CLINICAL REVIEW

Henry T. Hoffman, MD, Section Editor

FUNCTIONAL ANATOMY OF THE LYMPHATIC

DRAINAGE SYSTEM OF THE UPPER AERODIGESTIVE
TRACT AND ITS ROLE IN METASTASIS OF SQUAMOUS
CELL CARCINOMA
Jochen A. Werner, MD,1 Anja A. Dünne, MD,1 Jeffrey N. Myers, MD, PhD2
1
Department of Otolaryngology, Head and Neck Surgery, Philipps University Marburg, Deutschhausstr. 3,
35037 Marburg, Germany. E-mail: j.a.werner@mailer.uni-marburg.de
2
Department of Head and Neck Surgery, University of Texas M. D. Anderson Cancer Center, Houston, Texas

Accepted 28 October 2002

Published online 31 January 2003 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/hed.10257

Keywords: system; upper aerodigestive tract; head and neck

Abstract: Background. Although there is a significant under-
standing of the vascular anatomy of the upper aerodigestive tract
(UADT), there is less detailed knowledge of the architecture and
drainage patterns of the lymphatic system. Detailed knowledge of
the lymphatic system is critical for understanding the role of
sentinal node identification in the management of different can-
cers.
Methods. We have combined microscopic techniques with in
vivo and in vitro lymphographic studies to survey the architecture
and drainage patterns of the lymphatic system of the UADT in
850 organ specimens.
Results. These studies show an interaction of superficial and
deep lymphatic networks that vary in density but have a constant
distribution characterized by predictable patterns of lymph drain-
age into the regional lymph nodes.
Conclusions. Detailed knowledge of the lymphatic system of
the UADT contributes to a better understanding of the patterns of
metastatic spread of carcinomas of the UADT and provides a
strong rationale for the practice of sentinel node identification in
the management of these tumors. © 2003 Wiley Periodicals, Inc.
Head Neck 25: 322–332, 2003
Correspondence to: J. A. Werner
© 2003 Wiley Periodicals, Inc.
cancer; lymph node; metastasis; sentinel node
Regional nodal metastasis is the most important
prognostic predictor of regional recurrence and
death from disease in patients with head and
neck squamous cell carcinoma (HNSCC) of the
upper aerodigestive tract (UADT). It is also the
most reliable predictor of the development of dis-
tant metastases The number of metastatic lymph
nodes and the presence of extracapsular spread
(ECS) of tumor outside the lymph node capsule
are additional pathologic staging criteria that fur-
ther establish a patient’s risk for regional and dis-
tant recurrence and death from disease.1 The
statements are highlighted by the 5-year overall
survival rates of 73%, 50%, and 30% in patients
treated for oral tongue cancer found to be patho-
logically negative (pN0), pathologically positive
without ECS (pN+ECS−), and pathologically posi-
tive with ECS (pN+ECS+), respectively.2
There have been many attempts to predict the

322 System of the Head and Neck HEAD & NECK April 2003
risk of metastatic spread in patients with clini-
cally node negative HNSCC using a variety of dif-
ferent molecular markers, including the epider-
mal growth factor (EGF) receptor, 3 matrix
metalloproteinases,4–6 E-cadherin,7,8 proliferat-
ing cell nuclear antigen (PCNA),9,10 p53,11–13 and
cyclin D1.14 As these molecular marker data ac-
cumulate, there is increasing emphasis placed on
the molecular biologic mechanisms rather than
the functional anatomic mechanisms of metasta-
sis. However, the success achieved with the tech-
nique of sentinel lymph node identification and
resection in patients with a wide variety of ma-
lignancies, such as carcinoma of the breast and
melonoma, argue that the distribution and den-
sity of the regional lymphatic vessels is critically
important. Therefore, the goal of this report is to
provide a survey of current knowledge of the
lymph vessel architecture in the region of the oral
cavity, pharynx, and larynx based on our investi-
gations conducted during the past 15 years. This
is particularly relevant at this time because up
until the present, analyses of lymph vessel archi-
tecture focused only on single areas of the par-
ticular region. In addition, the methods used in
the previous studies for describing lymph vessels
were prone to errors. In this report, we describe
the distribution of lymph vessels from the ante-
rior part of the oral cavity to the piriform sinus.
Furthermore, information regarding lymph
drainage into the regional lymph nodes demon-
strates a correlation between the direction of lym-
phatic drainage and frequency of lymphatic me-
tastases.
MATERIAL AND METHODS
Eight hundred fifty specimens of the UADT were
collected at a single institution; these included
362 specimens collected at autopsy and 488 col-
lected intraoperatively. The tissue specimens
were examined by several different methods, in-
cluding light and transmission electron micros-
copy. Histochemical analysis was performed to
assess the density of lymphatic vessels in particu-
lar sites, and lymphographic studies were per-
formed to assess the functional drainage path-
ways. Additional lymphographic studies were
performed in patients who underwent sentinel
node identification.
Conventional Light Microscopy. For conventional
light microscopy, paraffin-embedded tissue was
sectioned sagittally, frontally, and horizontally
(6–8 ␮m). Routine staining procedures, including
System of the Head and Neck
H&E, Giemsa, Goldner, Azan, and toluidine blue
at pH 2.5, were performed. To characterize lymph
vessels, additional staining for the perivascular
fiber apparatus, which is characteristic for lymph
vessels was performed; this staining included or-
cein, hematoxylin according to Verhoeff, resorcin-
fuchsin, and the modified aldehyde fuchsin stain
of Gerli et al.15,16
Histochemistry. Histochemical studies were per-
formed exclusively in freshly excised surgical
specimens.17 Studies, including immunohisto-
chemical measurement of laminin, fibronectin,
type IV collagen, and factor VIII–related antigen,
were performed on cryostat cuts with commer-
cially available antibodies (Medac, Hamburg,
Germany).
Lymphatics were proven by 5⬘-nucleotidase
activity in sagittal and horizontal serial sections.
In addition, the activities of alkaline phospha-
tase, aminopeptidase, and dipeptidyl peptidase
IV in the specimens were used as a control, be-
cause the activity of these enzymes is known to be
lower in tissue than in blood vessels.18 The first
cut depicted 5⬘-nucleotidase activity, the second
alkaline phosphatase activity, the third adenylate
cyclase activity, and the forth dipeptidyl pepti-
dase IV activity.19 This approach allowed accu-
rate of discrimination between lymphatic and
vascular capillaries.
Transmission Electron Microscopy. Tissue pre-
pared for transmission electron microscopy was
cut immediately after excision to a length of 2 mm
and ultrathin cuts were made. The ultrathin cuts
were contrasted on copper nets with uranyl ac-
etate and lead citrate and examined under a Zeiss
electron microscope EM 902.20
Lymphography. Indirect lymphography on tissue
specimens was carried out under the operating
microscope. For examinations of the endolaryn-
geal mucosa to be performed in a closed laryngec-
tomy specimen, additional microscopically con-
trolled endolaryngeal dye applications were
performed with a shortened microlaryngoscopy
tube. For color injection (Methylenblau IV VITIS,
Neopharma, Aschau, Germany), lymphography
cannulas with a diameter of 0.3 mm (Krauth,
Hamburg, Germany) or 0.2 mm (Schneider, Med-
intag, Zurich, Switzerland) were used. In larger
mucosal areas, the lymphographic dye was in-
jected according to the technique described by
HEAD & NECK April 2003 323
Mann21 using an injection pump at a flow rate of
0.2 mL/min.
Results of examinations of an intraoperative
proof-of-sentinel node (SN) in HNSCC were in-
cluded in the analysis of drainage of the lym-
phatic system of the UADT. These tissue speci-
mens were collected in 82 patients (13 women, 69
men; median age, 64 years [range, 33–79 years]).
Primary tumor location among these 82 patients
was varied, with 11 oral cavity tumors, 30 oral
pharynx tumors, 28 laryngeal tumors, and 4 hy-
popharynx tumors. All were staged as N0 neck by
B-mode sonography; 1.2 mCi 99mTc-nanocoll dis-
solved in 0.2 mL normal saline (oral cavity, oro-
pharynx) or in 0.35 mL normal saline (larynx, hy-
popharynx) was administered by means of three
to four peritumoral injections at the beginning of
the surgical procedure (resection of primary tu-
mor and neck dissection). The tracer substance
was injected at the perimeter of the tumor and
was performed under microscopic visualization.
The SN was detected intraoperatively within
6.5 hours (range, 1.5–6.5 hours) of injection. Us-
ing standard procedures, a 14-mm gamma-probe
(Navigator Gamma Guidance System, Auto Su-
ture, Tönisvorst, Germany) was used to detect the
hottest node (SN) as well as further nodes (SN2,
SN3) that showed tracer uptake, albeit to a lesser
degree.
We abstained from blue dye injection for sev-
eral reasons. Accidental damage to the lymphatic
duct may lead to extravasation of blue dye, which
might not only cause impaired overall view of the
surgical field but could also lead to delayed wound
healing.22 Furthermore, it has been reported, as
early as 1985 that anaphylactic reactions after
subcutaneous injections of blue dye may be evi-
dent in up to 2% of cases.23 With regard to these
complications and the resulting potential danger
of accidental damage to functionally relevant
structures, the additional application of blue dye
does not seem to be justified, especially when con-
sidering that the scintigraphy method gives good
results.24
A neck dissection was performed on the basis
of suspected lymphatic spread. The number and
location of the excised sentinel nodes in relation
to the level of lymph nodes25 and the location of
the primary tumor were documented. Further-
more, histologic results of the SN and the excised
lymph nodes were compared with the results of
the neck dissection specimen. Description of the
location of the draining lymph nodes is in accor-
dance with the classification system of Robbins.26
324 System of the Head and Neck
RESULTS
Anatomy of the UADT Lymphatic System. The
most peripheral vessels of the lymphatic system
are avalvular capillaries that have wide vascular
lumen (30–50 ␮m diameter) and drain into valve-
bearing precollecting vessels. These capillaries
can increase their capacity and expand to a diam-
eter of 100 ␮M. The walls of the capillaries consist
of one layer of overlapping endothelial cells sur-
rounded by an incomplete and interrupted basal
lamina. These endothelial cells can be organized
without contact or may be connected by means of
interendothelial junctions that function as intake
and draining valves. An elastic fiber network
typically surrounds these capillaries, and because
there are no pericytes surrounding lymphatic ves-
sels, this network plays a critical role in the trans-
mission of forces that regulate fluid transport and
cell migration into and out of the lymphatic ves-
sels.
The UADT has two relatively dense communi-
cating lymphatic networks: a deep and a superfi-
cial network, and lymph is normally transported
from the superficial to the deeper network. The
superficial network is made up of capillaries that
drain into precollecting vessels at the junction of
the mucosa and submucosa. The precollecting
vessels then join lymph-collecting vessels called
the peripheral collecting vessels, which carry the
lymph to the first lymph node station. The post-
nodal collecting vessels carry lymph to the right
or left lymphatic ducts, as well as in the paired
jugular lymphatic trunks. On both sides of the
neck, the collecting ducts empty into the circula-
tory system at the junction point of the internal
jugular vein and the subclavian vein.
The Lymphatic System of the Oral Cavity. The lin-
gual, floor of mouth, and mandibular gingival
lymph is drained through the system of the floor
of the mouth, where some regular lymph vessels
can be observed crossing the midline in the super-
ficial and the deeper network. The density of the
lymph vessels of the floor of the mouth exceeds
that of the upper and lower lips, the gingiva, and
the buccal mucosa. As shown in Figure 1, drain-
age of the floor of the mouth occurs primarily dor-
sally, directed along the mandibular axis and
then by way of collecting vessels that flow into
lymph nodes in the submandibular space. As
shown in Figure 2, single collecting vessels drain
the anterior region of the floor of the mouth in a
caudal direction to submental lymph nodes and
the posterior floor of the mouth along the medial
HEAD & NECK April 2003
 FIGURE 2. Lateral view of the drainage of the tongue. The arrows
indicate drainage, and “o” points out drainage directed into the
depth.

FIGURE 1. Drainage of the buccal mucosa. The arrows indicate

drainage, and “o” points out drainage directed into the depth.

surface of the mandibular angle to the orophar-

ynx.
The mucosa of the tongue contains particu-
larly dense lymphatic networks. The superficial
plexus increases in density as one moves from the
tip of the tongue toward the tongue base. In the
deep network, a significant increase in the num-
ber and wall diameter of the ventrodorsal precol-
lecting vessels is observed. The density of lym-
phatic capillaries is seen to be higher in the
mucosa than in the muscle layer. Conversely, the
number of precollecting and collecting vessels in-
creases as one transitions from mucosa and sub-
mucosa to the muscle layers. Different areas of
the tongue have different lymphatic drainage pat-
terns. As shown in Figure 3, drainage of the ven-
tral surface of the mobile tongue occurs primarily
in a medial direction and then continues dorsally
by way of at least two main collectors. A portion of
the lymph fluid flows together with lymph fluid
from the floor of the mouth toward the subman-
dibular region, and the remainder flows to upper
jugular nodes. From the mucosa of the dorsum of
the mobile tongue, the lymph fluid drains primar-
ily laterally to the submandibular lymph nodes by
way of marginal collectors. As shown in Figure 4,
lymph fluid is drained from the base of the tongue FIGURE 3. Drainage of the floor of the mouth and the undersur-
predominantly to the lymph nodes of levels II and face of the tongue. The mapped arrows show the drainage, and
III. Lymph fluid of the mucosa located around the “o” points out drainage directed into the depth.

System of the Head and Neck HEAD & NECK April 2003 325
 caudal part of the soft palate, which includes the
uvula, as shown in Figure 5.

Lymphatic System of the Nose and Nasopharynx.

The lymph collectors of the lateral nasal wall
drain to the nasopharynx and, in the region of the
nasopharyngeal folds, form the pretubal plexus,
which lies between the levator and tensor palatini
muscles. Some of the lymph collectors originating
from the sphenoethmoidal recess and the supe-
rior nasal meatus drain over the pharyngeal for-
nix to the lateral retropharyngeal lymph nodes,
whereas a few drain to the subdigastric lymph
nodes. The collectors originating from the nasal
septum run together with blood vessels of the up-
per vessels of the lateral nasal wall at the pha-
ryngeal fornix to the lateral retropharyngeal
lymph nodes. The collectors of the middle and
lower parts of the nasal septum run caudally to
the nasal floor and drain into the pretubal plexus.
In the region of the natural openings, the collec-
tors of all paranasal sinuses are in contact with
the collectors of the nasal cavity, and drainage is
directed to the lateral retropharyngeal and sub-
gastric lymph nodes.
Figure 6 shows that the physiologic drainage

FIGURE 4. Drainage of the dorsum and the base of the tongue.

The mapped arrows show the drainage.

midline flows vertically to the submandibular

(anterior tongue) and upper jugular lymph nodes
(posterior tongue) by way of five to seven collec-
tors located between the genioglossal muscles.
The dense lymphatic system of the buccal mu-
cosa drains primarily into the submandibular
space through 8 to 10 collectors that extend
through the buccal muscle in the direction of the
facial artery and vein. The buccal lymph system
continues without interruption on to the alveolar
ridge. Maxillary and mandibular gingivae are
streaked with dense superficial and deep lymph
systems that cross the midline in the inner and
the outer sulcus. By use of interstitial lympho-
graphic dye, a few vessels can be visualized over
very short distances in the neighboring periostea
of the maxilla and the mandible.
The mucosa of the hard and soft palate is
streaked by a dense superficial system. A few
crossing lymph vessels are located in the midline
of the hard palate, and a significant transition of FIGURE 5. Drainage of the soft and hard palate. The mapped
the midline can be observed in the deeper and arrows show the drainage.

326 System of the Head and Neck HEAD & NECK April 2003

FIGURE 6. Direct communication of the system of the upper
aerodigestive tract, view from behind. The mapped arrows show
the drainage, and “o” points out drainage directed into the depth.
of the nasopharynx passes from the nasopharyn-
geal fornix first in a dorsolateral then in the dor-
solateral caudal direction. In addition to this lat-
erally orientated transport, there is drainage
parallel to the posterior midline; thus, lymph
fluid flows over 8 to 12 collectors from the fornix
and the nasopharyngeal posterior wall to the pos-
terior midline. The collectors penetrate the pha-
ryngeal fascia at the level of the base of skull and
run between the pharyngeal wall and the longus
capitis muscle. Most of the collectors drain to the
retropharyngeal lymph nodes; others empty into
the deep jugular lymph nodes.
Lymphatic System of the Oropharynx. Figure 5
demonstrates that lymph collectors are directed
along the palatoglossal muscle and the palatopha-
ryngeal muscle at the anterior and posterior pala-
tine arches. The palatine tonsils contain the most
subepithelial lymphatic in the lateral areas near
the tonsillar capsule, where septal, interfollicu-
lar, and subreticular vessels penetrate. No lymph
vessels can be demonstrated in the germinal cen-
ters. In the region of blood vessel passages, pas-
sages of lymph vessels can be seen in the capsule
formed by the fascia of the superior constrictor
muscle of the pharynx. Lingual tonsil and pha-
ryngeal tonsil show a similar distribution of lym-
phatics.
From the region of the base of tongue, lymph
fluid is drained through collectors that run along
the lingual veins that course through the pharyn-
geal wall. Most of these collectors run to the cra-
System of the Head and Neck
niojugular region. The collectors of the left and
right part of the tongue are connected by some
precollecting vessels, which cross the midline.
Midline passages are observed from the lingual
surface down to the mylohyoid muscle.
Lymphatic System of the Hypopharynx. After the
nasopharynx, the mucosa of the hypopharynx has
the highest density of lymphatics in the UADT.
As shown in Figure 6, the network of the oral
cavity communicates in an unobstructed way
with that of the hypopharynx. The lymph fluid of
the cranial portion of the hypopharynx flows to-
gether with the lymph fluid of the glottic and su-
praglottic space in a dorsoventral direction and
from the retrolaryngeal mucosa in a mediolateral
direction through the lateral part of the thyrohy-
oid membrane near the superior laryngeal artery
to collecting vessels. The lymph fluid of the caudal
hypopharyngeal region moves through collectors,
which drain through the cricothyroid membrane.
Additional lymph drainage occurs in a craniocau-
dal direction at the posterior wall of the hypo-
pharynx along the median line, which is tra-
versed by numerous lymph vessels.
Lymphatic System of the Larynx. Figure 7 shows
the two communicating networks of the laryngeal
mucosa: one is a closely meshed superficial one,
and the other is a widely meshed profound one.
Figures 6 and 7 show that both networks connect
FIGURE 7. Drainage of the trachea. The mapped arrows show
the drainage.
HEAD & NECK April 2003 327
in an uninterrupted fashion with those of the
pharynx and trachea.
The laryngeal system is characterized by re-
gional differences in density. In the larynx, there
is no barrier that separates the laryngeal system
into superior and inferior areas, and both mucosal
and submucosal lymphatic vessels are seen to
cross the midline. In the supraglottic region, the
laryngeal density of lymphatic vessels is highest.
An exception is the mucosa in the area of the epi-
glottic petiole and the tissue around the thyroepi-
glottic ligament, where the density of the lym-
phatic vessels is significantly lower.
The lymph fluid of the supraglottic space
drains through the lateral part of the thyrohyoid
membrane in the mediolateral direction over
three to six collectors. The lymph fluid of the la-
ryngeal surface of the epiglottis also drains in the
direction of the lingual surface of the epiglottis.
Figure 8 shows that the main drainage flows by
way of the free epiglottic ridge.
The lymphatic system is less well developed in
the region of the anterior third of the vocal folds.
This system, which is orientated primarily in the
direction of the vocal ligament, becomes more
dense below the epithelium. A zone of higher den-
sity lies below the areas adjacent to the transi-
tional epithelium. Across the entire mucosa of the
vocal folds, only a few precollectors and no lymph
collectors are observed. In comparison, the vocal
FIGURE 8. Drainage of the larynx, view from behind. The
mapped arrows show the drainage.
328 System of the Head and Neck
muscle contains many more precollectors, and the
muscular tissue normally contains two to three
lymph collectors. In the vocal ligament, the pres-
ence of lymph vessels can only rarely be detected.
Only a few lymph vessels are contained in the
connective tissue of the vocal cord tendon (Broyles
tendon) that pass from the so-called elastic lymph
nodes into the skeleton of the thyroid cartilage.
The free edge of the vocal cords does not divide
the laryngeal network into a subglottic and a su-
praglottic part. Injected dye particles are trans-
ported to the arytenoids by way of capillaries,
which are oriented in the direction of the longitu-
dinal axis of the vocal cords. Drainage of the ary-
tenoid region then occurs by the same pat drain-
age pathways as the supraglottic larynx. Dye
transport to the subglottic region or the laryngeal
ventricle is only rarely observed, and dye move-
ment between the supraglottic and the subglottic
regions in the anterior two thirds of the free edge
of the vocal was observed in only 2 of 24 speci-
mens examined with this technique. The glottic
system continues without interruption into the
subglottic network, where the lymph vessels are
oriented horizontally, thereby restricting subglot-
tic drainage to one side only.
The highest density of lymph collectors can be
found in the supraglottic region in the triangle
formed by the epiglottis, false vocal fold, and ary-
epiglottic fold. Lymph collectors are not present
in the mucosa of the vocal cords but are present in
the muscles. Approximately 2 cm beyond the glot-
tic level, horizontally orientated lymph collectors
are observed in the subglottic mucosa.
Lymph fluid of the supraglottic and glottic re-
gions flows to the level II and III lymph nodes.
The subglottic lymph fluid leaves the endolaryn-
geal space ventrally by way of collectors through
the cricothyroid ligament and dorsally through
the cricotracheal ligament. Therefore, lymph fluid
from the subglottis flows to the jugular lymph
nodes, as well as to recurrent chain nodes, prethy-
roidal, and pretracheal and paratracheal lymph
nodes, and rarely to the prelaryngeal lymph node.
Location of the Sentinel Node in UADT Cancer. By
use of gamma probe–guided intraoperative iden-
tification of the SN and measuring accumulation
of radioactive tracer, a hottest node, which was
defined as the SN and further hot nodes (SN2,
SN3) were observed in all 82 cases of clinically N0
UADT cancers that we evaluated with this tech-
nique.
In carcinomas of the anterior oral cavity (n ⳱
HEAD & NECK April 2003
11), the intraoperatively identified SN in carcino-
mas of the mobile tongue (n ⳱ 8) were located in
level IB (n ⳱ 2) and level IIA (n ⳱ 6); in carcino-
mas of the floor of the mouth (n ⳱ 3), the SN was
located in level IB. In carcinomas of the orophar-
ynx (n ⳱ 39), the SN in carcinomas of the tonsil
(n ⳱ 23) was located primarily in level II (16 ob-
servations of level IIA and 3 observations of levels
IIB), with a few (4 of 23) in level III. In carcino-
mas of the base of tongue (n ⳱ 16), the SN also
was located in level IIA (4 of 16) or in level III (12
of 16). In carcinomas of the larynx (n ⳱ 28), the
SN in glottic carcinomas (n ⳱ 11) was most often
found in level IIA (4 of 11) or in level III (7 of 11);
in supraglottic carcinomas (n ⳱ 17), the SN was
also found in levels II (13 of 17) and III (4 of 17).
Whereas, in carcinomas of the hypopharynx (n ⳱
4), the SN was usually located in level III (3 of 4)
or level IV (1 of 4).
DISCUSSION
During lymphatic metastasis, tumor cells pen-
etrate vessel walls with missing and/or discon-
tinuously developed basement membranes.27 Tu-
mor cells are transported with lymph into the
subcapsular sinus of the lymph nodes, where they
may remain and begin to form a colony.28,29 The
initial metastatic colony is limited to the first
draining lymph node of the primary tumor, which
is the basis for the concept of SN identifica-
tion.25,27–34 Analysis of the UADT lymphatic sys-
tem as described herein is based on different
examination methods and allows a nearly con-
tinuous description of the architecture of the lym-
phatic networks. Adding the technique of indirect
lymphography, performed with dye or with a ra-
dioactive tracer, it is possible to demonstrate the
continuity of the lymphatic system of the UADT
with the cervical lymph node system.
Our findings contrast with some previous de-
scriptions of the UADT lymphatic drainage sys-
tem, which describe strict compartmentalization
of single segments of the UADT.35–37 In addition,
in contrast to the work of other groups, we found
that there are bilateral drainage pathways in
nearly all areas of the UADT.38
These regional differences in the density and
orientation of the lymphatic vessels of the UADT
are important in consideration of the direction
and frequency of lymph node metastases. These
differences also are important in consideration of
SN identification, particularly with the observa-
tions that advanced carcinomas are able to me-
tastasize to different lymph node levels. This lat-
System of the Head and Neck
ter finding argues for the identification of SNs
from each of the different nodal basins that drain
a particular UADT region.
Oral Cavity. The lymph fluid of the anterior oral
cavity is directed primarily to the lymph nodes of
level I.39 However, drainage from the lateral oral
tongue and the posterior floor of the mouth is di-
rected to lymph nodes in level II. Although meta-
static spread in lingual lymph nodes has not been
widely described,40,41 the presence of both medial
and lateral groups of lingual spread was noted in
our study.42 The lymph nodes of the lateral group
are located either lateral to the genioglossal
muscle or on the hypopharyngeal muscle along
the lingual artery and vein. Lymph nodes of the
medial group are located along the central lymph
vessels that course in the direction of the floor of
the mouth. Even though this finding is rarely
seen, these lymph nodes could serve as the start-
ing point of local recurrences.41 Ozeki et al40 have
shown three cases of metastases in the lingual
lymph nodes in carcinomas of the tongue; this ob-
servation has led these physicians to perform an
en bloc resection, because the lingual lymph
nodes located beyond the omohyoid muscle are
normally not resected in the course of a classic
neck dissection.
Nasopharynx. The physiologic drainage of the
nasopharynx flows from the nasal fornix first in a
dorsolateral direction, then in a dorsolateral cau-
dal direction.43 There is additional drainage par-
allel to the posterior midline that corresponds to
the findings of Rouvière.42 According to Rouvière,
lymph fluid drains from the fornix and the poste-
rior nasopharyngeal wall by way of 8 to 12 collec-
tors parallel to the posterior midline. The collec-
tors drain to the retropharyngeal lymph nodes
and to the lymph nodes of level II and particularly
level V. Thus, nasopharyngeal carcinomas metas-
tasize mainly into the lateral retropharyngeal,
level II, and level V groups of lymph nodes.44
Oropharynx. Drainage of the palatine tonsil and
the base of the tongue is directed primarily to the
lymph nodes of level II and to a lesser extent by
way of collectors that drain to the retropharyn-
geal lymph nodes and to the lymph nodes in level
III.45 Drainage of the posterior pharyngeal wall is
directed into the retropharyngeal lymph nodes
where the lymph fluid is also conducted by means
of collectors to the lymph nodes in level II and III.
This observation serves as the basis for the high
HEAD & NECK April 2003 329
rate of metastasis of oropharyngeal carcinomas in
the retropharyngeal lymph nodes.46 There is also
direct drainage from the posterior pharyngeal
wall into level II and III.
With this information, it is important to note
that occult oropharyngeal carcinoma may present
as a large, necrotic, lymph node metastasis, pre-
dominantly located in level II and often misdiag-
nosed as branchiogenic carcinoma.47
Hypopharynx. Lymph fluid from the hypophar-
ynx is drained by way of collectors primarily to
the lymph nodes in levels III and IV. A direct
connection to level I was not detected in any of the
cases studied, and drainage to the lymph nodes of
level II was observed only infrequently.41
Larynx. Lymph fluid of the supraglottic and the
glottic regions flows to the lymph nodes of levels
II and III. From the subglottic space, lymph fluid
is conducted ventrally through the cricothyroid
ligament and dorsally through the cricotracheal
ligament.48 Subglottic lymph fluid flows to the
lymph nodes of levels III and VI. The presence of
a prelaryngeal lymph node located in level VI (the
Delphian lymph node) depends on the age of the
patient; although this lymph node can be regu-
larly observed in children up to the age of 10, only
half of the examined adults between the ages of
40 and 75 possessed this node.
The direction of metastatic spread in laryn-
geal carcinomas corresponds typically to the
drainage in levels II and III.
Alterations in Physiologic Drainage. Despite pre-
vious reports of consistent lymphatic drainage
patterns to lymph nodes localized in specific lev-
els of the neck, uncommon locations of lymph
node metastasis are often observed. This phenom-
enon can be explained by changes in the physi-
ologic lymph drainage by means of occlusion of
the draining lymph collectors or lymph nodes.
This leads to an extension of the precollectors and
collectors, which inhibits sufficient closure of the
valves. Possible mechanisms for this include tis-
sue infections, radiotherapy, previous surgical ap-
proaches, and primary tumor growth. For ex-
ample, after resection of an oropharyngeal
carcinoma and reconstruction by means of a myo-
cutaneous flap, metastases can be generated in
uncommon regions such as the origin of the myo-
cutaneous flap.49,50 Furthermore, after primary
radiotherapy or radical neck dissection, contralat-
eral lymph node metastases can be observed. This
330 System of the Head and Neck
phenomenon can be explained in part by develop-
ment of a contralateral drainage after ipsilateral
lymph node dissection.51
In the past, three mechanisms have been pro-
posed and discussed to explain the uncommon lo-
cations of lymph node metastasis. One mecha-
nism is drainage by means of existing crossing
lymphatics. Another explanation is that in cases
of advanced lymphogenic metastatic spread, tu-
mor emboli may occlude the afferent lymph col-
lectors, leading to misdirection of lymphatic
drainage along other available pathways. The
third mechanism describes specific anatomic re-
gions with intensive midline crossing (eg, naso-
pharynx, posterior pharyngeal wall) that are
characterized by an existing drainage into both
sides of the neck.52
In summary, the observations described
herein demonstrate that there is consistent archi-
tecture of the lymphatic vessels and consistent
drainage into regional lymph nodes. This demon-
stration justifies further investigation of the SN
concept in patients with clinically node-negative
neck cancer. In considering the SN concept, inves-
tigators should consider the observation that is
based on the location of the primary tumor; there
may be drainage into two adjacent neck node lev-
els. Furthermore, previous alterations such as
surgery or radiotherapy can disturb drainage; tu-
mor emboli within the draining lymph vessels
also can disturb drainage, and one must take this
into consideration when selecting patients on
whom this procedure may be performed.
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