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Surg Oncol Clin N Am

16 (2007) 1–16

Anatomy of the Lymphatics


John E. Skandalakis, MD, PhD, FACSa,*,
Lee J. Skandalakis, MD, FACSa,
Panagiotis N. Skandalakis, MDa,b
a
Centers for Surgical Anatomy & Technique, Emory University School of Medicine,
1462 Clifton Road NE, Suite 303, Atlanta, GA 30322, USA
b
Department of Surgery, Medical School, University of Athens, Mikras Asias 75,
GR 11527 Athens, Greece

The lymphatic vessels are the absorbing vessels, all over the body; . these,
all together, with the thoracic duct, constitute one great and general system
. William Hunter (1718–1783) [1]
Although visualization of the lymphatics through lymphography that
was unattainable in earlier eras is realized today, a general lack of appreci-
ation for the anatomy of the lymphatics still exists in medical training and
literature. In 1985, the President of the International Society for Lymphol-
ogy wrote, ‘‘It is perhaps rather unusual for an international society to feel
that it is essential to draw attention to the very existence of its subject mat-
ter.. such is the general lack of knowledge about the lymphatic system’’ [2].

Embryology
The genesis of the lymphatics is an enigma. Perhaps the lymphatics
develop from the endothelium of the veins, or perhaps they are the product
of angiogenic mesenchyme. It is even possible that the venous system is re-
sponsible for the genesis of the lymph vessels, but it may be said that, from
an embryologic standpoint, the lymphatic system originates and terminates
in the venous system [3]. Although the blood vessels and the heart develop
much earlier than the lymphatic vessels during ontogeny, Wilting and col-
leagues [4] found growing evidence that the first vascular system occurring
after ontogeny and phylogeny has lymphatic functions.
Harvey and Oliver [5] stated, ‘‘The specification of cell fate is integral to
embryonic development. Recent research has identified several molecules
that are involved in the development of the embryonic vasculature. Their

* Corresponding author.
E-mail address: cfroman@emory.edu (J.E. Skandalakis).

1055-3207/07/$ - see front matter Ó 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.soc.2006.10.006 surgonc.theclinics.com
2 SKANDALAKIS et al

combined actions are required for the specification and development of the
arteries, veins and lymphatic vessels.’’

Anomalies of the lymphatics


Anomalies of the lymphatics are shown in Table 1. It should be remem-
bered that congenital anomalies are relatively rare [6]. On the basis of
human embryo dissection, van der Putte and van Limborgh [7] concluded
that lymphatico-venous communications outside the prevertebral region
‘‘always point to developmental aberrations or to pathology.’’
Cystic hygromas form when a primordial lymph sac fails to reestablish
communications with the central venous system from which it arose, or
from an aberrant bud arising from a primordial lymph sac [8].
Gross anatomic abnormality of the lymphatic vessels is found in all cases
of clinical lymphedema. These abnormalities include absence, hypoplasia,
discontinuity, varicosity with valvular incompetence, and obstruction [9].
Although it is not within the scope of this article to discuss lymphedema
in depth, the senior author (J.E.S.) remembers a well-known professor, Dr.
Emmanuel Kondoleon (1879–1939), with whom he studied as a second-year
medical student. The senior author watched him perform the Kondoleon
operation for elephantiasis on a patient’s lower extremity. From the incision
to the closing, the thrill of observing ‘‘the master’’ remains with him today,
with fond and proud memories.
Remember that the formation of lymphangiomas is a rare phenomenon
[10].

Anatomy
It is not in the scope of this article to discuss the lymphatic drainage of
the several organs. We present what is new about the overall anatomy of
the lymphatics, perhaps the most complicated system of Homo sapiens.
A drainage system parallel to the venous network, the lymphatics begin
with the initial lymph vessels in the periphery of the body, with interposed
lymph nodes. In the region of the right and left venous angles, the lymphatic
connecting trunks join the venous system (Fig. 1) [3]. The lymphatic system
consists of lymph vessels and lymphatic organs. The lymph vessels conduct
lymph toward the venous system. This vessel network drains interstitial fluid
from tissues and returns it to the blood [11]. Lymphatic vessels are impor-
tant for the maintenance of normal tissue fluid balance, immune surveil-
lance, and adsorption of digested fats [12]. Extravasated fluid and
macromolecules are transported unidirectionally from tissues [13] through
the branching hierarchy of vessels [14]. The lymphocytes and antigen-
presenting cells enter lymphatic capillaries in the periphery and migrate
through the lymphatic vessels to the lymph nodes.
Table 1
Anomalies of the lymphatic system
First appearance Sex chiefly Relative
Anomaly Origin of defect (or other diagnostic clues) affected frequency Remarks

ANATOMY OF THE LYMPHATICS


Variations in the course of the 2nd month No pathologic structures Equal Common d
thoracic duct
Cystic hygroma (cystic 6th to 9th weeks? At birth or infancy Equal (neck); Uncommon Invasive growth;
lymphangioma) male (groin) may be a neoplasm
Primary lymphedema: 3rd month? At birth Equal? Rare Familial tendency
Milroy’s disease
Lymphedema praecox
Mesenteric, omental and ? At any age Equal? Rare d
retroperitoneal Uncommon
Male (children);
lymphatic cysts
female (adults)
From Skandalakis JE, editor. Skandalakis’ surgical anatomy: the embryologic and anatomic basis of modern surgery. Athens (Greece): Paschalidis
Medical Publishers; 2004; with permission.

3
4 SKANDALAKIS et al

Fig. 1. Lymph trunks and node groups of the body quadrants. 1. Left internal jugular vein;
2. left subclavian vein; 3. thoracic duct; 4. parotid lymph nodes; 5. submandibular lymph nodes;
6. accessory and comitant lymph nodes of the accessory nerve; 7. internal jugular lymph nodes
with left jugular trunk; 8. supraclavicular lymph nodes with left supraclavicular trunk; 9. axil-
lary lymph nodes with left subclavian trunk; 10. intercostal lymph nodes with left intercostal
trunk; 11. parasternal lymph nodes with left parasternal trunk; 12. anterior mediastinal lymph
nodes with left anterior mediastinal trunk; 13. tracheobronchial lymph nodes with left tracheo-
bronchial trunk; 14. cisterna chyli; 15a. left lumbar trunk; 15b. right lumbar trunk; 16. mesen-
teric lymph nodes; 17. lumbar lymph nodes; 18. left common iliac lymph nodes; 19. right
external iliac lymph nodes; 20. internal iliac; 21. inguinal lymph nodes; 22. right lymphatic
duct. (From Földi M, Földi E, Kubik S. Textbook of lymphology. Munich (Germany): Urban
& Fischer; 2003; with permission.)

Lymphocytes are found within the ‘‘lymphomyoloid complex’’ [15], an


extensive network of vessels containing lymph (proteins of plasma and large
numbers of cells, the lymphocytes) and several masses of lymphatic tissue.
Another characteristic of this vascular lymphatic system is the multiple
channels associated with lymph nodes, which are located in special areas.
Perhaps these areas should be called ‘‘lymphatic stations.’’
The beginning and the end of the lymphatics may be as follows:

Tissue lymph/tissue vessels/lymph node/veins

Lymph sacs
By definition, lymph sacs are loose confluent connections of capillary
plexuses or lymphatic spaces commencing as clefts in local angiogenic
ANATOMY OF THE LYMPHATICS 5

mesenchyme [16]. Mammalian lymph nodes develop in regions occupied by


lymph sacs and lymph sacs are transformed into lymphatic plexuses [17].
Almost 100 years ago, Sabin [18] presented the positions of primary lymph
sacs as follows (Fig. 2):
1. Jugular lymph sacs (right and left)
2. Retroperitoneal lymph sacs
3. Cisterna chyli
4. Posterior lymph sacs (right and left)
The jugular lymph sac develops at the junction of the subclavian vein
with the precardinal, involving also both internal and external jugular veins.
The retroperitoneal lymph sac is located at the mesenteric roots, close to the
adrenal glands at the prerenal part of the inferior vena cava. The cisterna
chyli is located at the area of the third and fourth lumbar vertebrae. The
posterior lymph sacs are related to the left lower iliac vein [16].
The rare occurrence of a lymphatic diverticulum arising from lymphatic
vessels has been attributed to partial persistence of embryonic posterior
lymph sacs [19].

Lymphatic network
The overall lymphatic network may include the following categories
(Fig. 3) [6]:

Fig. 2. Relative position of the primary lymph sacs. (From Standring S, editor. Gray’s anat-
omy: the anatomical basis of clinical practice. 39th edition. Edinburgh (UK): Elsevier Churchill
Livingston; 2005; with permission.)
6 SKANDALAKIS et al

Fig. 3. The lymphatic network.

 Capillaries (minute lymph vessels)


 Larger lymph vessels
 Lymph glands
 Large lymph vessels
Each one of these categories performs the following special work:
 The complicated network of irregular capillaries, which consists of min-
ute lymph vessels, drains the lymph of the body (with the exception of
hyaline cartilages, epidermis, and the cornea)
 The larger lymph vessels drain the capillaries
 Lymph glands accept lymph from the lymph vessels and filter the lymph
 Large lymph vessels are responsible for draining the lymph into the
veins
It is accepted today that the lymphatic vessels for all practical purposes
follow the peripatos of the veins. There are also lymphatic vessels that arise
de novo from the mesenchyme and form some connections with preexisting
vessels [16].
Kelly [20] termed as ‘‘strategic’’ the remarkable distribution of lymphoid
tissue and organs throughout the human body, with an especial richness in
areas prone to insult or pathogen invasion. These tissues include the tonsils,
adenoids, and connective tissue nodules without fibrous capsules. The organs
include the lymph nodes, thymus, spleen, and perhaps others. Again, we
remind the reader that we will not describe the lymphatics of these entities.
The 600 to 700 lymph nodes are encapsulated by dense connective tissue
with blood and lymphatic vessels and nerves attached to them at specific in-
dentations [3]. The lymph nodes serve as a filtration unit (Fig. 4) [21]. It is
not within the scope of this article to present the physiology of the lymphatic
system, but remember that this system both protects the body from infection
and directs fluids into the circulation.
The sentinel or first lymph node, a term that originated from the work of
Cabanas [22], is the node receiving lymph from a malignant neoplasm.
Leong and colleagues [23] discussed the sentinel lymph node and human
solid cancer. The sentinel node concept is under the most intensive investi-
gation in melanoma and breast cancer, but it is also being investigated for
multiple other malignancies [24].
The principal elements of the lymphatics are the right lymphatic duct, the
thoracic duct, and the cisterna chyli (Figs. 5 and 6).
ANATOMY OF THE LYMPHATICS 7

Fig. 4. The lymph node as a filtration unit. (From Nieweg OE, Essner R, Reintgen DS, et al,
editors. Lymphatic mapping and probe applications in oncology, Oxford (UK): Routledge/
Taylor&Francis Group, LLC; 2000; with permission. Copyright Ó 2000.)

Right lymphatic duct


The right lymphatic duct typically begins with the union of three lym-
phatic trunks: right jugular, right subclavian, and right bronchomediastinal.
The right bronchomediastinal trunk is regarded as the vestigial portion of
the terminal (cranial) segment of the embryologic right thoracic duct. It re-
ceives lymphatic drainage from the right lung, lower left lung, right dia-
phragm, most of the drainage from the heart, and some drainage from
the right lobe of the liver.
The right lymphatic duct is approximately 2 cm long. It is very closely re-
lated to the anterior scalene muscle. In the majority of cases, the right lym-
phatic duct empties into the junction of the right subclavian and right
internal jugular veins. However, as demonstrated in Figs. 7 and 8, its termi-
nation also has numerous variations.

Thoracic duct
The thoracic duct is approximately 45 cm long and 2 to 5 mm in diame-
ter. It drains both lymph and chyle into the confluence of the great veins in
the root of the neck [25]. The thoracic duct is the largest lymphatic channel
in the body. It collects lymph from the entire body except the right hemi-
thorax (thoracic wall, right lung, right side of the heart, part of the
8 SKANDALAKIS et al

Fig. 5. The general plan of the lymphatic system. (From Woodburne RT, Burkel WE. Essen-
tials of human anatomy. 9th edition. New York: Oxford University Press; 1994; with
permission.)

diaphragmatic surface of the liver, lower area of the right lower lobe of the
liver), right head and neck, and right upper extremity.
The lower end of the duct receives descending paired posterior intercostal
lymph vessels that drain the lower six or seven intercostal spaces. As it
ascends, the duct receives additional tributaries from posterior mediastinal
nodes and the upper intercostal spaces. Its terminal tributaries are the left
jugular, subclavian, and bronchomediastinal trunks. According to Riquet
and colleagues [26], little is known about these intrathoracic tributaries of
the thoracic duct and their drainage patterns.
The duct can be subdivided into three parts: abdominal, thoracic, and
cervical. The abdominal part of the thoracic duct originates from the cranial
part of the cisterna chyli. With the aorta on its left and the azygos vein on its
right, the thoracic duct passes through the ‘‘aortic hiatus’’ of the diaphragm
to form the thoracic part. It maintains this relationship as it passes through
the posterior mediastinum. During its ascent, the thoracic vertebrae, right
intercostal arteries, and terminal portions of the hemiazygos and accessory
hemiazygos veins are posterior to the thoracic duct; the esophagus, dia-
phragm and pericardium are anterior to it.
At the level of T7, the thoracic duct travels obliquely behind the esoph-
agus to the level of the fifth thoracic vertebra (Fig. 9). At T5, it reappears
from behind the esophagus to continue its upward journey on the left of
the esophagus and medial to the pleura. In the base of the neck, the thoracic
ANATOMY OF THE LYMPHATICS 9

Fig. 6. Principal elements of the lymphatic system. (From Nieweg OE, Essner R, Reintgen DS,
et al, editors. Lymphatic mapping and probe applications in oncology, Oxford (UK): Rout-
ledge/Taylor&Francis Group, LLC; 2000; with permission. Copyright Ó 2000.)

duct passes posterior to the common carotid artery, internal jugular vein,
vagus nerve, left anterior scalene muscle, and left phrenic nerve. It passes an-
terior to the vertebral artery and vein and the sympathetic trunk. The duct
proceeds upward to the level of C7, whereupon it descends across the sub-
clavian artery. It ends in the junction of the left subclavian vein and left
internal jugular vein, thus forming the cervical part of the thoracic duct.

Fig. 7. Variations of the lymphatic junctions at the right venous angle. (A) Entry of the
tributaries into the right lymphatic duct. (B) Partial entry into the right lymphatic duct. (C) Sep-
arate entry of the tributaries near the right venous angle. (From Baumeister RGH. Surgical anat-
omy of the lymphatic system. In: Heberer G, van Dongen RJAM, editors. Vascular surgery. New
York: Springer-Verlag; 1989. p. 38; with permission of Springer Science and Business Media.)
10 SKANDALAKIS et al

Fig. 8. Variations in the terminal lymph trunks of the right side. (a) Jugular trunk; (b) subcla-
vian trunk; (c) bronchomediastinal trunk; (d) right lymphatic duct; (e) lymph node of paraster-
nal chain; (f) lymph node of deep cervical chain. (From Williams PL, editor. Gray’s anatomy.
38th edition. New York: Elsevier; 1995; with permission. Copyright Ó 1995.)

Jacobsson [27] investigated 122 autopsy cases to study the anatomy and
pathology of the thoracic duct, dissecting 100 cadavers and performing 22
angiographies. A thoracic duct was present in all cases. The thoracic duct
always started below the diaphragm, passing through the posterior medias-
tinum, and discharging in the confluence of the veins at the left side of the
neck; in 4% a branch emptied into the right side. In 20% of the cases, the
thoracic duct originated from the confluence of the lumbar and intestinal
trunks; in 55% it formed after the intestinal trunk joined either the duct
or one or both lumbar trunks; in 24%, the duct ascended from a plexus
of the lumbar and intestinal trunks; in 1%, the duct had a completely plex-
iform structure.
According to Jacobsson [27] the cervical part of the thoracic duct corre-
sponds to one of nine types:
1. Single trunk with one opening into the venous system (36%)
2. Single trunk with two openings (13%)
3. Single trunk with three openings (3%)
4. One or several insulae with one opening into the venous system (18%)
5. One or several insulae with two openings (3%)
6. One or several insulae with three openings (1%)
7. One or several plexuses with one opening (14%)
8. One or several plexuses with two openings (9%)
9. One or several plexuses with three openings (3%)
Jacobsson [27] found the cervical part of the thoracic duct to be the widest,
and the lower part of the thoracic duct the narrowest. However, the diameter
increased once more in the abdomen. Valve attachments were found to be
more frequent in the cervical part of the duct. Occasionally, a reduction of
the cusps was observed, ranging from slight shrinkage to complete absence
(most commonly in the lower cervical or the upper parts of the thoracic).
Heart failure and cirrhosis of the liver were responsible for dilatation of
ANATOMY OF THE LYMPHATICS 11

Fig. 9. The oblique thoracic course of the thoracic duct, resulting from the anastomosis of the
right and left thoracic ducts. The definitive duct represents the retention of the proximal part of
the right thoracic duct and the distal segment of the left thoracic duct. (From Skandalakis JE,
editor. Skandalakis’ surgical anatomy: the embryologic and anatomic basis of modern surgery.
Athens (Greece): Paschalidis Medical Publishers; 2004; with permission.)

the upper part of the thoracic duct. Dilatation or shunt-like branching of the
thoracic duct was observed caudal to the site of compression of the duct, from
lymph node metastases in the mediastinum and left supraclavicular fossa.
The volume of flow through the thoracic duct is between 60 and 190 ml/hr;
consequently, large quantities of plasma proteins can be lost quickly from the
blood in the event of trauma to the duct or in association with malignant
tumors. Simple ligation of the vessel is followed by gradual restoration
of normal levels of blood fat over a period of about 2 weeks, as collateral
channels reroute the flow [28].
Regurgitation of blood from the jugulosubclavian confluence into the
thoracic duct is not possible in life because the opening of the thoracic
duct into the subclavian vein is protected by valves. In cadaveric specimens,
backflow of blood into the thoracic duct from the jugulosubclavian venous
junction is often apparent, causing the duct to resemble a vein.
12 SKANDALAKIS et al

There are several variations in the termination of the thoracic duct


(Fig. 10). Jdanov [29] reported termination in the following sites:
 Internal jugular vein, 48%
 Subclavian vein, 9%
 Junction of the internal jugular and subclavian veins, 35%
 Left brachiocephalic (innominate) vein, 8%
Kinnaert [30] dissected 49 cadavers and collected 480 additional cases. He
reported the termination of the thoracic duct as follows:
 No evidence of left thoracic duct, 0 to 4.5%
 Multiple terminal openings (in others’ cases, 10% to 40%; in his cases,
21%)
 Termination into the internal jugular vein, 36%
 Termination into the subclavian vein, 17%
 Termination into the junction of internal jugular and subclavian veins,
34%
Shimada and Sato [31] found that only 38% of Japanese had thoracic
ducts that terminate in the jugulosubclavian angle. In comparison, previous
studies by Kihara and Adachi [32] found this occurrence in 78.2% of

Fig. 10. Variations of the entry of the thoracic duct into the venous system. (A) A single tho-
racic duct and a simple junction. (B) Plexiform ramification of the final segment of a thoracic
duct, but with a simple junction. (C) Delta-like entry of the thoracic duct. (D) Duplication of
the final segment of the thoracic duct and two separate junctions. (E) Ampullary enlargement
of the thoracic duct with multiple terminal branches. (From Baumeister RGH. Surgical anat-
omy of the lymphatic system. In: Heberer G, van Dongen RJAM, editors. Vascular surgery.
New York: Springer-Verlag; 1989. p. 37; with permission of Springer Science and Business
Media.)
ANATOMY OF THE LYMPHATICS 13

Japanese and in 33% of European subjects. Shimada and Sato [31] noted the
following sites and frequencies of termination of the trunk of the thoracic
duct, each major type also possessing subtypes not discussed here:
 Venous angle, 38%
 Internal jugular vein, 27%
 External jugular vein, 28%
 Other complex configurations, 7%
Shimada and Sato [31] noted that although the multiple complex config-
urations occurred only 7% of the time, this termination was highly corre-
lated with an increased risk of metastasis in cervical or mediastinal lymph
node dissections. Also, there was a high risk of injury to the terminations
of the duct during radical neck dissection.

Cisterna chyli
The cisterna chyli is an elongated and sometimes dilated sac about 5 cm
in length. It is located in the shadow of the right side of the aorta and behind
the right diaphragmatic crus at the surface of L2 (variably, T12–L2). It re-
ceives the right and left lumbar trunks, the intestinal trunk, and the lowest
intercostal vessels (Fig. 11).
According to Browse [33], the cadaveric cisterna chyli has an approxi-
mate width of 1 to 2 cm, but with lymphography is 1 cm wide and 2 cm
long. These authors emphasize that, ‘‘it is rarely seen to be as large as the
typical anatomy textbook description.’’
Jacobsson [27] reported the presence of the cisterna chyli in 52% of the
cases, with an average diameter of 6.7 mm (range 4–14 mm). In the thoracic
part, insulae and plexus formations of the thoracic duct were found in 32%.

Fig. 11. The cisterna chyli. (From Brantigan O. Clinical anatomy. New York: McGraw-Hill
Book Company; 1963; with permission.)
14 SKANDALAKIS et al

Multiple sacculations may be present as a result of the contributing ves-


sels. However, sacculations are not present after the convergence of the con-
tributing vessels with the cisterna chyli. Alternatively, the meeting place of
the principal vessels may be thoracic rather than abdominal. Because of
the relative infrequency of a distinctly dilated cisterna, the term should be
understood to be of topographic convenience but not necessarily related
to the degree of distension.
The right and left lumbar trunks transmit lymph from the abdominal wall
below the level of the navel, pelvis, kidneys, and adrenal glands. The intes-
tinal trunk, which receives the lymph and chyle from the parts of the gastro-
intestinal tract supplied by the celiac and superior mesenteric arteries,
occasionally empties directly into the cisterna chyli. However, in most cases
the intestinal trunk is a tributary of the left lumbar trunk. The intercostal
trunks enter the upper part of the cisterna chyli or empty into the beginning
of the thoracic duct.

Summary
There is still much to be learned about the lymphatic system. New discov-
eries in lymphatic anatomy, embryogenesis, malformations and physiology
await researchers. Studies of the relationship of the lymphatics and the cen-
tral nervous system [34] computer modeling [35], and molecular biology [36]
suggest exciting vistas.

Acknowledgment
We thank Carol R. Froman for editorial assistance.

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