Lymphatic drainage of head & neck

Presented by :Dr. Manish Kumar

Introduction
Historical Perspective & Current View
Embryological Development
Functions of Lymphatic System
Components of Lymphatic System
Lymph Nodes of Head & Neck
Lymphatic Drainage
Applied Aspects
Lymph-adenopathy
Clinical Assessment
Laboratory Investigations
Differential Diagnosis
Conclusion

Of all the body systems, the lymphatic system is perhaps the
least familiar to most people. Yet without it, neither the
circulatory system nor the immune system could function—
circulation would shut down from fluid loss, and the body
would be overrun by infection for lack of immunity.

The lymphatic system is an endothelium-lined network of blindended capillaries found in nearly all tissues, draining via
collecting vessels into large vascular trunks that eventually
empty via an evolutionarily conserved drainage point into the
blood circulatory system.

Birth Defects Res C Embryo Today. 2009 September ; 87(3): 222–231. doi:10.1002/bdrc.20155.

The lymphatic system.
(A) Schematic illustration of the human lymphatic vascular system. (B) Structure of lymphatic
vessels. (C) Schematic representation of a lymph node. (D) Connection of the lymphatic
system with the blood vasculature at the subclavian veins.

Hippocrates first described vessels containing “white blood”
around 400 B.C.
Gasparo Aselli re-identified lymphatic vessels in the
1600’s, noting the presence of lipid-filled “milky veins” in the gut
of a “well-fed” dog (Aselli, 1627).
Historically, the most widely accepted view of lymphatic
development was proposed by Sabin in the early twentieth
century (Sabin 1902, 1904).


Sabin’s Model :
The isolated primitive lymph sacs originate from endothelial
cells that bud from the veins during early development.
The two jugular lymph sacs were proposed to develop in the
junction of the sub-clavian and anterior cardinal veins by
endothelial budding from the anterior cardinal veins.
The remaining lymph sacs originate from the mesonephric vein
and those in the dorsomedial edge of the Wolffian bodies in the
junction of the subclavian and anterior cardinal veins.

GENES & DEVELOPMENT 16:773–783 © 2002 by Cold Spring Harbor Laboratory Press ISSN 0890-9369

The retroperitoneal lymph sac forms near the primitive
inferior vena cava and mesonephric veins; the cisterna chyli
forms near the Wolffian bodies; and the posterior lymph sacs
appear near the junctions of the primitive iliac veins and the
posterior cardinal veins.

The peripheral lymphatic system originates from the primary
lymph sacs, then spreads by endothelial sprouting into the
surrounding tissues and organs, where local capillaries are
formed.


Schematic representation of the primitive lymphatic system showing the
primary lymph sacs in a 42-day-old human embryo, after Sabin (reprinted
from Human Embryology, by W.J. Larsen, 1993, Harcourt, NY; with permission
from Harcourt International).

Alternative Model / Centripetal Model :proposed by Huntington and McClure 1910.
They suggested that the primary lymph sacs arise in the
mesenchyme, independent of the veins, and secondarily
establish venous connections.
This model was supported by Schneider et al. 1999.


Perhaps the most definitive evidence for a venous origin for
early lymphatic endothelial cells has come from the zebra fish
(Yaniv et al., 2006).
Recent studies have shown that the zebra fish possesses a
lymphatic vascular system with many of the morphological,
molecular, and functional characteristics of the lymphatic's of
other vertebrates.


There are several markers that show different profiles of
expression in blood and lymphatic vasculature, e.g. :Vascular endothelial growth factor receptor – 3 (VEGFR-3 /
Flt-4)
Lymphatic endothelial hyaluronan receptor - 1 (LYVE – 1; a
CD44 homolog)
Secondary lymphoid chemokine (SLC / 6C Kine / Exodus-2 /
CCL21)
Podoplanin; a surface glycoprotein
Desmoplakin; a cytoplasmic protein
Prox-1 (prospero-related homeobox 1)


All venous endothelial cells are initially bi-potent and the
expression of at least Prox-1 gene causes those cells to initiate
the program of lymphatic differentiation.
As the development proceeds, the sub-population of LYVE-1 and
Prox-1 positive cells start to bud from the veins in an initially
Prox-1 independent manner; however maintenance of the
budding requires Prox-1 activity.
As the cells bud they start to express higher levels of additional
markers such as SLC and VEGFR-3.


The expression of Prox-1, LYVE-1,SLC and VEGFR-3 may indicate
that the cells are irreversibly committed to the lymphatic
pathway.


Recent studies indicate that Sox18 controls expression of Prox1
(Francois et al., 2008).
SOX18, an SRY-related HMG domain transcription factor, was
implicated in lymphatic development by the identification of
SOX18 mutations in individuals with hypotrichosis-lymphedematelangiectasia syndrome (Irrthum et al., 2003).
Lentiviral expression of Sox18 in both differentiating Embryonic
stem cells (ES cells) and blood vascular endothelial cells induced
expression of Prox1 and Podoplanin (Francois et al., 2008).

Birth Defects Res C Embryo Today. 2009 September ; 87(3): 222–231. doi:10.1002/bdrc.20155

At embryonic day (E) 9.0 in mice and gestation week 6 in
humans, after arterial-venous separation, cells of the cardinal
vein start to lose blood endothelial characteristics and acquire a
lymphatic endothelial cell (LEC) identity. This process is
controlled by the sequential expression of Lyve-1, Sox18 and
Prox1.

Int. J. Dev. Biol.2011;55:483-494 doi: 10.1387/ijdb.103226ia

At E10.5, LEC then bud off the cardinal vein, migrate into the
surrounding tissue and form primary lymphatic sacs. This
process is dependent on VEGF-C/VEGFR3/Nrp2 signaling.
Subsequently, the primary lymphatic sacs separate from the
cardinal vein and by further growth and spreading into the
tissue, gives rise to a primitive lymphatic plexus.

At E14.5, remodeling of the primitive lymphatic vasculature
begins and lasts until after birth.


During this period a hierarchical network consisting of collecting
lymphatic vessels and lymphatic capillaries are formed.

This maturation process involves changes in protein expression
leading to a quiescent, non-growing vessel, the formation of
lymphatic valves and the acquisition of a smooth muscle coat.
With the accumulation of basement membrane proteins at
E16.5 recruitment of NG2-positive mural cells begins to finally
generate the smooth muscle cell coverage observed in major
lymphatic vessels (Norrmen et al., 2009).


The lymphatic system begins to develop at the end of week 5,
approximately 2 weeks later than the cardiovascular system.

IN WEEKS 6-9, local dilatations of the lymphatic channels and
formation of 6 primary lymph sacs occurs.
Two jugular lymph sacs near the junction of the
subclavian veins with the anterior cardinals (future
internal jugular vein)
Two iliac lymph sacs near the junction of the iliac veins
with the posterior cardinal veins
One retroperitoneal lymph sac in the root of the
mesentery on the posterior abdominal wall
One cisterna chyli dorsal to the retroperitoneal lymph
sac, at the level of the adrenal glands
EMBRYONIC DEVELOPMENT & STEM CELL COMPENDIUM; LIFE MAP DISCOVERY.

Lymph vessels development –
it grows from the lymph
sacs, along the major veins,
to the head, neck, and arms
from the jugular sacs;
to the lower trunk and legs from
the iliac sacs; and
to the gut from the
retroperitoneal and cisternal
sacs.

Embryology Atlas ; Chapter 23: Lymphatic System; Embryological Development by John F. Neas

The cisterna chyli is connected to the jugular lymph sacs by 2
large channels, the right and left thoracic ducts.

An anastomosis forms between the 2 ducts, thus, the definitive
thoracic duct is formed by the caudal portion of the right
thoracic duct, the anastomosis, and the cranial portion of the
left thoracic duct.
The right lymphatic duct is derived from the cranial part of the
right thoracic duct.

EMBRYONIC DEVELOPMENT & STEM CELL COMPENDIUM; LIFE MAP DISCOVERY

Both the right and left thoracic ducts join the venous system at
the angle of the subclavian and internal jugular veins at the base
of the neck

Lymph node development, at about month 3.

Except for the anterior part of the sac that produces the
cisterna chyli, all lymphatic capillary plexuses become
invaded by mesenchymal cells that proliferate and
aggregate to form groups of lymph nodes.
The lymph nodule and germinal centers of lymphocyte
production do not appear in the nodes until just before or
after birth


SPLEEN –

It develops from an aggregation of mesenchymal cells in the
dorsal mesentery of the stomach.
Development involves establishment of mesenchymal
trabeculae within a blood vascular network consisting of a
large number of endothelial sinuses.


THYMUS –
It arises as endodermal diverticula of the ventral part of the
third pharyngeal pouches.
The two thymic diverticula grow inferiorly in the neck to
reach the superior mediastinum and fuse into a two-lobed
organ.
The thymus achieves maximum size at puberty and
gradually regresses thereafter, being replaced by fatty
tissue.


TONSILS –
The palatine tonsils form from the second pair of
pharyngeal pouches
The tubal (pharyngotympanic) tonsils develop from
aggregations of lymph nodules around the openings of the
auditory tubes
The pharyngeal tonsils (adenoids) develop from an
aggregation of lymph nodules in the nasopharyngeal wall

The lingual tonsils develop from aggregations of lymph
nodules in the root of the tongue

The lymphatic system has three functions:

Fluid recovery.
Immunity
Lipid absorption
The lymphatic vessels of the small intestine receive the special designation of
lacteals or chyliferous vessels.

Anatomy and physiology - The unity of form and function (Saladin K. - 2003 - 3rd ed. - McGraw-Hill)

The main functions of the lymphatic system are as follows:
to collect and transport tissue fluids from the intercellular
spaces in all the tissues of the body, back to the veins in the
blood system;

it plays an important role in returning plasma proteins to the
bloodstream;
digested fats are absorbed and then transported from the villi
in the small intestine to the bloodstream via the lacteals and
lymph vessels.
new lymphocytes are manufactured in the lymph nodes;

Lymphocytes attack a cancer cell.

antibodies and lymphocytes assist the body to build up an
effective immunity to infectious diseases;
lymph nodes play an important role in the defence mechanism
of the body. They filter out micro-organisms (such as bacteria)
and foreign substances such as toxins, etc.
it transports large molecular compounds (such as enzymes and
hormones) from their manufactured sites to the bloodstream.

The components of the lymphatic system are :Lymph, the recovered fluid;
Lymphatic vessels, which transport the lymph;
Lymphatic tissue, composed of aggregates of lymphocytes and
macrophages that populate many organs of the body; and
lymphatic organs, in which these cells are especially
concentrated and which are set off from surrounding organs by
connective tissue capsules.


Lymph is usually a clear, colorless fluid, similar to blood plasma
but low in protein. Its composition varies substantially from
place to place.
Origin of Lymph :Lymph originates in microscopic vessels called lymphatic
capillaries. These vessels penetrate nearly every tissue of
the body but are absent from the central nervous system,
cartilage, bone, and bone marrow.
The gaps between lymphatic endothelial cells are so large
that bacteria and other cells can enter along with the fluid.


Origin of Lymph :-

The overlapping edges of the endothelial cells act as valve
like flaps that can open and close.
When tissue fluid pressure is high, it pushes the flaps inward
(open) and fluid flows into the lymphatic capillary. When
pressure is higher in the lymphatic capillary than in the
tissue fluid, the flaps are pressed outward (closed).


Lymphatic Capillaries. (a) Relationship of the lymphatic capillaries to a bed of
blood capillaries. (b) Uptake of tissue fluid by a lymphatic capillary.


They have a tunica interna with an
endothelium and valve, a tunica
media with elastic fibers and smooth
muscle, and a thin outer tunica
externa.
Their walls are thinner and their
valves are more numerous than
those of the veins.


Lymph takes the following
route from the tissues back to
the bloodstream:
lymphatic capillaries ->
collecting vessels ->
six lymphatic trunks ->
two collecting ducts ->
subclavian veins.
Thus, there is a continual
recycling of fluid from blood
to tissue fluid to lymph and
back to the blood


Lymph flows under forces similar to those that govern venous
return, except that the lymphatic system has no pump like the
heart.
Lymph flows at even lower pressure and speed than venous
blood; it is moved primarily by rhythmic contractions of the
lymphatic vessels themselves, which contract when stretched by
lymph.
The lymphatic vessels, like the veins, are also aided by a skeletal
muscle pump that squeezes them and moves the lymph along.

Also like the medium veins, lymphatic vessels have valves that
prevent lymph from flowing backward.

Since lymphatic vessels are often wrapped with an artery in a
common sheath, arterial pulsation may also rhythmically
squeeze the lymphatic vessels and contribute to lymph flow.
A thoracic (respiratory) pump aids the flow of lymph from the
abdominal to the thoracic cavity as one inhales, just as it does in
venous return.
Finally, at the point where the collecting ducts join the
subclavian veins, the rapidly flowing bloodstream draws the
lymph into it.
Considering these mechanisms of lymph flow, it should be
apparent that physical exercise significantly increases the rate of
lymphatic return.

T lymphocytes (T cells). These are so-named because they
develop for a time in the thymus and later depend on thymic
hormones. There are several subclasses of T cells.

B lymphocytes (B cells). These are named after an organ in birds
(the bursa of Fabricius) in which they were first discovered.
When activated, B cells differentiate into plasma cells, which
produce circulating antibodies, the protective gamma globulins
of the body fluids.


T Cells “Inspecting” Macrophages in a Lymph Node for Antigen Presentation. From R.
G. Kessel and R. H. Kardon, Tissues and Organs: A Text-Atlas of Scanning Electron
Microscopy (W. H. Freeman & Co., 1979).


Macrophages. These cells, derived from monocytes of the
blood, phagocytize foreign matter (antigens) and “display”
fragments of it to certain T cells, thus alerting the immune
system to the presence of an enemy. Macrophages and other
cells that do this are collectively called antigen-presenting cells
(APCs).

Dendritic cells. These are APCs found in the epidermis, mucous
membranes, and lymphatic organs. (In the skin, they are often
called Langerhans cells.)


The Action of an Antigen-Presenting Cell (APC). (a) Stages in the processing and presentation
of an antigen by an APC such as a macrophage. (b) Macrophages phagocytizing bacteria.
Filamentous extensions of the macrophage snare the rod-shaped bacteria and draw them to
the cell surface, where they are engulfed.

Reticular cells. These are branched cells that contribute to the
stroma (connective tissue framework) of the lymphatic organs
and act as APCs in the thymus.


Mucosa-associated
lymphatic
tissue.
The simplest form of
lymphatic tissue is diffuse
lymphatic tissue—a sprinkling of
lymphocytes in the mucous
membranes and connective
tissues of many organs.
It is particularly prevalent
in body passages that are open
to the exterior—the respiratory,
digestive,
urinary,
and
reproductive tracts—where it is
called
mucosa-associated
lymphatic tissue (MALT).

Peyers patches.
In some places, lymphocytes and
other cells congregate in dense
masses called lymphatic nodules
(follicles).
Lymphatic nodules are, however, a
relatively constant feature of the
lymph nodes and tonsils.
They also form clusters called Peyers
patches in the ileum, the last
segment of the small intestine.

Understanding Human Anatomy and Physiology - Sylvia S. Mader

Primary Lymphatic Organs :-

Lymphatic (lymphoid) organs contain large numbers of
lymphocytes, a type of white blood cell that plays a pivotal
role in immunity.
The primary lymphatic organs are
the red bone marrow and
the thymus gland.
Lymphocytes originate and/or mature in these organs.

Understanding Human Anatomy and Physiology - Sylvia S. Mader

Red Bone Marrow
It is the site of stem cells that are ever capable of dividing and
producing blood cells.
Some of these cells become the various types of white blood
cells: neutrophils, eosinophils, basophils, lymphocytes, and
monocytes.
In a child, most of the bones have red bone marrow, but in an
adult it is limited to the sternum, vertebrae, ribs, part of the
pelvic girdle, and the proximal heads of the humerus and
femur.

Red bone marrow is the site of stem cells that are ever capable
of dividing and producing blood cells. Some of these cells
become the various types of white blood cells:
neutrophils, eosinophils, basophils, lymphocytes, and
monocytes .

In a child, most bones have red bone marrow, but in an adult it
is limited to the sternum, vertebrae, ribs, part of the pelvic
girdle, and the proximal heads of the humerus and femur.

The red bone marrow consists of a network of reticular tissue
fibers, which support the stem cells and their progeny.

They are packed around thin-walled sinuses filled with venous
blood. Differentiated blood cells enter the bloodstream at these
sinuses.
Lymphocytes differentiate into the B lymphocytes and the T
lymphocytes.
Bone marrow is not only the source of B lymphocytes, but also
the place where B lymphocytes mature.
T lymphocytes mature in the thymus.

The thymus is a member of both the lymphatic and endocrine
systems.
It houses developing lymphocytes and secretes hormones that
regulate their activity.
It is located between the sternum and aortic arch in the
superior mediastinum.
The thymus is very large in the fetus and grows slightly during
childhood, when it is most active.

After age 14, however, it begins to undergo involution
(shrinkage) so that it is quite small in adults.

In the elderly, the thymus is replaced almost entirely by fibrous
and fatty tissue and is barely distinguishable from the
surrounding tissues.
Reticular epithelial cells secrete hormones called
thymosins, thymulin, and thymopoietin, which promote the
development and action of T cells.
If the thymus is removed from newborn mammals, there will
be lack of immunity development.

The secondary lymphatic organs are
the spleen,
the lymph nodes and
other organs, such as the tonsils, Peyer patches, and the
appendix.

All the secondary organs are the places where lymphocytes
encounter and bind with antigens, after which they proliferate
and become actively engaged cells.

The spleen is the body’s largest lymphatic organ. It is located in
the left hypochondriac region, just inferior to the diaphragm
and dorsolateral to the stomach.

It has a medial hilum penetrated by the splenic artery and vein
and lymphatic vessels.
Its parenchyma exhibits two types of tissue named for their
appearance in fresh specimens (not in stained sections):
red pulp, which consists of sinuses gorged with
concentrated erythrocytes, and
white pulp, which consists of lymphocytes and
macrophages aggregated like sleeves along small branches
of the splenic artery.

The Spleen. (a) Position of the spleen in the upper left quadrant of the
abdominal cavity. (b) Histology.

Functions –
It produces blood cells in the fetus and may resume this role in
adults in the event of extreme anemia.
It monitors the blood for foreign antigens, much like the lymph
nodes do the lymph.
Lymphocytes and macrophages of the white pulp are quick to
detect foreign antigens in the blood and activate immune
reactions.

The spleen is an “erythrocyte graveyard”—old, fragile RBCs
rupture as they squeeze through the capillary walls into the
sinuses. Splenic macrophages phagocytize their remains, just as
they dispose of blood-borne bacteria and other cellular debris.
The spleen also compensates for excessive blood volume by
transferring plasma from the bloodstream into the lymphatic
system.
A person can live without a spleen, but is somewhat more
vulnerable to infections.

Lymph nodes serve two functions:
to cleanse the lymph and
alert the immune system to pathogens.
There are hundreds of lymph nodes in the body.
They are especially concentrated in the cervical, axillary, and
inguinal regions close to the body surface, and in thoracic,
abdominal, and pelvic groups deep in the body cavities.

Most of them are embedded in fat.

Structure –
A lymph node is an elongated or bean-shaped structure, usually
less than 3 cm long, often with an indentation called the hilum
on one side.
It is enclosed in a fibrous capsule with extensions (trabeculae)
that incompletely divide the interior of the node into
compartments.
The interior consists of
a stroma of reticular connective tissue (reticular fibers and
reticular cells) and
a parenchyma of lymphocytes and antigen-presenting cells.

Anatomy of a Lymph Node.
(a) Bisected lymph node showing pathway of lymph flow.
(b) Detail of the boxed region in a.

Anatomy of a Lymph Node - Stroma and immune cells in a medullary sinus.

Between the capsule and parenchyma is a narrow space called
the subcapsular sinus, which contains reticular fibers,
macrophages, and dendritic cells.
The parenchyma is divided into an outer cortex and, near the
hilum, an inner medulla.

The cortex consists mainly of ovoid lymphatic nodules.
When the lymph node is fighting a pathogen, these nodules
acquire light-staining germinal centers where B cells multiply
and differentiate into plasma cells.

The medulla consists largely of a branching network of
medullary cords composed of lymphocytes, plasma cells,
macrophages, reticular cells, and reticular fibers.
The lymph node is a “bottleneck” that slows down lymph flow
and allows time for cleansing it of foreign matter.
The macrophages and reticular cells of the sinuses remove
about 99% of the impurities before the lymph leaves the node.
On its way to the bloodstream, lymph flows through one
lymph node after another and thus becomes quite thoroughly
cleansed of most impurities.

The tonsils are patches of lymphatic tissue located at the
entrance to the pharynx, where they guard against ingested
and inhaled pathogens.
Each is covered by an epithelium and has deep pits called
tonsillar crypts lined by lymphatic nodules.
The crypts often contain food debris, dead leukocytes,
bacteria, and antigenic chemicals.

Below the crypts, the tonsils are partially separated from
underlying connective tissue by an incomplete fibrous capsule.

There are three main sets of tonsils:
a single medial pharyngeal tonsil (adenoids) on the wall of the
pharynx just behind the nasal cavity,
a pair of palatine tonsils at the posterior margin of the oral
cavity, and
numerous
lingual
tonsils,
each
with
a
single
crypt, concentrated in a patch on each side of the root of the
tongue.

The palatine tonsils are the largest and most often infected.

Ectopic or tertiary lymphoid tissues develop at sites of
inflammation or infection in peripheral, non-lymphoid organs.

These tissues are architecturally similar to conventional
secondary lymphoid organs, with separated B and T cell areas,
specialized populations of dendritic cells, well-differentiated
stromal cells and high endothelial venules.
Most important of these sites are those tissues with direct
contact with the “external” environment, primarily the skin and
mucosal lining of the gastrointestinal, pulmonary, and
genitourinary tracts.

Semin Immunol. 2008 February; 20(1): 26–42.
Ann Rheum Dis 2010;69(Suppl 2):A1–A76

Lymph nodes in the head and neck are arranged in two
horizontal rings and two vertical chains on either side of the
neck.
The outer, superficial, ring consists of the occipital, preauricular
(parotid), submandibular and submental nodes, and the inner,
deep, ring is formed by clumps of mucosa associated lymphoid
tissue (MALT) located primarily in the naso- and oro-pharynx
(Waldeyer's ring).

Waldeyer's tonsillar ring, consisting of an unpaired pharyngeal
tonsil in the roof of the pharynx, paired palatine tonsils and
lingual tonsils scattered in the root of the tongue. (Modified
from Kahle et al. Color Atlas and Textbook of Human Anatomy).

The vertical chain consists of superior and inferior groups of
nodes related to the carotid sheath.
All lymph vessels of the head and neck drain into the deep
cervical nodes, either directly from the tissues or indirectly via
nodes in outlying groups.
Lymph is returned to the systemic venous circulation via either
the right lymphatic duct or the thoracic duct.

Node

Location

Afferent

Efferent

Superficial Lymph Nodes of the Head
Occipital (2-4)

Superior nuchal line
between
sternocleidomastoid
and trapezius

Occipital part of scalp

Superficial
cervical lymph
nodes
Accessary lymph
nodes

Mastoid (1-3)

Superficial to
sternocleidomastoid
insertion

Posterior parietal scalp
Skin of ear, posterior
external acoustic
meatus

Superior deep
cervical nodes
Accessary lymph
nodes

Preauricular (2-3)

Anterior to ear over
parotid fascia

Drains areas supplied
by superficial temporal
artery
Anterior parietal scalp
Anterior surface of ear

Superior deep
cervical lymph
nodes

Textbook of Head and Neck Anatomy (Hiatt - Gartner, 4th Ed. 2010)

Parotid (up to 10 or
more)

About parotid gland
and under parotid
fascia
Deep to parotid
gland

Facial
Superficial(up to 12) Distributed along
Maxillary
course of facial
Buccal
artery and vein
Mandibular
Deep

Distributed along
course of maxillary
artery lateral to
lateral pterygoid
muscle

External acoustic
meatus
Skin of frontal and
temporal regions
Eyelids, tympanic
cavity
Cheek, nose
(posterior palate)

Superior deep
cervical lymph
nodes

Skin and mucous
membranes of
eyelids, nose, cheek

Submandibular
nodes

Temporal and
infratemporal fossa
Nasal pharynx

Superior deep
cervical lymph
nodes


Cervical Lymph Nodes
Superficial

Anterior jugular vein
between superficial
cervical fascia and
infrahyoid fascia

Skin, muscles, and
viscera of infrahyoid
region of neck

Deep

Between viscera of
Adjoining parts of
neck and investing
trachea, larynx,
layer of deep cervical thyroid gland
fascia

Superior deep
cervical lymph nodes

Superior deep

Anterior cervical/Superficial
Submental (2-3)

Submental triangle

Chin
Medial part of lower
lip
Lower incisor teeth
and gingiva
Tip of tongue
Cheeks

Submandibular
lymph node to
jugulo-omohyoid
lymph node and
superior deep


Submandibular Submandibular
(3-6)
triangle adjacent
to submandibular
gland

Superficial
cervical (1-2)

Facial nodes
Chin
Lateral upper and lower
lips
Submental nodes
Cheeks and nose,
anterior nasal cavity
Maxillary and mandibular
teeth and gingiva
Oral palate
Lateral parts of anterior
2/3 of tongue

Along external
Lower part of ear and
jugular vein
parotid region
superficial to
sternocleidomastoi
d muscle

Superior deep
cervical lymph
nodes and juguloomohyoid lymph
nodes

Superior deep
cervical lymph
nodes


Deep Cervical Lymph Nodes
Superior deep
cervical

Surrounding internal
jugular vein deep to
sternocleidomastoid
and superior to
omohyoid muscle

Occipital nodes
Mastoid nodes
Preauricular nodes
Parotid nodes
Submandibular nodes
Superficial cervical
nodes
Retropharyngeal
nodes

Inferior deep
cervical nodes or
separate channel to
jugulo-subclavian
junction

Jugulodigastric

Junction of internal
jugular vein and
posterior digastric
muscle

Palatine and lingual
tonsils
Posterior palate
Lateral portions of
the anterior 2/3 of
tongue

Inferior deep
cervical lymph
nodes


Jugulo-omohyoid Above junction of
internal jugular vein
and omohyoid
muscle

Posterior 1/3 of
tongue
Submandibular
nodes
Submental nodes

Inferior deep
cervical lymph
nodes

Inferior deep
cervical

Along internal
jugular vein below
omohyoid muscle
deep to the
sternocleidomastoid
muscle

Transverse cervical
nodes
Anterior cervical
nodes
Superior deep
cervical nodes

Jugular trunk

Retropharyngeal
(1-3)

Retropharyngeal
space

Posterior nasal cavity
Paranasal sinuses
Hard and soft palate
Nasopharynx,
oropharynx
Anditory tube

Superior deep
cervical nodes


Accessory (2-6)

Along accessory
nerve in posterior
triangle

Occipital nodes
Mastoid nodes
Lateral neck and
shoulder

Transverse cervical
nodes

Transverse cervical
(1-10)

Along transverse
cervical blood
vessels at level of
clavicle

Accessory nodes
Apical axillary nodes
Lateral neck
Anterior thoracic
wall

Jugular trunk or
directly into thoracic
duct or right
lymphatic duct or
independently into
junction of internal
jugular vein and
subclavian vein


Imaging-based nodal classification :1998 modification of the 1991 AAO-HNS (American Academy of
Otolaryngology – Head and Neck Surgery) classification
Level I

The sub-mental and sub-mandibular nodes.
They lie above the hyoid bone, below the mylohoid
muscle and anterior to the back of the sub-mandibular
gland.

Level IA

The sub-mental nodes.
They lie between the medial margins of the anterior
bellies of the diagastric muscles.

Level IB

The sub-mandibular nodes.
On each side, they lie lateral to the level IA nodes and
anterior to the back of each sub-mandibular gland.

Arch Otolaryngol Head Neck Surg. 1999;125:388-396.

Level II

The upper internal jugular nodes.
They extend from the skull base to the level of the
bottom of the body of hyoid bone.
They are posterior to the back of the sub-mandibular
gland and anterior to the back of sternocleidomastoid
muscle.
Level IIA

A level II node that lies either anterior, medial, lateral or
posterior to the internal jugular vein. If posterior to the
vein, the node is inseparable from the vein.

Level IIB

A level II node that lies posterior to the internal jugular
vein and has a flat plane separating it and the vein.


Level III

The middle jugular nodes.
They extend from the level of the bottom of the body of the
hyoid bone to the level of the bottom of the cricoid arch.
They lie anterior to the back of sternocleidomastoid muscle.

Level IV

The low jugular nodes.
They extend from the level of the bottom of the cricoid arch to
the level of the clavicle.
They lie anterior to a line connecting the back of the
sternocleidomastoid muscle and the posterolateral margin of the
anterior scalene muscle.
They are also lateral to the carotid arteries.


Level V

The nodes in the posterior triangle.
They lie posterior to the back of the sternocleidomastoid muscle from
the skull base to the level of the bottom of the anterior scalene muscle
from the level of the bottom of the cricoid arch to the level of the
clavicle.
They also lie anterior to the anterior edge of the trapezius muscle.

Level VA

Upper level V nodes extend from the skull base to the level of the
bottom of the cricoid arch.

Level VB

Lower level V nodes extend from the level of the bottom of the cricoid
arch to the level of the clavicle.

Level VI

The upper visceral nodes.
They lie between the carotid arteries from the level of the bottom of
the body of the hyoid bone to the level of the top of the manubrium.


Level VII

The superior mediastinal nodes.
They lie between the carotid arteries below the
level of the top of the manubrium and above the
level of the innominate vein.

Supraclavicular nodes

They lie at or caudal to the level of the clavicle
and lateral to the carotid artery on each side of
the neck.

Retropharyngeal nodes

Within 2 cm of the skull base, they lie medial to
the internal carotid arteries.


Lymph drainage of
external nose
Lymph drainage of external
nose is primarily to the
submandibular group of
nodes although lymph from
the root of the nose drains
to superficial parotid nodes.

Lymph vessels from the anterior region of the nasal cavity pass
superficially to join those draining the external nasal skin, and
end in the submandibular nodes.
The rest of the nasal cavity, paranasal sinuses, nasopharynx
and pharyngeal end of the pharyngotympanic tube, all drain to
the upper deep cervical nodes either directly or through the
retropharyngeal nodes.
The posterior nasal floor probably drains to the parotid nodes.

The lymphatic drainage of the tongue can be divided into three
main regions, marginal, central and dorsal.
The anterior region of the tongue drains into marginal and
central vessels, and the posterior part of the tongue behind the
circumvallate papillae drains into the dorsal lymph vessels.
The more central regions drain bilaterally into sub-mental and
sub-mandibular nodes.

The lymph vessels from the teeth usually run directly into the
ipsi-lateral submandibular lymph nodes.
Lymph from the mandibular incisors, however, drains into the
submental lymph nodes.

Occasionally, lymph from the molars may pass directly into the
jugulo-digastric group of nodes.

When a lymph node is under challenge from a foreign antigen,
it may become swollen and painful to the touch— a condition
called lymphadenitis.
Commonly palpated and accessible lymph nodes are - the
cervical, axillary, and inguinal.
Lymph nodes are common sites of metastatic cancer because
cancer cells from almost any organ can break loose, enter the
lymphatic capillaries, and lodge in the nodes.
Lymphadenopathy is a collective term for all lymph node
diseases

Treatment for malignant disease is the removal of the lymph
nodes of the anterior and posterior triangles of the neck and
their associated lymph channels, together with those structures
which must be excised in order to make this lymphatic ablation
possible.

Usually involves the upper part of the deep cervical chain
(from tonsillar infection).
These infected nodes may adhere very firmly to the internal
jugular vein which may be wounded in the course of their
excision.

The upper deep cervical lymph nodes act as pathways of spread
for malignant tumours of the supraglottic larynx: up to 40% of
these tumours will have undergone such spread at the time of
clinical presentation.
The glottis is very poorly endowed with lymphatic vessels: 95%
of malignant tumours confined to the glottis will present with a
change in voice or airway obstruction but will not show signs of
spread to adjacent lymph nodes at presentation.

Tumours of the subglottic larynx will often spread to the
paratracheal lymph node chain prior to clinical presentation.
However, the presenting symptoms may be voice change and
airway obstruction rather than a mass in the neck, because the
paratracheal lymph nodes occupy a deep-seated position in
the root of the neck and so their enlargement may remain
occult.

Lymphadenopathy - enlargement of the lymph nodes.

It may be an incidental finding in patients being examined for
various reasons, or it may be a presenting sign or symptom of
the patient's illness.
Soft, flat, submandibular nodes (<1 cm) are often palpable in
healthy children and young adults;
Healthy adults may have palpable inguinal nodes of up to 2 cm,
which are considered normal.

Generalized lymphadenopathy
It has been defined as involvement of three or more
noncontiguous lymph node areas.
Generalized lymphadenopathy is frequently associated with
nonmalignant disorders such as
infectious mononucleosis [Epstein-Barr virus (EBV) or
cytomegalovirus (CMV)],toxoplasmosis, AIDS, other viral
infections,
systemic lupus erythematosus (SLE), and
mixed connective tissue disease.

Acute and chronic lymphocytic leukemias and malignant
lymphomas also produce generalized adenopathy in adults.

Localized or regional lymphadenopathy
implies involvement of a single anatomic area.
The site of localized or regional adenopathy may provide a
useful clue about the cause.
e.g. Occipital adenopathy often reflects an infection of the
scalp, and preauricular adenopathy accompanies conjunctival
infections and cat-scratch disease.

Infectious diseases
Viral

infectious mononucleosis syndromes (EBV, CMV), infectious
hepatitis, herpes simplex, herpesvirus-6, varicella-zoster
virus, rubella, measles, adenovirus, HIV, epidemic
keratoconjunctivitis, vaccinia, herpesvirus-8

Bacterial

streptococci, staphylococci, cat-scratch disease, brucellosis,
tularemia, plague, chancroid, melioidosis, glanders,
tuberculosis, atypical mycobacterial infection, primary and
secondary syphilis, diphtheria, leprosy

Fungal

histoplasmosis, coccidioidomycosis, paracoccidioidomycosis

Chlamydial

lymphogranuloma venereum, trachoma

Parasitic

toxoplasmosis, leishmaniasis, trypanosomiasis, filariasis

Rickettsia

scrub typhus, rickettsialpox, Q fever

Immunologic diseases
Rheumatoid arthritis
Juvenile rheumatoid arthritis
Mixed connective tissue disease
Systemic lupus erythematosus
Dermatomyositis
Sjögren's syndrome
Serum sickness
Drug hypersensitivity—diphenylhydantoin, hydralazine,
allopurinol, primidone, gold, carbamazepine, etc.
Angioimmunoblastic lymphadenopathy
Primary biliary cirrhosis
Graft-vs.-host disease
Silicone-associated
Autoimmune lymphoproliferative syndrome

Malignant diseases
Hematologic—Hodgkin's disease, non-Hodgkin's
lymphomas, acute or chronic lymphocytic leukemia, hairy
cell leukemia, malignant histiocytosis, amyloidosis
Metastatic—from numerous primary sites

Lipid storage diseases—Gaucher's, Niemann-Pick, Fabry, Tangier
Endocrine diseases—hyperthyroidism, Adrenal insufficiency,
Thyroiditis.

Other disorders
Castleman's disease (giant lymph node hyperplasia)
Sarcoidosis
Dermatopathic lymphadenitis
Lymphomatoid granulomatosis
Histiocytic necrotizing lymphadenitis (Kikuchi's disease)
Sinus histiocytosis with massive lymphadenopathy (Rosai-Dorfman
disease)
Mucocutaneous lymph node syndrome (Kawasaki's disease)
Histiocytosis X
Familial Mediterranean fever
Severe hypertriglyceridemia
Vascular transformation of sinuses
Inflammatory pseudotumor of lymph node
Congestive heart failureAbbreviations: CMV, cytomegalovirus; EBV,
Epstein-Barr virus.

classification depending upon the clinical presentation.
Presentation

Common

Uncommon

Rare

Acute
Unilateral

-Staphylococcus aureus
-Group A streptococcus
-Anaerobic bacteria

-Group B streptococcus -Anthrax
-Tularemia1
-Pasturella multocida
-Gram negative bacteria
-Yersinia pestis

Acute
Bilateral

-Numerous common upper
respiratory tract viruses
-Herpes Simplex Virus
-Epstein-Barr virus1,2
-Cytomegalovirus1,2
-Group A streptococcus
-Mycoplasma pneumoniae

-Roseola 2
-Parvovirus B19

Corynebacteri
um
diphtheriae
-Measles
-Mumps
-Rubella

Courtney Hallum, MD, LPCH Blue Team and PEC Rotations, February 2009

Presentation

Common

Uncommon

Rare

Chronic Unilateral

-Nontuberculous
mycobacterium
-Cat-scratch
disease

-Tuberculosis
-Toxoplasmosis
-Actinomycosis

-Nocardia
brasiliensis
-Aspergillosis

Chronic Bilateral

-Epstein-Barr virus
-Cytomegalovirus

-HIV
-Tuberculosis
-Toxoplasmosis
-Syphilis

Brucellosis
-Histoplasmosis

Courtney Hallum, MD, LPCH Blue Team and PEC Rotations, February 2009

The physician will be aided in the pursuit of an explanation for
the lymph-adenopathy by
a careful medical history,
physical examination,
selected laboratory tests, and
an excisional lymph node biopsy.

Medical History :It should reveal the setting in which lymphadenopathy is
occurring.
Symptoms such as sore throat, cough, fever, night sweats,
fatigue, weight loss, or pain in the nodes should be sought.
The patient's age, sex, occupation, exposure to pets, sexual
behavior, and use of drugs such as diphenylhydantoin are
other important historic points.

Medical History –
For example, children and young adults usually have benign (i.e.,
nonmalignant) disorders that account for the observed
lymphadenopathy such as viral or bacterial upper respiratory
infections; infectious mononucleosis; toxoplasmosis; and, in
some countries, tuberculosis.
In contrast, after age 50, the incidence of malignant disorders
increases and that of benign disorders decreases.

Physical examination :It can provide useful clues such as
the extent of lymphadenopathy (localized or generalized),
size of nodes,
texture,
presence or absence of nodal tenderness,
signs of inflammation over the node,
skin lesions, and
splenomegaly.

Size of the lymph node(s)
Nodes <1.0 cm2 in area (1.0 cm x 1.0 cm or less) are almost
always secondary to benign, nonspecific reactive causes.
In one retrospective analysis of younger patients (9–25 years)
who had a lymph node biopsy, a maximum diameter of >2 cm
served as one discriminant for predicting that the biopsy would
reveal malignant or granulomatous disease.
Patients with node(s) 1.0 cm2 should be observed after
excluding infectious mononucleosis and/or toxoplasmosis
unless there are symptoms and signs of an underlying systemic
illness.

The texture of lymph nodes may be described as soft, firm,
rubbery, hard, discrete, matted.
It may be tender or non-tender.

It may be movable or fixed.
Tenderness is found when the capsule is stretched during rapid
enlargement, usually secondary to an inflammatory process.
Some malignant diseases such as acute leukemia may produce
rapid enlargement and pain in the nodes.

E.g. Nodes involved by lymphoma tend to be large, discrete,
symmetric, rubbery, firm, mobile, and non tender.

JIADS vol-2 Issue 1 Jan-March, 2011, 31-33

Nodes containing metastatic cancer are often hard, nontender,
and nonmovable because of fixation to surrounding tissues.

The co-existence of splenomegaly in the patient with
lymphadenopathy implies a systemic illness such as
infectious mononucleosis,
lymphoma,
acute or chronic leukemia,
SLE,
sarcoidosis,
toxoplasmosis,
cat-scratch disease, or
other less common hematologic disorders.

PALPATION OF LYMPH NODES –
Lymph node and chain palpation starts with the parotid and
preauricular area which may also be palpated bimanually.
Palpating with light finger pressure against underlying firm
tissues (bone or muscle), or bimanually where appropriate.
The head and neck lymph examination continues down the
mandible to the submandibular region where bilateral palpation
proceeds forward to the submental nodes just under the chin.

With the patient seated upright, head tipped slightly forward,
the cervical lymphatic chains are palpated against the
sternocleidomastoid muscle.
Superficial cervicals lymph nodes are found along the anterior
border, and deep superior and inferior chains found along the
posterior border.

The laboratory investigation of patients with lymphadenopathy
must be tailored to elucidate the etiology suspected from the
patient's history and physical findings.
Complete Blood Count, CBC
provide useful data for the diagnosis of
acute or chronic leukemias,
EBV or CMV mononucleosis,
lymphoma with a leukemic component,
pyogenic infections, or
immune cytopenias in illnesses such as SLE.

Serologic studies – may demonstrate
antibodies specific to components of EBV, CMV, HIV, and
other viruses;
Toxoplasma gondii;
Brucella;
antinuclear and anti-DNA antibody in case of SLE.

Chest x-ray –
usually negative
the presence of a pulmonary infiltrate or mediastinal
lymphadenopathy
would
suggest
tuberculosis,
histoplasmosis, sarcoidosis, lymphoma, primary lung cancer,
or metastatic cancer

Lymph node biopsy –
The indications for biopsy are imprecise, yet it is a valuable
diagnostic tool.
The decision to biopsy may be made early in a patient's
evaluation or delayed for up to two weeks.
Prompt biopsy should occur if the patient's history and
physical findings suggest a malignancy;
E.g. a solitary, hard, nontender cervical node in an older
patient who is a chronic user of tobacco;
supraclavicular adenopathy; and
solitary or generalized adenopathy that is firm, movable,
and suggestive of lymphoma.

Fine-needle aspiration –
It should not be performed as the first diagnostic procedure.
Fine-needle aspiration should be reserved for thyroid
nodules and for confirmation of relapse in patients whose
primary diagnosis is known.

Normal cervical nodes appear sonographically as somewhat
flattened hypoechoic structures with varying amounts of hilar
fat.
US appearance of normal lymph node. Image
shows flattened hypoechoic cigar-shaped structure
(arrow).

Used to determine the long (L) axis, short (S) axis, and a ratio of
long to short axis in cervical nodes.
An L/S ratio of <2.0 has a sensitivity and a specificity of 95% for
distinguishing benign and malignant nodes in patients with head
and neck cancer.
J Nucl Med 2004; 45:1509–1518
Dentomaxillofacial Radiology (2000) 29, 133 - 143

Malignant infiltration alters the US features of the lymph nodes,
resulting in enlarged nodes that are usually rounded and show
peripheral or mixed vascularity.
Using these features, US has been shown to have an accuracy of
89%– 94% in differentiating malignant from benign cervical
lymph nodes

J Nucl Med 2004; 45:1509–1518

US image of a deep cervical (level four)
lymph node in a patient with a
nasopharyngeal SCC. The nodal hilum is
hyperechoic relative to the hypoechoic
peripheral cortex. The increased size
(14 mm) and the eccentric cortical
widening are indicators of
malignant involvement

J Nucl Med 2004; 45:1509–1518

Identifcation of cervical lymphadenopathy is critical to the
management and outcome of diseases that present with
malignant nodal infiltration.
Squamous cell carcinoma(SCC) of the head and neck is the
commonest tumour of the upper aerodigestive tract and the
presence of cervical lymph node metastases in these patients is
of particular prognostic and therapeutic significance, with a
single lymph node metastasis reducing survival by one-half.


The imaging criteria used to determine metastatic cervical
lymphadenopathy include –
nodal necrosis
an heterogeneous appearance on CT or MRI and
eccentric cortical widening on US.
Recent imaging advances have concentrated on potential
differences in the `function' of malignant lymph nodes as
demonstrated by
differential uptake of radio-labelled fluorodeoxyglucose
(FDG) positron emission tomography (PET) or
tissue specific MRI contrast media.


CT remains the most widely used modality for neck imaging.

The CT examination is performed in the axial plane with
contiguous sections of 3 ± 5 mm whilst a bolus of intravenous
contrast media is administered.
CT criteria for assessing lymph node metastases are based on
size, shape, the presence of central necrosis and the appearance
of a cluster of nodes in the expected lymph drainage pathway
for the tumour.


The most effective size criteria for indicating metastatic involvement are now defined as minimum axial diameters in excess of
11 mm in the jugulodigastric region and in excess of 10 mm
elsewhere.
Using these sizes a sensitivity of 42% and specificity of 99% per
node were produced.
With the use of spiral CT, it is possible to reconstruct the image
in any plane with good quality, allowing more accurate
calculation of the maximal axial and longitudinal dimensions and
thus assessment of nodal shape.


Nodal grouping in the drainage chain of a tumour is a further
indicator of metastatic disease . This is defined as three or more
contiguous or confluent lymph nodes, each of which has a
minimal axial diameter of 8 ± 10 mm.

Axial CT scan with
intravenous contrast
demonstrating bilateral
deep cervical (level two)
lymph nodes.


The most accurate CT predictor of metastasis is the presence of
central necrosis, which has been said to have a 100% specificity.
This is seen as a central area of low attenuation surrounded by a
thick, irregular rim of enhancement and is due to nodal
replacement of the medulla by less enhancing tumour.


Axial CT scan with intravenous contrast demonstrating a leftsided tongue SCC extending across the midline. There are
bilateral enlarged submandibular (level one) lymph nodes
demon-strating marked necrosis.

Nodal necrosis may be mimicked by lipid metaplasia which
represents fatty degeneration secondary to inflammation or
irradiation.
However, this fatty change generally occurs at the periphery of
the node. Abscess formation may also have a similar appearance
but such suppurative transformation is usually evident clinically.


Axial CT scan with intravenous contrast demonstrating lipid
metaplasia (arrow) eccentrically placed in a left submandibular
(level one) lymph node which has a 6mm minimum axial
diameter.

Standard protocols for MRI of the cervical lymph nodes include
a selection of T1- and fast spin echo T2- weighted axial, coronal
and sagittal images.
STIR sequences allow a combination of T1- and T2-weighting
with fat suppression, and malignant nodes are clearly demonstrated as high signal.
T1-weighted images depict lymph nodes as being of
intermediate signal intensity, similar to muscle, whilst T2weighted images show them as hyperintense signal.


a

b

(a) T1 weighted and (b) T2 weighted sagittal MRI scans demonstrate a large
pathological deep cervical lymph node (level two/ three) which is of
intermediate signal on T1 and high signal on T2

Most head and neck PET imaging is performed with the
radiolabelled glucose analogue FDG which has increased uptake
in viable malignant tumour due to enhanced glycolysis.
The result can be expressed as a standardised uptake value
(SUV), with those values greater than two being considered
abnormal.
PET scanning provides functional rather than anatomical
imaging.

Dentomaxillofacial Radiology (2000) 29, 133 – 143

A 57-y-old woman with chest pain after lobectomy for lung cancer 4 mo earlier. (A)
Axial CT scan shows mixed soft tissue and fluid in left pleural space. Prevascular and
axillary lymph nodes were interpreted as normal. (B) Axial dual PET/CT scan shows
increased uptake in soft-tissue mass as well as small prevascular and axillary lymph
nodes, indicating recurrent disease with metastatic nodal spread.

J Nucl Med 2004; 45:1509–1518

Planar lympho-scintigraphy
Hybrid SPECT/CT imaging
Dynamic contrast – enhanced MR imaging
Ultra-small super-paramagnetic iron oxide (USPIO) enhanced
MRI
Gadolinium enhanced MRI

In conclusion, the lymphatic system and its organs are
widespread and scattered throughout the body. It
functions to service almost every region of the body.
Because the vessels of the lymphatic system span the
entire body it becomes an easy portal for the spread of
cancer and other diseases, which is why disorders and
diseases of this system can be so devastating.

Textbook of Head and Neck Anatomy (Hiatt – Gartner) 4th Ed. 2010
Grant's Atlas of Anatomy,13th Ed.
Gray's Anatomy – 40th Ed.
Anatomy of the Human Body - Henry Gray
Saladin: Anatomy & Physiology: The Unity of Form and Function, 3rd Edition
Embryology Atlas , John F Neas
Life Map – Embryonic development & stem cell compendium
Butler M G, Isogai S, Weinstein B M. Lymphatic development, Birth Defects
Res C Embryo Today. 2009 September ; 87(3): 222–231.
Albrecht I, Christofori G, Molecular mechanisms of lymphangiogenesis in
development and cancer; Int. J. Dev. Biol. 55: 483-494
Ferrer R, Lymphadenopathy: Differential Diagnosis and Evaluation; Am Fam
Physician. 1998 Oct 15;58(6):1313-1320
Som P M, Hugh D C, Mancuso A A, An imaging-based classification for the
cervical nodes designed as an adjunct to recent clinically based nodal
classification;Arch Otolaryngol Head Neck Surg. 1999;125:388-396.

Oliver G, Detmar M, The rediscovery of the lymphatic system: old and new
insights intothe development and biological function of the lymphatic
vasculature; Genes Dev. 2002,16: 773-783
Sambandan T, Mabel C R, Cervical lymphadenopathy- a review;
JIADS,2011,2,1:31-33.
Torabi M, Aquino S L, Harisinghani M G, Current concept in lymph node
imaging; J Nucl Med, 2004; 45:1509-1518.
Connor SEJ, Olliff JFC, Imaging of malignant cervical lymphadenopathy – a
review; Dentomaxillofacial Radiology, 2000;29:133-143.

“The earliest evidence of ancient dentistry -an amazingly detailed dental work on a
mummy from ancient Egypt that archaeologists have dated to 2000 BCE. The work
shows intricate gold work around the teeth. This mummy was found with two donor
teeth that had holes drilled into them. Wires were strung through the holes and then
around the neighboring teeth.” Source: metalonmetal blog.

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