimes inducing blockage groups [30]. Additional, often isolated nodes are classified
of the latter by metastatic cellular thrombi [26,29]. as the facial and retropharyngeal groups [15].
B. Lengelé et al. / Radiotherapy and Oncology 85 (2007) 146–155 149

Fig. 1. Major collecting ducts of the lymphatic system. An anterior anatomical view of the main ducts and trunks, with the corresponding
anatomical and CT sections at the thoracic level. The key structures for the delineation of the thoracic duct area (green frame) are as follows:
the azygos (AZ) and hemiazygos veins (HAZ), thoracic aorta (Ao) and the oesophagus (Oe). TD, thoracic duct; RLV, right lymphatic duct; ST,
subclavian trunks; JT, jugular trunks; BMT, bronchomediastinal trunks; CC, cisterna chyli; LT, lumbar trunks; PST, presacral trunk; DT,
digestive trunks; IC, intercostal nodes.

• The occipital nodes are usually from one to three in num- as the subcutaneous pre-auricular node, it drains lymph
ber. Lying near the lateral insertions of the trapezius from the frontal skin, the eyelids and the conjunctiva
muscle, they always occupy a subfascial plane and into the intraparotid nodes which lie within the parotid
receive their afferent vessels from the posterior part of space. Among these, the superficial intraparotid nodes
the hairy scalp. Their efferent vessels run downwards in are usually two to three in number, and are situated on
the posterior cervical triangle and join the upper part the external surface of the gland beneath the parotid fas-
of the posterior cervical accessory chain. cia. On the contrary, the deep intraparotid nodes are
• The mastoid nodes are located in the retro-auricular scattered throughout the glandular tissue and are mainly
area, lie superficially to the attachments of the sterno- grouped along the external carotid artery and the intra-
cleidomastoid muscle and are covered by the fascial parotid part of the external jugular vein. One of these
extension of the auricularis posterior. Draining the tem- nodes is invariably situated in the lower extremity of
poral region of the hairy scalp, the posterior surface of the gland near the mandibular angle. All these intrapar-
the auricle and the posterior wall of the external acous- otid nodes mainly receive their afferent vessels from
tic meatus, they have efferent vessels which traverse the the anterior surface of the auricle, the anterior wall of
upper insertions of the sternocleidomastoid muscle to the external acoustic meatus, the tympanum, the frontal
join the superior deep lateral cervical lymph nodes. and temporal areas, and the root of the nose. Neverthe-
• The parotid nodes are divided into four subgroups less, some of the deep intraglandular nodes are also con-
according to their specific relationship with the parotid nected to the subparotid nodes which are located
gland and its fascial sheath [22]. The most superficial between the parotid gland and the pharynx near the ret-
of these nodes is situated in the subcutaneous tissue, rostylian space. In close contact with the internal carotid
immediately in front of the tragus. Usually characterised artery and internal jugular vein, these nodes receive
150 Delineation of head and neck lymph node areas

belly of the digastric muscle, cranially by the mylohyoid


muscle and laterally by the medial surface of the mandi-
ble, from the mylohyoid line downwards to its basilar
border. The submandibular nodes are usually from three
to ten in number and are located on the bony and cuta-
neous surfaces of the submandibular gland, although
some may be found on its deep surface facing the mus-
cles of the floor of the oral cavity. One node is always
present at the anterior end of the gland, while the others
are located between the gland and the mandible, in front
of and behind the facial artery where the latter curves
around the bone. Additional nodes in this group also sur-
round the course of the facial vein on the cutaneous sur-
face of the gland, or are embedded in the glandular
tissue itself. Their afferent vessels arise in the following
areas: the alae, dorsum and tip of the nose, the cheek,
the mandibular and maxillar alveolar ridges, the upper
lip and lateral part of the lower lip, and finally the ante-
rior third of the lateral borders of the tongue. Their
efferent vessels cross the hyoid bone and terminate in
the upper deep lateral cervical nodes.
• Some of the afferent lymphatic vessels to the submandib-
ular nodes make an additional relay in small facial nodes,
also described as genian or buccal nodes [22]. Located
under the superficial musculo-aponeurotic layer of the
face, these small nodes are distributed throughout the
oblique course of the facial vessels in the infra-orbital
area (malar node), within the nasogenian groove (nasola-
bial nodes), on the outer surface of the buccinator mus-
cle near Stenon’s duct (buccinator node), or between the
anterior border of the masseter and the posterior border
of the depressor anguli oris, beneath the platysma (man-
dibular node).
• The submental nodes are located within the median
suprahyoid triangle bounded posteriorly by the body of
the hyoid bone and laterally by the medial borders of
both anterior bellies of the digastric muscles. Lying in a
subfascial plane, the submental nodes rest on the outer
surface of the mylohyoid muscles and display a variable
Fig. 2. Lymphatic nodes of the head and neck. Lateral view of the arrangement between the mandibular symphysis anteri-
superficial and deep node groups of the cervicocephalic region.
orly and hyoid bone dorsally. Their afferent vessels drain
Node groups are identified by different colours corresponding to the
surgical and radiological classification given in Fig. 3. B, buccal n.;
the integuments of the chin, the central part of the lower
DAJ, deep anterior jugular n.; DiP, deep intraparotid n.; F, facial lip, the floor of the oral cavity, and finally the tip of the
n.; iH, infrahyoid n.; JD, jugulodigastric n. (Kütner’s); JO, jugulo- tongue. Often decussating over the midline, their effer-
omohyoid n. (Poirier’s); LDC, superior (s), middle (m) and inferior ents join the nodes of the submandibular group or pass
(i) lateral deep cervical n.; LsC, lateral supraclavicular n.; M, malar directly in the middle deep cervical lymph nodes [18].
n.; MsC, medial supraclavicular n.; PDC, superior (s), middle (m) • Located behind the cephalic part of the pharynx, the ret-
and inferior (i) posterior deep cervical n.; M, mastoid n.; pA, ropharyngeal nodes can be considered the deepest-
preauricular n.; pL, prelaryngeal n.; pT, pretracheal n.; R, seated part of the peri-cervical circle. Facing the longus
recurrent n.; SAJ, superficial anterior jugular n.; sA, subauricular capitis that covers the lateral mass of the atlas, these
n.; SEJ, superficial external jugular n.; SiP, superficial intraparotid
nodes are usually two in number and occupy the narrow
n.; sMd, submandibular n.; sMt, submental n.; sO, suboccipital n.;
sP, subparotid n.; rPh, retropharyngeal n.
space between the prevertebral and peri-pharyngeal fas-
ciae. They are laterally located, are highly inconstant on
afferent lymph vessels from the nasal cavities, the naso- the midline and are in close relation with the pharyngeal
pharynx and the eustachian tube. Also linked to the ret- constrictors anteriorly and the internal carotid artery lat-
ropharyngeal nodes, they share the caudal drainage of erally. They receive afferent vessels from the nasophar-
the intraparotid nodes into the superior nodes of the ynx, the eustachian tube and the soft palate [2]. Their
deep lateral cervical chains. efferent vessels pass behind the internal carotid artery
• The submandibular nodes are located beneath the cervi- to mainly reach the upper deep cervical lymph nodes.
cal fascia in the submandibular triangle. The latter is Nevertheless, some of them drain into the nodes of the
bounded medially by the lateral border of the anterior subparotid group [23].
B. Lengelé et al. / Radiotherapy and Oncology 85 (2007) 146–155 151

Descending cervical chains vessels from the upper and middle node groups of the
The cervical chain nodes are distributed within the ante- chain, and also drain the lymph vessels from the supra-
rior and lateral areas of the neck, mainly alongside the var- clavicular nodes. Their efferent vessels drain into the
ious jugular veins (Fig. 2). Most of them form part of the jugular trunk or directly into the right or left collecting
deep lateral cervical chain which runs along the lateral side ducts [18].
of the internal jugular vein located deep within the sterno-
cleidomastoid muscle, and which drains directly into the
jugular lymphatic trunk [22]. Other nodes, however, join The deep posterior cervical chain
to form alternative pathways i.e. the posterior cervical The deep posterior cervical nodes are distributed within
accessory chain, the superficial external jugular chain, the posterior cervical triangle, bounded anteriorly by the
and two anterior cervical chains known as the superficial posterior border of the sternocleidomastoid, posteriorly by
anterior jugular chain and the deep prelaryngo-tracheal the anterior border of the trapezius and inferiorly by the
chain. In the lower part of the neck, a paratracheal recur- clavicle. They are usually small in size and round, and are
rent chain is also present [29]. situated on the dorsal aspect of the internal jugular vein,
on the muscular bellies of the splenius, levator scapulae
The deep lateral cervical chain and scaleni muscles [20]. Embedded in the cellulo-adipose
The deep lateral cervical chain is variably described as tissue that occupies the space between the superficial and
the carotid, internal jugular or substernomastoid chain. deep laminae of the cervical fascia, they show close rela-
Extending from the tip of the mastoid process downwards tionships with the branches of the cervical plexus cranially,
to the clavicle, it contains three groups of large lymph and with those of the brachial plexus in the subclavian area.
nodes, which are always arranged in a chain parallel to Depending on their location in the upper, middle and lower
the antero-lateral side of the internal jugular vein medially parts of the posterior cervical triangle, they can be classi-
and located beneath the sternocleidomastoid muscle later- fied into three successive groups [29]:
ally [22]. According to their respective locations, these
nodes are termed superior (upper), middle or inferior (low- • The superior posterior cervical nodes are located in the
er) deep lateral cervical nodes [21,30]. narrow apex of the triangle, above the point where the
spinal accessory nerve exits the posterior border of the
• The lymph nodes of the superior deep lateral cervical deep surface of the sternocleidomastoid muscle. They
group lie in the triangular area delineated by the poster- are connected to the occipital nodes and drain the lymph
ior belly of the digastric muscle cranially, the upper third from the posterior hairy scalp [13].
of the internal jugular vein dorsally and the thyrolinguo- • The middle posterior cervical nodes surround the subcu-
facial venous trunk caudally. Also known as Kütner’s jug- taneous course of the accessory nerve. Occupying the
ulodigastric nodes, they receive afferent vessels from the middle part of the posterior cervical triangle, they are
parotid, submandibular and submental groups but are linked proximally to the submandibular and retropharyn-
also directly connected to lymphatic vessels that drain geal nodes and thus collect the lymph from the naso- and
the tongue and the oropharynx. Their efferents extend oro-pharyngeal regions in addition to the nuchal region.
to the nodes of the middle and lower groups of the lateral Distally, their efferents terminate in the nodes of the
cervical chain, or directly join the jugular trunk [22]. supraclavicular group.
• The middle deep lateral cervical nodes are related to the • The inferior posterior cervical nodes occupy the supra-
middle third of the internal jugular vein. Usually less clavicular or subclavian area, and are situated distally
numerous and smaller in size than those of the upper to the posterior belly of the omohyoid muscle. They
group, they are located between the hyoid bone and cri- are connected to one another, and form a slightly oblique
coid cartilage, above the point where the intermediate chain directed anteriorly and located around their
tendon of the omohyoid muscle crosses the internal jug- accompanying anatomical structure, i.e. the cervical
ular vein. Usually one of these nodes displays greater transverse artery. Their main afferent vessels originate
development than the others. It lies directly on the inter- from the upper (supraspinal) and middle (perispinal)
mediate tendon of the omohyoid and is known as Poiri- groups of the posterior cervical chain. However, these
er’s jugulo-omohyoid node. Most of the afferent vessels infraspinal supraclavicular nodes also drain additional
in this group arise from the upper deep lateral cervical lymphatic vessels from the integuments of the arm and
nodes, while the efferents descend into the lower nodes. pectoral regions, and sometimes efferent vessels from
However, Poirier’s main node is also connected to the the axillary nodes [26].
efferent vessels from the submandibular and submental
nodes [18]. Furthermore, the latter receives direct path-
ways that drain the tongue and the floor of the oral cavity The superficial lateral cervical chain
[3,25]. The superficial external jugular chain extends along the
• The inferior deep lateral cervical nodes lie between the external jugular vein and includes three to five superficial
distal part of the sternocleidomastoid muscle and the cervical nodes situated on the outer surface of the sterno-
lower third of the internal jugular vein. Their area is cleidomastoid muscle. Collecting the lymph from the lobule
limited cranially by the omohyoid muscle and caudally of the auricle, the floor of the acoustic meatus and the skin
by the sternal end of the clavicle. They receive afferent over the angle of the mandible, the highest node of the
152 Delineation of head and neck lymph node areas

group is usually located near the point where the external Functional drainage pathways
jugular vein leaves the lower extremity of the parotid gland Arising from the various superficial or visceral parts of
[22]. Distally, the efferent vessels of this subcutaneous chain the cephalic region, the lymphatics of the head and neck
pass around the borders of the sternocleidomastoid muscle follow several drainage pathways depending on their origin
to enter the middle or lower deep lateral cervical nodes. (Fig. 3). Taking into consideration the usual metastatic no-
dal extensions that can develop in malignant tumours from
The anterior cervical chains various sites, these preferential pathways can be classified
The superficial anterior jugular chain runs parallel to the as follows [15,21]:
anterior jugular vein and comprises two to three small
inconstant nodes located between the superficial and pre- • The main lymphatic pathway starts from the submental
tracheal lamina of the cervical fascia at the surface of the nodes (level Ia) and passes through the submandibular
infrahyoid muscles. Draining the lymph from the anterior (level Ib) and anterior jugulodigastric (level IIa) groups.
cervical skin regions, these nodes are connected proximally So reaching the upper part of the internal jugular chain,
to those of the submental group and their efferent vessels the lymph then descends along the middle (level III) and
extend into the nodes of the deep lateral cervical chain. lower (level IV) deep lateral cervical nodes and finally
Distally, the lower node occupies the suprasternal space reaches the jugular collecting trunk. Connected proxi-
and can sometimes use the bronchomediastinal trunk as mally to the parotid and buccal groups of nodes, this cen-
an efferent pathway [18]. tral pathway basically drains the superficial areas of the
The deep anterior cervical chain contains several small face and the anterior segments of the oral and nasal
lymph nodes which are situated beneath the lamina pretra- cavities.
chealis of the cervical fascia and usually below the infrahy- • The posterior accessory pathway originates from the pos-
oid muscles, immediately in front of the larynx and trachea. terior part of the jugulodigastric group (level IIb) and
Depending on their specific location, they are referred to as thereafter traverses the middle (level Va) and lower
the infrahyoid, prelaryngeal and pretracheal nodes, and are (level Vb) deep posterior cervical groups. So running suc-
usually represented by a single inconstant node at each le- cessively alongside the accessory nerve and alongside the
vel [30]. If present, the infrahyoid node is located in front transverse cervical vessels, this additional lymphatic
of the thyrohyoid membrane. The prelaryngeal node, known pathway offers an alternative means of drainage to the
as the ‘delphian’ node, is present on the cricothyroid mem- deep dorsal parts of the visceral cavities of the face
brane, in the narrow V-shaped space between the two crico- including the nasopharynx, the oropharynx, the velum
thyroid muscles. Finally, the pretracheal nodes are spread and the root of the tongue.
along the anterior aspect of the trachea in close relation • The anterior lymphatic pathway is connected with the
with the isthmus of the thyroid gland cranially and caudally drainage of the median part of the lower lip, the anterior
with the inferior thyroid veins. All these nodes receive their oral floor and the apex of the tongue. It follows direct
afferent vessels from the glottic and subglottic parts of the connecting channels spread between the submental
larynx, the hypopharynx and the thyroid gland. Their effer- (level Ia) and the jugulo-omohyoid (level III) nodes or,
ent vessels run downwards into the inferior nodes of the more rarely, reaching the lower internal jugular (level
main internal jugular chain [18,22,27]. IV) nodes. This alternative anterior pathway of nodal dis-
The recurrent chain is associated with the recurrent lar- semination explains the routine clinical observation of
yngeal nerve. Deeply located in the visceral spaces of the inferior cervical skip metastases developing in the course
neck, these nodes are very small and usually remain unrec- of anterior tumours of the oral cavity. In cases of super-
ognised during a cervical surgical procedure. Scattered ficial or deep tumours located in the anterior cervical tri-
within the areolar adipose tissue between the trachea and angle (level VI), these may also extend along the
the oesophagus, they form a chain which continues caudally superficial or deep anterior cervical chains, respectively,
without any clear demarcation with the tracheobronchial before reaching the distal part of the main lymphatic
group. As afferents, these nodes receive the lymphatic ves- pathway (level IV). Efferent vessels from the anterior
sels from the inferior laryngeal pedicle, the lateral lobes of cervical triangle never seem to drain distally in the upper
the thyroid gland and the cervical parts of the trachea and mediastinal lymph nodes although these nodes, located
oesophagus. Their efferent vessels usually terminate in the below the sternal notch in front of the large neck vessels,
lower deep lateral cervical or supraclavicular nodes. They have sometimes been grouped in an additional cervical
never seem to drain into the neighbouring upper mediastinal level coded VII. Despite the obvious topographic continu-
node groups [18,26,29]. ity that exists between the lower part of the anterior

c
Fig. 3. Surgical and radiological delineation of head and neck lymph node areas. Node groups are currently classified into six levels (I–VI) to
which should be added the parotid (P), retropharyngeal (rp) and buccal (B) areas. An additional external jugular level (VIII, in fact real VII)
should also be considered. The corresponding volumes are delineated on anatomical sections and corresponding CT images of the head and
successive neck regions, respectively. The key structures for the delineation of the various target volumes are as follows: the
sternocleidomastoid (SCM), infrahyoid (IH), digastric (D), pterygoid (Pt), longus capitis (LC), scaleni (S), splenius (Sp), levator scapulae (LS)
and trapezius (T) muscles. Other landmarks are the internal (IJV), external (EJV), anterior (AJV) and posterior (PJV) jugular veins, the facial
vein (FV), the submandibular (SMG) and thyroid glands (TG), cervical transverse artery (CTA) and the facial (FN), lingual (LN), vagus (VN) and
spinal accessory (SAN) nerves. Legends and colours used to indicate the node groups are identical to those in Fig. 2.
B. Lengelé et al. / Radiotherapy and Oncology 85 (2007) 146–155 153
154 Delineation of head and neck lymph node areas

cervical neck space and the upper mediastinum, there is • The jugulocarotid area (Fig. 3,C1–C6) forms a long
no anatomical or functional rationale to consider any inverted pyramid which comprises the three groups of
intrathoracic node group as being part of the efferent the deep lateral cervical chain and extends from the cra-
cervical pathways [15,21]. nial base downwards to the clavicle. Its surfaces are
• Finally, the superficial lateral pathway is associated bounded laterally by the deep surface of the sternoclei-
with the external jugular chain. Connected to the domastoid, medially by the large vessels of the neck,
occipital and the mastoid node groups, it terminates and posteriorly by the prevertebral muscles. This area
in the deep main pathway. Functionally speaking, it is is filled with adipose tissue and in addition to the blood
solely linked with the lymphatic drainage of the integ- vessels also contains the lymphatic structures of levels
uments of the posterior scalp and retro-auricular area II, III and IV and the vagus nerve.
[13,15]. • The posterior cervical area (Fig. 3,C1–C6) is the last
pyramidal-shaped volume located adjacent to the dorsal
In this complex lymphatic network consisting of numer- side of the previous area. Distally based in the supracla-
ous vessels and nodes, each tumour has a preferential vicular zone, it has a narrow apical part located in the
pattern of dissemination whereby metastases enter the suboccipital plane. The volume then enlarges progres-
main chain, often invading a first group of nodes depend- sively in a caudal direction, and its lateral subcutaneous
ing on where the primary tumour is located. From that face follows the posterior border of the sternocleido-
point however, further spread may also follow several dif- mastoid and the anterior border of the trapezius.
ferent routes, for instance via the anterior or posterior Responding anteriorly to the posterior face of the caro-
additional pathways. The more anterior the primary site, tid artery and internal jugular vein, it is bounded dor-
the greater the likelihood of the potential involvement sally by the bellies of the deep cervical muscles.
of the anterior chain [16,17,21]. Conversely, the deeper Including the lymphatic vessels and nodes of the poster-
seated the tumour, the higher the risk of lymphatic ior and transverse cervical chains (level V), this dorsal
metastases in the posterior accessory and transverse cer- cellulo-adipose area also contains the accessory nerve,
vical chains [23]. When considering the three potential the nerve roots of the cervical and brachial plexuses
chains of dissemination, cancer of the tongue provides a and the transverse cervical vessels.
clear example of this anatomical and functional reality
[20,25]. In addition to these four main lymphatic areas, there are
four laminar zones that circumscribe the buccal, anterior
cervical, external jugular and retropharyngeal areas
Delineation of lymph node areas (Fig. 3,C1–C3).
As an immediate corollary of the anatomical landmarks
mentioned in the previous description, the lymph node • The buccal area is located between the nasolabial fold
areas of the head and neck can be identified on CT or anteriorly and the anterior border of the masseter pos-
MR images as four pyramidal-shaped volumes correspond- teriorly. Bounded superiorly by the infraorbital fora-
ing exactly to the anatomical spaces cleared by the men, it extends downwards to the lower mandibular
surgeon performing a parotidectomy and a neck dissection edge and contains the satellite lymph nodes of the
(Fig. 3) [6–9]. facial vessels.
• The anterior cervical area (Fig. 3,C5–C6) is located in
• The parotid area (Fig. 3,C1) is a cranially-based pyra- front of the larynx and the trachea with the lateral bor-
midal space bounded anteriorly by the pterygoid mus- ders of the infrahyoid muscles as external boundary.
cles and the mandibular ramus, and posteriorly by a Extending from the hyoid bone to the suprasternal notch,
plane following the anterior border of the sternocleido- it crosses the midline and contains the superficial and
mastoid, the posterior belly of the digastric muscle and deep anterior cervical chains (level VI), connected to
the stylian muscles. Its lateral surface faces the skin, the anterior jugular veins.
and its apex is located at the point where the sterno- • The external jugular area (Fig. 3,C3–C6) forms a narrow
cleidomastoid muscle encounters the mandibular angle. plane extending over the external surface of the sterno-
This space contains the parotid gland, the facial nerve, cleidomastoid muscle and should be considered as an
the external carotid and jugular vessels, in addition to additional cervical level (level VIII, in fact real level
the pre-auricular, superficial and deep parotid nodes VII). Covered superficially by the thin layer of the pla-
[15]. tysma, it includes the superficial lateral cervical lymph
• The submental and submandibular nodes lie within the nodes and the external jugular vein.
pyramidal volume between the inner side of the mandi- • The retropharyngeal area (Fig. 3,C1) is located at the
ble laterally and the suprahyoid muscles medially. The level of the first two cervical vertebrae between the lat-
inferior surface of this submandibular area (Fig. 3,C3) eral half of the posterior pharyngeal wall and the prever-
faces the platysma at a subcutaneous level. Its apex cor- tebral muscles. More laterally this space, which contains
responds to the mandibular symphysis and its base is the retropharyngeal nodes, then becomes continuous
bounded by the hyoid bone. In addition to level I nodes, with the retrostylian space containing the subparotid
this space contains the submandibular gland, the facial nodes, internal carotid artery, the proximal part of the
vessels, and on its medial wall, the vascular and nerve internal jugular vein and the last four cranial nerves (this
bundles of the tongue. area was recently re-discussed by Bussels et al. [2]).
B. Lengelé et al. / Radiotherapy and Oncology 85 (2007) 146–155 155

dissect the apex of level V in mucosal head and neck cancer.


* Corresponding author. Pierre Scalliet, Department of Radia-
Head & Neck 2005;27:963–9.
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Catholique de Louvain, Cliniques Universitaires Saint Luc, 10 small breast cancers. J Clin Oncol 1994;12:2229–34.
Avenue Hippocrate, 1200 Brussels, Belgium. E-mail address: [15] Lengele BG. The lymphatic system. In: Gregoire V, Scalliet P,
pierre.scalliet@imre.ucl.ac.be Ang KK, editors. Clinical target volume in conformal and
intensity modulated radiotherapy. A clinical guide to cancer
Received 15 January 2007; received in revised form 30 January treatment. Berlin, Heidelberg, New York: Springer Verlag;
2007; accepted 6 February 2007; Available online 23 March 2007 2004. p. 1–36.
[16] Lindberg R. Distribution of cervical lymph node metastases
from squamous cell carcinomas of the upper respiratory and
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